(Oceanography and Marine Biology 22) Harold Barnes (Ed.), Margaret Barnes (Ed.) - Oceanography and Marine Biology, Vol. 22-Aberdeen University Press (1984)

OCEANOGRAPHY AND
MARINE BIOLOGY
AN ANNUAL REVIEW
Volume 22
HAROLD BARNES, Founder Editor
MARGARET BARNES, Editor

The Dunstaffnage Marine Research Laboratory
Oban, Argyll, Scotland
ABERDEEN UNIVERSITY PRESS

FIRST PUBLISHED 1984
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© Aberdeen University Press 1984
British Library Cataloguing in Publication Data
Oceanography and marine biology.—Vol. 22
1. Oceanography—Periodicals 2. Marine
biology—Periodicals
551.46′005 GC1
ISBN 0-203-40062-3 Master e-book ISBN
ISBN 0-203-70886-5 (Adobe eReader Format)

ISBN 0-08-030392-7 (Print Edition)
CONTENTS
page
PREFACE v
Currents in the Eastern Irish Sea 2

M.J.HOWARTH
Emergence of Optical Instrumentation for measuring Biological 47
Properties
CLARICE M.YENTS AND CHCHARLES S.YENTSCH
Mixing and Plankton: an Interdisciplinary Theme in Oceanography 90
P.TETT AND A.EDWARDS
Effects of Physical Processes on Planktonic Ecosystems in the Coastal 116
Ocean
KENNETH L.DENMAN AND THOMAS M.POWELL
Manganese in the Marine Environment 164
G.P.GLASBY
Heavy Metals and Coral Reefs 192
L.S.HOWARD AND B.E.BROWN
Ecological Energetics from Total Lipid and Total Protein: Fact and 210
Artifact using a Gravimetric Method for Lipid and a Biuret Method for
Protein c.c.
E.HOPKINS, J.V. SEIRING, O.NYHOLMEN AND
A.HERMANNSEN
Biochemical Metabolic Regulatory Responses of Marine Invertebrates 263
to Natural Environmental Change and Marine Pollution
JOHN BLACKSTOCK
Aspects of Flowering and Pollination in Marine Angiosperms 317
J.M.PETTITT
Feeding in the Chaetognatha 350
DAVID L.FEIGENBAUM AND ROBERT C.MARIS
iv
Ecophysiology of Marsupial Development and Reproduction in 417

Mysidacea (Crustacea)
KARL J.WITTMANN
Competition between Marine Organisms: Ecological and Evolutionary 458
Implications
G.M.BRANCH
AUTHOR INDEX 628

SYSTEMATIC INDEX 666
SUBJECT INDEX 675
PREFACE
Manuscripts continue to be submitted to this series of Annual Reviews. The

desire to publish in it must reflect its importance and value to marine scientists in
general. Many experts are still willing, and even anxious, to accept invitations to
contribute articles. This is all very gratifying to me as the editor and to the
publishers; it ensures the continuation of the Series.
As always, it is a pleasure to acknowledge the help of all the contributors and
their willingness to accede to editorial requests. I am especially grateful for the
help and advice of many colleagues including, in particular, Drs A.D.Ansell,
R.N.Gibson. and T.H.Pearson.
OCEANOGRAPHY AND MARINE
BIOLOGY
AN ANNUAL REVIEW
Volume 22
Oceanogr. Mar. Biol. Ann. Rev., 1984, 22, 11–53

Margaret Barnes, Ed.
Aberdeen University Press
CURRENTS IN THE EASTERN IRISH SEA
M.J.HOWARTH
Institute of Oceanographic Sciences, Bidston Observatory,
Birkenhead, Merseyside L43 7RA, U.K.
INTRODUCTION
Since 1952 low level liquid waste from the British Nuclear Fuels Limited
nuclear re-processing plant at Windscale (now called Sellafield), Cumbria, U.K.
has been discharged into the Irish Sea. The chemical composition and the
amount of the waste has varied over the years as the plant being operated at
Windscale has changed and as the number and types of nuclear reactors in the
U.K. have changed. Monthly or annual limits, in Curies, of the quantity which
may be discharged for each radionuclide are specified by the Ministry of
Agriculture, Fisheries and Food and the Department of the Environment. More
details are given by Mauchline (1980), Smith, Parker & Kirby (1980), and an
annual report on radioactivity in surface and coastal waters of the British Isles,
the most recent of which is for 1980 (Hunt, 1982).
Most of the radionuclides in the waste have half-lives of less than a few days
and are discharged in small amounts—causing a small increase in radioactivity in
the vicinity of the outfall. A few, however, have half-lives of a year or longer and
so have the potential to increase the level of radioactivity or toxicity over a large
region. The manner of their movement depends on whether they are in solution or
particulate form on leaving the outfall. Only a few radionuclides stay in solution;
examples are most compounds of strontium 90 and caesium 134 and 137. These
either move with the currents or become trapped in the interstitial water in the
sediments. Most radionuclides, however, descend to the sea floor as colloids or
particles; examples are compounds of ruthenium 106, of cerium 144, and of
highly toxic plutonium 238, 239, 240, 241 and americium 241. These
radionuclides are adsorbed by the sediments by several different processes
depending on the chemical composition of the sea water, sediment, and
radionuclides. Since most of these processes are surface-area dependent the
radionuclides are attracted to the fine sediment-silts and muds (Hetherington &
CURRENTS IN EASTERN IRISH SEA 3
Jefferies, 1974). Unless the sediments are disturbed, for instance by fast tidal or
wave orbital currents or by bioturbation, this radioactivity decreases
exponentially with depth into the sediment. In contrast, the radioactivity from
soluble radionuclides decreases more slowly with depth since the interstitial
water frequently penetrates tens of centimetres. Whether a radionuclide stays in
solution or is in particulate form depends on its chemical composition, for
instance plutonium in some forms is particulate and in others is soluble. Most of
the plutonium released from Sellafield appears to be particulate (Nelson &
Lovett, 1981).
About 103–104 m3/day of effluentis discharged from the outfall, which is 20 m
below chart datum and 2 km from the shore at Sellafield. Since the effluent is
composed mainly of fresh water, which is less dense than sea water, initially it
rises towards the sea surface (Mauchline, 1980). The transport of the long-lived
radionuclides away from the outfall is determined by the currents in the Irish Sea,
either directly or indirectly via dispersion and sediment transport. Those in
solution can be transported a long way—caesium 137 from Sellafield, which
forms a significant proportion of the waste, has been detected in the North Sea,
Baltic Sea and along the Norwegian coast (Kautsky, Jefferies & Steele, 1980;
Kautsky, 1981; Kautsky & Murray, 1981) and plutonium and americium from
Sellafield have been detected in the water column in the North Minch, 600 km
away (Livingston & Bowen, 1977). Net sediment transport not only depends on
the currents but also on the nature of the sediment (whether it is cohesive, like
mud, or non-cohesive, like sand) and on whether the transport process is by bed-
load or in suspension. There is no accepted theory for predicting sediment
transport in the sea and very few in situ observations. Most transport processes
are almost certainly non-linear and hence the net sediment transport will depend
on the tidal currents (as will the initial dispersion).
This paper reviews the present knowledge of tidal and low frequency currents
in the eastern Irish Sea (see p. 23 and 28, respectively) to form the basis for
understanding and predicting the distributions of radionuclides there. In turn,
these will provide feedback to improve comprehension of the Irish Sea’s
dynamics. The background is given on pages 12–17 by describing briefly the
salient features of the physical oceanography of the Irish Sea and on pages 18–23
by commenting on measuring currents with recording currents meters and on
predicting them with numerical models, two techniques which, over the last 15
years, have greatly increased our knowledge and understanding of the dynamics
of the Irish Sea.
PHYSICAL OCEANOGRAPHY
Detailed descriptions of the physical oceanography of the Irish Sea are given by
Bowden (1955, 1980). A brief account is given here concentrating on the region
near Sellafield and excluding tides and currents.
4 M.J.HOWARTH
Fig. 1—Map of west coast of Britain: the 100 and 200-m depth contours are shown.
TOPOGRAPHY
The Irish Sea consists of a deep channel in the west, to the east of which are
large, shallow bays. The channel extends from the St George’s Channel in the
south to the North Channel in the north, these being the only entrances to the
Irish Sea, both indirectly connecting it with the Atlantic Ocean. The minimum
depth along the channel’s axis is 80 m. The two largest bays are Cardigan Bay
and the area to the east of the Isle of Man—the eastern Irish Sea, which has an
area of approximately 15000 km2 (Fig. 1). Depths in the eastern Irish Sea seldom
exceed 55 m and are shallowest between the Isle of Man and Cumbria where
they seldom exceed 30 m (Fig. 2) whereas to the west of the Isle of Man they
reach 130 m. Near Sellafield the isobaths are parallel to the coast, but become
more confused to the east and northeast of the Isle of Man where there is a
shallow region and several banks. Between the Isle of Man and Cumbria the sea
floor is composed of mud, silt or sand, with a patch of mud occurring off the
coast near Sellafield (Williams, Kirby, Smith & Parker, 1981).
SALINITY, TEMPERATURE AND DENSITY

The distribution of the salinity and temperature of the water in the Irish Sea is
determined by the properties and volume fluxes of its sources (Atlantic water,
river discharge, and evaporation/precipitation), by advection and mixing within
the Irish Sea, and by the heat fluxes at the sea surface.
Fig. 2—Bathymetry of eastern Irish Sea: the 20-m (dotted line) and 50-m (dashed line)
depth contours are shown.
Atlantic water enters the Irish Sea through the St George’s and North
Channels having crossed the Celtic Sea and Malin Shelf Sea, respectively. Its
salinity is more or less constant throughout the year but its temperature has a
small annual cycle. Fresh water enters as river discharge and precipitation/
evaporation. The river discharge occurs principally in the eastern Irish Sea
(about twice as much as for the rest of the Irish Sea) and peaks in winter and
spring. Over a year the river discharge contributes about three times as much
fresh water to the Irish Sea as does precipitation minus evaporation. This also
has an annual cycle with small net evaporation in winter and large net
precipitation in summer (Bowden, 1950).
Since in most places the salinity varies little throughout the year the annual
mean sea surface distribution for the Irish Sea is shown in Figure 3. The pattern
of isohalines in the western Irish Sea is consistent with a net northward flow from
the St George’s Channel to the North Channel of 2·5×104 m3/s, equivalent to a
mean current of 0·006 m/s through the North Channel (Bowden, 1950; Wilson,
1974). Because of the freshwater input by rivers the eastern Irish Sea is less saline
than the western, the salinity decreases from 34·0‰ near the Isle of Man to
32·0‰ near the coasts. Also near the coasts there is a small annual cycle
6 M.J.HOWARTH
Fig. 3—Mean annual surface salinity of (‰) of the Irish Sea (from Bowden, 1980).
associated with the river discharge, with a salinity minimum in spring and a
maximum in late autumn.
The sea surface temperature has a much larger annual variation which
dominates its distribution. Generally, the minimum is in February (Fig. 4) and
the maximum in August (Fig. 5) reflecting the variation in heat input at the
surface, which is least in February and greatest in August. The effect on the
water temperature of the surface heat flux is greater in shallower water, since the
heat flux is applied to a smaller volume of water. Hence, the temperature range is
larger in shallow water—near Sellafield it is over 10°C—than in deep water—to
the west of the Isle of Man it is about 6°C. Near the coasts the maximum is in
August and the minimum in February, in phase with the heating cycle. In deeper
water the peaks are about one month later as heat is transferred in summer from
the warmer (coastal) water to the cooler (deeper) water and the reverse in winter.
Vertical variations in temperature and salinity occur if lighter water near the
surface, due to surface heating in the summer or freshwater input, is not mixed
down through the water column. Both storms and tidal currents generate mixing
but tides, since they are always present, seem to be more important. In general,
tidal currents are strong in the Irish Sea (Fig. 6) and the water column is
homogeneous throughout the year. For stratification in summer due to solar
heating at the surface Simpson (1971) has suggested that the parameter h/u3,
Fig. 4.—Mean sea surface temperature (°C) for February for the Irish Sea (from Bowden,
1980).
where h is the water depth and u is the M2 current amplitude, is significant,
stratification occurring if the parameter is large. To the west of the Isle of Man
tidal currents are very weak (Fig. 6) and so stratification occurs in summer. To
the east of the Isle of Man the currents are slightly stronger and the depths
shallower, so that there is only weak stratification in summer. Also to the east of
the Isle of Man there is a significant freshwater input which can lead to
stratification in winter and spring near the coast with fresh, cool water above
denser, salty, warmer water (Jones & Folkard, 1971).
The density of sea water depends on its temperature and salinity. At a given
time the sea surface density distribution reflects the salinity distribution, lighter
water near the coast (the lightest in Liverpool Bay) and denser water in the
middle of the Irish Sea—a mean difference of the order of 2 kg/m3 between the
waters off Cumbria and to the west of the Isle of Man. At a given place the
annual temperature cycle dominates the time variation of sea surface density—
near the coasts it has an amplitude of the order 2 kg/m3, in the deeper water of
the order of 1 kg/m3, lighter in summer. denser in winter.
8 M.J.HOWARTH
Fig. 5.—Mean sea surface temperature (°C) for August for the Irish Sea (from Bowden,
1980).
RECORDING CURRENT METERS AND NUMERICAL
MODELS
Over the last 15 years our understanding of the dynamics of the Irish Sea has
been greatly improved through the complementary techniques of measuring
currents with recording current meters and predicting them with numerical
models. Since this report is largely based on their results, this section is devoted
to a discussion of both techniques with particular reference to the Irish Sea.
RECORDING CURRENT METERS

Currents occur in the sea over a wide frequency range, from surface waves (1 to
0·05 Hz), through tidal and inertial (7×10−5 to10−5 Hz), storm driven (10−5 to10−6
Hz) tocirculation (<10−6 Hz, with anannual cycle). In the Irish Sea the weakest
currents are associated with circulation (0·01 to 0·05 m/s) and the strongest with
tides (up to 1·5 to 2 m/s), although near the surface wave orbital velocities are
occasionally larger than and wind driven currents comparable with tidal currents.
Tidal energy occurs at well defined frequencies grouped in bands, mainly from
1 to 6 cycles/day. Within each band the frequencies are closely spaced so that at
Fig. 6.—M2 tidal currents in the Irish Sea, maximum speed in m/s (from Robinson, 1979).
least one month’s and preferably six months’ or a year’s data are needed to
determine most of the major constituents. The longer record lengths would also
improve confidence limits for the analyses. Since the time variation of tides is
predictable, it is easy to synthesize data obtained at different times. One
observation per hour is the minimum needed to define the higher frequencies and
the timing must be accurate to within a few seconds/day because some
frequencies are closely spaced. Since the fourth diurnal and higher frequencies
are generated by a non-linear response of the sea, non-linearities in the response
of an instrument will degrade measurements at these frequencies (and also at low
frequencies). In the Irish Sea for tidal currents vertical gradients are small,
except near the sea floor, as are horizontal gradients, except near amphidromes,
so that spatially observations can be sparse. An accuracy of the order of 0·01 m/s
in speed and 1° in direction is desirable.
At frequencies below 1 cycle/day energy is in a continuum. Clearly, there are
seasonal variations in the number and severity of storms and in the driving forces
for circulation, so that at least a year’s observations are desirable. In addition, it
can be difficult to synthesize estimates of low frequency currents obtained at
different times. Both circulation and storm-driven currents can have large spatial
gradients—for the latter, particularly, close to coasts and in the vertical where the
10 M.J.HOWARTH
currents are in the direction of the wind near the surface and can be opposed to it
near the sea floor. The desired accuracy for storm-driven currents is similar to
that for tidal currents while for circulation a speed accuracy of 0·001 m/s is
desirable, since the currents are weak.
To what extent can recording current meters satisfy these requirements? Since
the capacity of data loggers precludes sampling fast enough (2 Hz) to measure
wave orbital velocities as well and since there is a gap in the energy spectrum
between surface wave and tidal frequencies instrument systems have been
designed with a sample rate of about 10−3 Hzwhich remove the wave energy by
averaging and which will record for 1 or 2 months. In the Irish Sea most
observations have been made with Plessey MO21 current meters by the Fisheries
Research Laboratory, Lowestoft, U.K. (Baxter & Bedwell, 1972) or with
Aanderaa RCM4 meters by Institute of Oceanographic Sciences, Bidston,
Birkenhead, U.K. The meters have similar designs and specifications—for the
Aanderaa it is
Speed (m/s), Range : 0·025 to 2·5, threshold 0·02

Accuracy : the larger of ±0·01 and ±2% of the speed
Direction, Accuracy : ±7·5° for 0.025<speed (m/s)<0·05
or 1 <speed (m/s)<2
and ±5° for 0·05 <speed (m/s)<l
The accuracies are quoted for an individual observation and if the errors are
random, an important qualification, will be improved statistically for tidal and
low frequency analyses.
A major source of non-random errors is surface waves because they are so
energetic. Neither the Plessey nor the Aanderaa meter completely removes the
wave energy in their averaging process, both because the speed sensors are non-
linear, in this respect the Aanderaa’s rotor is worse than the Plessey’s impeller
(Hammond & Collins, 1979), and because the sampling scheme does not strictly
average the flow—the mean speed is recorded but only a spot direction, with a
time constant of several seconds. Since wave energy is occasionally significant
throughout the water column large errors can occur in tidal and especially low
frequency recorded currents (for instance Beardsley et al., 1981). Wave orbital
velocities at the buoy supporting the mooring are also important because
movement of the buoy is transmitted by the wire to the meters (Halpern &
Pillsbury, 1976). Hence the meters are moored in a taut wire beneath a sub-
surface buoy; this, however, precludes measurement close to the surface. For
measurements near the sea floor, meters have been deployed in a frame sitting on
the sea floor; the main problem is now to design a stable frame which does not
interfere with the flow.
Since in the Irish Sea the semi-diurnal tidal currents are large any faults in the
measuring system, meter and mooring, can lead to serious errors in estimates of
circulation or higher tidal frequencies. One such source is a non-linear compass
(Gould, 1973) although the effects can largely be removed since calibration of
Aanderaa meters have shown a repeatability of ±1°. Another source is
deformation of the mooring by the drag of the current. Then the height of the
meter above the sea floor varies through the semi-diurnal and spring/neap cycles
(by over 10 m in badly designed rigs). Also the wire is not vertical, although the
suspension arrangement of both Aanderaa and Plessey meters copes with this to
some extent. Largest wire angles occur nearest the sea floor implying a minimum
height above the sea floor for deployment of the meter.
By comparing the results from closely spaced current meters of different
designs or in different moorings, which approximate to a greater or lesser degree
to the ideal, some indication of their accuracy may be gauged. Halpern (1980) has
written a recent review of many inter-comparisons. In shallow seas dominated by
tidal currents well maintained Aanderaa and Plessey meters record similar currents
to other meters at the dominant tidal and storm-driven frequencies but
differences occur for higher tidal frequencies and also for the lowest frequencies,
especially in the cross-tidal direction (see also Howarth, 1981a, b; Howarth &
Jones, 1981; Pearson, Schumacher & Muench, 1981). The meters are presumably
reliable, even during storms, because the tidal currents are stronger than the wave
orbital velocities for most of the time, so that high frequency flow reversal at the
meters rarely occurs. In the frequency ranges where uncertainties are high
supporting evidence, either from other meters or better from different types of
measurement, is necessary before much credence can be given to the
measurements.
Recording current meters measure currents frequently at a fixed point,
operating unattended in all weather conditions, providing reasonable temporal
coverage but poor spatial coverage, both in the horizontal and the vertical. The
problem of poor spatial coverage is aggravated by the meters’ inability to
measure near the sea surface and by data losses which arise either through meter
failures or, more commonly, through equipment losses from component failures
(corrosion, bad weather) or from human activity (mainly fishing). Recording
current meters are able to satisfy the requirements for measuring the dominant
tidal currents but at present are less satisfactory for other frequencies, despite
providing much of present knowledge at these frequencies, since they can fail to
give adequate spatial coverage, record length or accuracy.
NUMERICAL MODELS
Models predict the behaviour of a system under the action of a set of forces and a
set of constraints. An important step in any model is its validation against
observations. Some models are statistical, relating one set of numbers to another
with little account taken of the physical processes involved, whilst in others these
processes are accurately included. The latter are more flexible, since changes in
the constraints can be studied, for instance the effect on the dynamics of an
estuary caused by introducing a barrier, and also the physical processes
12 M.J.HOWARTH
themselves studied, their relative importance determined or changes in their

representation assessed. Numerical models of the tidal and low frequency
dynamics of shelf seas are in this group.
The dynamics of a sea are described by the Navier-Stokes equations, applied
to a rotating frame of reference (the Earth), together with an equation for the
conservation of mass. At frequencies less than 1 cph (cycle per hour) the
following assumptions introduce negligible errors.
(a) The vertical component of velocity is small and in most cases can be
neglected (the water depth, h, is much less than the horizontal dimensions of
the sea).
(b) The pressure in the sea is hydrostatic—the pressure at a point is determined
solely by the height and density of the water above the point. This is
equivalent to neglecting vertical accelerations.
(c) Sea water is incompressible.
At these frequencies the dominant mechanism for dissipation is, however,

turbulence rather than molecular friction and so is dependent on the properties of
the flow itself as well as of the fluid. The equations of motion can be derived
from the Navier-Stokes equations in a tractable form only if the turbulent friction
is specified. Then there are three non-linear coupled partial differential equations
with three unknowns—the sea surface elevation, ξ (x, y, t), and the horizontal
components of velocity, u(x, y, z, t) and v(x, y, z, t)—assuming the density field
is known (Proudman, 1953), where x and y are horizontal space coordinates, z is
a vertical coordinate, and t is time. The non-linearities occur in the advective
terms , in most specifications of turbulent friction and sometimes through
a surface boundary condition. Because the equations are non-linear, solutions to
different problems cannot be calculated separately and added since they may
interact (for instance tides and surges) and also oscillatory motion can generate a
mean flow (for instance tides).
To calculate only the elevation, ξ , the equations can be simplified by removing
their depth dependence by integrating from the sea surface to the sea bed. The
problem is then reduced to two spatial dimensions, the velocity unknowns
becoming the two horizontal components of depth mean velocity—and the
turbulent friction term is simplified, becoming the difference between the
stresses applied at the sea surface and the sea floor.
Analytical solutions of either the two- or three- dimensional equations are only
possible in the simplest of cases and geometries. A solution for a real geometry—
coastlines and depths—can only be obtained numerically by approximating,
using finite difference or finite element methods and solving the resulting
simultaneous equations on a computer. The problem is similar to others in fluid
dynamics particularly to the motion of the atmosphere and to weather prediction,
to which much effort has been applied. The techniques are fully described by
Roache (1976) and for marine hydrodynamics by Ramming & Kowalik (1980).
In the finite element technique (Fix, 1975) the sea area is split up into a number
of elements and the spatial variation within each element is given by a series
solution based on a set of functions. There are, however, no finite element
models of the Irish Sea and so the method will not be discussed further.
In the finite difference method the sea area is generally covered with a
rectangular grid, giving a set of finite difference equations which can be
integrated forward in time to calculate values of the variables at each grid point.
The spatial calculation can be performed either explicitly, grid box by grid box,
or implicitly, all at once. The implicit technique involves a matrix inversion
which can require a large rapid access store but, in theory, is stable for any time
increment. The explicit technique, however, has a stability criterion, relating
water depth, grid size and time increment. Most of the Irish Sea models
discussed here are explicit, having maximum time increments of the order of one
minute and thus needing many calculations to complete one tidal cycle.
The accuracy of a shallow sea model depends on the grid size since this
determines the scale of the bottom topography and of the coastline represented in
the model. Often the accuracy of a model can be best improved by reducing the
grid size, especially near the coast where the depth can change appreciably over
short distances (banks and channels) and where much of the energy is dissipated.
In some areas, for instance Morecambe Bay, the model must accommodate the
position of the coastline changing significantly with state of the tide as banks are
covered and uncovered. In models the coastline is usually represented by straight
line segments with two perpendicular orientations. The resulting sharp corners
impose unrealistic gradients on the motion, suggesting that near the coast the
solution, especially for currents, will be less accurate. To reduce these problems
some models have variable grid size and others nest models with different grid
sizes.
The model’s output depends not only on its formulation but also on the initial
or boundary conditions. Usually the currents and/or elevations around the
boundary (coast and open sea) and the stress at the sea surface and sea floor are
specified. The stress at the sea surface arises from the drag of the wind and at the
sea floor from bottom friction. Both can only be calculated with empirical
equations involving ‘constants’ which can be altered to ‘tune’ models. Bottom
friction is related to the near bottom current speed, usually by a power law
(Proudman, 1953). The condition at the coasts is no flow perpendicular to the
coast, whilst at the open boundary, the most difficult area, currents and/or
elevations may be specified from interpolation between observations or values
guessed and the model iterated until agreement is reached with observations at
internal positions. A ‘radiation’ condition relating elevations to currents at the
open boundary is useful since energy can then leave the model through the
boundary and not be reflected unrealistically by the boundary. The boundary
conditions drive the model but only approximate to reality, so errors there will be
reflected in the model solution, particularly near the boundaries.
14 M.J.HOWARTH
Two-dimensional models, with or without advection and with quadratic bottom

friction, have been used extensively for tide and surge studies (for instance,
Heaps, 1969). Elevations at the coasts are accurately predicted—for the
dominant semi-diurnal constituent, M2, amplitudes within 5%, and phases within
10° (Proctor, 1981) and surges with an RMS error of about 0.3 m (Davies &
Flather, 1978). The inclusion of the non-linear terms enables the accurate
prediction of some of the higher order tides (Pingree & Maddock, 1978) and of
tide surge interaction (Prandle & Wolf, 1978) but also means that for the
accurate determination of the M2 tide the models must be run for a full spring to
neap cycle. One of the limits on the model’s accuracy is the specification of
bottom friction which is calculated from depth mean currents instead of more
realistically from bottom currents. Observations show that bottom currents are in
advance of depth mean currents (by about half an hour) so that the phase of
friction in the model is in error.
To overcome this and also to predict the variation of the currents with depth,
three-dimensional models are being developed (Heaps, 1979). The vertical
variations are either modelled by grid boxes in the vertical or by a series solution
based on continuous, orthogonal functions. If constant size grid boxes are used
the vertical resolution is poor in shallow areas but this can be solved by
transforming the vertical coordinate (for instance, Johns, 1978). In models of the
Irish Sea the series solution technique has been used. Vertical structure of
comparable complexity is obtained by using m grid boxes in the vertical or m
terms in the series solution, although the latter converges more rapidly (Davies &
Stephens, 1983). In both cases the memory needed and the time taken to
calculate a solution is approximately m times the equivalent two-dimensional
model and so three-dimensional models can only be run on large computers. The
time taken can be reduced by calculating the advection term every few time steps
—a process called “time splitting”—without loss of accuracy (for instance,
Davies, 1980). The turbulent friction has to be specified in these models and is
usually represented in an eddy viscosity form with a coefficient which varies
horizontally (for instance, dependent on water depth and current speed),
vertically and with time (for some examples see Proctor, 1981, pp. 176–187).
Models developed for the study of tides and surges can also be used in the
study of circulation. Heaps (1978) has shown that the two-dimensional low pass
filtered equations of motion are linear—including a friction term whose
coefficient depends on the amplitude of the tidal current. Hence the contribution
of non-linear tides, mean wind stress, horizontal density gradients, and elevation
gradients along or between the boundaries can be calculated separately and
summed to give the circulation and their relative importance assessed.
The main advantages of numerical models are their ability to give synoptic
coverage and their cheapness in relation to making observations. Two-
dimensional models are relevant to the study of tides and storm surge elevations
in a vertically homogeneous sea but three-dimensional models are necessary for
the study of currents at frequencies lower than tidal since these vary in the
vertical—here two-dimensional models can give misleading results. An

additional complication, now beginning to be modelled, is the effect of
stratification which reduces the exchange of mass and momentum between the
surface and bottom layers.
TIDES
Motion in the Irish Sea is dominated by the tides. Hence the initial dispersion and
mixing of the effluent plume at Sellafield is predominantly controlled by the
tides. (Similarly the importance of tidal mixing in determining where the water
column stratifies in summer has already been mentioned.) Although tidal motion
is oscillatory with periods mainly less than one day it will be shown below that it
can contribute significantly to bed load transport and also to net water
movement. Tides in the Irish Sea have been extensively studied—see for
instance Taylor (1919), Defant (1920), Proudman (1953, art. 150) and further
references in Mungall & Matthews (1978). Cotidal charts based on observations
of the most important constituents are displayed in Robinson (1979).
Over the last 10 years there have been several two-dimensional tidal
numerical models of the Irish Sea (Hunter, 1972; Horwood, 1974; Flather &
Heaps, 1975–only of Morecambe Bay and concerned with the computational
problems caused by drying banks; Mungall & Matthews, 1978; Proctor, 1981),
several of the Northwest European shelf seas (for instance, Flather, 1976;
Pingree & Griffiths, 1979, 1981a, b), and one three-dimensional tidal model of
the eastern Irish Sea (Proctor, 1981). These models have concentrated on the M2
constituent, particularly on its elevation distribution which agrees reasonably
with observations. The grid box size is smallest in the models of Proctor and
Pingree & Griffiths, both of which also contain all the non-linear terms. Both
models have simulated the tides for a spring to neap cycle, thereby not only
predicting the solar semidiurnal (S2) distribution but also a more accurate M2
distribution because of non-linear interaction in the dissipation. (Pingree &
Griffiths, 1981b, also predict the distribution of the next largest semi-diurnal
constituent N2.) Both models predict the M4 distribution.
ELEVATIONS
The tides propagate into the Irish Sea from the Atlantic Ocean—the Irish Sea
itself is too small significantly to respond directly to the tide generating forces of
the Moon and the Sun. In the Atlantic Ocean the most important tidal
constituents are semi-diurnal—at the shelf edge the amplitudes of M2 and S2 are
1·1 and 0·4 m, respectively compared with 0·07 and 0·08 m for the largest
diurnal constituents, O1 and K1 (Cartwright, Edden, Spencer & Vassie, 1980).
The predominance of the semi-diurnal constituents is maintained within the Irish
Sea—at Liverpool 97·5% of the variance in the sea surface elevation record is at
semi-diurnal tidal frequencies.
16 M.J.HOWARTH
The semi-diurnal tides propagate into the Irish Sea by two routes—from the
south through the Celtic Sea and St George’s Channel and from the north
through the Malin Shelf Sea and the North Channel. The two waves meet near
the Isle of Man and are reflected by the Lancashire and Cumbrian coast, forming
a standing wave in the eastern Irish Sea. Hence high water occurs at the same time
(to within 1 h) throughout the eastern Irish Sea and is also approximately the
time of slack water. The corresponding elevation nodes (and current maxima) are
in the North Channel near Islay and in the south of the St George’s Channel. The
latter takes the form of a degenerate amphidrome, inland of Courtown, Eire,
since much of the energy of the incoming wave is dissipated in the St George’s
Channel and eastern Irish Sea (Pugh, 1981). The tidal wave is also modified by
the Earth’s rotation, leading to larger tidal ranges toward the right in the direction
of propagation. Hence the tidal range on the Irish coast is smaller than on the Welsh
and English coasts, with the largest ranges between Liverpool and Barrow-in-
Furness—a mean spring range exceeding 8 m.
The amplitude of the twice daily tide varies over a fortnight (spring to neap
cycle) and also significantly over a month and over six months. In the eastern
Irish Sea mean spring amplitudes are twice mean neap amplitudes for both
elevations and currents and spring tides occur about 1¾ days after full Moon or
new Moon. The monthly and six monthly modulations have average amplitudes
of 14% and 7% of the M2 amplitude, respectively.
Outside the semi-diurnal frequency band the most important tidal constituents
are O1 and K1 at diurnal frequencies and M4 and MS4 at fourth diurnal
frequencies. Throughout most of the Irish Sea amplitudes for these constituents are
in the range 0·05 to 0·1 m (Robinson, 1979). The diurnal tides propagate into the
Irish Sea as free waves in much the same way as the semi-diurnal tides but their
distribution is different since their wavelength is twice as long. Tides at
frequencies higher than semi-diurnal are not generated directly by the
gravitational attraction of the Moon or Sun but arise from non-linear
interactions, mainly to the semi-diurnal tides, a process which also generates low
frequency currents (fortnightly and mean). The interactions occur mostly in
shallow water but also locally where the topography changes, for instance near
headlands. Hence the fourth diurnal tide not only propagates into the Irish Sea
through the St George’s and North Channels as a free wave with a wavelength
one half the semi-diurnal’s but is also generated within the Irish Sea, particularly
in the shallow eastern Irish Sea where between Liverpool and Barrow-in-Furness
the M4 amplitude exceeds 0·2 m. The sixth and higher diurnal constituents have
small amplitudes (less than 0·05 m) and vary greatly in space.
CURRENTS
Semi-diurnal tidal currents are largest in the western St George’s Channel, to the
north of Anglesey, to the north of the Isle of Man, and in the North Channel
(mean spring amplitudes greater than 1 m/s, see Fig. 6, p. 17). Minima occur
where the two waves meet—to the west and east of the Isle of Man (mean spring
amplitudes less than 0·15 and 0·5 m/s, respectively).
The observed mid-depth M2 currents for the eastern Irish Sea based on 29 or
14 day analyses are shown in more detail in Figure 7. The M2 current is a two-
dimensional vector in harmonic motion so that during one period the tip of the
vector traces out an ellipse. The ellipse parameters—semi-major and semi-minor
axes, and the phase and direction of the maximum current are shown in the
Figure. Both to the north and south of the Isle of Man the M2 currents are
essentially rectilinear east to west with maximum amplitudes (greater than 0·9 m/
s) close to the Scottish and Anglesey shores. The current strength decreases
shoreward and as the region between the Isle of Man and Cumbria is
approached, where the amplitude is less than 0·4 m/s. In this region the two tidal
waves meet and the currents become elliptic (at one point the ratio of the semi-
minor to the semi-major axis is 0·6). Close to the Cumbrian coast the currents are
still elliptic but with the maximum flow parallel to the coast and so occurring 2–
3 h earlier (Fig. 8). This flow pattern implies that little tidal mixing occurs in a
direction perpendicular to the Cumbrian, Welsh, and Scottish coasts, so that the
radionuclides from Sellafield will be dispersed by tidal mixing parallel to these
coasts.
Figure 7 shows the contour plots for mid-depth M2 currents but for sediment
transport, which will control the movement of the particulate radionuclides, near
bottom currents are more important. Throughout most of the water column there
is little change in the current with depth, the largest changes occurring in a layer
a few metres thick near the sea floor. In the region between the Isle of Man and
Cumbria comparing values 1 m above the sea bed with mid-depth values, the
maximum magnitude is about a half, it occurs about 10 min earlier, the direction
differs by less than 5° and the shape of the ellipse is, if anything, slightly fatter.
Bed-load transport is thought to depend on the difference between the near
bottom current speed and a threshold speed for sediment movement, according to
a power law. Since the semi-diurnal tidal current is oscillating it cannot by itself
drive net bed-load transport, but in association with the higher harmonics
(particularly the fourth diurnals, Pingree & Griffiths, 1979) or a mean flow, it
can do so. The dependence can be simply illustrated if the power law is assumed
to be cubic and the threshold zero. Consider a current, U, composed of the sum
of a mean flow with amplitude A, a semi-diurnal current with frequency ,
amplitude B, and phase b, and a fourth diurnal current with
frequency , amplitude C, and phase c,
then the mean of U3 over a tidal cycle, ξ 3, is given by
The first term dominates. In it the net transport due to the fourth diurnals is of the
same order as that due to the mean current and depends on the fourth diurnal’s
amplitude, C, and the phase difference, . The M4 amplitude is a minimum
18 M.J.HOWARTH
Fig. 7.—M2 tidal currents in the eastern Irish Sea: A, maximum amplitude in m/s; B,
minimum amplitude in m/s, if positive the current vector rotates anti-clockwise; C, phase
of maximum current; D, direction of maximum current in degrees relative to north; the
contours are based on observations at the positions shown by dots.
between the Isle of Man and Cumbria (0·03 to 0·04 m/s) and rises to 0·07 to 0·08
m/s to the north and south of the Isle of Man. The phase difference, , is 0°
±20° in Liverpool Bay but becomes more scattered between the Isle of Man and
Cumbria. Hence, to the south and east of the Isle of Man transport from this
cause will be significant and is directed eastward—supporting evidence is given
by sand wave profiles (Belderson & Stride, 1969). Between the Isle of Man and
Cumbria the transport will be much weaker. The numerical model of Pingree &
Griffiths (1979) agrees with both results.
Fig. 8.—M2 tidal ellipses from Sites 22 and 23: for positions see Figure 11: the current
hour by hour is shown relative to the same time origin.
In general, the amplitude of the fourth diurnal tide is proportional to the square
of the amplitude of the semi-diurnal tide so that at mean springs it will be four
times that at mean neaps. Hence transport at springs will be at least an order of
magnitude greater than at neaps—this argument is enhanced when a threshold
speed is included—suggesting that for tidally-generated net sediment transport
spring tides (particularly at the equinoxes) will be important.
LOW FREQUENCY CURRENTS

The low frequency (period longer than one day) dynamics of continental shelf
and coastal seas have been studied extensively over the last decade (for reviews
see Csanady, 1976; Winant, 1980; Beardsley & Boicourt, 1981). In the vertical,
pressure, p, at a depth z is hydrostatic: where ξ is the
elevation of the sea surface about its mean, ξ is sea-water density, g is
acceleration due to gravity, and p(atmos) is the atmospheric pressure. In the
horizontal, the driving forces are either balanced by a pressure gradient
(equivalent to an elevation gradient) or the fluid is accelerated and an opposing,
frictional, force generated. In most of the seas around the British Isles oscillatory
tidal motions dominate and the strength of the frictional force depends on the
tidal current amplitude and linearly on the low frequency flow (Heaps, 1978).
Any flow is influenced by the Earth’s rotation, variations in topography and
vertical density stratification. In the eastern Irish Sea the latter is usually not
important since as has been shown above, the density stratification there is at
most slight. The effect of the Earth’s rotation on a current is to accelerate it
perpendicular to the flow (to the right in the Northern Hemisphere). Variations in
topography tend to cause the current to follow the isobaths or coasts so that the
vertically averaged flow perpendicular to the isobaths is usually small. When the
flow is blocked by topography a pressure gradient will be generated, together
with secondary flows.
20 M.J.HOWARTH
DRIVING FORCES
There are four main causes of low frequency currents in shallow seas—
meteorological (wind stress and atmospheric pressure gradients), spatial
variations in sea-water density, oceanic or far field (usually transmitted by a
pressure gradient), and non-linear tidal. In most places the largest flows are
caused by wind stress during a storm, sometimes comparable with the oscillatory
tidal currents, and hence are intermittent. Significant continuous flows can occur
locally near sharp changes in topography—headlands, islands, sandbanks—
generated by non-linear interaction between the oscillating tides and the
topography.
Meteorological
Meteorological forces (Winant, 1980; Beardsley & Boicourt, 1981) drive the low
frequency dynamics of shallow seas in two ways—by applying a horizontal
stress at the sea surface through wind drag, and by varying the vertical force on
the sea surface through changes in atmospheric pressure. Both forces are largest
during storms and hence have a time scale of 2–10 days and a space scale of at
least 1000 km. Storms affecting the Irish Sea normally follow the same pattern—
a large scale depression moves eastward to the south of Iceland and to the north
of Scotland accompanied by winds which veer from southerly to northwesterly.
Occasionally, smaller, secondary depressions attached to this system will pass
eastward over the British Isles. These move quickly and cause the most intense
and rapidly varying conditions over the Irish Sea. The frequency of storms varies
seasonally and from year to year so that the meteorological forces will vary on
yearly and longer time scales.
The Irish Sea responds quickly to the application of meteorological forces with
a response of time of the order of the inertial period (15 h for the eastern Irish
Sea). The wind stress generates a surface current of 2–4% of the wind speed
which decays rapidly with depth. In deep water away from a coast the wind
stress can be balanced by internal friction within the water column over a typical
depth scale of 50 m. In shallow water the wind stress is balanced by bottom
friction and the current’s direction is controlled by the topography. In this case
the wind stress is assumed to be applied to the whole water column and so its
effect will be greatest in the shallowest water giving rise to a coastal boundary
layer a few kilometres wide (for instance, Murthy & Dunbar, 1981). Where the
flows are blocked by coasts, for instance within the Irish Sea, an elevation
gradient perpendicular to the wind is set up and, by continuity, a return flow will
occur either at depth or in deeper water. If the flow is not blocked and the coast
is straight, for instance on the continental shelf to the west of Scotland and
Ireland, the alongshore component of wind generates an alongshore current
which is accompanied by a transverse elevation gradient, balancing the effect of
the Earth’s rotation. Hence sea-level variations at the coast will be correlated
with the alongshore wind stress (for instance, Allen, 1980).
Changes in atmospheric pressure are usually assumed to occur so slowly that
the static inverted barometer response holds whereby a 100 Pa (1 mb) change in
pressure causes a 0·01 m (approximately) change in sea level and the associated
currents are negligible. For a discussion of the discrepancies that can occur
because of this assumption see Crepon (1976). It is also possible that resonance
will occur if the storm moves at the speed which long waves travel in the ocean
(′ ξ gh, where h is water depth) and then the sea-level response will be
amplified.
On a shorter time scale, inertial currents are generated by the wind. These are
a free response of the water determined by the Earth’s rotation in which the
currents are circular and periodic, in the Irish Sea the period is 15 h. They appear
to be easily damped out, usually occurring significantly in the near surface layer
in stratified water. They do not seem to be important in the Irish Sea.
Horizontal density gradients

A simple model of flow in estuaries, where fresh, light river water enters at the
head and heavy, salty sea water at the mouth, is for the lighter water to flow
seaward on the surface and the heavier water landward near the bottom. The
magnitude of the surface flow increases from the estuary’s head to its mouth,
where it can be many times the freshwater input, since water is entrained across
the interface separating the two layers. The surface layer is decoupled from
bottom friction by the interface and so the surface flow is influenced more by the
Earth’s rotation—tending towards the right hand shore and to turn right on
leaving the estuary in the Northern Hemisphere—and sometimes by centrifugal
accelerations.
Similarly, in a vertically homogeneous sea with depth contours parallel to a
straight coast and a density gradient perpendicular to it, the currents can be
deduced to be towards the coast at the bottom rotating anti-clockwise from this
towards the surface (Heaps, 1972). The current is driven by the density gradient
but its structure arises from friction (bottom and internal) and the Earth’s
rotation. The amplitude is small (typically less than 0·05 m/s) but the current is
persistent. Since the horizontal density gradient is largely determined by river
discharge which varies seasonally so will the resulting currents.
Pressure gradients
Events occurring in the ocean or on the shelf some distance from the Irish Sea
can be transmitted to it by pressure gradients and, perhaps, small volume fluxes.
On the shelf, shelf waves can be generated by a storm (Mysak, 1980) although
such waves will have difficulty penetrating the entrances to the Irish Sea—only
events occurring close to the Irish Sea will be significant there. Also most
22 M.J.HOWARTH
oceanic events (eddies, Rossby waves) will be damped out on the shelf close to
the shelf edge (Huthnance, 1981b). The only likely cause of a significant
pressure gradient is large scale oceanic circulation. For instance Csanady (1976)
and Beardsley & Boicourt (1981) postulated such a gradient along the eastern
coast of the United States. These pressure gradients will vary slowly and
probably seasonally.
Tidal
The current vector, u, can be considered in two different frames of reference—
Eulerian, where the flow is determined at points fixed in space, uE, and
Lagrangian, where the movement of parcels of water is followed, uL. In an
oscillatory flow, tides for instance, the mean velocities measured in the two
frames will usually differ because of spatial gradients in the velocity field. The
difference, uL−uE, is known as the Stokes velocity, us, and to a first
approximation is given by:
where the overbar denotes a time average (Longuet-Higgins, 1969).

At its simplest, if the flow is rectilinear and the sea floor horizontal
In this case the Stokes velocity is a maximum for a progressive wave and zero
for a standing wave. Since the semi-diurnal tide in the eastern Irish Sea is
approximately a standing wave, the Stokes velocity there would be expected to
be small. The numerical model of Proctor (1981) confirms this, showing only a
small difference between calculated Eulerian and Lagrangian tidal residuals.
Hence, recording current meter measurements and Eulerian residuals calculated
by the numerical models should both show the movement of the soluble
radioactive waste.
The semi-diurnal tide generates a mean and low frequency (MSf) flows and
higher harmonics (M4, MS4, M6) because its propagation as a long wave in
shallow water is non-linear. (There are also astronomically generated low
frequency tides but these are small.) That the non-linearities are only weak is
shown by the success of linear dynamics in explaining most tidal phenomena and
by the small amplitude in most places of the higher harmonics. The non-
linearities have three sources—shallow water, when the tidal elevation amplitude
is significant compared with the water depth, h; advection, when the velocity
field has spatial gradients (the term in the momentum equations); and
dissipation, both from horizontal and vertical turbulent mixing and from bottom
friction—usually a square drag law. The effect of shallow water occurs both in
the depth averaged continuity equation, as and also in the bottom
friction term in the depth averaged momentum equations, as
There are two length scales—the M2 wavelength ( if

m, T is the M2 period and c its phase velocity) and the M2 particle excursion
. Generation of M4 mainly occurs on the longer
length scale where the most important source is shallow water (see Pingree &
Maddock, 1978, for a discussion of M4 generation in English Channel; most of
their conclusions should be applicable to the eastern Irish Sea). Mean currents
are generated by variations in topography—either changes in depth or coastline—
and their magnitude is controlled by friction. On the larger length scale they tend
to be weak (less than 0·1 m/s), in geostrophic balance and follow f/h contours
(Huthnance, 1981a; Loder, 1980), where f is the Coriolis parameter. Mean flows
on the shorter length scale have been extensively studied recently, mainly in terms
of vorticity (round sandbanks—Huthnance, 1973; near headlands—Tee, 1976;
Pingree & Maddock, 1979; near small islands—Pingree & Maddock, 1980;
general—Robinson, 1981; Zimmerman, 1981). Mean (and low frequency)
currents with the shorter length scale in addition to being generated by the
processes mentioned above for the longer length scale can be generated by
friction, either in association with topographic changes or non-linearly with
velocity shears, or by the advective terms in the momentum equation. Large
mean currents can be generated (′ 0·5 m/s near Portland Bill) which decrease
rapidly away from the source. The amplitudes both of fourth diurnal and of the
mean current depend on the square of the semi-diurnal amplitude and so should
show a more pronounced spring to neap cycle (in the eastern Irish Sea variation
by a factor of four).
OBSERVATIONS
Lagrangian
Apart from current meters, most methods of measuring currents are Lagrangian—
following the movement of water particles—and involve inherent low pass
filtering both in space and time since often only the time and position at the start
and end are known.
The first measurements of low frequency currents in the Irish Sea, starting in
1894, were of surface drift by drift bottles. There are several difficulties with this
technique, the most important are that the effect of wind and waves on the bottle
can be considerable and results can only be based on the returned bottles not on
the total launched. The most extensive experiment lasted two years (1925–1927)
when bottles were released on a line between Dublin and Holyhead (Daniel &
Lewis, 1929). About half were recovered—the majority either around the
northeast Irish Sea or having departed through the North Channel—one reaching
Norway. The results were consistent with a slow northward movement through
24 M.J.HOWARTH
the western Irish Sea together with a good correlation between bottle movement
and wind, so that northerly winds could reverse the mean flow. Similar results
have been obtained for bottles liberated in the North Channel and Clyde Sea
Area (Barnes & Goodley, 1961).
Mean currents near the sea floor have been measured in a similar way, with
Woodhead sea-bed drifters (for example Harvey, 1968). Recovery rates are,
however usually less than for surface drifters and the motion of the drifter is
complex. One has been observed to jump up in the water column during fast
currents, travelling for appreciable distances several metres above the sea floor
(Harden-Jones, Walker & Arnold, 1973)—which may or may not copy sediment
movement. Experiments are reported for the eastern Irish Sea by Ramster (1965)
and Harvey (1968); for Liverpool Bay by Halliwell (1973); for Morecambe Bay
by Phillips (1968, 1969); and for the Solway Firth by Perkins, Bailey & Williams
(1964). The bottom drifts were generally towards the shore, as predicted by
Heaps (1972), with a weak southward drift parallel to the English coast south of
St Bees Head. Planktonic organisms (although non-conservative) can also be
used as drift indicators—the distribution of two species in the eastern Irish Sea
are consistent with this drift pattern (Williamson, 1952, 1956a; Khan &
Williamson, 1970).
Another Lagrangian measurement is the bulk use of tracers. At its simplest a
box model can be formulated, based either on a tracer’s spatial distribution or on
correlating its time variations at different places, to calculate the volume flow
through the box. In such models of the Irish Sea dispersion by tidal currents
cannot be neglected, but can be included in an eddy diffusion coefficient whose
value, however, is open to dispute. In the Irish Sea two tracers are readily
available—salt and the radioisotopes of caesium in the Sellafield effluent. First
calculations were based on the salinity distribution—without diffusion
(Knudsen, 1907) and with diffusion (Bowden, 1950)—and with caesium 137
(Wilson, 1974). All showed a weak northward flow through western Irish Sea,
with a best magnitude estimate of (see p. 14).
Bassett (1910) inferred from the shape of the isohalines (Fig. 3, see p. 15) that
the majority of this northward flow went to the east of the Isle of Man. The water
there reaches its maximum salinity in spring. Its spatial and temporal distribution
could, however, arise from the variations in freshwater supply, so that Bassett’s
hypothesis is not now thought to be true. Indeed, observations and calculations
suggest that most of the northward flow goes to the west of the Isle of Man.
The spatial distribution of caesium 137 discharged from Sellafield has been
used by several authors to infer mean currents. Within the Irish Sea the shape of
the distribution, as opposed to its magnitude, varies little from year to year. The
caesium stays close to the English, Scottish, and Welsh shores before joining the
northward drift through the western Irish Sea (Fig. 9). All measurements support
this northward flow, the concentration of caesium 137 in the North Channel
being of order 20 times greater than in the St George’s Channel. The flow
appears to increase through the North Channel and to extend along the western
Fig. 9.—Concentration of caesium 137 in (Bg/kg) in filtered surface water from the Irish
Sea, April 1980 (from Hunt, 1982).
and northern Scottish coasts and across the North Sea to Norway and the Baltic
(Jefferies, Preston & Steele, 1973; Kautsky, Jefferies & Steele, 1980; Kautsky,
1981; Kautsky & Murray, 1981).
Quantitative estimates of the drift can be made if the time history of the amount
of caesium 137 discharged at Sellafield is known—not only does it vary from
year to year but there is a marked seasonal cycle, peaking in autumn. The most
recent estimate for the mean transit time from Sellafield to the North Channel is
six months (McKinley, Baxter & Jack, 1981) based on data from 1972–1977. As
deduced from the caesium measurements, the northward flow through the Irish
Sea is not constant; the mean over several months can vary by an order of
magnitude (Jefferies, Steele & Preston, 1982). Moreover, these observations
suggest that the flow rate doubled for the period 1976 to 1978, the end of the
observations, compared with 1971 to B 1975. Since caesium has two radioactive
isotopes with different half lives (137–30·1 years, and 134–2·1 years) further
estimates of transit times can be obtained by comparing the ratio of their
abundance with that of the discharge and this gives results consistent with those
described.
Eulerian—current meters
The first reported current meter measurements of the low frequency currents in
the eastern Irish Sea were made intermittently between 1962 and 1965 (Sharaf el
Din, 1970, 1972). At several locations near the coast between Liverpool and
26 M.J.HOWARTH
Fig. 10.—The Lagrangian circulation of the northern Irish Sea (from Ramster & Hill,
1969): A, near-surface; B, near-bottom.
Barrow-in-Furness measurements were made over one tidal cycle by deploying

a direct reading current meter from an anchored ship. Since the measurements
were so short, their means are unlikely to be accurate estimates of circulation but
they indicated that near the surface there was a generally clockwise movement
around Liverpool Bay and near the bottom a shoreward motion.
Since 1966 workers at the Fisheries Research Laboratory at Lowestoft have
deployed Plessey recording current meters in the eastern Irish Sea, usually for a
period of a week to a month, and conducted bottom drifter studies (Ramster &
Hill, 1969; Hill & Ramster, 1972; Ramster, 1973). A one-year long measurement
was made in Liverpool Bay from March 1970 to February 1971 (Ramster, 1971).
The circulation schemes deduced from these measurements are shown in
Figure 10. The near surface scheme has an anti-clockwise motion near the coasts
of the eastern Irish Sea, in contrast to
TABLE I
Details of current meter records, March—May 1977: the meters at Sites 10 and 12 were
mounted in a frame resting on the sea floor; there was a gap in each of the records from
Sites 12 and 27; A, Aanderaa measurements by IOS Bidston; P, Plessey measurements by
the Fisheries Research Laboratory, Lowestoft
Site Water depth below Meter height above Type of meter Low frequency record
chart datum (m) sea floor (m)
Start End Length (days)
1 21 5 A 22 Mar. 14 Apr. 24
2 22 11 A 23 Mar. 16 Apr. 25
3 21 8 A 19 Mar. 13 Apr. 26
5 21 10 P 1 Apr. 10 May 40
6 38 18 A 20 Mar. 13 Apr. 25
8 A 20 Mar. 13 Apr. 25
7 47 33 P 1 Apr. 8 May 38
8 59 35 A 23 Mar. 15 Apr. 24
8 A 23 Mar. 15 Apr. 24
9 15 6 A 20 Mar. 15 Apr. 27
10 37 0·75 A 20 Mar. 13 Apr. 25
11 41 25 A 20 Mar. 11 Apr. 23
16 A 20 Mar. 3 Apr. 15
12 42 0·75 A 24 Mar. 13 Apr. 15
13 21 8 A 24 Mar. 22 Apr. 30
14 22 9 P 31 Mar. 18 Apr. 19
15 37 24 A 24 Mar. 21 Apr. 29
8 A 24 Mar. 16 Apr. 24
16 56 35 A 23 Mar. 14 Apr. 23
19 71 51 A 28 Mar. 16 Apr. 20
8 A 28 Mar. 21 Apr. 25
22 23 9 P 31 Mar. 10 May 41
23 23 10 P 31 Mar. 12 Apr. 13
27 54 8 P 30 Mar. 1 May 24
28 52 36 P 30 Mar. 9 May 41
30 24 10 P 30 Mar. 1 May 33
the measurements of Williamson (1952, 1956a), Sharaf el Din (1970, 1972)

and Khan & Williamson (1970), whilst for the near bottom scheme there is no such
conflict, the motion being generally shoreward.
Since 1969 workers at the Institute of Oceanographic Sciences at Bidston have
deployed Aanderaa recording current meters in Liverpool Bay and have
conducted two joint experiments with Lowestoft workers, the first in September
28 M.J.HOWARTH
1971 covering the whole Irish Sea (Howarth, 1974; Ramster & Medler, 1976),
and the second in March—April 1977 concentrating on the eastern Irish Sea.
Because the latter experiment involved the most comprehensive coverage to date
(21 current meter rigs, of simultaneous low frequency observations in the eastern
Irish Sea) it will be discussed further. Some of the measurements are displayed in
Alcock & Howarth (1978) and have been discussed in Proctor (1981). The rigs
were moored for about 1 month in depths of water ranging from 15 to 71 m
below chart datum. The meters were deployed mainly at mid-depth–18 were at
between 25 and 75% of the water depth and eight were below 25% (see Table I
and Fig. 11). Twenty-six records (five rigs contained two meters) were low pass
filtered and re-sampled at one value per day. The filter’s half-power point was at
0·0215 cph and data for three days were lost at the beginning and end of each
record.
The overall mean currents were weak except at three sites (8, 27, 28) which
were different for three reasons. At only those sites did (a) the vector mean speed
exceed 0·03 m/s, (b) the kinetic energy of the mean currents exceed the kinetic
energy (half the variance) of the low frequency record (Table II), and (c) the ratio
of vector to scalar mean speed exceed 0·8, this indicating that the directional
scatter of the low frequency currents was small at only those sites.
The variance of the low frequency records showed large spatial variations—a
factor of 50 between the most energetic (at Sites 14 and 23) and the least (at
Sites 8 and 12, Table II). An area of low variance extended eastward from
between Anglesey and the Isle of Man with the variance increasing sharply as
the English (particularly the Cumbrian) and Scottish coasts were approached.
The variance varied from being rectilinear parallel to the isobaths close to the
Cumbrian and Scottish coasts (most noticeably at Sites 14 and 23) to being
nearly circular in the central area (for instance at Site 22). At those rigs with two
meters there was little variation of energy with depth.
Most of the low frequency records were significantly correlated indicating the
following mode (or its reverse)—an anti-clockwise flow near the Welsh,
English, and Scottish coasts and a westward flow in the middle of Liverpool
Bay. The records from Sites 8 and 12 were, however, not correlated with this
mode and the correlations from the sites near to 8 and 12 were weaker than the
rest.
Since much of the variance in the low frequency records was expected to be
caused by wind forcing, the low frequency observations were regressed against
the wind stress at Valley, Anglesey. Valley was chosen for the following
reasons. Four stations around the eastern Irish Sea list winds in the Daily Weather
Reports of the Meteorological Office (the Mull of Galloway, Ronaldsway on the
Isle of Man, Squires Gate near Blackpool, and Valley). The winds at Valley were
stronger than those at Ronaldsway
TABLE II
Fig. 11.—The response of the eastern Irish Sea to a 1 Pa wind stress, from a multiple
linear regression between the daily current observations and wind stresses at Valley: A,
eastward wind stress; B, northward wind stress; T, top meter; B, bottom meter; dashed
line, 10 fm (18 m); dotted line, 20 fm (36 m).
Statistics of low frequency records: the kinetic energy/unit mass of the mean is a half the
mean speed squared and of the low frequency record is half its variance.
Site (Vector mean speed)2 (m/s) Variance (m/s)2×10−5 % Variance explained by
2×10−5 multiple linear regressions
with wind stress
1 6 139 41
2 73 131 47
3 21 211 55
5 29 152 40
6T 5 104 29
6B 45 104 61
7 63 177 39
8T 231 64 6
8B 38 30 4
9 0 537 47
10 61 112 51
11T 26 73 47
11B 3 125 60
12 27 49 3
13 15 287 53
14 99 1467 92
30 M.J.HOWARTH
Site (Vector mean speed)2 (m/s) Variance (m/s)2×10−5 % Variance explained by

2×10−5 multiple linear regressions
with wind stress
15T 78 216 44
15B 48 225 34
16 1 94 42
19T 40 85 32
19B 39 78 37
22 77 118 39
23 104 1465 92
27 336 211 17
28 664 299 33
30 49 594 50
and (significantly so) than those at Squires Gate but were weaker than those at
the Mull of Galloway. The highest correlations between current meter records
and the winds were for those from Valley. The correlation was not improved by
taking the mean wind stress of all four stations. The wind stress, ′ , was
calculated from the 6-hourly observations of wind speed, s, by:
where
and
(Smith & Banke, 1975)
The data were then passed through a filter, with the same characteristics as
that for the currents, to give daily values. For most of the period spanning the
measurements, 19 March–10 May 1977, the daily wind stress was weak, less
than 0·3 Pa. Between 29 March and 3 April however, it, reached 0·7 Pa whilst
veering from northward to eastward as the centre of a depression moved
eastward close to the north of Scotland. Most of the low frequency current
records covered this storm period, but a few started in the middle of it. The
highest low frequency currents at each site were recorded during this storm,
mainly up to 0·1 m/s but at Site 14 up to 0·3 m/s.
Multiple linear regressions between each component of current at each site and
the two components of wind stress at Valley were calculated. The percentage of
variance in the current records which could be accounted for by the wind varied
from 90% near the Cumbrian coast (at Sites 14 and 23) to less than 5% between
Anglesey and the Isle of Man at Sites 8 and 12, with a mean value of 42%
(Table II). The currents at the sites to the north of Isle of Man (Sites 27, 28, 30)
had the highest residual variance (observed—wind fitted), about 0·0020 m2/s2;
whereas at each of the other sites it was about 0·0008 m2/s2 equivalent to a
standard deviation of 0·03 m/s. At sites 27, 28 and 30 there was a significant
improvement in the regression when the wind lagged by one day was also
included—their (observed—wind fitted) variance was reduced to 0·0011 m2/s2—

whilst at the other sites there were only slight improvements. The regression
weights for those three sites indicated that westward flows (the low frequency
was predominantly in the east/west direction) were being largely driven by the
previous day’s northward wind. This suggests that storm driven currents to the
north of the Isle of Man are caused by a combination of (a) the action of the wind
there, (b) the action of the wind over the whole of the eastern Irish Sea forcing the
motion to the north of the Isle of Man, and (c) by continuity from sea level
changes in the area of the Solway Firth.
The responses of the meters to a 1 Pa eastward and a 1 Pa northward daily
mean wind stress calculated from the unlagged regressions are shown in
Figure 11. A wind stress of 1 Pa is caused by a wind of 20 m/s. Since the
analysis is linear the responses to the eastward and northward winds can be
combined to give the response to a wind in any direction. An eastward wind
stress generated an anti-clockwise flow near the coast with fastest currents in the
vicinity of the Cumbrian coast and a westward flow off Blackpool. A northward
wind stress generated a weaker and more varied response which flowed anti-
clockwise near the coast also, but only to the north of Blackpool, and southward
in the middle. There was no response at Site 8 to either wind direction. Over the
range 10–70% of the water depth the response varied little with depth—the
maximum change in direction was 55° and the current usually rotated clockwise
with depth, as expected in Ekman dynamics. A typical storm in which the wind
veers from southerly through to northwesterly will, therefore, tend to drive water
northwestward along the Cumbrian coast in an anti-clockwise coastal flow and
westward off Blackpool.
From the regressions it is clear that the patterns and correlations observed in
the low frequency currents reflect the sea’s response to wind forcing. The
strongest response was near to and parallel with the coast, especially the English
coast, and produced the largest variance in the currents. The currents with the
smallest variance were between Anglesey and the Isle of Man in an area where
there was little response to the wind forcing. One caveat is that the strongest
responses occurred at Rigs 14 and 23 but are based on short low frequency
records (19 and 13 days, respectively) which only started half way through the
storm. The results from Rigs 14 and 23, however, agree closely and even if they
were ignored the description of the response would not be qualitatively changed.
This response is obviously not the direct response to wind forcing which is in
the direction of the wind, or somewhat to its right, but which is confined to a
surface layer. Since the topmost meter was at least 10 m below the sea surface,
this layer must have escaped observation. The currents have arisen as secondary
flows to the pressure gradients which balance the wind stress with bottom
friction making a significant contribution only in shallow water.
Other observations generally support this picture. For instance, two rigs were
deployed in the area of weak response near Sites 8 and 12 in October and
November 1977. The low frequency records lasted 33 days spanning a very
32 M.J.HOWARTH
windy period—the daily wind stress at Valley exceeded 0·7 Pa on three separate
occasions and on two of these it exceeded 1 Pa. The response to the wind was
again very weak—the low frequency variances were similar to those at Site 8
(Table II) and the maximum speed was 0·06 m/s. On this occasion 40% of the
variance in the low frequency records was accounted for by a multiple linear
regression against the unlagged wind stress at Valley and the resulting responses
agree well with those calculated for Site 8 (Table IIIa)
The only other measurements made by IOS Bidston close to Sellafield were
off Morecambe Bay in October 1972 (Table IIIb). Sites A and B were the same
as Sites 9 and 13, Site C was between Sites 13 and 15 and Site D was between
Sites 14 and 23. The low frequency records were, however, short, 14 or 15 days,
and the winds were weak; the largest daily wind stress at Valley was 0·15 Pa.
Hence the variance of the low frequency records was much less–0·00174 m2/s2
at Site A compared with 0·00537 m2/s2 at Site 9. The measurements again show
an increase in the response to wind forcing as the coast is approached and very
good agreement in the magnitude of the response to a northward wind stress
(Table III). For an eastward wind stress the responses differ, the 1977
measurements having a northwestward to northward response whereas the 1972
measurements have a westward response, indicating a broader westward flow in
1972 (see Table IIIb and Fig. 11A).
The mean currents calculated from the unlagged regressions of the March to
April 1977 measurements against wind stress at Valley are shown in Figure 12A.
These should be a more accurate estimate of the non-wind-driven flow than the
mean of the observed currents; in fact the directions were very similar—the
average difference was 3°±26°–but the regressed mean currents were stronger,
by a factor of 1·4, this being more noticeable where the effect of the wind was
greater. The mean currents are spatially (horizontally and vertically) more varied
than the wind-driven currents and suggest a clockwise flow around Liverpool
Bay.
Two checks on the reliability of these estimates are measurements at the same
sites at different times and long term measurements, although the
TABLE III
Comparisons of the response to wind forcing calculated from multiple linear regression
analysis of sites at two different times: all the current meters were Aanderaas except for
an AMF Vector Averaging Current Meter at Site A in (a) and Plessey meters at Sites 14
and 23 in (b); the meter at Site 12 was mounted in a frame resting on the sea floor.
Site Position Water Meter Record Response to 1 Pa stress
N:W depth height length
(m) (m) (days)
Eastward wind Northward wind
Speed Directio Speed Directio
(m/s) n (m/s) n
(degrees (degrees
) )
(a)
Mar.-
Apr.
1997
8 53°39′: 59 35 24 0·023 246 0·051 070
4°22′
8 24 0·040 218 0·026 107
12 53°46′: 42 0·75 15 0·062 108 0·130 233
4°08′
Oct.-
Nov.
1977
A 53°43′: 42 20 33 0·021 245 0·077 76
4°14′
D 53°46′: 42 22 33 0·020 257 0·059 85
4°07′
16 33 0·022 221 0·052 94
8 33 0·014 200 0·051 108
(b)
Mar.-
Apr.
1977
9 53°46′: 15 6 27 0·353 302 0·203 003
3°18′
13 53°54′: 21 8 30 0·236 005 0·163 011
3°30′
14 54°01′: 22 9 19 0·528 328 0·520 328
3°20′
23 54°14′: 23 10 13 0·546 333 0·398 331
3°33′
Oct.
1972
A 53°45′: 15 7 15 0·688 265 0·241 003
3°19′
34 M.J.HOWARTH
Site Position Water Meter Record Response to 1 Pa stress

N:W depth height length
(m) (m) (days)
Eastward wind Northward wind
(m/s) n (m/s) n
(degrees (degrees
) )
B 53°53′: 22 13 15 0·165 265 0·386 008
3°32′
5 15 0·111 277 0·162 007
C 54°01′: 33 25 14 No correlation
3°44′ with wind
15 14
5 14
D 54°07′: 22 13 14 0·228 257 0·384 339
3°33′
5 14 0·151 251 0·418 330
TABLE IV
Three comparisons of mean currents calculated from the unlagged regressions against
the wind stress at Valley obtained at different times: all the current meters were
Aanderaas except in (a) Sites 14 and 23 which were Plessey meters and in (c) Site A was
an AMF Vector Averaging Current Meter; the meters at Sites 10 in (b) and 12 in (c) were
in a frame resting on the sea floor; (a) Sites A and 9, B and 13 were the same, C was between
13 and 15, and D between 14 and 23; (b) Sites A and 10 were the same; (c) Sites D and
12 were the same, A was between 8 and 12.
Site Meter Record Mean current Site Meter Record Mean current
height length height length
(m) (days) (m) (days)
(m/s) n (m/s) n
(degrees (degrees
) )
(a) October
Mar.- 1972
Apr.
1977
9 6 27 0·015 131 A 7 15 0·013 162
B 13 15 0·013 213
13 8 30 0·024 217 5 0·009 266
15 24 29 0·035 003 C 25 14 0·011 320
8 24 0·026 098 003 15 14 0·020 212
5 14 0·021 218
Site Meter Record Mean current Site Meter Record Mean current
height length height length
(m) (days) (m) (days)
(m/s) n (m/s) n
(degrees (degrees
) )
14 9 19 0·076 152 D 13 14 0·026 163
23 10 13 0·087 149 5 14 0·015 152
(b) Feb.-
Mar.- Mar
Apr. 1974
1977
A 20 33 0·012 060
10 0·075 25 0·030 130 10 33 0·015 082
(c) Oct.-
Mar.- Nov
Apr 1977
1977
8 35 24 0·048 003 A 20 33 0·020 334
24 0·021 033
D 22 33 0·004 220
16 33 0·004 308
12 0·75 15 0·018 183 8 33 0·008 201
latter have only been made in Liverpool Bay. Table IV contains the means from
three sets of measurements at different times. The agreement in direction is
good, most are within 30°, but in each comparison the March-April 1977 mean
currents are stronger. Two long term sets of measurements have been made in
Liverpool Bay—at 53°32′N: 3°33′W from March 1970 to February 1971 with two
Plessey meters (Ramster, 1971) and at 53°27′N: 3°40′W at various times
(Table V) with Aanderaa meters. Both sets of measurements gave similar results
—a southward flow in the bottom 10 m of the water column, varying little in
direction throughout the year but varying appreciably in strength, and above this
a more variable flow, generally northward to westward. The shoreward flow near
the bottom has been confirmed by bottom drifter experiments (Halliwell, 1973)
and the two-layer nature of the flow has been accurately predicted (Heaps, 1972)
based on the horizontal density field. Both checks suggest that the uncertainties
associated with the estimate of the non-wind-driven flow shown in Figure 12A
are less for direction than for magnitude.
An estimate of the circulation of the region is obtained by adding to this flow
the response to the mean wind stress. The only available estimate of the mean
wind stress is by Hellerman (1967) and quoted by Proctor (1981) for the Irish
36 M.J.HOWARTH
Sea as 0·07 Pa eastward and 0·03 Pa northward. Using these values creates some
uncertainty since the regression equations were based on daily wind stresses at
Valley. In general, the currents calculated in
TABLE V
Mean observed currents at 53 °27ξN:3 °40ξ W, water depth 28 m: the mean observed
current at Site 1 March-April 1977 has been included, although in shallower water; all
the measurements were made with Aanderaa meters.
Mean current
Period Meter height (m) Speed (m/s) Direction (degrees)
12 June–29 June 1970 20 0·064 003
12 June–8 July 1970 13 0·036 343
12 June–8 July 1970 5 0·015 188
26 Feb.–20 Apr. 1971 20 0·033 342
26 Feb.–20 Apr. 1971 8 0·066 193
20 Apr.–3 June 1971 8 0·063 189
20 Apr.– 3 June 1971 5 0·069 188
22 Dec.–31 Jan. 1972 20 0·014 296
22 Dec.–31 Jan. 1972 5 0·063 192
31 Jan.–7 Mar. 1972 20 0·012 265
31 Jan.–3 Mar. 1972 5 0·049 192
7 Mar.–17 Apr. 1972 20 0·026 347
7 Mar.–15 Apr. 1972 5 0·026 185
22 Mar.–14 Apr. 1977 5 0·008 222
response to the mean wind stress oppose those shown in Figure 12A, so that the
combination is weak and varied (Fig. 12B) and the directions have a high degree
of uncertainty.
A summary of the low frequency currents near Sellafield based on the
measurements follows. It must be noted that the observations in general spanned
one month only, and that some of the calculations, particularly the numerical
values, might have been different if the measurements had lasted longer or been
made at a different time of the year. Most of the conclusions were highly
significant, statistically, so that the summary should, at the very least, be a
qualitative description of reality at that time.
(1) The currents were highly correlated with the wind stress measured at Valley,
Anglesey.
(2) The mean and the wind-driven currents together accounted for over 90% of
the energy of the low frequency currents.
(3) The mean current was about 0–08 m/s in the direction of 150°.
(4) The wind-driven currents were parallel to the shore (i.e. only along 150° or
330°). The maximum response occurred for a wind directed towards 060° (a
southwesterly wind) and was then of the order of 5% of the wind speed—
although the currents were related to the wind stress (proportional to the
square of the wind speed) rather than the wind speed. The maximum
response occurred for winds perpendicular to the shore (and hence the
currents) and the zero response occurred for winds parallel to the shore.
(5) During a typical storm, winds veer from southerly to northwesterly and so will
tend to drive water along 330°, opposing the mean flow. A wind speed of
the order of 10 m/s will reverse the mean flow.
(6) The magnitudes of the mean non-wind-driven and mean wind-driven
currents were of the same order but their directions were opposite, so that
the estimate for the long term mean current was weak and of uncertain
direction.
These conclusions suggest that the soluble effluent from Windscale will
oscillate, flowing southeastward parallel to the coast during weak winds and
northwestward during storms. It will eventually leave the eastern Irish Sea either
between Anglesey and the Isle of Man or to the north of the Isle of Man and then
flow generally northward out of the Irish Sea. The northward flow through the
western Irish Sea is also influenced by the winds—the flow through the North
Channel is highly correlated with the component of the wind along it (Howarth,
1982). The flow pattern in the Irish Sea is supported by the distribution of
caesium 137. It is not a slow continuous process but episodic, dominated by
storms (see also Williamson, 1956b).
NUMERICAL MODELS
Two-dimensional numerical models of non-tidal motion in the Irish Sea are
reported by Hunter (1972), Horwood (1974), Horwood & Bedwell (1978),
Pingree & Griffiths (1980), and Proctor (1981); three-dimensional are mentioned
by Heaps (1973, 1974, 1979), Heaps & Jones (1975, 1977, 1979) and, for the
eastern Irish Sea only, by Proctor (1981). The models are forced by surface wind
stresses, atmospheric pressure gradients and tides—the latter since tidal currents
are necessary for calculating dissipation. The models were developed to predict
tides, particularly the M2 constituent, and storm surges, with periods of several
days, but have also been used to investigate the dynamics of longer period flows
(Heaps & Jones, 1977; Heaps, 1979; Proctor, 1981). Two-dimensional models
predict sea levels and depth mean currents, but three-dimensional models predict
current structure as well—in the eastern Irish Sea storm surge and lower
frequency currents often have at least a two-layer structure. The model of
Proctor (1981) is discussed below since it has the smallest grid size.
The predicted response of the eastern Irish Sea to wind stresses of 0·1 Pa
towards the east and north (Figs 13, 14) is two-layered (Proctor, 1981). The
38 M.J.HOWARTH
Fig. 12.—Mean currents after the multiple linear regression between the daily current
observations and wind stresses at Valley: A, mean currents; B, mean currents plus current
predicted by the regression for the annual wind stress; T, top meter; B, bottom meter;
dashed line, 10 fm (18 m); dotted line, 20 fm (36 m).
currents near the surface are in the direction of the wind and near the bottom are
generally opposed to it, as a result of sea surface gradients. In some shallow
areas the response is, however, all in the direction of the wind, for instance near
the Welsh coast for an eastward wind and near the English coast for a northward
wind. The response is linear to wind stress amplitude and so Figures 13 and 14
can be compared with Figure 11A, B, deduced from observations. As expected
the observed currents are more similar to the computed bottom currents than the
surface currents, indeed the model predicts the bottom layer to extend to within
10–15 m of the surface. There is good agreement in the region to the south of the
Isle of Man apart from the null point observed by both meters at Rig 8, which is
not predicted in the model. The rig is, however, close to the boundary of
Proctor’s model where uncertainties are greater. The three-dimensional model of
the whole Irish Sea of Heaps & Jones (1977) shows a null point there for a
northward wind, but not for an eastward wind. Off Sellafield the observations
and the model predictions disagree for an eastward wind stress. Close to the
coast the observations indicate a strong northward flow whereas the predicted
currents are weaker and westward becoming northwestward further away from
the coast. The model results are in general supported by the model results of
Heaps & Jones (1977) although their larger grid size seriously affects the
calculations in the vicinity of the Isle of Man (at minimum there are only three
grid boxes between the island and the Scottish and Cumbrian coasts). For an
eastward wind the magnitudes of the observed and predicted currents are similar.
The predicted currents for a northward wind are, however, stronger than for an
eastward wind, in contrast to the observations.
One advantage of numerical models is their capability to resolve the
importance of different driving forces. For currents with periods of a week or
less the importance of tides and winds is clear and it is fairly simple to
disentangle them—tides have distinct frequencies and wind-driven currents are
either inertial or related to storms. For longer period currents the position is not as
clear—there are four driving forces with responses of potentially the same order.
Their relative importance in the Irish Sea has been investigated by a three-
dimensional model (Heaps & Jones, 1977; Heaps, 1979) and a two-dimensional
model (Proctor, 1981). The only observational check on the predictions is the
total flow through the Irish Sea, approximately northward (see p.
14) based on the distributions of salinity and caesium 137. The model predictions
of flow through the Irish Sea caused by three of the driving forces (non-linear
tide, density, and mean wind stress) are each northward and of similar
magnitude (each about the size of the total observed flow). There are
uncertainties associated with each of the predictions since slight changes to the
model or its boundary conditions can change the magnitude of the non-linear
tidal flow by a factor of two (Proctor, 1981) and since neither the mean density
nor the mean wind stress field is known accurately. The fourth driving force is an
elevation gradient. The models show that east-west gradients are not associated
with significant flows through the Irish Sea, in contrast to north-south gradients,
where even a small gradient will produce a large flow. To give the observed total
flow through the Irish Sea, the models predict that the mean sea level at
Portpatrick is at most 0·09 m higher than at Fishguard (Heaps, 1979), compared
with an observed value of 0·15 m (Thompson, 1979), although there are large
uncertainties associated with the observations.
The models are not yet refined enough to explain the circulation of the eastern
Irish Sea—in Heaps’s model the grid is too coarse and although in Proctor’s it is
finer, this model is two-dimensional, which, while suitable for the non-linear
tidal term, is not suitable for the others. A few comments can, however, be made.
(1) Similar results were obtained by changing the order of including the driving
forces (Proctor, 1981), implying that the four responses did not interact with
each other and so could be calculated separately and added to give the total
(as predicted by Heaps, 1978).
(2) The elevation gradient forcing did not generate a significant response in the
eastern Irish Sea away from the Isle of Man.
(3) The clockwise gyre in Liverpool Bay appears to be derived from density
gradients.
(4) The southward flow along the Cumbrian coast appears to be derived from
non-linear tidal forcing.
(5) The tidal residual based on M2+S2 was not significantly different from that
based on M2 only.
40 M.J.HOWARTH
Fig. 13.—Predicted response by Proctor’s (1981) three-dimensional numerical model of

the eastern Irish Sea to an eastward wind stress of 0·1 Pa: the currents are shown
schematically, the larger the arrow the faster the current; A, elevation in cm; B, depth
mean currents; C, surface currents: D. bottom currents.
(6) The residuals generated in the near bottom layer by the mean wind field
oppose those in (3) and (4) above, as noted for the observations.
Fig. 14.—As for Figure 13, but for a northward wind stress of 0·1 Pa (Proctor, 1981).
CONCLUSIONS
TIDAL CURRENTS
The dynamics of the Irish Sea are dominated by the semi-diurnal tides. Observed
and predicted semi-diurnal elevations and currents agree well. In the eastern Irish
Sea the weakest currents, generally elliptic, occur off Sellafield and the
42 M.J.HOWARTH
strongest, rectilinear east-west, to the north of the Isle of Man and of Anglesey.
The dynamics of sediment transport is not well known, but probably depends on
the current amplitude to some (high) power. The higher tidal harmonics then
become significant; uncertainties in observing or predicting them are, however,
larger. If the power law is cubic, then the net bed load transport will be small off
Sellafield, but large and eastward to the north and south of the Isle of Man and in
Liverpool Bay, having a pronounced spring-neap cycle.
LOW FREQUENCY CURRENTS

The strongest low frequency currents in most places occur during storms. In the
eastern Irish Sea the response is two-layered. The near-surface flow is
approximately in the direction of the wind, in a layer 10–15 m thick. The near-
bottom flow is secondary, driven by pressure gradients which have arisen from
the wind-driven flow being confined by topography. Because it is difficult to
measure currents accurately in the presence of waves, all the observations have
been made in the near-bottom layer. The models and observations broadly agree
but one area of disagreement is off Sellafield, for an eastward wind stress.
During a typical storm the wind stress veers from northward to southeastward
and both models and observations indicate that the response near Sellafield is a net
northwestward flow, the observations suggesting a stronger response especially
near the coast, and in Liverpool Bay an anti-clockwise flow.
For periods longer than 10 days the currents are generally weaker,
observations suggesting a clockwise flow in Liverpool Bay and a stronger, south-
eastward flow past Sellafield. The overall currents in the Irish Sea are weak,
northward in the western Irish Sea and shoreward near the bottom near the
coasts. In the vicinity of Sellafield there is weak stratifiction in summer. This
will probably change the low frequency flow pattern since then the surface layer
becomes de-coupled from the bottom layer. There are no published observations
or numerical model results of this. In general, the uncertainties in both models
and observations are large. For observations they would be reduced by obtaining
year (or longer) records, preferably at several sites simultaneously, and for
models by developing a fine grid three-dimensional numerical model for the
whole of the Irish Sea. The large computational requirement has so far prevented
this but it should now be possible on a computer with the power of a Cray.
MOVEMENT OF RADIOACTIVE WASTE

Soluble effluent from Sellafield will move episodically, depending on the
occurrence of storms. Initially it will move clockwise around the eastern Irish
Sea during periods of weak winds and anti-clockwise during most strong winds.
Eventually it will join the flow through the western Irish Sea and the stronger
northward movement past the west coast of Scotland.
The important gap in our knowledge is the movement of radionuclides in the

sediment. Because the processes involved are not fully understood it is
impossible to model them at present. Since the transport depends on currents
near the sea floor, a prerequisite is the measurement of such currents near the
outfall for an extended period. In the short term the movement of the
radionuclides themselves suggests it takes the order of six months for some to
come ashore near Sellafield. In the long term (some of the isotopes of plutonium
have half-lives over 1000 years) the movement is unknown.
ACKNOWLEDGEMENT
This research has been carried out under contract for the Department of the
Environment, as part of its radioactive waste management research programme.
The results may be used in the formulation of Government policy, but at this
stage they do not necessarily represent Government policy.
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Barnes, H. & Goodley, E.F.W., 1961. Bull. mar. Ecol., 5, 112–150.
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EMERGENCE OF OPTICAL
INSTRUMENTATION FOR MEASURING
BIOLOGICAL PROPERTIES
CLARICE M.YENTSCH
and
CHARLES S.YENTSCH
Bigelow Laboratory for Ocean Sciences, McKown Point, West
Boothbay Harbor, Maine 04575 U.S.A.
THE TIME-SPACE DILEMMA

In some cases, methods of research are as important as the research itself.
Historically, the oceanographer has been wed to the research vessel and its
umbilicals of ropes or wires on which sensors or collectors are suspended. This
has heavily restricted and frequently determined experimental design. Against
the background of the enormity of the oceans and its manifold physical,
chemical, and biological processes, we can honestly ask whether or not the ship-
based research technique is providing the information for the proper
interpretation of ocean environments (Fig. 1).
Remote sensing from satellite altitudes is emerging at a time when
interpretations based on sea observations can be validated. It is yet very early—
but clearly from what we have seen from SEASAT and Coastal Zone Colour
Scanner (CZCS) “the balloon is up”. We now know that biological
oceanographers must quickly move towards instrumentation that provides a
broad and rapid sampling of time and space. No longer can we be satisfied with
discrete cuvette measurements. It is unlikely that these measurements which are
widely spaced in time and space will provide further fruitful information on the
rate of processes in the oceans. We can no longer be satisfied nor can we rely on
the broad ocean boundaries featured in text-books. Ocean biologists need
instrumentation that at least matches the capability of data sampling and handling
of their chemical and physical colleagues.
We believe that optical techniques are among the most useful to arrive at this
goal. Unlike other physical measurements, life and visible light are closely
related and we, along with others (e. g. Bricaud, Morel & Prieur, in press),
believe that their combined potential has yet to be thoroughly realized and
utilized.
48 CLARICE M.YENTSCH AND CHARLES S.YENTSCH
Fig. 1.—Time-space domains for oceanic phenomena as described by Esaias (1980). A,

portrays area in square kilometres for physical events of internal waves, tidal mixing and
storms, as well as time-space relationships of algae, patches, zooplankton and fish. B,
portrays time and space coverage by various platforms used for gathering oceanographic
data; note that buoys and ships offer no advantage for synoptic measurements.
While the initial fascination and lure of the sea was promoted by the interest in
transportation and in the weird and bizarre marine organisms, eventually there
arose an effort to describe the physical and chemical environments in which
living organisms existed. The interrelationships between ocean biology,
chemistry, and physics are hypothesized from scant and sporadic documentation.
The present goal for biological oceanographers is to test these hypotheses and
measure the synergy and subtle dynamics of biological processes. Organisms,
with their complicated intrinsic responses dictated by physiology and
biochemistry bounded by genetic limits, must respond to ever-changing extrinsic
geophysical variables. An understanding of this can only be achieved by
substantial information based on distribution of life patterns and processes in
both time and space.
An entirely new class of instruments important to the biologist has evolved.
These are compatible with sampling frequencies and resolution of the automated
instruments important for chemical and physical oceanography. These
instruments are in large part optical, that is, exploit optical properties of the
water mass and/or its components. As a consequence, optical oceanography with
its once rather isolated and insulated set of researchers has become wed to
biological oceanography. This coalescence, in association with rapid advances in
electronics, laser and computer technology, has resulted in an evolution of optical
instruments which gives flexibility to biological studies in that some biological
components can be sampled in a time frame compatible to that of physical
changes in time and space. In our summary table we have taken care to highlight
the limitations as well as the advantages. We advocate that the single most
OPTICAL INSTRUMENTATION 49
important unifying characteristic of important modern instrument advances is

rapid measurement which can result in near-real-time synoptic measurements.
None of these instruments is at present fully developed. Their current impact
and challenge will probably occupy the efforts of a generation of ocean
researchers. As a consequence this contribution is not intended as an extensive
review, nor as a summary of the exciting resulting science, but it should serve as
an indication of the recent instruments born from a need to test time and space
hypotheses. Data are given for the purpose of example only. Instruments present
today will be the precursors to the devices which eventually may allow full
testing of existing and new hypotheses.
WHY ARE OPTICAL INSTRUMENTS IDEAL TO TEST

TIME AND SPACE PROBLEMS?
In the evolutionary course of photosynthesis, organisms developed antennae for
capturing sunlight which is the primary source of energy for the marine
ecosystem. These antennae appeared as pigmented proteins which absorb light in
a manner similar to coloured dyes. The pigmented proteins fill the visible
window of the sunlight’s radiation. Since none of these proteins would survive in
the presence of ultraviolet radiation, a step in their evolution must have involved
partial submergence of the cells thereby using sea water as a protective shield
prior to establishment of the atmospheric ozone blanket. But the cells could not
reside too deeply in the water column because water itself absorbs the energy
especially at the long wavelengths of visible light (Fig. 2A). Thus, the optimal
choice for the pigmented antennae had to be somewhere between the ultraviolet
and the near infrared, that is, the so-called visible window of sunlight. In the
course of their evolution, algae of one sort or another have virtually filled the
visible window with their antennae, establishing firmly their potential to utilize
practically all wavelengths in this region for photosynthesis (Fig. 2B).
But why then is the ocean not filled with these organisms? The answer to this
question is at the crux of why we measure many aspects of phytoplankton. Not
only do we depend upon understanding the physiology of the phytoplankton, but
also we need knowledge of the dynamics of the water mass movements in the
oceans.
The modern ocean is an unbalanced medium for phytoplankton growth. That
is, the light energy necessary for photosynthesis penetrates to a depth above the
reservoir of nutrients which lies in deeper waters. Thus, the upper photosynthetic
(euphotic) layer generally contains too low concentration of nutrients to support
vigorous plant growth. This situation is characteristic for stable ocean water
masses separated by a thermocline which results in two layers of different
densities. The nutrient-light imbalance is corrected only when the two layers mix,
and the occasions for mixing may occur on times scales of days to months,
depending on the source(s) of energy needed to mix the layers, and spatial scales
from metres to thousands of kilometres.
Fig. 2.—Absorption of light. A, by water absorption. B, by different algal pigments in the

windows of ‘clarity’ of water; the spectra for the pigments approximate those measured in
vivo; fucoxanthin and peridinin are superimposed.
WATER COLOUR AS A SOURCE OF INFORMATION

Light upwelling from the sea is the result of downwelling light minus the
absorption of pure water, organic (predominantly phytoplankton) particles,
inorganic particles, and dissolved yellow substance minus scattering of water,
organic and inorganic particles.
A case can be made for an apparent relationship between the absorption by
major algal pigments and the major windows of clarity in the water spectrum.
The major “clear window” for water lies between 425–475 nm and is filled with
the Soret absorption bands of chlorophylls a, b, c, and carotenoid bands from all
groups of algae found in the marine environment. The window of clarity between
525–575 nm is filled with absorption by the carotenoids, fucoxanthin and
peridinin, of diatoms and dinoflagellates, respectively, and the phycoerythrins of
red algae and cyanobacteria (=blue-green algae). The third conspicuous window
between 575–650 nm is filled by another blue-green pigment, the chromoprotein
phycocyanin. The fourth window between 665–680 nm, positioned next to a
strong water absorption band, is filled with the long wavelength absorption
bands of chlorophyll.
In natural populations, most of the information on total attenuation of light by
phytoplankton has come from comparisons of chlorophyll content and the total
diffuse attenuation coefficient; Riley (1965) pioneered the use of partitioning the
diffuse attenuation coefficient into the components responsible for the total
attenuation, namely, water, phytoplankton, and other attenuating substances.
Since then, a number of workers have used this approach to estimate the amount
of light being absorbed by phytoplankton in a water column and to estimate the
maximum theoretical yield of primary production (Steele & Menzel, 1962;

Yentsch, 1963; Bannister, 1974).
There is a considerable amount of data in the literature which has been treated
by this partitioning technique, the most extensive of which was collected at
Scripps Institution of Oceanography and analysed by Smith & Baker (1978a, b).
In general, the attenuation by phytoplankton in natural waters does indeed follow
Beer’s Law; that is phytoplankton chlorophyll would relate in linear fashion to
Kt (=total diffuse attenuation) if no detritus were present, or if the proportions of
the two were constant. Throughout the literature, there are a number of
comparisons between Kt and chlorophyll a (Yentsch, 1980). A hypothetical
relationship between the diffuse attenuation coefficient for phytoplankton added
to that for pure water shows that at a chlorophyll level <2·0 μ g/l the water
attenuation dominates; at >2·0 μ g/l phytoplankton dominates the attenuation of
light. If one assumes that the chlorophyll content in coastal waters is frequently
higher than 2·0 μ g/l, then the Kt of coastal waters is dominated by phytoplankton
if no other attenuators are present. In oligotrophic waters, where chlorophyll
content is less than 2·0 μ g/l, the water absorption dominates the Kt value. A
schematic representation is given in Figure 3.
One concludes that the overall effect of the combination of absorption by
phytoplankton and that by detritus is to give the particulate matter an apparent
absorption at short wavelengths, which is much greater than would be predicted
by phytoplankton alone (Shimura & Ichimura, 1973). Thus, at short
wavelengths, the detritus and phytoplankton ‘compete’ for light energy. On the
assumption that the short wavelength absorption is due to organic detritus, the
chances are that these substances are primarily absorbers of ultraviolet light. The
absorption of light by detritus alone is unknown. One speculation is that it
resembles the spectra obtained in deep water below the euphotic zone.
Another complexity is the fact that the spectrum of phytoplankton changes as
a function of environmental stress. Light deficiency causes increased chlorophyll
per cell as reviewed by Richardson, Beardall & Raven (1983). In some species,
nitrogen deficiency causes the decrease of chlorophyll per cell, as opposed to an
increase of carotenoids. The overall spectral effect is a high blue: red ratio
(Yentsch, 1962; Shimura & Ichimura, 1973).
LIGHT ABSORPTION BY INORGANIC PARTICLES

The overlap by organic and inorganic particles can be considerable. This can be
with respect to size (Fig. 4), index of refraction (Spinrad, 1978), as well as
absorption properties. These customarily have a combined effect.
Thus, when interpreting absorption signals, such as CZCS imagery, a variety
of conflicting interpretations can result. These effects are serious in areas of
intense tidal mixing, as demonstrated by J.Simpson and colleagues (pers.
comm.). For the case in point, the frontal zone of the western Irish Sea,
suspended sediments contribute substantially to the CZCS water colour signal.
Fig. 3.—Contribution of phytoplankton (scattering plus absorption) and water (scattering

plus absorption) to water colour for oligotrophic oceanic water, mesotrophic slope water,
and eutrophic coastal water; in some locations seston, zooplankton and/or yellow
substances can be highly significant contributors to water colour.
E.Mitchelson (pers. comm.) found reflectance ratio to be useful in detecting the
inorganic fraction of the total seston in tha geographic region.
LIGHT ABSORPTION BY DISSOLVED YELLOW

SUBSTANCES
Many areas of the world’s oceans, especially the coastal waters, are discoloured
by a dye-like material called “Gelbstoff”, a term adopted by early German
oceanographers (Kalle, 1938; Leyendekkers, 1967; Jerlov, 1976). In a general
sense, Gelbstoff appears to be u.v. absorbing compounds which overlap the
visible portion of the spectrum (Fig. 5). It is also weakly fluorescent; when
excited at 350–390 nm, it fluoresces in the blue-green (Traganza, 1969;
Duursma, 1974). As to the source of yellow substances, they have been isolated
from algae and are abundant in many salt marshes, mangrove swamps, and
estuaries. The manner and rate of release of yellow substances are not well
understood.
Fig. 4.—Inorganic and organic particle size limits from 0–200 m demonstrating
considerable overlap.
Fig. 5.—Contribution to light attenuation (per metre) of yellow substances to water

absorption at three chlorophyll levels, 2.5 μ g·l−1, 5 μ g·l−1, and 10 μ g·l−1.
Yellow substances ‘compete’ with phytoplankton for short wavelength light

and as such they alter water colour. In terms of attempting to implicate water
colour change due to the abundance of phtoplankton chlorophyll, serious
misinterpretation can occur when the chlorophyll content is relatively low as
compared with yellow substances. At high chlorophyll concentrations (i.e., those
approaching 10 μ g/l) the concentration of yellow substances is not a significant
interference.
Oceanographers have recognized the correspondence between the amount of
terrigenous discharge (Højerslev, 1974, 1980; Jerlov, 1976; Baker & Smith,
1982), the surface salinity, and yellow substances. The distribution of Gelbstoff
Fig. 6.—Logarithmic scattering diagram showing angular variability from an individual

particle, after data from Kullenberg (1968): light source is at the right.
in oceanic and coastal waters can be directly related to the freshwater inflows.
For example, the Amazon discharge discolours the adjacent ocean many miles
out to sea (Yentsch, 1971). The colour gradient decreases moving seaward from
the river mouth. One can rightly question the ‘conservative’ nature of this
substance. Why are the oceans not yellow? Although evidence is sparse, the
disappearance of Gelbstoff from the water column appears to be the result of
adsorption on particles which sink, slow microbial oxidation, and photo-
oxidation (Moreth & Yentsch, 1970).
LIGHT SCATTERING BY WATER

Scattering of light by water occurs at the molecular level once beyond the initial
refraction and reflection at the sea surface. There are two principal types of
scattering, one called Rayleigh scattering, the result being the amount of light
scattered is inversely proportional to the fourth power of the wavelength. There
is no shift in wavelength. In addition, there is Raman scattering which is
somewhat analogous to fluorescence, that is, there is a spectral shift of scattering
emitted such that the light scattered is always of greater wavelength than the
excitation source.
LIGHT SCATTERING BY PARTICLES

The scattering of light by a particle is a well-described function and is dependent
on the angle of incidence of the light beam. A logarithmic scattering diagram
showing this angular variability, after data from Kullenberg (1968), is presented
in Figure 6. For small cells, index of refraction is as important as cell size. In the
case of large particles and high index of refraction, the variability is low. Small
biological particles are often in the concentration range given in Figure 7 by
Spinrad (in prep.) and the stated size and index of refraction region. Figure 7
Fig. 7—Percentage of light transmitted at various depths for particles of 2 μ m and 5 μ m

diameter at 104·ml−1 with a refractive index of 1·01(+) and 1·03 (′ ) relative to sea water:
these values are for scattering contribution only—therefore assumes no absorption by
particle; courtesy of R.Spinrad.
Fig. 8.—Schematic diagram to scale depicting wavelengths of light used for various
excitation demands and size of particles in relationship to wavelength of light particles.
shows the attenuative effect of scattering alone, and absorption by the pigmented
cell can be just as important as scattering. That is, the effect is additive. The
change in attenuation due to the inclusion of absorption (i.e. from a relative
refractive index of 1·01 for a non-absorbing cell to 1·01+0·01i for an absorbing
cell) is roughly the same as the change obtained due to the shift of relative
refractive index in a non-absorber from 1·01 to 1·03. C
One important feature in the scattering of small particles (<1 μ m) is that the
wavelength of light is approaching the particle size (Fig. 8). Accordingly, the
Fig. 9.—The variation of scattering with particle size and wavelength from Van de Hulst
(1957): m=relative refractive index of particle; ′ =wavelength; r=particle radius;
K=scattering coefficient per particle/area of particle.
Fig. 10.—Relative scattering coefficient vs wavelength in air for various size particles
normalized at 550 nm with an index of refraction of 1·15 relative to water (after J.Williams,
1970).
variation of scattering with particle size and wavelength approaches the region of
largest oscillation of the effective scattering area coefficient as described by Van
de Hulst (1957) and presented in Figure 9. The result is that for very small
particles there is a great deal of scattering at shorter wavelengths while at longer
wavelengths there is relatively less scattering. Relative data are presented in
Figure 10, and a summary schematic representation is given in Figure 11.
Fig. 11.—Schematic representation of importance of size, refractive index and slope to

scattering measurements at forward angles and 90°: courtesy of R.Spinrad.
LIGHT EMITTED BY BIOLOGICAL PROCESSES
FLUORESCENCE EMISSION BY THE PHYTOPLANKTON

As early as 1833, D.Brewster, a clergyman in Scotland, noted a red glow from
plants under certain light conditions. By 1838 he had formalized his observations
into a discovery of “internal dispersion” in fluorespar (a natural fluoride of
calcium), quinine, and chlorophyll. G.Stokes recognized the widespread
occurrence of the phenomenon in nature and in 1852 termed the reaction
“fluorescence” and put forth what is now known as Stokes’ Law—that is, that
light resulting from fluorescence emission is always of longer wavelength than
the exciting light. The wavelength difference is called the Stokes’ shift.
Fluorescence spectral analysis had become a reality by 1868 pushed by
F.Goppelröder who recognized that fluorescent band spectra were characteristic
of specific substances. By 1871, A.von Baeyer synthesized the first fluorescent
dye, fluorescein.
With all of the landmark discoveries of fluorescence occurring over a century
ago (see Table I, compiled from Kasten, 1983), the rhetorical question is, why
has the acceptance and exploitation of fluorescence as a research tool been so
slow, particularly in phytoplankton research?
Since 1963 phytoplankton ecologists (Yentsch & Menzel, 1963) have
routinely measured phytoplankton fluorescence to estimate phytoplankton
biomass. In vivo research was pioneered by Lorenzen (1966). Yet the
fluorescence properties of phytoplankton are highly variable, and thus there has
been hesitation in using fluorescence as a measure of phytoplankton biomass.
Strickland (1968) noted immense differences between species. Kiefer (1973a)
found immense differences in fluorescence according to growth state. The

immediate light history of the cell can result in an order of magnitude change in
fluorescence response (Kiefer, 1973b; Loftus & Seliger, 1975). Yet in marked
contrast to an absorption signal, seston, detritus, zooplankton, and yellow
substances usually do little to contaminate the fluorescence signal. In vivo
chlorophyll was one of the first biological properties to be measured
continuously.
In addition to reflecting the growth state or the physiological state of the cell
and immediate light history prior to measurement, there is a great deal of
information in the fluorescent signal as described by Yentsch & Yentsch (1979).
They used the variety in fluorescence spectral signatures, both excitation and
emission, to characterize phytoplankton to taxonomic group based on pigments.
TABLE I Table of early significant advances in the application of fluorescent techniques

Year Event Individual
1833 Red fluorescence and chlorophyll D.Brewster
1838 Discovery of “internal dispersion” in D.Brewster
fluorespar (a natural fluoride of calcium)
quinine and chlorophyll
1852 Widespread occurrence of internal dispersion G.Stokes
in nature termed reaction fluorescence;
Stokes Law=fluorescent light is of longer
wavelength than the exciting light
1868 “Fluoreszenz” analyses, clear indication that F.Goppelröder
fluorescent band spectra were characteristic
of specific substances
1871 Synthesis of fluorescein dye A.von Baeyer
1887 660 fluorescent compounds frequently with K.Noack
six-membered heterocyclic ring structure
1889 Synthesis of acridine orange C.Benda
1903 Development of u.v. filters “Wood’s light” R.Wood
nitrosodimethylaniline
1904 Groundwork for u.v. absorption microscope A.L.Köhler
1908 1700 fluorescent compounds known H.Konen
1911−13 Invention of fluorescence microscope O.Hemstädt and H.Lehmann
1911 First systematic investigation of auto- H.Stübel
fluorescence of bacteria, protozoans and
animal organs
1911 Observations of auto-fluorescence in plant M.Tswett
tissues identified as chlorophyll in
chloroplasts
1914 Expansion of chlorophyll fluorescence A.Willschke
observations
Fig. 12.—Excitation (Ex) and emission (Em) spectra from natural populations in Gulf of
Maine coastal waters (from Yentsch, 1983b).
Year Event Individual

1914 First example of “vital fluorochroming” and S.von Provazek
introduction of fluorochromes at the
microscopic level
1923 Struck by beautiful fluorescent colours from F.Lloyd
accessory pigments in blue-green algae and
diatoms
1931 Discovered each plastid developed its J.von Loui
chlorophyll independently from dumbell-
shaped proplastids
1935 Used eosin and erythrosin exclusion from H.Döring
cells as vitality test
1942 Beginnings of immuno-fluorescence using A.H.Coons
fluorescein
We know from microscopic counts of microorganisms in the sea that the

populations that belong to different taxonomic groups are not in fixed
proportions everywhere in the oceans. From species enumerations, one would
anticipate that the dominance of diatoms and dinoflagellates would be obvious in
the characteristics of the bulk fluorescence spectra—and they are. For example,
note the shoulder at 525–530 nm in the excitation spectrum shown in Figure 12.
This shoulder results from the absorption of light by fucoxanthin and peridinin,
which are the accessory pigments which transfer light energy to chlorophyll a at
685 nm. The intensity of this absorption varies, presumably as a function of the
percentage of diatoms and dinoflagellates present. Because these groups are
abundant in eutrophic coastal waters, the intensity of absorption at these
wavelengths is greater in coastal waters than in the open ocean.
A strong emission peak at 570–580 nm is present in every measurement. The

association of the phycoerythrin emission with small cell size has been
confirmed by comparison of fluorescence measurements on material collected by
fine plankton nets (30 μ m mesh opening) with those made on material retained
by 0·45 μ m membrane filters (Yentsch, 1983a). The spectra of organisms
retained by the netting is characteristic of diatoms and dinoflagellates and no
phycoerythrin is observed. Phycoerythrin is observed, however, in the organisms
retained by the 0·45 μ m filter. This is due to small (′ 1·0 μ m) coccoid cyanobacteria
fluorescence originally noted by Waterbury, Watson, Guillard & Brand (1979) as
confirmed by epifluorescence microscopy.
BIOLUMINESCENCE EMISSION
When a material is heated sufficiently to give off light it is said to be
incandescent. If a substance gives off light without being heated to a high
temperature it is said to be luminescent; both bioluminescence and fluorescence
are kinds of luminescence.
In the case of bioluminescence, two ‘reagents’ within the cell and/or organism
are required. These are the enzyme luciferase and the corresponding substrate
luciferin. The spectra of bioluminesced light varies, yet is similar from all
organisms, with the bulk of the light conforming both to the maximal sensitivity
of the eye and the greatest transmission in water. Luciferin fluoresces with a
spectrum similar to the bioluminescence spectrum (see Fig. 13A). Visually there
are two gross categories of bioluminesced light: one, a discrete flash and the
other a milky glow.
WHOLE POPULATION INSTRUMENTS
BEAM ATTENUATION—TRANSMISSOMETRY
The measurement of the attenuation of light from a collimated beam that passes
through a fixed light path is a useful measurement for many studies in ocean
sciences. An optical oceanographer’s measurement is referred to as beam
transmission or beam attenuation and is defined as
where a represents the absorption of light and b the scattering of light. There are
a number of commercial instruments available to make these measurements. One
example is given in Figure 14. Generally they are lowered over the side of a
research vessel or moored at some depth. Some of these instruments have the
capability of varying the length of light path which changes the relative
sensitivity of the unit. Long light paths are traditionally used in extremely clear
open-ocean waters while shorter light paths are used in coastal areas where
turbidity is higher. Some units employ white light only, others lasers, but for the
Fig. 13.—Fluorescence excitation (Ex) and emission (Em) spectra for various groups of
phytoplankton present in abundance in oceanic waters: A, bioluminescent dinoflagellates-
luciferin, (excitation spectra similar to bioluminescence spectra); B, chlorophyll-
dominating green unicells and prasinophytes; C, chlorophyll plus fucoxanthin or peridinin,
diatoms and dinoflagellates; D, phycoerythrin containing cyanobacteria; E, phycocyanin
containing cyanobacteria; F, phycoerythrin containing cryptomonads which emit at
chlorophyll wavelengths.
most part, investigators requiring a measure of total scattering use an instrument

that is filtered to accept only the long, red wavelengths of light. Although water
types are generally characterized by the measurement of downwelling irradiance,
Fig. 14.—Schematic of transmissometer or beam attenuation meter: courtesy of Sea Tech,

Inc.
in the classical sense Jerlov’s water types, measurement of the beam
transmission provides the observer with more detailed vertical distribution of the
factors causing the attenuation in the water column. In general, this attenuation,
c, is referenced against the standard, which is the collimated light passing
through air.
The research of Spinrad, Zaneveld & Pak (1978) has demonstrated that the
distinction between total downwelling diffuse attenuation and beam attenuation
in red light is useful for determining relative amounts of short wavelength,
yellow light attenuation (yellow substance) and attenuation by particulates (see
Fig. 15). Note that in this comparison the water masses studied by Spinrad et al.
have very similar values for total downwelling attenuation (Kt), however, beam
attenuation (c) is quite different for the two water masses. Thus the Kt/c ratio is a
useful index for typing water mass and gives the observer the relative importance
for the proportions of the attenuation due to particulates as opposed to those due
to compounds such as yellow substances.
In the context of the ‘continuous monitoring’ theme of this paper the biological
oceanographer finds the measurement of c is useful primarily for profiling
attenuation properties in the water column. It has been generally used as a
companion measurement for chlorophyll fluorescence and can provide useful
information as to the vertical distribution of biogenic or organic as well as non-
biogenic or inorganic properties (Fig. 16). Therefore, c can also be measured
underway by towing the instrument or placing it in line with the fluorometer
where both units are serviced by shipboard pumping systems. Measurements of c
made in this fashion have become an important factor in determining the errors
involved in estimating chlorophyll content by water colour (Gordon, Clark,
Mueller & Hovis 1980) which is pivotal to the development of the chlorophyll
algorithm for the Coastal Zone Colour Scanner on NIMBUS G.
Although a number of workers have tried to expand the value of c so that
quantitative information as to particle size can be obtained by utilization of
different wavelengths, etc., the present limitation of the measurement is that it is
not easy to specify the nature of the material that is causing the attenuation in the
light pattern. Generally speaking the ease with which the instrument can be used
Fig. 15.—Data from Spinrad et al. (1978) demonstrating additional information on

particle distribution in the water column obtained using transmissometer vs relative
irradiance for two stations off the west coast of the Americas.
and its capability for continuous monitoring allows it to be a natural part of a
suite of instruments for analysing properties in the water column.
In vivo FLUOROMETRY AND PUMPING SYSTEMS

By far the most widely used continuous sampling device in biological
oceanography is in vivo fluorometry. Initial use at sea involved the conventional
Turner 111 Design which was a device originally designed for clinical research,
but was quickly adapted to the measurement of rhodamine dye in dispersion
studies and eventually chlorophyll measurements in natural populations. More
recent designs by Turner have incorporated features that allow the instrutnent to
be more compatible with the rigours of sea .observations and the activities
ancillary to the measurement of phytoplankton distributions. These fluorometers
are sensitive to the complete range of chlorophyll observed in the oceans. The
data are generally recorded in analog form. In some cases, the data are converted
to digital form and stored in a shipboard or small computer. The instruments are
standardized against a pure solution of chlorophyll or against an extracted
sample of mixed phytoplankton. Standardization of these units is a problem. As
Fig. 16.—Data from Holligan et al. (in prep.) in the Gulf of Maine coupling chlorophyll in
vivo fluorometry, temperature, and transmissometry profile with nutrient and irradiance
data.
mentioned previously, fluorescence emission is actually a kinetic parameter and

only partially a total index of the concentration of the pigment within the cell.
The variation in the kinetic signal with reference to total chlorophyll is a function
of a number of environmental factors, namely light, nutrients, and the amount of
degraded pigments that is in the sample.
In vivo fluorometry has been the mainstay for persons interested in mapping
the distribution of phytoplankton populations. It generally is used in a manner
which facilitates taking surface water with a shipboard pumping system, passing
it first through a unit for de-bubbling and then to the fluorometer. It can also be
used in conjunction with submersible pumps, either the deep well or surface
pumping types. In this case, multiple fluorometers are used to examine the
effects of more than one excitation wavelength. One is for chlorophyll a, one for
peridinin and fucoxanthin, and the other for phycoerythrin and phycocyanin.
This system has the advantage that it can be used in a profiling mode or readily
switched to the underway mode using a three-hole system. The array is totally
compatible with use of a transmissometer, autoanalyzer and/or particle counting
equipment such as the Coulter electronic particle counter unit. In this case, the
signals from these instruments are registered in near real time and provide the
observer with a horizontal and vertical field of these variables.
In situ FLUOROMETRY
The development of the measurement of chlorophyll using submersible
fluorometers has followed the historical path similar to the pump fluorometers.
That is, the first in situ fluorometers utilized for looking at rhodamine B and
dispersion studies were found to be easily adaptable to studies of chlorophyll
fluorescence. Most of these units used a pulsed light source which was chopped
to minimize the effects of sunlight. The fluorescence signal is viewed by a
filtered photodetector orientated at 90° to the excitation source. Most units had
depth sensors as well as temperature sensors so it was possible to profile
fluorescence as a function of temperature and depth. Comparison of the
fluorescent profiles using the Turner design and in situ fluorometers has revealed
that the response time of the Turner design tends to smooth out much of the finer
scale features of the profile. Part of this is due to the mixing within the hose
servicing the Turner design system, however, the response time of the instrument
is decidedly slower than that used by the in situ device.
In situ fluorometer profiles have far better resolution than pump profile? and
detect fine scale changes in biological structure directly comparable with fine
scale changes in physical structure. Several submersible, therefore in situ,
fluorometers have been built. Yet these instruments have been shown to have
problems of low sensitivity, therefore it has been impossible to detect low open-
ocean chlorophyll concentrations; interference by ambient sunlight, especially in
near-surface waters and/or electronic noise due to RF produced by the flashing
xenon lamp has caused problems.
In situ MULTICHANNEL FLUOROMETER

Kullenberg, Hundahl and Yentsch have developed a double excitation and
emission fluorometer which will allow profiling of excitation and emission at
multiple wavelengths. This instrument will provide the same information as three
Turner design fluorometers with different excitation/emission filters.
Multichannel in situ fluorometers permit data acquisition of appropriate
biological indices of (1) bioluminescence (based on fluorescence of luciferin
molecule, not flashing or glow), (2) the carotenoid fucoxanthin and peridinin
accessory pigments characteristic of diatoms and dinoflagellates, (3) the
biliprotein phycoerythrin and phycocyanin accessory pigments characteristic of
cyanobacteria and cryptomonads, the small (<3 μ m) but common phytoplankton,
as well as (4) the more traditional chlorophyll a generally characteristic of
phytoplankton. The recent Kullenberg-Hundahl multichannel design is sensitive
down to 0·05 μ g/l chlorophyll a which is adequate for open-ocean work. Ambient
light presents no interference problems, and the electronic circuitry is shielded
from RF extraneous signals.
The scheme of the multichannel in situ fluorometer (Fig. 17) is based on
pulsed flashing light sources, one required for each excitation wavelength. The
Fig. 17.—Design of multichannel in situ fluorometer by Institute of Physical

Oceanography, University of Copenhagen.
flashing rate for each lamp is 200 milliseconds. Mirrors are used to direct the
excitation beam through a lens which focuses the beam on a finite spot or the so-
called detecting volume. This volume is of the order of several millilitres and can
be calibrated directly for each instrument. The emission beam is then transmitted
through Plexiglass cones, focused by lenses and screened by bandpass and
interference filters and transmitted to pin-diodes and amplifiers. The peaks of the
emission signal are detected and amplified appropriately prior to entry into an
analog multiplexer. A plastic flow cuvette which fits into the view volume of the
instrument can be used for calibration and underway surface observations under
continuous flow. The entire instrument is bridled with the main cable being
seven conductor wire with appropriate winch and recorder or minicomputer on
shipboard or buoy.
BIOLUMINESCENT PHOTOMETERS
The present bioluminescence measuring devices grew out of very early
measurements made by G.Clarke who was interested in light levels in the deep
sea. He used a sensitive photomultiplier fitted into a pressure casing. At
considerable depths below the smallest levels of ambient light, Clarke observed
pulses of light which he attributed to bioluminescence. He found by moving his

photodetector, he could elicit more bioluminescent responses. Seliger, Fostie &
McElroy (1961) and Backus, Yentsch & Wing (1961) simultaneously developed
a pumped bioluminescence photometer which is basically the prototype for the
units used today. These units consist of a rapid response photomultiplier which
uses an area stimulated in a cuvette. In some cases this can be as simple as
having a photomultiplier looking at the pumping impellor; in other cases some
obstruction can be placed into the flow through the photometer (Fig. 18). Some
units record the total amount of light produced; others utilize pulsed counting
techniques and pulse height counting techniques. Reynolds (1981) exploited
image intensification.
All of these devices have been found useful for measuring bioluminescence in
the sea. The main problem is to treat rigorously the cause of bioluminescence
and to equate this numerically to some aspect of the organic biomass in the water
column. In an attempt to identify the flashing of organisms, some workers have
utilized microscopic sampling during the course of the pumping technique or
simultaneously sampling the water and counting the organisms, say
dinoflagellates, in that sample. Others have attached small nets for separating the
particular size of the flashing organisms and at present there is considerable debate
over what organisms are actually contributing to the bioluminescence in various
areas of the oceans. The central dogma, that dinoflagellates are the major
flashing source, is being challenged, especially in the regions of the open
oligotrophic oceans (Swift, Biggley, Verity & Brown, 1983).
Bioluminescence has been reviewed by Tett & Kelly (1973). The amount of
bioluminescence has been observed to vary diurnally, thus it is necessary to
select a regime of time to look at biomass distributions and bioluminescence in
both time and space.
INSTRUMENTS IN COMBINATION
Probably one of the important messages in reviewing these continuous optical
devices is to say that used together, they can give an informative data base—
simply, that the whole is greater than the sum of the parts. In the pumping mode,
it is clear that one can both continuously profile and steam, that is examine
properties horizontally and profile vertically. With devices such as the Batfish
(Herman & Denman, 1977) and the Toyo it becomes possible to profile while
underway. Because of the adaptability of autoanalytical techniques and Coulter
counting, systems of this sort can provide the widest information on the
distribution of variables in the water column. The optically based in situ profiling
devices are limited to measurements of fluorescence and beam attenuation at the
present time.
Oceanographers interested in trophic exchange have concentrated themselves
in great detail with particle size analysis and these requirements have been at
least partially met by the use of Coulter electronic particle techniques. Whatever,
Fig. 18.—Sea-water phototube assembly for the measurement of bioluminescence (from

Losee & Lapota, 1981).
Fig. 19.—Data from Pugh (1978) depicting coupling of individual particle counts from
electronic particle counter in three size ranges (10–20 μ m; 20–60 μ m; and 40–60 μ m),
with in vivo chlorophyll fluorescence and temperature profiles at a station in the North
Sea.
these data represent a bench mark on which power spectra may be calculated and
the small-scale distribution detected. There was a concerted effort by particle
counter users to have compatible in vivo chlorophyll fluorescence profiles (e.g.,
Pugh, 1978; Fig. 19) where a portion of the flow from the pumping system was
fed into a Turner Model 111 Fluorometer. As Pugh accumulated particle counts
in the various size ranges (usually for 60 s every 5 min during horizontal
profiling), the channel threshold settings were placed on the basis of the octave
or log2 scale as suggested by Sheldon & Parsons (1967a) and reinforced by Platt
& Denman (1977) and now commonly referred to as the Sheldon Spectrum.
Data are displayed as ppm reflecting volume concentration in each channel
(size range). There are predictable problems associated with the conversion of
surface area and/or equivalent diameter to an average volume concentration. On
the average, the volume concentration of a particle is inversely proportional to
the particle diameter, thus mean volume and diameter can be calculated.
Electronic counting was first introduced to enumerate phytoplankton by
Hastings, Sweeney & Mullin (1962). Further refinement into better estimates of
particle volume has greatly advanced our understanding of the marine ecosystem
both theoretically (Kerr, 1974; Platt & Denman, 1977, 1978; Silvert & Platt,
1978) and observationally (Sheldon & Parsons, 1967b; Sheldon, Prakash &
Sutcliffe, 1972).
LARGE SCALE INSTRUMENTS
LIDAR FLUOROSENSING
The Airborne Oceanographic LIDAR (AOL) (Fig. 20; LIDAR stands for light
detection and ranging) developed at the NASA Goddard Wallops Flight Station
is the primary fluorosensor in operation today. The details are summarized by
Esaias (1980). In its original chlorophyll a fluorosensing experiments, the system
used a frequency doubled Nd : Yag (garnet crystal) laser that fires a 532 nm light
pulse into the water from an aircraft flying at low altitude (500–1000 ft). The
pulses are fired at a rate of 6·25 pulses per second which gives a spatial sampling
rate of 1 pulse every 15 to 25 m, depending on the aircraft speed.
The NASA system uses 40 photomultiplier tubes to record the emission signal
induced by the laser 532 nm excitation. In its fluorosensing mode, the 40
emission channels are spectral bands, 11 nm wide, which classically have peaks
corresponding to chlorophyll a fluorescence (685 nm), phycoerythrin
fluorescence (580 nm) and a water Raman scattering channel at 645 nm. The
Raman signal is a relative measure of the number of water molecules assessed by
the laser and, therefore, is used to normalize other channels to correct for spatial
variations in attenuation (i.e., laser penetration depth).
In its LIDAR mode, the 40 channels are all set at a fixed spectral band but are
timed-gated, such that each channel represents a different depth. This gives the
system a limited capability of looking at vertical profiles. It is limited in terms of
the maximum depth from which the emission signal originates. For example, at
present if one wanted to do vertical profiling of chlorophyll fluorescence, the
LIDAR system can only profile the upper 4 m at best. Although laser light at 532
nm might penetrate much deeper than that, the returned red fluorescence is so
Fig. 20.—Schematic arrangement of LIDAR (Light Detection and Ranging) for Airborne
Oceanographic LIDAR (AOL).
strongly absorbed by the water that only signals from the upper 4 m are
received.
The first major improvement of the AOL included the addition of a second
laser. The system now has an excimer dye laser that provides an additional
excitation at 427 nm. This laser fires between the pulses of the Nd: Yag giving a
combined firing rate of 12·5 pulses per second. The latest improvement has been
to re-configure the electronics so that the 40 photomultiplier tubes record the
passive, spectral radiance signal between laser pulses. Thus, in addition to the
active fluorosensing, the system acts as a passive, 40-channel spectral
radiometer.
A challenging future goal is to exploit the differences in these measurements
to estimate fluorescence yield. The colour-based estimate is controlled by the
absorbance properties of chlorophyll and accessory pigments, whereas the
fluorescence is controlled by the absorbance of the exciting light and the
fluorescence yield of the chlorophyll. It is believed that the ratio of two such
chlorophyll measurements would give a relative measure of fluorescence yield.
Figure 21 is a series of line plots showing a comparison of passive (MOCS)
and active (AOL) remote chlorophyll estimates along a series of east-west flight
lines, spaced 10 km apart, over Nantucket Shoals. These data were collected on 8
May, 1981, between 0830 and 1040 EDT. The AOL normalized chlorophyll a
fluorescence (normalized by the Raman signal) had been converted to
chlorophyll estimates by regressing it against the MOCS chlorophyll using a
linear equation:
It is believed that the new AOL with its alternating passive-active signals can,
therefore, be used to monitor such shifts in fluorescence yield. Thus, that
indicator of primary productivity can be viewed on the synoptic scales accessible
to aircraft remote sensing along with simultaneous measurements of chlorophyll,
accessory pigments, and temperature.
SPECTRAL RADIOMETERS
As with LIDAR, aircraft used for remote sensing provide a valuable intermediate
sampling platform between ships and satellites. Used interactively with ship-
based investigations, aircraft can provide the synopticity needed to orientate the
ship relative to mesoscale phenomena, e.g., frontal systems, areas of high
chlorophyll, etc., while data from aircraft transects through a region can be
correlated with ‘slices’ through satellite images, and thus can be used to calibrate
and locate satellite data relative to the ships.
Although aircraft remote sensing techniques have advanced considerably in
recent years, their use in oceanographic investigations has been restricted
because of the high operational cost of large aircraft required to carry the
available present-day experimental instruments. Recent advances make possible
a compact aircraft remote sensing system for measuring surface chlorophyll
concentrations and temperatures that can be flown on lighter and much less
expensive aircraft.
The system consists of the following components: a commercially available
infrared radiometer; a spectral radiometer having 3, 15 nm wide bands centred at
460, 490 and 520 nm, for estimating chlorophyll concentrations; an aircraft
Loran C system for recording the position of the aircraft versus time; a marine
radio for real-time voice communication with vessels and for transmittal of data
to a shipboard receiver; and a desk-top computer which, in addition to recording
data, can display the data for monitoring input, and can collect and transmit
formatted data to the radio for transmittal to the vessel. A key component of the
system is the 3-channel spectral radiometer for estimating surface chlorophyll
concentrations. A simple 3-band algorithm has been tested and validated, both
empirically and theoretically by Campbell & Esaias (1983), for estimating
chlorophyll concentrations in real time, using raw count data without the need
for radiance calibrations, sun-angle and ambient light corrections or atmospheric
corrections.
The system is small enough to fly on a twin-engine aircraft that can be
chartered locally. Nadir-viewing components (telescope and related optics) could
be mounted on the door of an aircraft or could utilize camera ports which are
relatively common on aircraft used for photogrammetry. The system would be
transportable to the site of an experiment.
Fig. 21.—Series of line plots showing comparison of passive (MOCS) and active (AOL)
remote chlorophyll estimates along a series of east-west flight lines spaced 10 km apart
over Nantucket Shoals, northwestern Atlantic: courtesy of J.W.Campbell.
COASTAL ZONE COLOUR SCANNER

The imaging colour scanner, Coastal Zone Colour Scanner (CZCS), reported by
Hovis et al. (1980, Fig. 22) flown on the NIMBUS satellite has been the
prototype for ‘biological’ remote sensors. The NIMBUS satellite is positioned
about 600 miles above the earth in a sun-synchronous orbit. The instantaneous
field of view is about 1 km; the total swath (scanning width) is approximately
2000 km. In this imager, the spectral channels have been positioned to sense
passively back-scattered light from substances which affect ocean colour and
surface temperature. As mentioned earlier, detritus and yellow substances affect
ocean colour in addition to phytoplankton pigments, namely chlorophyll a, and
thus complicate interpretation of the results.
A team of scientists assembled by NASA, the NET (NIMBUS Experimental
Team) in general, and H.Gordon and D.Clark in specific, laboriously developed
algorithms based on statistical best-fit for correcting the collected data for the
atmospheric effects, and for estimating chlorophyll a from the detected colour
changes in surface waters. The charge of the NET experimental team was to
validate the sensor and to discern whether meaningful measurements might
Fig. 22.—CZCS (Coastal Zone Colour Scanner) configuration with five wavelength
passive sensors.
result from this optical experiment. Sathyendranath & Morel (1983) have
reviewed algorithms based on present theoretical knowledge.
As suspected, colorimetric estimates of chlorophyll are most difficult in coastal
waters where the interferences by yellow substances and suspended sediments
are the greatest. In offshore waters, however, the colorimetric estimates of
chlorophyll from two CZCS channels (443/550) correlates greater than 0·85 with
ground truth data, with the worst estimate in error by a factor of two (Gordon et
al., 1980). In addition, the algorithm has been tested by direct measurement of
light absorption in natural populations of phytoplankton (e.g., Yentsch, 1980)
and it has been demonstrated that the extracted chlorophyll can be estimated with
an error of 15% at the 95% confidence level.
Present-day and future versions of ocean colour scanners represent exciting
new dimensions for the biological oceanographer, especially in concert with
other oceanographic measurements (e.g., Allan, 1983; Apel, 1983; Yentsch,
1983b). Such can provide the means for assessment of the large-scaled
patchiness omni-present in the world’s oceans and in a manner only dreamed
about by early oceanographers (e.g., Fig. 23).
The limitations must be emphasized. In the CZCS system, it is doubtful
whether the effects on water colour due to yellow substances, seston, and detritus
can be thoroughly resolved using five wavelength sensors in the absence of
independent sea truth. An opinion shared by many is that this tool should be an
adjunct to seagoing operations—thus expanding the coverage of measurements
at sea level.
NARROW FOCUS SINGLE CELL INSTRUMENTS:

ANOTHER NEW LOOK
FLOW CYTOMETRY
Flow cytometry is a general term for the rapid measurement of particles in a
moving fluid. Information is obtained through the use of various optical
properties of particles in the 1–150 μ m size range. A variety of instruments were
developed during the 1960s and 1970s (Horan & Wheeless, 1977; Melamed,
Mullaney & Mendelson, 1979; Kruth, 1982). In these and later instruments, the
particles in a stream flow are illuminated by an intense light source. The
fluorescence and/or 90° light scatter is detected by photomultiplier tubes;
forward angle light scatter, which is some function of cell size, is detected by a
photodiode. Use of lasers permits selection of specific coherent excitation
wavelengths at high intensity which maximizes fluorescence emission.
Using laser-based flow cytometry, pigment auto-fluorescence, stain-induced
fluorescence and light scatter are used as probes to quantify subpopulations of
phytoplankton cultures and natural populations. This technique, when combined
with biochemical selective stains and immuno-fluorescence technologies, makes
possible simultaneous measurement of multiple variables (e.g. chlorophyll,
protein, DNA, forward angles, plus 90° light scatter) on individual cells and/or
particles. Measurements are made at rates in excess of 1000 cells·s−1. The ability
to process large numbers of particles permits rigorous statistical analysis for even
heterogenous natural samples.
Figure 24 is a portion of the configuration of a flow cytometer. The
simultaneous measurement of multiple variables on individual cells, providing
information on correlation among or co-occurrence of such variables at the
cellular level should not be under-estimated. By judicious selection of excitation
wavelength, dichroic mirrors and barrier filters, two natural pigment systems, or
some combination of a stain and a natural pigment system, or two stains can be
excited by a single laser and each emission measured by a separate
photomultiplier tube. A second laser allows for additional measurements and
flexibility.
Applications of auto-fluorescence to pigment group discrimination are given
in Table II. Other features useful for aquatic particles are given in Table III and a
sampling of fluorescent probes inducing fluorescence is given in Table IV. Flow
cytometry requires careful handling and/or preparation of cells and/or particles;
sophisticated instrumentation, with a variety of models currently in use ranging
from epifluorescence microscope adaptations (Olson, Frankel, Chisholm &
Shapiro, 1983) to three laser systems; and extended data analysis. The total
procedure is summarized in Figure 25. The principal manufacturers are Coulter
Electronics, Becton-Dickinson, and Ortho Instruments.
The advent of single cell analysis has permitted fast (at data acquisition rates
in excess of 1000·s−1), accurate (quantitative but relative, therefore the data axes
Fig. 23.—Data snapshot of ocean colour for spring bloom off coast of central Atlantic
States, Long Island Sound, and Nantucket Shoals during April, 1981: image has been
corrected for atmosphere and the chlorophyll algorithm (Gordon and Clark) applied at
Goddard Space Flight Center; the Gulf Stream (dark) and various developmental stages of
Warm Core Rings are evident; dark portions at right are clouds.
Fig. 24.—Configuration of optical components of flow cytometer to detect two fluorescent

variables (PMTs) as well as forward angle light scatter: emission beam is split by dichroic
mirror (D); other circles represent filters which are employed judiciously; beam stop is
necessary to prevent burnout of forward angle light scatter photodiode sensor.
must be calibrated by traditional methods), and nearly continuous (thus

permitting rate experimentation) measurements. The degree to which these
measurements are informative and thus can advance our understanding of the
oceanic micro-environment is just beginning to be investigated and appreciated.
There has been a recent revolution in fluorescent probes. In addition to
nature’s chromophores (chlorophyll a, b, and c; phycoerythrin; phycocyanin;
fucoxanthin; peridinin; luciferin; nicotinamide adenine dinucleotide (NAD);
nicotinamide-adenine dinucleotide phosphate (NADP)), a large variety of stains,
many vital, have become highly useful. Immuno-fluorescent probes (Ward &
Perry, 1980; Campbell, Carpenter & Iacono, 1983) as well as more specific
monoclonal antibodies and flow cyto-enzymology (Dolbeare & Smith, 1979) are
highly promising new ventures.
By quantifying single cells, subpopulations and variance within
subpopulations can be identified and studied in cultures, and in natural
populations (Fig. 26). Previously in oceanography, individual particle
measurements have been restricted to characterization by electronic counting; the
addition of fluorescence as a simultaneous measurement has resulted in a new
generation of instruments, a microchemical tool. Information derived from this
new technology is at present being compared with the traditional bulk
measurements which to date have typified description of plankton rate processes
in the oceanic environment (Yentsch et al., 1983).
Optimal fluorescent yield, minimum interference from auto-fluorescence,
minimum energy transfer to pigments, and uniform uptake of stains is imperative
for the central dogma—that is, that fluorescence is proportional to concentration
—to be true. Of course, this limitation too has potential for exploitation. Removal
of the pigments from fixed cells has been approached by photo-oxidation
(Yentsch, Mague, Horan & Muirhead, 1983) and solvent extraction (Olson et al.,
1983).
Development of extended data analysis has lagged behind instrument
development. Rarely have biologists encountered such vast amounts of data.
Simply reducing up to six parameter fingerprints of each cell to one
TABLE II
Excitation wavelengths of argon ion laser, and response of major phytoplankton
pigments: ×=excitation; +=positive fluorescence emission at said wavelength excitation;
−=no detectable fluorescence emission at said wavelength excitation.
Wavelength (nm) argon-ion Wavelength (nm) measureable
excitation emission
457 488 514 ′ 530 ′ 590 ′ 680
Cyanobacteria × − − −
(phycobi × − + −
lins)
× − + −
Cryptomonads × − + +
(phycobi × − + +
lins)
× − + +
Greens × − − +
(chl a) × − − +
× − − −
Diatoms × − − +
Wavelength (nm) argon-ion Wavelength (nm) measureable

excitation emission
457 488 514 ′ 530 ′ 590 ′ 680
(fucoxan × − − +
thin)
× − − +
Dinoflagellate × − − +
s
(peridini × − − +
n)
× − − +
TABLE III
Probes, in addition to auto-fluorescence from pigments (Table II) useful with flow
cytometry: quantitative non-fluorescent measurements on single particles
Parameter Measurement
FALS—forward angle light scatter (1.5– Generally related to particle size
19°)
Coulter volume/resistivity Particle volume
90° light scatter Generally related to cell surface, texture,
refractive index
Time-of-flight in laser beam Particle diameter
TABLE IV
A sampling of fluorescent stains which can be used in a quantitative manner with flow
cytometry
Stain Variable “Best” laser line Emission
measured for excitation, maximum, nm
nm
FITC
fluorescein-iso-thiocyanate Protein 488 517
SR 101 sulforhodamine Protein into 488 635
(Eastman 14318) fixed cells
Cyanine Di—O—C7 Membrane 488 504
potential live
cells
diheptyloxycarbocyanine
Cyanine Di—O—C8 to Di—O Lipids 488 emission by
—C14 several nms for
each-C-added
None-to-date Carbohydrate
FDA, fluorescein Viability live or 488 –500 green
dead
Fig. 25. Components of flow cytometer techniques: items in stippling denote instrutnent
capabilities.
Stain Variable “Best” laser line Emission
measured for excitation, maximum, nm
nm
diacetate –630 red
PI, propidium iodide Viability DNA 488, 514 625
+RNA into dead
cells only
Hoechst DNA into live
and dead cells
33258 365 460
33342 365 460
33662 365 460
AO, acridine orange DNA, RNA 488 530
(rather non-
specific) into
live and dead
cells
parameter histogram, two parameter scattergrams or three dimensional plots with

frequency of events on the z-axis is a waste of a valuable information base and
defeats the goal of multiple parameterization. New models now need to be
constructed to account for this multivariant approach—heralded as desirable by
ocean ecologists (e.g. Legendre & Legendre, 1983).
FLUORESCENCE-ACTIVATED CELL-SORTING
In addition to fluorescence analysis, some of the cyto-fluorometric instruments
are equipped with fluorescence-activated cell-sorting capabilities, a technique
originating with Bonner, Hulett, Sweet & Herzenberg (1972). The cell-sorting
capability of flow cytometry is critical both for validation of signals from aquatic
particles and for isolation of subpopulations for conducting further study.
Sorting is accomplished by setting up a sort logic (up to 24 questions to which
“yes” must be the proper response in each case). Gates are easily set on
Fig. 26. Flow cytometric analysis of natural population, 3 August, 1983, from coastal
Boothbay Harbor, Maine, U.S.A.: x-axis is log of fluoresence signal excitation, 514 nm,
emission, >630 nm; y-axis is linear forward angle light scatter, 1·5–19° (FALS); z-axis is
number of events which total 4848; picoplankton, principally cyanobacteria, dominate the
low ranges of both chlorophyll and light scatter, while diatoms and dinoflagellates
dominate the high range.
fluorescence and/or light scatter criteria. The cells are in a saline sheath.
Individual droplets are broken off by vibration of a piezoelectric crystal. A time
delay is calculated between analysis and sort mode. Then the droplet passes
through a charging collar. Droplets containing a cell and meeting pre-set criteria
are charged, others are not charged. The droplets are then passed through a
deflection plate and cells sorted right (+) or left (−) (Fig. 27) depending upon the
charge, or rejected into a centre reject vial. The time required and purity of the
sort is controlled by flow rate, concentration of desired particles in the sample
and differential in fluorescence signal; 99% purity sorts are not uncommon. The
instrument operator must determine what purity of sort is tolerable for a given
experiment and must verify sort purity using epifluorescence microscopy with
excitation and emission filter combinations most comparable to the flow
cytometer and/or sorter.
The basic instrumental design, a result of the objective of sort purity, has
resulted in computer controlled anti-coincidence feed-back loops which result in
highly pure sorts to the right and to the left. The reject container, however, is in
no way a ‘pure’ sample. Contents will include (1) particles failing to meet sort
criteria, (2) particles which meet sort criteria but are rejected due to coincidence
and/or improper spacing between droplets, (3) debris, and (4) excess sheath
fluid. To clear the reject container of particles which meet sort criteria but are
rejected due to coincidence, the reject container must be re-sorted, a process
which in some cases must be done repeatedly.
Biological oceanographers have been convinced for decades of the importance
of partitioning trophic levels. Sakshaug (1980) summarizes this nicely in his
review chapter entitled Problems in the methodology of studying phytoplankton.
He states that pelagic communities constitute numerous groups of organisms:
bacteria, phytoplankton, zooplankton, etc., with a wide range of sizes within each
group. This feature raises persistent problems with regard to the determination of
chemical properties for the various groups of organisms. The problem of
separation between groups of organisms and detritus is far from adequately
resolved. He continues, “In phytoplankton ecology, in particular when dealing
with chemical methods, it is crucial to separate groups of organisms from each
other and from detritus (dead organic matter) so that chemical data can be
assigned correctly to the various groups of organisms and a correction made for
detritus. This is one of the most difficult methodological problems in
phytoplankton ecology…. Problems increase with maturity of a community.
Thus, the simplest case to handle is a unialgal bloom and the most dif ficult one
the complex oligotrophic warm water community close to climax.”
Partitioning of natural populations, although heretofore restricted to
fractionation based on size or filter retention, has advanced our understanding of
the marine ecoystem (e.g., Derenbach & Williams, 1974; Durbin, Krawiec &
Smayda, 1975). Now, fluorescence-activated cell sorting is possible. A scheme is
presented in Figure 28. Examples of actual sort data for a cultured rather than a
natural population are shown in Figure 29.
To date there have been successful sorting experiments to partition autotrophs
and heterotrophs, based on exploiting chlorophyll plus phycoerythrin auto-
fluorescence; procaryotes from eucaryotes, based on phycoerythrin content of
procaryotic cyanobacteria; two distinct forms or species of cyanobacteria from
each other, based on phycoerythrin dominance compared with phycocyanin
dominance (Wood et al., in prep.; in fact a cell from this sort was used to
establish a clonal culture WH 8203); and viable from non-viable cells, based on
exclusion of nucleic acid stain propidium iodide by live cells.
So in approaching oceanographic questions we must be aware of the following
basic constraints.
(1) We can have two relatively pure sorts per mass of sample through the
instrument, yet some of the desired particles may appear in the reject
container.
(2) Volumes are not conserved due to sheath dilution, thus sheath fluid should
be of identical osmotic and chemical characterization to sample (basically,
Fig. 27.—Basic arrangement of fluorescent-activated cell-sorting instrumentation.

we use the sample sea water filtered through a 0·2 μ m Nuclepore® or
Millipore® membrane filter).
(3) While the instrument is exceedingly rapid, at least 1h·ml−1 of sample is
required for sorting. Just what sort time is permissible (seconds minutes,
hours, days) for appropriate experimentation will certainly vary according to
experimental objective.
In combination with the capability to partition natural populations by

fluorescence activation, there is another significant advantage to flowsorting. We
know precisely how many cells or particles are sorted into each left and right
vessel. This is important for all subsequent measurements on the sorted cells.
Thus, the 10–20% error common in cell-counting via microscopic estimates of
small aliquots is eliminated. To reiterate, we know precisely the number of
Fig. 28.—Representation of fluorescence activated cell-sorting where a protein stain is

used to identify and sort desired phagotrophic micro-flagellates and auto-fluorescence of
chlorophyll a plus accessory pigments is used to identify and sort autotrophic
phytoplankton: by narrowing autofluorescent emission criteria, cyanobacteria are sorted
from other autotrophic phytoplankton.
sorted particles, and the upper and lower limits of fluorescence intensity of each;
the sample volume, however, is neither measured nor conserved.
Sorting has been used for experimentation even when using a clonal culture so
that cell numbers can be known precisely. Such sorting is essential to establish
the minimum number of cells on which reliable bulk measurements can be
attempted. This is especially important for intercalibration of this instrument with
more traditional methods for carbon, nitrogen, and chlorophyll analysis per cell.
At the time of writing, sorting experiments have not been attempted at sea.
SUMMARY
Instrumentation has been presented with detection ranges which span fourteen
orders of magnitude of spatial scale (Table V, adapted from Denman & Markas,
1978). Optical measurement capabilities range from multiple scatter and
fluorescent properties of single cells of the small 1 μ m cyanobacteria to semi-
Fig. 29.—Flow cytometric analysis of chlorophyll per cell of 181 248 cells from a culture
of Dunaliella tertiolecta (clone Dun) sorted into: low fluorescence per cell (A) and high
fluorescence per cell (B) as depicted by sort windows (AL=A lower and AU=A upper,
BL=B lower and BU=B lower) with re-analysis of 10000 sorted cells from each fraction;
data courtesy of D.Phinney.
global data snapshots of ocean colour where the signal is dominated by

phytoplankton chlorophyll. The time scale range is far more limited, being
between milliseconds and hours. Yet with frequent sampling over time there is
potential for appreciation of seasonal, annual, and inter-annual variability. Limits
and dynamics of productive areas and times can be ascertained.
The impact of any instrumentation remains a function of sampling technique
(Fig. 30). With rapid instrumentation and resulting masses of data, the
management, sub-sampling and analysis of these data become as critical to
correct interpretation of the environment as the actual sampling method and
experimental design.
At this time, we are still uncertain as to whether the micro, meso- or mega-
scale is the most important to study to advance our meagre understanding of
ocean productivity (e.g. Haury, McGowan & Wiebe, 1978; Gower, Denman &
Holyer, 1980; Yentsch, 1982; Yentsch & Phinney, 1984). When the cellular
level dominates and physiology imposes a reaction to the physical and chemical
environment, then certainly flow cytometers, transmissometers and in situ
fluorometers will play a major rôle. When broad physical and chemical features
of the environment always dominate, then remote sensors will be the most useful
instrumentation, with flow
TABLE V
Normal spatial scales which can be sampled appropriately with various instruments
TABLE VI
Limitations and advantages of various optical instruments
Instrument Variable Platforms Major Major
measured limitations advantages
Particle Particle Ships Correspondenc Measurement
counters plus volume size e vs. on per cell
in vivo spectrum simultaneous basis; rapid
fluorometry measurement; 1000/sec
depth
resolution/m
Flow Chl a per cell; Seaside Sample size Can yield
cytometry; accessory laboratories to very small 0– characterizatio
cytofluorometr pigments per date; ship 150 μ m size n and
y (FCM) cell; Coulter potential range concentration
of pigment
groups present
in
phytoplankton;
rapid 1000/sec
Fluorescence- Validation of Seaside Low yield of Fluorescence-
activated cell- FCM laboratories to particles at activated; rapid
sorting date; ambient 1000/sec;
shipboard? concentrations; overcomes
0–150 μ m size fractionation;
range based on size
exclusively
In vivo Chl a with Ships; small Pumping Inexpensive;
fluorometry temperature, boats to causes mixing can use on any
with pumping salinity, research which limits vessel with AC/
system nutrients vessels fine scale DC current;
resolution; rapid profile 1
depth m/min
resolution 1 m
In situ Chl a with Ships with Fine scale Loose nutrient
fluorometry temperature, winch; buoys resolution; profile; rapid
salinity depth profile 1 m/min
resolution 1 cm

In situ Bioluminescen Ships with Fine scale Rapid profile 1
multichannel ce potential via winch; 7 resolution plus m/min
fluorometry fluorescence of conductor accessory
luciferin, chl a wire; buoys pigmentation;
and accessory characterize
pigments phytoplankton;
depth
resolution 1 cm

Bioluminescen Stimulated Ships; buoys An adequate Stimulated
ce photometer bioluminescen measure of bioluminescen
ce bioluminescen ce vs in situ
ce potential; levels; no
rapid 1 m/min corresponding
data; cannot
resolve
distance vs
intensity; rapid
1 m/min
Beam Light Ships; small Best when By-passes
attenuation: transmitted boats; seaside corresponding apparent light
transmissometr through given laboratory in situ particle characteristics;
y water volume, and inexpensive;
therefore total chlorophyll rapid 1 m/min;
less absorbed data are continuous
and scattered available
AOL, LIDAR Chl a and Aircraft Spectral Limited
accessory signatures; resolution with
pigments accessory depth; heavy
pigmentation; power
gross charac- requirements
terization of
phytoplankton;
little
interference
from detritus
and yellow
substances; 1
m resolution
CZCS Chl a and Satellites Interference Broad scale;
accessory from detritus, 1000 km +
pigments; seston and resolution
seston; yellow yellow
substances substances on
chl a signal;
Fig. 30.—Use of instrumentation in combination.

data reduction
costly; data
and sensor
accessibility
cytometers, transmissometers and in situ fluorometers being used for shipboard

validation and calibration, and measurement of the imposed physiology.
Whatever, light—that still poorly defined aspect of physics encumbered by the
duality of properties of both waves and particles, and the manner in which it
interacts with water and the component particles and dissolved materials—is
certain to lead us to a better understanding of biology in the oceanic
environment. The optical characteristics of light-scattering, fluorescence and
bioluminescent emission, and absorption are clues about the living organisms
which demand probing by all of us who profess to be students of the sea.
ACKNOWLEDGEMENTS
Special thanks are due to Janet W.Campbell, David A.Phinney and Rick
W.Spinrad who have made substantial contributions to this manuscript. Peg
Colby and Pat Boisvert typed the manuscript and Jim Rollins and Kim Knowlton
assisted with illustrations and photography. We are grateful for their help. Partial
support was received from NSF, NASA, NOAA/NEFC, ONR and the State of
Maine.
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MIXING AND PLANKTON: AN
INTERDISCIPLINARY THEME IN
OCEANOGRAPHY
P.TETT
and
A.EDWARDS
Scottish Marine Biological Association, Dunstaffnage Marine
Research Laboratory, Oban, Argyll, Scotland.
INTRODUCTION
An ad hoc committee of interdisciplinary studies met during a NATO workshop
on Coastal Oceanography convened by Professor H.G.Gade at Os, near Bergen
in Norway, between 6th and 11th June, 1982. Amongst suggestions discussed by
the committee was the preparation of a review of selected interdisciplinary
studies in oceanography, with the aim of providing pointers to future work. What
follows began as an attempt at such a review. It was not intended to be
exhaustive either of themes or references. In the final version we decided to
concentrate on only two topics, which are indeed closely inter-related, and to
illustrate these sparingly with references to work that seems to us to have
involved fruitful collaboration between the disciplines of physical, chemical, and
biological oceanography. A loosely ontological approach has been adopted not
only as a structuring device but because we believe in using historical
development as a pointer to topics that might hereafter prove fruitful. According
to this, scientific development results from a combination of stochastic and
deterministic processes: cf. Equation (12) (p. 114).
Since this review is aimed at encouraging collaboration amongst the
disciplines we have tried to avoid technicalities and have kept the mathematical
treatment as simple as possible. At the same time we have neglected most of the
biological (and chemical) diversity of marine planktonic ecosystems. Our main
theme is the relationship between mixing and plankton, and we have interpreted
‘plankton’ in the strict sense as those organisms whose movement depends
completely on that of the water surrounding them. Phytoplankton is that
component of the plankton that can photosynthesize and whose growth is
dependent only on sunlight and a supply of inorganic compounds of carbon,
nitrogen, phosphorus, and a few other elements. Zooplankton is the animal
MIXING AND PLANKTON: AN INTERDISCIPLINARY THEME 91
component, whose needs for energy, carbon, nitrogen and phosphorus are met by
eating other plankton.
VERTICAL MIXING AND PRIMARY PRODUCTION

A central theme in interdisciplinary oceanography has been the relationships
amongst vertical mixing, the penetration of light, the supply of dissolved mineral
nutrients, and the biological productivity of the sea. During the 1920s the
chemist A.P.Orr and the biologist S.M.Marshall studied the seasonal changes in
phytoplankton biomass in the Firth of Clyde in western Scotland. Marshall &
Orr (1927) hypothesized that, each year in the fjordic Loch Striven, a series of
mixing events brought mineral nutrients from deep water to the illuminated zone
near the sea surface, each event giving rise to a bloom of phytoplankton.
Gaardner & Gran (1927) and Marshall & Orr (1928) experimentally defined the
compensation depth, that at which plant respiration during 24 hours exactly
consumes the organic material made by photosynthesis during the same period,
and thus set the lower limit to the euphotic zone, in which illumination is
sufficient for phytoplankton growth. In most seas in temperate latitudes
phytoplankton biomass diminishes during the darkness of winter, to revive in a
great flowering in early spring. Marshall & Orr (1930) discussed the control of
the start of this “spring increase” in Loch Striven, concluding that it “is decided
chiefly by total light, which depends both on the length of day and brightness.
Only such a comparatively constant external factor could account for the narrow
limits of time within which the increase begins. Vertical mixing may alter this date
a little, but the increasing light gradually overcomes this factor and allows the
spring increase to begin. As soon as the loch becomes stabilized the increase
runs its normal course.”
In pointing to the relationship between vertical mixing, illumination and
phytoplankton growth (even though they played down the former), Marshall & Orr
anticipated the concept of critical depth, first suggested by Gran & Braarud
(1935) and Riley (1942), and precisely defined by Sverdrup (1953). Sverdrup’s
concept is illustrated in Figure 1, where it is contrasted with compensation depth.
Given an adequately deep mixed water column, there is a hypothetical depth,
zcrit, such that between the sea surface and zcrit the sum of 24-hour gross
photosynthesis equals the sum of 24-hour plant respiration. If zcrit is large
compared with 1/′ , it can be estimated from:
(1a)
where A refers to the diffuse attenuation coefficient for downwelling
photosynthetically effective irradiance in the sea between the surface and zcrit, I0
is the 24-hour mean irradiance immediately beneath the surface, and Ic is the
compensation irradiance at which gross photosynthesis just balances respiration.
Replacing Ic by RB/ξ , the ratio of biomass-related phytoplankton repiration to its
92 P.TETT AND A.EDWARDS
Fig. 1—Critical and compensation depths: the critical depth is that for which areas I and
II are equal; the compensation depth is that at which photosynthesis and respiration are
equal; based on Sverdrup (1953).
photosynthetic ‘efficiency’ (the latter defined as photosynthetic rate per unit

biomass per unit irradiance), gives:
(1b)
Sverdrup proposed that the status of phytoplankton in a mixed water column of
depth H could be determined by comparing zcrit and H. Only zcrit/H>1 allows
population growth; otherwise the respiration of phyto plankton in that water
column exceeds their total photosynthesis. This inequality includes parameters
for mixed depth, optical transparency, surface illumination, and the two relevant
biological processes of photosynthesis and respiration. The further development
of such interdisciplinary indices is discussed below. It is, however, worth noting
here that Sverdrup’s concept can be applied to a homogeneous mixed layer of
thickness h at any (mean) depth z in the sea. Only if the following inequality is
true can phytoplankton growth occur in the layer:
(2a)
ξ is the layer mean illumination, given by:
Fig. 2.—Nitrogen circulation in the euphotic zone (after Dugdale & Goering, 1967): in
some oceans, blue-green algae may ‘fix’ dissolved nitrogen gas by converting it into
organic nitrogen; the importance of this process is not adequately known.
(2b)
The inequality refers only to the possibility of growth; some other factor may be
limiting.
During much of the three subsequent decades interest focussed on these other
limiting factors, and especially on the problem of the supply of mineral nutrients
to algae in the euphotic zone. It has generally, but not universally, been held (e.g.
Steele, 1974) that nitrogen is the dominant nutrient element limiting
phytoplankton growth in the sea. Building on earlier work by marine chemists such
as Harvey (1926) and Riley (1963), Dugdale (1967) and Dugdale & Goering
(1967) formalized a theory for the control of primary production by nitrogen and
the circulation of this element through the euphotic zone ecosystem (Fig. 2).
Given a thermally stratified water column, no advection, and no significant
nitrogen-fixation by algae, the model of Dugdale & Goering may be stated as
follows. Nitrate enters the euphotic zone by turbulent diffusion through the
thermocline. Its uptake by phytoplankton gives rise to ‘new’ primary production,
some of which is consumed by zooplankton. Part of the nitrogen harvested in
this way is recycled through excretion as ammonia and further uptake by
phytoplankton. Thus, turbulent diffusion provides for a basic level of primary
production, which might be multiplied up to 10 times by continued euphotic
zone recycling. This point has recently been illustrated by Harrison et al. (1983).
King & Devol (1979) assumed equilibrium between nitrate diffusion through
the thermocline and the uptake of nitrate by phytoplankton in the euphotic zone
of the eastern tropical Pacific. They estimated the former flux (QN) by measuring
the latter. Using observations on the nitrate gradient (ξ s/ξz) in the thermocline
they then estimated vertical turbulent diffusivity (KZN):
(3a)
obtaining values in reasonable agreement with thermal diffusion coefficients
(KZH) calculated from heat flux (QH) and temperature gradient (ξ ξ/ξz) in the
thermocline:
(3b)
During the 1970s oceanographers had considerable success with models that
used only vertical exchanges to predict physical conditions in shelf seas. Such
seas are stirred by tidal streams and wind, and potentially stratified by surface
heat and fresh water. It was found that the distribution of stratified or mixed
water columns could often be predicted by the simple parameter QHH/U3. QH
refers to heat flux, H to water column depth and U to tidal stream amplitude.
Where QH can be regarded as spatially uniform, H/U3 is the main determinant of
stratification. When it is less than some critical value, the water column is always
mixed; when greater, there is stratification, at least in summer (Pingree &
Griffiths, 1978; Simpson & Hunter, 1974; Simpson, Hughes & Morris, 1979;
Simpson, 1981). Pingree & Griffiths (1978) used a tidal model to predict in
detail the distribution of mixing and stratification about the British Isles.
The strength of vertical mixing was used by Pingree, Pugh, Holligan & Forster
(1975) and Pingree, Holligan & Mardell (1978) to explain the midwater
chlorophyll maximum, an often observed feature of the distribution of
phytoplankton in coastal seas. A stratified water column can be considered as
having three layers (Fig. 3), the success or failure of phytoplankton growth in
each layer being explained in terms of light supply, nutrient supply and mixing
time scale. For a layer of thickness h the time scale is given by:
(4)
In the superficial, wind-mixed, layer A there is adequate light for plant growth,
but the water is almost completely depleted in nutrients in summer. In the deep,
tidally-stirred, layer C there is a good supply of nutrients, and there may at the
top of this layer be adequate illumination. The time scale of mixing is, however,
much less than a day, and phytoplankton do not remain long enough near the top
of the deep layer to make significant growth. That is to say that the inequality
(Equation 2a) is not satisfied in this layer, which thus does not support a growing
phytoplankton, and any plant biomass found here must have diffused out of the
thermocline layer B. In the thermocline, by contrast, there are light, nutrients,
which diffuse into the layer from below, as in the scheme of Dugdale & Goering,
and tξ is about one week, long enough for phytoplankton to exploit the favourable
conditions. In this layer, or in its sublayers, the inequality (Equation 2a) is
satisfied and this, then, is a layer supporting phytoplankton growth and biomass.
The parameter ξ ξ/R B does not take account of nutrient limitation, however, and
is thus inadequate for the superficial layer. Tett (1981) incorporated the
Fig. 3.—Mixing regimes and phytoplankton growth zones in a thermally stratified coastal
water column.
generalized Sverdrup idea and the nitrogen cycling scheme of Dugdale &
Goering into a formal mathematical model based on the lightnutrient-mixing
hypothesis of Pingree et al. (1975). This model was used to predict the steady-
state distribution with depth of phytoplankton biomass (x), nitrogen contained in
phytoplankton (N) and dissolved combined nitrogen (s), and was based on the
following equations:
(5a)
(5b)
(5c)
Here u refers to algal nutrient uptake rate, g to the rate of zooplankton grazing on
the phytoplankton, and μ to phytoplankton specific growth rate, given by:
(5d)
whichever is the smaller. The model was driven by the vertical distributionof Kz,
which was determined from observed temperature gradients, usingEquation (3b).
The Dugdale-Goering scheme was modified by definingalgal biomass distinct
from algal nitrogen content, and allowing the ratioN/x not only to vary but also to
control growth rate when nitrogen islimiting This and the threshold hypothesis of
limitation advanced inEquation (5d) were derived from the Cell-Quota model of
Droop (1968,1983), and thus from experiments on laboratory-grown algae.
The model of Equations (5) is one of several that are dominated by vertical
turbulent mixing. Others include the models of Radach & Maier-Reimer (1975),
Steele & Henderson (1976), Jamart et al. (1977) and Jamart, Winter & Banse
(1979). Like several earlier models reviewed by Riley (1963), Equations (5)
suppose a steady state, in this case for reasons connected with the
parameterization of Kz and the use of a simplified form of the Droop Cell-Quota
model. The equations were originally devised to synthesize the ideas discussed in
this section, but we have since used the model with some success to predict the
distribution of phytoplankton biomass in one shelf sea in summer. But are steady-
state, vertical process models sufficiently precise or catholic to be of much use in
interdisciplinary oceanography?
As Riley’s (1963) review implies, the assumption of a steady state in early
ecohydrodynamic models was often, and perhaps only, a numerical convenience.
In precise terms this part of the question concerns whether physical conditions
remain stable over several time scales of phytoplankton growth. Legendre (1981)
argues that phytoplankton production is favoured by the alternation of stratified
and mixed conditions. Pingree et al. (1975) also advanced a “trailing bloom”
hypothesis, suggesting that the superficial layer phytoplankton blooms often
observed in frontal regions form, during neap tides, as stratification advances
into previously mixed and therefore nutrient-rich water.
The QHH/U3 model implies that wherever and whenever there is little change
in depth, tidal stream amplitude or heat flux, there should be constancy in vertical
state. Conversely, the model predicts that changes in U in particular will lead to
changes in stratification, and hence in resulting chemical and biological
distributions. Simpson & Bowers (1981) have, however, shown that a water
column tends to retain its state once stratified or mixed and that, as a result of
this, frontal displacements due to the spring—neap cycle are in fact quite small.
A steady-state assumption for chemical distributions and primary production
in shelf seas in summer may thus be tenable. But what about the supposed
dominance of vertical processes? Simpson (1981) argued that “a satisfactory
first-order account of the distribution of stratification and fronts can be given in
terms of models of vertical mixing alone without any allowance for advective
effects”, but many authors have considered the effects of advection and
horizontal mixing on vertically structured features (e.g. James, 1981; Mork,
1981, concerning frontal regions in coastal seas), and Dooley (1981), in particular,
has suggested that a current flowing from a mixed, nutrient-rich region into a
stratified region might give rise to an increase in productivity in the latter. In
upwelling regions, of course, the distribution of plankton cannot be explained
without explicitly considering vertical and horizontal advection (e.g. O’Brien &
Wroblewski, 1973; Howe, 1982).
There are several approaches to the question of whether horizontal processes
play a generally significant part in the distribution of plankton and dissolved
substances. We examine on with the following equation for the processes

affecting phytoplankton biomass:
(6)
where y stands for horizontal distance, v for mean horizontal velocity and Ky for
horizontal diffusivity. In coastal seas v, after removing the effect of tidal
oscillations, might be 0·1 to 0·01 ms−1, Ky 0·1 to 10 m2s−1, and KZ 0·00001 to
0·01 m2s−1. Horizontal biomass gradients might be of order 0·0001 to 0·001 mg
chl m−4, and vertical gradients 0·01 to 1 mg chl m−4. The second derivatives can
be estimated by dividing the gradients by the relevant length scales, which are
1000–100000 m horizontally and 10–100 m vertically. The magnitudes of the
terms in Equation (6) are thus:
horizontal advection : 10−4 to 10−6 mg chl m−3s−1

horizontal mixing : 10−5 to10−10 mg chl m−3s−1
vertical mixing : 10−3 to 10−9 mg chl m−3s−1
Hence, it is likely that vertical mixing sometimes dominates the distribution of

biomass in coastal seas, but regard must also be paid to horizontal advection, and
an exact conclusion requires a knowledge of velocities and diffusivities in the
region of interest.
One problem is not only measuring diffusivity but also properly representing a
process whose nature is chaotic, and we believe that advances in this
interdisclipinary field depend upon the resolution of these difficulties. Turbulent
diffusion is often treated through a statistical analysis of the instantaneous
products of fluctuating velocities (e.g. Pond & Pickard, 1978), leading to
simplification by the application of a Fickian relationship (such as that of
Equations (3)) which is strictly correct only for molecular diffusion. This
simplification assumes that the behaviour of dissolved or particulate components
of sea water can be broken down into a representation of their average
distributions by a gradient and a representation of the process of turbulent
exchange by a single coefficient of diffusivity. The limitations of this treatment
are well known (for introductory discussions see Smith, 1975, and Rodi, 1980)
and an alternative is to follow the ‘random walks’ forced on each member of the
plankton or each packet of sea water by a turbulent environment, averaging only
after this analysis. Woods & Onken (1982) have recently applied this approach
(which they term “Lagrangian-ensemble” by contrast with “Eulerian-continuum”
models exemplified by Equations (5)) to the Sverdrup problem of the start of the
spring increase. Their model follows the trajectory and light-controlled growth
of an individual phytoplanktonic organism in a complex vertical environment. In
general its predictions support conclusions drawn from Eulerian-continuum
models, although this need not be the case. As Woods & Onken point out,
“averaging non-linear equations before integration does not give the same
Fig. 4.—Stratification and depth-scaled-by-transparency diagram, slightly altered from

that of Bowman et al. (1981): the vertical axis gives the number of optical depths in the
water column; the stratification index a is based on sea-bed depth H and depth mean tidal
stream amplitude U, and is calculated according to Simpson (1981) rather than Pingree
(1978); the arrow represents a typical annual cycle of environmental conditions and
dominant phytoplankton in temperate seas.
answer as averaging them after integration. The latter procedure is correct.” In

effect, because of the many non-linear processes of growth, predation, and
environmental interaction, the history of the mean individual is not a
representation of the mean history of individuals. In the past, the complexity of
the processes has limited attention to the history of the mean, in the hope that
this would represent the mean history. At a time when digital computers allow us
to focus on the detailed history of many individuals in an ensemble taken to be a
model of a developing population, the importance of this approach, exemplified
by the Lagrangian ensemble, cannot be overstated. There are thus compelling
reasons for extending it.
All the treatments discussed so far have dealt with phytoplankton not only as
“passive contaminants of water motion” (Fasham & Pugh, 1976), but also as
homogeneous green stuff. Diversity of organisms is, however, a characteristic
feature of biological systems, even though it has so far proved difficult to explain
convincingly why there are so many species of plankton. Gause’s “exclusion
principle” postulates that, in the long term, only one species can occupy each
ecological niche. Hutchinson’s “paradox of the plankton” (1961) arises because
there do not seem to be sufficient niches in the water-column environment to
support the diversity of organisms observed there. Bowman, Esaias & Schnitzer
(1981) drew on theory from Margalef, Estrada & Blasco (1979), Pingree (1978),
and Pingree et al. (1978) to investigate the relationship between physical factors
and the dominance of the phytoplankton by different sorts of microalgae.
Hutchinson (1957) thought of an ecological niche as a hypervolume in which
each dimension refers to a quantifiable environmental property important to the
species in question. Bowman et al. (1981) defined two new dimensions (Fig. 4)
to such a hypervolume by considering stratification, based on the Simpson-
Hunter H/U3 index, and water-column depth scaled in relation to transparency
(ξ H). Domains representing typical environmental conditions were plotted on the
stratifiction-depth plane for each of the main groups of phytoplankton that
succeed each other through the year. Bowman et al. (1981) were able to show
that samples from Long Island Sound and dominated by diatoms or by
microflagellates did indeed plot in the right regions of this diagram. The next
step, it would seem to us, might be the addition of a third dimension representing
nutrient supply, perhaps making use of the Dugdale-Goering scheme and the
ratio of ‘new’ to ‘regenerated’ nitrogen.
A final problem of the vertical domain involves sinking. Consideration of this
process is relevant not only to phytoplankton production but also to any
investigation of the movement of particulates in the ocean. Steele & Yentsch
(1960) and others have proposed models that explain midwater maxima in
phytoplankton concentration as the result of sinking, whereas the light-nutrient-
mixing hypothesis of Pingree et al. (1975) and Tett (1981) explains them by
growth.
In an environment of uniform vertical mixing:
(7a)
where S is a sinking rate. Given a steady state and negligible growth and grazing,
it can be shown that the ratio of biomasses x1 and x2 at any two depths z1 and z2
is given by:
(7b)
That is, for any sinking rate there is an equilibrium biomass gradient that allows
sinking to be balanced by turbulent mixing. Given S of 2 m/day and Kz of 50 m
sq/day in a wind-mixed superficial layer, the resulting gradient of biomass is of
order 50% in 10 metres: not a great deal. Boundary conditions are important,
however, and if a layer with high diffusivity is underlain by one with low
diffusivity, the latter will for some time act as a trap for sinking particles.
Bienfang, Szyper & Laws (1983) showed that some planktonic diatoms sink
more slowly at low illuminations typical of the lower part of the euphotic zone.
They point, however, to the importance of size. Subtropical phytoplankton are
mostly small and in their case there is “little need to invoke sinking rate
variability to explain maintenance of deep chlorophyll maxima”, whereas
“sinking rate deceleration probably plays an important rôle in the development
of subsurface chlorophyll maxima in temperate waters having a shallow mixed

layer, a well-developed pycnocline and phytoplankton populations characterized
by the abundance of larger-celled organisms.”
In the model of Bienfang et al. (1983), as in the review by Walsby &
Reynolds (1980), sinking is seen mainly as a property of the organism; we,
however, prefer to emphasize the interaction between sinking and turbulence in
the determination of distribution. There may be seasonal differences; as Woods &
Onken (1982) discuss, spring in the ocean is typified by hour-to-hour and day-to-
day variation in the depth of the thermocline, giving rise to conditions in which
phytoplankton may accumulate for a time at a temporary thermocline, to be
stirred back into the mixed layer when an increase in turbulence extends the
latter downwards. This leads to the suggestion, in some ways quite contrary to
the steady-state hypothesis advanced above, that some physical variations may
be of crucial importance to the distribution of particulates in the ocean, giving
rise to changes in the concentration of the latter of a magnitude much greater
than the underlying physical change. This takes us into the realm of stochastic
and non-linear processes, and perhaps one of the most fundamental questions for
interdisciplinary oceanography to resolve in relation to vertical processes,
therefore, concerns the relative frequency of conditions that can be treated as
steady-state and those that are dominated by diverging perturbations.
DISPERSION, PATCHINESS AND SCALES

Whenever plankton secure food in excess of their maintenance requirements,
individual growth occurs. Reproduction may lead to population growth but such
a patch of growing plankton is subject to dispersion. An important theme in
interdisciplinary oceanography has involved the relationship between physical
dispersion and chemical and biological patchiness in the ocean. This relationship
has been investigated through the idea of critical length scales and through a
search for significant covariance between physical and chemical or biological
variables, sometimes after transformation into the frequency domain.
The starting point has often been a simplified version of Equation (6):
(8a)
Thus, Kierstead & Slobodkin (1953), and Skellam (1951), considered only
horizontal mixing and the intrinsic rate of increase of phytoplankton. A small
patch has a lot of edge in relation to its area. Since population growth is
proportional to area and dispersion to edge, such a patch may lose organisms by
diffusion outwards into the background faster than the population can grow.
There is a critical length-scale lc at which population growth just balances
diffusion; this scale defines the smallest size of patch that can continue to exist.
Kierstead & Slobodkin showed that for a circular patch:
(8b)
Thus for μ of 0·1 to 1·0 per day and Ky of 10000 to 1000000 m2 per day, the
critical patch diameter is between a half and 10 km.
Okubo (1978a) reviews the further development of this approach.
Wroblewski, O’Brien & Platt (1975) and Platt & Denman (1975) included the
effect of grazing; in our terms μ is then replaced by :
(8c)
where the parameter g is, as before, the phytoplankton-specific rate of

zooplankton grazing, with the same units (reciprocal time) as μ . When the
patch must, obviously, vanish. The effect of grazing is clearly to require a larger
critical length for a given K and μ than does the Kierstead-Slobodkin model.
As pointed out earlier, a Fickian description of turbulent diffusion is not
always adequate. The value of Ky can be shown to increase with scale, and this
effect was used by Okubo (1971) in an empirical model of critical scale
(8d)
where k is an empirical constant, value 0·0687 cm0·85 per second, akin to (but
dimensionally different from) diffusivity. The model predicts lc of 17 to 1·1 km
for μ from 0·1 to 1·0 per day. Most of the models reviewed by Okubo (1978a)
lead to predicted values of lc between 1 and 50 km depending on growth and
grazing.
Okubo (1972, 1978b) examined the effects of advection on patch size. A
convergence increases the ability of phytoplankton to grow in the face of
diffusion, whereas a divergence makes patch survival less likely. Indeed, if v
refers to the absolute velocity of divergence, a patch can persist only when
. In general:
(9a)
where
(9b)
A positive sign in Equation (9b) refers to a convergence, a negative sign to a

divergence. Margalef et al. (1979) viewed the parameter as “production
potential”, a measure of a patch’s tendency to expand into its surroundings. The
equivalent vertical parameter can be deemed to refer to a patch's ability to
survive sinking, sinking rate replacing advective velocity in Equation (9b). Both
parameters have the dimensions of speed and may thus be seen as measures of
the rate of propagation of the growth phenomenon into the surrounding fluid.
Okubo (1980) considers these matters in detail.
These treatments are reminiscent of Sverdrup's (1953) approach to critical

depth. lc is a single parameter that depends upon physical and biological
components and is employed in an inequality to determine patch survival or
death. As the reasoning behind Sverdrup’s idea has been developed into
mathematical models that predict phytoplankton biomass as a continuous
function of time and depth, so the arguments leading to critical length scale can
be developed into models that predict biomass as a continuous function of time
and horizontal distance.
Such a model has been described by Dubois (1975a, b). In addition to terms for
advection and eddy diffusion in the two horizontal directions it employs the
Lotka-Volterra equations familiar to population biologists (see for example
Slobodkin, 1962) to describe the interaction between zooplankton and their
phytoplanktonic prey. In our terms the model is:
(10a)
(10b)
where x1 refers to phytoplankton and x2 to zooplankton biomass, and the operator
refers to a vector of horizontal gradients: thus K x1 implies
, where y1 and y2 are the two horizontal directions. m
refers to zooplankton mortality, perhaps as a result of predation by larger
animals. (1—e) refers here to the efficiency with which grazed phytoplankton is
converted to zooplankton. All variables are averages over depth and over several
tidal cycles.
Dubois used the model to simulate the development of patches of zooplankton
and phytoplankton in the Southern Bight of the North Sea, for which estimates of
residual currents v were available from the mathematical model of Nihoul &
Ronday (1975). The results are interesting. “Starting from an initial small patch
of prey-predator populations, numerical simulations show two distinct phases: (i)
an ‘explosive’ phase corresponding to a bloom of phytoplankton and, (ii) after
that, a decrease in the quantity of phytoplankton at the centre of the patch leading
to a ring structure. The ring propagates in increasing its radius with constant
intensity and velocity. The prey behaves like an ‘activator’ and the predator like
an ‘inhibitor’. The ring is thus similar to an active wave. When two waves meet
each other, the simulation shows their ‘annihilation’” (from Dubois, 1975b).
After 20 simulated days the ring diameter was of order 100 km.
Dubois cited observations by Wyatt (1973) that appeared to confirm the
predictions of ring structure. Although there is a scarcity of the repeated synoptic
observations on phytoplankton and zooplankton needed to verify Dubois’ model,
it nevertheless sheds some useful light on the problem of zooplankton grazing in
the sea. Laboratory experiments show a grazing threshold, a concentration of
phytoplankton below which zooplankton do not graze. In many cases the mean
concentration of phytoplankton in the sea is less than this threshold. Patchiness
Fig. 5.—Spectral analysis of changes in the abundance of the diatom Skeletonema

costatum in Loch Creran, Scotland, in 1979: the upper diagram shows the data and the
best-fit Fourier series plotted against time; the Fourier series, with ten pairs of
coefficients, was fitted using a program supplied by Hewlett-Packard Ltd for their 9825
microcomputer and based on algorithms in Acton (1970) and Hamming (1962); the lower
diagram shows the variance for each coefficient-pair plotted against period.
may offer a solution to this difficulty, so long as there are an adequate number of
phytoplankton patches exceeding the grazing threshold. The results of Dubois’
simulations suggest, however, not an active exploitation of passive
phytoplankton patches by zooplankton exploiting current shear for their transport
between dinner tables (see e.g. Hardy, 1970), but a simpler and more convincing
dynamic interaction of the growth of plants and animals.
Patchiness has so far been treated deterministically. But because of the rôle of
chance in the life of planktonic organisms and because of the ‘random-walk’
nature of turbulence, patchiness might better be examined through statistical
aggregate properties such as variance, rather than by predicting the behaviour of
a single, identified or typical, patch. Earlier statistical treatments (reviewed by
Cassie, 1963) often used as data the number of planktonic organisms per sample,
and compared the observed frequency of different sample abundances with those
predicted by models of physical, biological, and statistical distribution. Such

analyses indicated contagious (clumped) distributions of plankton—that is,
patchiness—on many scales, but they seem to have led to no penetrating insights
concerning the factors responsible for the distribution of marine organisms,
perhaps because it became evident that sampling was generally not (and might
never be) adequate to distinguish amongst conflicting hypotheses about the
effects of these factors (see Pielou, 1969).
Fasham (1978a) objects further to an analysis based on numbers per sample,
and he and Platt (1978) review an alternative approach, that of spectral analysis.
This has typically been applied, in interdisciplinary work, to series of data
collected with continuously recording instruments mounted on or towed by a
moving ship. Phytoplankton chlorophyll concentration can be estimated from the
red fluorescence emitted by phytoplankton when illuminated with blue light; in
vivo fluorometry (Lorenzen, 1966) has become a powerful tool for examining the
distribution of phytoplankton, and lends itself to the collection of continuous
data-series. Spectral analysis is familiar to physical oceanographers through
wave-height analysis and in the description of turbulence. Biological
oceanographers may, however, find it easier to approach the topic through
analysis of time-series (see e.g. Jenkins & Watts, 1968; Chatfield, 1975). An
example is given in Figure 5. The points in the top graph represent estimates of
the abundance of the diatom Skeletonema costatum in Loch Creran in western
Scotland during 1979, based on cells counted microscopically in a weekly
sample from the loch.
Clearly, the diatom’s abundance varies with time in a way that seems partly
regular. Fourier analysis offers one method of resolving the time-series data into
components, each component representing the variation occuring at a particular
frequency or wavenumber. If D is the period for which data are available for the
time-series x(t), then:
(11)
where each pair (n) of components in the summation refer to a particular

frequency n/D or period D/n. is the variance for that frequency, and the
mean amplitude of variation is given by the square root of the variance.
The smooth curve fitted to the Skeletonema data is drawn from such a Fourier
series. The variances are plotted as a discontinuous spectrum against period in
the lower graph (Fig. 5). If the original data were continuous, then the spectrum
could be made continuous. It represents a transformation of a function in time x
(t) into a function in frequency space, with the hope that the transformed function
will be easier to interpret than the original. Thus, the peaks in the Skeletonema
spectrum might be related to the frequencies of time-varying environmental
conditions affecting the diatom or—it must be admitted—to the sampling
procedure, in Loch Creran.
Denman & Platt (1975), Denman (1976), Fasham & Pugh (1976), and others,
applied spectral analysis to series of continuous measurements of chlorophyll
and temperature, obtained either by towing instruments behind a moving ship or
by recording time-series from instruments suspended beneath a stationary vessel.
They found that the chlorophyll and temperature variance spectra were generally
similar at wavelengths greater than 100 m. (In this as in many cases a time-series
has been converted into a spatial series, by assuming the spatial distribution to
remain ‘frozen’ during the sampling time.) Thus, with some exceptions, “most of
the observed variance in the chlorophyll is attributed to internal waves and
vertical mixing effects” (see Denman, 1976), and “…over space scales between
40 m and 1 km, phytoplankton behaves as a passive contaminant of fluid
motion” (see Fasham & Pugh, 1976). That is, on these scales, nothing
distinguishes phytoplankton from green dye added to the ocean. Physical
processes occur too rapidly for phytoplankton growth to be of any consequence.
Fasham (1978a, b) and Platt (1978) review this work. Fasham (1978a) considers
stochastic models that might generate the observed variance spectra. It is for
example possible to add a stochastic term ξ (t) (one that varies randomly with
time) to the Kierstead-Slobodkin Equation (8a):
(12)
A variance spectrum for x(t) transformed into the frequency domain can be
obtained if the variance spectrum of ξ (t) is known. The simplest assumption is
that e(0 is a purely random time-series, with any value (between specified limits)
equally likely to occur in any time interval. This is ‘white noise’ and the variance
of the series is independent of frequency. The predicted variance spectrum for
this model resembles spectra observed for chlorophyll, but after analysing other
models Fasham concludes that “considerable caution should be used in the
interpretation of spectral slopes. For a given model this slope may change with
time, in the case of the spring bloom, and also, in the case of zooplankton counts,
may be critically affected by the sampling methods.”
Platt (1978) also discussed spectral theories of plankton patchiness, and
pointed to the problem of knowing what value of μ to use in these models.
Despite these difficulties in the spectral approach, one general and important
conclusion has emerged (Denman & Platt, 1976; Platt, 1978). Plankton behave
as passive contaminants of the fluid flow only on certain size scales; on other scales
biological features like the tendency to grow, or to be eaten, or to migrate
vertically, become important. Platt (1978) uses ′ to refer to the physical time-
scale of turbulence. It is the time taken for eddies of a given length-scale to
transfer their kinetic energy (the variance of measured velocities within the
eddy) to eddies of half the size. is here used by us to refer to the realized
rate of growth of phytoplankton, net of grazing and other effects.
In the subrange where “structures in the phytoplankton
distribution…are destroyed by mixing into a much larger volume of fluid as the
Fig. 6.—Time and space scales for plankton (phyto-, P; zoo-, Z), nekton (F) and
turbulence in the ocean (from Steele, 1978).
kinetic energy is transferred to smaller scales. Reproduction has a negligible

effect and the spectral shape for chlorophyll should not be different from that
predicted for a conservative passive scaler, such as temperature” (Platt, 1978).
In the subrange where “features in the phytoplankton distribution
are accentuated by reproduction before the eddies transfer their energy to smaller
scales. Reproduction cannot now be negelected and the chlorophyll spectrum is
expected to differ from that predicted for temperature” (Platt, 1978). Although
Platt does not argue this, the subrange where ′ is roughly equal to
clearly corresponds to the critical length scale of a plankton patch, and is thus
likely to refer to spatial scales of 1 to 50 km or time scales of 1 to 10 days.
The topic of scales of physical, chemical, and biological variation in the ocean
is discussed by Steele (1978), Legendre (1981) and Nihoul (1981), amongst
others. Figure 6 is derived from Steele (1978) and shows the typical time and
space scales associated with the plankton and nekton. Onto this diagram Steele
plotted a relationship derived from Okubo (1971) and based on observations of
increases in the mean size of dye patches with time after point source injection of
the dye. This line specifies one time-space relationship for turbulence. The
biological and physical time-space relationships appear similar. Does this
suggest that, disregarding all other complexities and the effect of behaviour,
biological material is smeared in its own lifetime over a scale determined by the
physical processes operating during that lifetime? Or, that different populations,
separated too far (in the sense that physical processes will fail to bring them
together in their lifetime or within important behavioural time-scales), will
develop independently and hence remain distinguishable? Steele does not attempt
to answer these questions but proposes instead that “patchiness might be seen as
a deviation of the biological spectrum from the physical spectrum of turbulence
rather than as increases or decreases from a uniform spatial distribution”.
Perhaps the smallest scale that has been of concern in production studies is that
associated with microzones of nutrient enrichment in the sea. These microzones
result from the excretion of ammonia and other nutrients by zooplanktonic
organisms, and have length scales of order 10−2 to 10−5m (10− 3 to 10−7m
according to Williams & Muir, 1981). Some marine biologists (e.g. Goldman,
McCarthy & Peavey, 1979) have suggested that uptake of nutrients from these
enhanced microzones is a process that may allow phytoplankton to grow in
otherwise nutrient-depleted waters. Jackson (1980) and Williams & Muir (1981)
consider the dynamics of these patches. Even if dispersion takes place by
molecular diffusion alone, with a dispersion coefficient of order 10−9 m2·s−1, it
can be shown that “there cannot be enough of these patches, nor can they persist
long enough to be of importance in maintaining primary productivity in the
ocean” (Williams & Muir, 1981). This conclusion can be also reached by a more
general argument about scales. The time-scale of nutrient uptake by
phytoplankton is of order 0·01 to 0·1 day, one or two orders of magnitude faster
than growth (e.g. Droop, 1968). Figure 6 indicates a spatial scale of about 10 m
corresponding to this time-scale. Only a whale could provide such a microzone!
DISCUSSION AND CONCLUSIONS

This review has dealt with plankton and mixing. We conclude that a surprisingly
simple theoretical treatment of plankton is able to explain many aspects of the
distribution of planktonic organisms as resulting from turbulence or advection
acting on organisms without independent powers of movement. For many
purposes photosynthesis, respiration, mineral nutrient uptake, and nutrient-
controlled growth can be treated as bulk properties of the phytoplankton and as
sufficient to explain its growth. Zooplankton are larger and live more complex
lives than the plants; nevertheless their distribution and abundance can
sometimes be modelled in a similar fashion, using simple bulk properties relating
to grazing and food conversion efficiency.
We have discussed the applicability of steady-state, vertical process, models
(pp. 105–109). Such models allow reliable physical predictions. Further work is
needed on their applicability to chemical and biological oceanography. Methods
include model validation or the construction of budgets; a recent investigation by
Harrison et al. (1983) used the budgeting approach to conclude that a steady state
does indeed prevail in nitrogen cycling in the Middle Atlantic Bight in summer.
The H/U3 type of model is inadequate in itself to predict plankton distribution,
but the vertically continuous models described on pp. 104–105 are numerically
cumbersome and require perhaps unwarranted assumptions in order to
parameterize vertical mixing coefficients. J.Simpson (pers. comm.) has,
therefore, suggested that an extension of an H/U3 model to three layers
exchanging water and heat might suffice as an adequate basis for predicting
primary production from a few physical parameters, including depth, tidal stream
amplitude, wind stress, and surface heat influx, without requiring any explicit
knowledge of vertical turbulent diffusivities. Another powerful approach is the

use of a stratification predictor such as H/U3 or of observed bulk stratification as
one of several dimensions defining the conditions under which ecologically
different groups of phytoplankton may flourish.
It appears that much, but not all, can be explained by models that describe
water and plankton in terms of average properties. Recent large decreases in the
cost/performance ratio of digital computers now make it feasible to examine both
turbulence and phytoplankton growth using discontinuous models whose units
are the individual organisms or packets of water. These units are made the
subjects of non-linear and sometimes semi-random processes. This topic needs
further interdisciplinary exploration; it may be that the results of “Lagrangian-
ensemble” models are sufficiently close to those of “Eulerian-continuum”
simulations of plankton for continued use of the latter. But we doubt this. Even
in the trivial case of two initially coexistent populations with different biological
rates, it is clear that the various conditioning inequalities we have discussed may
be satisfied for one but not for the other. The developments of the populations
would then be divergent and could not be discussed in terms of some imagined
population with contrived mean biological rates. Conversely, selection may
operate to ensure that ‘the plankton’ tends always to exploit the available
resources, and in this case the continuum models might be adequate for
predicting total biomass and production under steady-state conditions, ensemble
models being needed to describe transient states and the distribution of
individual species.
Although modelling has played an important part in interdisciplinary
oceanography, we have, like Steele (1974), neglected the algebraic and numerical
aspects of models in favour of the ideas embedded therein. The volumes edited
by Goldberg, McCave, O’Brien & Steele (1977) and Platt, Mann & Ulanowicz
(1981) should be consulted for references to and details of recent models in
biological oceanography.
Our discussion of vertical mixing and primary production (pp. 100–109)
concluded with a question concerning the relative importance of ‘steady-state’
and ‘perturbed-and-diverging’ conditions (p. 109). ‘Catastrophe theory’ contains
generalized accounts of systems that may have several values of each state
variable for a set of single values of the driving variables. The mathematical
treatment can provide elegant explanations of systems that switch suddenly from
one state to another or which display ‘memory’—meaning that to describe
adequately their present state requires some information on previous states, even
if the present state is stable. Deakin (1978) provides an introduction to the theory
and discusses (Deakin, 1980) applications in biology and the social sciences. In
order to be useful the approach must lead to predictions that are not otherwise
apparent. The discussion by C.Hearns in Simpson (1981) suggests that the
question of the stability of tidal fronts might be examined in this way, but it seems
probable that a more conventional approach is adequate to deal with the physical
system. Since catastrophe theory (Deakin, 1978) can represent the behaviour of a
complex system with a few control variables, it may thus be most useful in
oceanography in describing the biological consequences of bistable physical
systems, such as fronts, or of systems where an alternation between two states
results from interactions amongst physical and biological components.
A catastrophe theory of prison riots (Zeeman et al., 1976) has been much
discussed (see Deakin, 1980). It is hypothesized that as the values of two driving
variables (measuring the behaviour of the guards and the state of mind of the
prisoners) change smoothly, small perturbations may cause the system to switch
abruptly from a state of quiescence to one of riot, or back. Can red tides of toxic
phytoplankton, and associated fish kills, be explained in analogous terms? Non-
linear processes, such as aggregation by vertical migration, may be important in
the formation of a red tide of, for example, the dinoflagellate Gyrodinium
aureolum, and in the case of the salmon kills reported by Jones et al. (1982) it
seems possible that synergism between the effects of the dinoflagellates on the
fishes and those of the fishes on the dinoflagellates led to the death of all. An
explanation in terms of catastrophe theory would, presumably, have two parts.
The first would be the development of an adequate algebraic model for the
growth, distribution and toxicity of red-tide-forming species. The second stage
would be an examination of the general mathematical properties of this model
with an added stochastic component.
‘Scale’ is a vital concept in oceanography (see pp. 109–116). Nihoul (1981)
made a plea for hydrodynamics to provide information on physical processes on
time and space scales relevant to the main chemical and biological processes.
The establishment of these scales is, in the first instance, the responsibility of
chemical and biological oceanographers, but doing so clearly requires close
collaboration with the physical discipline, as demonstrated in studies of patch
size. Some physical processes occur on scales of little biological or chemical
interest, and vice versa; our own plea is for oceanographers of the three
disciplines to establish those scales on which they can work together at sea.
Shelf-sea fronts have since the middle 1970s provided good sites for such
collaboration (see for example Bowman & Esias, 1977; Swallow, Currie, Gill &
Simpson, 1981). They have horizontal scales of kilometres and vertical scales of
metres, contain many features of physical, chemical, and biological interest, and
are susceptible to study by existing instrumentation. Much of their physics and
biology can be explained in terms of vertical mixing and steady state (e.g.
Pingree et al., 1975; Simpson, 1981; Tett, 1981). Island mixing zones on
continental shelves have similar scales and their physical and biological
behaviour can be explained in much the same way as those of fronts (e.g.
Simpson et al., 1982).
Upwelling regions have dominant scales up to ten times those of the tidal
coastal phenomena just mentioned, and have provided a focus for
interdisciplinary work since the 1960s (e.g. the review of upwelling and fish
production by Cushing, 1971), and the integrated models of J.J.Walsh and his
students (e.g. Walsh, 1977; Howe, 1982) have synthesized much of this work.
The proceedings (Hempel, 1982) of a symposium on the upwelling system of the

Canary Current contain many reports of recent interdisciplinary work.
The idea of scale might aid in the search for extra dimensions in which to
accommodate the many niches implied by Hutchinson’s (1961) paradox of the
plankton. In particular, we suggest frequency and wavenumber, the inverse of
period and wavelength, respectively. It is commonplace in the physical sciences
to describe and separate phenomena by their position in frequency and
wavenumber space. Wind waves, for example, are found near frequencies of 0·1
per second and wave numbers of 0·01 per metre, corresponding to periods of 10
seconds and wavelength several hundred metres. They are thus distinct from
coastal tidal waves with frequencies of order 10−5 per second and wavenumber
10−5 per metre, corresponding to periods of about a day and wavelengths of a few
hundred kilometres. Woods (1975) illustrates this point of view by applying it to
many physical oceanic phenomena, and Platt et al. (1981) urge its use in
designing sampling techniques.
It seems to us that species occupying the same physical space may, by virtue of
perhaps only slightly different biological characteristics, be found to produce
patterns on rather different time and space scales and, therefore, to be present in
different parts of frequency and wavenumber space. They could thus be deemed
to inhabit different ecological niches. Biologists may like to consider the
implications for natural selection of two species whose niches differ only in
dominant frequency. Is a frequency dimension a more general way of expressing
the population-response characteristics known to ecologists (e.g. Whittaker,
1975) as K- and r-strategies? K-strategists maintain stable populations over
periods of time that are long in human terms; r-strategists have a high intrinsic rate
of increase and their populations fluctuate greatly.
Hutchinson’s paradox derives from Gause’s exclusion axiom. “Given a …
physical space in which two species persist indefinitely at (or close to) a steady
state, there exists one or more properties of the environment or species…that
ensures an ecological distinction between the two species, [such that there is in
multidimensional niche space] a region…that is part of the fundamental niche of
one of the species but not of the other…” (Slobodkin, 1962, p. 123). The
difficulty with the plankton is that many species occupying the same physical
space do not appear to differ in what is known of their fundamental niches. Some
authors resolve this paradox by arguing that phytoplankton, especially, are r-
strategists, and thus do not persist long enough for competition to eliminate those
with completely common real-space projections of their niches. Our suggestion
is in essence that two species of plankton with differing dominant frequencies or
wavenumbers effectively share their use of a common resource, by matching
different aspects of that resource’s fluctuation in time or space. We thus differ
from Kilham & Kilham (1980). They see r- and K-strategies as devices for
improving the competitive success of phytoplankton, the former being better in a
resource-scarce, and the latter better in a resourcerich, environment. We view the
frequency and wavenumber characteristics as extra dimensions in which
fundamental niches can differ (assuming that selection favours such differences),
so that species may avoid competing until extinction.
We began by asserting that scientific development results from a combination
of stochastic and deterministic processes. We should perhaps end philosophically
by emphasizing the stochastic element in genuine collaboration, which is itself a
non-linear process akin to biological reproduction with genetic recombination.
The main purpose of this review is to encourage collaboration amongst the
oceanographic disciplines. We will have succeeded if we have done this, even if
our extrapolations of the topics discussed here are only weak predictors of future
developments.
ACKNOWLEDGEMENTS
We are grateful for discussion with the other members (M.Bowman, H.
Freeland, H.Gade, J.Matthews and J.O’Brien) of the ad hoc committee at the
NATO Workshop on Coastal Oceanography in Norway, June 1982, to other
participants in the workshop, especially P.Malkki and J.Nihoul, for material, and
to J.Shaw for the diagrams. J.Matthews and J.Simpson made valuable comments
on the penultimate draft. The Scottish Marine Biological Association is grant-
aided by the Natural Environment Research Council.
APPENDIX
Symbols, definitions, and dimensions
Symbol Definition Dimensions

a coefficient in Fourier series as dependent variable
A variable in patch scale Equation (9) none
a photosynthetic ‘efficiency’ M−1T2
b coefficient in Fourier series as dependent variable
c specific heat of sea water L−2T−2K−1
e excreted proportion of grazed nutrient ratio
ξ (t) a random function of time T−1
g phytoplankton-specific zooplankton grazing rate T−1
h layer thickness L
H depth of water column L
ξ layer average photosynthetically effective irradiance MT−3
Ic compensation irradiance for photosynthesis MT−3
Io sea-surface photosynthetically effective irradiance MT−3
Ky coefficient of horizontal turbulent diffusivity L2T−1
Kz coefficient of vertical turbulent diffusivity L2T−1
lc critical length-scale for a plankton patch L
Symbol Definition Dimensions

ξ diffuse attenuation coefficient for downwelling L–1
photosynthetically effective irradiance
m zooplankton mortality rate T−l
μ phytoplankton specific growth rate T−1
n coefficient pair number in Fourier series none
N phytoplankton particulate nutrient M L−3
pB biomass standardized photosynthesis T−1
QH heat flux M T−3
QN nitrate flux ML−2T−1
RB biomass standardized phytoplankton respiration T−1

ξ density of sea water M−3
s concentration of dissolved nutrient M L−3
S sinking rate LT−1
ξ stratification parameter in Figure 4 none
t time T
ξ time scale for turbulence T
ξ temperature K
u phytoplankton specific nutrient uptake rate T−1
U horizontal tidal current velocity LT−1
V horizontal residual current velocity LT−1
x (phyto)plankton biomass M L−3
y horizontal distance L
z depth L
zcrit Sverdrup’s critical depth L
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EFFECTS OF PHYSICAL PROCESSES ON
PLANKTONIC ECOSYSTEMS IN THE
COASTAL OCEAN
KENNETH L.DENMAN
Institute of Ocean Sciences, P.O. Box 6000, Sidney, B.C., Canada
V8L 4B2
and
THOMAS M.POWELL
Division of Environmental Studies, University of California, Davis,
CA 95616, U.S.A.
INTRODUCTION
The sea’s most productive areas are found in the coastal ocean. Figure 1 details
the global distribution of productivity in the sea, showing the extreme
concentration of biological activity along coastlines. For example, areas of
coastal upwelling present photosynthesizing organisms with ample supplies of
nutrients in the euphotic zone, and support the greatest primary production
(Ryther, 1969). Walsh (1981) has described and compared the processes
operating in several coastal ecosystems that have recently undergone intensive
study. The findings from these studies point out the critical importance of
physical processes, like upwelling, to the ocean’s most productive areas, the
coastal seas.
Upwelling is only one of several physical processes that affect biota in the
coastal ocean. How might one construct a framework in which to explore the
general impacts that the physical environment has upon planktonic ecosystems in
the coastal ocean? No theory exists that explains the details of how the physical
regime influences the response of populations and communities of organisms.
Moreover, the many physical and biological processes of importance operate on
a wide variety of characteristic space and time scales. For example, surface
gravity waves with periods of several seconds circulate plankton in the upper few
metres of the mixed layer. These motions may have indirect effects on the
photosynthetic rates of phytoplankton since they determine the average light
intensity that these organisms experience. The turnover times of algal
populations, however, are roughly one to several days (Parsons, Takahashi &
Hargrave, 1977). Thus, during its mean lifetime an algal cell will average the
light intensity variations over many thousands of surface wave periods. Longer
period waves, such as internal waves that move organisms vertically in
synchrony with the solar diurnal cycle, could be much more effective in
PHYSICAL PROCESSES AND PLANKTONIC ECOSYSTEMS 117
Fig. 1.—Geographic distribution of primary productivity in the sea showing concentration

in coastal seas (from Gross, 1972).
increasing the production within phytoplankton populations because they occur

over similar time scales. Conversely, when phytoplankton respond very rapidly,
say on the scale of several seconds, to light intensity fluctuations, then the short
period motions could be more important than the above considerations indicate
(Marra, 1978a, b; Harris, 1980; Abbott, Richerson & Powell, 1982).
Generalizing the above example, we propose that an initial exploration of the
coupling between physical and ecological processes concentrate on finding those
processes that operate on the same spatial and temporal scales. We seek situations
in which the space and time scales of variation in the physical environment
correspond approximately to those that individuals, populations, and
communities of marine organisms display within the coastal environment.
Correspondence of scales, however, does not establish cause and effect;
knowledge of the mechanisms themselves must follow to establish that coupling
or forcing actually occurs. In such situations, collaborating marine ecologists and
physical oceanographers have often uncovered the direct and indirect mechanisms
that couple physical and biological processes. Such coupling in the coastal ocean
is the subject of this review.
Underlying our approach is a basic and naive assumption that one can identify
spatial and temporal scales of physical and biological processes by investigations
that concentrate on one of these processes alone. For example, physical
oceanographers can describe the spatial characteristics of coastal fronts, and
biologists can estimate the turnover times of phytoplankton populations. Such a
view might be termed a linear, or zero-order, picture by a modeller. Currents
may bring populations of algae into nutrient-rich water, but the resultant growth
of organisms is assumed not to affect the movement of water. At least one simple
biological example immediately violates this assumption—self shading
(Shigesada & Okubo, 1981). As photosynthesizing organisms absorb solar
radiation and grow, they absorb more light in certain wavelength bands,
118 KENNETH L.DENMAN AND THOMAS M.POWELL
changing the light transmission characteristics of the water column, thus

affecting their growth rates. Such couplings are essentially non-linear; they are
not well documented in the ocean and will not be treated in detail in this review.
We shall emphasize the rôle that physical processes play at the ecosystem level
rather than at the level of individual organisms. The ecological concerns might
include, but are not limited to, the rate at which photosynthesis occurs in the
entire phytoplankton community (primary productivity), or the rate at which a
limiting nutrient becomes available, or the rate at which biomass accumulates in
the zooplankton community (secondary productivity). Not all interesting
ecological questions at the ecosystem level are of this kind. Information on the
particular species, or collection of species, of phytoplankton and/or zooplankton
is not addressed by such concerns. Studies that demand knowledge of the
responses of individual species might be: determining the outcome (i.e. exclusion
or coexistence) when several species compete for a scarce resource, or the effects
of a species of zooplankton preying selectively on a number of phytoplankton
species, or which temporal pattern, if any, describes the seasonal shift in species
composition within the coastal phytoplankton assemblage, or why certain coastal
areas are more diverse than others.
At present we seem best able to utilize physical information when addressing
topics such as energy flow (e.g. primary or secondary productivity) or nutrient
cycling, topics that ecologists commonly approach in terms of budgets—budgets
for energy (i.e. trophic level schemes) or budgets for mass (biogeo-chemical
cycles of nutrients) (Walsh, 1983). This analogy to the conservation laws for
energy, mass and momentum, so familiar in the physical sciences, is a powerful
technique, but conversation laws for mass, energy and momentum (the basic
tools of physical oceanographers) are not sufficient to understand such general
biological characteristics as competition, predation, species succession and
diversity, etc. that organize our thoughts about the biota of the coastal
environment.
A review of this kind does not fit well within the traditional boundaries of
oceanography. Is it biology? Is it physics? The answer is both, and yet neither.
What follows reflects the background and prejudices of the authors, both of
whom are physicists, but who have worked for approximately a decade with
biologists. We hope in what follows to engage readers with interests in both the
biology and physics of the coastal oceans. For background material, readers from
the physical sciences may wish to refer to several texts (Cushing, 1975; Bougis,
1976; Parsons et al., 1977; Levinton, 1982), compilations of salient papers
(Nybakken, 1971; Cobb & Harlin, 1976; Cushing & Walsh, 1976: Longhurst,
1981; Platt, 1981), and reviews (Owens & Esaias, 1976; Harris, 1978).
Biologists may refer to modern texts in physical oceanography like Pond &
Pickard (1978), LeBlond & Mysak (1978), Pedlosky (1979), Csanady (1982),
and Gill (1982), or the edited volume of Warren & Wunsch (1981).
We discuss first the notion of selecting the spatial and temporal scales over
which biological and physical processes are presumed to act. The greater part of
the review then focuses on the physical processes at work in the coastal ocean,
the main effects on the plankton ecosystems from these processes, and the few
examples of truly coupled biological-physical investigations that exemplify the
impact that the physical environment has on coastal ecosystems. Despite the
dearth of such studies, they are sufficient to demonstrate the importance of the
physics of the coastal ocean to the biology of the planktonic organisms at the
ecosystem level and to suggest the design of future integrated studies. Moreover,
the attempt to view the interaction of organisms with their physical environment
from the unified perspective of characteristic space and time scales is worthy of
consideration from both biologists and physicists; it should provide them with a
common basis from which to explore more complicated and subtle interactions.
TEMPORAL AND SPATIAL SCALES

The coastal planktonic ecosystem exists in an environment that varies both in
space and time. Associated with each phenomenon or process are specific time
and space scales. The effects that time variability and spatial heterogeneity
(patchiness) have upon biological processes is an active area of research. Reviews
of a general nature are provided by Levin (1976), Wiens (1976), Chesson (1978)
and Okubo (1980) as well as articles by Roughgarden (1977, 1979). Overviews
of activity specifically directed to the marine environment appeared in Platt &
Denman (1975, 1980), Steele (1976, 1978), and Denman & Platt (1978), while
Monin, Kamenkovich & Kort (1974) discussed the somewhat larger question of
variability in the ocean. In the sea for example, patchiness not only makes
reproducible sampling impossible (Hardy, 1936; Wiebe, 1970) but also can
affect competition and predation processes (Steele, 1974b; Fasham, 1978;
Tilman, 1982; Tilman, Kilham & Kilham, 1982). Similarly, the response of
phytoplankton to rapidly varying light intensities and nutrient concentrations can
be significant (Marra, 1978a, b; Turpin & Harrison, 1979; Turpin, Parslow &
Harrison, 1981; Abbott, Richerson & Powell, 1982). Noting that increasingly
both theoretical and experimental investigations suggest that variability is a
critical aspect in the biology of coastal marine organisms, we advance to the time
and space scales of the processes themselves.
There is an intuitive aspect to the concept of scale, that it is the time or space
over which a process occurs. We can define the temporal scale, Tq, of a process
as the time over which some quantity of interest, q, varies significantly while the
process is occurring. If (<q> is a characteristic value of q (some statistic like the
mean), and <dq/dt> is a characteristic value for the rate of change of q, then
. An analogous definition can be made for the spatial scale Lq,
associated with the distance over which q varies significantly.
In general, the temporal scales of interest are determined by the rates at which
biological processes proceed. For example, phytoplankton populations double
their biomass in periods of one to ten days, while zooplankton doubling times
can vary over two orders of magnitude, i.e. between one week (protozoans) and
two years (Antarctic euphausiids; Parsons et al., 1977). Figure 2 summarizes

data on biological temporal scales, with the observation that doubling times for
phytoplankton, zooplankton, and higher predators are roughly proportional to
organism size (Sheldon, Prakash & Sutcliffe, 1972; Steele, 1978;). Interactions
between organisms also have characteristic time scales. For example,
competition between algal species and predation from zooplankton may
eliminate (or at least lower significantly) one species or more from the
phytoplankton community, a process usually occurring over several weeks to
months (e.g. Kilham & Kilham, 1980). The classic pictures of seasonal
succession within marine phytoplankton communities in, for example, the
Sargasso Sea (Hulbert, Ryther & Guillard, 1960) or the Mediterranean Sea
(Margalef, 1961) show shifts over several months superimposed on an
approximately annual cycle. Given the above rough values for time scales of
some processes of biological interest, one might speculate upon possible causal
links to physical processes. For example, it seems unlikely that semidiurnal tides
will play a direct rôle in determining the outcome of competition between marine
algae. Competition acts over a much longer time scale than 12 hours. Tidal
activity of such a period, however, might play a direct rôle in determining
production rates of algae, whose doubling times are of order one day. Indeed,
theoretical calculations of Kamykowski (1974, 1976, 1979) show that the effects
of semidiurnal internal tides on the growth and clumping of migrating
dinoflagellates may be important. There is a strong analogy here to tuning or
resonating, effects that are common in many physical situations. Garrett (1972,
1975) has demonstrated one example in the tides of the Bay of Fundy and Gulf
of Maine. Because of the geometry of these basins, their collective resonant
frequency of oscillation coincides closely with the period of tidal forcing,
resulting in large tidal amplitudes. We assert that such tuning can also occur in
biological systems whose time scales (or resonant frequencies) coincide with
external physical forces.
Once the time scales of the ecological processes of interest in a problem are
determined, the important physical processes should be found among E those
physical processes with the same time scales. The spatial scales of ecological
importance are then basically the spatial scales of the important physical
processes. The reason stems from the nature of plankton—passive organisms
whose horizontal movements are almost entirely determined by the motions of
their fluid environment (the phytoplankton at the base of the food web
significantly change their spatial position only as a result of water movements).
Although one thus expects water movements to set the spatial scale of significant
ecological effects, two important qualifications to this picture of physical control
of spatial scale are necessary. First, even phytoplankton can move vertically by
passive sinking (Smayda, 1970; Walsby & Reynolds, 1980; Bienfang, 1981), and
also actively under their own control (Cullen & Eppley, 1981). This sinking is an
important motion of the organisms that is independent of water movement.
Secondly, many physical (and biological) processes are characterized by both
Fig. 2.—The relationship between doubling time and particle size for phytoplankton (P),
zooplankton (Z), invertebrate carnivores or omnivores (I), and fish (F) (from Steele,
1978).
time and space scales, e.g. diffusion and sinking. As an illustration, consider the
time, T, required for a patch of some quantity to diffuse some distance, L. When
the patch is initially small, then , where K is a diffusivity that describes
the dispersion of the observed quantity. This coupled nature of space and time
scales for such processes does not, however, preclude identifying separate space
and time scales in certain instances. As a hypothetical counter-example, consider
a physical inhomogeneity (a front) 10 km across, where the concentration of a
limiting nutrient varies significantly. A patch of phytoplankton, of extent ′ 1 km,
diffusing across this front is described by a diffusivity of 10 m2·s−1 (=K). In one
day (=T), an estimate of the phytoplankton doubling time, the patch size will
increase by ′ 1 km (=L). This length scale is only a small fraction of the
dimension of the frontal discontinuity. We thus expect that the growth (and
dispersion) of the patch will continue largely unchanged by the presence of the
front over this time scale. The important length scale in the problem is the cross
frontal dimension–10 km; the phytoplankton doubling time—one day—remains
the important time scale. If the patch persisted for ten days, continuing to grow
and disperse, its size would then approach the cross frontal dimension, and one
would expect significant changes in that portion of the patch that had ‘crossed’
the discontinuity into nutrient-rich water. Note that dramatic changes could
occur only when the size (=length scale) of the biological structure (a patch)
reached the dimensions of the physical structure (the front), illustrating the
biological amplification possible when scales of biological and physical
processes coincide.
Not all plankton ecologists accept our generalization about the biological
control of temporal scales and the subsequent physical control of spatial scales.
Cushing & Dickson (1976) and Cushing (1982) have argued that the physical
environment sets up conditions over very long time scales that determine the
production responses of whole ecosystems. Also, at small scales, Harris (1980)
pointed out that previous investigations have neglected important, rapid, very
small scale effects in algal ecology. He reasoned that the organisms have evolved
mechanisms to take advantage of the rapid variability imposed by the physical
environment over small scales. Whether physics or biology ultimately controls
variation at small scales is still an open question. Finally, from observations in the
St Lawrence River estuary, Demers & Legendre (1979, 1981) found periods
when natural endogenous rhythms (e.g. circadian rhythms) of the phytoplankton
community dominated the response of photosynthetic rates; at other times,
physical forcing (the tides) caused the largest response. Observing and
understanding such ‘switching’ between biological and physical control should be
an important future research topic.
Near coastlines direction is of critical importance in any consideration of
spatial changes: longshore changes (parallel to the coastline) are generally much
less dramatic than offshore changes (perpendicular to the coastline). Indeed, even
in the offshore direction two length scales are important. The first, a result of
local bottom topography, is the distance from the coastline to the shelf break.
This distance can vary greatly from place to place. For example, the shelf is
narrow along the Pacific coast of North America (tens of kilometres). The
location of the shelf break has much biological importance and will be discussed
later. The second length, the internal Rossby radius of deformation (or simply
Rossby radius), relates local depth, D, the inertial frequency, f (i.e. the Coriolis
parameter=2′ sin ξ where and ξ =latitude), and a measure of
stratification, N, the buoyancy frequency where ξ 0 is density and
z is a vertical space coordinate. The Rossby radius, DN/f, commonly of order 10
to 100 km, separates small scales where rotation is unimportant from large scales
where waves are predominantly controlled by the earth’s rotation and are
essentially in geostrophic balance. For waves travelling along a coast, the internal
Rossby radius represents the distance from the coast within which most of the
wave energy is trapped. All significant vertical displacement of isopycnal
surfaces must occur within this distance from the coast. This length scale forms a
loose dynamic boundary, in some sense separating mid-oceanic from coastal
regimes.
Variation in the longshore direction may occur over much greater distances,
hundreds of kilometres or more. Associations of benthic organisms show distinct,
large-scale zoogeographic provinces whose boundaries are closely correlated
with physical factors (Valentine, 1966). For example, the boundary between the
Southern California Bight and the California Current provinces at Point
Conception on the southern Californian coast is particularly sharp. The warmer
waters south of Point Conception are characteristic of the semipermanent gyre in
the Southern California Bight (Emery, 1960) while the colder waters to the north
are similar to those found off northern California, Oregon, Washington and
British Columbia, which often undergo coastal upwelling. The associations of
Fig. 3.—Satellite images of surface temperature (A) for 6 Aug. 1981, and surface
phytoplankton pigment concentration (B) for 10 Aug. 1981, for the ocean off Vancouver
Island, Canada: the images are roughly 350×250 km centred at 49°N: 125°30W; lighter
areas are colder temperatures (linear grey scale) and higher pigment concentrations
(logarithmic grey scale), and white sections denote cloudy areas that have been masked
out; (courtesy Drs. G.A.Borstad and J.F.R.Gower).
species that are best adapted to the particular complex of physical and chemical
conditions existing in these provinces emerge through natural selection. The
boundaries that we identify at present also exist in fossil and sediment records
(Valentine, 1973; Soutar & Isaacs, 1974) strengthening the view that the
organisms become associated over long, evolutionary time scales. Such province
boundaries may also exist for coastal pelagic organisms (Fager & McGowan,
1963; McGowan, 1974; Mackas, in press), and we assume that they have also
evolved over long time scales. For eastern boundary current coastal regimes,
however, the scale of variation in the longshore directions may not be nearly so
great (Walsh, 1977). Satellite imagery has shown the importance of shoreline and
bottom topography (Fig. 3); in such areas, offshore and longshore variations may
be of the same general scale.
The variety of physical phenomena and regimes pertaining to biological
questions is large. The coastal region is the site of a multitude of physical
processes acting over a wide range of spatial scales. Traditional sampling over this
very substantial range is nearly impossible, yet understanding of the biology of
the coastal zone demands understanding of the impact of processes acting over
all these scales. Recent advances in satellite remote sensing present a promising
alternative and supplement to traditional sampling schemes. In particular, the use
of the Coastal Zone Color Scanner (CZCS) (e.g. Smith & Baker, 1982; Smith,
Eppley & Baker, 1982; Borstad et al., 1982) shows the wide variety of patterns
expected from the melange of interacting scales in a biologically important
variable, chlorophyll (Fig. 3). Initial analyses of similar data (Gower, Denman &
Holyer, 1980) indicate that statistical techniques may be effective in resolving
the scales and identifying processes that interact with the organisms of the coastal
zone to form the rich mosaic of life found there.
In the sections that follow we consider those physical regimes that are
dominated by processes having characteristically small scales, proceeding
sequentially to larger scales. We include the dynamics of the mixed layer and the
meteorological forcing at work near the surface, internal motions (notably
waves), the wide variety of frontal structures, upwelling effects, the influence of
coastal and bottom topography, and the impact of impinging eddies and changing
oceanographic regimes, both seasonal and climatic. In each of these sections we
review the biological effects that are associated with these physical phenomena.
We do not treat estuarine, benthic or intertidal ecosystems.
UPPER OCEAN PROCESSES

The upper ocean is biologically the most important zone of the sea. The common
existence of a distinct surface mixed layer is not unique to coastal regions;
hence, many of the effects to be discussed in this article result from interactions
of the surface layer with the coastal regime. In upwelling regimes for example,
surface fronts occur where the thermocline at the base of a mixed layer intersects
the sea surface (Mooers, Collins & Smith, 1976). In many areas, a nearshore
zone characterized by high turbidity, high productivity and high resuspension of
sediments exists inshore of where the mixed layer penetrates to the bottom.
Horizontal changes in the structure of the mixed layer then are of primary
importance in coastal areas (de Szoeke & Richman, 1981). Spatial scales of the
mixed layer are its thickness (10–100 m) and the extent of horizontal patterns.
For fronts, which are of prime interest to biologists, the cross frontal distance
may be as short as a few metres, and the length of the front itself may, on the
continental shelf, be several hundred kilometres. Time scales in the mixed layer
are as short as several seconds for surface waves and as long as a year for the
formation and decay of the thermocline. At mid-latitudes the synoptic
meteorological ‘event’ scale (′ 5 days) dominates, and at certain times of year,
the sea breeze-land breeze cycle and the daily heating cycle impose a strong
diurnal periodicity. A major resonant frequency for oceanic oscillations in the
mixed layer is the inertial frequency, f. The period of inertial oscillations
decreases with increasing latitude, from ′ at the equator to 16·9 h at 45°, to 12
hours at the poles.
Since the classic work of Ekman (1905), wind-mixing in the surface layer and
its rôle in the heat exchange between the atmosphere and the ocean interior have
been actively studied in physical oceanography. Of equal interest to biologists is
the situation when the upper ocean is not only being mixed but also being
warmed and stratified through heating by the sun. This period of formation and
consolidation of the seasonal thermocline, which is characterized by a series of
‘transient thermoclines’ forming during calm, sunny days and mixing down at
night or during high winds (Tully & Giovando, 1963; Denman & Miyake, 1973;
Dillon & Powell, 1979) overlaps closely the period of highest primary
production by phytoplankton in most aquatic systems.
Early explanations of the structure of the upper layer and the thermocline
made use of vertical turbulent eddy coefficients (Ekman, 1905; Rossby &
Montgomery, 1935; Munk & Anderson, 1948). Although such ‘K-theories’ were
used to estimate vertical fluxes of materials in the upper ocean, oceanographers
consider the eddy-coefficient formulation to be an inherently weak one. During
the last decade a series of ‘slab models’ has been developed to simulate
deepening of the mixed layer in response to winds and heat exchanges with the
atmosphere. In these models, mixing occurs instantaneously and the layer is
always completely mixed by turbulence generated either at the sea surface
(Kraus & Turner, 1967; Denman, 1973) or at the interface at the base of the
mixed layer (Pollard, Rhines & Thompson, 1973). Niiler (1975) and Niiler &
Kraus (1977) combined the two approaches. Denman & Miyake (1973)
presented observations and model simulation of mixed layer behaviour for a two-
week period in June at Station Papa (50°N:145°W) where stormy periods
alternated with calm periods of solar heating, a situation highly relevant to
plankton productivity (Fig. 4).
The ‘slab models’ have a major disadvantage for modelling the planktonic
ecosystem: they do not allow for any diffusive transport below the instantaneous
mixed layer, which during sunny calm periods would be non-existent in the
ocean and only a few metres thick in a model. For turbulent transport below a
mixed layer one needs a ‘K-theory model’ where the vertical turbulent transfer of
scalar variables (heat, salt, phytoplankton, oxygen, dissolved nutrients, ‘small’
Fig. 4.—Comparison between a mixed-layer model and observations at Station Papa (50°
N: 145°W): a and b, inputs to the model; c and d, model predictions and simultaneous
observations; (from Denman & Miyake, 1973).
particles) is formulated in terms of an eddy coefficient K multiplied by the

vertical gradient of the scaler variable q, ξ q/ξz, in a manner analogous to
molecular diffusion. (The turbulent eddy coefficients for the various scalars should
be all equal.) The ‘K-theory model’ of Munk & Anderson (1948) did allow
turbulent diffusion below a sharp thermocline, but their model was not time-
dependent. Mellor & Durbin (1975), Garwood (1977), and Kundu (1980) all
produced ‘K-theory models’ that reproduce the basic behaviour of the upper
mixed layer but their turbulent closure schemes (i.e. recipes for K) all set K to
zero in the thermocline with the result again that vertical diffusion in and below
the thermocline is not allowed. Vertical diffusive transport across a strong
thermocline, however, can be accomplished by breaking internal waves, and a
simple formulation of this process has been attempted by Munk (1981).
Because the annual cycle of primary production by phytoplankton at mid and
high latitudes corresponds to the annual cycle of solar heating, the upper ocean is
often not completely mixed during periods of highest biological activity.
Formulae for vertical and horizontal diffusive mixing in coastal and oceanic
areas have been developed that depend on length scale (Okubo, 1971) and on
wind speed and near surface vertical gradients in current and density (Kullenberg,
1971). This work, including the coupling between horizontal and vertical mixing
and the implications for marine ecosystems, has been reviewed recently (Evans,
1978; Kullenberg, 1978; Okubo, 1978; Denman & Gargett, 1983).
Although the majority of studies in biological oceanography focus on the

upper ocean, we restrict ourselves here to three areas that specifically depend on
the behaviour of the upper layer. They are the interaction of light and mixing on
primary production by phytoplankton, the importance of nutrient entrainment
into the surface layer, and the implications of the dispersion of layers of
phytoplankton by wind-mixing on grazing by organisms at higher trophic levels
in the aquatic food chain.
Because photosynthetic primary production requires light, we can see that the
euphotic zone (where phytoplankton at any level gain more energy through
photosynthesis than they lose through respiration) must overlap with the upper
mixed layer. The bottom of the euphotic zone is often identified with
compensation depth, i.e. that depth where the daily average net production
(photosynthetic production—respiration) is zero. A rule-ofthumb developed from
many studies is that the compensation depth corresponds to the depth where the
submarine light level is 1% of that at the surface (Parsons, Takahashi &
Hargrave, 1977).
Gran & Braarud (1935) determined that the compensation depth concept was
inadequate to explain primary production in turbulent waters when
phytoplankton are uniformly distributed through the mixed layer and cycle
through the mixed layer rapidly relative to the daily light cycle. In such cases, a
more appropriate concept is the critical depth, at which photosynthesis balances
respiration when integrated from the sea surface to the critical depth. When the
mixed layer is deeper than the critical depth, then the phytoplankton spend too
much time at low light levels and there can be no net production; when the mixed
layer is shallower than the critical depth, then there can be net production. Riley
(1942) and Sverdrup (1953), in two elegant papers, formulated the concepts
mathematically and showed how the timing of the spring bloom of
phytoplankton depends on the mixed layer becoming shallower under increasing
solar heating until it is less than the critical depth. Sverdrup (1953) calculated the
critical depth to be about five times the compensation depth. A thorough
mathematical treatment of these concepts is given in Platt, Denman & Jassby
(1977).
Another interaction of mixing with light can be found on a physiological level.
Recently, the functional dependence of primary production on light has been
found to vary with fluctuating light (Harris & Lott, 1973; Marra 1978a, b).
Vertical excursions of phytoplankton resulting from turbulent eddies are an
important source of light fluctuations seen by phytoplankton: Legendre, Ingram
& Poulin (1981) and Demers & Legendre (1979, 1981) observed the effects of
stratification (and, by implication, mixing) on production of the St Lawrence
estuary and in Hudson Bay. They concluded that alternating periods of
stabilization and de-stabilization enhance production. Stochastic models of the
effect of mixing on production have been developed (Platt & Gallegos, 1980;
Falkowski & Wirick, 1981), but they lack accurate cycle times for turbulent
eddies. Denman & Gargett (1983) have made estimates from recent turbulent
microstructure measurements for different states of mixed layer stability and

turbulent intensity. For vertical excursions of say 10m, the estimates vary from a
few minutes to a few months, a range of approximately four orders of
magnitude, depending on current shear and stratification. An experimental
analogue of fluctuating light fields resulting from vertical mixing has been
incorporated into 14C productivity measurements by Gallegos & Platt (1982)
without clearcut results. In recent field experiment, Lewis et al. (in press),
however, observed a clear dependence of the variation in the maximum potential
photosynthetic rate between the top and bottom of the mixed layer on the
dissipation rate of turbulent energy within the layer, a variable considered to be
an indication of the intensity of turbulence in the ocean. The largest variation
was for small dissipation rates suggesting that under such calm conditions the
upper ocean was stable enough for organisms at different depths to have adapted
to the different light intensities at those depths.
Gran & Braarud (1935) discussed the effects of horizontal changes in the
intensity of turbulent mixing, the transparency of the water and the temperature
on primary production in the Gulf of Maine and the Bay of Fundy. Around
George’s Bank, Riley (1942) found in early spring that at stations shallower than
50 m the phytoplankton biomass was much higher than at deeper stations,
presumably because the depth of the bottom was less than the estimated critical
depth. During the spring bloom increasing biomass correlated with increasing
water column stability over the top 50 m but later in the season the correlation
reversed, presumably because of nutrient depletion in the surface layer and lack
of entrainment from below. He found a good relationship between the rate of
population increase and the reciprocal of the depth of the mixed layer for stations
where effects of horizontal currents were minimal but a clear relationship did not
exist for the group of stations (about 50%) where horizontal advection was
significant. Recently, Fasham, Holligan & Pugh (1983) performed a similar
study of the development of the spring bloom in the Celtic Sea. They were able
to obtain an accurate representation of horizontal gradients even in the presence
of small scale horizontal variability by using averaged data from an undulating
recorder. Nevertheless, their simulations were only partially successful, and they
concluded that they needed better data on the photo-adaptation of phytoplankton
and nutrient regeneration, and a better formulation of vertical eddy diffusivity.
Once a stable seasonal thermocline has been established, the spring bloom of
phytoplankton terminates usually because of a combination of grazing by
zooplankton and nutrient depletion in the surface layers. For significant primary
production in the surface layer, there must be a continual or sporadic process that
supplies inorganic nutrients into the surface layer. Upward entrainment at the
base of the mixing layer is one possible mechanism. For want of better data, Steele
(1974a) represented this exchange as a fraction (typically 0·01) of the mixed
layer that is exchanged with the layer below each day. Evans (1978) used a two-
layer model with shear-induced diffusion (Evans, 1977) to transfer nutrients into
the mixed layer. Measurements of the rate of uptake of 15N-nitrate by marine
phytoplankton now allow more direct estimation of the rate of diffusive flux of
nitrates through the seasonal thermocline into the mixed layer. Eppley, Renger &
Harrison (1979) and King & Devol (1979) obtained reasonable estimates of the
vertical eddy coefficient of turbulent diffusion in the seasonal thermocline by
this method.
The seasonal evolution of mixing effects on primary production described in
Riley (1942) also occurs on an episodic time scale of days to weeks in upwelling
ecosystems. Huntsman & Barber (1977) found depressed levels of production
when the wind-mixed layer remained excessively deep for periods of several days
or longer. Low winds resulted in enhanced production until nutrient levels in the
upper layer decreased. Walsh et al. (1978) found that while wind-events in the
New York Bight dispersed phytoplankton in the vertical plane, they aggregated
organisms at certain positions in the horizontal direction, providing centres for
more efficient grazing by zooplankton. In addition, they estimated that at least
33% of the nitrogen demand of the system was met by wind-driven entrainment
of deep nitrates up into the euphotic zone. Iverson, Curl & Saugen (1974), with a
model where exchange from the bottom to the surface layer varied according to a
wind-speed dependent coefficient times the nutrient difference between the two
layers, were able to simulate the episodic nature of primary production in a bay
in Alaska. Iverson (1977) showed that a hurricane crossing the Gulf of Mexico
could mix deeply enough along a swath about 100 km wide to double the
nutrients in the photic zone by entrainment from below.
A dramatic example of the importance of mixing episodes in the upper ocean
on higher trophic levels occurs along the California coast (Lasker, 1975, 1978).
He showed in the laboratory that first-feeding larvae of the northern anchovy
Engraulis mordax are able to eat phytoplankton and that their rate of feeding
increases with increasing concentration of phytoplankton. A minimum threshold
concentration of phytoplankton must, however, exist before any feeding occurs
at all. In March and April 1974 Lasker observed a dense layer of phytoplankton
about 100 km long off the Californian coast that was able to support successful
feeding by the larvae. A storm created a mixed layer 20 m deep that dispersed
the layer of phytoplankton to concentrations below the feeding threshold of the
anchovy larvae. High winds persisted, effectively destroying the population of
larval anchovy by starvation.
In coastal areas and on continental shelves vertical mixing may be insignificant
compared with horizontal advection by ocean currents or by an estuarine flow
regime. O’Brien & Wroblewski (1973) performed a scale analysis of a typical
phytoplankton biomass conservation equation that showed advection to dominate
in upwelling regimes and in major currents like the Gulf Stream. Tidal advection
in coastal seas is often the dominant process controlling the movement and
distribution of phytoplankton (Figure 10 in Denman & Herman, 1978). Bowman
& Esaias (1977) and Pingree & Maddock (1977) showed enhanced horizontal
advection of ecological importance around headlands and over features in the
bottom topography. The increased mixing and horizontal gradients that occur in
such regions often result in fronts and residual circulations, both of which will be
discussed later.
In coastal areas, the advective or mixing mechanism that dominates will vary
temporally, and any scale analysis will not be valid at all times. The most
thorough investigation to date of the time varying nature of the physical control
of a coastal ecosystem was the coupled observational and modelling study of
Puget Sound near Seattle by Winter, Banse & Anderson (1975). They found that
the critical depth concept discussed earlier did not explain the timing of the
spring bloom. The main transport mechanism responsible for bringing deep
nutrients up into the euphotic zone there is not vertical mixing but an estuarine
flow regime whereby deep inflowing water is entrained upwards into an outward
flowing surface layer. Furthermore, sustained strong winds negatively affect the
phytoplankton populations, removing them from the area studied by horizontal
advection.
No discussion of physical-biological interactions in the surface layer would be
complete without mention of Langmuir circulations (Langmuir, 1938; Pollard,
1977). They are helical vortices that form with weak to moderate winds, aligning
themselves along the wind direction, and are sites for the convergence and
divergence of marine plankton and for the formation of small particles (Sutcliffe,
Baylor & Menzel, 1963; Faller & Woodcock, 1964; Sutcliffe, Sheldon, Prakash
& Gordon, 1971). While the surface windrows can be dramatic and obvious, the
vertical extent and structure of the cells has not been well documented but
appears to be usually less than 10 m (Pollard, 1977). Denman & Gargett (1983)
estimated an average transit time around a circulation cell to be about 20 min, the
same order as for the large energy containing eddies in the mixed layer. Only
recently have realistic theories for the generation and persistence of Langmuir
circulations been developed (e.g. Leibovich, 1983). Planktonic organisms can be
aggregated at convergences in the cells, either at the surface or at depth
depending on the organisms’ buoyancy and vertical swimming speeds, if any
(Stavn, 1971; Evans & Taylor, 1980). The ability of some planktonic organisms
to alter their swimming speed and direction at different times of the day, thereby
changing their modes of interaction with the Langmuir circulations, is indeed
fascinating but in the coastal zone, tidal mixing and advection, internal wave
displacements, and estuarine frontal circulations should dominate such effects.
INTERNAL WAVES
Investigation into the nature and causes of the sea’s internal wave field has been
particularly intense in the last decade. Much of this effort was prompted by
Garrett & Munk (1972, 1975), who proposed a universal form for the spectrum of
internal wave motions in the mid-ocean. Throughout much of the allowed
frequency domain for internal wave activity, , the spectrum is
continuous and closely proportional to ξ −2; f is the inertial frequency, N is the
local buoyancy frequency, and ξ is the (angular) frequency. In addition,
, where E is the total energy of internal wave motion, is predicted to be a

universal curve. An enormous amount of field observation has confirmed this
prediction (and a comparable effort has been expended to provide a theoretical
basis for the Garrett-Munk form). Thus, in the mid-ocean one expects to find
most internal wave.energy near the inertial frequency, i.e. those motions having
periods of order 15 to 20 h in mid-latitudes (e.g. 17 h at 45°). Descriptions of
earlier work on internal waves in the sea can be found in Krauss (1966), Briscoe
(1975), and Roberts (1975), while the basic hydrodynamic questions are detailed
in Turner (1973) and Phillips (1977). LeBlond & Mysak (1978) and Lighthill
(1978) treated internal waves as special cases of more general wave motions.
Reviews of recent activity can be found in Garrett & Munk (1979), and Gregg &
Briscoe (1979).
The nature of internal wave activity in the coastal ocean may be more complex
than that seen in the mid-ocean. Coastal boundaries can act as sites of generation
and decay for internal waves. Moreover, embayments, basins, and other
topographically non-uniform structures of the coastline can select and enhance a
small number of the many modes found in the entire internal wave field,
especially those forced at tidal frequencies. Wunsch (1976) found that over Muir
Seamount in the North Atlantic the energy in internal wave activity differed
significantly from that predicted by Garrett & Munk (1972, 1975).
Measurements at increasing distances from the Seamount, however, showed a
rapid return to the Garrett-Munk energy level. Even over Muir Seamount, the
spectrum continued to follow the universal shape, roughly proportional to ξ −2.
Wunsch’s general observations showed that regions where the flow of a stratified
fluid intersects a topographic inhomogeneity (a common occurrence near
coastlines) have complex and changeable internal wave fields. Interpreting these
regions as sites for generation and dissipation of internal waves (Osborn, 1978,
observed increased turbulent dissipation at the base of the mixed layer within 5
km of an island), one expects that the internal wave processes will not be
stationary in either time or space. Rather, the internal wave field will depend
upon the timing of causal events as well as on the spacing of irregularities which
generate and dissipate them. Caldwell, Brubaker & Neal (1978) interpreted
substantial microstructure and irregular step-like structures in vertical thermal
profiles near a shelf break in a large lake in this way. A much reduced level of
irregularity occurred in mid-lake profiles away from the shelf.
The recent interest in internal waves extends to the effects such motions might
have on a variety of other processes. For example, Cacchione & Wunsch (1974)
concluded from experiments in the laboratory and in the Bering Sea that internal
waves could transport substantial amounts of sediment in shallow coastal
regions. Winant (1974) made similar observations off southern California. Such
transports could be important in supplying nutrients to coastal areas. Denman
(1977), investigating short-term variability in vertical chlorophyll at a single
station in a coastal bay, noted substantial changes in both the position of maxima
and the shape in chlorophyll profiles over a 26-h period. These changes were
Fig. 5.—Depths of isopleths of chlorophyll a concentration and specific density (ξ t) along

a transect line in the eastern Gulf of Maine parallel to the Nova Scotia coastline (from
Denman & Herman, 1978).
attributed largely to internal waves. The variability in chlorophyll on a constant ξ t
surface was, however, of a different nature—much longer in period, because of
‘real’ variability in biomass resulting from advective inputs by other water
masses due to tidal motion. Denman & Herman (1978), using data collected with
a vertically undulating towed vehicle, the BATFISH, showed intense internal
wave distortions of a layer of phytoplankton in a coastal area (Fig. 5). When
phytoplankton chlorophyll concentration was displayed on constant ξ t surfaces
(Fig. 6), the mesoscale patterns, which had been distorted by internal wave
displacements, became obvious. Similar effects have been noted by Haury,
Briscoe & Orr (1979) in Massachusetts Bay. These observations point out the
need for a careful distinction between the confounding effects that ever present
internal waves have on biological sampling programmes and the shifts in water
masses and/or organisms that lead to change in, for example, primary
production, zooplankton grazing pressure, aggregation of phytoplankton, and
other processes of genuine biological significance.
One approach to making such distinctions between sampling effects and
actual biological effects is to seek processes whose time scales coincide roughly
with those describing biological activity. For example, phytoplankton
populations have doubling times of approximately one day; internal wave
motions with periods in these ranges might alter algal productivity. Kamykowski
Fig. 6.—Isopleths of chlorophyll a concentration on a plot of specific density (ξ t) against

distance for the data of Figure 6: the large vertical excursions of isopleths of chlorophyll
in Figure 5 have been virtually eliminated by plotting against specific density; the
sawtooth lines represent the track of the towed BATFISH through the water; (from
Denman & Herman, 1978).
(1974, 1976) has explored such considerations with extensive simulations of the
effects of semidiurnal internal tides on phytoplankton populations. Large effects
seem possible. Modelling the internal tide as a sinusoidal wave at the interface
between two fluids that do not mix, he found that phytoplankton at certain
spatial positions along the wave can be moved upward into shallower depths of
high light intensity in rough synchrony with the solar cycle, thus enhancing
production. At certain positions along the wave the plankton also can experience
considerable horizontal movement that causes aggregation of the algae,
suggesting a method of generating patches. These effects would be most
pronounced near the thermocline (the interface in his model) for algae that can
adjust their vertical position in the water column, a behaviour that is observed in
some important classes of coastal phytoplankton (Eppley, Holm-Hansen &
Strickland, 1968; Kamykowski & Zentara, 1977; Tyler & Seliger, 1981).
Kamykowski’s simulations made no attempt to model all the complexities of
internal motions near coastlines and, therefore, have not been substantiated in
detail. They point, however, to definite and significant biological effects, i.e.
enhanced primary productivity and patchiness, that can depend critically upon
internal waves, Abbott, Powell & Richerson (1982) presented evidence from the
thermocline of a large, deep lake for patches that are associated with a single
mode of an internal wave.
Internal waves could also affect the functional response of photosynthesis to
light. Marra (1978b) for example, showed that the photo-inhibition effect became
evident after phytoplankton were exposed to high light intensities for periods
shorter than two hours. Semidiurnal internal tidal waves have periods of 12·4
hours, and thus are capable of subjecting organisms sitting on the crest of the
wave to higher than normal light intensities for times in excess of two hours.
Kamykowski (1979) included photo-inhibition in his internal wave model and
demonstrated that organisms on the wave crests near midday should experience
suppressed photosynthetic production. This model still simplified reality by
ignoring the ‘light history’ effects demonstrated in Marra’s work.
Internal waves cause mixing when they become unstable and break (Thorpe,
1977a, b). There are presumably biological effects of such enhanced vertical
transport (e.g. Haury et al., 1979: Herman & Denman, 1979), but we are
unaware of any direct studies linking internal waves and, e.g., increased primary
productivity. The time and space scales of such breaking processes are difficult
to determine, but Bell (1974) and Munk (1981) have made initial attempts to
parameterize this important mechanism for vertical transport. Certainly the
ubiquitous nature of internal waves on continental shelves, often with
magnitudes in excess of 10 m, suggests that they always must be considered in
any process-orientated study of coastal ecosystems.
FRONTS
TYPES OF FRONTS
There are probably as many definitions of fronts as there are scientists studying
fronts. We define a front as a discontinuity in the horizontal distribution of water
mass properties on the scales of observation. In estuaries, tide lines may be only
metres wide (Ingram, 1976); in the open ocean, fronts separating major oceanic
regimes may be several degrees of latitude wide (Roden, 1977). Fronts also have
a length as well as a width; the length of a front over which the discontinuity
extends would usually be orders of magnitude larger than its width (e.g.
Legeckis, 1978). The properties and types of fronts have been conveniently
discussed in Bowman & Esaias (1978), Owen (1981) and Swallow, Currie, Gill
& Simpson (1981); we have drawn on their work where appropriate. Fronts form
where there are horizontal gradients in energy generation and dissipation
processes. It is commonly thought that, for fronts to be maintained over any
significant time period, they must be zones of convergent circulation. By
continuity, convergence usually requires compensatory vertical circulation.
Associated with the high gradients are high current shears causing fronts to be
regions of enhanced mixing and diffusion. Even where frontal gradients are not
reflected in the density structure, vertical instabilities can occur through double
diffusion processes and cabbeling.
Several types of fronts are important to coastal and continental shelf
ecosystems. Shelf break fronts occur near the outer edge of the continental shelf
at the boundary between shelf waters and slope or oceanic waters. According to
Mooers, Flagg and Boicourt (1978) these are retrograde fronts in the sense that
isolines tend to be orientated perpendicular or obliquely to bottom slope. Shelf
break fronts may be thermohaline fronts where the sharp temperature and salinity
changes are nearly density compensating, resulting in small net density
gradients. Upwelling fronts are prograde fronts as isolines tend to be orientated
parallel to bottom slope. They are essentially the surface manifestation of an
inclined pycnocline. Shallow sea fronts occur between shallow wind- and tidally-
mixed waters and deeper stratified waters. Estuarine plume fronts occur at the
boundaries of riverine flow discharging into coastal waters. Fronts can be
affected by, and in fact caused by, large oceanic flows intruding onto continental
shelves, with associated biological effects (Owen, 1981) but such phenomena
will be treated separately.
SHELF BREAK FRONTS

The hydrographic description of shelf break fronts is relatively complete,
because of their proximity to the eastern United States and Canada. In this region
they exist between cold, low salinity shelf waters and warmer, more saline slope
waters, and on average they are located near the shelf break. Bigelow (1933) and
Bigelow & Sears (1935) first documented their existence. More recently, Gatien
(1976) developed an overall structure for the hydrographic studies of shelf break
fronts by labelling several associated water masses which have distinct
properties. The seasonal changes in hydrographic properties and the large scale
structure have been studied along the eastern North American seaboard by
Beardsley & Flagg (1976), Boicourt & Hacker (1976), and Wright (1976), and in
the Bering Sea by Kinder & Coachman (1978), and Schumacher, Kinder,
Pashinski & Charnell (1979). Little is known about the actual circulation near
these frontal zones and even less about the associated surface convergences.
During the winter seasons, shelf break fronts are often structurally similar to
shallow sea tidal fronts. At such times the shelf waters are vertically well-mixed,
and the front intersects the bottom at the shelf break then slants upwards in a
seaward (retrograde) direction.
Density fronts are considered to be convergent zones but, in addition, are sites
for exchange of materials by mixing of different water masses. There is intense
interleaving of layers in the horizontal along the shelf break front between the
shelf and slope waters north of the Gulf Stream, as documented by Voorhis,
Webb & Millard (1976) and Horne (1978a, b). Mixing and vertical exchange
across the interleaved layers of this front (which is predominantly thermohaline)
are accomplished by double diffusion with waters above and below (Horne
1978a, b; Garrett & Horne, 1978; Bowman & Okubo, 1978). This cross-frontal
mixing by double diffusion, and by shear instabilities (Coachman & Walsh,
1981), is often tidally-driven (Herman & Denman, 1979). The frontal zones off
the east coast of North America are often intensified and distorted by eddies in, or
breaking off from, the Gulf Stream; these effects will be discussed later.
In describing the impact of all types of fronts on marine ecosystems, one must
always ask the crucial questions: do the enhanced levels of phytoplankton
biomass (or standing stock) usually found near a front result from convergence
of organisms at the front, or do they result from higher rates of primary
productivity there? The difficulty in making in situ growth rate measurements in
biological oceanography in general, and in the vicinity of dynamically changing
fronts in particular, often makes resolution of the problem nearly impossible. We
point out, however, that surface convergences can concentrate phytoplankton
only if the organisms are positively buoyant.
Shelf break fronts certainly affect the distribution of phytoplankton and
nutrients. Iverson, Whitledge & Goering (1979) found elevated concentrations of
phytoplankton chlorophyll in a band about 30 km wide for a distance of 170 km
along the front. Nutrient concentrations were reduced, but not limiting to
productivity, in the areas of highest phytoplankton biomass indicating that the
phytoplankton production had occurred locally. Gradients of properties
perpendicular to the shelf break and changes with season have been studied by
Leigh-Abbott, Coil, Powell & Richerson (1978) and Fournier (1978). Tidally-
forced instabilities on the front cause intense vertical mixing and advection of
phytoplankton and nutrients over periods comparable with the semidiurnal tide
(Herman & Denman, 1979). The cumulative effect of these mixing events on a
seasonal scale is to enhance phytoplankton standing stocks and primary
production in the frontal region (Fournier, Marra, Bohrer & van Det, 1977;
Fournier, van Det, Wilson & Hargreaves, 1979).
UPWELLING FRONTS
Upwelling fronts occur where the pycnocline intersects the sea surface in an
active wind-driven upwelling zone during upwelling-favourable winds
(equatorward along the eastern edges of ocean basins). Off Oregon, they are
located about 5–10 km offshore, roughly a distance comparable to the local
Rossby radius of deformation defined earlier (Collins et al., 1968; Mooers,
Collins & Smith, 1976). Inshore of the front, cool, dense nutrient rich waters
have been transported into the euphotic zone to replace the offshore Ekman
transport in the surface layer. When the equatorward winds are blowing, this
denser water is in dynamic equilibrium with offshore surface waters; when the
upwelling-favourable winds relax, the offshore surface waters shift back towards
the coast and the front disappears (Halpern, 1976; Zuta, Rivera and Bustamante,
1978). A model by de Szoeke & Richman (1981) confirms this general
description of the dynamics.
Despite the massive observational programmes over the last decade, physical
oceanographers are still not in agreement whether the cross-shelf circulation in
upwelling areas consists of one or two distinct closed cells (Johnson, 1981;
Smith, 1981). It is, however, generally agreed that the inshore upwelled water is
driven downward (and offshore) at the front, where a strong convergent surface
flow has been observed (Stevenson, Garvine & Wyatt, 1974). Some of the
downwelled water recirculates back into the inshore upwelling zone; this return
flow is best illustrated in the numerical model of Thompson (1978), where the
noise of the real ocean is avoided,,
Biological studies in upwelling areas have rarely concentrated on the frontal
zones. The few studies that have been done infer or require the existence of a
closed circulation cell inshore of the upwelling front for retention of planktonic
organisms. Pearcy & Keene (1974) analysed multispectral colour records
obtained by airborne remote sensing: they found abrupt changes in ocean colour
in the thermal front which they attributed to changes in particulates and
phytoplankton chlorophyll. Ryther (1967) observed a plankton bloom contained
on the inshore edge of the upwelling front off Peru, and Packard, Blasco &
Barber (1978) argued that Mesodinium rubrum, a non-toxic red tide ciliate, is
capable of sufficiently high vertical migration rates (either from buoyancy or
active swimming mechanisms) to be maintained in a band in the convergence
zone on the inshore edge of upwelling fronts. Wroblewski (1977) showed that even
neutrally buoyant phytoplankton could reach very high concentrations at the
centre of the nutrient-rich inshore circulation cell in a simulation model coupled
to the physical model of Thompson (1978) (Fig. 7). Peterson, Miller &
Hutchinson (1979) presented the most compelling evidence for the retention of
planktonic organisms inshore of the front; they found extremely high (ξ 104·m−3)
concentrations of small copepods (and eggs) inshore of the front or below the
pycnocline when the upwelling had relaxed. Other species were found
predominantly offshore of the front, and during upwelling some species were
concentrated on either side of the front suggesting a retention mechanism in the
outer circulation cell as well. Wroblewski (1982) simulated the nearshore
retention of the copepod Calanus marshallae showing that, in addition to the
frontal circulations, vertical migration may also be important in retarding the
alongshore transport of the organisms. Blackburn (1979) did not note the impact
of frontal circulations on distributions of zooplankton off West Africa in 1974,
but that upwelling regime was dominated by longshore currents resulting from
steady high winds rather than the episodic winds and currents usually observed
off Oregon.
SHALLOW SEA FRONTS

These fronts are found mainly in shallow coastal seas characterized by large tidal
currents. They separate stratified waters over deeper areas from well-mixed
waters over shallower banks or in constricted passes (Simpson, 1971).
Dynamically, one can consider these fronts to be the boundary that separates
regions where the bottom mixed layer (over shallow areas or areas with more
intense tidal mixing) penetrates to the surface from regions where a surface
stratified layer remains. On the well-mixed side of the front, the turbulent energy
generated by bottom friction is sufficient to overcome the buoyancy input near
the surface due to solar heating. Simpson & Hunter (1974) and Fearnhead (1975)
compared these energy sources and sinks; Simpson & Hunter mapped the ratio,
Fig. 7.—Upwelling circulation (A), depth integrated primary productivity (B), and depth
distribution of primary production (C) after ten days of longshore winds from a coupled
physical-biological model of coastal upwelling off Oregon: A, circulation in a plane
transverse to the coastline, bottom topography, and wind stress with maximum horizontal
and vertical velocities of 6·1 cm·s−1 and 5·2×10−2 cm·s−1, respectively; B, primary
productivity expressed in units of nitrogen concentration per area per time; i.e., nitrogen
uptake and cell growth are considered equivalent; C, isopleths of cell concentration
(equivalently, nitrogen concentration) with contour intervals of 1·6 mmoles-N·m−3; (from
Wroblewski, 1977).
(h is the water depth in metres and us is the near bottom amplitude of the
tidal current in m·s−1) over the Irish Sea during summer and found fronts where
. More detailed studies of the hydrography and currents
and tests of this criterion around these fronts in the Irish and Celtic Seas were
carried out by Simpson (1976), by Allen, Simpson & Carson (1980), and by
James (1978) in a numerical model.
With the possible exception of estuarine input of fresh water, shallow sea
fronts do not form in the winter because of the absence of a thermocline. The
development of the seasonal thermocline and frontal regions and their

progression onto the shelf regions around the British Isles as the solar heating
increases in spring was studied by Pingree (1975), Simpson, Hughes & Morris
(1977) and modelled numerically by James (1977). Likely positions of fronts and
possible movement with changing radiation and tidal intensities have been
studied by mapping with numerical models of tidal currents (Pingree &
Griffiths, 1978; Garrett, Keeley & Greenberg, 1978). The latter considered
stability effects resulting from freshwater run-off and the sensitivity of predicted
frontal areas to changes in tidal currents that might result from hydroelectric
tidal barriers (in the Bay of Fundy, Canada). Changes in the horizontal extent and
structure of shallow sea fronts can best be observed in series of satellite images.
Simpson, Allen & Morris (1978), Pingree (1978a), and Simpson & Pingree
(1978) observed instabilities on frontal boundaries with wavelengths of order 25
km and time scales of several days.
The biological effects of shallow sea fronts are dramatic. They appear to obey
the classical concept of near-surface convergence: Pingree, Forster & Morrison
(1974) observed net tow catches of planktonic Crustacea inside a frontal region
of the English Channel to be 75 times as abundant as outside the frontal region.
From drogue measurements, they estimated near-surface convergent velocities to
be about 0·25 m·s−1. Transects across these fronts (Fig. 8) showed peaks of
phytoplankton biomass right in the front, as defined by the sharpest temperature
gradient (Pingree, Pugh, Holligan & Forster, 1975; Savidge, 1976; Pingree,
Holligan & Head, 1977). Series of vertical profiles across these fronts revealed
this as a high chlorophyll concentration following the maximum temperature
gradient downwards away from the front. In addition, phytoplankton were
abundant and growing in the near-surface waters above the thermocline on the
stratified offshore side of the front where nutrient and light conditions were
optimal (Simpson et al., 1979). If sunny, calm conditions persist during several
days of neap-tide conditions, these populations along the front can develop into
red-tide dinoflagellate blooms (Pingree et al., 1975, 1977). These observations
suggest that the blooms of phytoplankton in the frontal zone did not result from
convergence but were produced locally. Pingree (1978b) and Pingree, Holligan &
Mardell (1978) classified coastal areas for primary productivity by plotting them
on graphs of (where CD is the bottom drag coefficient) against kh
(where k is the extinction coefficient for light in m−1). Thus, the two effects,
vertical mixing by tidal currents and light availability at depth, can be scaled so
that different regions can be compared directly without measurements of vertical
diffusion or primary production. Bowman, Esaias & Schnitzer (1981) have
plotted on such a graph station locations and contours of plankton concentrations
at each station for Long Island Sound to see what light and mixing environments
correlate with different classes of phytoplankton. Diatom abundance correlated
with high light levels and near-frontal areas; microflagellate abundance
correlated with low light levels and stratified areas away from fronts.
Fig. 8.—A, isopleths of chlorophyll a (in mg·m−3) along a section (Stations A-G) through
a frontal region off the southwest coast of Great Britain in summer; B, simultaneous
isotherms along the same section; (from Pingree, 1978b).
ESTUARINE PLUME FRONTS

The ecology of estuaries has received much attention from researchers but little
work has been done specifically on the ecological significance of estuarine
fronts. Recent advances in instrumentation have stimulated several studies which
we shall outline. Our early understanding of the physical processes controlling
estuarine plume fronts resulted largely from studies of the Connecticut River,
both observational (Garvine & Monk, 1974) and theoretical (Garvine, 1974).
These fronts involve a dynamic balance between interfacial friction and/or
upward mass entrainment and net pressure gradients resulting from the sloping
sea surface and plume interface. The Connecticut River front, readily observable
from the air, penetrates only a few metres into the water and is less than 100 m
wide. Other estuarine fronts often penetrate much farther from the surface: a front
in the St Lawrence River estuary studied by Ingram (1976) occurs near an abrupt
change in bottom depth, and the discontinuity in hydrographic properties can be
observed down to a depth of 35 m. In addition, this front, which is most intense
just after high tide, disappears on the ebbing tide.
In their summary of estuarine and plume fronts, Bowman & Iverson (1978)
presented data on the biological consequences of the Hudson River plume front.
The plume front is described by a sharp salinity interface, and the maximum
concentrations of phytoplankton chlorophyll were not in the front but in the
estuarine waters, with an abrupt drop in concentration across the front itself.
Malone et al. (1983) have found that the Hudson River plume also has
characteristics associated with upwelling frontal systems—cross shelf circulation
and upwelling—that can extend up to 100 km offshore. Seliger et al. (1981)
found that in the upper part of the Chesapeake Bay, fronts occur repeatedly in
several areas, each one with its own particular nutrient distribution and often
with a different dominant assemblage of phytoplankton species. Tyler & Seliger
(1978, 1981) described an intriguing sequence of events whereby the red-tide
dinoflagellate Prorocentrum mariae-lebouriae is concentrated and grows at a
front in the lower Bay in February, sinks and is advected towards the head of the
Bay by the subsurface estuarine flow. There it is entrained into the surface
waters in May or June where a bloom occurs if the timing and strength of the run-
off driven estuarine flow has been favourable. Tyler & Seliger (1981)
demonstrated how the organism has specific time-variable physiological
adaptations to light, temperature, and salinity that allow it to take advantage of
the estuarine flow pattern of Chesapeake Bay. Near the front, winter high salinity
tolerance and positive phototaxis (i.e. they appear to adjust their buoyancy to rise
to higher light levels) of the organisms combine to enhance the convergence
capabilities of the front in the lower Bay in late winter.
We see from this example the difficulty of matching timescales of physical
and biological processes. The fronts may last only several weeks yet their
existence is critical to a cycle that takes a whole year to be completed. Similarly,
shallow sea fronts are important throughout the whole summer season, yet most
individual fronts exist for times shorter than the fortnightly modulation of the
tides. Given the right meteorological conditions, this period is long enough for a
plankton bloom to occur. These examples demonstrate how knowledge of the
detailed life histories of the organisms is essential in selecting appropriate time
scales of physical processes that couple to biological processes. Furthermore,
each riverine plume front appears to possess its own individual character; we
hope that with increased study, more general characteristics of riverine fronts
will emerge.
UPWELLING ECOSYSTEMS
In the last decade, the tremendous scientific effort applied to the study of
upwelling has been justified on economic grounds—the Peru anchovy fishery
supplies about one half of the global fish meal demand. Consequently, a large
body of literature on upwelling systems has recently been published, and we
shall only outline the effects of the main physical processes operating in
upwelling ecosystems; the impact of smaller scale processes such as fronts,
mixed layer dynamics, headland plumes etc. are discussed elsewhere in this
review. We refer readers to the excellent conference proceedings on upwelling
systems edited by Boje & Tomczak (1978) and Richards (1981).
Does a unique entity such as an upwelling ecosystem exist? Among the
protagonists are Barber & Smith (1981) who describe coastal upwelling as “…a
circulation pattern that overrides both the nutrient limitation of stratified waters
and the light limitation of well mixed waters that develops when the wind
transports water offshore in the surface layer, resulting in an equal amount of
water welling up near the coast to replace this water”. Furthermore, “The
simultaneous occurrence of three processes in a narrow coastal band makes
coastal upwelling ecosystems different in a modal sense from other marine
ecosystems. The processes are: 1. vertical transport of inorganic nutrients to the
euphotic zone, 2. formation of a divergent surface Ekman layer that is distinct
from the convergent subsurface flow and 3. the presence of a two-layered
alongshore flow with a poleward undercurrent beneath the equatorward flow.”
Expanding on these concepts, the earth’s rotation requires that an alongshore
wind stress (with land on the left in the northern hemisphere) drive a net near-
surface (Ekman) transport of water at right angles offshore (to the right in the
northern hemisphere). Nutrient-rich water from just below the pycnocline moves
onshore and upwards to replace the surface offshore flow. Observations show
this onshore-offshore flow superimposed on a two-layered alongshore flow with
the subsurface layer moving poleward.
Much attention has been given to explanations of the dynamics controlling
these observed flow patterns. Allen (1980) reviewed the theories for wind-driven
shelf currents and concluded that the cross-shelf flow is in general balanced by
the alongshore wind stress, and the larger alongshore flow is in approximate
geostrophic balance as expressed by the ‘thermal wind equation’. However, a
dominant property of wind-driven upwelling systems is the extreme variability in
both the wind forcing and the currents on time scales of several days, which is
the synoptic meteorology time scale. Allen (1980) and Mysak (1980) reviewed
our knowledge of shelf waves; on these time scales, shelf waves of several
hundred kilometres wavelength (the spatial scale of synoptic meteorological
disturbances) which propagate poleward in eastern ocean margins are possible.
R.L.Smith (1978), for example, documented these disturbances and found that
they may be forced remotely as well as locally. Although the two-layer cross-shelf
flow (offshore near the surface, onshore below) has been widely observed
(Barber & Smith, 1981), the details of the flow patterns are a subject of debate.
Mooers et al. (1976), and Johnson & Johnson (1979) concluded that their
observations were consistent with a two-celled cross-shelf structure that results
in a convergent surface front at mid-shelf; Peterson et al. (1979) inferred a
similar structure from distributional patterns of zooplankton. Regardless, the
problem must be considered as three-dimensional because of the dominance of
the alongshore flow; initial numerical models of three dimensional flow are
encouraging in their ability to reproduce detailed flow patterns (O’Brien et al.,
1977).
Ecologically, the important physical processes are the seasonal upwelling of
nutrients into the euphotic zone and the two-layered flow that maintains vertical
stability necessary to keep the phytoplankton in the euphotic zone. The coupling
of these processes has been modelled by Walsh (1975) and Wroblewski (1977).
Fig. 9.—Hypothetical variance spectrum of habitat variability in a coastal upwelling

system: the peaks correspond roughly to the doubling times for phytoplankton (P),
zooplankton (Z), and nekton (N); (from Walsh et al., 1977).
The two-layered flow, in addition to supplying new nutrients, recycles sinking

organic matter and phytoplankton. In fact, the onshore subsurface flow is often
shallow enough to be in the euphotic zone thereby possibly preconditioning the
organisms to light prior to their being upwelled into the surface layer. Although
western oceanic boundaries do experience upwelling, the onshore flow is often
nutrient-poor because nutrient-rich waters are deeper there than in eastern
boundary regions. The advective effects of upwelling operate at higher trophic
levels as well; Peterson et al. (1979) concluded that zooplankton were also
maintained within the upwelling zone by the flow patterns.
The three ‘event’ time scales in upwelling systems—diurnal, monthly and
annual—were shown to coincide with growth cycles of phytoplankton,
zooplankton and fish in a hypothetical variance spectrum presented by Walsh et
al. (1977) (Fig. 9). The high degree of variability is necessary because intense
sustained upwelling would transport the organisms and nutrients offshore before
the production cycle could be completed, as was observed off West Africa during
1974 (Huntsman & Barber, 1977). The relaxation periods between upwelling
events allow the phytoplankton blooms to occur and the necessary transfer of
organic matter to higher trophic levels to take place. Each upwelling ‘event’ is an
analogue of the spring bloom that occurs in other temperate and polar waters
(Huntsman & Barber, 1977; Walsh et al., 1977; Jones & Halpern, 1981). The
fortuitous fact for upwelling productivity is that of order four to six spring blooms
occur each year, not just one.
TOPOGRAPHIC INFLUENCES
TYPES
In coastal fishing grounds, fishermen often concentrate their efforts in certain
areas where anecdotal reports of persistent eddies are common. With the recent
advent of remote sensing capabilities and of computers that are large and fast
enough to handle non-linear numerical models on fine grid spacings, we have
been able to test the importance of shoreline and bottom topography in
explaining local circulation patterns on continental shelves. In this section, we
discuss examples of patterns of residual circulation forced by tidal stresses,
currents in and around submarine canyons and bumps, and currents around capes
and headlands.
RESIDUAL CIRCULATIONS
Tides and storm surges can exchange energy through non-linear Reynolds stress
terms with a residual circulation that varies negligibly over several tidal cycles.
Nihoul & Ronday (1975) and Ronday (1975) presented results from a numerical
model that showed several closed eddies present in the residual circulation in the
North Sea. Tee (1976, 1977) developed a model for the upper Bay of Fundy,
showing even smaller scale eddies that correspond to patterns inferred from
arrays of moored current meters. Nihoul (1980) has generalized the model results
so that they produce maps showing areas where the residual circulation gains or
loses energy through wind stress, bottom frictional stress and tidal stress, all of
which vary in time and/or space.
Closed eddies can capture and isolate distinct biological populations for a
number of tidal cycles allowing the phytoplankton populations to pass through
several generations. Nihoul (1975) showed how these distinct biological-
chemical zones in the southeastern North Sea corresponded to distinct zones in
the Nihoul-Ronday model. In particular, a gyre off the Belgian coast contained
higher concentrations of suspended particles, many of biological origin, while
the sediment type underlying the gyre was predominantly organic muds. A large
portion of the phytoplankton population was dead, suggesting low grazing by
zooplankton. Dubois (1975) simulated coupled phytoplankton—zooplankton
patches growing and being distorted by residual circulation patterns in the
Nihoul-Ronday model.
Zimmerman (1978a, b) investigated smaller scale residual circulations caused
by tidal stress over irregular bottom topography. Particle paths are displaced from
the tidal current streamlines by the irregular bottom features. This ‘random tidal
dispersion’ can result in effective horizontal diffusion coefficients of order 103 m2·s
−1, large for the relevant length scale of 2km (cf. ′ 2m2·s−1 ‘from Okubo, 1971).
Zimmerman (1978a) demonstrated how a patch of tracer substance could be split

in two over a tidal cycle by random tidal dispersion. Horizontal dispersion from
the shear flows associated with internal waves can also distort patches, but
probably on scales of 100 m or less (Young, Rhines & Garrett, 1982). The
implications of these processes for the spatial distribution of plankton are
obvious; the importance of horizontal turbulent diffusion interacting with
reproductive rate in the development and control of phytoplankton patchiness
has been demonstrated by Kierstead & Slobodkin (1953), Denman & Platt
(1976), and Denman, Okubo & Platt (1977).
SHELF EDGE CANYONS AND BUMPS

Studies of currents in a variety of submarine canyons (Inman, Nordstrom &
Flick, 1976; Shepard, Marshall, McLoughlin & Sullivan, 1979) found that, in
most canyons, the near bottom currents are predominantly up and down the
canyon axis. Several sets of recent observations on the deflection of shelf edge or
coastal currents by submarine canyons have not yet reached publication, but
Hsueh (1980) presented a theory for wind-driven shelf currents being deflected
up the axis of Hudson Shelf Valley off the eastern United States that agrees with
available observations. Interestingly, Shepard et al. (1979) found that in the
Monterey submarine canyon, the largest canyon they studied on the west coast of
North America, the currents were not predominantly along the canyon axis
suggesting that large scale currents were deflected by the canyon but did not lose
appreciable energy to up or down canyon flow. Preller & O’Brien (1980)
developed a model of circulation over a bump in the continental slope (which
creates, effectively, a canyon immediately upstream). Current streamlines were
deflected by the topography creating an upwelling maximum in the vicinity of
the bump. Here we see again the selection of processes by relevant scale; while
large Gulf Stream meanders would be unaffected by a canyon or bump with
dimension 100 m, surface gravity and edge waves and internal waves (and their
induced flows) would definitely be affected by the same canyon.
The deflection of deeper offshore currents up canyon (Freeland & Denman,
1982) can transport nutrients into the euphotic zone on the continental shelf
resulting in high levels of biomass and biological production (Fig. 10). Denman
et al. (1981) and Brink et al. (1981) found areas of sustained enhanced
production that can be attributed to irregularities in bottom topography.
On smaller scales, coral reef grooves (scale 30 m) can interact with ambient
currents and wave-induced flow to produce extremely energetic turbulent
currents in and around the grooves (Roberts, Murray & Suhayda, 1977).
Biological effects resulting from enhanced material transport are not hard to
imagine. Tunnicliffe (1982) documented breaking and removal of corals by these
enhanced flows, and Woodley et al. (1981) described the havoc wreaked by
hurricane-induced waves and currents on the same coral reef ecosystem.
CAPES AND HEADLANDS

Eddies, fronts and enhanced mixing often result from flow around capes and
headlands. Pingree, Bowman & Esaias (1978) reviewed these circulations with
regard to frontal formation. Pingree & Maddock (1977) and Tee (1976, 1977)
reported on tidal residual models that generated residual eddies around capes,
also supported by observation. Bowman & Esaias (1977) investigated the nitrate
Fig. 10.—A, contours of ξ t at 50 m depth in the vicinity of a submarine canyon off British
Columbia: note the closed eddy structure centred at the head of the submarine canyon. B,
contours of oxygen along transect line A-B (see Fig. 10A): note the thick lens of low
oxygen near B. (From Freeland & Denman, 1982).
and chlorophyll concentrations in the vicinity of several headlands in Long

Island Sound and concluded that the main effects of biological consequence were
enhanced mixing and frontal development. Unfortunately, more closely coupled
biological-physical studies have not been performed even though the physical
studies of capes and headlands have often been motivated by biological
phenomena.
IMPINGING EDDIES AND CHANGING OCEANOGRAPIC

REGIMES
LONGER TIME SCALES

The processes we have discussed so far occur, for the most part, on time scales
less than 10 days. The physical events that often precipitate the most extensive
changes to the continental shelf ecosystem, however, occur on time scales longer
than 10 days and usually over spatial scales of hundreds of kilometres or more.
These processes, which replace or significantly alter the water masses on the
continental shelves, include impinging mesoscale eddies, annual changes in large
scale ocean circulation, and interannual trends or fluctuations in large scale
oceanic water mass characteristics associated with short term climate
fluctuations. Time scales can be as large as decades and the influence can extend
globally.
IMPINGING EDDIES
Our awareness of, and ability to study, oceanic eddies have resulted largely from
the development of satellite remote sensing (Fig. 11). Previously, even 27 years
of intensive ship sampling on a grid spacing of 80 km of the California Current
system, although it did imply the existence of mesoscale eddies, could not
delineate the development and evolution of individual eddies. Bernstein, Breaker
& Whritner (1977) demonstrated the powerful capability of satellite imagery to aid
our interpretation of eddy structures by presenting images following an
individual eddy for over a month. From simple baroclinic theory, they estimated
for the area a characteristic eddy wavelength of 230 km, phase speed of 1cm·s−1
and generation time of 98 days.
Observations from several other areas established the universality, the scales,
and the large volumes of such impinging eddies. Cresswell & Golding (1980)
documented several eddies impinging on the west Australian continental shelf.
Morgan & Bishop (1977) estimated the volume of water transported onto and off
the shelf in the Mid Atlantic Bight to be a significant factor in diluting the
riverine input in the region. P.C.Smith (1978), for the Atlantic shelf off Nova
Scotia, estimated the volume exchanged to be approximately 104 km3·yr−1, nearly
an order of magnitude larger than that by small scale frontal exchange (Voorhis,
Webb & Millard, 1976; Horne, 1978a). In the South Atlantic Bight, Atkinson,
Singer & Pietrafesa (1980) found that each eddy exchanges an average of 20%
of the volume of Onslow Bay; the eddies occur on periods of 14 to 60 days. In a
thorough statistical study of Gulf Stream meanders off the Mid Atlantic Bight,
Halliwell & Mooers (1979) obtained an average wavelength of 320 km and a
period of 50 to 60 days.
Theoretical calculations by Kroll & Niiler (1976) established the possibility

that such disturbances were topographical Rossby waves and that they could travel
across the continental shelf to depths as shallow as 25 m before being damped out
by friction. Petrie & Smith (1977) found evidence from the Nova Scotian shelf
for current fluctuations on scales from 10 to 60 days, and Garrett (1979) showed
that surface current observations on the east Australian shelf reported by Hamon,
Godfrey & Grieg (1975), which contained a peak in energy at periods near 120
days, were consistent with topographic Rossby waves propagating onto the shelf
to within 6·5 km of the coastline and into water less than 70 m deep.
Figure 11.—Phytoplankton pigment image from the Coastal Zone Color Scanner (CZCS)
for 22nd April 1979 depicting eddies off the Queen Charlotte Islands, Canada: the image
is roughly 350 km on a side and is centred at about 53°N: 135°W; lighter areas are higher
pigment concentrations (logarithmic grey scale); (courtesy Drs G.A.Borstad and J.F.R.
Gower).
What are the implications of these impinging eddies for continental shelf
ecosystems? They occur in these areas several times a year, and each eddy
exchanges a significant portion of the waters over the continental shelf. The
eddies off California transport subsurface waters to the surface layer that are rich
in nutrients needed for phytoplankton production (Traganza, Nestor &
McDonald, 1980). From data collected off the Scripps pier over a 20-year
period, Tont (1976) found diatom blooms of five to six weeks’ duration to be
correlated with low temperature anomalies considered to be the signature of
California Current eddies that carried nutrient-rich waters from higher latitudes.
Owen (1981) argued that a stationary eddy off Southern California is a
“reproductive refuge” for certain zooplanktonic organisms (Euphausia pacifica)
and controlled the distributional pattern of sardine eggs.
For the Nova Scotian shelf, P.C.Smith (1978) calculated that the low
frequency motions at periods greater than 10 days transported sufficient nutrients
onto the shelf to supply the new nitrogen required by the phytoplankton there
(Fournier et al., 1977). Similarly, for Onslow Bay, Paffenhofer, Deibel, Atkinson
& Dunstan (1980) reported that the Gulf Stream eddies intruding into the bottom
waters of the shelf contained nutrient-rich waters with initial concentrations
greater than 8 mmoles·m−3 of NO3-nitrogen. In these intrusions, phytoplankton-
sized particles and small zooplankton were more abundant than in the surface
waters on the shelf, suggesting that both phytoplankton and zooplankton were
supplied to the shelf waters in abundance with the potential for additional
enhanced production at both trophic levels.
Cresswell & Golding (1980) hypothesized on the importance of impinging
eddies to higher trophic levels of the continental shelf ecosystems. After
hatching, larvae of the rock lobster that inhabits the inshore reefs of the west
Australian shelf spend 9 to 11 months at sea before changing to the puerulus life
history stage and returning to the shelf where they are eventually deposited on
the inshore reefs. Cresswell & Golding suggested that the impinging eddies are
responsible for returning the puerulus stage to the shelf and that the random
occurrence of the eddies can explain the large year-to-year variability in the
success of settlement on the inshore reefs. Again we note that the life history
cycle of the organism matches the time scale of the eddies.
CHANGING OCEANOGRAPHIC REGIMES

Climate variability is of such current interest that we would be remiss not
to discuss some ramifications of climatic fluctuations to coastal ecosystems. We
consider two time scales here: the annual cycle where seasonal changes in large
scale oceanic current patterns cause the waters on adjacent shelf regions to be
replaced by waters with different water mass characteristics yearly, and climatic
time scales where significant changes in water mass characteristics occur from
year to year on up to several decades.
Annual cycles in water properties caused by large scale advection have been
documented, together with changes in the biological regime, along the west coast
of North America and more recently off Somalia in the Indian Ocean. In the
atmosphere over the northeast Pacific Ocean, the Aleutian low pressure system
persists throughout the winter months but is displaced to the northwest in spring
by the strengthening and northward movement of the North Pacific High (See
Fig. 1 in Tabata, 1975). The large scale ocean current patterns adjacent to
western North America change in response to the altered atmospheric forcing
(Hickey, 1979), with the spring transition occurring abruptly. Off southern
California, the southward flowing California Current intensifies and reaches the
coast during the spring (Hickey, 1979; Chelton, 1981), bringing relatively
nutrient-rich water from the north. During periods that it occupies the California
shelf, both phytoplankton and zooplankton biomass are greatly enhanced
(Bernal, 1981; Tont, 1981; Chelton, Bernal & McGowan, 1982). From Oregon to
British Columbia, the northward flowing winter currents on the mid to outer
shelf shift abruptly to southward currents in the spring (Huyer, Sobey & Smith,
1979; Freeland, pers. comm.). Off southern Vancouver Island, interaction of the
current system with bottom topography causes the shelf water to be replaced by
low oxygen, nutrient-rich water that persists throughout the summer months
(Freeland & Denman, 1982) causing substantial elevated primary production and
phytoplankton biomass (Denman et al., 1981). Off Oregon and Washington
where the coastline is more regular, wind-driven upwelling occurs during the
same period, but it is episodic rather than persistent (e.g. Wroblewski, 1977).
Off Somalia in the Indian Ocean, the advent of the southwest monsoon during
May causes a cold water eddy with associated upwelling to displace warmer
water on the Somalian shelf and to remain there for several months each summer
(Bruce, 1979; Brown, Bruce & Evans, 1980). The cold waters contain elevated
levels of dissolved nutrients and support higher phytoplankton biomass and
productivity (Smith & Codispoti, 1980). During the southwest monsoon, primary
productivity was approximately 120 mg C·m−3·day−1 at depths where the light
levels were above 50% of surface light; during the northeast monsoon season,
values were approximately 10 mg C·m−3·day−1, comparable with measurements
in the Sargasso Sea, an oceanic desert. The elevated primary production during
the southwest monsoon lasts a minimum of two months.
Interannual variations in these annual oceanographic cycles ought to affect the
marine ecosystem. Sutcliffe, Loucks & Drinkwater (1976) documented the
connections between year to year variations in the St Lawrence River outflow,
salinities and temperatures in the Gulf of Maine, and large scale air
temperatures. From 40 years of annual fish catch data for 17 commercial species,
Sutcliffe, Drinkwater & Muir (1977) found significant correlations between
annual catch and sea surface temperatures in the Gulf of Maine for 10 of the
species. Loder & Garrett (1978) found evidence at several coastal sites around
North America for an 18·6-yr cycle in sea surface temperatures which they
attributed to variations in tidal mixing caused by the 18·6-yr period modulation of
the tides. Rust & Kirk (1978) and Van Winkle, Kirk & Rust (1979) presented
evidence that this cycle affected striped bass catches for several stocks along the
Atlantic Coast of the U.S.A. Existing time series, however, are too short to
resolve between an 18·6-yr and, say, a 20-yr periodicity.
On longer time scales characteristic of climatic fluctuations, physical and
biological changes often extend over whole ocean basins: Cushing & Dickson
(1976) and Cushing (1982) reviewed the biological response in the sea to
climatic changes on a global scale; the continental shelf ecosystems off Peru and
off western Europe have been particularly studied for several decades. The
vagaries of the Peruvian anchovy fishery have received widespread attention
recently because of its tremendous economic importance (e.g. Quinn, Zopf,
Short & Kuo Yang, 1978). The El Niño, an oceanographic event that suppresses
the Peru upwelling and hence biological production there, has been shown
(Quinn et al., 1978; Enfield & Allen, 1980; Chelton, 1981) to be correlated with
much larger scale phenomena such as the Southern Oscillation. The prevailing
theory that the El Niño is caused by anomalously strong trade winds in the
central tropical Pacific in the two years preceding an event (Wyrtki, 1975)
suggests that El Niño should not be confined only to the southern hemisphere.
Chelton (1981), Chelton & Davis (1982), and Enfield & Allen (1980) have
shown the stronger El Niño events to be correlated with similar sea level and
steric anomalies as far north as Alaska and Tont (1981) and Chelton (1981) have
shown the biological consequences to be similar. Net poleward flow persisting
sometimes for several years correlates with lower phytoplankton and
zooplankton biomass off southern California. Chelton found zooplankton
biomass to be correlated with steric height anomalies for several months
previous with a peak correlation at one month lag. Mysak, Hsieh & Parsons
(1982) attributed these anomalies to poleward propagating baroclinic waves and
found correlations of about 5-yr periods with commercial fish populations off
British Columbia, Canada.
Perhaps the most dramatic documented biological response in the ocean to
climatic variation is the Russell cycle (termed by Cushing & Dickson, 1976) that
has occurred in the continental shelf biota around the British Isles. In the western
English Channel, catches of young fish, numbers of zooplankton, and the
concentration of dissolved phosphate all dropped sharply around 1930 and
remained at the lower levels (approximately 5% for fish and zooplankton,
approximately 70% for phosphate) until about 1970 when they rose equally
abruptly to their earlier levels where they have remained since (Russell,
Southward, Boalch & Butler, 1971; Southward, 1980). In support of
Southward’s finding, Colebrook, Reid & Coombs (1978) in the southern North Sea
observed in time series 15 to 20 years long a significant increase in 1970 in
phytoplankton colour index and in the abundance of several species of Ceratium.
The sea surface temperature, as well as several biological variables, however,
correlate with the 11-yr sunspot cycle (Southward, Butler & Pennycuick, 1975),
leading to speculation that the Russell cycle itself may be but a portion of a
longer fluctuation correlated with the 180-yr modulation of the sunspot cycle.
From these two examples we see that changes in physical climatic indicators
can amplify into sometimes catastrophic changes in marine ecosystems.
Furthermore, the present intense interest in marine climate changes off western
Europe and in the equatorial Pacific has in both cases been stimulated by the
search for the cause of ecosystem changes that have affected man on a large
scale.
CONCLUDING REMARKS
We have reviewed the dominant physical processes occurring in coastal seas and
the concomitant effects on coastal ecosystems. We have proceeded from the
smallest to the largest scales in both space and time for two reasons: first, to provide
an order or organization to the ideas, and secondly (and more important), to
match the physical and biological processes that are most likely to be connected,
under the assumption that connections are most likely between processes of
similar scales. Definite connections have been established at many scales, but
they centre around one main theme. Certain physical processes act to increase
nutrient availability and retention in the euphotic zone (near surface layer);
primary productivity and hence biomass increase; and transfer to higher levels of
the food chain is often effected, resulting in increased stocks of zooplankton and
ultimately fish. Such processes can be expressed in terms of conservation
equations analogous to those commonly used by physical oceanographers (e.g.
the concept of energy flow through ecosystems). Many ecologists largely view
the behaviour or functioning of ecosystems in terms of other non-conservative
and less immediately quantifiable properties such as competition, predation,
stability, length of food chain, community structure, succession, transfer
efficiency, and others. These properties describe the dynamics and functioning of
ecosystems at the level of complexity where we often require answers. For
example, the length of a marine food chain has practical importance because
shorter food chains, such as the Peru upwelling ecosystem terminating in the
anchovy, should result in the harvesting of a greater fraction of the biomass first
formed through primary production. Similarly, community structure and the
factors that control it are of very real importance to man as a harvester: food
chains that terminate in fish are useful to us, food chains that terminate in large
jellyfish are not. Physical oceanographers are not fully familiar with these
concepts, and biologists are still developing acceptable quantitative measures for
them. Yet the impact of physical processes on these ecosystem properties is an
important and unsolved problem.
In addition, our scale matching has not always produced results. Some very
energetic physical phenomena produce biological effects of little or no
ecological consequence, e.g. horizontal inertial oscillations. The coastal
ecosystem integrates over these phenomena remaining unperturbed. Other
physical phenomena result in catastrophic biological events (the obvious
example being the crash of the Peru anchovy fishery in response to an El Niño
event). Resonance or receptiveness of the ecosystem on the same scales as a
physical process are required for dramatic coupling.
We have neglected processes on one scale that is at present receiving
much attention—the microscale—corresponding to the small size of the
planktonic organisms themselves. Purcell (1977) reviewed a sample of the
surprising effects on biota that occur in this regime where the molecular
processes of viscosity and diffusion dominate. We note several other microscale
processes of potential importance in the coastal ocean. As phytoplankton take up
nutrients from the sea by transport across the cell wall, they may deplete a zone
around them if molecular diffusion cannot supply nutrients at the rate that the
organisms assimilate them. Pasciak & Gavis (1974, 1975) suggested that this
depletion may limit the production of some phytoplankton species. Hulbert
(1970) earlier calculated that the average spacing between individuals was large
enough so that such zones would not overlap. Thus the effects of diffusion
limitation on phytoplankton populations that are competing for nutrients is not

likely to be large. The recycling of nitrogen from the excreta of zooplankton may
supply the major fraction of the sea’s most limiting nutrient to phytoplankton
(Harrison, 1980). Indeed, McCarthy & Goldman (1979) and Goldman, McCarthy
& Peavey (1979) attributed the maintenance of algal populations in the very low
nutrient environment of the open ocean to the encounters with small patches of
nutrient-rich water created by zooplankton excretion (or perhaps bacterial
degradation). Jackson’s (1980) calculation of the rapid dispersal of such patches,
however, suggested that they exist for too short a period to sustain production.
Finally, Koehl & Strickler (1981) filmed zooplankton capturing their algal prey
and noted a distinctly different behaviour than indicated by earlier studies
(Marshall & Orr, 1955). They reasoned that the dominance of viscous forces at
these very small scales accounts for the observations. These findings are from
theoretical or laboratory studies; confirmation from observations of the impact of
microscale processes on coastal marine plankton requires carefully designed field
studies and some luck.
In our approach of matching scales, typically we have identified a particular
physical process and then hypothesized on the biological consequences on
comparable scales. Our subsequent search for the expected ecological studies
has, as often as not, been unsuccessful. Even where studies of certain physical
phenomena were motivated by attempts to explain apparent biological
consequences, coupled joint physical-biological studies rarely followed. We
must make a plea for more well-designed, well-integrated biological-physical
studies of ecosystems in the coastal ocean. In addition, to study two systems on
similar scales requires matched sampling technologies. Biologists have learned
much by continuous sampling from underway ships, but physicists have been
slow to exploit this mode of sampling. Recent mapping of surface currents from
moving ships (e.g. Joyce, Bitterman & Prada, 1982) will prove, however, to be
extremely useful in the interpretation of biological data. On the other hand,
biologists must develop more systems like the moored fluorometer of
Whiteledge & Wirick (1983), which are analogous to the moored instrument
systems used by physical oceanographers for over a decade, to monitor
ecosystems when on site sampling from ships is not possible.
We emphasize that by matching similar scales in the biological and physical
sectors, we have presumed that their dominant interactions are linear, i.e. cause
and effect occur on similar scales. Correlations alone. however, do not establish
cause and effect. In addition, we caution the reader that ample theoretical (e.g.
May, 1976) and experimental (Dwyer & Perez, 1983) evidence exists to suggest
that the components of ecosystems often behave in a non-linear fashion. The
functional responses of phytoplankton growth to light and/or nutrients and of
zooplankton feeding to their algal prey both exhibit saturating (non-linear)
forms, and many other examples could be cited. None the less, identification of
the space and time scales over which processes act is often the first step towards
uncovering the causes of observed, but unexplained phenomena. For example,
Koehl & Strickler (1981), in their studies of the details of zooplankton feeding
behaviour, were led to consider the importance of viscous forces because fluid
flow at the scales of individual zooplanktonic organisms (′ 1 mm) is dominated
by viscosity. By representing in dimensionless form their proposed conservation
equations for phytoplankton biomass in the upper ocean, several authors
(O’Brien & Wroblewski, 1973; Denman & Platt, 1977; Platt, Denman & Jassby,
1977; Lyne, 1983) have addressed the general question of spatial and temporal
scaling for coupled biological and physical processes in aquatic habitats. They
identified (non-dimensional) groups of variables that can aid in designing field
experiments to isolate and observe particular processes. Carefully designed,
process-orientated studies will push our knowledge beyond mere correlation of
biological and physical scales towards establishing causal mechanisms. These
studies are both challenging and fascinating, and the potential for future
understanding is great!
ACKNOWLEDGEMENTS
The authors wish to thank Dr Mark Abbot and three anonymous reviewers for
constructive comments on an earlier version of this paper. We also acknowledge
the financial support of the U.S. Aeronautics and Space Administration Oceanic
Processes Program under grant number NAG 5–217. Finally, we thank Drs Gary
Borstad and J.F.R.Gower for preparing and making available to us the satellite
imagery in Figures 3 and 11.
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MANGANESE IN THE MARINE
ENVIRONMENT
G.P.GLASBY
New Zealand Oceanographic Institute, Department of Scientific
and Industrial Research, P.O. Box 12–346, Wellington, New
Zealand
INTRODUCTION
The occurrence of manganese as ferromanganese oxide concretions on the sea
floor stems from three characteristics which make the geochemistry of
manganese unique amongst the elements of the periodic table: (1) its high
abundance in the lithosphere (being the eleventh most abundant element with an
average concentration of 0·8%) (Parker, 1964); it is therefore available for
incorporation in sedimentary systems; (2) its existence in two valency states (di-
and tetravalent) whose stability boundary lies within the range of the natural
environment; manganese can be therefore transported from areas of low redox
potential to well-oxidized environments; and (3) the high adsorption
characteristics of manganese oxides; this means that adsorption of divalent
manganese ions from aqueous solution is autocatalytic and that the manganese
oxides can act as efficient scavengers of other transition metal ions. The
adsorption is a function of the pHZ.P.C (pH of the zero point of charge). The
pHZ.P.C. of ξ MnO2 is 2.25 (Murray, 1974; Balistrieri & Murray, 1982a)
compared with about 7·1 for goethite (Balistrieri & Murray, 1979, 1981) (cf.
Parks, 1975). In sea water (pH 7·8) (Balistrieri, Brewer & Murray, 1981),
manganese oxides are negatively charged and, therefore, strongly adsorb cations
whereas iron oxides are near their zero point of charge and, therefore, do not
adsorb cations as strongly (Murray, 1975; Forbes, Posner & Quirk, 1976; Murray
& Brewer, 1977; Takematsu, 1979a, b; McKenzie, 1980; Li, 1981a, 1982;
Moorby & Cronan, 1981; Tipping, 1981; Balistrieri & Murray, 1982b, 1983).
This factor explains the inter-element relationships found in manganese nodules
(Glasby & Thijssen, 1982).
In addition, manganese is not significantly hydrolysed in aqueous solution
(Perrin, 1962; Broecker & Peng, 1982) but exists principally as the Mn2+ ion
over a wide pH range, although about 23–28% of the manganese in sea water is
MANGANESE IN THE MARINE ENVIRONMENT 165
complexed, mainly with chloride and sulphate ions (Crerar, Cormick & Barnes,
1980; Carpenter, 1983). Under suitable conditions, manganese can attain
moderately high concentrations (by geochemical standards) in aqueous solution.
In general, manganese migrates from zones of reducing conditions in the
divalent state and is fixed in oxidizing zones in the tetravalent state. This
manganese remobilization may take place within a sedimentary profile such as in
deep-sea sediments where less oxidizing conditions develop at depth or within a
lake or ocean system where redox conditions vary across the basin. This
migration ultimately leads to the high concentrations of manganese and the
formation of manganese nodules in deep-sea sediments which are well-oxidized
environments and represent the ultimate ‘sink’ for manganese in the sedimentary
system.
Berner (1981) has recently classified sedimentary environments and shown
that manganese oxides form in oxic environments which may be present to depths
of a metre or more in some deep-sea sediments but only to a few millimetres in
nearshore muds. Rhodochrosite (manganese carbonate) is formed in anoxic
environments (such as the surface sediments of Loch Fyne, Scotland or the
Panama Basin, eastern Pacific: Johnson, 1982; Pedersen & Price, 1982). It has
also been reported in Deep Sea Drilling Project cores (Borella & Adelseck,
1980). Manganese sulphide (alabandite) is thermodynamically stable only at very
high sulphide concentrations and is rarely found in marine sediments. A mixture
of authigenic manganese carbonate and sulphide has, however, been reported in
the central anoxic basin of the Baltic Sea (Manheim, 1961; Suess, 1979). On
burial within the sediment column, trapped oxygen is consumed in the oxidation
of organic matter during early diagenesis of the sediment. The sequence in
reduction of oxidants within deep-sea sediments has recently been studied by
Froelich et al. (1979) who showed that manganese oxides are the first species to
be reduced after oxygen. The depth at which manganese is reduced to the
divalent state—and therefore enriched in the sediment pore waters—is variable
and depends on the organic carbon content of the sediment and the sedimentation
rate. In nearshore continental shelf areas (and especially estuarine and fjord
systems), this depth is very small and much of the manganese is remobilized into
the overlying water column or, less commonly, trapped near the sediment surface
as rhodochrosite or manganese oxide concretions; this reflects the more reducing
conditions developed in this type of environment (Baas Becking, Kaplan &
Moore, 1960; Price, 1975; Heath, Moore and Dauphan, 1977; Müller & Suess,
1979; Müller & Mangini, 1980). In deep-sea sediments with low organic carbon
contents, on the other hand, the onset of this manganese remobilization varies
from over 20 cm to more than one metre. Because of the welloxidized nature of
deep-sea sediments and their low sedimentation rates, this manganese is trapped
in the surface layers of the sediment, often as manganese micronodules, or at the
sediment surface as manganese nodules (Marchig & Gundlach, 1979;
Klinkhammer, 1980a; Takematsu, 1981). A schematic representation of this
remobilization of manganese in deep-sea sediments is given in Figure 1 which
166 G.P.GLASBY
Fig. 1.—Schematic representation of trends in pore water profiles for equatorial Pacific
sediments: depth and concentration axes are in arbitrary units; (from Froelich et al., 1979).
also shows a mechanism of the separation of manganese from iron in the

sedimentary column. The importance of this manganese migration to the deep-
sea environment can be seen by the fact that the Pacific Ocean is estimated to
contain about tonnes of manganese nodules lying at the sediment
surface (Mero, 1965). The fractionation and enrichment of manganese has also
occurred in shallow basins and the huge sedimentary manganese ores at Nikopol
and Chiatura in the U.S.S.R. (Varentsov & Rakhmanov, 1980) and Groote
Eyland in Australia (Varentsov, 1982) are examples of this type. These
sedimentary deposits constitute the largest share of the world’s ore reserves of
manganese (Roy, 1981).
Much new work has recently accumulated on the geochemistry of manganese
in differing marine environments, such as estuaries and fjords, as well as the
deep sea. In this review, some characteristics of the distribution of manganese in
the marine environment will be discussed with a view to establishing the
pathways of manganese through the system. Because of the very large amount of
work on this subject which has been carried out over the last decade, no attempt
will be made to be comprehensive, merely to attempt to show some of the factors
involved in controlling the manganese geochemistry in the marine environment
and concentrating on more recent work. Previous reviews on manganese nodules
in this series include Tooms, Summerhayes & Cronan (1969) and Glasby (1973,
1974). Because manganese nodules have been extensively discussed elsewhere
(e.g. Glasby, 1977), they will receive only cursory treatment here. General
overviews of the geochemistry of manganese have been given by Crerar et al.

(1980) and Wedepohl (1980a).
SEA WATER AND PORE WATER

The extreme difficulty of accurate analysis of manganese in sea water is well
illustrated by the work of Riley & Taylor (1968, 1972) using a chelating ion
exchange method followed by atomic absorption spectrometry. Riley & Taylor
(1972), for example, reported a range of manganese concentrations in sea-water
samples from the equatorial North Atlantic of 1·5 μ g.l−1 with a relatively uniform
distribution in the area. Subsequently, however, Bender, Klinkhammer &
Spencer (1977) determined the ‘total dissolvable manganese’ (TDM) in sea
water by graphite furnace atomic absorption spectrophotometry following
acidification to pH 2 and pre-concentration (cf. McArthur, 1977; Klinkhammer,
1980a). They obtained a maximum value (with one exception) of 0.3 μ g·l−1 for
western North Altantic and northeastern Pacific sea water. This is an order of
mangnitude lower than the data of Riley & Taylor (1972). Bender et al. (1977)
stated, “We believe it is unlikely that so much variability truly exists in sea
water; we suspect such discrepancies arise during either sample collection or
analysis.” It is, therefore, probable that much of the earlier work on the analysis
of manganese in sea water is in error. This point has been made by Brewer (1975)
and Brewer & Spencer (1975). Brewer & Spencer (1975) suggested that the
improvement in analytical accuracy has been made possible by the “remarkable
sensitivity and specificity” of graphite furnace atomic absorption
spectrophotometry. The impetus of the GEOSECS programme, an ambitious
project designed to study the element budgets on a world-scale far more
meaningfully than before, has also played a major rôle. Meaningful data on the
manganese content of open ocean sea water has, therefore, probably been
available only since the mid-1970’s (cf. Bewers, Dalziel, Yeats & Barron, 1981)
and this development is now having a major impact on the study of the
manganese distribution and pathways in marine (and freshwater systems. This
problem has been nicely put into perspective by Turekian (1977) who stated that
“one has the feeling that the whole field of trace metal marine geochemistry
would have been completely dull over the last fifty years if it weren’t for
analytical errors”. A summary of the element contents of sea water has recently
been given by Quinby-Hunt & Turekian (1983).
From their data, Bender et al. (1977) were able to conclude that the TDM in
Pacific Ocean bottom waters is about one quarter of that in the surface waters
(0·1 μ g·l−1). In contrast to other transition metals, such as copper, nickel, zinc and
cadmium, the downward transport of manganese to the sea floor with falling
biogenic debris and regeneration in the deep sea is not the principal mechanism
controlling the distribution of this element in deep-sea environments (Landing &
Bruland, 1980). Subsequent studies by Klinkhammer & Bender (1980) showed
that manganese has a short residence time in ocean surface waters (5 to 25 yr)
168 G.P.GLASBY
and that there is a manganese maximum at the oxygen minimum in the water
column. Broecker & Peng (1982) have commented on the rapid removal of
manganese from sea water.
One of the principal features controlling the trace metal chemistry of sea water
which accounts for the very low metal contents is “the role particles play as
sequestering agents for reactive elements during every step of the transport
process from continent to ocean floor” (Turekian, 1977) (cf. Hunt, 1983). For
manganese, this statement is a corollary of the fact that manganese is grossly
undersaturated in sea water (Glasby, 1974). Very considerable effort is now
being directed to an understanding of the flux of particulate matter to the sea
floor and recent work has indeed shown that, with increasing depth in the water
column, the manganese content of particulate matter does increase, indicating
adsorption of manganese oxides on this material as it descends to the sea floor
(Brewer, Nozaki, Spencer & Fleer, 1980; Callender & Bowser, 1980; Landing &
Bruland, 1980; Martin & Knauer, 1980, 1982, 1983; Balistrieri et al., 1981;
Broecker & Peng, 1982).
Other studies have shown that manganese is an essential micronutrient to
organisms. Recent evidence suggests that photoreduction of manganese by
dissolved organic substances may take place in the upper layers of sea water and
thereby influence the manganese distribution in the photic zone (Sunda, Barber &
Huntsman, 1981; Sunda, Huntsman & Harvey, 1983). The input of manganese into
the oceans from atmospheric particulate matter has also been studied (Buat-
Mernard & Chesselet, 1979). More recently, a number of studies have dealt with
the distribution of manganese in coastal waters (Kremling & Petersen, 1978,
1981; Campbell & Yeats, 1982; Kremling, 1983a, b). Of particular interest is the
observation of Kremling (1983a) of an enrichment of manganese in surface
waters on the European continental shelf compared with those from further
offshore. This may be due to remobilization of manganese from the shelf
sediments. The manganese content of particulate matter in coastal waters has
been reported by Price & Calvert (1973).
In the case of sediment pore waters, analytical and sampling problems are
equally severe, especially in deep-sea sediments where manganese
concentrations in the pore waters are low. Callender & Bowser (1980) have also
stressed the importance of the temperature of storage and squeezing of the cores
on the determined manganese contents of the interstitial waters (cf. Bischoff & Ku,
1970, 1971). Presley, Brooks & Kaplan (1967), for example, obtained much
higher manganese concentrations in pore waters from calcareous ooze and red
clay than later workers. Similar high values were obtained by Li, Bischoff &
Mathieu (1969). The idea that manganese may be remobilized in the sediment
column after burial under locally reducing conditions was first suggested by
Murray & Irvine (1894) and later by Brujevicz (1938). Such migration was not
experimentally confirmed by studies of pore water chemistry until the work of Li
et al. (1969) on a sediment core from the Arctic Basin. Subsequent work showed
that this migration process is well defined in sediments of Loch Fyne, Scotland
(Calvert & Price, 1972; Duchart, Calvert & Price, 1973), in various estuaries on
the eastern seaboard of the U.S.A. (Holdren, Bricker & Matisoff, 1975;
McCaffrey et al., 1980; Aller & Benninger, 1981; Elderfield, 1981; Elderfield,
McCaffrey et al., 1981) and elsewhere (Krom & Sholkovitz, 1978; Murray,
Grundmanis & Smethie, 1978; Lyons et al., 1980), but only recently have
reliable data become available for deep-sea sediments (Michard, Grimaud &
Lavergne, 1974; Addy, Presley & Ewing, 1976; Gundlach, Marchig & Schnier,
1977; Froelich et al. 1979; Callender & Bowser, 1980; Klinkhammer, 1980b;
Gieskes, 1981; Hartmann & Müller, 1982; Klinkhammer, Heggie & Graham,
1982; Tsunogai & Kusakabe, 1982; Sawlan & Murray, 1983); these data have
permitted modelling of manganese flux rates through the sediments (Burdige &
Gieskes, 1983). In deep-sea sediments, it is now believed that manganese is
reduced within the sediment column and diffuses upwards to be re-oxidized and
trapped in the upper layers of the sediment column (Klinkhammer, 1980b) (cf.
Tsunogai, Yonemaru & Kusakabe, 1979). Because of this, manganese is only
very inefficiently cycled back into the ocean bottom waters and less than 5% of
the manganese introduced into the sediment is thought to migrate through the
sediment-water interface and, therefore, to be available for manganese nodule
genesis (Callender & Bowser, 1980). Evidence has also been presented for the
release of manganese in the dissolution of siliceous tests on the sea floor
(Gieskes, 1981); the manganese content in the silica fraction of siliceous
frustules has been found to be in the range 2 to 11·5 μ g·g−1 (Martin & Knauer,
1973). The problems of measuring trace metal contents of pore waters of deep-
sea sediments can be better appreciated, however, when it is realized that the
manganese content of such water is about 1000 times lower than that in Loch
Fyne pore waters with values of the order of μ g·l−1.
NEARSHORE ENVIRONMENTS AND LAKES

Nearshore environments represent a whole range of marine and semimarine type
areas such as estuaries, fjords, inland seas with restricted access (such as the
Black Sea) as well as the open continental shelf. In some cases where restricted
circulation prevails (as in the Black Sea and a limited number of fjords), the
waters of the basin may become density stratified and reducing conditions
develop at depth within the water column. Because the redox gradients are most
marked in such situations, considerable effort has gone into studying the
geochemistry of nearshore environments over the last few years. In this section, a
limited number of studies are quoted as examples of the sort of processes
controlling manganese distribution in this type of environment. For convenience,
lake studies are included here. Whilst lakes and sea water obviously display
different salinity characteristics, the influence of redox characteristics on metal
distribution is similar.
Freshwater ferromanganese concretions are widespread in the temperate
latitudes of North America, Europe and the Soviet Union and have been
170 G.P.GLASBY
excellently documented by Callender & Bowser (1976), Sozanski & Cronan

(1976, 1979), and Dean & Ghosh (1980). Typically, these deposits occur in
formerly glaciated regions where glacial debris derived from Precambrian shield
rocks is present. Manganese is easily leached from such material. This type of
region is also typically afforested with deciduous trees which results in abundant
tree litter and humus. As a result, the ground waters and streams tend to be acidic
with a high humus content, both of which favour manganese and iron migration
(Borchert, 1980; Winterhalter, 1980). Black coatings of manganese oxides can
be found in stream sediments in such regions, particularly in fast flowing streams
where dissolved oxygen is plentiful (Chao & Theobald, 1976; Carpenter &
Hayes, 1980; Cerling & Turner, 1982). Manganese concretions in the lakes
represent the precipitation of manganese and iron oxides under the more
oxidizing conditions encountered there. Also favouring the deposition of the
manganese and iron oxides in lakes are the settling out of the particulate matter
carried by the river water and the dilution of the humic complexes by lake water.
The manganese concretions in lakes tend to be found associated with sand and
gravel sediments which are well sorted and have low sedimentation rates. The
combination of available nuclei for concretion growth and a welloxygenated
environment favour such concretions. The concretions are not generally found in
the deeper parts of the lakes where less-oxidizing conditions prevail. Typically,
recycling of manganese and iron takes place from the sediments in the deeper
parts of the lake as a result of redox gradients. Lake concretions tend to show a wide
variety of characteristics dependent on their location in the lake and the relative
influence of direct precipitation from lake water and diagenetic remobilization
from lake sediments. The concretions are usually small and sometimes have
“skirts” reflecting a source of diagenetically-derived manganese from the
underlying sediments. These freshwater concretions are quite different in
character (particularly in size, shape, composition, and growth rates) from their
deep-sea counterparts. Lake concretions, for example, tend to have much higher
Fe/Mn ratios than marine nodules, although the iron content of freshwater
concretions can be variable both within individual concretions (Moore, 1981) or
across the lake (as, for example, in Green Bay, Michigan, where the Fe/Mn ratios
of the concretions decrease away from the input source: Callender & Bowser,
1976). The higher iron contents of freshwater concretions compared with their
marine counterparts are attributed to two factors: the more reducing conditions
prevalent in lake sediments compared with nearshore marine sediments which
results in the remobilization of both iron and manganese within the sediment
column and the fact that reduction of sulphate to sulphide is not possible in
freshwater systems (because of the low sulphate concentrations) so that trapping
of iron as iron sulphide within the sediment column (as in nearshore marine
systems) cannot take place. The much higher rate of growth of freshwater
concretions (mm per 100 yr) Moore, Dean, Krishnaswami & Borole, 1980)
compared with their deep-sea counterparts (mm per 106 yr) reflects the higher
rate of input of manganese and iron into the lake system under favourable
conditions. The obverse of this, however, is that lake concretions represent only
transient phenomena within a lake system and are likely to ‘dissolve’ when
sedimentation conditions change and the nodules become covered by sediment. A
mass balance study of manganese in Oneida Lake, New York, has shown that
about 95% of the manganese deposited in the lakes is in the form of manganese
nodules, although this is unusual (Dean & Ghosh, 1978; Dean, Moore & Nealson,
1981; Chapnick, Moore and Nealson, 1982). In some lakes, anoxic conditions
develop within the deeper section of the lake on a seasonal basis. Davison (1981)
and Davison, Woof & Rigg (1982) have made a detailed study of the effects of
anoxia on the supply of manganese to the lake basin in the case of Esthwaite
Water in the English Lake District (cf. Sholkovitz & Copland, 1982a). Using
mass balance calculations, Davison concluded that the major source of
manganese in the anoxic layer of the lake is the dissolution of particulate material
sedimenting through the water column rather than the remobilization of
manganese from the sediment. Similar studies have been carried out in Lake
Windermere (Sholkovitz & Copland, 1982b) as well as in a coastal pond in
Massachusetts (Horne & Woernle, 1972). The manganese content of interstitial
waters in the sediments of Lake Ontario have been reported by Weiler (1973).
In Lake Michigan, an attempt has been made to calculate the dissolved
manganese profile in the sediments (Robbins & Callender, 1975). More recently,
Laxen & Chandler (1983) have studied the particle size distribution of
manganese in lake waters and shown that manganese is more likely to be in the
soluble than in the particulate form in such waters. These results illustrate the
complex nature of manganese distribution and cycling in lake waters. The
surface change characteristics of manganese oxides in lake waters have also been
shown to be modified by the adsorption of humic substances (Tipping & Heaton,
1983).
One of the most comprehensive studies of manganese in an anoxic marine
basin is in the Black Sea which is the world’s largest anoxic basin (Brewer &
Spencer, 1971; Spencer & Brewer, 1971; Spencer, Brewer & Sachs, 1972). The
exchange of water between the Black Sea and the Mediterranean through the
Dardanelles and Bosphorus is inadequate to flush the Black Sea on a reasonable
time scale. Below 275 m therefore, the waters of the Black Sea become anoxic
and are characterized by the presence of hydrogen sulphide. The waters are, of
course, salinity stratified. The surface waters have a salinity of 17·2 to 18·3‰
compared to the deep water with a salinity of 22·4‰. The manganese
distribution in the water colunm shows clearly the influence of redox conditions
on the distribution of the manganese with a very significant enrichment of
manganese in the anoxic bottom water (Fig. 2). Spencer & Brewer (1971) have
developed an elegant model to account for this distribution in detail. Similar
situations to the Black Sea are encountered in the Cariaco Trench off Venezuela
(Bacon et al., 1980) and in certain anoxic fjords (Jacobs & Emerson, 1982). In
the Baltic Sea, Balzer (1982) has documented the remobilization of manganese
in the sediment colunm directly by placing a bell jar in situ on the sea floor and
172 G.P.GLASBY
observing the chemical reactions over a prolonged period (cf Hartmann, 1964;
Kremling & Petersen, 1978; Boström, Burman, Pontér & Ingri, 1981; Kremling,
1983b).
Estuaries are important because they represent the mixing of fresh water and
sea water in an enclosed situation. The dissolved manganese may behave
conservatively or non-conservatively depending on the estuary considered. The
chemical reactions involved are complex (cf. Morris, Bale & Howland, 1982a, b)
and Liss (1976) and Aston (1978) have outlined some of the processes involved.
These include hydroxide formation, redox reactions, adsorption-desorption and
biological effects. In addition to processes occurring in the water column,
manganese can be recycled from the sediment back into the water column
reducing conditions develop.
A particularly interesting study has been carried out in the Gulf of St
Lawrence in Canada (Sundby, 1977; Yeats, Sundby & Bewers, 1979; Sunby,
Silverberg & Chesselet, 1981). Here, it was shown that, in the sediments of the
Laurentian Trough, the manganese content in the upper 20 mm of the sediment
column is high (up to 0·7% depending on location) but drops rapidly to
background (0·05 to 0·09%) below this depth. Within the water column,
maximum dissolved manganese concentrations are found close to the sediment-
water interface whereas the particulate matter has the highest manganese
concentration 30 to 100 m above the bottom. These concentration gradients are
interpreted as being due to the diagenetic release of manganese from the sediment
and the oxidation of the manganese in the water column. This sequence depends
on the tidal cycle with particles settling to the bottom, being redissolved into the
water column and so on. The net effect after each tidal cycle, however, is the
movement of the particles seaward. This has been named by Sundby et al.
(1981) the “broom effect”. From mass balance calculations, these authors were
able to show that the sediments of the Gulf of St Lawrence do not act as
significant traps for the riverine manganese introduced into the estuary but rather
that there is a net export of manganese from the Gulf of about (or
about 60% of the manganese introduced into the Gulf by rivers). Based on a
consideration of the total river input into the world’s oceans, Sundby et al.
(1981) estimated that of manganese are introduced into the
oceans in this way. This represents a significant proportion of the total flux of
manganese to deep-sea sediments, namely 15% of the total flux to deep-sea
sediments based on the calculations of Bender, Klinkhammer & Spencer (1977).
Wedepohl (1980a), on the other hand, gave slightly higher estimates for the
continental supply of manganese by rivers to the oceans, namely
suspended manganese and dissolved manganese. Similar
calculations by Trefry & Presley (1982) demonstrated the flux of manganese
from Mississippi Delta sediments into the Gulf of Mexico. These calculations
agree with Turekian’s assertion that only minor leekage of manganese from
estuaries is necessary to provide the flux of manganese to the deep-sea floor (cf.
Lyons & Gaudette, 1979). Other studies by Evans, Cutshall, Cross & Wolfe
Fig. 2.—Profile of the concentrations of dissolved manganese in Black Sea waters: data
plotted with depth relative to the oxygen zero boundary; (from Spencer & Brewer, 1971).
(1977), based on Newport River Estuary, North Carolina, have sugges ted that
this “net export” of manganese from riverine sediments is usually compensated
by riverine bed load supply. This component is usually ignored in mass balance
equations because of the difficulty of measuring it. Recent studies of dissolved
and particulate matter in river waters are important in these flux calculations
(Gibbs, 1977; Sholkovitz, Van Grieken & Eisma, 1978; Martin & Meybeck,
1979; Teraoka & Kobayashi, 1980; Yeats & Bewers, 1982). Martin & Meybeck
(1979) point out that manganese is transported in rivers dominantly (>90%) in
the particulate phase and that, on average, the particulate fraction of river water
contains 0·1% manganese.
Numerous other studies on the distribution of manganese in estuaries have
been carried out over the last decade. These include estuaries on the eastern
seaboard of the United States (Wolfe, Cross & Jennings, 1973; Graham, Bender
& Klinkhammer, 1976; Evans et al., 1977; Lyons & Gaudette, 1978; Sanders,
1978; Luedtke & Bender, 1979; Hess & Moore, 1980; Aller & Benninger, 1981;
Elderfield, Luedtke, McCaffrey & Bender, 1981; Klinkhammer & Bender, 1981;
Sigleo & Helz, 1981; Wilke & Dayal, 1982), in the U.K. (Holliday & Liss, 1976;
Morris, Mantoura, Bale & Howland, 1978; Sholkovitz, 1978, 1979; Boyden,
Aston & Thornton, 1979; Moore, Burton, Williams & Young, 1979; Morris &
Bale, 1979; Knox & Turner 1980; Knox et al. 1981; Sholkovitz & Copland,
1981; Morris, Bale & Howland, 1982a, b; Hirst & Aston, 1983), in the Rhine,
Sheldt, and Weser estuaries (van der Weijden, Arnoldus & Meurs, 1977;
Duinker & Nolting, 1978; Duinker, Wollast & Billen, 1979; Wollast, Billen &
174 G.P.GLASBY
Duinker, 1979; Duinker, Hillebrand, Nolting & Wellershaus, 1982), off Japan
(Hirata, Takimura & Shiozawa, 1978; Hoshika, Takimura & Shiozawa, 1978;
Tsunogai & Uematsu, 1978; Kitano & Fujiyoshi, 1980; Sakata, Kitano &
Matsumoto, 1981; Shiozawa, Hoshika, Takimura & Tanimoto, 1982; Uematsu &
Tsunogai, 1983), in Korea (Yearn & Park, 1978), in New Zealand (Lee, 1983), in
the Amazon Estuary (Sholkovitz & Price, 1980) as well as in an anoxic fiord on
the west coast of Canada (Grill, 1978, 1982; Emerson, Cranston & Liss, 1979;
Emerson et al. 1982; Jacobs & Emerson, 1982). A study of the influence of
summertime anoxia on manganese concentrations in Chesapeake Bay has been
described by Eaton (1979).
On the open continental shelf, there are a number of sediment and mineral
types (including manganese nodules). The geochemistry of these has been well
documented by Calvert (1976). Because of the influence of diagenetic
remobilization of manganese in shelf sediments, the geo-chemistry of shallow
water, continental shelf manganese nodules is fundamentally different from that
of deep-sea nodules (Manheim, 1965; Calvert & Price, 1977). Cronan (1980a)
has, however, suggested that all ferromanganese deposits can be considered to be
members of a continuous spectrum. In spite of the three-fold lower content of
manganese in nearshore sediments from the northwest African continental shelf
compared with Atlantic deep-sea sediments, Elderfield (1972a), none the less,
found that the manganese content of shelf sediments retains a substantial (>60%)
hydrogenous character.
THE DEEP SEA

Deep-sea sediments cover approximately 50% of the earth’s surface. The high
manganese content of these sediments has been noted and its origin speculated
on since the initial work on the material collected during the Challenger
Expedition of 1872–1876 (Murray & Renard, 1891). Lynn & Bonatti (1965)
have summarized three possible explanations for this manganese enrichment
based on earlier work.
(1) Manganese is supplied by the weathering of continental rocks, carried into

the ocean and slowly precipitated at the bottom, thus being concentrated in
areas with low rates of terrigenous sedimentation.
(2) Manganese is supplied by submarine volcanism.
(3) Manganese is enriched in the surface sediments by a secondary process,
namely the post-depositional remobilization of manganese from lower,
reduced layers in the sediment column to upper, oxidized layers where it
would then re-precipitate.
Other models have been discussed elsewhere (Elderfield, 1972a, 1976, 1977;
Broecker, 1974; Chester & Aston, 1976); that of Chester & Aston (1976) is the
most comprehensive. In fact, Lynn & Bonatti (1965) demonstrated the
importance of mechanism (3), particularly in the hemipelagic areas off the west
coast of the United States of America (Wangersky 1962; Bonatti, Fisher, Joensuu
& Rydell, 1971). Similar confirmation has been carried out in the northwestern
Pacific (Volkov, Rozanov & Sokolov, 1975; Rozanov, 1982) (cf. Price, 1975).
Indeed, there is evidence that, in some areas such as the Bering Sea, manganese-
rich horizons may be climatically related and reflect conditions at the end of the
Last Glaciation (Gardner, Dean, Klise & Baldauf, 1982). A similar effect has
been noted in the equatorial Pacific (Berger, Finkel, Killingley & Marchig, 1983;
cf. Anonymous, 1983).
Using a different approach, Bender (1971) noted that, on average, deep-sea
sediments contain 0·67% manganese on a carbonate-free basis compared with
0·03 to 0·16% for the major continental rock types and he defined the difference
between the manganese content of a deep-sea sediment (on a carbonate-free
basis) and 0·1% manganese (that of the average shale) as the “excess”
manganese content of deep-sea sediments. This enrichment of manganese in
deep-sea sediments is also accompanied by a marked fractionation from iron
(Wedepohl, 1980b).
Apart from the high manganese content of deep-sea sediments, considerable
variation in its concentration on an ocean-wide basis is known. This has, for
example, been well documented in the Pacific (Goldberg & Arrhenius, 1958;
Cronan, 1969; Boström, Kraemer & Gartner, 1973; Skornyakova, 1976; Leinen
& Stakes, 1979) and Indian (Bender & Schultz, 1969) Oceans. The distribution of
manganese in Pacific Ocean sediments is given in Figure 3. The fact that the
manganese content of surface sediments in the Atlantic Ocean (on a carbonate-
free basis) is higher in the central region of the ocean and related to the low
accumulation rates was recognized in early studies (Turekian & Imbrie, 1966).
Three principal theories (the trace element veil theory, the differential transport
theory, and the active ridge theory) accounting for these variations have been
summarized by Elderfield (1972a) and various models for the incorporation of
transition elements into deep-sea sediments were discussed by Chester & Aston
(1976). More recently, the systematic increase in the manganese content of
sediments across a major oceanic basin such as the Southwestern Pacific Basin
with increasing distance from land has been noted (Glasby, Hunt, Rankin &
Darwin, 1979; Meylan, Glasby, McDougall and Kumbalek, 1982). Selective
leaching experiments have also shown that, in deep-sea sediments, manganese is
dominantly (>90%) in the hydrolysate (non-lattice held) fraction of the
sediments (Chester & Hughes, 1969; Krishnaswami, 1976; Takematsu, 1978;
Bischoff, Heath & Leinen, 1979; Bowser, Mills & Callender, 1979; Förstner &
Stoffers, 1981). Some of this manganese is in the form of micronodules. None
the less, care must be taken in interpreting the results of leaching experiments
which are largely dependent on the experimental conditions used (Wakefield,
1980; Van Valin & Morse, 1982).
Of particular interest in assessing the origin of the high manganese content of
deep-sea sediments is that material balance equations based on the derivation of
176 G.P.GLASBY
Fig. 3.—Schematic map of the distribution of manganese in Pacific surface sediments (on
a carbonate-free basis): dotted line marks the boundary of the oxidized layer with a
thickness greater than one metre; (from Skornyakova, 1976).
sedimentary rocks from igneous rocks show that manganese, amongst other
elements, is not in balance and that another source of the element is required
(Rubey, 1951; Goldberg & Arrhenius, 1958; Horn & Adams, 1966; Chester &
Aston, 1976; Krishnaswami, 1976; Li, 1981b). Bender and his co-workers have
considered the problem of the source of manganese in deep-sea sediments and
manganese nodules. In their earlier work, Bender, Ku & Broecker (1966, 1970)
and Bender (1972) showed that manganese nodules and sediments from the same
area of the ocean floor accumulated manganese at approximately the same rate.
These findings suggested that manganese nodules exist “not because of some
unusual ability to attract available manganese but rather because some
mechanism prevents objects like sharks’ teeth and volcanic fragments from being
covered with sediment. They remain on the surface and accumulate manganese
at roughly the same rate as the surrounding sediment.” Subsequent theoretical
calculations showed that the upward migration of Mn2+ ions cannot supply the
excess manganese in marine sediments when the manganese needs to be
transported more than 1 m (Bender, 1971). This situation does not prevail in
deep-sea sediments where the manganese-rich zone is at least 10 m thick. This
mechanism cannot, therefore, be a major factor in controlling the composition of
deep-sea sediments. This view is echoed by Elderfield (1976) and Boudreau &
Scott (1978) (cf. Michard, 1971). Finally, on the basis of a detailed study of the
manganese content of sea water, Bender et al. (1977) concluded that the “excess”
manganese in pelagic sediments is derived not from the dissolved manganese in
sea water or from a hydrothermal input but rather from terrigenous particles (cf.
Li, 1981b). This idea is not incompatible with those of Turekian (1977), Sundby,
Silverberg & Chesselet (1981), and Trefry & Presley (1982). Wedepohl (1980b)
concluded, on the basis of mass balance calculations, that reduced sediments on
the continental margins and reactions during hydrothermal leaching of basalt at
spreading ocean ridges are the major sources of pelagic manganese (see p. 183).
There also appears to be evidence that the manganese contents of deep-sea
sediments are inversely related to the rate of sedimentation (Goldberg &
Arrhenius, 1958; Krishnaswami, 1976; Glasby et al., 1979). Sediment surfaces
with a long contact time with sea water (i.e. low sedimentation rate) having the
highest manganese (and iron) contents. This also accounts for the increasing
darkness in colour of deep-sea sediments with increasing distance from land.
Chocolate brown clays with high manganese and iron contents are found only in
the remotest parts of the deep oceanic basins. Li (1981a, 1982) has suggested
that adsorption of elements on the hydrous oxide surfaces of iron oxide,
manganese oxide and clay minerals is the most important mechanism in the
removal of many transition elements from sea water.
Of particular interest in the deep sea are the manganese nodules, commonly
found at the sediment surface, which can occur in amounts in excess of 20kg·m−2
and contain up to 3% nickel+copper+cobalt in favourable cases. These deposits
are found in highest abundances in regions of the ocean floor where
sedimentation rates are low. It is believed that the high nickel and copper
contents of these deposits are due to the dissolution of siliceous tests on the sea
floor (Glasby & Thijssen, 1982) (see, however, Cronan, 1980b; Cronan &
Moorby, 1981). Only nodules from the high productivity regions of the equatorial
Pacific and Indian Oceans, therefore, contain the high nickel and copper contents
required for commercial exploitation; these deposits represent only a small
percentage of the total nodules available. Whilst such nodules represent the
‘glamour’ aspects of the manganese cycle in the marine environment because of
their unique nature and the interest of commercial companies in their
exploitation, it must be emphasized that they represent only a part of the marine
geochemical cycle. Although the deep-sea environment may be regarded as the
ultimate ‘sink’ for manganese, manganese nodules are by no means the most
important part of this sink quantatively since deep-sea sediments contain more
manganese (cf. Bender et al., 1966, 1977). Wedepohl (1980a), for example, has
estimated that about tonnes of manganese are stored in manganese
nodules compared with about in deep-sea sediments (i.e. a ratio of 1:
178 G.P.GLASBY
2000). Much of the effort now directed towards the study of manganese nodules,
particularly in the United States, is a detailed understanding of the flux of metals
to the upper and lower surfaces of the nodule from sea water and pore water,
respectively, in a range of different environments. It is now recognized that
manganese nodules are polygenetic (depending on location) and have several
sources of element supply. Bonatti, Kraemer & Rydell (1972) classified the
deposits as hydrogenous (derived from sea water), hydrothermal (derived from
hydrothermal activity in the sea floor) and diagnetic (derived from post-
depositional redistribution of elements within the sediment coloum). To this end,
the MANOP programme funded by the United States is putting a “bottom
lander” on the sea floor to measure directly element fluxes across the sediment-
water interface at five type locations on the floor of the Pacific Ocean (Bender,
1983). In addition, estimates of metal fluxes to the upper and lower surfaces of
nodules have been made by means of radiochemical studies of individual
nodules (Moore et al., 1981). In one nodule from the equatorial Pacific, for
example, the flux of manganese on to the nodule top is the range 200 to 230
μ g·cm−2·1000 yr−1 whilst the flux to the nodule bottom is in the range 600 to 870
μ g.cm−2·1000 yr−1. This suggests that the greatest contribution of manganese to
the nodule is from the pore water rather than the sea water, although this
situation is probably reversed in red clay environments (cf. Tsunogai, Nakanishi
& Yamada, 1982). There is some evidence that the trace metal contents of
nodules are related to nodule growth rate (Heye & Marchig, 1977; Takematsu,
Sato & Okabe, 1981; Glasby & Thijssen, 1982; Lyle 1982). It should be
emphasized, however, that deep-sea manganese nodules have growth rates of the
order of mm·106 yr−1 which makes them one of the slowest growing mineral
deposits on this planet. Based on a geochemical study of siliceous ooze
sediments from the equatorial north Pacific, Marchig & Gundlach (1979, 1982a)
have concluded that manganese micronodules are remobilized in the upper 35 cm
of the sediment column and that this mechanism supplies 96% of the metal
content of the nodules in area. Because only a minor proportion of the metal in
the sediment column is mobilized, it has not proved possible to detect this
depletion of the metals in the sediment directly. This work shows clearly the
importance of the upper 50 cm of the sediment column in controlling the
chemical characteristics of manganese nodules. It must be emphasized, however,
that this situation applies only in the biologically productive region of the
equatorial Pacific and would not be so pronounced in less productive areas of the
ocean such as the red clay regions of the temperate latitudes.
HYDROTHERMAL INPUTS
One of the most exciting recent findings in oceanography is that manganese is
being injected into the ocean bottom waters by hydrothermal activity, principally
at the axes of mid-ocean ridge systems—the so-called “zones of divergence”—
where new ocean crust is being formed. The occurrence of metalliferous
sediments near the axes of mid-ocean ridge systems such as the East Pacific Rise
was first recognized by Boström & Peterson (1966) and much work has been
carried out in documenting these deposits (cf. Hekinian & Février, 1979; Cronan,
1980b; Bonatti, 1981; Dymond, 1981; Fyfe & Lonsdale, 1981; Meylan, Glasby,
Knedler & Johnston, 1981; Marchig & Gundlach, 1982b; Rona, 1982; Edmond &
von Damm, 1983; Varnavas & Papaioannov, 1983). Recently, metalliferous
sediments have been discovered as basal sediments in a marginal basin (Bonatti,
Kolla, Moore & Stern, 1979).
It is now becoming apparent that hydrothermal processes represent a major
source of manganese in the oceans (Boström, 1967; Ellis, 1968; Bender et al.,
1971; Corliss, 1971; Hart, 1973; Bischoff & Dickson, 1975; Elderfield, 1976,
1977; Lyle, 1976, 1981; Wolery & Sleep, 1976; Elderfield, Gunnlaugsson,
Wakefield & Williams, 1977; Corliss et al., 1979; Edmond et al., 1979a, b,;
Mottl, Holland & Carr, 1979; Hariya, 1980; Klinkhammer, 1980c; Wedepohl,
1980b; Edmond 1981; McMurtry, Veeh & Moser, 1981, Seyfried & Mottl, 1982;
Edmond & von Damm, 1983). Lyle (1976) has estimated the flux of
hydrothermal manganese to the oceans to be about based on the
occurrence of manganese in metalliferous sediments. The importance of this flux
was not fully appreciated by previous workers (cf. Glasby, 1973; Bender,
Klinkhammer & Spencer 1977). (p. 181). The release of manganese during the
palagonitization of basaltic glass has also been calculated (Staudigel & Hart,
1983). In addition to metalliferous sediments sensu stricto, fast growing
manganese crusts of hydrothermal origin have been found at the axes of some
mid-ocean ridge systems (Scott et al., 1974; Moore & Vogt, 1976; Cann, Winter
& Pritchard, 1977; Lalou, Brichet, Ku & Jehanno, 1977; Lonsdale 1977; Rona,
1978, 1980a, b; Toth, 1980; Grill, Chase, MacDonald & Murray, 1981; Lalou,
Brichet, Jehanno & Perez-Leclaire, 1983). Hydrothermal manganese deposits
have also recently been reported from an active island arc in the southwestern
Pacific (Cronan et al., 1982) as well as on volcanic seamounts in the Tyrrhenian
Sea (Kidd & Ármannson, 1979; Morten et al., 1980; Rossi, Bocchi & Lucchini,
1980).
The sequence of hydrothermal precipitation at oceanic spreading centres has
been formulated by Cronan (1980c) who divided metal-rich hydrothermal
deposits into three types: (1) base metal and iron-rich sulphides, sometimes
associated with oxides and silicates; (2) sharply fractionated oxides and silicates;
and (3) widely dispersed ferromanganese oxides. Cronan (1976) also proposed
the use of geochemical exploration methods to locate submarine geothermal
activity. At the TAG (Trans-Atlantic Geotraverse) hydrothermal field on the Mid-
Atlantic Ridge, for example, Cronan, Rona & Shearme (1979) found a
distribution halo of manganese in the sediments about 20 km in diameter (cf.
Shearme, Cronan & Rona, 1983). Bignell, Cronan & Tooms (1976) also found a
10-km wide manganese dispersion halo around the Atlantis II Deep in the Red
Sea. Similar trends were reported at Santorini in the Aegean Sea by Smith &
Cronan (1983).
180 G.P.GLASBY
None the less, it is only comparatively recently that direct evidence of these
hydrothermal emanations based on visual evidence from submersibles as well as
local sea-water chemistry has become available, particularly at the axis of the
Galapagos Rift in the eastern Pacific (Edmond et al., 1979a, b; Dymond, 1981;
Edmond, 1981, 1982; Edmond, von Damm, McDuff & Measures, 1982). It is
now believed that sea water permeates the fractured and fissured basalts in active
mid-ocean ridges and emerges as hot (′ 350°C), acidic springs at the ridge crest.
These solutions are substantially modified on their passage through the basalts
and leach a number of elements including manganese. This finding represents
one of the most dramatic pieces of evidence for the dynamic nature of the ocean
crust. Equally remarkable is that these hydrothermal systems support an abundant
flora and fauna not ultimately dependent on photosynthesis as an energy source
(Jannasch & Wirsen, 1979; Karl, Wirsen & Jannasch, 1980; Felbeck, Childress &
Somero, 1981). These hydrothermal vents in fact represent one of the major
oceanographic discoveries of recent times. In some cases, sulphide chimneys are
formed at the vents and manganese oxides form crusts a few metres away (Haymon
& Kastner, 1981). Fractional precipitation of manganese and iron can also lead to
the formation of manganese oxide crusts overlying nontronite (an iron-silicate)
(Corliss, Lyle, Dymond & Crane, 1978; Hekinian & Février, 1979; Honnorez et
al., 1981; Varnavas & Cronan, 1981; Barrett & Friedrichsen, 1982).
The belated discovery of these hydrothermal systems reflects the fact that their
occurrence on the ocean floor is extremely localized and searching for them is
highly dependent on chance. This is so even at a known hydrothermal field. At
the TAG field, for instance, only one dredge haul in ten recovered hydrothermal
material (Rona, 1982). About 50 sites of hydrothermal deposits are at present
known at spreading centres along the 50000 km mid-ocean ridge system. This
distribution is thought to be an artifact of the present early stage of exploration
rather than a reflection of their real frequency of occurrence and it has been
estimated that a high intensity hydrothermal vent should occur every 100 km or
so along an intermediate- to fast-spreading mid-ocean ridge (Rona, 1982).
The injection of high concentrations of manganese into overlaying sea water
from these vents is now well established at the Galapagos Rift where
concentrations up to 50 times normal have been reported (Klinkhammer, Bender
& Weiss, 1977; Weiss, 1977; Bolger, Betzer & Gordeev, 1978; Klinkhammer,
1980c; Lupton et al., 1980) as well as on the Juan de Fuca Ridge off the west
coast of the United States (Jones, Johnson & Delaney, 1981). The manganese
concentration in the water column is detectable at a dilution of about 106 with sea
water and can be measured at distances of tens of kilometres from the source
(Rona, 1982). More local volcanic influences on manganese concentrations in
sea water have been noted at Deception Island, Antarctic (Elderfield, 1972b),
Heimaey Island, Iceland (Olafsson, 1975) and Santorini (Smith & Cronan,
1983). High manganese contents in the brines of the central depressions of the
Red Sea have also been recorded (Danielsson, Dryssen & Granéli, 1980). In
these brine systems, manganese-rich sediments are formed around the margins of
the deeps at the contact between the anoxic brines and the. overlying oxic sea water
as might be expected from redox considerations (Bignell, 1978). Manganese is
therefore seen to be a sensitive tracer of the discharge of submarine
hydrothermal fluids at active spreading centres. Other sensitive indicators of this
component are temperature and the He3, CH4, and silica contents of the overlying
bottom waters.
In addition to the effect of hydrothermal fluids on sea-water chemistry,
sediment composition is also affected. Sediments within 100 km of the East
Pacific Rise, for example, have a >80% hydrothermal component (Dymond,
1981) and bottom current winnowing is believed to be the mechanism by which
this hydrothermal component is transferred away from the ridge crest (McMurtry
et al., 1981). The precise mode by which manganese is dispersed from the ridge
crest has been described by Edmond et al. (1982) and Stommel (1982). In spite of
this element enrichment Gundlach & Marchig (1982) and Marchig, Gundlach,
Möller & Schley (1982) have shown the difficulty of discriminating between
metalliferous sediments of hydrothermal origin and pelagic sediments subject to
diagenetic enrichment of transition elements on compositional grounds alone.
Finally, it should be emphasized that, quite apart from the intrinsic interest of
these active hydrothermal systems, study of their mode of formation has led to an
evaluation of the genesis of their fossil analogues as, for example, the Troodos
Massif, Cyprus (Robertson, 1975), the Semail Nappe, Oman (Fleet & Robertson,
1980), the Italian Apennines (Bonatti, Zerbi, Kay & Rydell, 1976) and the Afar
Rift, Ethiopia (Bonatti et al., 1972) where manganese deposits are all found.
In summary, the discovery of metalliferous sediments and later of submarine
hydrothermal vents has not only shown the importance of convective recycling
of sea water through the ocean crust at active mid-ocean ridge systems on the
composition of sea water, marine sediments, and minerals but also led to the
development of a valuable conceptual model for ore exploration on land. It has
also resulted in a probable solution to the source of ‘excess’ manganese in deep-
sea sediments.
CONCLUDING REMARKS
Over the last decade, there has been a huge increase in our knowledge of the
marine geochemistry of manganese, principally as a by-product of the
commercial interest in manganese nodules which began in earnest in the early
1970s but also as a result of the U.S.-based GEOSECS programme to understand
the geochemistry of ocean waters on a worldwide scale in much more detail, the
discovery of hydrothermal vents at the crest of active mid-ocean ridge systems
and the increasingly numerous studies of the distribution and speciation of
manganese in freshwater and coastal marine systems. Of particular importance
has been the improved accuracy of analysis of manganese in natural waters
which has contributed greatly to the understanding of the pathways of this
element in the marine system and the factors controlling its distribution.
182 G.P.GLASBY
Because of its unique characteristics of relatively high abundance in the

lithosphere, variable valency within the limits encountered in the natural
environment and the high scavenging ability of its oxides, manganese is one of
the half dozen most important elements in controlling the geochemistry of the
oceans. This is reflected by the high abundance of manganese nodules on the
ocean floor which are the fourth most abundant marine deposits after alumino-
silicate clays, calcium carbonate, and biogenic silica and which act as a sink for a
number of transition elements. Of particular importance has been the discovery of
submarine hydrothermal vents at active mid-ocean spreading centres. These may
account, in part, for the previously missing ‘excess’ manganese.
ACKNOWLEDGEMENTS
I would like to thank Drs P.N.Froelich and P.G.Brewer for permission to
reproduce diagrams from their papers and Drs C.D.Curtis and S.A. Moorby for
their useful comments on the manuscript.
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HEAVY METALS AND REEF CORALS
L.S.HOWARD and B.E.BROWN
Dove Marine Laboratory, Cullercoats, North Shields, Tyne and
Wear, U.K.
INTRODUCTION
The tropical marine environment is increasingly threatened by heavy metal
pollution from a variety of sources yet little appears to be known of the potential
effects of heavy metals upon coral reefs—an ecosystem which has previously
been cited as particularly vulnerable to man-made pollutants (Johannes, 1975).
Authors discussing the effects of power plant discharges (Neudecker, 1981),
desalination plant effluents (Zieman, 1975), drilling muds (Hudson, Shinn &
Robbin, 1982; Dodge & Szmant-Froelich, in press), and chemical effluents
(Johannes, 1975) on coral reefs all conclude that our knowledge of the toxicity of
heavy metals to corals is strictly limited. Early studies on coral skeletons and the
metal levels that they contained (Harriss & Almy, 1964; Wolf, Chilingar &
Beales, 1967; Veeh & Turekian, 1968; Livingston & Thompson, 1971; St. John,
1973, 1974) mainly focused on the idea that trace elements in corals might
reflect the chemistry of specific water masses and thus regional oceanographic
patterns. It is the aim of the present review to consider this relatively extensive
literature in the light of more recent papers and theoretical considerations, to
speculate, on the basis of current knowledge of the biology of corals, on the
possible incorporation of metals into the coral tissues, and finally to highlight
research areas awaiting further investigation.
SOURCES OF HEAVY METAL POLLUTION IN

TROPICAL ENVIRONMENTS
Mining and dredging operations constitute the most obvious potential threat to
shallow- and deep-water reef communities with activities centred in southeastern
waters, particularly around Thailand, Malaysia and Indonesia (Webb, 1978).
Fifty six large scale mining operations are also reported in the Caribbean
HEAVY METALS.AND CORAL REEFS 193
(Yanchinski, 1981), all discharging effluent, with little regulation, into waters
showing incomplete and slow mixing characteristics. In the Red Sea proposals
are going ahead to exploit the metalliferous sediments of the Atlantis II Deep,
which contain economically important concentrations of zinc, copper, silver,
cadmium, lead, and other sulphides. The extraction of these elements could also
lead to increased metal levels in close proximity to extensive reefs. Although it is
proposed to separate and concentrate the elements 150 km from the shore, the
concentrates (20–30% Zn, 5–6% Cu) will be brought ashore for refining and
transport (Mustaffi & Amann, 1978; Georghiou & Ford, 1981), where transfer
from ship to shore will invariably involve spillage. Mine tailings are to be
discharged below 350 m water depth, and although vertical water movements in
the open Red Sea do not apparently occur, there are indications from nutrient
transport that lateral upwelling currents to the reef-covered coasts exist (Mustaffi
& Amann, 1978).
Associated with mining and dredging operations are smelting processes.
Brown & Holley (1982) found slightly elevated levels of copper and zinc and
relatively high concentrations of tin in the silt fraction of reef sediments near to a
tin smelter at Ko Phuket, Thailand. Analyses of biota from the reef near the
smelter suggested that the major metal burden was in particulate rather than
soluble form.
Offshore drilling operations present another potential source of metal
enrichment since they involve the use of drilling muds which contain a wide
range of chemicals. The muds are discharged into the surrounding sea water
more or less continuously at relatively low levels during drilling and occasionally
in bulk (up to 2000 barrels′ 148 tons) when the muds require renewal or on
termination of drilling activities (Monaghan, McAuliffe & Weiss, 1980;
Thompson, Shinn & Bright, 1980). Other aspects of offshore gas and oilfield
operations may also result in environmental enrichment of trace metals, such as
the presence of platform structures for petroleum production activities which
have been implicated in the input of barium, cadmium, chromium, copper,
manganese, lead, strontium, and zinc to surface sediments (Tillery & Thomas,
1980).
Effluents from desalination plants (Zeitoun, Mandelli, McIlhenny & Reid,
1969) and thermal discharge (Marsh & Doty, 1976; Neudecker, 1981) are a
source of metals in ionic form which may be up to 30–40 times the metal
concentrations of the receiving waters and may be detectable up to 60 m from the
source (Fishelson, 1977). Sewage effluents are a major source of metals in many
chemical forms but assessment of their influence on coral reefs is difficult in
view of the blanketing effects of nutrient enhancement which promotes algal
overgrowth of corals (Marszalek, 1981). Enrichment of carbonate sediments by
terrigenous debris introduces a number of metals into the reef environment
(Friedman, 1968; Brown & Holley, 1982) and the fate of these metals, together
with those originating from smelting activities remains to be fully investigated.
194 L.S.HOWARD AND B.E.BROWN
Fig. 1.—Direct and indirect pathways of metal incorporation into scleractinian corals
UPTAKE OF HEAVY METALS BY CORALS

Several pathways by which heavy metals may be incorporated into corals have
been described (Harriss & Almy, 1964; Livingston & Thompson, 1971; Amiel,
Friedman & Miller, 1973; Barnard, Macintyre & Pierce, 1974; St John, 1974;
Goreau, 1977a, b; Buddemeier, 1978). These may be summarized schematically
as shown in Figure 1.
The above pathways have, for the most part, been identified from studies not
concerned with pollution per se, but in the use of coral skeletons as palaeo-
environmental recorders of the metal composition of sea water. It is intended to
review the findings of these workers with respect to the possible pathways by
which polluting metals may be accumulated by corals. Pollution strictly implies a
deleterious effect on an ecosystem which is usually assessed with respect to the
biota. Detrimental effects of metals on corals would result in impairment of
physiological processes. Metals in the deposited skeleton may be considered as
being detoxified as they are isolated from, and thus unlikely to influence the
living tissue. This is not to say that incorporation of metals into the skeleton may
not lead to structural weakness of the aragonite.
INCORPORATION OF METALS INTO CORAL TISSUES

Unfortunately, studies concerned with the influence of metals on the physiology
of corals are limited (Mitchell & Chet, 1975). Speculation on the ability of corals
to take up metals from various sources must be based upon existing skeletal
studies as, presumably, the metals have been structurally incorporated into the
aragonite matrix having first passed through the living coral tissues. Metals
adsorbed on to aragonite directly from sea water are discussed later (see p. 203).
Soluble metals in sea water probably represent the most obvious and direct route
of metal uptake available to corals, although this pathway may not be the
primary contributing factor to their metal status. The feeding activities of corals
may represent a significant input of metals. Corals may show three principal
feeding mechanisms (Lewis & Price, 1975) one of which is the tentacular
capture of zooplankton. When the food source is exposed to elevated metal
concentrations, then enrichment may occur. Copepod exoskeletons (chitin) have
been shown to accumulate cadmium, cobalt, copper, iron, magnesium,
manganese, nickel, lead, strontium, and zinc (Martin, 1970). Boyland, Rutgers,
Zeitlin & Andrews (1980) cite the concentration of copper and nickel in the
plankton pool as being a primary step in the transport to, and incorporation in,
manganese nodules. Hu (1981) observed the incorporation of mining discharge
particles less than 4 μ m diameter into the faecal pellets of five species of tropical
copepods, although no analyses of copepod tissues were given.
A second method of feeding by corals is the utilization of mucous nets which
trap not only zooplankton but fine particulate material, the mucus and entrained
material being periodically ingested. The third important method of feeding
outlined by Lewis & Price (1975) involves the extrusion of mesenterial filaments
into the surrounding substratum presenting the possibility of metal uptake
directly from contaminated sediments. St John (1974) implies the involvement of
the last two processes and suggests that heavy metal concentrations in colonial
corals are related in part to feeding on bacterial plankton and inorganic matter.
Thus, in areas exposed to elevated soluble and particulate metal concentrations,
there may be enrichment of metals through the food chain. In a personal
communication to Goreau (1977b), Trench comments on the ability of the
zoanthid Palythoa to take up detrital magnetite particles and to incorporate them
into the mesentery indicating that coelenterates can transport small particles
through their tissues and deposit them in structural units. Granules similar to
those responsible for metal detoxification in other invertebrates (Brown, 1982)
are present in the mesenterial filaments of the temperate anthozoan Actinia
equina (Van-Praët, 1977). The granules are associated with flagellar and
vacuolar cells of the endoderm and although the author proposes an excretory
function such a rôle has not been demonstrated.
The presence of zooxanthellae in the tissues of hermatypic corals has been
shown to exert a major influence on the calcium deposition rate as well as
stimulating the coral host’s metabolism through the secretion of organic
materials (Goreau & Goreau, 1960). Zooxanthellae have been described as
directly influencing the skeletal concentrations of metals (strontium and
uranium) through enhancement of calcification rates (Livingston & Thompson,
1971) and Buddemeier, Schneider & Smith (1981) have similarly concluded that
the concentrations of minor and trace alkaline earth elements in coral skeletons
are controlled by a calcification process where the large discrimination factors
observed are perhaps related to activity of zooxanthellae. Zooxanthellae may be
involved in the direct uptake of metals in cases where potentially toxic metals are
metabolically substituted for vitally essential elements such as phosphorus.
Pilson (1974) studied arsenate uptake and reduction by Pocillopora verrucosa
and observed a steady conversion of added arsenate from As V to As III over a
period of 3–6 h. During the reduction, some of the arsenic was converted to the
organic form. It was presumed that coral, zooxanthellae or both were responsible
for the conversion although the effect of bacterial action could not be overlooked.
In areas low in phosphorus, arsenic may exceed the former in concentration. As
the two elements are chemically similar, significant quantities of arsenic may be
absorbed. Benson & Summons (1981) studied arsenic uptake in a number of
invertebrates from the Great Barrier Reef and although they did not include
corals in their survey they found accumulation was greatest in organisms bearing
symbiotic algae, particularly large Tridacna and Hippopus clams. During arsenic
accumulation arsenate is absorbed and methylated to trimethylarsoniumlactate
(non-toxic) and its derivatives. Isolated zooxanthellae have been shown in this
study to be capable of converting arsenic to these compounds. Wainwright (1963)
described one of the functions of zooxanthellae in Pocillopora as providing
chitin precursors during photosynthesis. Should chitin synthesis control the rate
of skeletogenesis in this coral as Wainwright suggests, then skeletal deposition
may be indirectly affected by zooxanthellae influenced by toxic metals.
As well as being implicated in metal uptake the zooxanthellae may be
adversely affected by exposure to metals. In experiments using cultured
dinoflagellates, Gymnodinium splendens suffered a decrease in growth when
exposed to mercuric acetate (Kayser, 1976). Addition of 0–01 mg per litre Hg
decreased the test culture density to nearly 2% of the control within two weeks.
No recovery was observed. Hannan & Patouillet (1972) reported toxicity results
depended upon the composition of test medium used, with toxicity varying
inversely with the concentration of nutrients present. Their observations
suggested that organisms in low nutrient tropical waters may be particularly
sensitive to pollutants which may be metabolically substituted.
It is clear then that possible incorporation of heavy metals by zooxanthellae
and their potentially toxic effects may have a direct influence on the host coral
both in terms of inclusion of metals in the skeleton and possible growth
inhibition.
INCORPORATION OF METALS INTO THE CORAL

SKELETON
Theoretical substitution of calcium by metals in aragonite

The incorporation of some 30 to 40 metals into the skeleton of at least 22
scleractinian genera, including transition elements, rare earths and radioisotopes,
has been documented by several workers (Table I). The possible substitution of
metals for calcium in the aragonite lattice may be predicted from theoretical
considerations. The aragonite crystal structure is not restricted to calcium
carbonate, since it is also found in barium, strontium, and lead carbonates. Many
compounds of the general formula ABO3 crystallize with either calcite or
aragonite structures (Wells, 1945). The tendency to form calcite or aragonite
structures corresponds to a ratio referred to as the “radius ratio” by Pauling (cited
by Wells, 1945) and is the ratio between ionic size of the metal ion (A) and the
size of the complex ion (BO3). The size of the calcium ion, 0·99Å, coincides with
the lower size requirement and thus can form both calcite and aragonite. The
upper size limit is not clearly defined but may be estimated as approximately
1·40Å.
TABLE I
Metals reported in coral skeletons: all metal concentrations are in μ g·g−1 except where
marked* which denotes per cent; N/D, metal analysed but not detected; where more than
one result has been reported for a metal per family the lowest and highest values only are
noted; references: 1, Goreau, 1977a, b; 2, Livingston & Thompson, 1971; 3, St John,
1973, 1974; 4, Amiel, Friedman & Miller, 1973; 5, Schofield & Haskin, 1964; 6, Swart,
1979; 7, Sreekumaran & Gogate, 1972; 8, Harriss & Almy, 1964; 9, Veeh & Turekian,
1968; 10, Brown & Holley, 1982; 11, Polyakov & Krasnov, 1976
Metal Pocillopori Poritidae Faviidae Acroporid Fungiidae Reference
dae ae s
Lithium 1–21 1 2
Sodium 5510 4600– 5670– 4260– 4, 6, 7, 8,
7380 6890 9080 11
Potassium 410 104–448 349–423 136–542 4, 7, 8
Rubidium 0·77 0·87 0·73–0·93 0·90–1·59 7
Magnesiu 1700 1880– 1100– 1000– 1, 4, 6, 7,
m 2950 2760 4000 8
Calcium* 34·1 34·3–37·0 32·6–39·6 31·6–38·2 1, 6, 7
Strontium 0–668 0·71–103 0·64–0·80 0·61–1·10 1, 2, 4, 6,
* 7, 8, 11
Barium 15·0 10·0– 2
250·0
Scandium 0·008– 0·013– 2
0·043 0·015
Metal Pocillopori Poritidae Faviidae Acroporid Fungiidae Reference

dae ae s
Titanium 50·0 50·0 2
Chromium N/D N/D–2·0 N/D–10·0 N/D 2, 7
Manganes N/D N/D–15·0 N/D–5·0 N/D– 2, 7, 8
e 14·67
Iron 0·3–49·5 N/D– N/D– N/D– 1, 2, 3, 7,
210·0 560·0 138·0 8, 10
Cobalt N/D–0·29 N/D–2·0 N/D–0·47 N/D–1·03 0·001– 2, 3, 7, 9
0·002
Nickel N/D–0·40 N/D0–2·0 N/D–1·10 N/D–1·10 2, 3
Copper 0·10–1·17 0·02–7·0 0·08–4·0 0·02–2·76 2, 3, 7, 10
Zinc 0·08–4-90 0·71–4·60 0·80–40·0 0·50–4·0 2, 7, 10
Yttrium 0·124 5
Silver 0·018– 0·024– 0·014 0·022– 9
0·034 0·10 0·065
Cadmium N/D–0·20 N/D–0·20 N/D–0·27 N/D–0·20 3
Antimony 172 237 211 80–258 7
Tellurium 24·2 23·14 16·48 20·58– 7
29·41
Lead 0·04–0·50 0·11–0·60 00·10– 0·05–0·70 2, 3
0·90
Lanthanid N/D–2·70 5
es
Uranium 2·03–2·11 N/D 1·5–3·0 2·82 2·06– 2, 4, 9
2·19
Thus, metal ions smaller than calcium tend to form a calcite structure whereas
ions larger than calcium adopt the aragonite structure. With ions greater than
approximately 1·40Å neither structure is possible. Initially then, the packing
together of ions is largely determined by geometrical considerations, i.e., by their
overall sizes and relative numbers of the different kinds of ions. The electrostatic
requirements of the crystal lattice must also be satisfied and therefore, with
respect to aragonite, monovalent and polyvalent ions cannot be tolerated in other
than low levels and will be discriminated against in favour of divalent ions.
Bearing these factors in mind it is possible to rank metals on their tendency to be
incorporated into the aragonite lattice (Table II).
TABLE II
Comparison of divalent metal ions with calcium with respect to compatibility for
substitution in the aragonite lattice:+indicates that element may be incorporated into the
crystal lattice while others (−) will be discriminated against.
Metal Divalent ionic radius (A) Electronegativity Compatible crystal structure
Magnesium 0·66 1·2 −
Nickel 0·69 1·8 −
Copper 0·72 1·9 −
Iron 0·74 1·8 +
Zinc 0·74 1·6 −
Manganese 0·80 1·5 −
Tin 0·93 1·8 +
Cadmium 0·97 1·7 −
Calcium 0·99 1·0 +
Europium 1·09 1·1 +
Mercury 1·10 1·9 −
Strontium 1·12 1·0 +
Lead 1·20 1·8 −
Barium 1·34 0·9 +
Radium 1·43 0·9 −
Cobalt 1·72 1·8 −
On grounds of size, electronegativity, and preferred crystal structure (i.e.,

basic stereochemical similarity) good substitutes for calcium would appear to be
limited to strontium and europium. Barium and radium are at the upper size limit
and tin does not form a natural carbonate.
How do these basic theoretical considerations compare with the reported
incorporations of metals in corals? There is a tendency for metals to be generally
dispersed throughout skeletal material with little evidence of differential growth
rates influencing the distribution of the minor elements (Harriss & Almy, 1964;
Livingston & Thompson, 1971; St John, 1974). Discrimination, with respect to
calcium uptake from sea water, is shown to varying degrees against copper, iron,
zinc, cadmium, lead, manganese, nickel, scandium, silver, cobalt, magnesium,
lithium, sodium, and potassium (Veeh & Turekian, 1968; Livingston &
Thompson, 1971; St John, 1974). Little or no discrimination has been reported
against strontium, uranium, and barium (Veeh & Turekian, 1968; Livingston &
Thompson, 1971; Goreau, 1977a, b; Amiel, Miller & Friedman, 1973).
Sreekumaran & Gogate (1972) reported similar results but suggested that
strontium was slightly favoured over calcium. Magnesium apparently does not
compete and is easily removed from skeletal material by washing, inferring
adsorption rather than structural incorporation (Goreau, 1977b; Amiel, Friedman
& Miller, 1973). Harriss & Almy (1964) reported that metals tended to be
incorporated in the order of Sr>Mn>Fe>Mg>Na>K.
Uranium is the only metal which appears to be present in concentrations

greater than expected according to the skeletal model. The metal ion has a
valency of +4 or +6 with radii of 0·97Å and 0·80Å, respectively. Uranium,
however, is present in sea water not as the free ion but in complex form (Swart &
Hubbard, 1982) and thus we must presume an alternative method of
incorporation for this metal. A possible explanation for the high levels of
uranium in corals may be found by considering the rôle of organic materials within
the skeleton (described on p. 203); such a theory may be equally applicable to
complexes of metals other than uranium.
In general, the above observations would seem to confirm the principles
outlined here. It would appear that on purely physicochemical considerations,
corals would not be expected to accumulate most metals in their skeletons and so
would be poor indicators of environmental levels. There is, however, a general
concensus that metal concentrations in coral skeletons are indicators of metal
levels in sea water (St John, 1973; Barnard, MacIntyre & Pierce, 1974; Goreau,
1977a; Buddemeier, 1978; Schneider & Smith, 1982). This may not be due to
structural incorporation of metals into the aragonite but to the inclusion of
particulate materials into skeletal cavities. Barnard et al. (1974) highlighted the
importance of included detrital material as an influence on the relative
abundance of trace elements in corals from different areas. A mixture of mineral
fractions was identified which were not embedded in the skeletal carbonate
matrix. The authors suggested that most, if not all, iron, aluminium, and silicon
(along with some alkali and alkaline earths) reported in coral heads were
attributable to detrital alumino-silicates and other detrital materials, rather than to
material incorporated in the skeletal carbonate. Other elements reported as being
associated with the detrital phase are sodium and potassium (Amiel, Friedman &
Miller 1973), iron (Goreau, 1977b), silicon, titanium, and chromium (Livingston
& Thompson, 1971). Levy & Noshkin (1977) described concentrations of some
ξ -emitters in damaged regions and cavities in the coral texture; these areas,
referred to as “hot-spots”, corresponded with years in which atomic tests took
place. Other ξ -emitters were heterogeneously distributed in growth bands. Swart
& Hubbard (1982), experimenting with the uptake of uranium from sea water by
corals, found living material contained a homogeneous distribution of the metal.
Dead skeletons, on the other hand, showed heterogeneities in uranium
distribution which were related to lithothamnoid algal encrustations and
endolithic sponges.
The incorporation of particulates into skeletal material tends to be random and
leads to erratic variations in metal analyses between and within sites as observed
by Goreau (1977a) with respect to iron in Montastrea annularis. Such
incorporation of detritus should not be taken as a foregone conclusion as
undamaged corals have less chance of collecting particulates. Brown & Holley
(1982) did not find incorporation of particulates into samples of Porites,
Acropora, Montipora, and Pocillopora from reefs at Ko Phuket, Thailand, which
are subject to high sedimentation and suggest this may be due to ‘size-specific’
sorting of sediments by the corals or alternatively to the nature of suspended

materials. Furthermore, the samples of Porites were small heads (maximum age
5–6 yr) not suffering from considerable bioerosion and, therefore, had few
cavities. Acropora, Montipora and Pocillopora are all branching corals, a factor
possibly reducing their susceptibility to sedimentation (Hubbard & Pocock, 1972).
Enrichment of metals may also occur through surface adsorption on exposed
areas of dead skeleton. Kitano, Kanamori & Yoshioka (1976) studying the
adsorption of metals on to aragonite from sea water reported that 100% of added
copper and 90% of added zinc were removed from solution. Adsorbed metals were
not removed by washing. The adsorption of uranium and magnesium on the
surface of aragonite is reported by Amiel, Miller & Friedman (1973). St John
(1974) described higher heavy metal concentrations in massive corals (Poritidae
and Faviidae) when compared with the ramose forms (Pocilloporidae and
Acroporidae); he attributed this difference to a greater surface area of carbonate
per unit mass not covered with living coenosarc in massive forms relative to
ramose forms and hence a greater adsorption potential in the former. Thus, heavy
metal abundances in scleractinian carbonates can possibly be related to the form
of the colony under investigation. Referring to the sampling of radionuclides by
corals, Buddemeier (1978) suggests that corals may also function as reliable
samplers for many dissolved materials in the water, yet accepts that the
mechanism for this sampling remains unclear. St John’s observations may offer
one such mechanism.
The interpretation of analyses of metal concentrations in corals, taking into
account detrital inclusions and adsorption, would suggest that relatively few
metals can be incorporated into the structural aragonite matrix. Thus, the
chemical properties of aragonite may give the appearance of an ability by corals
to exclude or regulate the uptake of metals. This interpretation of the data may
incorrectly lead one to the conclusion that metals pose little or no threat to
corals. There are, however, other aspects of metal uptake which need to be
considered and prominent among these is the rôle of organic constituents in the
secretion of the skeleton.
The possible rôle of organic materials in incorporation of

metals into the coral skeleton
Scleractinian aragonites appear to contain organic materials laid down as a
framework on which the calcification process is initiated (Goreau, 1959;
Wainwright, 1963). The organic components have been described as protein
(Young, 1971; Mitterer, 1978) and polysaccharide (Wainright, 1963).
The possible incorporation of metals into the protein matrix may have far-
reaching effects. Due to the low level of organics constituting skeletal material
(0·1–6·0%) high concentrations of metals in this fraction would be swamped by
the low levels in the skeletal mass. There has been a tendency by workers to
ignore the metal contribution of the organic phase. Pre-treatment procedures prior
to digestion and analysis have included removal of soft tissues by washing or

bleaching (Veeh & Turekian, 1968; St John, 1974; Goreau, 1977a) and removal
of lipids by extraction with acetone and ether (Livingston & Thompson, 1971).
Amiel, Miller & Friedman (1973) studying the incorporation of uranium in
modern corals concluded that the metal was partitioned between three sites,
namely, (1), skeletal aragonite, (2) the crystal lattice, and (3) organic
components. Skeletal uranium levels were 0·04–0·06 μ g per g and lattice
inclusions about 3 μ g per g whereas organics contained a relatively massive 40–
70 μ g per g. As the organics were, however, only 0·1% of the total weight of the
corals examined (Diploria and Montastrea) the total concentration was not large.
Brown & Holley (1981) working with corals exposed to tin smelting activities
compared skeleton with attached tissues and skeleton alone and found no
significant difference between metal analyses. Perhaps this is not surprising in
view of the small proportion that the organics contribute to the total weight. St
John (1974) recognized that it was “probable that a certain amount and possible
that a large amount of the trace metals extracted in the present study was
originally bound to organic material rather than the carbonate lattice” in his study
of corals from the Coral Sea.
The metal-binding properties of proteins have been widely discussed and
publicized, recently being reviewed by Roesijadi (1981). Mitterer (1978)
analysed amino acids and assessed the metal-binding capacity of skeletal
proteins of corals after removing the soft tissues. The bulk of amino-acid
residues in five species of coral (three genera) were composed of aspartic acid,
glutamic acid, glycine, and alanine. The total acid residues comprised almost
half the protein. Acid plus neutral residues accounted for approximately 80% of
total amino acids. The potential significance of the free carboxylic acid groups
for binding calcium ions was highlighted. The proteins present were described as
a mixture of different protein fractions rather than a single repeating unit.
Mitterer’s data provided no direct evidence regarding interaction of the
‘calcifying protein’ with metal ions. Experiments showed, however, that the
calcifying protein of the alcyonarian, Eunicea tourneforti, had the ability to bind
terbium ions to a moderate degree. Because of its preponderance in the soluble
fraction and its negative charge, aspartic acid was suggested to be the most likely
protein constituent involved in binding metal ions. Mitterer concluded that the
results supported the concept of an organic matrix acting as a template which
initiated and controlled crystal nucleation and growth either by epitaxial growth
or by a simple concentration of appropriate ions. The resulting abundance of
negative charges distributed along the protein chain provided many sites for the
attachment and orientation of not only positively charged calcium ions but also
presumably, other metals.
Harriss & Almy (1964) suggested that slight generic and specific effects on
distributions of metals may be due to differences in protein matrices which serve
as nuclei for the individual aragonite crystals. Seasonal variations in magnesium
content in Montastrea reported by Goreau (1977a) may reflect seasonal changes
in protein concentrations because Goreau suggests that variations are

physiologically meaningful when the constancy of calcium/ magnesium ratios in
sea water are considered.
While metal-binding properties of proteins are much discussed the fact that
chitin also has considerable metal-binding properties has received relatively little
attention from biologists. Wainwright (1962, 1963) identified and discussed the
function of chitin, a polymer of N-acetyl-ξ -glucosamine, in the organic matrix of
Pocillopora damicornis. He postulated that the amide group of chitin was
responsible for the ability of certain organic substances to be calcified, i.e., the
presence of protein was not necessary. Chitin has subsequently been identified as
being included in the organic matrices of Astrangia and Favia (Wilfert & Peters,
1969), Tubastrea, Herpolitha, Porites, Fungia, Lobophyllia and Turbinaria
(Young, 1971). The chemistry of the metal-binding properties of chitin has been
described by Muzzarelli (1977). Three processes are available to bind metals;
these are ion-exchange, adsorption, and chelation. All three are important in
varying degrees for each metal. For calcium the ion-exchange process
dominates. For transition metals, experimental evidence suggests that the
chelating ability of chitin is important. Thus, the transition metals would tend not
to be available for inclusion in the aragonite lattice. Rates of adsorption of
transition metals on to chitin are related to second ionization potentials. The
tendency of metals to be adsorbed from solution by chitin is
copper>nickel>zinc>cobalt>iron>manganese. The adsorption of metals by chitin
from solutions of mixed metal ions does not follow a stoichiometric path,
suggesting that there may be more than one active site for the different metals on
the surfaces of the polymer.
The presence of chitin in arthropod exoskeletons is invariably associated with
protein in both calcified and non-calcified forms. Free N-acetylglucosamine and
chitin can react with ξ -amino acids to give stable complexes. Chitin in ξ - or ξ -
form is covalently linked to arthropodin and sclerotins to form more or less
stable glycoproteins (stable in hot alkali, unstable in hot acids). Wainwright
(1963) conducted 27 different tests for lipids, proteins, and polysaccharides and
failed to detect any protein associated with chitin in the organic matrix of
Pocillopora. Mitterer (1978), on the other hand, did not analyse for
polysaccharides in addition to proteins in samples of Porites, Oculina, Agaricia
and Acropora. Thus, in the latter study one is left to speculate on the co-
existence of the two materials. Wilfert & Peters (1969) and Young (1971)
surveyed a number of scleractinian genera and found both protein and chitin
together in various proportions. Proteins were reported in all organic matrices
examined whereas chitin was restricted in distribution and abundance. The
differences in organic matrix constitution between genera and species may result
in apparent ‘specificity’ for concentrating certain metals. A case in point is the
concentration of uranium by organics observed by Amiel, Miller & Friedman
(1973) leading to lower discrimination by corals against this element as reported
by Veeh & Turekian (1968) and Livingston & Thompson (1971).
There is a strong possibility, in view of the above comments, that corals

exposed to elevated metal levels may concentrate metals in their skeletal organic
matrices. It is possible that metal incorporation may inhibit or prevent skeletal
deposition by interfering with the regular position of calcium in the aragonite.
This may in turn result in local imperfections in crystal structure rendering the
coral susceptible to physical stress such as storm damage. The incorporation of
heavy metals may be accentuated in the event of increased environmental levels
of metals by the effective further concentrations of these elements in actively
growing areas. Taylor (1977) describes good evidence for active intracolonial
transport of calcium ions and organics to the growing tips of Acropora
cervicornis. Pollutants may also be transported and thus higher net
concentrations may be achieved within areas of growth with respect to
concentrations in the surrounding water. Elevated metal concentrations inhibit
the enzyme chitin synthetase in vitro (Muzzarelli, 1977) and thus may retard
chitin synthesis. Such processes may inhibit growth in those coral species
utilizing chitin as a calcification framework.
EFFECTS OF HEAVY METALS ON THE PHYSIOLOGY

OF CORALS
Literature concerning the effects of heavy metals on the physiology of coral
polyps is strictly limited. Evans (1977) exposed Pocillopora damicornis and
Montipora verrucosa to solutions of copper sulphate in an experimental flow-
through system in Hawaii. Concentrations of 10, 1·0, 0·1, and 0·01 mg per 1
were used; the lowest concentration being reported as slightly above ambient for
coastal waters. At exposures of 0·1 mg per 1 or greater all corals died within 24
h. After 48 h exposure to 0·01 mg per 1 copper, test corals showed symptoms of
“severe stress” with polyps withdrawn and whitened; these were all dead by the
sixth day of exposure. No further data were described as the responses of the
corals to copper formed only part of a larger study. The results quoted above
would imply that the toxic effects of copper may be exerted at concentrations
much lower than 0·01 mg per 1. Mitchell & Chet (1975) studied the effects of
what were described as “low concentrations of chemicals” on coral heads of
Platygyra from the Red Sea. Their use of 100 mg per 1 and 1000 mg per 1 copper
sulphate, however, can hardly qualify as low concentrations and would be better
described as totally unrealistic. Natural oceanic copper concentrations are of the
order of several μ g per 1 or less (Alexander & Corcoran, 1967; Fonselius, 1970;
Danielsson, 1979). Even in areas polluted by copper, concentrations in sea water
rarely exceed 1 or 2 mg per 1 (Zeitoun et al. 1969). Due to the low solubility of
non-complexed metals in sea water the actual concentration to which Platygyra
was exposed during the experiment must be questioned. Mitchell & Chet (1975)
inferred that the massive production of mucus which resulted in response to 100
mg per 1 CuSO4 prevented the metal from entering the tissues. This was
“confirmed” by exposing the corals to 1000 mg per 1 CuSO4 which also resulted
in massive production of mucus. Associated with increased production of mucus

was an increase in bacterial numbers which the authors found surprising in view
of the bacteriocidal nature of copper sulphate. It was inferred that the mucus also
coated, and therefore protected, the bacteria. None the less, a response to the
addition of copper ion, recognized as the toxic form of copper (Steemann Nielsen
& Wium-Andersen, 1970) was to produce copious quantities of mucus (48 times
the control) which must have required considerable expenditure in terms of
energy. Prolonged production of mucus upon exposure to soluble metal ions may
result in an energy drain on the coral which exceeds it metabolic capabilities.
Production of mucus as a ‘stress’ response has been described for Porites
divaricata, P. furcata, P. astreoides, Montastrea annularis, Acropora
cervicornis, and Agaricia agaricites following exposure to a chrome
lignosulphate (FCLS) drilling mud (Thompson, Shinn & Bright, 1980). The
concentration of FCLS in the test mud was not known. Krone & Biggs (1980)
investigated the sub-lethal response of Madracis mirabilis to FCLS, which is
added to drill muds to control filtration and flow properties (Monaghan,
McAuliffe & Weiss, 1980), by exposing the coral to a mixture of 100 mg per 1
drill mud and 3 mg per 1 FCLS. Test corals were not statistically different from
controls with respect to respiratory rate yet excreted a significantly greater
amount of ammonia. Other observations made on FCLS stressed corals were (1)
a smaller number of polyps expanded, (2) extrusion of zooxanthellae, and (3)
bacterial infections with subsequent algal overgrowth. When removed from
FCLS exposure, corals recovered quickly and were normally expanded and
feeding within 48 h. Thompson (1977) and Thompson & Bright (1980) carried
out experiments on Madracis and found that the coral could survive 29 days
continuous exposure to 100 mg per 1 drill mud whereas coral exposed to 10 mg
per 1 FCLS showed curtailed polyp expansion. Corals exposed to 100 mg per 1
FCLS died within five days. Dilution rates of drill muds on discharge to the sea
have been reported as between 103 and 104 within 100 m downstream of the point
of discharge (Thompson et al., 1980; Monaghan et al., 1980) and maximum
dilution may occur within 6 m of source (Shinn, Hudson & Lee, 1980). Drill
muds vary considerably in their make-up, FCLS concentrations being anywhere
between 24 to 6,675 mg per 1 (Monaghan et al., 1980) which after dilution
would represent up to 6 mg per 1 FCLS within 100 m of discharge. The
investigations by Thompson (1977) and Thompson & Bright (1980) may
represent the extreme acute exposure situation during bulk dumping of drilling
mud whereas the concentrations used by Krone & Biggs (1980) are perhaps more
representative of normal drilling operational levels. It must be borne in mind that
most of the FCLS is adsorbed on to clay particles in the drilling mud but may be
desorbed on dilution with sea water. Data on long term chronic effects of FCLS
are lacking but it may be implicated in the decreased growth rates of Montastrea
annularis resulting from short-term exposure to FCLS drilling mud (Hudson &
Robbin, 1980). Trace element analysis suggested that neither barium (present in
large quantities as sulphate in drilling muds) nor chromium were incorporated
into coral skeletal material and the authors concluded that the reasons for the
observed reduction in growth rate were not really known. In recent work, Dodge
(1982) exposed Montastrea annularis for six weeks to suspensions of drilling
mud in a flow-through system and observed an impairment of growth rate at 100
mg per 1 ‘used’ mud. Lower calical relief was found in exposed corals when
compared with controls and it was suggested that this may result in a decreased
sediment-shedding capability which may remain effective for some time after the
period of exposure. The mud constituent(s) causing the reduction in growth was
not identified. Investigating the effects of offshore oil drilling in the Philippines,
Hudson, Shinn & Robbin (1982) reported the appearance of a rusty brown stain
covering rocky surfaces and sediments in the discharge zone closely
approximating the area of reduced coral cover. Hudson et al. (1982) inferred that
the staining probably originated as pipe scale but point out that it is not known
whether oxidized iron is sufficiently toxic to be lethal to corals or to inhibit their
growth. Dodge & Szmant-Froelich (in press) comprehensively review the effects
of drilling fluids on reef corals, and conclude that more research is urgently
required on the toxicity of drilling muds and their effects on corals.
CONCLUSIONS
It can be appreciated from the foregoing that our knowledge concerning the
effects of heavy metals on coral physiology is very poor. With the continuing
growth of industry and the exploitation of natural resources the encroachment on
nearshore coral reefs continues. If the impact of man’s activities is to be
minimized, efforts must be made to increase our understanding of the
susceptibility of corals to metal pollution from physiological and skeletal
considerations such that biological and physical implications may be identified.
The recurring use of conjecture and speculation in the text more than adequately
illustrate the current awareness of this aspect of coral biology. Studies
concerning the effects of realistically elevated metal concentrations on aspects of
coral physiology (e.g., incorporation into organic skeletal components;
production of mucus), behaviour (e.g., feeding response), and reproduction (e.g.,
planulation and settlement) are needed to form a basis from which to minimize
the ecological impact of metallic discharge to the tropical marine environment.
ACKNOWLEDGEMENTS
We acknowledge the co-operation of numerous investigators who gave us access
to manuscripts in press and in preparation and also the assistance of the librarians
at the Marine Biological Association, Plymouth. The work was carried out while
one of us (L.S.H.) held a Natural Environment Research Council Studentship.
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ECOLOGICAL ENERGETICS FROM
TOTAL LIPID AND TOTAL PROTEIN:
FACT AND ARTIFACT USING A
GRAVIMETRIC METHOD FOR LIPID AND
A BIURET METHOD FOR PROTEIN
C.C.E.HOPKINS, J.V.SEIRING, O.NYHOLMEN
Aquatic Biology Group, Institute of Biology and Geology,
University of Tromsø, P.O. Box 3085 Guleng, 9001 Tromsø,
Norway
and
A.HERMANNSEN
INTRODUCTION
Institute of Fisheries, University of Tromsø, P.O. Box 3083 Guleng,
9001 Tromsø, Norway
The last decade or two have seen much progress in the transformation of marine
ecology from an essentially descriptive discipline towards one of ever increasing
quantification. In many cases the ultimate aim seems to be the building of
various forms of mathematical model, be they at one extreme wholly empirical
or at the other wholly rational, or either deterministic or stochastic (Platt, Mann
& Ulanowicz, 1982). No matter what type of quantitative investigation, the
general goal ought to be to produce results that, as far as possible, are identical with
those in the natural system that one is attempting to mimic. Any deviation from
the absolute will either be the result of poor raw data inadequately describing the
state of an individual or population, or a poor model for treating the data, or a
combination of both. Whatever the cause of deviation from the absolute, it has to
be accepted that even the most intricate model is only as good as the data upon
which it is built. Unfortunately, there appears to be a general tendency to be less
occupied by sources of error in the raw data than in the way in which the data is
subsequently treated.
Studies of ecological energetics and the construction of energy budgets are
one particular field of marine ecology which has advanced greatly in recent years
(see Conover, 1978, for a review). In many cases the reproducibility of the
results is, however, essentially unknown. There is a pressing need for
quantification and objectivity regarding the quality of raw data collected; this
especially applies to ecological energetics, where the objective is the rational
comparison of individuals, populations, and communities from different
localities. There is a pressing need for a quantitative standardization of analytical
techniques, such that investigations conducted by different scientists are directly
ECOLOGICAL ENERGETICS FROM LIPID AND PROTEIN 211
comparable. Many of the analytical techniques used as daily tools of the trade in
ecological energetics have many sources of variation, and many are put forward
and used as if they produced more or less infallible data. It is of vital importance
to be aware that biological material differs with regard to consistence and
composition from species to species such that analytical techniques often need to
be modified in order to obtain dependable data.
The analytical techniques that are applied in today’s ecological energetics are
legion and we will make no attempt to go through the many sources of error that
can be met in applying each and all. We will examine the technique of Folch,
Lees & Sloane Stanley (1957) for determining total lipid, and the biuret
technique of Gornal, Bardawill & David (1949) for determining total protein. We
do not attain to describe or quantify all possible sources of error; we hope to draw
attention to the limitations of the techniques and to pinpoint some of the more
obvious pitfalls of which many of the participants are unaware. Many of the points
we bring to light in this article are relatively well known to lipid and protein
biochemists. What is perhaps unusual is that we have concentrated on providing
numerical evidence, supported by statistics, to document them. Although of
interest to the biochemist, our article is primarily aimed at the growing multitude
of marine biologists and ecologists who apply these techniques routinely in their
research. Many of these techniques used in studies of ecological energetics did
not have their origin in the biological sciences nor were they originally used to
collect the type of data that they are used for now. In this paper we essentially
ask “What are we really measuring?” and “How can we compensate for errors?”
Although we have concentrated on the methods of Gornall et al. (1949) and
Folch et al. (1957) for determining total protein and total lipid, respectively, the
same basic considerations and questions can be posed, for example, for the
Lowry, Rosebrough, Farr & Randall (1951), Kjeldahl (Bradstreet, 1965), and
Dorsey, McDonald & Roels (1977) methods for determining total protein, as
well as the methods of Bligh & Dyer (1959) (see also Hansen & Olley, 1963)
Soxhlet (Augustinsson, 1966), and Barnes & Blackstock (1973) for determining
total lipid. Many of these techniques in their original descriptions were certainly
not considered for use in the sphere of marine ecology, where they are now often
used on whole organisms with varying types of exoskeleton, which in numerous
cases contain large quantities of resistant inorganic material. Most of these
techniques originate from the medical and biomedical laboratories where
mammalian tissues are the most common material used, and where the
composition of the protein and lipids tend to be less diverse than in marine
organisms.
We can draw attention to a large proportion of the more obvious artifacts
arising when using the techniques of Gornall et al. (1949) and Folch et al.
(1957). Our tests have been performed on whole prawns of the species Pandalus
borealis, which represent material of about average lipid content (Båmstedt,
1974; Seiring & Hopkins, in press), and on the swimming muscle of capelin,
Mallotus villosus, which represents relatively lipid-rich material (Jangaard,
1974). Specific aspects of the sources of error in applying the basic methods
without modification or compensation for over- or under estimates will be taken
212 C.C.E.HOPKINS ET AL.
up when they are encountered. The techniques of Folch et al. (1957) and Gornall
et al. (1949) have one particular virtue, in that they can be combined without too
much difficulty to determine lipid and protein from the same sample, thus
reducing the amount of tissue required and the number of analyses needed. The
combination of the two methods is sketched in Figure 1.
No matter to what end data on protein and lipid content are to be used, it is
important that the wet weight or dry weight of the material to be analysed is
measured accurately. It is often a simple matter to take both these weights as this
opens the way to very much more information about the animal or tissue
concerned. Although Childress (1977) has made a strong case for presenting
biochemical data as weight or proportions per unit of wet body weight, it should
not be overlooked that ′ 80% of wet weight is water and that this will tend to
‘blur’ the sensitivity to decipher or follow accurate changes in the variables
studied (Hopkins et al., in press). A special pitfall is present in the ability of one
unit weight of fatty acid on oxidation to produce slightly more than the
equivalent weight of water (Sargent, 1976), such that wet body weight may well
increase while the total organic reserves of the body, in lipid-rich organisms,
probably will have decreased. This phenomenon is particularly well documented
in fish (Love, 1970). In addition, there is much evidence to show that the
precision of weighing dry weight as opposed to wet weight is higher (Lovegrove,
1966). Further discussions of the variability in wet and dry weights are to be
found in Hopkins et al. (in press).
The manner in which dry weight is determined plays an important rôle in
determining which fatty acids and amino acids one ends up with in one’s material
(Morris & Culkin, 1976; Christie, 1982). In many cases the biologist/ecologist
may only be interested in determining total lipid or total protein; none the less,
oxidation of fatty acids at higher temperatures and on lack of speedy freezing of
samples is a factor which can well modify the total weight of lipid recorded and,
indeed, the lipid class composition. It is not the intention of this review to
summarize recent advances in the field of lipid chemistry as these are well
described in the works of Morris & Culkin (1976) and Christie (1982). These
authors, however, draw attention to the fact that methods of preservation can
significantly influence lipid composition. Ineffective freezers can result in
significant increases in the free fatty acid content due to hydrolysis of some
phospholipids, and the possibility exists that storage at−15°C for even three
months can decrease the triglyceride content of fish muscle by as much as 50%
(El-Bastavizi & Smirnova, 1970). A condensation of the wealth of literature in this
area points to a number of safeguards that ought to be taken at the onset.
1. As little time as possible should have elapsed after the organisms have
been collected and they are put in the deep-freeze.
2. Animals or samples should preferably be kept in low temperature
deep-freezers (−20°C or colder) if biochemical determinations cannot be
carried out within about three to four months. Storage of fresh, wet material,
and indeed dried material, is enhanced by keeping under an atmosphere of

nitrogen. Keeping samples in liquid nitrogen (−196°C) is close to ideal.
Implementation of this latter point even with normal temperature-range
deep-freezers appears to enhance the preservation of samples for periods of
at least 9 months.
3. Drying of wet material to obtain accurate dry weights and yet
maintain well preserved samples for detailed lipid analyses is difficult to
achieve. Accurate dry weights are obtained when drying results in stable
weights. This is often achieved by either increasing the time of drying
using relatively passive methods, such as self-indicating silica gel in a
desiccator, or alternatively by increasing the speed of drying through active
methods. The use of freeze drying (lyophilisation) ought to be encouraged;
this is standard practice in many biochemical procedures, e.g. protein
purification. It should not be overlooked, however, that freeze drying may
alter the solubility of macromolecules. Active methods involving
temperatures above 50°C are not to be recommended as oxidation
problems are increased drastically. Small sized samples can be dried
quickly at 50°C owing to surface area:volume considerations. Although
desiccator drying often can increase drying times, replacing the air with an
atmosphere of nitrogen will inhibit oxidation problems greatly. Even faster
desiccator drying can be achieved by passing a slow stream of nitrogen
through the desiccator.
It is becoming more and more accepted that determinations of several variables

from the same material is desirable. The only way to be sure that the subsamples
analysed are identical is to take them from homogenized material. It needs
emphasizing here that homogenization of fresh material releases tissue hydrolases
(lysosomal) and also ensures even mixing of substrates with hydrolases, e.g. the
mixing of gut hydrolases with internal tissue substrates. Thus it is essential to
homogenize at temperatures not exceeding 0–2°C when using aqueous media.
Addition of chloroform-methanol, for example, should be proceeded with as fast
as possible. Well dried material generally causes little problems for modern
homogenizers or even pestles and mortars. On the other hand lipid-rich material
may on homogenization become two “phased”; homogenized “dry” material with
a high proportion of lipid on the one hand, and fluid, dripping lipid on the other.
Taking true replicate samples from such material is not easy. Some of the
problems with such material crop up time and again during the analytical
procedure, as will be seen later.
Fig. 1.—Flow chart showing the main analytical steps involved in the methods of Folch et
al. (1957) and Gornall et al. (1949) for determining total lipid and total protein.
THE BASIC METHODS
DETERMINATION OF TOTAL PROTEIN AND LIPID

The requirement for performing determinations of both total protein as well as
total lipid from the same tissue or material, mainly inaugurated on zooplankton
where large amounts of tissue are not available for independent analyses, led to
the methods of Gornall et al. (1949) and Folch et al. (1957) often being used in
combination. A sketch of the salient steps involved in this combined method,
modified after Båmstedt (1974) is shown in Figure 1. The biuret reagent is made
from a water-soluble solution of 0·15% CuSO4·5H2O, 3·6% NaOH, and 0·6%
C4H4O6KNa·4H2O (potassium-sodium tartrate). The blank is made from 1 N

NaOH+biuret reagent, in the proportion of 1:4.
When performed on its own without the influence of the effects of lipid-
extracting solvents the biuret method of Gornall et al. (1949) is normally
initiated at stage 4 in Figure 1, with points 1–4 being excluded. Some workers
(e.g. Båmstedt, 1974) when carrying out determinations of total protein, but not
total lipid on a given material, first remove any lipid present. This is presumably
done to remove any possible interference effects of lipid on protein extinction
measured spectrophotometrically. Lipid can be affected by the turbidity of the
final solution. The gravimetric determination of total lipid both performed on its
own as well as independently of determinations of total protein generally
involves stages 1–3 followed by stages 9–12 in Figure 1.
CONSTRUCTION OF THE PROTEIN STANDARD CURVE

Determination of protein by the biuret method is dependent on comparing the
extinction of the material to be analysed against a known standard curve of
bovine serum albumin (B.S.A.). It goes without saying that the accuracy of the
data used in constructing the standard curve plays an important part in estimating
protein levels from extinction data. It thus pays to spend time in obtaining a good
standard curve. B.S.A. is used as the standard source of protein. Later we shall
see that the protein we have in our material often has characteristics far removed
from pure, semi-transparnet B.S.A. The protein standard curve is based on
measuring the optical density (extinction) at 550 nm in the spectrophotometer. A
standard curve for B.S.A. is shown in Figure 2. In this case we have used a
quartz crystal cuvette as these are more resistant to scratching than the more
normally used glass cuvettes. Extinction read from quartz cuvettes and glass
cuvettes with identical quantities of B.S.A. will obviously not be similar. In any
work with cuvettes and optical extinction it is vitally important to check for the
presence of new scratches in the cuvettes and to compensate automatically for
these by applying cuvette constants. Use of the same or matched cuvettes
throughout a particular study is expedient. High standards of cleanliness in
handling cuvettes provide better quality results.
The biuret reaction measures reaction of Cu2+ with peptide links (—CONH—)
in alkaline solution. All protein in solution should, theoretically, react essentially
similarly on an equal weight basis. This does not, however, detract from the
likelihood that handling and treatment procedures prior to performing the biuret
reaction may affect results, e.g. possible losses incurred in the aqueous phase of
chloroform-methanol (C-M) extraction for lipid (Folch et al., 1957). It is
pertinent to note here that the often used Folin-Ciocalteu method of protein
determination (Lowry et al., 1951) is essentially a combination of a biuret
reaction and reaction of tyrosine and tryptophan in a separate reaction. The latter
reaction will depend on the protein in question, specifically on the tyrosine and
tryptophan content of the protein.
Fig. 2.—Protein standard curve based on three sets of determinations: extinction at 550
nm as a function of bovine serum albumin loadings; 95% confidence limits and the best-
fit regression are indicated.
The relationship between optical extinction and protein concentration is

expected to be linear. Problems with non-linearity become prevalent with high
concentrations of protein; saturation effects result in unexpectedly low optical
extinction levels. This is seen in Figure 2 for B.S.A. concentrations of >20 mg.
Problems of non-linearity can also exist at low concentrations of B.S.A.
(′ <2mg). The well-known tendency for relatively greater inaccuracy to be
present when weighing small samples suggests that these parts of the standard
curve should be avoided. Likewise, one should avoid working on the upper range
of a calibration graph when signs of non-linearity are seen; it is unreliable and only
a matter of time before errors occur. This will play an important part in
determining the optimal weight-range of samples that ought to be chosen to
maintain high accuracy. The best-fit linear regression equation estimating optical
extinction as a function of protein concentration is of the type , where
Y is the estimated extinction at 550 nm, and X is the amount of protein (as bovine
serum albumin units) per sample. Knowing the values of the constants a and b it
is simple to estimate protein from optical extinction values read off from the
material whose protein content we wish to determine. Regression analyses are a
standard part of many statistical computing packages such as Statistical Package
for the Social Sciences (SPSS) and Biomedical Computer Programs (BMDP),
making it easy to test the quality of our regressions.
STATISTICAL METHODS
The methods of analysis used for determinations of total lipid and total protein
follow those outlined in Figure 1. Where modifications or changes have been
made these are named in the specific materials and methods sections in the text.
In most cases data are presented as total lipid and/or total lipid as percentages of
dry weight. Presentation of data for basic biochemical composition as
percentages can present dangerous pitfalls for the unwary, generally because
“percentage only represents the partitioning of materials within the 100% entity,
not the absolute amount of a material present” (Childress, 1977). The crux of the
danger with percentages is, expressed in simple English, that normally when one
dominant component increases in absolute weight terms the other components
often show a percentage decrease, even though their absolute weight levels may
in fact have remained constant or even increased slightly. Childress (1977) cites
a number of instances of confusion surrounding use of percentages when
working in terms of per cent dry body weight. We have none the less used
percentages related to dry body weight in this article in order to reduce the
variability due to the subjectivity of arriving at accurate wet weight
determinations. The problems highlighted in interpreting percentages regarding
changes in proportional and absolute composition (Childress, 1977), however,
are not pertinent to our data. Our goal is simply to examine the degree of
homogeneity of sample means resulting from applying different methodology to
identical biological material. As far as possible tests were performed using the
same batches of reagents. Frequent calibrations, however, were made to reduce or
eliminate possible variations when different batches had to be used.
It is known from statistical theory that percentages or proportions form a
binomial, rather than a normal, distribution, the deviation from normality being
great for small or large percentages (0 to 30% and 70 to 100%). In cases where
small and large percentages were involved arcsine transformations have been
made such that the resultant data have an underlying distribution that is nearly
normal (Zar, 1974).
Tests of statistical significance have been carried out, where applicable, using
one way or two way analysis of variance (ANOVA), with the null hypothesis
(H0) that there is homogeneity of sample means. Statistics were performed using
either Minitab (Ryan, Joiner & Ryan, 1976) or BMDP (Dixon & Brown, 1979)
computer programs.
GLOSSARY OF MATHEMATICAL AND STATISTICAL

SYMBOLS
Probability levels are quoted in the text and various tables using a system of
asterisks as follows:
* = significant difference at 5% level, 0·05>P>0·01

** = significant difference at 1% level, 0·01>P>0·001
*** = significant difference at 0·1% level, P<0·001
– = no significant difference
Other symbols used are:
= sample mean
s = sample standard deviation
n = number of replicates
CV = coefficient of variation (%)
d.f. = degrees of freedom
F = variance ratio
SS = sum of squares
MS = mean squares
H0 = null hypothesis
SIMPLE TESTS WITH HOMOGENIZED PANDALUS

BOREALIS
HOW MUCH MATERIAL TO ANALYSE?

One may over-simplistically answer this by saying that this depends on how
much material we have available. Even given the potential weight range of
samples (hereafter referred to as “sample-loading”) described in the methods of
Gornall et al. (1949) and Folch et al. (1957), we should, however, bear in mind
that random use of varying sample-loadings during the course of a series of
analyses may in itself be a major source of error. We considered it necessary to
find out just how varying quantities of homogenized material (sample-loadings)
influenced the amount of protein and lipid recorded, and how the reproducibility
of the results so obtained was affected.
Methods
A large quantity of dried homogenized P. borealis was obtained from several
prawns. Sample-loadings ranging from 15 to 30 mg, in 5 mg steps, were used for
determinations of total protein and total lipid using the steps outlined in Figure 1.
Ten replicates were used for each sample-loading for both protein and lipid.
Results
The results of the total protein and total lipid determinations are shown in
Table I. The results of treating the data obtained for both protein and lipid to a
one way analysis of variance (one way ANOVA) are shown in Table II. The per
cent lipid extracted shows a general tendency to decrease with
TABLE I
Dried, homogenized Pandalus borealis: lipid and protein, as per cent dry weight recorded
as a function of varying sample-loadings; in this and subsequent Tables see text p. 218 for
symbols.
Sample—loading (mg)
15 20 25 30 35 40 45 50
Protein
40·62 42·70 41·68 42·88 42·17 41·65 39·82 38·06
s 1·33 0·67 0·92 0·25 0·72 0·40 0·42 0·27
CV 3·27 1·57 2·21 0·58 1·71 0·96 1·05 0·71
n 10 10 9 9 10 10 10 10
Lipid
18·98 16·33 16·25 15·84 15·38 15·91 14·69 13·86
s 2·09 1·31 1·41 0·95 1·32 1·05 0·74 0·53
CV 11·01 8·02 8·68 6·00 8·58 6·60 5·04 3·82
n 9 10 10 10 10 9 10 10
increasing sample-loading. On the other hand, there is also a trend for the
coefficient of variation (CV) to decrease with increasing sample weight,
indicating that reproducibility of the results improves. The results of a one way
ANOVA using all the available data show that sample-loading has a highly
significant influence on the per cent lipid
recorded.
Results of running the ANOVA with all possible sample weight combinations
against each other clearly show that there is no significant difference in the lipid
recorded as proportion of dry weight for sample weights of 20 to 40 mg,
inclusive. The 15-mg sample, however, gave significantly higher
TABLE II
One way ANOVA based on raw data incorporated in Table I: the numbers in parentheses
refer to F-values (variance ratio); the others refer to degrees of freedom d.f1 and d.f.2; no
differences between the means for the respective sample-loadings; absence of an asterisk
indicates that H0 cannot be rejected at P=0·05
Sample 20 25 30 35 40 45 50
loading (mg)
Protein 1,18*** 1,17 1,17*** 1,18** 1,18* 1,18 1,18***
15 (19–68) (3–99) (25·25) (10·61) (5·58) (3·25) (35·74)
1,17* 1,17 1,18 1,18*** 1,18** 1,18***
20 (7·64) (0.58) (2·98) (18·10) (132·80) (415·27)
1,16** 1,17 1,17 1,17*** 1,17***
25 (14·02) (1·66) (0·01) (33·14) (140·20)
1,17* 1,17*** 1,17*** 1,17***
30 (7·80) (62·33) (358·86) (1614·4)
Sample 20 25 30 35 40 45 50
loading (mg)
1,18 1,18*** 1,18***
35 (3·98) (79·22) (285·81)
1,18*** 1,18***
40 (99·06) (553·53)
1,18***
45 (124·85)
Lipid 1,17** 1,17** 1,17*** 1,17** 1,16*** 1,17*** 1,17***
15 (11·20) (11·36) (18·46) (20·69) (15·52) (37·19) (56·38)
1,18 1,18 1,18 1,17 1,18** 1,18***
20 (0·02) (0.95) (2·67) (0·61) (12·01) (30·81)
1,18 1,18 1, 17 1,18** 1,18***
25 (0·60) (2·06) (0.36) (9·66) (25·29)
1,18 1,17 1,18* 1,18***
30 (0·80) (0·02) (9·04) (32·85)
1,17 1,18 1,18*
35 (0·92) (2·07) (11·37)
1,17* 1,17***
40 (8·63) (29·53)
1,18*
45 (8·17)
lipid percentages while sample-loadings of >45 mg gave lower lipid proportions

with some sign of a trend for decreasing lipid proportions with increasing
sample-loadings.
A combined one way ANOVA involving all the available protein data again
showed that sample-loading has a highly significant
influence on the per cent protein recorded. The trend for
protein with varying sample-loading is not so clear as for lipid. The one way
ANOVA for per cent protein recorded with the various sample-loadings
indicates that it is mainly loadings of 15 mg and >45 mg which are most
different from the others.
Discussion
Sample-loadings of 45 and 50 mg show markedly decreased protein percentages.
This appears to originate from two main factors which are difficult to separate
and quantify. First, it either appears that one has entered the area of the protein
extinction curve where saturation of the biuret reagent with this particular
material occurs earlier than with pure B.S.A. (i.e. ′ 18 mg of Pandalus protein, cf.
with >20 mg pure bovine serum albumin in Fig. 2) or, secondly, that the protein
in our homogenized Pandalus material is less available for extraction and
recording than the pure B.S.A. form. Lipid extraction is known to be influenced
by optimal tissue to solvent ratios (Folch & Lees, 1951). Whatever the reasons
for these discrepancies we can see that sample-loading plays an important part in
determining exactly how much protein and lipid is recorded.
The range of values can be highlighted by the fact that for 15 mg loadings the
sum of protein and lipid accounts for 59·6% of dry sample weight while a
loading of 50 mg gives a combined value of 51·9%. Given a normal adult P.
borealis of 2·5 g dry weight it is a simple matter to demonstrate how the
energetic content of the individual, based on conversion constants for protein and
lipid, can be incorrectly estimated with loadings of 15 mg or 50 mg in our
protein and lipid determinations. With 15-mg loadings we reckon that 1·016 g
are protein and 0·475 g are lipid, while using 50-mg loadings we reckon that
0·952 g are protein and 0·347 g are lipid. Using energy values of 5·65 kcal·g−1
forprotein and 9·45 kcal·g−1 for lipid (Mitchell, 1946) we obtain a value of 10·23
kcal·individual−1 using 15-mg loadings and 8·66 kcal·individual−1 using 50-mg
loadings. The difference in the two estimates provides an energetics discrepancy
of 18·2%. One really cannot afford to overlook such uncertainties in any energy
budget. The errors can in fact be greater or smaller depending on the composition
of the individual to be analysed, i.e. lipid-poor or lipid-rich. We shall come back
to this later when we examine the relatively lipid-rich capelin.
EFFECTS OF DIFFERENT TREATMENT ON TOTAL

PROTEIN RECORDED
Another point highlighted in these early tests using dried homogenates from whole
Pandalus is the effect of different methods of treatment of the protein fraction
(point 4, Fig. 1.) after addition of NaOH (point 5, Fig. 1). Addition of NaOH to
the dried protein fraction in the test-tube often results in the formation of a ‘cake’
of material in the bottom of the test-tube which appears not to dissolve well. This
situation possibly affects the breakdown of protein into peptide chains.
Methods
We have set up three situations regarding the degree of mixing of the contents of
the test-tube at this stage; (a) no mixing at all, (b) stirring of the contents with a
glass-rod, and (c) shaking the test-tube and its contents with an electrical test-
tube vibrator (“Whirlimixer”, Fisons Scientific Apparatus Ltd). Tests were
performed with sample-loadings of 25 mg and 40 mg. Nine replicates were used
in each instance, where all the material was taken from a large mass of dried,
finely homogenized Pandalus.
Results
The results of these tests together with a two way ANOVA testing the effect of
type of treatment (mixing) and sample-loading against each other are shown in
Table III. The ANOVA table, using all available data, shows that
TABLE III
Dried, homogenized Pandalus borealis: the results of different treatment (electrical
vibration, stirring with glass-rod, and no form of treatment) on per cent protein recovered
(using 25 mg and 40 mg sample-loading) and two way ANOVA on the basic data; see text
for symbols
Electrical vibration Glass-rod No treatment
25 mg 40 mg 25 mg 40 mg 25 mg 40 mg
42·88 41·40 42·68 41·17 41·68 41·65
s 1·11 0·38 0·69 0·44 0·92 0·42
CV 2·58 0·92 1·62 1·07 2·22 1·02
n 9 9 9 9 9 9
Two way ANOVA
Type of variation d.f. SS MS F

Sub-group 5 22·1327 4·4265
A (treatment) 2 2·0694 1·0347 2·0237
B (sample-loading) 1 13·7108 13·7108 26·8155***
A×B interaction 2 6·3525 3·1763 6·2122**
Error 48 24·54 0·5113
Total 53 46·6727
there is no significant difference between the type of treatment used

but that the effect of varying sample-loadings is highly significant
. There is, interestingly, a significant interaction between ‘treatment’ and sample-
loading.
Discussion
In short, the data show that ‘treatment’ does not play an important part in
affecting the results obtained, so long as one does not use variable sample-
loadings (interaction sample-loading×‘treatment’: F=6·212*) during analyses. It
is worth noting that, once having decided on a fixed sample-loading when
following the procedure for total protein determination outlined in Figure 1, there
is no point in carrying out any time consuming ‘treatment’. It should, however,
be self-evident that chemical reactions are subject to adequate mixing of
reagents, such that this requirement has to be satisfied. The results of these tests
apply specifically to P. borealis—later tests with capelin material provide some

further points for consideration.
HOW MANY WASHINGS WITH CHLOROFORM-

METHANOL?
Folch et al. (1957) in their description of the gravimetric method for determining
total lipid, recommended a weight ratio of at least 20:1 between
chloroform:methanol (C-M) and the homogenate. In our analyses we normally
used 9 ml of C-M with sample-loadings up to 50 mg, a situation which
more than meets the minimum requirements of 20:1. It is worthwhile finding out
whether so many washings with C-M are really necessary. Eliminating some of
the washings would certainly save some time and effort. We also examine the
effect of using varying amounts of C-M on the amounts of
protein and lipid recorded.
Methods
Three sets, each of 10 replicates of 30 mg of dried, homogenized P. borealis
were used. ml of C-M were added to the first set, ml of C-M to
the second set, and ml of C-M to the third set. Determinations of total
protein and total lipid were otherwise carried out following the procedures in
Figure 1.
Results
The results of this test are shown in Table IV. One way ANOVA tests performed
on the data show that there is a highly significant
decrease in the per cent protein (also real in terms of absolute amounts) between
the first and second washings (extractions) with C-M, while there is no
significant change between the second and third
washings. Lipid, although showing a highly significant
increase between the first and second washings
with C-M, continues to show a significant (but here only
) increase, in contrast to protein, between the second
and third washings.
TABLE IV
Dried, homogenized Pandalus borealis: the influence of varying amounts of chloroform:
methanol on protein and lipid, as per cent dry weight, recorded; 30-mg sample-loading
Chloroform: 1×3 ml Protein 2×3 ml 3×3 ml 1×3 ml Lipid 2×3 ml 3×3 ml
methanol
44·38 43·05 42·88 12·26 14·53 15·84
Chloroform: 1×3 ml Protein 2×3 ml 3×3 ml 1×3 ml Lipid 2×3 ml 3×3 ml

methanol
s 0·63 0·46 0·25 0·48 1·53 0·95
CV 1·42 1·07 0·58 3·92 10·53 6·00
Discussion
The larger F-values for protein compared with lipid draw attention to the
unexpected discovery that although the rôle of C-M is, of course, primarily
extracting lipid, its most noticeable effect is really upon protein. The greatest
effect is between the first and second washings. Interestingly, the increase in
lipid obtained between the second and third washings with C-M can only be
considered to be small compared with the additional effort involved. The
apparent loss of protein associated with washing with C-M is alarming.
The unsettling impressions gained from these simple methodology tests with
Pandalus material raised the question of what happens with relatively lipid-rich
material. The swimming muscle complex of capelin (Mallotus villosus) is
interesting in that being muscular it contains much protein but it also contains
large quantities of lipid at certain seasons (Jangaard, 1974). The problems of
dealing with such coarse and muscular, yet nevertheless often lipid-dripping
material, are myriad. The hindsight gained from the Pandalus material goaded us
to examine some of the pertinent problems in more detail. We purposefully have
avoided speculating on the many possible reasons for the apparent decrease in
total protein with additional washings with C-M as these have been examined in
detail later in this article (see p. 246), using capelin material. The most likely
explanation, nevertheless, was considered to be that lipoprotein or proteolipid
was lost in the aqueous phase of the Folch et al. (1957) extraction.
MORE SPECIFIC TESTS WITH CAPELIN MATERIAL
FACTORS INFLUENCING LIPID VALUES RECORDED

After C-M is added to the material in the test-tube the lipid containing extraction-
phase is transferred to a graduated centrifuge-tube. During this process a small-
fraction of non-fat containing material may also be transferred. NaCl solution is
added in order to wash the lower, lipid-containing phase of such material. During
pipetting of the upper (salt) water phase, after centrifuging, a small volume of
this will generally be left behind because one normally tries to avoid sucking up
any of the lower, lipid-containing phase. The volume of the salt-containing phase
remaining ought, obviously, to be kept to a minimum. Although procedures are
available (e.g. Sephadex G-25 columns, see Christie, 1982) for removing non-
lipid contaminants, use of them is generally time consuming. Most analysts
carrying out large numbers of total lipid determinations in conjunction with an

ecologically orientated programme, tend to save time by following the standard
Folch et al. (1957) method where such specialized purification is not involved.
First, it is important to stress that the aqueous phase obtained in the standard
Folch et al. (1957) technique should be removed completely for quantitative
work; this is quite easy using micro-separating funnels. A simpler way is to use
Whatman PS (phase separating) paper which is silanized cellulose. This passes
organic solutions but not aqueous solutions, although water will pass through if
the aqueous phase is left in contact with it too long. This technique works well
with the aqueous phase obtained in this case. Any organic phase left on the PS
paper can be washed through with the lower phase (i.e. 2:1 C-M) that has been
equilibrated with 0·2 vol. of 0·9% NaCl.
Bearing these considerations in mind we thought it necesary to calculate the
following.
(1) The weight of NaCl left behind in the water phase.

(2) The amount of material which may be inadvertently recorded as ‘lipid’ after
drying of the lower phase.
(3) The weight of lipid which may be lost or not recorded when determining
total lipid.
Methods
These experiments were carried out using purified capelin-lipid replicates of 12-
mg weight, corresponding to the lipid contained in about 30 mg of swimming
muscle. This amount was specifically chosen on the basis of later tests indicating
that about 30 mg of this material was optimal for combined lipid and protein
determinations.
Three methods were used for determining the weight of NaCl in the remaining
water phase. (i) Three sets of 10 test-tubes each containing 12 mg of pure lipid
had 3 ml, , and , respectively of C-M added to them; the standard
lipid analysis procedure described in Figure 1 was then carried out. (ii) Same as
(i) but omitting to add the NaCl solution. (iii) 10 centrifuge-tubes each had 10 ml
of C-M added followed by 2 ml of 0·9% NaCl solution; all the tubes were
centrifuged and the volume of the water phase was then measured before being
pipetted off; afterwards the volume of the remaining water phase was measured
using calibrated, graduated centrifuge tubes.
To determine the weight of non-lipid material which may be recorded as, or
become bound to lipid, 10 centrifuge-tubes each containing 12 mg of pure
capelin lipid had 10 ml of C-M added. H
In order to determine the amount of lipid lost during analysis, the results from
test (i) were combined with the results from test 2 to determine the weight of non-
lipid material that may be recorded or become bound to lipid.
Results
Table V shows the per cent lipid recorded after treating pure lipid with 3, 6, and
9 ml of C-M, with and without the addition of NaCl solution. The mean
percentages of lipid without the addition of NaCl solution range from 104·8 to
106·6% with increased levels of washing with C-M. The coefficient of variation
(CV) varies from 1·7 to 2·4%. With the addition of NaCl solution the values for
per cent lipid recovered range from 115·4 to 116·8%; the CV of 4·8 to 6·3% is
significantly greater than for the non-NaCl data. Use of one way ANOVA testing
shows that in both cases the use of varying amounts of C-M does not
significantly (P>0·05) affect the amount of lipid recovered (Table VI). There is,
however, significantly more (P<0·001) ‘lipid’ recovered with the addition of
NaCl solution (Table VII). The difference between the methods amounts to
about 10% in terms of recovered lipid.
Most, if not all, of the difference between the methods just described can
probably be accounted for by the extra weight of NaCl gravimetrically recorded
as ‘lipid’. This amount can be estimated with a high degree of accuracy. This has
been done, in the absence of evidence for significant within group variation with
varying amounts of C-M, by simply taking the means of the means for mg lipid
recorded after addition of 3, 6, and 9 ml C-M for treatment with and without
NaCl as given in Table VIII. The difference, 1·3 mg of 14·0 mg recorded as
being ‘lipid’, in this table can be considered to be due to NaCl, owing to this
being the only different factor between the two experiments.
TABLE V
Per cent lipid recovered after treatment of pure capelin lipid with 3, 6 and 9 ml of
chloroform: methanol with and without NaCl
Chloroform: methanol 1×3 ml 2×3ml 3×3 ml
Without NaCl
104·82 105·66 106·58
s 1·806 2·532 1·069
CV 1·72 2·40 1·75
n 10 10 10
With Nacl
115·38 115·36 116·77
s 6·287 5·490 7·374
CV 5·45 4·76 6·32
n 10 10 10
TABLE VI
One way ANOVA performed on the per cent lipid recovered after treatment of 12-mg lipid
replicates with 3, 6 and 9 ml chloroform: methanol with and without NaCl solution
Without NaCl
Between groups 2 0·1307 0·0753 1·19−
Error 27 1·4880 0·0551
Total 29 1·6187
With NaCl
Between groups 2 0·109 0·054 1·09−
Error 27 17·021 0·630
Total 29 17·130
TABLE VII
One way ANOVA comparing lipid percentages recovered with and without NaCl solution:
based on raw-data incorporated in Table V
Between groups 5 22·433 4·887 14·26***
Error 54 18·509 0·343
Total 59 42·942
TABLE VIII
Variation in the weight of ‘lipid’ recorded with or without NaCl added as a function of the
amount of chloroform : methanol used: a known sample-loading of 12 mg pure capelin-
lipid was used
Chloroform: methanol added (ml) Lipid recovered (mg)
Without NaCl With NaCl
3 12·64 13·97
6 12·74 13·94
9 12·80 14·08
12·72 14·00
Estimated NaCl contribution (mg) 1·28
The results of the test involving measuring the amount of the water phase with
10 replicates after (a) centrifuging, and (b) after pipetting, using 10 ml C-M and
2 ml 0·9% NaCl solution, showed that there were (mean±standard
deviation) ml of water phase, and of this phase left after pipetting.
These mean values have been used as the starting point for further calculations.
The original volume of the water phase added in the form of NaCl was 2 ml.
After centrifuging this was found to be 3·8 ml; an increase of 1·8 ml. Given that
1 ml of water weighs 1 g, and that the whole amount of NaCl contained in 2 ml of
NaCl solution before centrifuging also is contained in the 3·8 ml water phase
measured, we can calculate that the weight of NaCl present in the 0·29 ml
remaining after pipetting is about 1·4 mg. This value is almost identical with that
calculated as the difference between treatment with and without NaCl given in
Table VIII.
THE AMOUNT OF EXTRACTING-SOLVENT WHICH IS

ASSOCIATED WITH LIPID
It has been shown, with pure lipid as a starting point, that the amount of washing
with C-M does not have a significant effect on the amount of
lipid recorded at the end of the analysis. This applied to within treatments both with
or without NaCl. Lipid analyses carried out with C-M washings in the absence of
added NaCl resulted, however, in an average recording of about 6% more ‘lipid’
than the 12 mg pure lipid originally used (see Table VIII) This increase can be
tentatively considered as being due to some of the extraction solvent being bound
to the pure lipid, or else to inadequate drying or a combination of both. This is,
however, most likely to be water which can easily be removed by subjecting the
samples to a high vacuum (oil pump), e.g. in a desiccator.
Results
In this experiment the percentage of ‘lipid’ recorded for 10 replicates after 10 ml
of C-M was added to 12 mg of pure lipid was found to be with a CV
of 2·1%. A one way ANOVA carried out comparing the weights of ‘lipid’ recorded
before and after the direct addition of C-M shows that the differences are highly
significant . As no NaCl was added this
difference must be accounted for, in some way, by some of the C-M being
recorded together with the lipid. In this experiment this is calculated as 0·7 mg
added to 12 mg of pure lipid.
THE AMOUNT OF LIPID LOST DURING TOTAL LIPID

DETERMINATIONS
An approximate estimate of this can be arrived at by comparing (a) the amount
of ‘lipid’ recorded after 10 ml of C-M have been added directly to known
quantities of pure lipid and the test-tube contents dried and weighed (i.e. omitting
the other steps shown in Fig. 1), and (b) the amount of lipid recorded after
carrying out the complete lipid determination as shown in Figure 1 without the
addition of NaCl solution. A one way ANOVA testing the null hypothesis that
sample means are similar cannot be discarded .
Thus, it appears unlikely that there is significant loss of pure lipid during the
normal lipid analysis procedure. It must be borne in mind that this applies to pure
lipid, and that the situation may be different when the lipid has to be extracted
from naturally occurring material or tissue.
SUMMARY
We have described two alternative methods for determining the weight of NaCl
left behind in the upper, water-phase (point 10, Fig. 1) after pipetting. This NaCl
appears to be registered as ‘lipid’ by the Folch et al. (1957) technique. Both
methods provide almost identical estimates: 1·3 mg using a practical gravimetric
test-method involving lipid determinations with and without added NaCl and 1·4
mg using a theoretical test-method where the weight of NaCl is calculated from
measurements of the volume of the upper, water-phase before and after
pipetting. In the forthcoming tests we have chosen to estimate the amount of
NaCl remaining in the water phase as 1·4 mg. This amount is likely to be
constant irrespective of the sample-loading used. The weight of solvent bound to
lipid is estimated as 0·7 mg. This value, however specifically applies to a sample-
loading of capelin lipid corresponding to 30 mg of the dried muscle complex; it
ought to be estimated for other sample-loadings.
We deduce that, using sample-loadings of pure lipid only, none of this lipid
was lost during the course of the standard Folch et al. (1957) analysis. This holds
for varying sample-loadings. An estimate of the combined error from the factors
described above indicates that use of the standard Folch et al. (1957) method
provided us with 14·10 mg of lipid where we in fact only had 12 mg. We thus
over-estimate the real amount of lipid by 17·5 %. In the case of our capelin
muscle-complex material we know that 12 mg of lipid is recovered from 30 mg
of muscle complex i.e. we have 40% of dry weight as lipid. Unless compensated
for, NaCl and C-M recovered as ‘lipid’ will, in this case, raise lipid values to
47%. In tissues with large amounts of lipid these errors will not be great,
whereas they will play a proportionately greater rôle in lipid-poor tissue. We
recommend that the individual analysts appraise the importance of these errors in
determining the precision of their data, and when pertinent, make due
compensations.
SOME CONSIDERATIONS WHEN SELECTING A

SAMPLE-LOADING FOR PROTEIN AND LIPID
DETERMINATIONS USING THE STANDARD
TECHNIQUES
The proportion of lipid and protein in any tissue or material can vary greatly from
animal group to animal group, and often from season to season. The amount of
material chosen for analysis ought to take regard to the proportion of protein and
lipid present per unit weight of sample. Båmstedt (1974), for example,
considered that in the case of protein and lipid analyses using dried homogenized
Pandalus borealis the best results for lipid and protein were achieved with 50-
mg and 5 to 10-mg sample-loadings, respectively. Obviously where the aim is to
carry out accurate determinations of both lipid and protein large and significant
disparities between the optimal sample-loadings for these two variables make the
use of a common sample-loading for combined determinations impossible.
In this section we draw attention to a number of considerations which ought to
allow more accurate determinations of total protein and total lipid to be made
using the basic Gornall et al. (1949) and Folch et al. (1957) techniques sketched
in Figure 1. We emphasize, however, at this point that later tests carried out raise
serious doubts as to the ability of the former technique, as practised in its basic
form, to provide an absolute quantification of the protein levels actually present.
Nevertheless, although the real levels of protein recorded by the technique of
Gornal et al. (1949) can be questioned, following the relevant recommendations
outlined here will to a large extent, help cut down much of the inherent
variability present in unqualified use of these techniques. In this section we
attempt to provide a reasoned consideration of “What is optimal sample size?”
Method
Sample-loadings of dried, homogenized capelin swimming muscle complex were
accurately weighed from 15 to 50 mg in 5-mg steps. 10 replicates were used for
each sample-loading. After the addition of C-M the sample material was hand
stirred and any ‘clumps’ broken up and dispersed with a glass-rod. The reason
for using a glass-rod rather than the more expected electrical test-tube vibrator for
mixing up the contents of the test-tube with this material will be made clear in a
later section.
Results
The amount of lipid as per cent dry weight recorded from the various sample-
loadings is presented in Table IX. The greatest percentage of lipid was recorded
with sample-loadings of 15 mg, yet the CV from these data were also the
greatest. Both the mean per cent lipid recorded as well as CVs decreased rapidly
and markedly with increasing sample-loadings up to 25 mg, after which
stabilization occurred.
TABLE IX
Lipid, as per cent dry weight, recovered with varying sample-loadings
Sample-loading (mg)
15 20 25 30 35 40 45 50
57·43 50·85 44·71 45·37 43·42 41·85 43·68 41·80
s 4·82 2·82 1·69 1·31 1·63 0·82 1·55 1·19
cv 8·39 5·55 3·78 2·89 3·75 1·96 3·55 2·85
n 9 10 10 10 10 10 10 10
Fig. 3.— Protein extinction (550 nm) as a function of sample-loading (mg) of dried,
homogenized capelin swimming-muscle: 9 ml chloroformmethanol used (see Fig. 1 for
further details); means and 95% confidence limits shown.
Fig. 4.—Per cent protein as a function of sample-loading (mg) of dried, homogenized

capelin swimming-muscle: 9 ml chloroform-methanol used (see Fig. 1 for further details);
means and 95% confidence limits shown.
The extinction values recorded for protein as a function of sample-loading are

presented in Figure 3. As expected, the values increase with increasing sample-
loadings due to increasing concentrations of protein per unit volume of extracting
medium. The relationship between extinction and sample-loading is linear up to
and including sample-loadings of 35 mg, after which there are clear signs of a
curvilinear relationship. As explained before, this may be due to the protein in
the biuret reagent becoming saturated. The onset of non-linearity occurs at an
extinction of 0·5 which is at least 0·1 less than that using B.S.A. as the pure protein
standard. This indicates that in reality we should not use sample-loadings of this
capelin material that provide extinctions above 0·5. This emphasizes the point
often forgotten in protein determinations that our material does not have the
same physical properties as bovine serum albumin. It is vital to examine this
feature in the way just shown. An alternative approach when using the biuret-
method is to use dilutions of the extract rather than smaller sample-loadings.
The amount of protein recorded as a function of increasing sample-loading is
shown in Figure 4. These values were obtained by first converting the extinction
values to weights of protein (mg) using the regression for the protein standard
curve (B.S.A) before finally calculating the per cent protein. There is a trend for
an increasing per cent protein with increasing sample-loading up to and including
35 mg, after which there is a clear trend for the per cent protein to decrease. The
95% confidence intervals vary somewhat, however, 15-mg loadings have the
greatest confidence interval while 25-mg has the least.
THE EFFECT OF NACL ON LIPID VALUES WITH

VARYING SAMPLE-LOADINGS
The amount of ‘lipid’ recorded and the proportion of this which is in fact NaCl with
the capelin swimming muscle complex is shown in Table X. ‘Salt-free lipid’
applies to the lipid values obtained from the standard technique
TABLE X
The effect of NaCl on lipid levels with varying sample-loadings: NaCl=amount of NaCl
(mg) in the remaining water-phase; S-f lipid=‘salt-free’ lipid=mg lipid—mg NaCl; Lip.
1a=‘salt-free’ lipid as % dry weight; Lip. 2=lipid as % dry weight; Z=% of ‘lipid’
accounted for by NaCl
Sample-loading (mg)
15 20 25 30 35 40 45 50
Lipid, mg 8·83 10·29 11·24 13·62 15·21 16·80 19·69 20·94
NaCl, mg 1·4 1·4 1·4 1·4 1·4 1·4 1·4 1·4
S-f lipid, mg 7·43 8·09 9·84 12·22 13·81 15·40 18·28 19·54
Lip. 1a 48·35 43·94 39·14 40·72 39·42 38·37 40·58 39·01
Lip. 2 57·43 50·85 44·71 45·37 43·42 41·85 43·68 41·10
Z 9·08 6·91 5·57 4·66 4·00 3·48 3·10 2·79
as shown in Figure 1 after subtracting for the weight of NaCl. The mean per cent
lipid with 95% confidence limits as a function of varying sample-loadings for
both lipid determined using the standard Folch et al. (1957) method, as well as
for ‘salt-free’ lipid, is shown in Figure 5.
Fig. 5.—Per cent lipid as a function of sample-loading (mg) of dried, homogenized

capelin swimming-muscle: 9 ml chloroform-methanol used (see Fig. 1 for further details);
means and 95% confidence limits shown; I, per cent lipid recorded using the classical
Folch et al. (1957) technique; II, per cent salt-free lipid.
It is clear that the values for per cent lipid obtained with and without
subtracting NaCl are significantly different. The differences in terms of per cent
lipid between the two methods is greatest (′ 9%) with the lowest
TABLE XI
Sum of per cent ‘salt-free’ lipid and per cent protein for varying sample-loadings
Sample-loading (mg)
15 20 25 30 35 40 45 50
Protein 34·89 38·53 42·61 44·32 45·59 43·51 42·42 39·27
Lipid 48·35 43·94 39·14 40·72 39·42 38·37 40·58 39·01
Protein+lipid 83·24 82·47 81·75 85·04 85·01 81·88 83·00 78·28
sample-loadings. There is a clear trend for decreasing discrepancies between the

two methods with increasing sample-loading up to and including 25 mg, after
which there is a less clear trend for decrease. The difference between the two
methods is <5% for sample loadings <25 mg.
The sum of per cent salt-free lipid and per cent protein for varying sample
loadings is given in Table XI. The greatest difference exists between 15-mg and
50-mg loadings. The highest sum is obtained for loadings of 30 mg and 35 mg.
STATISTICAL ANALYSIS OF PROTEIN AND LIPID

VALUES OBTAINED WITH VARYING SAMPLE-
LOADINGS
One way ANOVAS were carried out to test the homogeneity of sample means,
for per cent lipid using the standard Folch et al. (1957) method with added salt
solution compared with those using salt-free lipid. In both cases it was clear that
there are very significant differences ; , for the
standard Folch et al. method: ; , for salt-free lipid)
in the per cent lipid obtained from different sample-loadings. The lower F-values
obtained for salt-free lipid are indicative of sample-loading having a lesser effect
on lipid returns than using the standard method.
A one way ANOVA was performed testing the homogeneity of sample means,
for per cent protein recorded with varying sample-loadings. Here again it was
clear that there were very significant differences ; , )
in the per cent protein recorded. The relatively low F-value obtained for protein
compared with lipid indicates that this variable is less affected by varying
sample-loadings than lipid is using either of the two lipid determination
techniques.
CHOOSING A SAMPLE-LOADING
There are several criteria for choosing a sample-loading designed to cut down
unnecessary variability in analytical technique. In most cases it is possible to
simplify the process of choosing the ‘optimal’ sample-loadings for determining
accurately the amounts of protein and lipid from a single sample by using a
system of ranking. We have awarded from 1 to 8 points to each of a number of
variables one ought to take into account when choosing the optimal sample-
loading. The higher the point awarded the higher the priority or desirability.
Table XII shows the results of ranking for various sample-loadings (15–50 mg of
dried, homogenized capelin swimming muscle complex) according to the per
cent salt-free lipid, per cent protein, and respective CVs. The results obtained
with the Folch et al. (1957) method involving adding NaCl have been re-
calculated in terms of salt-free lipid.
We have awarded high points for high percentages of total lipid and total
protein recorded. The most desired situation can be considered to be one
producing the highest combined lipid and protein percentages. Sample-loadings
providing low CVs for the replicates are to be preferred to ones providing high
CVs; ‘replicability’ is an important criterion. The ‘optimal’ sample-loading is
that receiving the highest sum of points awarded for (a) % lipid, (b) % protein,
(c) CV lipid, and (d) CV protein.
TABLE XII
Rankings for results from various sample-loadings, based on values for per cent ‘salt-free’
lipid, per cent protein, and respective coefficients of variation: Lip.=mean% ‘salt-free’
lipid; P=mean% protein; CV1=coefficient of variation for lipid; CV2=coefficient of

variation for protein; R= ranking values from 1–8, high values are most sought after;
CV1;
Sample-loading (mg)
15 20 25 30 35 40 45 50
Lip. 48·35 43·94 39·14 40·72 39·42 38·37 40·58 39·01
CV1 9·92 6·34 4·30 3·19 4·14 2·13 3·83 3·04
P 34·89 38·53 42·61 44·32 45·59 43·51 42·42 39·27
CV2 11·75 5·71 3·36 5·32 3·88 8·99 5·94 3·85
R Lip. 8 7 3 6 4 1 5 2
R CV1 1 2 3 6 4 8 5 7
E1 9 9 6 12 8 9 10 9
RP 1 2 5 7 8 6 4 3
R CV2 1 4 8 5 6 2 3 7
E2 2 6 13 12 14 8 7 10
E1+E2 11 15 19 24 22 17 17 19
It is clear from Table XII that 30-mg sample-loadings provide lipid and
protein data which we can consider to satisfy the criteria described above. One
ought to bear in mind that we have here considered the situation in capelin
swimming muscle complex from August which is relatively lipid-rich (′ 40% of
dry weight). The swimming muscle complex of capelin can, however, just prior
to spawning be comparatively lipid-poor (Jangaard, 1974). We suggest that in
material which undergoes large variations in the amount of lipid and protein
present (especially prevalent in high latitude marine ecosystems where lipid is
the main material anabolized and catabolized in times of food plenty and scarcity
or starvation, respectively (Sargent & Whittle, 1981; Clarke, 1983) that basic
corroborative tests be carried out, especially on lipid-rich or lipid-poor material.
In choosing an ‘optimal’ sample-loading for combined analyses of lipid and
protein we have not included the effect of C-M in the results as we have earlier
argued that this is constant. In Table XIII, however, for the ‘optimal’, 30-mg
sample-loading we provided a breakdown of the various components involved in
determining what we are measuring as ‘lipid’. In this Table we have defined
‘pure lipid’ as the quantity we are left with after we have subtracted for both
NaCl and the weight gained by pure lipid due to C-M treatment. Using the
classic, unmodified Folch et al., (1957) technique one records the per cent lipid
(as % dry weight) as 45·4%, whereas the more realistic figure is probably 38·4%
calculated as ‘pure lipid’. Of this over-estimation, about two-thirds is accounted
for by NaCl while the remaining one-third is due to C-M effects.
TABLE XIII
The influence of NaCl, and solvent on lipid registered using a 30-mg sample-loading
mg lipid 13.62
Mass of NaCl (mg) in the remaining water-phase+mass of solvent recorded 2·10
in lipid
mg lipid—(NaCl+solvent) 11.52
“Pure” lipid as per cent of dry weight 38·40%
Lipid as per cent of dry weight 45 ·40%
The proportion of “lipid” (%) which NaCl+solvent accounts for 6·97%
The proportion of “lipid” (%) which NaCl accounts for 4·65%
The proportion of “lipid” (%) which solvent accounts for 2·32%
SOME IMPORTANT POINTS

It is clear that the presence of NaCl is a major source of error in determining the
absolute amount of pure lipid using the gravimetric method of Folch et al.
(1957). The proportion of the ‘lipid’ this accounts for becomes greater with
decreasing sample-loading; in the case of a 15-mg sample-loading NaCl
accounts for about 9% of the total ‘lipid’. Nevertheless, it is evident from
Table X that the smallest sample-loadings (15 and 20 mg) have the highest mean
salt-free lipid values. A possible reason for this may be that the salt solution
(NaCl) has not managed to wash successfully the lipid phase of non-fat remains
which may have been randomly transferred during pipetting. Such remains will,
in the same way as for NaCl, be a source of error which increases with
decreasing sample-loading. The high CVs for 15-and 20-mg sample-loadings
strengthen this suspicion about some arbitrary transfer of material. This will have
to be solid material as small amounts of material soluble in C-M will almost
certainly be removed during the subsequent washing with 0·2 vol. 0·9% NaCl.
It is desirable to compensate for the weight gain by pure lipid due to the C-M
treatment in precise determinations of lipid levels. With the ‘optimal’ sample-
loading for capelin swimming muscle complex, 30 mg dry weight, this source of
error accounts for about 2·3% of the 7% disparity between the per cent ‘lipid’
recorded by the unmodified Folch et al. (1957) method and the per cent pure
lipid obtained after compensating for the effect of NaCl and C-M. We have not
tried to provide comparable estimates for other sample-loadings, however, the
amount of C-M which becomes ‘bound’ to lipid is probably dependent on the
amount of lipid exposed to C-M.
It is important to be aware that the standard curve for B.S.A. represents a
condition where one is dealing with pure protein alone. The relationship between
extinction and sample-loadings of B.S.A. will have its own characteristic form as
seen in Figure 2, where the linear relationship ceases above values of about 0·6.
Determination of protein spectrophotometrically, as in the biuret method
(Gornall et al., 1949) requires that one is aware that light absorptions can be
influenced by various pigments existing in our ‘natural’ samples which are not
present in B.S.A. It is thus important to get a measure of the effect of this by

determining at what point extinction-linearity ceases in our sample material. It is
always easier and more precise to work within an area of the extinction response
which is linear. With the quartz crystal cuvettes used in this work our bovine
serum albumin standard curve indicates that one ought to restrict sample-
loadings to less than 20 mg of pure protein (B.S.A.) corresponding to about 0·6
nm extinction. Figure 3, however, indicates clearly that we in fact ought to keep
to extinction values of under 0·5, which in terms of B.S.A. units corresponds to
less than 16 mg of pure protein. Unless compensated for, the use of sample-
loadings for capelin swimming muscle complex of more than 35 mg dry weight
will provide erroneous protein data. Corresponding pilot studies ought to be
carried out by the particular analyst before proceeding with any serious work.
ANOVA testing of protein and lipid levels obtained with varying sample-
loadings show categorically that the amount of material used for analysis plays
an important rôle in determining what results we get. A simple system of
‘ranking’, as used here, enables one to choose a sample-loading which
significantly reduces the level of error due to varying methodology. In the case
of our capelin swimming muscle complex, 30 mg appeared to be optimal for
lipid considered on its own, while 35 mg was optimal for protein on its own. These
sample-loadings are so close to each other that either 30 or 35 mg loadings are
acceptable when taking both lipid and protein into account. As pointed out
before, sample-loadings of more than 35 mg bring one into an area of non-
linearity for protein, such that a point can be made for preferring the 30-mg
sample-loading for greater security.
OPTIMUM EXTRACTION OF LIPID: SHAKING,

STIRRING OR NO TREATMENT?
This test was designed to find a method of treatment for capelin material in C-M
which gives an optimal extraction of lipid. Two methods were tried: an electrical
test-tube vibrator (“Whirlimixer”, Fisons Scientific Apparatus Ltd), and glass rod
handstirring. In addition, the effect of these two methods of treatment on the levels
of protein recorded were also determined.
Method
Two sets, each with 10 replicates, of 15, 25, and 40 mg of dried, homogenized
capelin swimming-muscle complex were used for this test. After addition of 9 ml
of C-M to each of the replicates, one set was treated during the lipid extraction
process by using the electrical test-tube vibrator, while the other identical set was
treated by hand-stirring with a glass rod. The procedures otherwise followed
were identical to those described in Figure 1 for determining total lipid and total
protein.
Results
Mean percentages, with standard deviations and CVs for treatment with test-tube
vibrator and glass-rod using 15, 25, and 40 mg of capelin swimming muscle
complex for lipid and for protein are given in Table XIV and Table XV,
respectively. The most obvious difference between the two sets of treatment was
the inability of any of the replicates for 15 and 25 mg using the test-tube vibrator
to sediment during centrifugation. Sedimentation, however, did occur with the
40-mg sample-loadings using the test-tube vibrator. There were no problems
with sedimentation for any of the glass-rod treated sample-loadings or their
replicates.
A one way ANOVA testing the homogeneity of sample means for the
percentage of protein recorded for 40-mg sample-loadings using the test-tube
vibrator and the glass-rod indicated no significant difference ( ;
). A similar one way ANOVA performed on the lipid data with
40-mg sample-loadings indicated that the glass-rod treatment gave significantly
higher values .
TABLE XIV
Lipid, as per cent dry weight, recorded with varying sample-loadings when treated by
electrical whirl-mixer or by glass-rod stirring
Sample-loading (mg) Whirl-mixer Glass-rod
15 25 40 15 25 40
Inability to to sediment ent 39·42 49·61 43·56 42·06
s 1·31 4·02 1·09 1·15
CV 3·32 8·10 2·50 2·73
n 10 10 10 10 10 10
TABLE XV
Extinction values for protein with varying sample-loadings when treated by electrical
whirl-mixer or by glass-rod stirring
Sample-loading (mg) Whirl-mixer Glass-rod
15 25 40 15 25 40
Inability to sediment 0·591 0·242 0·397 0·594
s 0·017 0·015 0·008 0·016
CV 2·88 6·20 2·02 2·69
n 10 10 10 10 10 10
Discussion
Our tests have shown that the capelin swimming-muscle complex used has about
38% of its dry weight as pure lipid. This value is high compared with the
majority of marine organisms (Giese, 1966; Sargent & Whittle, 1981; Clarke,
1983). As shown previously in this work Pandalus borealis has less than 20% of
its dry weight as lipid. The swimming muscle of cod (Gadus morhua), towards
the other extreme, has only about 5–7% of its dry weight as lipid (Love, 1970;
Eliassen & Vahl, 1982). The high lipid content of capelin swimming-muscle
complex results in a tendency for the so-called dry homogenate to be relatively
‘fluid’ and sticky, such that material in the test-tube easily forms aggregates or
clumps. Material having a high proportion of lipid will also have a low specific
gravity.
The addition of C-M results in very lipid-rich material floating to the surface
in the test-tube. In our experience use of a glass-rod to break these clumps up
into smaller portions results in speedier extraction of lipid, the material gradually
increases its specific gravity and will more readily sediment. A test-tube vibrator
in many cases does not have the desired effect in breaking up lipid-rich material,
and adequate sedimentation of smaller sample-loadings may be a problem. In
many instances gentle finger-tapping of the test-tube is probably as good a
method as any for adequate mixing of the contents.
The use of the less sophisticated glass-rod resulted in about 3% more lipid
being recorded with this treatment than when using the electrical test-tube
vibrator with directly comparable sample-loadings (40 mg of dried tissue). This
difference was statistically significant. Part of the reason for the increased return
using the glass rod may be that during high-speed vibration small particles of
tissue and lipid become attached to the inside of the test-tube above the normal
level of the C-M, such that full extraction of lipid does not occur. Although
careful washing of this area of the test-tube may flush this material down, the
distinct possibility exists that use of the vibrator, in this case, does not result in
full recovery of all the lipid. The fact alone that sedimentation difficulties can
exist with small loadings of dried, high lipid-content material provides good
enough grounds for avoiding vibration. A quick test using the principles
outlined, here will provide the necessary data to make an informed choice.
Should there be no significant difference between the test-tube vibrator and the
glass-rod (see our data for Pandalus borealis in Table III) then ease and speed of
using the former provides a powerful argument in its favour.
THE AMOUNT OF CHLOROFORM: METHANOL FOR

ADEQUATE EXTRACTION OF LIPID
Extraction of lipid using C-M is time consuming, although Folch et al. (1957)
suggest washing the material three times, each with 3 ml of C-M, cutting down
on the number of washings with C-M and repeated centrifuging followed by
pipetting of the supernatant will save time and effort. As demonstrated
previously in this article, the effort in gaining the remaining, small fraction of
lipid using additional washings with C-M may in fact be associated with loss of
protein. A correct decision here may not only save time, but may provide better
quality data overall.
Methods
Dried, homogenized capelin swimming-muscle was used for this test. The effect
of using one, two, or three extractions of C-M (see Fig. 1) on the amount of lipid
and protein recorded was analysed. The test was performed using sample-
loadings of 15, 25, and 40 mg. 10 replicates were used in each case. The
interaction between sample-loading, amount of C-M used, and the balance
between lipid and protein recorded was examined.
Results
Figure 6 shows the lipid, expressed as per cent dry weight, recorded as a function
of sample-loading and number of extractions with C-M. With a single extraction
with C-M (i.e. washing with 3 ml C-M) the difference between the greatest (from
15 mg) and the least (from 40 mg) lipid percentages was 14·4%. The CV was
least for the sets treated with two extractions of C-M.
The amount of protein, expressed as extinction at 550 nm, recorded as a
function of sample-loading and number of extractions with C-M is shown in
Figure 7. A summary of these data using protein expressed as per cent dry
weight, instead of extinction values, is given in Table XVI. The statistical
significance of these data has been examined using one way and two way
ANOVA.
For 15-mg sample-loadings. There was a significant decrease in protein
extinction and per cent protein from the first to the second extraction with C-M
(one way ANOVA: ), but there was
TABLE XVI
Mean weights of protein (mg, ), and protein as per cent of dry weight returned with
varying sample-loadings and different amounts of chloroform: methanol
Chloroform: methanol
1×3 ml 2×3 ml 3×3 ml
Sample- 15 25 40 15 25 40 15 25 40
loading (mg)
9·1 15·9 25·5 7·8 13·4 20·0 7·5 13·2 19·6
CV 6·16 2·48 3·02 1·59 3·15 1· 49 3·24 1·96 1·35
60·67 63·60 63·75 52·00 53·60 50·00 50·00 52·80 49·00
no significant change from the second to the third C-M extractions (one way
ANOVA: ). There was no significant change in lipid
percentage or weight between the first and second C-M extractions (one way
Fig. 6.—Per cent lipid as a function of sample-loading (mg) of dried homogenized capelin
swimming-muscle and amount (ml) of chloroform-methanol used as extraction solvent:
means and 95% confidence limits are shown.
ANOVA: ), but there was a just significant
decrease in lipid between the second and third C-M extractions (one way
ANOVA: ).
extinction and per cent protein between the first and second extractions with C-M
(one way ANOVA: ), but there was no significant
difference in protein extinction between the second and third C-M extractions
(one way ANOVA: ). There was a significant increase
in lipid percentage and weight between the first and second C-M extractions (one
way ANOVA: , ), but no significant increase in the
lipid recorded between the second and third C-Mextraction (one way ANOVA:
, ).
extinction and protein percentage between the first and second C-M extractions
(one way ANOVA: ), while there was an only just
significant decrease in protein extinction between the second and third C-M
extractions (one way ANOVA: , ). There was a
significant increase in lipid percentage and weight between the first and second
C-M extractions (one way ANOVA: ), but there
was no significant change in these lipid values between the second and the third
C-M extractions (one way ANOVA: ).
The change in the mean weight of protein between the first and second C-M
extractions (Table XVI) showed an increasing trend with increasing sample-
loading and thereby also increasing amount of total lipid per sample; this change
was −14·3% for 15 mg, −15·7% for 25 mg and-23·7% for 40 mg. The change in
the mean weight of lipid, on the other hand, showed no corresponding trend with
Fig. 7.—Extinction (550 nm) of protein as a function of sample-loading (mg) of dried,

homogenized capelin swimming-muscle and amount (ml) of chloroform-methanol used as
extraction solvent: means and 95% confidence limits are shown.
increasing sample-loading; there was no significant change for 15 mg, while

there were significant changes for 25 mg and 40 mg sample-loadings of +7·5%
and +4·8%, respectively.
An examination of the consequential changes in mean protein weights and
mean lipid weights between the first and second extractions (washings) with C-M
with different sample-loadings (Table XVI) reveals a number of interesting
points. With a 15-mg sample-loading the weight of protein decreased by 1·3mg
while there was no significant change in lipid weight. With a 25-mg sample-
loading the weight of protein decreased by 2·5 mg while lipid increased by only
0·8 mg—a small but significant increase. With a 40-mg sample-loading the
weight of protein decreased by 5·5 mg while lipid again only increased by 0·8 mg
—a small but significant increase. Thus, the marked decreases in protein weights
cannot be accounted for by lipid gain as a result of protein loss. It is also clear,
even in this lipid-rich material, that nearly all the lipid present is extracted by the
first washing with C-M, even when using a large sample-loading of 40 mg.
Use of two way ANOVA allows one to obtain a better idea about the relative
importance of number of extractions with C-M, varying sample-loadings, and
interaction between C-M and sample-loadings in determining the amount of lipid
(Table XVII) and protein (Table XVIII) obtained. Both in the case of
comparisons between one and two extractions with C-M, and two and three
extractions with C-M it is clear that variations in sample-loading plays a much

greater rôle than number of extractions with C-M, or interactions between the
two factors. A comparison of F-values in Tables XVII and XVIII for lipid and
protein, respectively, when contrasting one and two extraction with C-M shows
clearly that the effect of variation in C-M and sample-loading are both more
important for protein than they are for lipid; C-M, however, plays a relatively
more important rôle compared with sample-loading for protein than it does for
lipid.
Nearly all the decrease in protein was registered between the first and second
extractions with C-M: as seen previously, only the 40-mg sample-loading
showed a significant chang in the per cent protein from the second to
the third extraction with C-M; it is the contribution of the 40-mg sample-loading
which is responsible for the high F-value (760·12***) recorded in the two way
ANOVA for protein (Table XVIII).
The sum of the values for per cent protein and per cent lipid in relation to
sample-loading and number of extractions with C-M are listed in Table XIX. Lipid
percentages in this Table have been calculated as ‘salt-free’. The sum of protein
and lipid for all sample-loadings are greatest when treated with a single
extraction with C-M (3 ml C-M), and provide totals of over 100%. In the case of
material treated with two and three extractions of C-M the sum came to less than
100%—the lowest total (88·5%) was recorded in the case of the 40-mg sample-
loading with three extractions of C-M.
TABLE XVII
Two way ANOVAs using per cent lipid values as a function of varying sample-loading and
volume of chloroform: methanol used: A=varying amounts of solvent; B=varying sample-
loadings; A×B=interaction between A and B
Chloroform: methanol Type of variation d.f. SS MS F
A 1 49·142 49·142 12·34***
3 versus 6 ml B 2 1655·094 827·547 207·82***
A×B 2 33·213 16·606 4·17*
Error 54 215·004 3·982
Total 59 1952·453
A 1 39·528 39·528 9·07**
6 versus 9 ml B 2 1025·049 512·524 117·58***
A×B 2 25·802 12·901 2·96−
Error 54 235·385 4·359
Total 59 1325·764
TABLE XVIII
Two way ANOVAs using protein extinction values as a function of varying sample-loading
(15, 25, and 40 mg) and volume of chloroform: methanol used: symbols as in Table XVII
Chloroform: methanol Types of variation d.f. SS MS F
A 1 0·12831 0·12831 583·23***
3 versus 6 ml B 2 1·70572 0·85286 3816·64***
A×B 2 0·04193 0·02097 95·32***
Error 54 0·01166 0·00022
Total 59 1·99762
A 1 0·00056 0·00056 7·00*
6 versus 9 ml B 2 1·22401 0·61201 760·12***
A×B 2 0·00005 0·00005 0·62−
Error 54 0·00422 0·00008
Total 59 1·22889
TABLE XIX
The sum of per cent protein and per cent ‘salt-free’ lipid as (percentage of dry weight) as
a function of varying sample-loading (mg) and amount of chloroform: methanol (ml) used
as solvent for lipid extraction.
Chloroform: methanol
1×3 ml 2×3 ml 3×3 ml
Sample- 15 25 40 15 25 40 15 25 40
loading
(mg)
mg lipid 8·21 11.07 16·34 8·20 11·98 17·13 7·75 11·52 17·19
mg NaCl 1·4 1·4 1·4 1·4 1·4 1·4 1·4 1·4 1·4
mg ‘salt- 6 ·81 9·67 14·94 6·80 10·58 15·73 6·35 10·12 15·79
free’ lipid
%’salt- 45·22 38·66 37·39 45·12 42·20 39·34 42·18 40·13 39·50
free’ lipid
% protein 60·67 63·60 63·75 52·00 53·60 50·00 50·00 52·80 49·00
Sum % 105·89 102·26 101·14 97·12 95·80 89·34 92·18 92·93 88·50
lipid+%
protein
Discussion
The Folch et al. (1957) method for the isolation and purification of total lipid is
well known as a simple, yet effective one. The emphasis in studies of the
effectiveness of this technique has concentrated, understandably, on the
following points of interest for lipid interested analysts: (a) is the majority of
lipid contained in the tissue or material successfully extracted, and (b) how pure
(i.e. free from non-lipid substances) is this lipid? The emphasis has thus been
essentially on the lipid and possible impurities present in the lower (chloroform)
phase, and on whether any lipid is lost to the upper (methanol-water) phase. In
these respects the technique is considered for brain lipids, using wet tissue (not
dried), as recovering over 99% of the tissue lipids and that the washing
procedure removes essentially all the non-lipid contaminants; after a single
washing with C-M, the lower (chloroform) phase (point 11 in Fig. 1) was
essentially free from ‘non-lipid substances’ (Folch et al., 1957). The initial use
of wet tissue probably facilitates subsequent removal of water soluble
components, including proteins, in the wash with 0·2 vol. 0·9% NaCl. Precise,
quantitative determination of total lipid using the technique of Folch et al (1957)
demands total removal of the upper aqueous phase (point 11 in Fig. 1). Failure to
this results in NaCl being recorded gravimetrically as ‘lipid’.
The biuret reaction has been documented as being a simple, and rapid method
for determining protein fractions; a quantification of its effectiveness and
accuracy has been carried out (Gornall et al., 1949). They state that with the
exception of bilirubin, which absorbs light very weakly at 540–550 nm, there are
practically no substances which give the biuret reaction, and none that cause
significant interference. Nevertheless, as a precautionary measure, some workers
(e.g. Båmstedt, 1974) remove lipid as a precursor to reading protein extinction.
There are likely to be many other pigments which will interfere with protein
extinctions.
Although the gravimetric method of lipid determination of Folch et al. (1957)
and the biuret method of Gornall et al. (1949) are often used in combination on
the same material, the accuracy of these two methods when used together has not
been studied. The prevalent interest shown by many marine ecologists working
on energetics has instigated a trend for drying samples. This provides a logical
stepping stone for obtaining data from the same biological material about the
water content, C/N, lipid, protein, total energy content using microbomb
calorimetry, and organic/ash content. Such an approach provides interesting
possibilities for analysing and understanding growth tactics and utilization of
various organic body-components during specific parts or the whole of the life
cycle.
It now appears to be generally agreed that a mixture of chloroform and
methanol in the ratio of 2:1 will extract lipid more exhaustively from animal,
plant, or bacterial tissues than most other simple solvents or solvent
combinations (Christie, 1982). The whole point of washing several times with C-
M is to make certain of effectively extracting and transferring any lipid that may
not have been transferred during the previous washings and pipettings. The
extractability of lipid from a tissue is variable and is likely to depend upon the
physical characteristics of the tissue and on the lipids themselves (Christie,
1982). In addition, larger sample-loadings for any given species or material will
contain more lipid on an absolute basis, such that these sample-loadings of very
lipid-rich material may, in theory, saturate or approach the limits of the carrying
capacity of a single extraction with 3 ml of C-M. Extra C-M may be required to
flush down the walls of the test-tube should lipid-rich particles adhere in this
region. Our data confirm the effectiveness of the technique of Folch et al. (1957)
in extracting lipid. With a 25-mg sample-loading, our dried capelin material
yielded about 95% of the presumptive total lipid content with the very first
washing with C-M. Our data show, however, that what may be gained in terms
of extra lipid through use of more C-M may appreciably reduce the protein levels
recorded using the methods given in Figure 1. Our data also indicate that random
methods can produce very large sources of variation in the results obtained with
the Folch et al. (1957) and Gornall et al. (1949) methods used on their own or,
even more so, when used in combination. First, there are slightly different trends
to be seen in the influence of sample-loading and varying numbers of extractions
with C-M on the per cent lipid recorded. The difference can amount to nearly
55% lipid being recorded with a 15-mg loading and a single C-M extraction
while a 40-mg loading treated identically with C-M results in about 40% lipid
being recorded (Fig. 6). In lipid-rich animals, such as are common in high
latitudes (Sargent & Whittle, 1981; Clarke 1983), this will result in especially
high levels of inaccuracy, and will cause large sources of error in energy budget
calculations.
Using sample-loadings varying from 15 mg to 40 mg it is clear that the
amount of ‘protein’ drops drastically from that recorded after the first C-M
extraction to after the second C-M extraction. How can this be accounted for?
Theoretically there may be a number of reasons for this. Real loss of protein
when the two methods are used in combination is most likely to occur through
pipetting of the supernatant (point 3 in Fig. 1) when some protein may
inadvertently be lost. This can either end up being transferred with the
chloroform phase, so that it is weighed together with the lipid, or it may end up
in the upper, water phase of the biphasic system resulting after treatment with
NaCl solution (point 11 in Fig. 1). In the latter case this protein will normally be
discarded, and not recorded with either the lipid or the protein weights. The third
possibility is that excess lipid may artifically increase the extinction read off as
pure protein. Fourthly, ‘loss’ of protein may be associated with some kind of
hydrolysis of peptide linkages, upon which the biuret method is dependent.
Methanol in the original C-M is supposed to denature proteins and these will
certainly be completely denatured in the alkali used in the biuret. This last
possibility, at least with our capelin material, is unlikely as this decrease would
in all probability not continue beyond the very first extraction with C-M.
Our data clearly show that the lipid weight gain is very much less than the
protein weight decrease thereby demonstrating that the ‘lost’ protein does not
become added to the lipid weight. The possibility that lipid remaining after the
first C-M extraction, but removed by the second C-M extraction, provides an
elevated protein extinction is less likely as the 15-mg sample-loading shows no
change in lipid weight between the first and second C-M extractions yet protein
decreases at the same time by 1·3 mg. Large sample-loadings, e.g. 40 mg,
provide a high concentration of lipid in the test-tube at the onset, yet more than
95% of the lipid was recovered after the first washing with C-M—only 0·8 mg
remained to be recovered in subsequent washings—yet protein decreased by 5·5
mg from after the first to after the second washing with C-M. The 25-mg sample-
loading resulted again in 0·8 mg of lipid being recovered between the first and
the second washings with C-M, yet protein decreased by only 2·5 mg this time.
This demonstrates that interference from lipid when the two methods are run in
combination is not the major factor responsible for decreased protein values
between the first and the second washings with C-M.
Our data clearly show that a major source of protein loss in the dried capelin
material lies in the ‘water’ phase of the supernatant. The supernatant when
treated with NaCl solution forms a biphasic system. After centrifuging at 4,000
r.p.m. (corresponding to a relative centrifugal force, RCF, of 2202 with our
centrifuge) for 10 min the lower phase is kept and dried for gravimetric lipid
determination (point 11, Fig. 1). As the protein weight loss is much larger than
the lipid gain in weight between the first and second C-M washings, it seems
most likely that the lost protein ends up in the discarded upper phase. The lost
protein originally removed on centrifuging at point 3 in Fig. 1 is unlikely to be
due to sucking up protein-containing fluid from the lower, methanol phase
during pipetting of the supernatant as this would be approximately equivalent
after each extraction. As pointed out previously, the protein loss occurring
between the first and the second extractions with C-M is very much greater than
between the second and third. It seems reasonable to speculate that the lost
protein is found close to or actually on the interphase between the two layers,
thereby accounting for the majority of the protein being lost on the very first C-M
washing. Our own observations indicate that the boundary between the two
layers may often be far from clean. This is at discord with Folch et al.’s original
method given in 1954 (Folch, Lees & Sloane Stanley, 1954) and reiterated in
1957 (Folch et al., 1957) that a “biphasic system without any interfacial fluff is
obtained”. This suggests a basic discrepancy between our findings. Interfacial
debris can often be observed with the type of material we have used. Although
Folch et al. (1957) cite centrifuging times of 20 min at 2,400 r.p.m. they provide
no details of RCF so that it is impossible to compare directly centrifugation
details. Nevertheless, an alternative but by no means exclusive possibility is that
the ‘lost’ protein is in fact soluble in C-M owing to it being partly hydrophobic,
but that it repartitions back into the aqueous phase in the presence of 0·9% NaCl
due to its hydrophilicity being greater than its hydrophobicity. It should be noted
that Folch & Lees (1951) found proteolipids which were soluble in the C-M
phase.
Our data clearly show that the third extraction with C-M, does not result in a
great return in lipid yield, especially considering the extra work involved. The
most important variation in the lipid percentage recorded is clearly due to the
effect of varying sample-loading. The capelin material used in this experiment is
lipid-rich, nevertheless, it is quite clear that the third C-M extraction
recommended by the standard Folch et al. (1957) technique appears to be in
essence unnecessary. The apparent loss in protein associated with extraction with
C-M is very disturbing, as the lipid data indicate that with medium-size sample-
loadings about 95% of the lipid is recovered by the first extraction with C-M and
nearly 100% by the second extraction. We have thus constructed an experiment
in the following section to locate the factor responsible for this apparent loss in
protein.
THE SOURCE OF PROTEIN LOSS WHEN TREATING

WITH CHLOROFORM-METHANOL
In this section we have constructed a number of tests designed to clarify, under
known and controllable conditions, the source of protein loss highlighted in a
number of previous tests. In the previous tests, however, we were working with
naturally occurring material, either from P. borealis or from the capelin, such that
we had no proof of exactly how much protein and lipid was in reality involved.
In the forthcoming tests we have used a ‘blend’ of a known quantity of B.S.A.
and a known quantity of purified capelin lipid to examine the following sources
of error. (a) Does C-M in some way influence the ability of protein (as bovine
serum albumin) to give the biuret reaction? (b) Does washing with C-M really
cause protein to be washed away in the supernatant? (c) Is it necessary to extract
lipid from the material in order to get a dependable reading for protein extinction
—i.e. is there interference from lipid at E550? (d) Does the presence of lipid
further upset the levels of protein recorded? With the answers to the above
questions we attempt to provide a credible interpretation of the interplay between
the various factors involved.
METHODS
The materials and methods used are best understood by referring to the flow
chart presented in Figure 1.
The standard curve using B.S.A. was constructed by carrying out the biuret
reaction as shown from points 4–8 in Figure 1. In order to exclude the possible
effects of changing protein levels due to washing away of protein with C-M
during pipetting off of the supernatant for subsequent lipid determinations, we
simply added 3 ml of C-M to 12 mg of B.S.A. in a test tube. The contents of the
test tube were then dried and allowed to stand for 24 h. No material was removed
by pipetting, nor was there any form of vibration or centrifuging. Afterwards the
extinction at the end of a standard biuret determination was recorded (points 4–8
in Fig. 1 followed). This was for the sake of statistics carried out 20 times. The
extinctions recorded were compared with that obtained using the standard
procedure used to construct the standard curve—i.e. when B.S.A. had not been in
contact with C-M.
The possible effect of centrifuging at point 3 in Figure 1 on protein extinction
was examined by adding 3 ml of C-M to about 12 mg of B.S.A. in a test-tube and
centrifuging for 10 min at an RCF of 2202 before evaporating off the C-M and
carrying out steps 4–8 in Figure 1. This was repeated 20 times, and the results so
obtained compared with (a) those obtained when C-M was added to the protein
and dried without previous centrifuging, and (b) those obtained after carrying out
a standard biuret determination with the same amounts of protein as sketched in
points 4–8 in Figure 1.
The effect of optical interference from the lipid was examined by weighing
about 12 mg of B.S.A. into a test-tube and adding about 9 mg of pure capelin-
lipid to it. The amount of protein and lipid, as well as the ratio between the two,
thus approximated that found in capelin swimming-muscle. The contents of the
test-tube were then subjected to the standard biuret determination following
points 4–8 in Figure 1, and the optical density at 550 nm recorded. This was
repeated 10 times, and the results so obtained compared with the optical densities
obtained when no lipid was added.
The effect of following the lipid determination part of the flow chart (points 1–
3 and 9–12 in Fig. 1) on the optical density of protein recorded with the biuret
technique was examined by weighing about 12 mg of B.S.A. into a test-tube and
recording the extinction obtained at point 8 in Figure 1 after washing with 3 ml of
C-M. The possible disturbing effect of lipid itself was eliminated by not having
any lipid present. At the same time the amount of protein lost in the supernatant
at point 11 was measured by subjecting the upper phase of the supernatant to a
standard biuret determination. The extinction of the protein recorded, both that
measured as normal using the standard biuret as well as the sum of this and that
recovered in the supernatant, was compared with the optical density expected
from the same amount of protein from the standard curve.
The effects of using 3, 6, and 9 ml of C-M at point 3 in Figure 1 on the optical
density of protein as well as the amount of lipid recorded was examined using
about 12 mg of B.S.A. and about 9 mg of pure capelin-lipid. This was repeated
10 times with each of the given amounts of C-M. The amounts of protein and
lipid recorded using the analytical techniques sketched in Figure 1 with differing
amounts of C-M were compared with each other and with the original.
RESULTS
When about 12 mg of B.S.A. had 3 ml of C-M added and was allowed to
evaporate to dryness the extinction resulting from a standard biuret analysis
was significantly less (one way ANOVA:
) than that obtained when the same amounts of
protein were treated by the biuret technique in the absence of C-M
. When 3 ml of C-M was, however, added to 12 mg
of bovine serum albumin in a test-tube and then centrifuged at an RCF of 2202
for 10 min and a standard biuret analysis carried out, the resulting extinction
was on average 13·3% greater than that obtained in
the preceding experiment performed without centrifuging. Comparisons of the
extinctions obtained in these two experiments showed that they were very
significantly different (one way ANOVA: ). The
difference in the protein estimates was about 1·7 mg.
The addition of about 9 mg of the capelin-lipid to about 12 mg of B.S.A.
produced an extinction of . This was a very significant
increase (one way ANOVA: ) in extinction when
compared with the extinction of the same amount of B.S.A. without lipid
.
TABLE XX
Comparisons of protein (bovine serum albumin, B.S.A.) and lipid (purified capelin-lipid)
returned from known loadings after treatment by the techniques of Gornall et al. (1949)
and Folch et al. (1957) using 3, 6 and 9 ml of chloroform: methanol; see Figure 1 for
details of procedures; OD=extinction at 550 nm; F=values and asterisks describe the
results of one way ANOVAs performed to test the null hypothesis of equality of sample
means; n=10 in each case; d.f.1 =1 and d.f.2=18 in each case.
3 ml chloroform: methanol
Protein
Known B.S.A. Predicted OD Measured OD
loading (mg) from standard
curve
12·040 0·375 0·258
s 0·212 0·006 0·010
F=1031·44**
*
Lipid
Known lipid Lipid returned % lipid
loading (mg) (mg) returned
9·050 9·956 110·0
s 0·242 0·428
F=33·23***
Protein
curve
12·090 0·377 0·246
s 0·218 0·006 0·017
F=495·76***
Lipid
Protein
curve
Known lipid Lipid returned % lipid
loading (mg) (mg) returned
9·040 10·200 112·8
s 0·217 0·291
F=102·28***
TABLE XX—continued
Protein
curve
X 12·090 0·374 0·251
s 0·314 0·006 0·014
F=627·82***
Lipid
Known lipid Lipid returned % lipid returned
loading (mg) (mg)
X 9·020 10·470 116·1
s 0·199 0·442
F=89·38***
When 12 mg of B.S.A. without any added lipid was washed with 3 ml C-M
and the protein extinction measured in the standard manner, including
centrifuging at an RCF of 2202 (see Fig. 1), the value obtained
was not significantly different (one way ANOVA:
) from the extinction , )
obtained from 12 mg of B.S.A. which had 3 ml of C-M added and centrifuged
for 10 min at an RCF of 2202 without removing any of the contents. The upper
phase obtained at point 11 in Figure 1, after the addition of NaCl solution, when
treated to the biuret reaction had an extinction which
showed that negligible amounts of protein were lost in this portion. Summing the
protein in the upper phase to that normally recorded in the standard biuret
technique confirmed that it made no significant difference to the result for total
protein (one way ANOVA: ). The mean extinction
of 0·423 obtained above from 12 mg of B.S.A. was very significantly different

from the mean extinction
obtained from 10 determinations used in constructing a standard curve in the
normal manner as outlined by Gornall et al. (1949).
The experiment designed to examine the effect of washing several times with
C-M when known amounts of B.S.A. as well as lipid were present showed that
significantly more lipid was recorded with the standard lipid technique than was
originally present (Table XX). There was a trend for the lipid percentage
returned to increase with increasing number of washings with C-M, however, the
lipid percentage has not been compensated to take account of the previously
demonstrated effect of C-M and salt to increase the actual amount of lipid present.
As observed in previous tests with capelin swimming-muscle, the weight loss of
protein is very much greater than the corresponding weight increase in lipid. It is
clear that at least 95% of the lipid originally present was recovered with the very
first washing with C-M. The protein extinction measured after the first washing
with C-M was 68·8% of that expected to be obtained using the standard curve
estimates based on the amounts of B.S.A. originally weighed. The difference
between the expected and measured protein extinctions were significant at
regardless of the number of washings with C-M. There was no
significant difference between the mean protein extinction values measured with
one, two or three washings with C-M (one way ANOVA:
. There was no significant difference in the mean
weights of B.S.A. or lipid originally weighed into the test-tubes for the tests
using 3, 6, or 9 ml of C-M (one way ANOVA: protein—
; lipid— ,
DISCUSSION
The tests carried out in this section show that combination of the technique of
Gornall et al. (1949) for determination of total protein with that of Folch et al.
(1957) for determination of total lipid provides a number of pitfalls for the
unwary.
It is clear that incorrect, and artificially elevated protein extinctions result from
the presence of lipid in the material to be analysed. We, therefore, stress that in
order to obtain quantitative measurements of protein using the biuret technique
of Gornall et al. (1949) the lipid ought to be extracted first before proceeding
further. The effect of C-M per se on protein (B.S.A.) appears to border on the
edge of significance. In order to extract satisfactorily lipid from material to be
analysed for total protein using the biuret technique it is, however, generally
standard procedure to centrifuge after C-M has been added. Our data show, at
least with certain proteins, that the process of centrifuging in the presence of C-M
causes a significant increase in the extinction of the protein that has not, as far as
we have been able to ascertain, been documented in the literature as a source of
error in total protein determinations. This increase in extinction occurs in the

absence of lipid.
Given that centrifuging in the presence of C-M provides a significantly higher
starting extinction than predicted from a standard curve using the same quantity
of B.S.A., it is clear that in the absence of lipid the end result of combining the
total lipid technique of Folch et al. (1957) with the biuret technique of Gornall et
al. (1949) as outlined in Figure 1 does not in itself cause any loss of protein in
the upper phase. In the presence of lipid, however, it is clear that there is a real
loss of protein. Our results indicate that a very significant amount of B.S.A was
carried over with the lipid in the C-M normally pipetted off for quantitative
determinations of total lipid. Having known the amount of pure lipid in the test-
tubes originally, we were able to calculate that little if any of the protein ended
up with the lipid after addition of the salt solution. Thus, the lost protein ends up
in the upper phase obtained after addition of salt solution. This phase is
normally aspirated and discarded: it is perhaps not coincidental that one of the
major areas of error in total protein determinations using the biuret technique is
here.
It is well known that albumin naturally binds large amounts of lipids and other
hydrophobic compounds. Albumin is the natural carrier in serum of items like
free fatty acids and bilirubin. Serum albumin is soluble in items like 96%
ethanol, methanol, and acetone. It is isolated by precipitating total serum proteins
with 10% trichloroacetic acid (T.C.A.) and extracting the precipitate with 96%
ethanol containing 1% T.C.A. This yields effectively pure albumin, but still
containing lipid (Debro, Tarver & Korner, 1957). It is well known that there are
often strong forces of association between tissue lipids and other cellular
contents such as proteins (Christie, 1982). It is to be expected that albumin will
become even more lipid-soluble in the presence of added lipid owing to lipid
already being bound to it. Other proteins involved with, for example, lipid
transport, binding and the like, can be expected to behave in a similar way. These
proteins, of course, are likely to be relatively common in lipid-rich animals;
‘loss’ of protein in the normally aspirated supernatant using the standard biuret
technique of Gornall et al. (1949) can be expected to be increasingly pertinent in
studies of polar marine organisms.
Although it now appears to be clear what is happening during the process it is
still not immediately clear what one has really been measuring when using the
standard biuret technique of Gornall et al. (1949). We can illustrate this by
reference to Figure 8, which shows, in the form of a flow chart, the various turns
of event when we attempt to provide a quantitative estimate of the amount of
protein present in our sample. The extinction recorded at the end-point of the
biuret technique cannot be directly compared with the normally constructed
standard curve for B.S.A., as we are dealing with protein whose characteristics
for giving a specific extinction with the biuret reaction have been significantly
changed from those which were originally present due to centrifuging in the
presence of C-M. It thus appears, on the basis of B.S.A. and capelin-lipid, that
Fig. 8.—Flow chart outlining changes in extinction (550 nm) of 12 mg of bovine serum
albumin (start extinction 0·372), with 9 mg of purified capelin-lipid subsequently added
when treated by the Gornall et al. (1949) and Folch et al. (1957) techniques as outlined in
Fig. 1: see text for further details.
one has previously been measuring a protein extinction which in terms of B.S.A.
units is neither ‘here nor there’.
There is obviously a need for standardization as regards what we are
measuring and what we are comparing against. First, as it is clear that B.S.A. is
affected by centrifuging in the presence of C-M, it appears to be more relevant to
construct a standard curve for B.S.A. whose extinctions have been measured
after carrying out this treatment. The extinctions obtained will be noticeably
greater than those obtained from B.S.A. in the standard manner. As lipid has
been shown to have considerable effects upon the protein extinctions recorded,
this implies that total protein should never be determined on material still
containing lipid, i.e. washing with C-M is unavoidable. Secondly, the best
estimate for total protein present in the material is likely to be obtained when the
amount of protein measured as standard after 3 washings with C-M is added to
that found to be present in the normally discarded supernatant (see Fig 1). In both
cases, of course, the ‘new’ standard curve ought to be used.
A major problem in any attempt to obtain an accurate estimate of total protein
in the material to be analysed will be dependent upon the extent to which the
component proteins, and the physical characteristics of the material itself,
resemble B.S.A. This will always be an unsurmountable obstacle. This can be
illustrated by comparing the fact that there was no significant difference in the
extinction obtained after the first washing (3 ml) with C-M (Table XX) and that
obtained after the second washing (6 ml) with B.S.A. (Table XX), whereas using
capelin swimming muscle with about the same amount of protein per sample
there was a highly significant decrease in the extinctions after the first and
second washings (Table XVI). The result of this is that provided an effort is
made to standardize procedures reliable comparisons can be made between the
same species, or perhaps the same basic types of material, whereas between
group comparisons are likely to be misleading. The greatest pitfall will arise
when attempts are made to estimate the amount of carbohydrate, for example,
when data for lipid, protein, and ash are available. The accuracy of the
carbohydrate estimate, in this case will be a product of the various inaccuracies
inherent in each technique. Protein estimates are likely to account for a major
portion of the blame. The temptation to estimate carbohydrate by difference should
be resisted.
NUMBER OF REPLICATES NECESSARY FOR GOOD

CONFIDENCE LIMITS
The number of replicates used to determine levels of total protein and total lipid
dictate the confidence limits, and thereby precision of the data collected. In
addition, the number of replicates required determine the amount of time spent in
collecting the data. To a certain extent decisions governing the number of
replicates one needs will be a compromise. It is important to obtain a
quantification of the expected variability in one’s analyses. The definition of the
‘minimum number of necessary replicates’ ought to include an evaluation of the
minimum number of replicates which provide the first of the start of a series with
a stable and narrow coefficient of variation.
METHOD
We have chosen to carry out this experiment with a 30-mg sample-loading because
it represents a sample size close to the optimal for determinations of both lipid
and protein. The results are based on determining stepwise CVs on dried,
homogenated capelin swimming muscle complex using 10 replicates each for
determining lipid weight (mg) and protein extinction (E550).
RESULTS
The variation in the mean amount of lipid recorded (mg) and 95% confidence
levels (C.L.) with increasing number of replicates is shown in Figure 9. The
mean changes little with number of samples. The 95% C.L., although showing a
trend for decreasing up to and including the eighth replicate, undergoes the
greatest change between the second and the third replicate. The variation in the
mean protein extinction at 550 nm together with 95% C.L.s with increasing
number of replicates is shown in Figure 10. The mean values vary slightly up to
the sixth replicate, however, thereafter little variation is shown. The 95% C.L.s
Fig. 9.—Variations in the means and 95% confidence limits of lipid recorded as a
function of number of subsamples (replicates) taken: each replicate consists of 30 mg of
dried, homogenized capelin swimming-muscle; means and 95% confidence limits are
shown; the choice of subsamples used was made using random numbers.
decrease appreciably to the fourth or fifth replicate, after which stable, low C.L.s
are maintained.
The coefficient of variation (CV%) for both protein and lipid values as a
function of the number of replicates taken is shown in Figure 11. It can be clearly
seen that the lipid analyses have a lower CV in all cases except when only two
replicates were used. The CV for protein is relatively variable until the fifth
replicate has been taken, while lipid, besides showing less variability than
protein, has achieved a high degree of stability in its CV by the fourth replicate.
DISCUSSION
The minimum number of replicates necessary to obtain reliable data (i.e. data
with little inbuilt variation) can be chosen using data such as that presented in
Figures 9, 10, and 11. As the data presented here is the result of random number
choice, it has to be borne in mind that a certain amount of the variation seen
using few replicates is without doubt the result of such random variation. This
will, however, in practice also apply to a standard laboratory situation. It is clear
that high quality data in terms of replicability are unlikely to be obtained in
instances where fewer than three replicates have been taken. It is clear that use of
five replicates provides data of high quality, however, one may question whether
the increased dividends are worth the extra time and effort required. In the case of
the data presented here, with the material and analysts used, one can suggest a
compromise by using four replicates.
It is surprising that the CV for protein is appreciably greater than that for lipid.
This observation, together with the data presented in Figures 9 and 10
Fig. 10—Extinction (550 nm) of protein as a function of number of subsamples

(replicates) taken: each replicate consists of 30 mg of dried, homogenized capelin
swimming-muscle; means and 95% confidence limits are shown; the choice of
subsamples used was made using random numbers.
Fig. 11.—Coefficients of variation (CV) for mean amounts of lipid (mg) and protein
extinction (550 nm) as a function of number of subsamples (replicates): 30-mg sample-
loadings of dried, homogenized capelin swimming-muscle used; the choice of subsamples
used was made using random numbers.
demonstrate that the lipid data collected is less variable, and accordingly
probably more reliable than that for protein. This, of course, is dependent upon
one being aware of the basic pitfalls associated with varying sample-loadings,
number of extractions with C-M etc. that have been highlighted earlier. It is
worth noting here that the majority of the analysts we have contacted tended to
believe that the combined error arising from extraction and spectrophotometric
determinations of protein (not bovine serum albumin) is less than that arising
during the gravimetric lipid method of Folch et al. (1957).
The amount of variability seen in the type of experiment described here will of
course be to a large extent a function of the characteristics of the material being
analysed, and the precision of the analyst. We emphasize the need for
quantifying this variability before engaging in any large scale programme for
total protein and total lipid determinations. I
CONCLUDING REMARKS
Although more and more biologists and ecologists are applying techniques for
determining total lipid and total protein in their research the pitfalls lying in wait
for the unwary are legion. Many data, particularly when largely varying sample-
loadings have been used, are likely to have unacceptably large margins of
inaccuracy. The biuret technique can provide estimates of total protein which
deviate greatly from the absolute levels present. Estimates of total lipid using the
method of Folch et al. (1957) can also be highly inaccurate, under certain
circumstances, but in general are likely to be much more accurate than biuret
estimates for total protein. The accuracy of both lipid and protein determinations
can be greatly improved by carrying out simple trials to examine sources of
variation arising from variability in treatment and technique.
A significant part of the artifact introduced when carrying out determinations
of total lipid and total protein using the methods of Folch et al. (1957) and
Gornall et al. (1949), respectively, can be avoided by following the details as
outlined in them with diligence. There appears to be nothing inherently deficient
in the actual methods themselves. Rather the problems have tended to arise when
applying the methods sequentially to facilitate the rapid processing of numerous
samples.
The basic limitations, and chief pitfalls in the gravimetric method for
determining total lipid of Folch et al. (1957), and the biuret technique for
determining total protein of Gornall et al. (1949), in short, are as follows. (1)
working towards the outer limits of the sample-loading range. (2) Not all of the
aqueous phase of the dilute salt fraction is removed during the conventional
Folch et al. (1957) extraction; this consequentially gives high lipid levels in the
subsequent dried phase owing to included NaCl. As many marine organisms,
especially invertebrates, frequently contain large quantities of inorganic salts
associated with ionic and osmotic balance (Hoar, 1966), this aspect of negligence
plays an accentuated rôle in marine ecology. This is, to a large degree, simply a
matter of not applying the original method correctly which clearly implies that
the aqueous phase be removed in full. (3) It is not realized that some protein
material can be extracted with C-M and subsequently transferred back into the
aqueous phase during the 0·9% NaCl wash. Since this aqueous phase is discarded
the protein it contains is obviously ‘lost’. Our data also question the general
applicability of B.S.A. as a general standard for protein; the increased extinction

of known quantities of crystallized, lyophilized B.S.A. (SIGMA Chemical Co.)
in the presence of C-M and centrifuging may possibly be associated with the
B.S.A. not being completely lipid-free. This phenomenon requires further
investigation. In the meanwhile, we recommend the use of lipid-free B.S.A. (also
available from SIGMA Chemical Co.) in the construction of standard curves. We
should also like to encourage an appraisal of the possible advantages of using
other protein standards, e.g. gamma globulin.
The specificity of standard curves for particular proteins has been clearly
demonstrated by Van Kley & Hale (1977) for the protein determination
technique presented by Bradford (1976). This proposed assay for
protein (Bradford, 1976) is based on the binding of Coomassie Brilliant Blue
G-250, and was put forward as providing a rapid, reproducible, and sensitive
method for quantitative determinations. Pierce & Suelter (1977) and Van Kley &
Hale (1977) have drawn attention to the limited analytical value of the
Coomassie Brilliant Blue G-250 protein-binding since it shows great variability
in its sensitivity to various proteins. It is especially noteworthy in the light of our
results, that the applicability of the Bradford method to the analyses of
conjugated proteins such as glycoproteins and lipoproteins was queried on the
basis of the potential of such proteins to bind differential amounts of dye (Pierce
& Suelter, 1977). It seems relevant when considering potential uncertainties in
quantifying protein levels in general to cite Van Kley & Hale’s (1977) comment
about the method of Bradford: “A standard curve prepared for a specific protein
is reproducible and useful for that protein but cannot be generally applied without
potential great error.”
Highly precise total lipid and total protein data obtained from the same sample
in a sequential way requires a high degree of care incorporating modifications of
the approach outlined in Figure 1, inevitably resulting in an appreciably longer
procedure. On the other hand, the implementation of a number of safeguards as
highlighted in this article will provide data of a quite acceptable quality for
certain types of application. The most obvious are studies of seasonal trends in total
lipid and total protein in a given species. Comparisons of absolute levels of lipid
and protein in a given species or family at several locations when these have
been carried out by different analysts, especially when variations in methodology
are appreciable, ought to be approached with a healthy trepidation. We have
probably approached a point in the development of marine ecology as a
numerical science where it is necessary to ask, “Is the quality of the data
sufficiently good to allow us to bear the conclusions or predictions that are being
made?” In short, we ought to accept in all humility where the boundaries around
our data go.
We propose that when the need for high quality data is dictated the following
procedure, based on determining total lipid and total protein on separate
subsamples, commonly used in biochemical laboratories can be followed. The
normal starting point is wet tissue, although there is no reason why dried tissue
(preferably freeze-dried) should not be used. The tissue is homogenized in a

known volume of aqueous medium (usually to give a 10–25% w/v homogenate)
and separate samples taken for analyses. Total lipid is determined on one sample
by direct application of the Folch et al. (1957) method. Total protein is
determined on another, usually by direct application of the Folin-Ciocalteu
reaction (Lowry et al., 1951). Should problems arise in the direct application of
the Lowry et al. (1951) method then it is usual to precipitate macromolecules
with, for example, 10% trichloroacetic acid (T.C.A.), wash out low molecular
weight material (non-precipitated) with T.C.A. washes, treat with hot T.C.A. to
remove nucleic acid constituents, extract with organic solvents (alcohol, ether,
acetone mixes) to remove lipid, at which point protein and carbohydrate remain.
The use of the denaturing T.C.A. avoids loss of proteins in organic solvents. The
procedure outlined is essentially the traditional Schmidt & Thannhauser (1945)
tissue fractionation scheme. It is unusual that problems are routinely encountered
in the direct application of the method of Lowry et al. (1951) to aqueous tissue
homogenates. The reaction is rather specific and very sensitive; modifications
exist whereby a detergent (deoxycholate) is incorporated in the analyses to
minimize and generally eliminate problems due to excess lipid (Campbell &
Sargent, 1967). Problems from lipid generally arise from light scattering due to
the non-solubility of lipid droplets in the reaction medium. Another modification
exists whereby intractable protein can be made soluble in strong alkali; the
conventional reaction of Lowry et al. (1951), like the biuret, is sensitive to pH
(Campbell & Sargent, 1967). Nevertheless, having stated all this, it is unlikely
that this methodology, or indeed any other in use at present, will be directly
applicable to all material under all circumstances.
There is obviously a pressing requirement for standardization of methodology
in techniques for estimating levels of total lipid and total protein. Energy budgets
constructed for both individuals as well as populations and communities are
tending to become more and more inquisitive and complex. Unless the basic data
put into these budgets and models are reliable, and the inbuilt sources of error are
located and compensated for, many of the outputs and conclusions are likely to
contain an unacceptably high level of artifact.
ACKNOWLEDGEMENTS
C.C.E.H. is obliged to the late Dr Harold Barnes for suggesting the theme for
this work, and for his help and encouragement during the early phases of our
research. We are grateful to Drs John Sargent and Andrew Clarke and also John
Blackstock for their valuable advice and criticisms of the manuscript; we take
full responsibility for any inaccuracies that remain. Finally, special thanks are
due to Dr Margaret Barnes for her editorial patience and counsel.
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BIOCHEMICAL METABOLIC
REGULATORY RESPONSES OF MARINE
INVERTEBRATES TO NATURAL
ENVIRONMENTAL CHANGE AND
MARINE POLLUTION
JOHN BLACKSTOCK
Scottish Marine Biological Association, Dunstaffnage Marine
Research Laboratory, Oban, Argyll, Scotland
INTRODUCTION
The term “marine pollution” can be broadly defined as the introduction into the
marine environment of a diverse range of materials, derived from human
activities, in such quantities that the environment is made less suitable for
existing life forms (see e.g. Menzel, 1979). The impact of a pollutant on a marine
system generally varies both spatially and temporally as a consequence of a large
number of interacting factors related to the nature and quantity of the material
which is introduced and hydrographical characteristics of the area receiving the
discharge. In nearshore areas of the marine environment, especially semi-
enclosed systems e.g. estuaries, sealochs, and fjords, the rates of water exchange
are frequently relatively low and, as a consequence, such areas are generally
observed to be most affected by pollutant inputs (Waldichuk, 1979). Most
attempts at definition of pollutant effects have, therefore, related to nearshore
areas.
The responses of marine biota to the introduction of a pollutant can be
detected at a number of different levels of organization. At the highest level of
impact the effects are acute and lethal to all biota and such catastrophic effects
are easily recognized. At the next level of effect the most sensitive species of
fauna are eliminated and a proliferation of relatively tolerant species may result
with a consequent distortion of the balanced biological conditions and wide
diversity of fauna normally associated with the natural environment. This concept
is the basis of biological monitoring of pollutant effects (for reviews see Pearson
& Rosenberg, 1978; Gray, 1979; Reish, 1979) and the much discussed utilization
of certain organisms as indicators of various degrees of impact of pollutants in
marine systems (see e.g. Reish, 1972, 1973). Further increase in pollutant levels
may result in the elimination of all surviving species and it is desirable that the
possibility of such consequences can be indicated before lethal conditions occur.
264 JOHN BLACKSTOCK
With this ultimate objective considerable research has been undertaken on

biochemical, physiological, and behavioural responses of individual organisms to
relatively subtle effects of pollution and attempts have been made to relate such
changes to the physical, chemical, and biological effects of pollutants in the
marine environment (see e.g. Giam, 1978; Bayne et al., 1979; Eisler, 1979;
Blackstock, 1980a; Pearse, 1980).
The nearshore marine environment is subject to considerable natural
fluctuations in physical and chemical conditions e.g. temperature, salinity,
nutrient concentrations. Many appreciable effects of natural environmental
influences have been reported both at the level of marine communities (Cushing,
1979; Pearson & Eleftheriou, 1981) and at the level of biochemical, physiological,
and behavioural responses of individuals (Bayne, 1973; Cripps & Reish, 1973;
Gabbott & Bayne, 1973; Mangum, 1978; Pionetti & Toulmond, 1980; Ivanovici,
Ranier & Wadley, 1981). If the latter, highly sensitive, level of response to
environmental change is to be utilized successfully for the indication of subtle
effects of marine pollution it is necessary that responses to natural and
anthropogenic environmental stimuli can be distinguished (see Bayne, 1976). In
addition, at the cellular level of organization, fundamental metabolic processes
are generally similar in a wide range of organisms and as a consequence
responses of different organisms to various environmental influences are often
qualitatively similar (Stebbing, 1979). Metabolic regulation is achieved in
response to changes in the internal environment which is attuned to changes in
the external environment of an organism (Mahler & Cordes, 1971). The
application of biochemical studies of metabolic regulatory responses to the
assessment of the effects of pollution on marine fauna can, therefore, be a most
useful, sensitive complement to chemical, biological and physiological
programmes of investigation of effects of pollutants. The earliest warning of
subsequently more damaging effects of pollution on marine ecosystems may
indeed be obtained at this biochemical level. It is clear, however, that reliable
interpretation of the biochemical information requires an appreclation of the
influence, on metabolic regulatory processes, of natural variations in both the
external and internal environment.
A diverse range of marine animals have been utilized in investigations of
effects of various types of marine pollution. Some widely used species of fish
and marine invertebrates have been selected on the basis of their virtually
ubiquitous distribution and their ability to accumulate various pollutants e.g.
bivalve molluscs of the genus Mytilus have been recommended for study in
world-wide pollution monitoring programmes (Goldberg, 1975; Goldberg, et al.,
1978) and are also the subject of co-ordinated multidisciplinary studies of the
relations between physiological and biochemical changes and pollutant-induced
effects on individuals (Bayne, Livingstone, Moore & Widdows, 1976; Bayne et
al., 1979; Widdows et al., 1982). It has also been recommended that programmes
of assessment of pollutant effects should utilize at least one representative of
several major phylogenetic groups, and that comparative studies of the responses
BIOCHEMICAL RESPONSES OF INVERTEBRATES TO ENVIRONMENT 265
of various species within single phylogenetic groups should also be included in

such programmes (Giam, 1978). The approach which is applied in the author’s
laboratory is that the selection of suitable species for detailed study is based on
co-ordinated environmental and biological monitoring of the areas to be studied
(Blackstock, 1978a, 1980a; Pearson, 1982; Pearson & Blackstock, 1984). This
approach offers the advantage of utilization of species of invertebrates that, by
virtue of their distribution in affected areas, can be considered to be sensitive to
the effects of the pollutant in the environment.
All species are tolerant of a certain amount of environmental variation and near
and beyond the tolerable limits characteristic biochemical responses relating to
the ultimate survival or death of the individual are elicited. The tolerable limits
of environmental change vary considerably between species even within the
same phylogenetic group and there is also more limited but nevertheless
appreciable variation in the magnitude of response between different individuals
of the same species. The response of an animal to a pollutant will depend on its
sensitivity to that particular material and the magnitude of non-specific metabolic
regulatory responses depends to some extent on the natural range of
environmental conditions which the species can tolerate. Over the last ten years
there has been a considerable increase in biochemical investigations of the
responses of marine organisms to pollutants. A large number of such
investigations are collected in various review and symposia volumes from which
detailed information and further references are readily obtainable (see e.g.
Vernberg & Vernberg, 1974; Vernberg, Calabrese, Thurberg & Vernberg, 1977,
1981; Giam, 1978; Hart & Fuller, 1979). Various recommendations for the
application of biochemical techniques to the monitoring of effects of marine
pollution have been published in proceedings of meetings arranged by
organizations, such as The International Council for the Exploration of the Sea
(ICES), see Lee et al. (1980). A comprehensive assessment of the diverse range
of biochemical investigations which have been applied to detection of pollution
effects is not within the scope of this review, which is directed towards
examination of relations between non-specific biochemical responses of marine
invertebrates to natural and anthropogenic environmental change. Carbohydrate
catabolism has a particularly fundamental rôle in determining the energy
production by marine animals and those biochemical changes which may
indicate regulatory responses of carbohydrate catabolism to environmental
changes are, therefore, emphasized. Similarities, or differences, in such
responses of various marine invertebrates to natural or anthropogenic
environmental variations are discussed with the primary objective of providing a
means for realistic comparison of the sensitivities of various species to
environmental perturbations. From this comparison an attempt has been made to
derive some useful guidelines to assist the selection of ‘target’ species and
biochemical tests for inclusion in future programmes of assessment of subtle
effects of marine pollution and natural environmental perturbations.
266 JOHN BLACKSTOCK
METABOLIC REGULATORY RESPONSES TO

ENVIRONMENTAL CHANGE
Metabolic regulatory responses to environmental change must be considered in
relation to the concept of homeostasis which has been defined as including those
processes that contribute to the maintenance of most steady-states in organisms
(Hughes, 1964). An essential feature of this concept is the interaction of a
number of factors which are directed towards maintenance of the existing
balance of metabolism of an organism at any given time. Stebbing (1981) has
described homeostasis as the capacity of an organism to counteract the effects of
environmental change and his definition is particularly useful for application in
the present context. The metabolic regulatory responses of organisms to
environmental stimuli can thus be considered to be designed to maintain the
biochemical homeostatis of the affected organisms. It must be emphasized,
however, that homeostasis does not exclude metabolic change. The concept
infers only that a steady-state or finely controlled balance of metabolism is
maintained. The balance can, however, be established at different levels of
metabolic activity. Metabolic regulatory responses are continuously applied to
the maintenance of normal functions of an organism, even in the absence of
pronounced changes in the external environment (see e.g. Atkinson, 1976).
When environmental change(s) are of greater magnitude than the range normally
experienced by an organism its “counteractive capacity” (Stebbing, 1981) may
be exceeded and the consequent loss of the delicate balance of metabolism may
have severe consequences for the individual and, subsequently, for communities
and ecosystems.
Using these concepts it is relevant to consider effects of a hypothetical
environmental change as a time-related sequence of effects on an organism
(Fig. 1). In this sequence environmental changes near and beyond the limits of
tolerance of the organism are being considered, and such changes may be termed
stress. The first event of importance to the organism is the detection of the
change by sensory receptors, followed by the appropriate hormone-induced
metabolic adjustment and behavioural reaction. Mobile fauna, e.g. pelagic fish
and those invertebrates which are capable of the necessary movement, may
simply migrate from the area affected by the perturbation. Sessile organisms, and
those having limited mobility within a relatively restricted area are unable to
utilize the escape response. Most bivalved molluscs, polychaetes and many
crustaceans are in this category and the initial effect of the perturbation will be
hormone-mediated changes in metabolic flux designed to improve the chances of
survival of the organism (or its offspring when a spawning response is elicited).
The flux of metabolites through a metabolic ‘pathway’ or reaction sequence is
controlled by means of the regulation of reactions catalysed by enzymes. Control
of enzyme reaction rates can be exerted at a number of different molecular levels
and on different time scales of response. The most rapid and finely poised level
of control of metabolism is achieved by modulation of the catalytic activity of
Fig. 1.—Time related sequence of effects of environmental stress on marine fauna.
those enzymes which catalyse non-equilibrium reactions and are frequently

termed “regulatory” enzymes (Newsholme & Start, 1973). It must be
emphasized, however, that enzymes catalysing non-equilibrium reactions do not
always control the flux through a pathway (Groen et al., 1982; see also p. 270).
Slightly slower responses include changes in enzyme activities in response to
changes in effector and substrate concentrations. The next level of response is
achieved by induction or repression of the synthesis of enzymes and changes in
their rates of degradation. Finally, the coarsest and slowest adjustment of
metabolism in response to environmental change is achieved by means of natural
selection of enzyme variants to assist survival of the species. These processes are,
however, interrelated and ‘adjustment’ or rapid responses will continue
simultaneously with the slower control mechanisms. All of the levels of response
are of fundamental importance to our understanding of the responses of marine
organisms to environmental change and are, therefore, considered here in some
detail.
HORMONAL REGULATION
Hormonal control of metabolism has been the topic of much research effort in
recent years and our rather fragmentary understanding of the processes involved
268 JOHN BLACKSTOCK
is rapidly being improved (for reviews see e.g. Newsholme & Start, 1973; Cohen,
1981; Schole, 1982). At the present time the rôles of cyclic-AMP dependent
protein kinases in the regulation of enzyme activities by means of
phosphorylation-dephosphorylation reactions is considered to be a major general
mechanism by which metabolic fluxes are controlled by external stimuli (Cohen,
1981). There is, however, an increasing appreciation of the structural and
metabolic complexities of eukaryotic cells and the existence of a variety of
important, rapid control mechanisms is widely recognized. These mechanisms
include binding of a wide variety of compounds to enzyme molecules and
changes in the tertiary and quaternary structure of enzyme molecules induced by
a variety of effectors (see e.g. Mansour, 1972; Groen et al., 1982).
Rapid control of metabolism in invertebrates has received relatively little
attention and our knowledge in this area of research, is, therefore, very limited. A
few studies may, however, be considered to be pertinent to the demonstration of
rapid, hormonally induced regulation of metabolism in invertebrates. Much of
the research effort on this topic has been directed towards the study of the
control of glycolysis in molluscs, particularly the marine mussel, Mytilus edulis.
In recent studies of the control of glycogen phosphorylase activity in adductor
muscle of M. edulis Ebberink & Salimans (1982) have shown that there is no
detectable conversion of phosphorylase b to phosphorylase a. The former
enzyme may exist in monomeric or dimeric form in the adductor muscle and
glycogenolysis is catalysed by an active monomeric form of phosphorylase b.
The active monomer is an AMP-phosphorylase complex and its production is
dependent on pH, but there was no evidence of activation of a phosphorylase
kinase during contraction. In this respect the Mytilus adductor phosphorylase
activity is regulated by a different means from the phosphorylase activity of
vertebrate muscle during contraction. In the latter case phosphorylase kinase is
activated and catalyses the conversion of dimeric phosphorylase b into the active
tetrameric phosphorylase a (Drummond, Harwood & Powell, 1969; Mahler &
Cordes, 1971). During relaxation of the adductor muscle of M. edulis, however,
the action of serotonin (5-hydroxytryptamine) increases cyclic AMP
concentrations with the resultant activation of a phosphorylase kinase and
conversion of phosphorylase b to a in a manner analagous to the effect of
epinephrine in vertebrate muscle (Ebberink, Salimans & Zandee, 1981).
Evidence for the mediation, by cyclic AMP, of effects of 5-hydroxytryptamine
have been observed in several other species of invertebrate including species
belonging to the genus Mytilus (Twarog, 1976; Satchell & Twarog, 1978; Köhler
& Lindl, 1980; Ishikawa, Murakami & Iwayama, 1981) and in decapod
crustaceans (Battelle & Kravitz, 1978; Lemos & Berlind, 1981).
Further evidence for the involvement of hormonally-mediated control of
glycogen metabolism in M. edulis has been presented by Cook & Gabbott (1978)
and Gabbott, Cook & Whittle (1979) who have shown that glycogen synthetase
exists in two forms in mantle, digestive gland and adductor muscle. The inactive
form of mantle glycogen synthetase was converted to the active form in the
presence of endogenous phosphatase activity in incubated extracts and

differences in kinetic properties between the two forms were consistent with the
existence of a phosphorylation-dephosphorylation mechanism of control of
activity. The production of insulin-like hormones in M. edulis has been suggested
by Fritsch, Van Noorden & Pearse (1976) and for the freshwater bivalves
Anodonta cygnea and Unio pictorum a direct rôle of a substance, related to
insulin, in the control of glycogen metabolism has been suggested (Plisetskaya,
Kazakov, Soltitskaya & Leibson, 1978).
The enzyme phosphofructokinase catalyses the first rate-controlling reaction
in the glycolytic degradation of glucose-6-phosphate. This enzyme catalyses the
conversion of fructose-6-phosphate to fructose-1, 6-bisphosphate and the rate of
this reaction, and of the reverse reaction catalysed by fructose-1, 6-
bisphosphatase determine the overall rate of carbon flux through glycolysis in
various vertebrate tissues (Underwood & Newsholme, 1967; Newsholme &
Crabtree, 1976; Newsholme, 1977). In addition it has been indicated that
maximal activities (i.e. activities measured under optimal reaction conditions) of
phosphofructokinase can provide an indication of the maximum rates of
glycolytic flux in muscles from vertebrates and invertebrates (Crabtree &
Newsholme, 1972; Zammit & Newsholme, 1976). The kinetic properties of this
enzyme are extremely complex and a range of ligand and pH-directed molecular
transformations have been described together with effects of a wide range of
metabolic effectors (Mansour, 1972; Kono & Uyeda, 1974; Goldhammer &
Paradies, 1979; Hesterberg & Lee, 1982). Some of the most important
modulators of phosphofructokinase activity are shown in Figure 2, but it is
emphasized that the effects of several of the compounds shown are dependent on
reaction conditions and the source of the enzyme. The investigation of regulatory
properties of phosphofructokinase is severely handicapped by modifications of
enzyme properties in vitro (see Mansour, 1972; Weidemann, Kolbuch-Braddon
& Hickman, 1977; Sand, 1981), but recent work on mammalian
phosphofructokinases has indicated that a cyclic AMP-dependent
phosphorylation-dephosphorylation mechanism is involved in the regulation of
activity (Van Schaftingen, Hue & Hers, 1980; Claus & Pilkis, 1981; Soling &
Brand, 1981).
In invertebrates the existence of a hormonally controlled, rapid regulation of
phosphofructokinase activity by means of a cyclic AMP-dependent kinase has
not been conclusively established. In the liver fluke, Fasciola hepatica, rapid
stimulation of phosphofructokinase activity by cyclic AMP and serotonin was
observed by Stone & Mansour (1967), who suggested that the regulatory effect of
serotonin on activity of this enzyme was similar to the action of epinephrine on
glycogen phosphorylase in vertebrates. More recently, Hofer, Allen, Kaeini &
Harris (1982) have suggested that phosphofruckokinase activity in the muscle of
Ascaris suum may be, at least in part, regulated by a cyclic AMP-dependent
protein kinase. In studies of the regulatory rôle of phosphofructokinase in
glycolysis in the adductor muscle of the marine mussel, Mytilus edulis, Ebberink
270 JOHN BLACKSTOCK
Fig. 2.—The reaction catalysed by phosphofructokinase, showing some modulators of the

reaction rate.
and co-workers (Ebberink & Zurburg, 1979; Ebberink & de Zwann, 1980;
Ebberink, Livingstone, Thompson & de Zwaan, 1981) have shown
that phosphofructokinase only controls the rate of carbon flow during the first
few hours of valve closure. They found that the most important regulators of
phosphofructokinase activity in this tissue are the nucleotides adenosine-5′-
triphosphate (ATP) and adenosine-5′-monophosphate (AMP),
phosphoenolpyruvate and pH.
There is, however, evidence of a diversity of control mechanisms for
regulation of phosphofructokinase activity in marine invertebrates. In muscle of
the squid, Symplectoteuthis oualaniensis, Storey & Hochachka (1975) found that
the reduced form of nicotinamide-adenine dinucleotide (NADH) was a potent,
specific inhibitor of phosphofructokinase activity and redox regulation of activity
was, therefore, suggested. Storey (1976) proposed that oyster (Crassostrea
virginica) adductor muscle phosphofructokinase activity was regulated by
arginine phosphate concentrations. He also noted that cyclic AMP had a
relatively small kinetic effect on enzyme activity. In studies of other invertebrate
phosphofructokinases activation effects of cyclic AMP have been found. Bennett
& Nakada (1968) observed that cyclic AMP was an allosteric activator of
phosphofructokinase of Mytilus californianus and Haliotus rufescens.
Phosphofructokinase activity in extracts of the polychaete Glycera alba has also
been observed to be activated by cyclic-AMP (Blackstock, 1978b, 1980c). In all
these studies, however, the cyclic-AMP concentrations used were above the
physiological level which would be expected as a consequence of hormonal
action in invertebrates (see e.g. Ishikawa et al., 1981) and the observed effects of
cyclic AMP are not necessarily a consequence of the rôle of this compound as a
mediator of hormonal activity. In some invertebrates, however, concentrations of
cyclic AMP produced as a consequence of hormonal activity are sufficiently high
to have a specific effect, distinct from allosteric activation effects on
phosphofructokinase activity (Stone & Mansour, 1967) and further investigation
is required to ascertain whether such specific hormonally induced effects may be
involved in the rapid regulation of phosphofructokinase activity in any marine

invertebrates.
Detailed studies of phosphofructokinase from muscles and hepatopancreas of
decapod crustaceans have been carried out by several investigators. In general
the kinetic properties of the enzymes from the Alaskan king crab, Paralithodes
camtschatica (Freed, 1971) and in crayfish Orconectes virilis (Freed & Kirk,
1976) and O. limosus (Lesicki, 1980) resemble those of mammalian
phosphofructokinases. It is of interest to note, however, that Lesicki (1980)
found that ADP had an important regulatory influence on the kinetic properties
of phosphofructokinase from O. limosus muscle.
The enzyme, pyruvate kinase, has been shown to have an important regulatory
rôle in the control of glycolysis in adductor muscle after the first few hours in the
‘catch’ condition (Ebberink & de Zwaan, 1980). The rôle of this enzyme in
molluscan catabolism and its regulation has been excellently reviewed by de
Zwaan (1976, 1977) who has emphasized the importance of the alternative
routes for the catabolism of phosphoenolpyruvate in the regulation of carbon flux
through glycolysis. It is generally accepted that rapid regulation of pyruvate
kinase activity in certain mammalian tissues (e.g. liver) can be achieved by
reversible phosphorylation-dephosphorylation mediated by a cyclic AMP-
dependent protein kinase (Engström, 1978; Hall, McCully & Cottam, 1979) but
in glycolytic tissue, e.g. muscle,
allosteric control of activity is considered to be most important and theexistence
of a cyclic AMP-dependent phosphorylation-dephosphorylationsystem for rapid
control of pyruvate kinase activity has not beendemonstrated in invertebrate
tissues (for review see Munday, Giles & Poat,1980). Major regulatory influences
on the pyruvate kinase in invertebratetissues are considered to be allosteric in
action e.g. adenylates,phosphagens, and fructose-1, 6-diphosphate exert
influence on the pyruvatekinase activity in the oligochaete, Tubifex tubifex
(Hoffmann, 1977, 1981).In the snail Helix pomatia (Weiser & Lackner, 1977)
and in preparations ofoctopus (Octopus cyanea) muscle (Guderley, Storey,
Fields & Hochachka,1976) modulation of pyruvate kinase activity by
phosphagens has also beenobserved. Later studies have, however, suggested that
the apparentinhibition by the phosphagen, arginine phosphate, may in fact be
aconsequence of the presence of the enzyme arginine kinase as a contaminantin
the pyruvate kinase preparations (de Zwaan & Ebberink, 1978; Poat,Giles &
Munday, 1980).
It is clear that the most rapid regulatory responses elicited by hormones are
not well understood in relation to the control of carbohydrate catabolism in
invertebrates and there is no clear division in time between hormonally induced
responses and some of the more rapid regulatory responses to changes in
substrate and effector concentrations. These topics require considerable further
investigation to permit a more precise understanding of the temporal relations
between the release of hormones, molecular effects on regulatory enzymes and
the subsequent interplay of effects of enzymes on substrate and effector
272 JOHN BLACKSTOCK
concentrations and vice versa. The magnitude and duration of these early
responses can have a critical influence on the subsequent metabolic condition of
animals which have been subjected to environmental perturbation. An
understanding of early biochemical responses is, therefore, fundamental to our
ability to predict the subsequent impact of environmental change on the health of
marine communities.
INTEGRATIVE REGULATION OF CARBOHYDRATE

CATABOLISM
In the previous section mechanisms for the rapid regulation of carbohydrate
catabolism have been summarized and the regulatory influences of a number of
metabolically important compounds on the activities of rate-controlling enzymes
have been mentioned. It is clear that the initiation of regulatory changes results in
a sequence of inter-related events, that are directed towards the integrated
control of metabolism and maintenance of biochemical homeostasis. To achieve
this it is absolutely essential that the rates of the various individual reactions in a
metabolic pathway are attuned to each other so that, for example, the products of
one regulatory reaction satisfies the substrate requirements of the next regulatory
reaction in a metabolic sequence, and the net energy production or utilization by
the pathway is, in turn, precisely attuned to the requirements of the cell, the
tissue, and the entire organism.
One of the most important mechanisms for control of metabolic reaction rates
is the feedback regulation of the activities of rate-controlling enzymes. The
concept of negative feedback control of enzyme activity was established by 1956
(see e.g. Umbarger, 1956; Yates & Pardee, 1956) and in
subsequent investigations it was proposed that the nucleotide AMP was of
particular importance in the regulation of the relative rates of energy-yielding
and energy-requiring or storing processes (Krebs, 1964; Ramaiah, Hathaway &
Atkinson, 1964). Atkinson and co-workers (see Atkinson & Walton, 1967;
Atkinson, 1968a) developed the concept that control of energy (ATP)-generating
processes and in particular the regulation of the interactions between ATP-
generating processes and those which utilize ATP is achieved in response to the
energy balance of the cell rather than to the concentrations of any individual
nucleotide. The “energy charge” was defined by Atkinson & Walton (1967) as
the molar concentration ratio (ATP+½ADP)/(ATP+ADP+AMP) which is
numerically equal to half of the number of anhydride bound phosphate groups per
adenosine group, and the theoretical value of the adenylate energy charge (A.E.C.)
can vary between 0 (only AMP present) and 1 (only ATP present).
The reaction velocities of enzymes that utilize ATP and are inhibited by ADP
or AMP have been postulated to give steeply sloped plots of change of velocity
as a function of adenylate energy charge (Atkinson & Walton, 1967). This
concept was further expanded by Atkinson (1968a) who indicated that the
generalized response to the adenylate energy charge of enzymes involved in
regulation of ATP-regenerating (R) and ATP-utliizing (U) metabolic sequences

had the form shown in Figure 3. Several enzymes which catalyse reactions in
glycolysis and the citric acid cycle are either inhibited or stimulated by ATP and
respond to the energy charge as indicated by curve R while several enzymes
involved in biosynthetic reactions give a U type response (Atkinson, 1968b;
Atkinson & Fall, 1967; Klungsøyr, Hageman, Fall & Atkinson, 1968).
The intersection of the two curves (Fig. 3) represents a stable metabolic state
and any decrease in adenylate energy charge will tend to increase the rate of R
type reactions and decrease the rate of U type reactions. These changes tend to
counteract the decrease in charge by initiating further net production of ATP.
Interaction in effects of feedback modulators of enzyme activity and energy
charge values are of considerable importance in the regulation of metabolism and
Atkinson (1968a) has indicated that when the supply of exogenous substrate is
adequate any tendency for the charge to fall in value will be opposed by an
increase in energy (ATP) production. When the supply of substrate, however, is
limited the rate of regeneration of ATP will decrease causing a decrease in the
energy charge and a new steady state will be established at a lower value of
energy charge i.e. intersection of the R and U curves will be at a lower value of
energy charge. The importance of adenylates and feedback regulation in control
of metabolism has been extensively discussed by Newsholme & Start (1973) and
Atkinson (1977). In his review of anaerobic energy metabolism in bivalve
molluscs de Zwaan (1977) has discussed effects of the adenylate energy charge
on activities of pyruvate kinase and phosphoenolpyruvate carboxykinase from
the adductor muscle of the mussel, Mytilus edulis.
In recent years considerable research effort has been directed towards the
utilization of adenylate energy charge values to assess the metabolic condition of
marine invertebrates which have been affected by natural and pollutant-induced
change in environmental conditions. In general, energy charge values in excess of
0·8 are considered to be characteristic for tissues of organisms subjected to near
optimal environmental conditions and lower values, between approximately 0·55
and 0·7 are generally considered to be indicative of a response to environmental
stress. The application of adenylate energy charge estimations to the assessment
of effects of natural and anthropogenic environmental changes on marine
organisms has been discussed by various investigators (see e.g. de Zwaan, 1977;
Skjoldal & Båmstedt, 1977; Skjoldal & Bakke, 1978; Ivanovici, 1980a, b) and it
is clear that the diagnostic reliability of adenylate energy charge remains
unproven (see Ivanovici, 1980b, for discussion). Some of the difficulties
associated with utilization of adenylate energy charge as an indicator of
metabolic condition of marine invertebrates are also discussed later (see p. 290).
It has been predicted that adenylate energy charge values of less than 0·5 are
incompatible with normal regulated metabolism. This prediction was based on the
in vitro responses of rate-controlling enzymes to changes in energy charge in the
presence and absence of modulating compounds (see e.g. Klungsøyr et al.,
1968). In the case of phosphofructokinase, which is generally considered to be of
274 JOHN BLACKSTOCK
Fig. 3.—Effect of the adenylate energy charge on activities of rate controlling enzymes
involved in ATP-regenerating (R) and ATP-utilizing (U) metabolic reaction sequences
(reproduced with permission from Atkinson, 1968a, copyright 1968 American Chemical
Society).
major regulatory importance in carbohydrate catabolism, the situation arises

where ATP is a substrate and the phosphofructokinase reaction is part of an ATP-
regenerating reaction sequence. At zero energy charge the reaction obviously
cannot proceed and an increase in reaction rate occurs as relatively low ATP
concentrations are increased. Optimal ATP concentrations are generally
relatively low. Further increases cause inhibition of the enzyme and the reaction
follows a typical R type pattern i.e. activity declining rapidly at increasingly high
values of energy charge (Shen, Fall, Walton & Atkinson, 1968). Marine tissue
phosphofructokinases that have been studied in detail include those from tissues
of molluscs (Storey, 1976; Ebberink & Zurburg, 1979), crustaceans (Freed,
1971; Freed & Kirk, 1976), and polychaetes (Blackstock, 1980c). In each case
typical allosteric properties, including inhibition by ATP, were found. These
properties are consistent with the importance of this adenylate in the control of
glycolytic flux. An exception to this general rule was observed, however, by
Storey & Hochachka (1975) who found that phosphofructokinase activity from
the mantle muscle of the fast swimming squid, Symplectoteuthis oualaniensis,
was not inhibited by ATP and that the major regulatory influence was the NADH
concentration which they considered to represent a more immediate metabolic
signal indicative of hypoxia.
In many marine invertebrates succinate, proprionate, and other fatty acids are
important end-products of glycolysis under anaerobic conditions and one of the
major metabolic control points in this pathway is the competition between the
enzymes, pyruvate kinase, and phosphoenolpyruvate carboxykinase for their
common substrate, phosphoenolpyruvate (Hochachka & Somero, 1973; de
Zwaan, 1977). Investigation of regulation at this metabolic branchpoint by the
adenylate energy charge in the mussel Mytilus edulis has shown that pyruvate
kinase from the adductor muscle exhibits a typical R type response to change in
adenylate energy charge (Ebberink, de Zwaan & Wijsman, 1976) and the activity
of the enzyme was considerably increased as energy charge values declined from
0·92 to 0·67. This range of regulation represented the decrease in energy charge
values observed during five days of exposure of Mytilus to air and may,
therefore, be considered to be the physiologically significant range of values
within which regulatory responses, directed towards counteraction of the
detrimental effects of air exposure, were operative (see Wijsman, de Zwaan &
Ebberink, 1976).
Active invertebrate muscles contain relatively high concentrations of
phosphagens of which arginine phosphate and creatine phosphate are the most
widely distributed (see e.g. Rockstein, 1971; Van Pilsum, Stephens & Taylor,
1972). The phosphagens provide a high proportion of the total energy required to
fuel bursts of mechanical activity and it has been suggested that they provide a
transient buffer of muscle ATP concentrations (Beis & Newsholme, 1975). Little
change in energy charge would, therefore, be expected until phosphagen stores
are largely depleted. In swimming bivalved molluscs it has been confirmed that
the phosphagen, arginine phosphate, provides most of the energy required for the
rapid contractions of the adductor muscle (Gade, Weeda & Gabbott, 1978;
Grieshaber, 1978; de Zwaan, Thompson & Livingstone, 1980). Approximately
70% of the anaerobic energy production in the phasic adductor muscle of the
giant scallop, Placopecten magellanicus, is derived from the utilization of
arginine phosphate with about 15% of the total energy during swimming being
obtained from an increased rate of glycolysis (de Zwaan et al., 1980). In the
catch part of the adductor muscle, however, glycolysis contributes some 55 to
70% of the energy required for the valve snap and closure responses. Further
investigations have indicated that in the phasic adductor a gradual decrease in
adenylate energy charge from 0·94 to 0·76 accompanied depletion of the muscle
phosphagen reserves (Livingstone, de Zwaan & Thompson, 1981). In the body
wall musculature of the polychaete Arenicola marina, Surholt (1977) has also
observed a concurrent depletion of the phosphagen, phosphotaurocyamine, and a
decline in adenylate energy charge during electrically stimulated muscular
activity.
In some marine invertebrate tissues a regulatory effect of phosphagen
concentrations on activities of rate-controlling enzymes has been reported e.g.
Storey (1976) has reported that arginine phosphate is a strong allosteric
(feedback) inhibitor of adductor muscle phosphofructokinase of the American
oyster, Crassostrea virginica. It is also of interest to note that in the freshwater
oligochaete, Tubifex tubifex, Hoffmann (1981) found that pyruvate kinase
activity was inhibited by the phosphagens, phospholombricine, and
phosphoarginine. He also found, however, that ATP exerted a stronger inhibitory
effect on this enzyme. The inhibition of rate-controlling glycolytic enzymes by
phosphagens does not appear to be generally applicable in marine invertebrate
tissues and one of the most important regulatory signals affecting pyruvate
kinase activity is achieved by means of ‘feed-forward’ activation by fructose
276 JOHN BLACKSTOCK
biphosphate, the hexose phosphate product of the reaction catalysed by

phosphofructokinase (see de Zwaan, 1977; Zammit, Beis, & Newsholme, 1978;
Zammit & Newsholme, 1978; Ebberink & de Zwaan, 1980).
From this outline of integrated control of the rates of several rate-controlling
reactions involved in carbohydrate catabolism it is possible to derived a
somewhat generalized scheme indicating some of the major rapid regulatory
influences which are directed towards counteraction of adverse effects of
environmental perturbation on the production of energy in marine invertebrates.
Such a scheme showing some interactions of major regulatory influences is
shown in Figure 4. It is emphasized, however, that any such representation is a
gross over-simplification of the multitude of interactions involved in regulatory
control of carbohydrate catabolism in vivo. Nevertheless, it is suggested that the
scheme embraces a number of regulatory responses which merit further
investigation in studies of the impact of environmental change on marine
invertebrates.
ACCLIMATION, ACCLIMATIZATION, AND ENZYME

INDUCTION
Traditionally, the terms acclimation (in response to a controlled environmental
influence) and acclimatization (in response to changes in the natural
environment) have been applied to the net effect of mechanisms that are directed
towards the counteraction of potentially detrimental effects of environmental
change and the re-establishment of homeostasis at an optimal metabolic level
within the life time of the individual. In contrast, the term adaptation should be
applied to responses achieved through genetic changes that occur in subsequent
generations as a consequence of the environmental change (Duncan, 1976). In
the process of acclimation an immediate response to a change in conditions is
followed by a stabilization period and a new steady state (Levinton, 1982). The
ability of an individual to acclimate successfully to an environmental change
will, however, depend on the magnitude of the stimulus in relation to the
tolerance of the individual. Acclimation and acclimatization are, therefore,
considered here as both coarser and slower controls directed towards
optimization of metabolic function following the rapid metabolic regulatory
responses that have already been discussed.
There is strong evidence to suggest that modulation of kinetic properties of
regulatory enzymes, post-translational modification of enzyme structure, and
enzyme induction are all important metabolic regulatory responses that can be
involved in acclimation and acclimatization. Enzyme induction involves the
synthesis of an enzyme through the intermediate synthesis of specific mRNA
(see e.g. Schimke & Doyle, 1970) and, therefore, involves the genetic material of
eukaryotic cells. The term ‘genetic regulation’ is applied here to those metabolic
regulatory mechanisms involving the genetic material. The most rapid genetic
regulatory control is exerted at the level of induction of enzyme synthesis. The
Fig. 4.—A generalized reaction scheme outlining some of the major regulatory influences
on potential rate-controlling reactions of carbohydrate catabolism in marine invertebrates.
Potential rate-controlling reactions are indicated by heavy arrows and the enzymes
catalysing these reactions are named in the adjacent rectangles. Regulatory influences are
indicated by the circles containing + , for activation effects or − , for inhibitory effects.
Only one mechanism for activation of phosphorylase is included; for discussion of
alternative mechanisms see p. 268. The pyruvate oxidoreductases vary between species
(see de Zwaan & Zurburg, 1981; Livingstone, 1983; Livingstone, de Zwaan, Leopold &
Marteijn, 1983; for discussions of the rôles and phylogenetic distributions of these
enzymes). The pyruvate oxidoreductase and malate dehydrogenase reactions are included
to provide an indication of the metabolic routes for formation of end-products of
anaerobic carbohydrate catabolism. For clarity the contributions of amino acids to these
pathways and the involvement of coenzymes in reactions have been excluded. The
reaction catalysed by phosphoenolpyruvate carboxykinase (PEPCK) is considered to have
regulatory importance in view of the competition between this enzyme and pyruvate
kinase for their common substrate phosphoenolpyruvate (see de Zwaan, 1977 for
discussion of these mechanisms).
slowest genetic regulatory control occurs at the level of inheritance of

structurally or functionally modified enzymes. Post-translational combinations of
monomers of different genetic or allelic origins to form active oligomeric
enzyme molecules can give rise to multiple forms of the enzymes (allozymes).
There are also numerous nongenetic regulatory processes which may operate to
278 JOHN BLACKSTOCK
produce multiple forms of enzymes (isoenzymes). (See Moss, 1979, for a

discussion of multiple forms of enzymes.)
One of the most frequently studied compensatory mechanisms is the
regulatory response of poikilothermic animals to change in environmental
temperature. Many of the earlier definitive marine-orientated investigations of
effects of temperature compensation on enzymes associated with energy-yielding
metabolism have reported studies of fish tissues (see e.g. Hochachka & Somero,
1968, 1973; Hazel & Prosser, 1970; Hochachka & Lewis, 1971; Moon &
Hochachka, 1972; Somero, 1973). The general conclusion to be made from these
investigations was that temperature acclimation could involve the induction of
enzymes and isoenzymes and the modulation of kinetic properties of enzymes by
cellular solutes. Hochachka & Somero (1973) have suggested that shorter time
courses of temperature change may restrict the enzymatic compensation
mechanisms available to the organisms, i.e. enzyme induction may be too slow to
counteract effectively adverse effects of relatively rapid temperature change and,
in the short term, they considered that non-genetic enzyme modification may be
more important. Similar opinions have been expressed in more recent
investigations. Thébault, Bernicard & Le Gal (1980) have shown that the
substrate affinity of lactate dehydrogenase from the tail muscle of the shrimp,
Palaemon serratus, initially acclimated at 12°C, varied as a function of the
period of their subsequent maintenance at 20°C. The time required for
acclimation was approximately three weeks and these authors considered that
enzyme induction was involved in the acclimative regulation and that the more
rapid diurnal changes in temperature experienced by P. serratus under natural
conditions may be primarily compensated for by conformational changes in
enzyme structure.
When more rapid temperature changes (heat shock) are considered there is
strong evidence of a rapid primary genetic response. In the polychaete,
Scolelepis fuliginosa, the application of a rapid increase in maintenance
temperature by 7°C in 10 mins has been shown to result in the formation, in
about 1 hour, of an additional esterase isoenzyme, which is electrophoretically
distinct from any of the pre-existing esterases (Guérin & Kerambrun, 1979).
Changes in isoenzymatic constitution of the esterases of Palaemon serratus
larvae have also been shown to follow thermal shock (Trellu, Ceccaldi, Maggi &
Lassus, 1978).
The mechanisms controlling gene expression in eukaryotes are at present the
subjects of intensive research, particularly in medical scientific disciplines and it
is clear that the processes involved in the regulation of gene activity and the
sequence of events relating environmental stimuli and changes in gene
expression remain little understood (see e.g. Rees, 1981; Darnell, 1982;
MacIntyre, 1982; for further discussion). Induced enzymes may possibly be
structurally and kinetically modified if a previously ‘silent’ gene is expressed and
there is some evidence to suggest that diverse forms of stress may activate such
genes (see e.g. Currie & White, 1981). Hammond, Lai & Markert (1982) have
remarked that in a number of different eukaryotic cells heat shock causes the
synthesis of groups of proteins that are absent prior to the shock. In addition,
they have demonstrated that in rat heart tissue the same group of ‘new’ proteins
are synthesized within 1–1·5 h of the application of heat shock or oxygen
deprivation. They concluded that the stress created an intracellular environment
which stimulated the selective activation of genes, production of new mRNA,
and the synthesis of previously absent proteins.
Induction of enzymes has been associated with effects of a number of other
environmental variables and natural physiological rhythms but in general the
time scales of changes involving the genetic material have been considered to be
somewhat slower than those discussed above. Synthesis of the digestive enzymes
amylase and trypsin in the brine shrimp Artemia salina (Boucher, Laurec,
Samain & Smith, 1976; Samain et al., 1976; Samain, Moal, Daniel & Le Coz,
1981) and in Calanus finmarchicus (Tande & Slagstad, 1982) have been shown
to be influenced by trophic conditions. Induction of enzymes associated with the
mixed function oxygenase (M.F.O.) system are considered to represent a
response which can facilitate metabolism, and hence detoxification, of
potentially harmful aromatic hydrocarbons present in the marine environment.
This mechanism has been shown to be operative in a wide range of marine
invertebrates including molluscs, polychaetes, and crustaceans (Bayne et al.,
1979; Lee, Singer, Tenore & Gardner, 1979; Lee, 1980; Moore et al., 1980).
The regulation of the catalytic activity of enzymes associated with energy-
yielding metabolism is essential for the maintenance of optimal energy
production throughout periods when energy demand fluctuates as a consequence
of natural physiological rhythms e.g. the annual cycles of energy storage and
utilization which are attuned to the reproductive cycle of many marine
invertebrates. Livingstone (1975) has suggested that the production of pyruvate
kinase isoenzymes may account for seasonal fluctuations in the substrate affinity
of pyruvate kinase from mantle tissue of the bivalve Mytilus edulis. On the basis
of this, and a later investigation of seasonal fluctuations in specific activity and
substrate affinity of glucose-6-phosphate dehydrogenase from the
hepatopancreas and mantle of M. edulis, Livingstone (1981) has suggested that
seasonal changes in catalytic activity of regulatory enzymes are more likely to be
due to altered rates of enzyme (or isoenzyme) synthesis than to regulation by
changes in effector concentrations. He suggested that the latter type of
mechanism would be primarily involved in short-term regulation of energy
yielding metabolism.
Demonstration of increased rates of enzyme synthesis requires a measure of the
synthesis of enzyme protein (by measuring the incorporation of radioactively
labelled amino acids) rather than estimates of enzyme activity or kinetic
constants and the required detail of investigation of synthesis has only
infrequently been applied in studies of effects of natural or anthropogenic
environmental change on marine invertebrates. One of the most comprehensive
studies of biosynthesis of a metabolic enzyme in a marine invertebrate has been
280 JOHN BLACKSTOCK
reported by Hand & Conte (1982) who have investigated temporal variations in
the synthesis of cytoplasmic malate dehydrogenase by larval brine shrimp,
Artemia salina, in response to increased salinity. These researchers used a radio-
immuno-electrophoretic technique to estimate the rate of incorporation of
radioactive amino acids into the enzyme protein and demonstrated that there was
an increased rate of synthesis of this enzyme approximately 24 h after the larvae
had been transferred to a high (2·5 M NaCl) salinity medium.
It is clear that acclimative responses to a wide range of changes in both the
external and internal environment can be achieved by both molecular and genetic
regulatory mechanisms. Most investigators agree that modulation of the kinetic
properties of rate-controlling catabolic enzymes is generally more rapid than
synthesis of enzymes (or isoenzymes). Recent advances e.g. investigations of
effects of thermal shock have emphasized, however, that regulatory changes in
gene expression can result in synthesis of proteins which are not present prior to
the stimulus. These events can occur within a time scale which is sufficiently
brief to result in concurrent operation of molecular and genetic mechanisms of
acclimation and may possibly indicate that the gene has a more important rôle in
short term metabolic regulation than has hitherto been suggested. A possible rôle
of cyclic-AMP, the mediator of major hormonal effects on carbohydrate
catabolism, in the regulation of gene expression, has frequently been postulated
(see e.g. Pastan & Perlman, 1972; Steinberg & Coffino, 1979) but no clear
evidence relating cyclic-AMP directly to gene stimulation has been obtained
(Coffino, 1981). At present, therefore, it is generally considered that cyclic
nucleotides are primarily involved in the ‘fine’ regulation of metabolism and the
genetic regulatory mechanisms may be primarily stimulated by the resultant
intracellular substrate concentrations (Schole, 1982).
There is considerable information on acclimative changes in rate-controlling
enzymes associated with energy-yielding metabolism of marine invertebrates and
at present there is discussion of the possible adaptive significance of isoenzymic
differences between groups of marine invertebrates (see also pp. 280–284).
There are obviously difficulties associated with the distinction of molecular and
genetic regulatory responses of marine invertebrates during the course of
acclimatization to environmental change. At the ecological level of many marine
studies the detailed investigation required to resolve the cellular mechanisms
underlying acclimative responses is often not considered to be as important as
the definition of the possible function of the observed response and its impact on
normal functions of the organisms. There are, however, virtually no detailed
marine studies of the evolutionary consequences of metabolic regulatory
acclimative responses and such knowledge is fundamental to our understanding
of adaptations of marine organisms to their environment. Marine research
workers have frequent access to relatively rapid breeding eukaryotes which can,
in many instances, be easily maintained under controlled environmental
conditions. Studies of acclimation and subsequent adaptation of such species to
environmental stimuli may rapidly advance our knowledge of the interrelations
between the successive component mechanisms which regulate metabolism in

response to environmental change.
REGULATION BY ADAPTATION
Adaptive regulatory responses to environmental change are those which occur on
an evolutionary, rather than an ecological, time scale and are considered to be
achieved by genetic selection in generations subsequent to those that are first
subjected to any particular environmental change of sufficient magnitude to
elicit a genetic response. This type of response can thus be considered to
represent the slowest and coarsest metabolic regulatory mechanism. Investigation
of adaptive responses is extremely complex and a combination of genetical,
physiological, biochemical, and biological studies are required if a relation
between environmental change, any subsequent change in genetic constitution of
marine invertebrate populations, and any functional advantage of the genetic
change is to be established.
In recent years a first approach to marine aspects of this problem has been the
assessment of the genetic make-up of marine invertebrate populations using the
frequency and number of electrophoretically separable enzyme variants as
genetic markers. This approach has been most often used for comparative studies
of spatially separated populations of marine invertebrate species belonging to
various phylogenetic groups. Species belonging to a number of genera of
Mollusca have been extensively studied in this way (see e.g. Koehn & Mitton,
1972; Berger, 1973; Snyder & Gooch, 1973; Gaines, Caldwell & Vivas, 1974;
Murdock, Ferguson & Seed, 1975; Campbell, 1978; Lassen & Turano, 1978;
Levinton & Suchanek, 1978; Buroker, Hershberger & Chew, 1979; Gosling &
Wilkins, 1981). Other groups of marine invertebrates that have been studied
include various species of Crustacea (see e.g.Schopf, 1974; Tracy et al., 1975;
Nelson & Hedgecock, 1980; Bulnheim & Scholl, 1981a), Echinodermata (Marcus,
1977), and Coelenterata (Walsh & Somero, 1981). In addition, the
electrophoretic approach has been applied to the differentiation of closely related
species (or sub-species) of marine invertebrates (see e.g. Avise, 1974; Ayala,
1975; Battaglia & Beardmore, 1978; Grassle & Grassle, 1978; Nicklas &
Hoffmann, 1979; Bulnheim & Scholl, 1981b; Gosling & Wilkins, 1981, for
examples of this approach).
There are various problems associated with the interpretation of the data, and
these difficulties are associated with the relatively poorly understood processes
comprising genetic adaptation and with the limitations of the widely used
electrophoretic techniques. It is clear from the results of the investigations
outlined above that allele frequencies are influenced by a number of factors
including the size groups of individuals in the populations (Boyer, 1974;
Chaisson, Serunian & Schopf, 1976) and seasonal changes in energy demand
imposed by natural physiological rhythms (Flowerdew & Crisp, 1976; Koehn &
Immerman, 1981). The genetic heterogeneity in an invertebrate species collected
282 JOHN BLACKSTOCK
at different geographic locations does not necessarily correlate with distance

between locations (see e.g. Gaines et al., 1974). It has also been observed that
latitudinally separate populations of a species may be genetically similar, as
determined on the basis of electrophoretically distinguishable protein (or
enzyme) variants, while their responses to the same environmental change may
be quite dissimilar (Walsh & Somero, 1981). It is widely considered that, under
constant environmental conditions, intraspecific changes will occur as a
consequence of random genetic drift i.e. an apparently non-selective shift in
estimated allele frequencies between generations as a consequence of inevitable
sampling errors when relatively small populations are being investigated (see
e.g. Ford, 1975). In addition, to account for the high frequency of occurrence of
multiple alleles and heterozygosity at gene loci, it has been suggested that most
of the variants were neutral in effect (see Kimura, 1979). At present, however,
there is considerable opinion that genetically determined differences in enzyme
heterogeneity are predominantly adaptive and this conclusion is the basis of the
use of biochemical genetic techniques to assess the impact of natural and
anthropogenic environmental changes on the genetic make up of marine
invertebrate populations (Berry, 1980). Any adaptive significance of the
electrophoretically detectable differences are, however, poorly understood
(Milkman, 1978; Burton, 1983), and the observed changes in the frequency of
individual alleles require further study before they can be related to an effect on
the fitness of the entire phenotype for survival or exploitation of environmental
change (see also Berry, 1980).
The widely used electrophoretic methods separate the protein variants
according to their net charge at the pH of the electrophoretic medium and in the
case of gel electrophoresis improved separations are achieved by utilizing
combinations of charge and molecular sieving effects. The separation achieved
is, therefore dependent on the molecular composition of the protein and the
resolving power of the technique. In addition, genetically determined changes in
amino-acid composition may not significantly affect the net charge on the enzyme
molecule (see e.g. Ferguson, 1980) and non-genetic (post-transcriptional)
enzyme modifications may affect net charge and hence, electrophoretic mobility
(see e.g. Moss, 1979). In spite of these obvious limitations in technique much
useful information on differentation and adaptation of marine invertebrate
populations has been obtained as a consequence of the application of the
electrophoretic method to marine studies. To establish a relationship between
environmental change and a subsequent adaptively significant genetic change it
is essential that environmental monitoring together with assessment of genetic
changes and studies of the functional significance of the observed changes (or
between-population differences) are undertaken in a co-ordinated manner.
Examples of such co-ordinated assessments of potentially adaptive genetic
changes in marine invertebrates are relatively rare in the literature. Several
investigations do, however, merit inclusion. Koehn and his colleagues have
recently reported a detailed investigation of the adaptive significance of variation
at the leucine aminopeptidase (LAP) locus of the marine mussel, Mytilus edulis
(Koehn, Bayne, Moore & Siebenaller, 1980; Koehn & Immerman, 1981; Koehn
& Siebenaller, 1981). Koehn et al. (1980) have indicated that differences in
specific activities of leucine aminopeptidase between estuarine and oceanic
populations were due, at least in part, to a lower concentration of one enzyme
variant in the estuarine bivalves. They related this enzymatic difference to
differences in the salinity normally experienced by each population in their
natural environments. Subsequently, Koehn & Immerman (1981) suggested that
high salinity environments induced high leucine aminopeptidase activity,
probably to facilitate an increase in intracellular free amino-acid concentrations.
Koehn & Siebenaller (1981) have demonstrated differences in the kinetic
properties of the allozymes and have discussed possible physiological
consequences of these differences on amino-acid metabolism and excretion of
nitrogenous compounds by individuals exposed to low salinities.
Studies of acclimation of the M. edulis populations to salinity change have
enabled Koehn et al. (1980) to relate the enzymatic changes to effects of change
in salinity. The demonstration of a particular environmental influence on enzyme
systems that are the subject of genetic investigations is of primary importance in
the establishment of a causal relation between the environmental influence and
subsequent genetic change. A combination of studies of invertebrate populations
from nearshore areas affected to different extents by pollution and experimental
laboratory studies has also been applied by Nevo and his colleagues (Nevo, Perl,
Beiles & Wool, 1981; Lavie & Nevo, 1982) to investigations of the adaptive
significance of allozymic changes. These investigators have shown that
significant differences in the frequencies of phosphoglucomutase (PGM)
isoenzymes between populations of the shrimp Palaemon elegans may confer an
increased resistance to heavy metal pollution to the genotype predominating in
polluted areas. Essentially similar conclusions have resulted from investigation
of effects of copper and zinc on different phosphoglucose isomerase genotypes
of the marine gastropods Monodonta turbinata and M. turbiformis (Lavie &
Nevo, 1982).
In general, studies of genetic changes in marine populations have concentrated
on those enzyme loci which have been found to be the most sensitive for the
demonstration of allele frequency differences between populations. For this
reason the leucine aminopeptidase locus has been most frequently investigated in
Mytilus edulis (see Koehn et al., 1980). The highly polymorphic esterases, and
the glycolytic enzymes phosphoglucose isomerase and phosphoglucose mutase
also tend to be prominent in marine studies. Rate-controlling enzymes e.g.
phosphofructokinase, pyruvate kinase associated with energy-yielding
metabolism have an extremely important rôle in the regulation of energy
production to meet the requirements imposed by a wide variety of natural
processes and environmental stimuli. Such enzymes tend to be extremely
susceptible to non-genetic modification. This can undoubtedly be reflected in
changes in their electrophoretic mobilities and, therefore, decreases their
284 JOHN BLACKSTOCK
usefulness as genetic ‘markers’. Investigation of genetically directed isoenzymic

variation in such enzymes, therefore, presents considerable difficulties. Different
properties of isoenzymic forms of this group of enzymes have, however, been
indicated (see e.g. Hochachka, 1972; Livingstone, 1975; Guderley et al., 1976)
and it has been suggested that this group may be particularly sensitive to genetic
selection (Hochachka & Somero, 1973). In view of the sensitivity of the
regulation of carbohydrate catabolism to environmental stimuli, however, much
useful information relating short-term and long-term regulatory responses of
individuals and populations to environmental change may be derived from
appropriately co-ordinated environmental, biochemical, and genetic studies.
Other enzymes involved in carbohydrate catabolism, but generally considered
to catalyse ‘non-regulatory’ reactions, are considered to exist in genetically
determined isoenzymic forms e.g. lactate dehydrogenase and, in those
invertebrates that utilize the ‘succinate’ pathway of anaerobic catabolism, malate
dehydrogenase. Changes in allozymic frequencies of the latter enzyme have been
considered to indicate adaptation of the opportunistic polychaete, Capitella
capitata, to changed environmental conditions (Grassle & Grassle, 1974). In
earlier studies malate dehydrogenase activities in the polychaete, Neanthes
arenoceodentata, were observed to increase in response to lowered dissolved
oxygen concentrations (Cripps & Reish, 1973). Pearson & Blackstock (1984)
have also observed increased malate dehydrogenase activities in groups of both
the non-opportunistic polychaete Glycera alba and the opportunistic Capitella
collected from organically enriched sediments. The greatest magnitude
(approximately 3-fold) of difference in malate dehydrogenase activities was
found between groups of Glycera alba from sediments beyond the area of
influence of the organically rich inputs and those collected from sediments which
were considerably organically enriched. In Capitella capitata only approximately
1·5-fold variations in mean malate dehydrogenase were found between groups.
In Glycera alba increases in malate dehydrogenase activity have been observed
within 24 h of experimental lowering of oxygen concentrations (to <1 mg·l−1) in
laboratory aquaria. In contrast, relatively little enzymatic response was observed
in groups of Capitella capitata subjected to similar changes in dissolved oxygen
concentrations (see Fig. 5; Blackstock, unpubl.). It is possible that the different
enzymatic responses of Glycera alba and Capitella capitata may relate to their
very different life histories and hence genetic plasticity. The longer lived, less
genetically plastic species may possibly require to rely more on rapid individual
responses to ensure survival of the species following environmental perturbation.
CONCLUDING REMARKS ON METABOLIC

REGULATORY RESPONSES
In the introduction to this section it was stated that the various levels of
metabolic regulatory response to environmental changes were interrelated and
the integration of the rapid metabolic adjustments, acclimative and adaptive
Fig. 5.—Mean malate dehydrogenase activities (±SE of the mean) in crude extracts of the
polychaetes Glycera alba and Capitella capitata during lowering of dissolved oxygen
concentrations in laboratory aquaria: the results are based on analysis of 8 to 16 C.
capitata and 4 to 7 G. alba at each time.
responses is emphasized throughout the various sections. Advances in genetic

studies and, in particular, evidence of relatively early involvement of the genome
in metabolic regulation have, however, resulted in an increased awareness of the
relatedness of the various levels of metabolic response. In Figure 6 some levels of
interaction between genetic and cellular regulatory mechanisms are suggested.
Many excellent investigations have contributed valuable knowledge of
mechanisms operating at the various levels of regulation of energy-yielding
metabolism and such knowledge is fundamental to our understanding of the
relations between individuals, populations and their environments. There have
been, however, extremely few investigations directed towards integrated study of
the relationships between environmental change and all three levels of response
and the sequence of adaptive-regulatory interactions shown is, therefore,
tentative. In fact Walsh & Somero (1981) have emphasized that no marine
species has been studied from the viewpoint of integration of rapid, acclimative
and adaptive responses to environmental change, and these investigators have
reported an investigation of relations between physiological, biochemical and
genetic aspects of temperature adaptation in the anemone, Metridium senile. In
the author’s laboratory comparative studies of regulatory responses of
polychaetes to environmental change are continuing in co-ordination with
environmental, biological, physiological, and genetic studies and it is suggested
that this is a further approach from which useful information relating
environmental change to subsequent genetic constitution of marine invertebrates
may be obtained.
As in studies of the impact of natural environmental change or pollutants on
individual metabolic regulatory responses, the selection of ‘target’ organisms is
crucial to the success of any integrated study of effects of environmental
influences on all three levels of response. In the natural marine environment
286 JOHN BLACKSTOCK
Fig. 6.—Generalized scheme indicating some interactions of molecular and genetic

regulatory responses to environmental stress.
conditions at any given time are determined by complex interactions of variable

physical, chemical and biological factors, and it is clearly difficult to resolve
possible causal influences that elicit major metabolic regulatory responses. The
careful examination of the potential usefulness of various species as target
organisms is, therefore, essential and in the subsequent sections this problem will
be considered in some detail, with particular reference to some ecological
influences on the sensitivity of various widely studied groups of invertebrates to
natural and anthropogenic environmental influences.
SENSITIVITY OF INVERTEBRATES TO
ENVIRONMENTAL CHANGES—SOME ECOLOGICAL
CONSIDERATIONS
All organisms exist in dynamic equilibrium with their natural environment and
are adapted to maintain homeostasis within the range of variation that normally
occurs in that environment. The relations between environmental fluctuations,

natural, physiological and biochemical rhythms, and the magnitudes and time
courses of metabolic responses to resultant fluctuations in energy demand are
extremely complex. The ability of an organism to counteract successfully
potentially damaging effects of a particular environmental change will, however,
depend to some extent on the relative magnitude of the change in comparison
with the limits of environmental variation that the organism usually experiences.
In addition, our ability to ascribe metabolic regulatory changes to effects of
particular environmental influences depends on the magnitude of the response in
relation to the amplitude of ‘baseline’ variation in that response as a consequence
of fluctuations in energy demand imposed by natural physiological cycles and
behavioural characteristics of the organism.
In this section the effects of a selection of important natural influences on
metabolic regulatory responses of marine invertebrates are examined with the
overall objective of assessing the relationships between ecological characteristics
of the invertebrates and their biochemical sensitivity to environmental changes
of greater magnitude than those that would be considered to represent ‘normal’
environmental variation. Comparative assessments of effects of particular
environmental stresses on various species of marine invertebrates are emphasized
in an attempt to establish the consistency, or inconsistency, of such relationships.
Emphasis is also directed towards studies of groups of invertebrates e.g. bivalve
molluscs, polychaetes, and crustaceans that are most frequently used as target
organisms in investigations of the impact of pollutants in the nearshore marine
environment.
HABITAT
The most contrasting habitats of nearshore marine organisms are the intertidal
and sublittoral environments, and some of the major differences in impact of
natural and anthropogenic influences on invertebrates in each of these
environments are summarized in Figure 7. Intertidal invertebrates are, in general,
subjected to considerable natural environmental fluctuations associated with the
tidal cycle and its consequences in terms of wide temperature fluctuations,
regular periods of exposure to the atmosphere and physical effects of wave
action. In addition, in shallow water, fluctuations in temperature, salinity and
light intensity are generally considerable and in comparison natural conditions in
sublittoral environments are relatively constant. Relative effects of any
individual pollutant in such areas will, however, depend on the major mode of its
transmission and relations between pollutant input and metabolic regulatory
responses of invertebrates are, therefore, complex.
One of the most widely accounted metabolic capabilities of marine
invertebrates is their ability to survive for relatively long periods in the absence
of oxygen (Von Brand, 1946). This ability and its energetic consequences have
been investigated in many marine invertebrates including bivalve molluscs (see
288 JOHN BLACKSTOCK
Fig. 7.—The relative impact of various natural and anthropogenic environmental

influences on intertidal and sublittoral invertebrates: differences between sublittoral and
intertidal environments are indicated on the basis of decreasing impact from the filled
arrows, to the outline arrows, to the linear arrows, to the broken arrows.
de Zwaan, 1977, for review), crustaceans (Barnes, Finlayson & Piatigorsky,

1963; Zebe, 1982) and polychaetes (see Scheer, 1969, for review of carbohydrate
catabolism in polychaetes). The ability to survive periods of anoxia is clearly of
ecological advantage to those invertebrates which regularly experience anoxic
conditions. In the intertidal zone anaerobic metabolism is associated with periods
of limited oxygen availability at low tide, when animals are confined to burrows,
tubes or interstitial refuges or, in some species, it is primarily a consequence of
valve closure to isolate tissues and fluids from the atmosphere to prevent
desiccation. Under such conditions internal oxygen supplies become limited. In
sublittoral environments anoxia may result from the deposition of organically
rich material on sediments with the creation of a biological oxygen demand
(B.O.D.) particularly in deep basins where there is little water exchange near the
sediment-water interface. The ability of marine invertebrates to survive periods of
anoxia and to rapidly re-establish homeostasis after such periods is achieved by
the net effects of a number of biochemical, physiological, and behavioural
adaptations which vary considerably between different species, even within
closely related phylogenetic groups. The continued production of energy for
maintenance of essential functions is achieved in facultatively anaerobic marine
invertebrates by means of improved efficiency of energy production compared
with that achieved by the classical Embden-Meyerhof glycolytic pathway
(glycogen′ lactate) which operates in vertebrate muscles. These biochemical
mechanisms have been extensively studied in marine invertebrates, particularly
bivalve molluscs and polychaete worms (for further details see Simpson &
Awapara, 1966; Stokes & Awapara, 1968; Hochachka & Mustafa, 1972; de
Zwaan & Zandee, 1972a; Hochachka, Fields & Mustafa, 1973; Zebe, 1975; de
Zwaan, 1976, 1977; Schroff & Schöttler, 1977; Dales & Warren, 1980; Ebberink
& de Zwaan, 1980; Felbeck & Grieshaber, 1980; Warren & Dales, 1980;
Zurburg & Kluytmans, 1980; Schöttler & Weinhausen, 1981; Livingstone, 1983).
Equally important and phylogenetically widespread characteristics facilitating

survival of periods of anoxia are the adaptations of respiratory pigments to
regulate the internal oxygen supply and the transfer of oxygen from body fluids
to tissues when external oxygen supplies are depleted. Extensive investigations of
the properties and functional significance, in environmental terms, of these
pigments have been reported by various groups of investigators (Mangum, 1970,
1973, 1976, 1977, 1980; Mangum & Carhart, 1972; Mangum & van Winkle,
1973; Garlick & Terwilliger, 1974, 1975, 1977, Mangum et al., 1975; Weber,
1975, 1978, 1980; Wells & Dales, 1975; Wells & Warren, 1975, 1982; Weber,
Sullivan, Bonaventura & Bonaventura, 1977; Weber, Bonaventura, Sullivan &
Bonaventura, 1978; Warren, Wells & Weber, 1981). Few marine invertebrates
can be considered to be genuine facultative anaerobes, because in general the
periods of anoxic tolerance are limited. Increased efficiency of anaerobic
catabolism and conservation of internal oxygen supplies, together with
behavioural responses designed to minimize energy utilization or maximize the
absorption of small amounts of oxygen from hypoxic media all make important
contributions to the capabilities of various species to survive limited periods of
anoxia.
A comparison of the capability of various marine invertebrates to survive
periods of experimentally induced anoxia can indicate how far this capability can
be related to the general nature of their habitats and to what extent this capability
may be determined by other characteristics of the species. In Figure 8 results of
several investigations of anoxic tolerance of a selection of marine invertebrates
are summarized. The results shown have been taken from studies by Dales (1958),
Theede, Ponat, Hiroki & Schlieper (1969), Theede, Schaudin & Saffe (1973),
Augenfield (1978), Ellington (1979), and Groenendaal (1980). In each of these
investigations the test organisms were maintained immersed in anoxic sea water;
the individuals were, therefore, not subject to desiccation. Many other studies of
anoxic tolerance of various species of marine invertebrates have been made under
a wide range of experimental conditions. It is considered, however, that the
results summarized in Figure 8 present a valid comparative assessment of the
anoxic tolerance of various invertebrate groups and provide an adequate
background for this discussion.
The relatively well-developed ability of the anemone Haliplanella luciae to
survive some 12 days of anoxic conditions was suggested by Ellington (1979) to
be a possible consequence of the adaptation of this intertidal species to exposure
to hypoxic conditions in tidal pools at low tide. Sassaman & Mangum (1972)
also found high anoxic tolerance (>11 days survival) in a burrowing form of
intertidal anemone, Haloclava producta. The periods of anoxic tolerance were
considerably longer than would be necessary for survival of periodic anoxic
conditions at low tide but Sassaman & Mangum (1972) concluded that, in general,
species associated with environments characterized by low or variable oxygen
concentrations could survive much longer periods or anoxia than they would
encounter in their natural environment.
290 JOHN BLACKSTOCK
Fig. 8.—Period of survival of some marine invertebrates in anoxic sea water: see text for
sources of data.
The crustaceans Carcinus maenas and Crangon crangon are relatively

intolerant of anoxic conditions and Theede et al. (1969) indicated that the anoxic
tolerance of relatively active species declined as metabolic rate increased. There
have been relatively few biochemical investigations of the utilization of
anaerobic metabolic pathways as an anoxic survival mechanism in Crustacea.
Achituv, Blackstock, Barnes & Barnes (1980) found that small amounts of
succinate and lactate were produced in larvae of the cirripede Balanus
balanoides during 4 h of anoxia, but protein and lipid were the major metabolic
substrates. In recent studies Zebe (1982) has found that the burrowing intertidal
shrimps Upogebia puttegensis and Callianassa californiensis survived
approximately 30 and 60 h anoxia, respectively. He also attributed this difference
to differences in metabolic rate between these species.
The difference in anoxic tolerance between the species of bivalve molluscs
shown in Figure 8 cannot be explained in terms of the differing oxygenation of
subtidal and intertidal habitats. The species shown, Cyprina islandica, Mytilus
edulis, and Cardium edule were all investigated by Theede et al. (1969) and it
was suggested that the exceptionally high tolerance exhibited by Cyprina
islandica was related to its habitat in sublittoral soft muds that are frequently
anoxic. The relatively high tolerance of Mytilus edulis was considered to relate to
the ability of this species to survive atmospheric exposure at low tide and the
relatively wide thermal and salinity variations associated with the littoral or
shallow sublittoral environments. Of the three species of bivalves, Cardium
edule was the most sensitive to anoxia and Theede et al. (1969) suggested that
the sensitivity may be associated with the adaptation of this intertidal species to
comparatively constant conditions in its normal habitat at a depth of several
centimetres in soft substrata. Clearly the relative anoxic tolerances of these three
species are determined by the net influence of a number of ecological and
environmental factors relevant to their survival in very different environmental
situations. From investigations of isolated tissues of several species of bivalve

molluscs Theede et al. (1969) have concluded that the period of survival of the
tissues in anoxic sea water was related to their capacities to utilize small
quantities of oxygen, to reduce their energetic requirements and to meet surplus
energetic demands from anaerobic metabolism.
Of the polychaetes included in Figure 8, Owenia fusiformis was most resistant
to anoxia and it is of interest to note that Dales (1958) found a relatively high
glycogen concentration (21.0 mg·g−1 fresh wt of total tissue) in O. fusiformis
from an intertidal environment. Augenfield (1978) has investigated the glycogen
contents of various species of polychaetes from different levels of the intertidal
zone in the vicinity of San Juan Island, Washington, on the west coast of the
U.S.A. He found that glycogen concentrations were generally higher in species
from the upper intertidal K zone than in those found near the low water mark and
he concluded that mean glycogen concentrations were correlated with the
probability of anoxic conditions occurring in the natural habitat of each of the
species examined. Many species of polychaetes have very varied littoral and
sublittoral distributions in different geographical areas and it is, therefore, difficult
to make valid interspecies comparisons of relations between glycogen
concentration and habitat on a wider geographic scale. In addition, glycogen
concentrations can vary considerably in polychaetes as a consequence of cyclic
fluctuations in energy requirements imposed by natural rhythms e.g. during
reproductive cycles (de Vooys, 1975) and in interspecies comparisons this source
of variation must be taken into consideration. Interpretation of the relationship
between glycogen concentration and anoxic tolerance of polychaetes is further
complicated by the knowledge that a large proportion of the total glycogen may
not be catabolised during prolonged anoxia and may not be readily available as a
substrate for anaerobic metabolism (see e.g. Dales, 1958; Scheer, 1969). The
sequence of anoxic tolerance of polychaetes shown in Figure 8 does, however,
appear to be at least superficially related to the frequency and duration of anoxic
periods in the habitat of each species. Arenicola marina has been found to be
associated with relatively variable intertidal habitats and has some tolerance of
effects of sulphide (Groenendaal, 1980). Capitella capitata is generally found in
sublittoral habitats but is often found in large numbers in organically enriched
sediments where conditions are frequently anoxic (Reish, 1973; Pearson &
Rosenberg, 1978) and a relatively high tolerance of low oxygen concentrations
would, therefore, be of ecological importance to this species. A series of
investigations of ecophysiological characteristics of several species of the
polychaete genus Nereis have also shown that tolerance of anoxia is greatest in
the species, N. diversicolor, which was considered to be found in a more variable,
more frequently anoxic environment than the somewhat less anoxia-tolerant N.
virens and N. pelagica (Theede et al., 1973). There is, therefore, evidence of a
general tendency for relatively higher anoxic tolerance in polychaetes from
comparatively variable environments, e.g. the intertidal zone and those
sublittoral habitats that are intermittently anoxic.
292 JOHN BLACKSTOCK
Within the classes of invertebrates that have been considered in this section
there are discernible trends towards higher anoxic tolerance in the least mobile
species i.e. those with generally lower rates of energy utilization, and in the
species that are adapted to survive in relatively variable or extreme environments.
It is, therefore, suggested that the capability to survive periods of anoxia will relate
primarily to a combination of these characteristics. The extents to which these
characteristics may relate to the magnitudes of their metabolic regulatory
responses to experimentally-induced changes in environmental conditions are
discussed below.
Responses of the bivalve mollusc, Mytilus edulis, to a wide range of natural
and experimentally induced environmental changes have been extensively
reported. The polychaete Arenicola marina is relatively tolerant of anoxia but is
generally subject to somewhat less environmental variability than Mytilus edulis.
As stated earlier (pp. 272–274) the adenylate energy charge may provide a
quantitative index related to the energetic condition of the cell. It is of interest to
compare the effects of anoxia on the adenylate energy charge in these species to
obtain an indication of a relatively rapid metabolic regulatory response of each
species to this environmental perturbation. In Figure 9 the effects of anoxia on
the adenylate energy charge and ATP content of total tissues of M. edulis
(exposed to air, from Wijsman, 1976) and Arenicola marina (from Surholt,
1977) are compared. It is evident that the most rapid change in adenylate energy
charge was observed in A. marina which is considered to be the more sensitive
of the two species to anoxic stress and may be considered to be the more mobile
species. Surholt (1977) suggested that the ability to maintain a stabilized energy
charge was not well developed in Arenicola, possibly as a consequence of the
low phosphagen content of the body-wall musculature. It is, therefore, of interest
to compare effects of anoxia on several more closely related species belonging to
the same phylogenetic group. Schöttler (1979) has compared the effects of
anoxia on adenylate energy charge values in three species belonging to the
polychaete genus Nereis (see Fig. 10). In N. pelagica, which was least tolerant of
anoxia, the adenylate energy charge decreased from 0·88 to 0·66 during 36 h
anoxia, and by this time 40% of the animals had died. N. virens and N.
diversicolor both survived at least 72 h under anoxic conditions and the initial
decline in adenylate energy charge values was slower than that found in N.
pelagica. It is, therefore, suggested that in those species of invertebrates that are
most sensitive to a particular environmental perturbation the metabolic
regulatory response to that perturbation may possibly be of greater magnitude
than in somewhat less sensitive species. In general, however, adenylate energy
charge values tend to stabilize at minimum values of approximately 0·6–0·7 and
values of 0·72 were found by Wijsman (1976) when he analysed Mytilus edulis
which had died during his anoxic tolerance experiments. In addition, initial
values of adenylate energy charge can vary considerably in relation to natural
metabolic fluctuations in marine invertebrates, see e.g. Båmstedt & Skjoldal
(1976). Absolute values of energy charge are, therefore, unlikely to be a reliable
Fig. 9.—Effects of anoxia on the ATP content and adenylate energy charge in Mytilus edulis
(′ and ′, respectively) and Arenicola marina (′ and ′, respectively) from data reported
by Wijsman (1976) and Surholt (1977).
index which can readily be interpreted in terms of the impact of environmental
perturbation on marine invertebrates. The initial rate of decline of energy charge
values on exposure of an organism to an environmental stress may, however, be
a more reliable early indicator of subtle effects of the stress on energy-yielding
metabolism.
Catabolism of metabolic substrates, e.g. carbohydrate, lipid and protein, is
necessary for the production of energy to maintain essential physiological
processes and it is suggested that any deleterious change in the ability of an
organism to produce energy may be rapidly reflected in the sequences of enzyme
reactions that comprise catabolism. There have been relatively few studies of
rapid, possibly hormonally mediated, enzymatic changes that may be indicative
of changes in the rate of energy production by marine invertebrates in response
to external environmental stimuli. In general, anaerobic catabolism is associated
with lower rates of energy production than the corresponding aerobic processes,
and in the polychaete Glycera dibranchiata all muscular activity has been
observed to cease on immersion in anoxic sea water (Mangum, 1970) indicating
conservation of energy under these conditions. In Glycera alba, cessation of
muscular activity under anoxic conditions has also been observed and is
accompanied by a rapid lowering of maximal activity of the enzyme,
phosphofructokinase, to about 35% of the activities found in control animals
(Blackstock, 1978a). A general correspondence between maximal
phosphofructokinase activity and apparent intensity of muscular activity has also
been observed in other species of polychaetes (see pp. 297, 299). Study of the
relation of rapid changes in enzyme activities to changes in the rate of energy
production is difficult, but it is suggested that with appropriate further
investigations, the rapid modulation of the activities of enzymes associated with
294 JOHN BLACKSTOCK
Fig. 10.—Effects of anoxia on adenylate energy charge in three species of Nereis: ′ , N.

virens; ′ , N. diversicolor; ′ , N. pelagica; from data reported by Schöttler (1979).
regulation of carbohydrate catabolism may provide the earliest reliable

biochemical indication of effects of environmental changes on the production of
energy by sensitive species of marine invertebrates.
In this section some rapid metabolic regulatory responses of invertebrates from
a habitat that may be considered to be ‘extreme’ or highly variable in certain
respects have been compared with the responses of species from a generally less
variable habitat. Possible correlations between environmental stability and the
genetic variability of fauna have been discussed frequently (see e.g. Ayala &
Valentine, 1978; Grassle & Grassle, 1978; Nelson & Hedgecock, 1980). It is now
clear that genetic variability may also relate to a number of ecological factors
including food supply, population size, reproductive behaviour and larval
dispersal capabilities of species from various habitats. Nelson & Hedgecock
(1980) have assessed relationships between a variety of ecological characteristics
and heterozygosity in 44 species of decapod crustaceans. They concluded that
environmental heterogeneity and trophic diversity were two of the most
important influences on genetic variability. Grassle & Grassle (1978) have
suggested that studies of genetic variation should be co-ordinated with studies of
life histories and population structure. It is suggested that studies of the relative
magnitudes of metabolic regulatory responses of invertebrates from various
habitats to environmental change should also be co-ordinated with genetic and
population studies. This approach would provide further information on the
relations between habitat, genetic variability and sensitivity of invertebrates to
environmental change and would considerably improve our understanding of the
dynamic equilibrium between invertebrates and their natural environment.
NATURAL PHYSIOLOGICAL RHYTHMS

In the majority of marine invertebrates cyclical fluctuations in energy demand
are imposed by natural physiological rhythms of which reproductive cycles and,
in Crustacea, the moulting cycle, have been most frequently studied. These
rhythms are regulated in a complex manner by endogenous factors controlling
cyclical biochemical changes within the organism (see e.g. Giese, 1959; Travis,
1957) and are also influenced by external environmental conditions e.g.
temperature, salinity, trophic conditions. Metabolic activity is regulated to satisfy
the fluctuations in energetic requirements imposed by these natural processes
which are responsible for considerable regular variation in those biochemical
systems that have potential as indicators of metabolic regulatory responses to
environmental perturbation. In this section the influence of natural rhythms on
metabolic regulatory responses is examined with the major objective of assessing
the contribution of such rhythms to ‘baseline’ variation in the measured responses.
In most invertebrates reproduction is associated with regular cycles of storage
and utilization of metabolic substrates to provide energy and metabolic
intermediate compounds required for syntheses of gametes (Giese, 1966).
Regular changes in the composition of marine invertebrate tissues as a
consequence of such storage cycles, have frequently been reported in bivalve
molluscs (Ansell & Trevallion, 1967; Ansell, 1972, 1974a, b, c, 1975; de Zwaan
& Zandee, 1972b; Comely, 1974; Ansell, Frenkeil & Moueza, 1980; Stephen,
1980; Zandee, Kluytmans, Zurburg & Pieters, 1980) and it is clear that seasonal
variations in carbohydrate contents of various tissues are a prominent feature of
these compositional changes. It is also clear that the regular changes in
biochemical composition reflect seasonal changes in availability of food as well
as reproductive influences. Moreover metabolic regulatory responses which are
potential indicators of effects of environmental perturbations on carbohydrate
catabolism reflect the net cyclical changes in energy demand (Livingstone &
Bayne, 1974; Chambers et al., 1975; Gabbott, 1975, 1983; Livingstone, 1975,
1981; Gabbott, Cook & Whittle, 1979; Kluytmans, Zandee, Zurburg & Pieters,
1979, 1980; Gabbott & Head, 1980; Zandee, Holwerda & de Zwaan, 1980; Zaba,
Gabbott & Davies, 1981).
Cycles of storage and utilization of metabolic substrates in association with
the reproductive cycles of polychaetes have received less attention. Dales (1957)
has found seasonal differences in lipid concentrations in the polychaetes
Amphitrite johnstoni and Nereis diversicolor. De Vooys (1975) has related a
rapid decrease in glycogen concentrations in muscle and gut to the production of
gametes in Arenicola marina, and has reported that young A. marina contained
higher glycogen concentrations than mature worms. In contrast, de Jorge &
Petersen (1969) found that mature individuals of the polychaete species
Telepsavus costarum contained higher glycogen concentrations than the
immature individuals. In studies done at the author’s laboratory seasonal changes
in total carbohydrate content in Nereis virens and Melinna palmata have been
296 JOHN BLACKSTOCK
found but conclusive evidence of a relationship between gametogenesis and

carbohydrate contents of these species has not been obtained (Blackstock, Barnes
& Barnes, unpubl.). It has also been found that temporal fluctuations in maximal
activities of certain glycolytic enzymes, particularly phosphofructokinase and
pyruvate kinase are consistent with metabolic responses to fluctuations in energy
demand during the reproductive cycles of several species of polychaetes
(Blackstock, unpubl). Some of the results of these investigations are discussed
later (see pp. 295–297).
In various species of Crustacea regular cycles of storage and utilization of
major metabolic substrates have also been reported. In this group it has been
widely reported that lipid is the major metabolic substrate utilized in gonad
production and that carbohydrate concentrations are relatively low (see e.g.
Raymont, Austin & Linford, 1966, 1967; Heath & Barnes, 1970; Morris, 1971,
1973; Båmstedt & Matthews, 1975; Båmstedt, 1976, 1978, 1980; Falk-Petersen,
1981). Carbohydrate catabolism is, however, intimately involved in the moulting
cycle (Heath & Barnes, 1970; Hohnke & Scheer, 1970; Parvathy, 1971, 1972). In
the cirripedes Balanus balanoides and B. balanus, however, Barnes, Barnes &
Finlayson (1963) have reported six- to ten-fold increases in glycogen content
concurrent with increased availability of food in the spring and early summer.
Reproductive cycles have been associated with large seasonal fluctuations in
adenylate energy charge of Euchaeta norvegica (Båmstedt & Skjoldal, 1976) and
Meganyctiphanes norvegica (Skjoldal & Båmstedt, 1976). In addition, changes
in activities of various enzymes associated with carbohydrate catabolism have
been demonstrated during the moulting cycle of several species of Crustacea e.g.
glycogen phosphorylase activity has been found to reach maximal values in
muscle and integument during the early intermoult phase in the decapod
Hemigrapsus nudus (Hohnke, 1971) and activities of the glycolytic enzyme
pyruvate kinase have been shown to increase during the premoult and postmoult
phases in the crayfish Orconectes limosu (Lesicki, 1977).
It is clear that in the three major groups of marine invertebrates which have
been discussed there is a distinct influence of natural physiological rhythms on
those metabolic regulatory responses that may be generally classified as rapid. In
addition, adaptations of marine invertebrates to fluctuations in energy demand
imposed by natural physiological (and environmental) rhythms are of great
importance in the maintenance of optimal energy production. Thus, the
regulation of catalytic activity by seasonal changes in enzyme (or isoenzyme)
synthesis may have considerable importance in the regulation of catabolism to
meet these demands (see also p. 278).
In the natural environment temporal metabolic regulatory changes will reflect
net changes in energy demand imposed by a number of ecological cycles of
varying periodicity. It is, therefore, difficult to resolve the impacts of the various
component rhythms on ‘baseline’ variation of metabolic regulatory responses to
environmental stimuli of invertebrates collected from the natural environment.
One useful approach to this problem is the comparison of seasonal variations in
enzymatic activity in groups of invertebrates that have different modes of

reproduction. This approach has been applied by the author to various
polychaetes that have different reproductive characteristics. Although most
species of polychaetes exhibit cyclical rhythms of reproductive activity there are
many that are monotelic and in individuals of such species regular metabolic
rhythms associated with reproduction may not be apparent for much of their life
span. Monotelic reproduction is a characteristic of polychaetes belonging to the
genus Glycera which have been considered to have a relatively short period of
reproductive activity near the end of their life span of several years (Klawe &
Dickie, 1957; Ockelmann & Vahl, 1970). A large majority of Glycera collected
from the natural environment may, therefore, be considered to be immature.
Melinna palmata is a sublittoral ampharetid polychaete which is common in soft
mud sediments in various sea lochs in the west of Scotland. The temporal pattern
of ovarian and oocyte development in this species is indicative of an annual
reproductive cycle similar to that observed by Hutchings (1973a, b) in the closely
related species Melinna cristata. Both Glycera alba and Melinna palmata were
collected from the same location (Blackstock, 1978a) in Loch Eil in the west of
Scotland during 1976–1977 and the seasonal fluctuations in phosphofructokinase
activity in these species was compared (Fig. 11). The seasonal changes in
phosphofructokinase activity in Glycera alba are irregular while in Melinna
palmata a regular pattern of change was found with maximum activity being
observed after spawning which occurs at the beginning of the year. By February
1977, phosphofructokinase activity in M. palmata had increased to
approximately 30% of the maximum activity found in February, 1976. There was
an approximately 3-fold variation in phosphofructokinase activity in Glycera
alba during the year while in Melinna palmata the variation was in excess of 10-
fold. The temporal changes in phosphofructokinase activity in Glycera alba may
relate to a high sensitivity of this enzyme to changes in energy demand imposed
by natural fluctuations in environmental conditions affecting G. alba because, in
this species, phosphofructokinase activities are considered to provide a sensitive
indication of effects of certain environmental changes (Blackstock, 1978a, 1980a,
b). It is, therefore, of interest to note that in the G. alba activities of pyruvate
kinase varied much less during the year (maximum variation ′ 1·4 fold). In
Melinna palmata pyruvate kinase activities varied by a factor of more than 10
and changed with season in a regular manner consistent with a metabolic
regulatory response to changes in energy demand imposed by the annual cycle of
reproductive activity.
In the opportunistic species of polychaete Capitella capitata differences in
activities of enzymes associated with carbohydrate catabolism have been found at
different stages of the reproductive cycle in female worms (Blackstock &
Pearson, 1979). The individuals used in these studies had fresh weights of
approximately 20 mg at the earliest stage of ovarian development (Group A, see
below) increasing to approximately 30 mg in fully gravid individuals. The fully
developed oocytes were some 200 μ m in diameter and breeding cycles of 5–6
298 JOHN BLACKSTOCK
Fig. 11.—Seasonalchanges in relative activities of phosphofructokinase in Glycera alba

(′ ) and Melinna palmata (′ ).
weeks were observed in the experiments. The individuals were, therefore,
somewhat larger than any of the sibling Capitella species described by Grassle &
Grassle (1976) and the development of oocytes in the laboratory populations
were relatively synchronous. Although the population was not examined for
allele frequency differences, it was considered to be highly unlikely that widely
differing (in terms of reproductive cycle) sibling species were inadvertently
grouped together. In Figure 12 differences in mean activities of
phosphofructokinase (expressed as activity relative to the maximum mean
activity) between groups of C. capitella which were at different stages of the
reproductive cycle are shown. The earliest stages of reproductive development
are represented by Group A in which the ovaries were too small to permit
samples of ovarian oocytes to be obtained. In Group B, almost fully developed
ovarian oocytes were present, but none had been released into the coelomic
fluid. In Group C, which represents the condition immediately before spawning
free oocytes, fully developed, were present in large numbers in the coelomic
fluid and in Group D, immediately after spawning the eggs were retained in a
brood-tube surrounding the adult, and hatching was imminent. In Group C, the
sexually ripe worms were considerably less active than at other stages of
reproductive development and it is considered that the low phosphofructokinase
activity observed in this group may relate to a decrease in muscular activity. It is,
therefore, clear that in addition to fluctuations in energy demand as a direct
consequence of energy requirements for gametogenic activity, behavioural
adaptations associated with the reproductive cycle in invertebrates have
considerable importance in determining their energy requirements.
The observation that in certain polychaetes regular cyclic changes relating to
metabolic regulatory responses occur in relation to natural physiological cycles
may be applied to some other groups of marine invertebrates, e.g. Livingstone
(1975) has reported a regular, approximately two-fold seasonal change in
pyruvate kinase activities in adductor muscle of the bivalve Mytilus edulis.
Similar amplitudes of seasonal change have been found for pyruvate kinase
activities in tissues of the bivalve Donax vittatus which is found in sandy
substrata near the mean low water level in the west of Scotland (Blackstock &
Ansell, 1981). Various other studies of seasonal fluctuations relating to
Fig. 12.—Relative changes in mean phosphofructokinase (PFK) activity during the

breeding cycle of Capitella capitata: the mean enzyme activities were calculated as ratios
of mean activity: maximum mean activity during the breeding cycle.
metabolic regulatory responses have been made (see papers quoted on p. 294) but
there have been insufficient directly comparable investigations to permit a
confident comparative assessment of the enzymatic data from numerous
investigations. In addition, the relations between changes in maximal enzyme
activities and net changes in flux of metabolites will vary between species and,
as a consequence of seasonal variations in kinetic properties of regulatory enzymes
(see e.g. Livingstone, 1975), within the same species at different times of the year.
In general, however, the limited comparison of temporal enzymatic changes in
Glycera alba, Melinna palmata and Capitella capitata together with the
evidence of regular temporal variations associated with reproductive and
moulting cycles in a wide variety of invertebrates is considered to indicate that in
the natural environment physiological rhythms make an important contribution to
the temporal variation in metabolic regulatory responses to environmental
change.
In the selection of invertebrates for target organisms for the biochemical
assessment of effects of environmental perturbations ‘baseline’ variation will be
reduced, and hence reliability of detection of environmental effects will be
increased, if the target organisms are immature individuals in which the
influence of reproductive cycles is considered to be negligible. If reproductively
active target organisms are to be used all the test organisms must be at the same
stage of reproductive development. In the case of Crustacea the stage of the
moulting cycle must also be taken into consideration. It is well known that
natural physiological cycles are influenced by external environmental conditions,
however, and in experimental systems organisms that are initially synchronous
with respect to reproduction and moulting may not remain so for the duration of
their exposure to environmental stress. The use of physiologically synchronous
target organisms in studies of effects of environmental change must, therefore,
be approached with caution.
300 JOHN BLACKSTOCK
BEHAVIOUR
A wide variety of behavioural responses of marine invertebrates to natural and
anthropogenic fluctuations in environmental conditions have been described in
the literature and for some species certain behavioural responses have been
considered to have potential for the diagnosis of effects of environmental
perturbation (see e.g., Eisler, 1979; Olla, Pearson & Studholme, 1980 for
reviews). Behavioural responses of marine invertebrates to environmental
stimuli usually involve changes in energy production by muscular tissue and the
relations between such changes and metabolic regulatory responses to
environmental change are examined in this section. It has been shown that the
capability of marine invertebrate muscles for energy production and for different
types of action can be related to the adenine nucleotide and phosphagen contents
of the muscle tissue (Beis & Newsholme, 1975; Ansell, 1977), and to the
maximal activities of enzymes associated with catabolism. Zammit & Newsholme
(1976) indicated that high activities of the glycolytic enzymes phosphorylase and
phosphofructokinase were indicative of a high capability for anaerobic
degradation of glycogen for energy production and Zammit, Beis & Newsholme
(1978) suggested that, in invertebrate muscles which were capable of the
anaerobic succinate pathway of carbohydrate catabolism the ratio of activities of
phosphofructokinase/pyruvate kinase was relatively high. High activities of
enzymes associated with the citric acid cycle, e.g. citrate synthase, NAD+ -linked
and NADP+linked isocitrate dehydrogen ases were considered to relate to
dependence on aerobic catabolism (as in insect muscles) or a capability for
sustained activity (Alp, Newsholme & Zammit, 1976).
In a number of marine invertebrates the biochemical mechanism utilized for
energy production has also been shown to relate to involvement of the
individuals in a particular behavioural response. In polychaetes of the genus
Nereis D-lactate has been shown to be the major end-product of anaerobic
glycolysis during extensive muscular work while succinate and volatile fatty
acids were the major end-products of glycolysis during survival of prolonged
periods under anoxic conditions (Schöttler, 1979), and glycolytic flux in
adductor muscle of Placopecten magellanicus varies with the behavioural
response (see p. 274).
The application of these general principles to the study of several species of
polychaete worms which have been shown to have different distributions within
spatial gradients of effects of organic enrichment has been attempted by
Blackstock & Pearson (1981), with the objectives of determining how
biochemical characteristics of each species may relate to their normal behaviour
and to their ecology. Capitella capitata and Melinna palmata are both considered
to be deposit-feeding polychaetes that are relatively inactive in comparison with
Glycera alba and Scolelepis fuliginosa which are both capable of bursts of
intense muscular activity. Maximal activities of certain enzymes associated with
energy-yielding metabolism e.g. phosphofructokinase, pyruvate kinase, and
citrate synthase differ between the species, possibly as a consequence of their

different metabolic activities under normal conditions (see Blackstock, 1979). In
Capitella capitata and Melinna palmata phosphofructokinase activities are
relatively low. In contrast activities of citrate synthase, which may have a rate-
controlling rôle in the regulation of entry of carbon units to the tricarboxylic acid
cycle, are relatively high in these species. In Glycera alba and Scolelepis
fuliginosa phosphofructokinase activities are higher and citrate synthase
activities are relatively low, and it is suggested that these results are consistent
with a greater requirement for anaerobic energy production during bursts of
muscular activity in these species.
Capitella capitata and Scolelepis fuliginosa are often found in high numbers in
organically enriched sediments and Glycera alba and Melinna palmata are
characteristically found in less enriched areas and are components of the normal
soft-mud faunal communities associated with sediments where there is a higher
availability of oxygen. The enzymatic profiles are, therefore, considered to relate
more closely to behavioural characteristics of each species than to their relative
abilities to survive effects of enrichment. The anoxic tolerances of Glycera alba
and Scolelepis fuliginosa are considerably different with the latter species
exhibiting the greater tolerance. This would be expected from a consideration of
their different environmental niches. The behavioural and enzymatic responses
of each to experimentally induced anoxia are, however, reasonably similar with a
decline in movement and a concurrent decline in activity of phosphofructokinase
occurring in each species. It is, therefore, concluded that the similarity in certain
behavioural and biochemical responses in these two species reflects a common
response to anoxia in spite of the very different oxygen concentrations each
species encounters in its particular habitat.
Metabolic regulatory responses to environmental change may, therefore, be
related to the behavioural responses of invertebrates to such changes and
understanding of the impact of a metabolic regulatory response on normal
function of invertebrates, therefore, requires that the impact of the related
behavioural response is understood. There have been very few co-ordinated
investigations of effects of environmental change on behavioural and metabolic
regulatory responses of marine invertebrates. It is suggested that biochemical
changes indicative of relatively rapid metabolic regulatory responses affecting
energy-yielding metabolism may reflect changes in energy demand caused by
adjustments of muscular activity following environmental stimuli. Further
investigation of such responses and their longer term effects on metabolic
characteristics and normal physiological function of marine invertebrates would
lead to a better understanding of the relations between marine invertebrates and
their natural environment.
302 JOHN BLACKSTOCK
DISTRIBUTIONS OF MARINE INVERTEBRATE

POPULATIONS
In the previous sections on relations between the ecology of marine invertebrates
and their sensitivities to particular environmental perturbations, the influence of
habitat, natural cyclical rhythms, and behaviour have been discussed. The overall
objective was the indication of the influence of some ecological characteristics
of selected species on the magnitude of their metabolic regulatory responses to
environmental stimuli. In the marine environment the distributions of
populations of marine invertebrates are determined by the net effects of many
environmental and ecological factors. Many of the factors are related and may be
synergistic in their action but at present we have relatively little knowledge of
the synergistic effects of most environmental variables (see Reish, 1979).
Environmental changes beyond the limits within which species can function
normally will have ultimate detrimental effects and, of course, these limits vary
for different species. In view of the complexity of interactions of various types of
environmental variation a useful first approach towards the assessment of the
sensitivity of marine invertebrates to an environmental perturbation can be
achieved by studying the distribution of invertebrate populations in spatial
gradients of effects of particular environmental changes in the natural
environment.
Marine invertebrates that have opportunistic life histories can compensate for,
or even exploit, environmental changes beyond those that most of the
invertebrate fauna can tolerate, and low species diversity is a characteristic of
extreme environmental conditions (see Vernberg & Vernberg, 1975, for
discussion of extreme environments). This feature of population distributions in
spatial gradients of environmental effects has found wide application in the
diagnosis of effects of pollution on benthic invertebrate populations. Certain
species of macrobenthic invertebrates that have opportunistic life histories have
been proposed as “pollution-indicator” species (Reish, 1972; Bellan & Bellan-
Santini, 1972) because they are frequently found in large numbers in polluted
areas where there is a generally low species diversity. Surveys of the numbers
and diversity of species of macrobenthic invertebrates have thus attained
considerable importance in the assessment of the impact of various types of
marine pollution (see Pearson & Rosenberg, 1978, for review) and a
generalized SAB diagram showing changes in numbers of species, total
abundance and total biomass of macrobenthic invertebrates along a spatial
gradient of organic enrichment effect is shown in Figure 13. The information
obtained from this type of study of macrobenthic invertebrate populations has
most frequently been used to detect disturbance of marine benthic communities
as a consequence of pollution with emphasis being given to increased biomass,
decreased species diversity and the presence of pollution-indicator species in the
most affected areas.
Fig. 13.—Generalized SAB diagram of changes in macrobenthic invertebrate populations

along a spatial gradient of organic enrichment: S, numbers of species; A, total abundance;
B, total biomass; PO, peak of opportunists; TR, transition zone between populations
characteristic of enriched sediments and normal community structure; after Pearson &
Rosenberg, (1978).
In recent years, the need for more detailed study of the relatively pollution-
sensitive species of macrobenthic fauna has become more widely recognized
because sub-lethal responses to effects of pollution may be more readily detected
in such species thereby providing an early indication of subsequently more
damaging effects of pollution on marine communities. Gray & Mirza (1979)
have used the departure from a log-normal distribution of individuals among
species to assess effects of environmental perturbation on marine communities
and by using an extension of this method of analysis of macrobenthic faunal
population data it has been shown that species sensitive to the effects of pollution
can be identified (Gray & Pearson, 1982; Pearson, Gray & Johannessen, 1983).
Pearson & Blackstock (1984) have extended this approach to co-ordinated
environmental, biological, and biochemical studies of effects of organic
enrichment along a transect of sampling stations situated at regular intervals from
the centre of a sewage sludge dumping ground in the Firth of Clyde in the west
of Scotland. Species comprising intermediate abundance groups at those
sampling stations where effects of pollution first become detectable in the
transect were considered to be demonstrably sensitive to the pollutant effects by
virtue of the change in their abundance in these locations and were also present
in sufficient numbers to make further collection, for biochemical analyses,
feasible. The nine species comprising the appropriate abundance groups in this
area were assessed for their suitability as potential target organisms on the basis
of size, reproductive type, growth characteristics, their continuous presence in
the normal benthic community in the area studied and genetic stability although
information on this last characteristic is somewhat limited. It was concluded that
the polychaete Glycera alba was the most suitable target organism in the area
304 JOHN BLACKSTOCK
and, in this species, activities of certain enzymes associated with catabolism e.g.
phosphofructokinase, pyruvate kinase, and malate dehydrogenase were found to
relate to changes in conditions in the sediments along the spatial gradient of
enrichment effect. In contrast changes in maximal enzyme activities of a
pollution-indicator species Capitella capitata, collected along a transect of
sampling stations in the vicinity of the centre of the dumping area, were less
pronounced (see p. 283).
Assessment of the physiological significance of the enzymatic changes and
their longer term impact on normal functions of the individuals is clearly
required together with studies of other potential target organisms before a valid
assessment of relations between species distributions and biochemical, or
physiological, sensitivity to environmental perturbation can be made. It is
suggested, however, that investigations of such relations in other groups of
invertebrates would be a valuable first approach to the selection of species for
study of biochemical or physiological responses to subtle influences of natural or
anthropogenic environmental perturbations.
CONCLUDING REMARKS ON ECOLOGY AND

SENSITIVITY TO ENVIRONMENTAL STIMULI
The influence of selected ecological factors on non-specific metabolic regulatory
responses of marine invertebrates to environmental perturbations has been
discussed, with particular reference to effects on carbohydrate catabolism. Many
different types of environmental stress that have not been discussed at present
have been shown to elicit related biochemical responses involving carbohydrate
catabolism in a wide range of marine invertebrates. In studies of effects of
anthropogenic perturbations metals, pesticides, petroleum hydrocarbons, and
organically rich industrial and domestic wastes have all been considered to exert
an influence on carbohydrate catabolism in various groups (see e.g. Rao et al.,
1979; Blackstock, 1980a, b; Gould, 1980; Carr & Neff, 1981, 1982; Widdows et
al., 1982). The relations between these non-specific metabolic responses and
subsequent damaging effects of the perturbations on normal functions of
invertebrates remains ill-defined at present and, therefore, the predictive
potential of these responses remains the subject of continuing investigations.
Most of the metabolic regulatory responses that have been discussed in the
preceding ecological sections have been relatively rapid ones in metabolic
regulatory terms and there is an urgent need for extension of environmental
response investigations to include studies of acclimative and adaptive responses
in the same species under the same environmental conditions. The eventual
consequences of the metabolic regulatory responses on the environmental fitness
of selected target organisms could then be evaluated through co-ordinated
biochemical, physiological, and population studies. The initial problem in this
sequence of studies is the selection of appropriate target organisms. It is clear that
no single organism can justify this rôle in every study of relationships between
organisms and their environment. At present, however, there is considerable

evidence in the literature that such organisms are often selected for diverse
reasons e.g. ease of collection or culture or a previous scientific interest in the
species. The prime reason should, however, be the sensitivity of the chosen
organism to effects, in the natural environment, of the environmental
perturbation that is being investigated. Such evidence can be obtained from initial
environmental and population studies in ‘test’ areas where a known gradient of
environmental effect can be demonstrated. Subsequently useful information may
be obtained from the use of the same test organisms to detect subtle effects of
similar environmental perturbations in other areas.
Reproductive cycles have so far been discussed largely in terms of their
influence on metabolic regulatory responses. it is well known that invertebrate
reproduction is influenced by many natural and anthropogenic environmental
factors (see e.g. Sastry, 1975) and that environmental stress can have profound
effects on the reproductive physiology of invertebrates (Bellan, Reish & Foret,
1972; Reish, 1974; Bayne, 1975; Bayne, Gabbott & Widdows, 1975; Carr &
Reish, 1976; Bayne, Holland, Moore, Lowe & Widdows, 1978; Reish & Carr,
1978). The impairment of normal reproduction is an important criterion in the
assessment of the effects of environmental perturbations on marine organisms
and is an important contributory factor to the low species diversities
characteristic of environments which can be considered to be extreme in certain
respects (Vernberg & Vernberg, 1975; Bayne et al., 1979). The demonstration of
reproductive impairment is, however, of limited value in providing an early
warning of subsequent deleterious effects of an environmental perturbation
because population changes are inevitable when reproductive impairment is first
detected. In several studies biochemical changes associated with energy-yielding
metabolism have changed in response to environmental perturbation before
reproductive abnormalities were detected (see e.g. Reish, 1974; Widdows et al.,
1982). Nevertheless studies of reproduction and larval survival are most
important components required in co-ordinated investigations of effects of
environmental perturbations on marine invertebrate populations since in many
species these processes represent the most vulnerable stages concerned with
survival during environmental perturbations.
It is inevitable that, in discussion of environmental changes beyond those
normally encountered by species in their particular environmental niches
examples of effects of marine pollution have predominated. Pollutant effects are
the most widely studied and reported environmental perturbations in this
category and prediction of subsequently damaging effects of pollution on the
marine environment is of considerable importance from both conservation and
economic viewpoints. In addition, in the case of non-specific metabolic
regulatory responses of marine invertebrates to environmental perturbations the
study of effects of anthropogenic activities are relevant to the improvement of our
understanding of animal-environment interactions in the naturally fluctuating
marine environment. In both types of study is is clear that appropriate target
306 JOHN BLACKSTOCK
organisms must be selected on the basis of their sensitivity to appropriate

environmental influences. ‘Signal : baseline noise’ will be minimized by the
selection of target organisms that are subject to the minimum possible normal
environmental and physiological variability by using sexually immature
individuals or those at a single stage in relation to natural physiological cycles of
activity. In conclusion, it is also emphasized that interdisciplinary co-ordination
involving environmental, biochemical, physiological, genetic, and biological
population studies are essential for the relation of metabolic regulatory responses
to environmental perturbations, and their possible damaging effects on marine
ecosystems.
GENERAL CONCLUDING REMARKS

At present rapid advances are being made in our understanding of metabolic
regulatory processes and their rôle in the interactions of marine invertebrates and
their environment. There are many potential applications of current metabolic
regulatory research in the marine sciences. In particular further developments in
relations between environmental conditions and the stimulation of cellular and
genetic response mechanisms will permit more confident assessment of the
causal relations between environmental change and regulatory processes. The
rapid advances in our understanding of the relatedness of the various levels of
metabolic regulation also offer scope for the improvement of our knowledge of
the sequence of events linking environmental change to subsequent changes in
marine invertebrate populations. As a consequence we shall also have at our
disposal more reliable techniques and scientific knowledge for applied
investigations of considerable importance economically and in conservation of
the marine environment.
Clearly many scientific problems remain to be solved before a more accurate
understanding of the interactions of marine invertebrates with their environment
can be obtained. In particular, our poor knowledge of many fundamental
mechanisms is at present retarding our progress. For example, at the taxonomic
level there are considerable problems associated with the definition of species
and recent research trends indicate the requirement for further co-ordinated
biological, physiological, and genetic approaches to this problem. Knowledge
relating to the hormonal control of marine invertebrate metabolism is minimal
and requires the co-ordinated application of biological, biochemical, and
physiological skills to the investigation of these processes and their impact on
normal function of marine invertebrates in a changing environment. There are
many other basic scientific challenges facing investigators in the marine sciences
and the majority require co-ordination between biologists and specialists in other
scientific disciplines if our scientific knowledge is to progress from its current
status.
In this overview the benefits of an interdisciplinary co-ordinated approach to
studies of the relations between environmental change, metabolic regulation in
marine invertebrates and subsequent changes in marine populations are apparent.

This approach requires the involvement of environmental and biological studies
designed to select the most appropriate target organisms and to assess the
subsequent impact of apparently subtle responses of the selected organisms to
environmental change on marine populations.
ACKNOWLEDGEMENTS
I am very much indebted to Dr T.H.Pearson for invaluable discussions of the
theme and constructive criticisms of the manuscript and to Dr J. Mauchline for
helpful comments on an earlier draft. The constructive and valuable comments
offered by Prof. R.J.Berry are gratefully acknowledged. I thank Mrs F.Simpson
for excellent assistance with the preparation of the manuscript and Mrs F.Gregge
for preparation of several of the figures.
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ASPECTS OF FLOWERING AND
POLLINATION IN MARINE
ANGIOSPERMS
J.M.PETTITT
Department of Botany, British Museum (Natural History),
Cromwell Road, London SW7 5BD, U.K.
INTRODUCTION
Pollination, being part of the sexual episode, is a principal event in the course of
the spermatophyte life cycle. Except in species which by-pass meiosis and
fertilization on an apomictic pathway, if pollination fails, no seeds will be
formed; but even some apomicts require pollination to stimulate the formation of
viable seeds. It is known that in the land-based flowering plants, successful
pollination requires harmonious co-adaptation between the pollen, protecting and
dispersing the male gametophyte, and the female receiving tissue of the pistil,
comprising the stigma, style and ovary. What is more, the process is now known
to provide sensitive and highly refined physiological mechanisms which,
together with more overt devices, such as structural adaptations or temporal
differences in development, serve to regulate breeding behaviour by ensuring a
greater or lesser amount of outcrossing in a population. The past decade has seen
rapid advances in the understanding of many structural, physiological, and
biochemical details of the pollination sequence in terrestrial flowering plants.
An orderly series of events is rapidly set in train when compatible pollen is
captured by the stigma. Immediately upon contact, the pollen grain is firmly
attached to the surface. This process admits a degree of specificity and binding is
a consequence of chemical interaction between components carried by the pollen
on the one side and coating the stigma on the other. Once adhesion is effected, the
grain begins to hydrate. In this phase water passes into the pollen from the
stigma, and any labile materials, usually low molecular weight carbohydrates and
lipids in addition to proteins and glycoproteins, contained in the outer, or exine
layer of the pollen wall are rapidly released. These emitted molecules bind to
receptors on the stigma surface, and in some species the macromolecular fraction
is known to have a rôle in the information exchange involved in pollen
recognition. As pollen germination begins and the pollen tube prepares to
318 J.M.PETTITT
emerge, proteins and related molecules held in the inner, or intine layer of the
pollen wall diffuse from the grain. This intine fraction usually includes acid
hydrolases, and there is evidence to suggest that a cutinase or cutinase precursor
released from the pollen tube tip is activated on contact with the stigma surface
to erode the stigma cuticle layer, in species where this remains intact
at pollination. The advancing tube tip then penetrates the epidermal layer of the
stigma and growth thereafter is through the tissue of the style towards the ovary
where the gametes ultimately unite. Since effective operation of the cuticle
lysing system appears to depend upon pollen-stigma complementation—a factor
on the stigma surface is required for enzyme activation—the process clearly
provides opportunities for regulating fertilization. Indeed, such opportunities
exist wherever the sporophytic tissue of the (prospective) female partner can
scrutinize the credentials of the pollen or contained male gametophyte—at pollen
capture, germination, tube penetration and growth through the pistil. Full
accounts of these various discoveries and discussion of their significance can be
found in recent papers by Heslop-Harrison (1975a, b, 1976, 1978a, 1983).
From the foregoing it will be clear that central to the physiological scheme of
pollen-pistil interaction in the terrestrial flowering plants is the process of
hydration. Whatever may or may not take place subsequently, imbibition of the
grain brings about the rapid release of diffusable molecules stored in the pollen
grain wall, including enzymes whose rôle in pollen tube penetration can be
defined. And therein lies the essence of the problem: it is difficult to conceive
how the operation and regulation of this general system—which obtains in the
terrestrial flowering plants with little variation—can accommodate hydrophilous
pollination. Yet the system seems far from being redundant in the aquatic
angiosperms, and it must be supposed that as the functional elements remain
essentially the same, the means to this end could hardly be served without some
recourse to adaptive compromise. However else?
Of the 12 genera (including some 50 or more species) of marine angiosperms
treated in den Hartog’s monograph Seagrasses of the World (1970), eight are
sexually polymorphic and dioecious. Of the remainder, one genus contains both
polymorphic dioecious and monomorphic species bearing diclinous flowers—
termed monoecious, two genera have only monoecious species, and one genus
has monomorphic species with monoclinous flowers—termed hermaphrodite.
The dioecious species are all taken to be obligately outcrossing since there are no
records of self-compatible hermaphrodite or monoecious individuals in any of
the populations examined. It can be surmised that the consequence of monoecy
will be similar. Cross-pollination between monoecious individuals can be
achieved, and self-pollination (geitonogamy) prevented, by dichogamy—either
protandry (where pollen is released before stigmas are receptive) or protogyny
(where stigmas are receptive before pollen is released). But even though
dichogamy may be strictly enforced developmentally, cross-pollination is not
thereby ensured. In protandry, for example, the timing difference can be bridged
if the pollen remains viable throughout the interval. Discussion of these topics
FLOWERING AND POLLINATION IN MARINE ANGIOS PERMS 319
and the related cytological and physiological questions which arise has,
however, been scarcely possible for need of sufficient information at this level.
In contrast with the situation for their land-based relatives, until quite recently
virtually nothing was known about the functional aspects of sexual reproduction
in the rather heterogeneous assemblage of plants popularly called seagrasses.
This review deals then with those studies which have a bearing upon the
mechanism of pollination in the marine domain, and which provide information
that allows us to begin to appreciate what evolutionary innovation or
experimentation has been necessary to preserve the basic elements of an efficient
functional system; since this is in fact what selection seems to have achieved.
Comprehensive coverage of many aspects of seagrass biology, including some
field observations on flowering not mentioned here, can be found in den
Hartog’s (1970) monograph.
ASPECTS OF FLOWERING
There have been a number of investigations of the flowering stage in the marine
angiosperms, and of the environmental factors affecting floral development and
anthesis. Some of these studies have combined field observations with an
analysis of the flowering process in plants from the same populations maintained
in culture under controlled conditions.
Among the species examined eelgrass, Zostera marina L., has received
particular attention. In 1929 Setchell suggested that the dominant environmental
variable determining the initiation and duration of sexual reproduction in Z.
marina is water temperature. The proposition that anthesis and seed formation in
the species occurred only at water temperatures from 15 to 20°C has found
support in the observations of Tutin (1938) and more recently, in those of
McRoy (1966); but some significant exceptions have been recognized. For
instance, Phillips (1969, 1980) has found that flowering in Z. marina in Puget
Sound, Washington, where water temperatures do not commonly exceed 15°C,
occurs at a lower temperature than the range suggested by Setchell, at 8 to 9°C in
fact.
Nevertheless, additional support for Setchell’s view comes from the study of
Churchill & Riner (1978) on Z. marina in Great South Bay, New York. These
workers found that a minimum water temperature of 15°C is required for
anthesis in the species at this locality, since the process began four to nine days
after the water temperature had exceeded this value. Anthesis continued for
approximately one month as successive spathes matured, and during the entire
period the water temperature fluctuated between 20 and 21°C, a discovery at
variance with Setchell’s (1929) and Tutin’s (1938) conclusion that flowering in
Z. marina ceases at temperatures above 20°C. As the interval immediately
preceding flowering in the plants growing in Great South Bay was characterized
by a rapid increase in water temperature—a rise from 12 to 20°C over 14 days in
May—the particular conditions required to stimulate the process could not be
320 J.M.PETTITT
specified. However, from the differences in temperature requirements of the kind

considered above, Churchill & Riner stress the need to examine the effect of
environment factors other than temperature on the course of sexual reproduction
in the species, a point also emphasized by Phillips (1969), McRoy (1970), and
Jacobs & Pierson (1981).
More recently, Silberhorn, Orth & Moore (1983) have studied anthesis and
seed production in Z. marina growing at various sites in Chesapeake Bay,
Virginia. In this location, as in New York, flowering was found to commence
when the water temperature approached 15°C, and the peak occurred while the
temperature fluctuated between 20 and 21°C. Pollination took place during a
three to four week period (from mid-April to mid-May), and the interval from the
start of pollen release to early seed development and liberation was some 28–30
days. This time interval is similar to that given by Churchill & Riner (1978) for
the plants in the New York population, and by de Cock (1980) for the species in
The Netherlands, but is somewhat longer than the period reported in high- and
low-littoral eelgrass beds in Brittany (Jacobs & Pierson, 1981). According to the
studies of Jacobs & Pierson (1981) and de Cock (1981a), however, the duration
of flowering of the species in European coastal waters is more prolonged than in
New York and Virginia. As Silberhorn et al. (1983) point out, the information on
reproductive behaviour given in the various published accounts clearly suggests
that the species in different regions is adapted to different temperature ranges, a
situation demonstrated by the fact that flowering may occur at a rather higher, or
markedly lower, limit than those originally suggested by Setchell (1929). In their
analysis of the published flowering and temperature data from the various
locations on the eastern seaboard of North America, Silberhorn et al. (1983)
show a difference in the timing of selected stages in the sexual process of Z.
marina that is related to latitude. Setchell (1929), referring to the observations of
Duval-Jouve (1873) on the Mediterranean flora, first called attention to the trend,
and the records for the various European sites have been collected and tabulated
by Jacobs & Pierson (1981). The findings for North America, taking one stage,
anthesis, as an example, are shown in Table I. The observations for North
Carolina (the southern limit of Z. marina on the east coast of North America) are
from Dillon (1971), the observations from New York are Churchill & Riner’s
(1978) and those from Nova Scotia are from Keddy & Patriquin (1978). These
last authors have suggested that the difference in the time of flowering which
they detected between an annual form of Z. marina and the perennial form could
serve to restrict pollen exchange, and that the forms may not be interfertile. It
would appear, however, from an electrophoretic comparison of 16 enzyme
systems that the annual eelgrass is a genetically integral component of the Z.
marina population in which it occurs, and that gene flow between the two types
is unrestricted and adequate to prevent sympatry of the annual form. Thus, it
seems, annual eelgrass must be considered a natural ecophenotype—an
environmental variant of the species (Gagnon, Vadas, Burdick & May, 1980).
TABLE I
Timing of anthesis in Zostera marina populations on the eastern coast of North America
(data from Silberhorn et al., 1983)
Location Teraperature (°C) Month
North Carolina, 35°45′ 15 February
Virginia, 37°25′ 14 April
New York, 40°40′ 15 May
Nova Scotia, 44°44′ 15–16 June
The possible influence of light on the course of the sexual reproductive

process in Z. marina has been briefly discussed by Blackman & Barilotti (1976),
by Jacobs & Pierson (1981), and by Silberhorn et al. (1983). The nature of the
responses to this environmental factor has been experimentally investigated by
de Cock (1981b) using plants from an intertidal annual population of Z. marina
from The Netherlands. No persistent endogenous flowering rhythm was revealed
by these experiments. The styles of more than 80% of the inflorescences were
exserted from the spathe—the arrangement favourable (or necessary) for pollen
reception—in the dark phase when plants were grown under conditions of 12:12
h (light : dark), and exsertion occurred regardless of whether the dark phase was
timed to coincide with the solar day or solar night. Stylar exsertion was also
stimulated in plants maintained both in continuous light and constant darkness.
The experiments were, however, inconclusive as regards anther dehiscence, and
while it seems this process may be influenced to some extent by photoperiod, the
sensitivity of anthers to an alternating regime appeared to vary through the
flowering term.
De Cock (1981c) has also used experimental methods to examine the effect of
temperature on flowering in annual plants from the same locality in The
Netherlands. From these experiments it appears that 20°C is the optimum
temperature required to induce style exsertion since the movement was found to
begin sooner and proceed more rapidly at this value than at either 15 or 25°C.
The rate was also found to be influenced by changes in temperature; lowering the
temperature in the water column from 20°C to 15°C accelerated the rate, even
though the higher value seemed most effective for promoting style exsertion
when applied continuously. Rather intriguingly, in view of the style responses,
no temperature optimum for anther dehiscence was discovered within the range
investigated by de Cock. Preparations for pollen release were seen quite
regularly at constant temperatures of 15, 20 and 25°C as well as during a regime
of 15:20°C and 20:25°C in alternating periods of 12 h. In those cultures maintained
at constant temperature, the rate of the process increasing with increasing
temperature, up to and including 25°C, the highest value investigated. Plants
exposed to the alternating temperature regime did not, however, reflect the
fluctuation in having corresponding periods with increased and decreased rates
of dehiscence. This contrasts with the situation on the female side, where the
322 J.M.PETTITT
same programme elicited a noticeable effect. Particularly interesting, however, is

the discovery that, although Z. marina is a diclinous species where protogyny is
the rule, in plants maintained at 25°C the characteristic dichogamous
development of the inflorescences is disturbed and homogamy results. This
would clearly provide an opportunity for geitonogamy, unless there are
physiological devices to prevent it. De Cock’s (1981b, c) interpretation of his
experimental results is that in the natural intertidal habitat for the species, low
water temperature, when coinciding with a period of darkness, tends to stimulate
the rate of style exsertion. Conversely, the combined effect of higher
temperatures and insolation during the day-time suppresses the process.
In a further study de Cock (1981a) has compared the development of the
flowering shoots in the annual ecophenotype of Z. marina grown from seed under
controlled conditions with the pattern of flowering in wild populations of the
annual plant growing in two dissimilar habitats in The Netherlands. The
conditions established for the laboratory cultures were a temperature of
approximately 20°C and a photoperiod of 16:8 h (light: dark). In the cultured
plants, de Cock found that there was an interval of one or more days between the
flowering of two successive inflorescences on the rhipidium; that is, between
anther dehiscence in one inflorescence and stylar exsertion for pollen reception
in the next youngest. Since this system does not always function perfectly, it by
no means precludes the possibility of geitonogamous fertilization (de Cock,
1980). Moreover, the fact that in the natural habitat relatively few inflorescences
are found at any one time with styles exserted for pollen reception is taken as
evidence that pollination takes place quite rapidly: once pollen has been received
the styles begin to reflex and return to the confines of the spathal sheath (see
Fig. 1). The anthers then dehisce and the pollen is released. The anthers become
partially detached from the spadix, project from the margin of the spathe and
split open. This event is of relatively short duration, and liberation of the grains
is calculated to take not more than 12 h if the period between the beginning of
flowering in two successive inflorescences is 10 days. This estimate is in
agreement with the observations made on plants maintained under controlled
conditions in aquaria (de Cock, 1980). Lastly, de Cock’s findings indicate that
the interval between flowering of successive inflorescences on the rhipidium was
rather protracted, whereas the duration of this particular stage, and of the entire
period of flowering—in other words, the temporal separation between stylar
exsertion and anther dehiscence—was the same for plants in the natural habitats
and for those in culture. The plants in the coastal populations in The Netherlands
monitored by de Cock continued to flower for a period of approximately two
months, and while the rate of flowering in the two localities was rather different,
the relative duration of each separate stage in the sequence was found to be
about the same (Fig. 1).
The general observations of Phillips (1960), Orput & Boral (1964), Tomlinson
(1969), Thorhaug (1979), Lot-Helgueras (1977), Grey & Moffler (1978), and
Moffler, Durako & Grey (1981) on the flowering process in the dioecious
Fig. 1.—Time sequence of dichogamous development in the inflorescence of annual

Zostera marina (after de Cock, 1980).
seagrass Thalassia testudinum Banks ex König, and those of Marmelstein,

Morgan & Pequegnat (1968) on the photoperiod factor, have been extended in a
detailed study by Phillips, McMillan & Bridges (1981). These workers examined
the conditions for reproductive development in the species, both in plants
growing in natural seagrass beds at five locations in the western tropical
Atlantic, and in plants grown under controlled conditions as laboratory cultures.
Their findings from the collections made regularly over a number of years at
various sites in Texas, Florida, and St Croix in the U.S. Virgin Islands, and from
an investigation of the cultured plantings, suggest that flowering in this species is
related to the temperature progressions that follow the winter minima. Cultured
plants originating in Texas were induced to flower at or below 23°C and reached
anthesis at this temperature, while those of more tropical origin, from St Croix
and individuals in cultures established from plants collected in Veracrux, Mexico,
flowered less frequently and at a slightly higher level, at 24 to 26°C. Plants of
different geographical origin were found to produce flowers under continuous
light, suggesting that photoperiod does not have a significant influence on the
flowering process in T. testudinum. Statistical analysis of one phenophase in the
reproductive development—the first indication of floral buds—and temperatures
measured prior to this phase, indicated that flowering in St Croix is preceded by
a significantly higher temperature progression than flowering in either Florida or
Texas. Evaluation of the data obtained from plants growing in the natural
seagrass beds under normal environmental conditions and from plants
maintained as cultures suggested that temperature responses for the St Croix
individuals were probably genotypically different from those of Texas and
Florida. The authors point to the possibility that the near coincidence in the time
of flowering in populations as separated as the Virgin Islands, Florida and Texas,
is the result of latitudinal differences in the temperature progression following
the winter minima combined with genotypic differentiation. Genetic variation
between the populations in question is, however, not illustrated by isozyme
analysis (McMillan, 1980a).
324 J.M.PETTITT
McMillan (1976) has employed laboratory culture methods complemented by

monthly observations on the parent clones in the natural habitat in Texas to study
aspects of reproductive behaviour in dioecious Halophila engelmanni Aschers.
Flowering of the species in the natural environment occurred principally during
April and May, extending to mid-June, whereas flowering in the cultures was
found to be essentially continuous if the temperature of the water column was
maintained at 22 to 24°C, with a day length of 14 h and a salinity of 27 to 35‰.
However, the plants remained vegetative if the water temperature was 18·5°C,
the day length 12 h, or the salinity 10 to 18‰. It would seem that temperatures
maintained above 23·5°C and salinity levels over 40‰ probably inhibit flower
production in the species, while day lengths in excess of 14 h, including
continuous light, serve to stimulate the process. McMillan concludes from an
examination of the various factors that in the wild populations, a coincidence of
temperature, salinity and day length would seem to be critical for flowering and
reproduction in H. engelmanni. In this connection, it is interesting to note that
McMillan (1976) reports continuous flowering of the dioecious species Halodule
wrightii Aschers. at the same locality in Texas during the summer months, a
circumstance which would seem to indicate that the reproductive adaptation of
this species is significantly different to that of L Halophila engelmanii. So far
Halodule wrightii has not been induced to flower under laboratory conditions
and, consequently, the influence of salinity, temperature and day length on floral
development, have not determined.
In another study McMillan (1980b) has used experimental methods to
investigate the flowering stage in dioecious Syringodium filiforme Kütz. Clonal
samples were collected from a number of sites in the Gulf of Mexico-Caribbean
and Bermuda, transplanted and grown in soil cultures. From seasonal field
observation of the natural seagrass beds, it appears that flowering responses in
the species are related to lengthening days and increasing temperatures that
follow winter temperature minima, but inflorescences may be formed at other
times of the year if temperatures are suitable. With photoperiods varying from 12
h light to continuous light, plants originating in Texas were induced to flower in
the laboratory at temperatures ranging from 20 to 24°C, whereas plants from the
southern Gulf of Mexico and the Caribbean were most readily induced at 23 to
24°C. S. filiforme collected in Texas proceeded to anthesis at temperatures above
22°C but plants from the Virgin Islands required somewhat higher temperatures,
above 25°C, for emergence of the flowers. McMillan found that flowers induced
with continuous light continued to anthesis under day lengths shortened to 11 h,
but in this regime further floral induction was inhibited, even at temperature
levels established as being inductive. Phenomena such as the frequency of
flowering which characterizes the species in certain seagrass beds and the rarity
of the event in others, as well as the absence of flowering in clones maintained in
culture under inductive temperature-photoperiod conditions, would seem to
indicate that the nutrient status of the sediment and/or water column may be an
important factor during certain stages of reproductive development. The
different temperature-related responses found for the species and mentioned

above raises the possibility of ecotypic variation among the Gulf-Caribbean
populations. While some differences in flowering responses were noted between
the plants of Texas and Florida, greater differences were found in respect of the
response between plants of the northern Gulf and those of the southern Gulf and
Caribbean. An electrophoretic study of several enzyme systems has, however,
provided no evidence of enzyme differentiation, which suggests that the species
in the populations concerned has not diverged genetically in any fundamental
way (McMillan, 1980a).
Using the same culture technique McMillan has succeeded in inducing flower
development in Cymodocea rotundata Ehrenb. & Hemper. ex Aschers. from the
Palau Islands, Micronesia (McMillan, 1979), and in five of nine species of
seagrasses collected in Kenya (McMillan, 1980c). Flowering in each of the five
species from the Kenyan sites involved a different set of environmental
conditions. Pistillate flowers were produced in dioecious C. serrulata (R.Br.)
Aschers. & Magnus at 31:27°C (day: night) after eight months in culture, and
flowering was found to be continuous for three months under these conditions,
but not at lower temperatures. The species showed an increase in flower
production with decreasing salinity from 35 to 25‰. Although the number of
flowering shoots was found to increase after changes towards lower salinity,
there were no indications that a rapid change back to the higher level
adversely affected flowers that were at anthesis. The production of staminate
flowers under controlled conditions in plants of this species from Kenya has been
reported in another paper (McMillan, 1980d), and on the male side the
experimental regimes suggested primary temperature controls of floral induction.
Two of six replicates that had been maintained in low temperature programmes,
25:24°C (day:night), or fixed temperatures of 28°C or below, with a day length
sequence of 12–13 h for ten months produced staminate flowers during the eight
months following transfer to higher temperature conditions of 31:27°C (day:
night) with 13-h photoperiods. Three of six plantings produced pistillate flowers
after these environmental manipulations. Two months before the staminate
flowers appeared on the cultured plants, the salinity of the water column had
been held at 25‰ for ten days. A number of specimens of C. serrulata from the
Palau Islands, which had been maintained in culture (McMillan, 1979), were
induced to flower under the same experimental conditions required for the
Kenyan plants. The plants from Palau had been grown at various temperatures
(27 to 32°C) for two and a half years before being transferred to reduced
salinities (25‰) and subjected to a 31:27°C (day: night) temperature regime.
Some two months after exposure to the revised environmental programme, the
plants produced pistillate flowers. A series of replicates of C. serrulata from
Thursday Island, Queensland, however, did not initiate flowering after four
months in culture with the plants of east African and Micronesian origin.
Comparisons showed no differences in the isozyme patterns for eight enzyme
systems among the three collections (McMillan, 1981).
326 J.M.PETTITT
Flowers were readily developed on gynoecious plants of the dioecious

Halophila stipulacea (Forsk.) Aschers. from Kenya at temperatures of 24, 26 and
at 26:24°C (day: night), but in those plants subjected to the fluctuating value
there was a cessation of flowering after approximately two months. The process
was resumed, however, upon the addition of chelated iron (EDTA, FeSO4). This
finding, together with the discovery that flowering invariably occurred at all the
experimental temperatures–24°C constant to fluctuating 31:27°C (day: night)—
after the water column had been refreshed, or chelated iron added, suggests that,
as with Syringodium filiforme, the presence or concentration of certain nutrients
might be an important requirement. Although no staminate flowers were
observed on the plants in culture, McMillan found that fruits containing
developing “ovules” were formed on the gynoecious individuals in some culture
series but not in all. Evidently, then, in this species there is an autonomous
apomictic cycle that is independent of pollination.
Two inflorescences developed on plants of monoecious Zostera capensis
Setchell from Kenya after these had been seven and a half months in
experimental culture. Flowering occurred two weeks after the day length had
been increased from 12 to 13 h and the temperature raised to 18 from 16°C,
although it seems likely that the changes associated with floral induction were
essentially determined under the first conditions. Near the completion of the 12-
month study, a single inflorescence appeared on one of three plantings at 24°C
and 13 h day length.
Flowers were not produced on dioecious Syringodium isoetifolium (Aschers.)
Dandy with temperature programmes of 31:27°C or 26:24°C (day: night), nor at
26 and 24°C, during the first nine and a half months of experimental study.
Flowers appeared, however, five weeks after the plants had been transferred to a
special synthetic sea-water medium at 26°C. The sea-water preparation, a
commercial product (“Instant Ocean”) deficient in a number of trace elements, was
also found to be effective in promoting flowering in the Gulf-Caribbean species,
S. filiforme (McMillan, 1980b). Some flowers appeared on plants of S.
isoetifolium maintained in the special sea-water medium at 24°C, but none were
formed during 12 months in the regular sea-water system at 26:24°C.
When plantings of dioecious Thalassia hemprichii (Ehrenb.) Aschers. that had
been grown at 31:27°C (day: night) continuously for 11 months were transferred
to a programme of 28:24°C for two weeks and then subjected to 26:24°C for two
weeks, flower buds appeared on a number of the short shoots. McMillan found
that plants treated with a range of temperatures during the study period, with 26,
24, and 28°C successively, did not produce flowers; nor did replicates that had
been maintained in culture continuously at 26:24°C show any evidence of floral
induction. The stimulation of flowering in those plants exposed to the declining
thermal pattern, both stages being combined with a 13 h day length, clearly
suggests that a lowering of the water temperature is a major inductive influence
of the process in T. hemprichii.
Four other species of seagrasses from Kenya, Halodule univervis (Forsk.)

Ashers., Halophila ovalis (R.Br.) Hook. f., Thalassodendron ciliatum (Forsk.)
den Hartog and Cymodocea rotundata survived in experimental culture but could
not be made to flower under any of the environmental variations tried by
McMillan. On the other hand, plantings of C. rotundata originating in the Palau
Islands have been induced to flower under the same temperature conditions that
promoted floral differentiation in C. serrulata from Kenya (McMillan, 1979). As
McMillan (1980c) points out, however, it could be important to this result that
the cultures of C. rotundata from Micronesia were maintained in water with a
constant salinity of about 35‰, whereas those of C. serrulata from east Africa
were exposed to levels which varied from 35 to 25‰.
Pettitt (1980) has reported a tidally synchronized rhythm of flowering in a
population of Thalassia hemprichii growing on the seaward fringe of a wavecut
platform in southern Kenya. Daily observations and collections were made
throughout a 29-day period in September-October, and the developmental
sequence revealed by the study is presented diagramatically in Fig. 2. The
flowers emerged during the time of neap tides, anthesis and pollination being
synchronous with the succeeding period of spring tides. Considering that the
preparatory events of pollination are precisely timed, this is the period when,
interestingly enough, there is considerable circulation across the platform and the
plants are alternately exposed, or bearly immersed in shallow scour pools, and
then covered by up to 4 m of cold, surging oceanic water. For individual plants
flower persistence was ephemeral, determined as a few hours, and flowering
lasted for not longer than three of four days in the population monitored. As
would be expected on the form of the rhythm, in this habitat plants collected in
the interval following the lowest spring tides (there were two such intervals
during the term of the study: Fig. 2) were found to have developing flowers or
developing fruits.
THE POLLEN AND STIGMA
THE POLLEN
The essential function of the pollen grain, and the pollen tube which it produces,
is to convey and safely deliver the male gametes to the embryo sac in the ovule.
Three fundamentally different types of pollen are encountered in the seagrasses.
The morphological and structural variation is principally related to shape, size
and wall construction since the organization of the contained male gametophyte
is more or less the same throughout the groups.
Spherical grains are produced by two genera of the Hydrocharitaceae, namely
Thalassia and Enhalus. An investigation of pollen development in Thalassia
hemprichii from south Kenya (Pettitt, 1981) has shown that meiosis in this
species occurs when the flower buds are some 3–4 mm in length. Synchrony in
328 J.M.PETTITT
Fig. 2.—Tidally-synchronized reproductive behaviour observed in Thalassia hemprichii

at Tiwi Beaches in southern Kenya: the tide range plotted is for Kilindini Harbour,
Mombasa, for the 29-day period in Sept.-Oct. (after Pettitt, 1980).
respect of the division is found within the sporogenous tissue of an anther but a
measure of asynchrony exists between the anthers of a flower. It could be
mentioned here that the two flowers produced by the androecious individual in
this species have been found to be developmentally out of phase; there is,
accordingly, a delay in anthesis (Pascasio & Santos, 1930; Pettitt, 1980). The
male meiocytes are isodiametric cells having a normal cytoplasmic appearance,
but fluorescence microscopy after Aniline Blue staining has failed to reveal a
callose (1, 3-ξ -glucan) special wall. An invasive tapetal periplasmodium,
staining strongly after cytochemical methods for RNA, protein and
polysaccharide, is seen to fill the spaces between the dividing cells. Although the
events of the chromosome cycle were not observed, the study of the flowering
rhythm in the species at one locality in Kenya (Pettitt, 1980) suggested that the
duration of the meiotic interval is relatively brief. Three distinct categories of
uniplanar tetrad configuration were found to result from simultaneous
partitioning of the pollen mother cells; isobilateral, linear, and T-shaped.
Occurring together with these were a few configurations geometrically
intermediate between isobilateral and T-shaped, and all four arrangements were
present within a single anther. Ultrastructural and cytochemical examination
suggested that in many of the tetrads the four daughter spores produced by
meiosis were normal and functional. In a number of cases, however, post-meiotic
mortality affected one or more of the cells. The factors responsible for
differential development in the tetrads were not discovered, but abnormal

nuclear behaviour preceding cytokinesis suggested that pollen sterility in these
plants is probably a consequence of genetic disability. Three tetrad variants could
be distinguished according to the number of sterile cells they contained. Tetrads
comprising four presumably fertile spores with a normal cytoplasmic appearance
were most numerous. Less common was a class with three fertile spores and one
sterile spore, and a class having an equal number of fertile and sterile spores.
Cytochemical staining at this stage in development showed that callose was
present in the walls partitioning the tetrad and could also be detected between
adjacent abortive spores. This finding would seem to indicate that synthesis and
deposition of the glucan occurred before the onset of cytoplasmic necrosis. No
callose was visible in the tetrad wall, but the material of this wall was shown to
possess a strong affinity for Alcian Blue (a copper phthalocyanin which, under
proper conditions, will bind by salt linkages to polyanions) at pH 2·5 and
dialysed iron (the specificity here resting on the affinity of free acid groups for
colloidal Fe3+ at pH 2·0), both reactions indicating the presence of acidic
polysaccharides. Interestingly, however, the walls that separate the daughter cells
and which contain callose were not stained by these methods.
The free-microspore period in the anthers of T. hemprichii commences when
the flower buds are about 5–6 mm in length. After the spores are released from
the tetrad, a phase of expansion takes place and cytoplasmic vacuolation begins,
which brings about polarization of the microspore contents. At this stage the
spherical, uninucleate microspores are about 35 μ m in diameter and the outer
wall layer of the future pollen grain, the exine, has already been formed. The
exine in this species is represented by a sexine consisting of widely-spaced, free
bacula the bases of which are embedded in a granular-fibrillar basement layer
which stains strongly for acidic and neutral polysaccharides. There is no distinct
nexine layer, but isolated lamellae can be resolved as inclusions in the fibrillar
basement adjacent to the roots of the sexine bacula, and similar structures can be
found between the spore plasmalemma and the inner surface of the
polysac charide stratum (Pettitt, 1976, 1980). The beginning of intine synthesis is
concurrent with the late vacuolate period of development. During deposition of
the intine, evaginations constituted from more of less perpendicular extensions
of the gametophyte plasmalemma and peripheral cytoplasm penetrate the layer,
and towards the close of the binucleate pollen stage the evaginations are isolated
from the gametophyte, to become intine inclusions. Light microscope
cytochemical methods have shown that the enzymes RNase and acid phosphatase
are represented in the intine at this time, and high resolution localization by
transmission electron microscopy has revealed that the principal phosphatase
activity is associated with the cytoplasmic intine inclusions (Pettitt, 1980).
Throughout the microspore period, the tapetal periplasmodium, which is
assumed to have been augmented by the remains of the abortive microspores,
contains distinct Feulgen-positive nuclei and stains for RNA, polysaccharide,
protein, and lipid. Increasing alcianophilia, however, suggests that a rise in the
330 J.M.PETTITT
concentration of acidic polysaccharides accompanies the gradual conversion of

the periplasmodium to the vicid thecal slime in which the pollen of T. hemprichii
is released (Pascasio & Santos, 1930; Pettitt, 1980). A layer of material derived
from the tapetum and staining for polysaccharide, lipid, and protein, the protein
including the enzyme non-specific esterase, can be detected as a covering on the
exine of the mature grain, while staining with ′ -glucosyl artificial carbohydrate
anitgen (Jermyn & Yeow, 1975) illustrates that arabinogalactans or
arabinogalactan-protein is present in, or localized just beneath, the intine layer of
the pollen wall. The carbohydrate content of the thecal slime in T. hemprichii,
measured colorimetrically using the phenol-sulphuric acid reagent with glucose
as a standard (Dubois et al., 1956), was found to be quite low, the amount present
being 5.0 to 5.5% by weight. The monosaccharide composition, determined by
gas chromatography of the trimethylsilyl derivatives (Bhatti, Chambers & Clamp,
1970), is shown in Table II. Electrophoresis of a pollen homogenate using
sodium dodecyl sulphate-polyacrylamide gels produced ten distinct bands
staining for protein and two of these showed a faint reaction following staining
for carbohydrates. These two bands probably indicate the presence of
glycoproteins. Qualitative analysis of the slime fraction by the same method
revealed a single mobile component which had a molecular size of the same
order as the minor of the two glycoproteins detected in the pollen extract. An
estimate of the difference in staining intensity of the bands showing similar
migration on the two sets of gels suggested, however, that the source of the
minor glycoprotein component detected in the pollen homogenate was, in all
probability, thecal slime adhering to the grains and contaminating the preparation
(Pettitt, 1980). In T. hemprichii binucleate pollen grains are characteristic of 6 to
7 mm flower buds. Shortly before pollen release the generative nucleus divides
to produce two gamete nuclei. The ripe pollen grain does not have pre-formed
germinal apertures and is some 80 to 100 μ m in diameter at the time of liberation.
Similarly, the ripe pollen grain in Enhalus acoroides (L.f.) Royle is spherical,
trinucleate, and inaperturate (Svedelius, 1904; Cunnington, 1909; Kausik, 1941;
Pettitt, 1980). The grains are 150 to 175 μ m in diameter and relatively few are
produced in each anther; the actual number has been
TABLE II
Monosaccharides (% by wt) in the thecal slime of Thalassia hemprichii (from Pettitt,
1980)
Monosaccharide % by weight
Rhamnose 2·57
Arabinose 7·83
Xylose 12·32
Mannose 58·83
Galactose 10·12
Glucose 8·33
variously assessed as 120 (Svedelius, 1904), 29 to 98 (Cunnington, 1909), and 56

(Kausik, 1941). Kausik (1941) has investigated flower development in the
species and illustrated the general events of microsporogenesis, and Pettitt
(1980) has described the fine-structural features of the pollen wall. As in Thalassia,
the periplasmodium in Enhalus is invasive (Kausik, 1941) and by the time of
first pollen mitosis the exine of the pollen wall is fully developed. The exine is
constructed of bacula linked to form continuous muri, giving the grain a
reticulate ornamentation (Pettitt, 1980). The bases of the bacula, inserted into a
granular-fibrillar stratum some 400 to 500 nm in thickness, are expanded to form
a continuous nexine 1 (foot layer). Light and electron microscope cytochemical
methods have shown that polysaccharides containing vicinal glycol groups are
present in the granular-fibrillar layer since it includes a component that is stained
by the Periodic Acid-Schiff (PAS) method and that will specifically bind silver
proteinate after brief oxidation with periodate. Ultrastructural staining with
phosphotungstic acid (PTA) in chromic acid and PTA in acetone has revealed
that the periodate reactive polysaccharide is associated with an acidic
component. A thin surface coating on the sculptural elements of the exine was
visible following these methods for polysaccharide detection, but the feature was
less perceptible when conventional uranium and lead salt section contrasting was
employed (Pettitt, 1980).
In the genus Halophila (Hydrocharitaceae) the mature pollen grain is an
ellipsoidal or somewhat reniform body 80 μ m in length and 40 μ m maximum
width. The pollen is released from the anther in ‘strings’, each individual pollen
‘string’ consisting of four grains contained within a transparent moniliform tube.
The morphogenetic processes leading to this strikingly specialized structure have
been described for H. ovata Gaud. by Kausik & Rao (1942) and in H. stipulacea
by Pettitt (1980, 1981). The pattern of development is essentially the same in the
two species. Flower buds 2 to 3 mm in length on the androecious plant of H.
stipulacea contain microsporocytes. These are elongate cells, 240 μ m in length
and 25 μ m in width, which are organized into perfectly parallel ‘files, the
orientation related to the length of the anther loculus. The tapetal tissue which
lines the loculus at this stage is some three or four cells in depth and stains
intensely for protein and RNA. Meiosis is observed in the anthers of 3-mm
flower buds. Successive cleavages divide the elongate mother cell transversely to
produce a dyad and then a tetrad of spores; each product of division is, therefore,
60 μ m in length and they are aligned end-to-end. This linear configuration is
maintained throughout pollen growth and differentiation in the anther, and forms
the unit of dispersal at anthesis. During the division interval, changes affect the
tapetal tissue. The inner, locular walls of the cells undergo dissolution and the
protoplasts combine to form a periplasmodium which, like the source tissue,
stains strongly for protein and RNA and diffusely for polysaccharide. The
combined results from light and electron microscope cytochemistry show that as
the periplasmodium begins to infiltrate between the linear tetrads of microspores
there is deposition of a fibrillar, polysaccharide-rich microspore wall. The
332 J.M.PETTITT
ultrastructural aspects of the process, however, suggest that the components for
this layer are exports from the gametophyte cytoplasm rather than from the
surrounding periplasmodium. Establishment of the microspore wall is soon
followed by formation of the first of the tube substance which will eventually
come to envelope the tetrad. With light microscope cytochemical procedures the
tube substance is found to give a weakly positive result in tests for neutral
polysaccharides but to stain strongly for acidic polyanions, as does the fibrillar
microspore wall beneath. In electron microscope preparations the tube substance
is resolved as a loose web of microfibrils staining with silver proteinate,
supported in a dielectronic matrix material. The microscopically structureless
tube matrix is not affected by periodate oxidation and is probably largely acidic
in nature (Pettitt, 1981). The circumstances of the depositional sequence during
this interval leave little doubt that the structural components of the tetrad tube
originate in the tapetal periplasmodium; none appears to be contributed by the
microspore. It is of interest, therefore, that while standard Coomassie Blue
staining reveals some protein in the microspore wall, none is present in the tube
substance, or perhaps the concentration here is too low to be detected by the
method. In the anthers of 4-mm flower buds that contain binucleate pollen grains,
Azure B and Coomassie Blue staining show that, as a consequence of pollen
growth and further accretion of the tube substance, the periplasmodium has
become compressed between neighbouring tetrads and has intruded along the
walls between the sister grains. Later, as degradation and consolidation of the
periplasmodium takes place, the tetrad tube acquires a continuous surface
overlay, derived directly from the periplasmodium and containing
cytochemically detectable amounts of RNA and protein. It can be supposed that
this superficial proteinaceous coat in Halophila makes intimate contact with the
stigma surface at pollination. Very recently, non-specific esterase activity has
been detected at the tube surface in H. stipulacea and there seems little doubt
that the enzyme is localized in the coat material (Pettitt, unpubl. obs.).
The majority of the marine angiosperms, probably all species included in the
Zosteraceae, Cymodoceaceae and Posidoniaceae, produce pollen grains that are
filiform in shape (Fig. 8 facing p. 334). Of the Zosteraceae, Rosenberg (1901a,
b) has studied pollen morphogenesis in Zostera marina using stained sections of
chemically fixed anthers, while Pettitt & Jermy (1975) have illustrated some
substructural details of microspore and early pollen development in the species.
Stewart & Rüdenberg (1980) have examined microsporocyte growth and meiosis
in Phyllospadix torreyi S. Watson, and the information in this account was
obtained from aceto-carmine stained squash preparations of anther contents fixed
in ethanol-acetic acid. Some genera included in the Cymodoceaceae have
received the same attention. Yamashita (1976) has followed the course of pollen
development in Halodule pinifolia (Miki) den Hartog and H. uninervis, Ducker,
Pettitt & Knox (1978) have investigated the same sequence in Amphibolis
antarctica (Labill.) Sonder & Aschers. ex Aschers., and Pettitt (1981) has
described the principal events in the anther of Thalassodendron ciliatum.
Sectioned and stained material was used in all these examinations. Since certain
features of morphogenesis are found to be common to the various genera, it seems
a reasonable inference that they are general for the entire family.
Successive cytokinesis in the more of less ellipsoidal sporocytes of T. ciliatum
(Pettitt, 1981), Amphibolis antarctica (Ducker et al., 1978) and the two species
of Halodule studied by Yamashita (1976) leads to isobilateral tetrads of
microspores that are the same length as the cells from which they arise. The
characteristic filiform shape of the mature pollen in these species, therefore, is
attained during post-reductional growth and differentiation. In the Zosteraceae,
however, the basic developmental pattern is altogether different, if that described
for Phyllospadix torreyi typifies the family. The available evidence suggests that
in this species the filiform shape is established before meiosis, and the pollen
grain is organized from the elongate division products. The microsporocytes
grow to a length of some 1500 μ m, to nearly the dimensions of the mature grain,
before and during the early stages of meiosis. As successive cleavages then
proceed to divide the mother cell longitudinally, the resulting microspores are at
once very large and filiform (Stewart & Rüdenberg, 1980). It would appear that
these conditions also obtain in Zostera itself (Rosenberg, 1901a, b). The
particular developmental variation, then, is taxonomically circumscribed; pollen
shape is determined either before and as meiotic division begins (Zosteraceae) or
when it is completed, in which case the products do not reach full size until much
later in morphogenesis (Cymodoceaceae).
The young tetrads of Amphibolis, Halodule, and Thalassodendron are
contained within clearly defined, membrane-limited vesicles in the
periplasmodium. In Amphibolis at least, a number of sterile cells in the anther
degenerate as the microsporocytes enter meiosis and evidently contribute to the
periplasmodium. Ultrastructural examination of the tetrad stage in pollen
development in A. antarctica (Pettitt, McConchie, Ducker & Knox, 1984) has
shown that there is no extracellular structure in close apposition to the
microspore plasmalemma that can be identified as a microspore wall. Between
the microspore plasmalemma and the vesicle membrane the lumen of the tetrad
vesicle is filled with a loose-textured fibrillar and flocculent material. This
lumenal material is also seen between, and separates, the sister spores of the
tetrad. In the mid-regions, equidistant from adjacent spores, granular plates can,
however, be resolved. These structures correspond in position to the callose
walls formed across the equator of the phragmoplast and discernible by
fluorescence microscopy (Ducker et al., 1978). At microspore release in A.
antarctica the thecal material infiltrates between the sister cells as they begin to
separate through dissolution of the callose plates. When the process is complete
each microspore is left segregated, quite independently, within a vesicle. The
situation is precisely the same in Halodule and Thalassodendron (Yamashita,
1976; Pettitt, 1981). Once it is formed, the vesicle remains intact, the size
increasing to accommodate growth of the contained microspore and future pollen
grain. Simultaneously with, or following shortly upon, separation of the cells
334 J.M.PETTITT
from the tetrad in all three genera examined—that is, Halodule, Amphibolis, and
Thalassodendron—the microspore nucleus migrates to the terminal position in
the cell. The factors responsible for controlling this behaviour are far from clear
but the observations on T. ciliatum have shown that there is no impedance of
poleward movement in either direction and the nuclei of sister cells can proceed
to opposite poles. On reaching the terminal position, the microspore nucleus
immediately divides to produce the generative and vegetative nuclei, and soon
after a transverse wall forms to define the limit of the generative cell cytoplasm.
The vegetative nucleus begins to return to a more central position in the
vegetative cell. Later in pollen development, as a result of continued extension
growth at the tips of the grain, the generative cell no longer occupies a terminal
position; the generative nucleus divides to form the two gamete nuclei shortly
before anthesis. The ripe pollen grain of Amphibolis antarctica is 2840±590 μ m
in length and 20±2 μ m in diameter and the grain in A. griffithii (J.M.Black) den
Hartog is slightly longer, 3000±600 μ m in length and 19±2 μ m in diameter
(McConchie, Knox, Ducker & Pettitt, 1982). Yamashita (1976) gives the length
of mature Halodule pollen as about 1000 μ m, and the length of the Zostera
marina grain as about twice this. Judging from the information available
(Rosenberg, 1901a, b; Stewart & Rüdenberg, (1980), the nuclear behaviour
described above—movement to a terminal position in the cell preceding mitosis
—is not a regular feature of microsporogenesis in the Zosteraceae. The
circumstances in the Posidoniaceae remain to be investigated.
More than a little attention has been paid to the structural differentiation and
chemical composition of the pollen wall in the filiform grains of the marine
angiosperms (Fig. 6 between pp. 334–335). The matter of interest here is, of
course, the degree of adaptive modification exhibited. Severe reduction or total
absence of the exine—a layer almost always present on the pollen of land-based
flowering plants—has now been documented for several species, although the
sample is still rather small to allow too wide a generalization. Staining of
sectioned anthers with the PAS method, Alcian Blue at low pH and with dialyzed
iron has shown that in Thalassodendron ciliatum during an early stage in the
free-spore period, more precisely, at the time of nuclear relocation, there is
synthesis and deposition of a polysaccharide wall material. Additional wall
polysaccharide is progressively added to the grain throughout the vacuolation
stage, at which time the tapetal periplasmodium is seen to have been reduced to a
residue lacking identifiable organelles. This thecal material stains with
Coomassie Blue and Azure B and is ultimately converted to a thin surface
coating on the walls of the pollen grains. The wall of the ripe, trinucleate pollen
grain in this seagrass consists of a layer of densely-packed microfibrillar
polysaccharide which grades into a less compact zone with more sparse
micro fibrillar content beneath. On the surface of the grain is the thin
proteinaceous deposit, a component acquired late in development, during the
final desiccation of the anther (Pettitt, 1981). Surface coat material, persumed or
shown to be derived from the same source, and presumed or shown to have a
composition which includes protein, carbohydrate and lipid, is distinguishable on

the filiform pollen in Zostera marina (Pettitt & Jermy, 1975), Z. muelleri Irmisch
ex Aschers. (see Fig. 6), Z. capricorni Aschers., Heterozostera tasmanica
(Martens ex Aschers.) den Hartog, Phyllospadix torreyi, and Posidonia australis
Hook. f. (Pettitt et al., 1984; see Fig. 5 facing p. 334) and on the grains of
Amphibolis antarctica (Ducker et al., 1978; Pettitt, Ducker & Knox, 1981;
Pettitt, McConchie, Ducker & Knox, 1980, 1983, 1984) and A. griffithii
(McConchie et al., 1982), as well as on the surface of the tubular dispersal unit in
Halophila decipiens Ostenfeld (Pettitt & Jermy, 1975) and H. stipulacea, as
mentioned earlier. Although it is usually moderately osmiophilic and
adielectronic, in none of these species is the film of extraneous material regarded
as an exine. There are, however, difficulties associated with this interpretation
that cannot be conclusively resolved microscopically. These difficulties arise
because the layer is often too thin to be confidently detected by light microscope
methods and, furthermore, the chemical composition of sporopollenin—the major
component of the exine—provides no means of reliably distinguishing this
polymer from other osmiophilic substances (lipids and related molecules) by
standard electron microscope staining methods. None the less, the evidence
obtained from certain species tends to support the view. For example, Ducker et
al., (1978) have illustrated spectral scans of thin sections through the pollen wall
in Amphibolis antarctica stained with Toluidine Blue at pH 5·0 which show a
single absorption maximum at 560 nm, a response identical to that produced by
the intine polysaccharide in the pollen of the land-based flowering plant used for
comparison. No absorption maxima corresponding to the exine layer of the
terrestrial pollen—in the species examined this was absorbing at 590 and 640 nm
—were detected in the wall of the seagrass grain. Neither was an exine stratum
detected in Amphibolis by fluorescence staining with Auramine O, a
fluorochrome which produces a strong yellow fluorescence in the exine of
terrestrial pollen (Heslop-Harrison, 1979).
To-date differentation of the wall in filiform seagrass pollen has been
investigated at the fine-structural level in a single species, A. antarctica (Pettitt
et al., 1984). An earlier light microscope study of pollen morphogenesis in this
plant (Ducker et al., 1978) indicated that wall formation begins at the vacuolate
period of pollen development when the grains are suspended in the
periplasmodium within membrane-limited vesicles. Electron microscopy
revealed that the first phase of wall deposition begins when grey-staining
particles and small vesicles migrate from the inner face of vesicle membrane,
where they were first detected, into the lumen of the vesicle to take up a position
some distance above the plasmalemma of the grain. Two parallel adielectronic
zones with a separation of approximately 8 nm can be resolved in the finely
granular substructure of the particles, and fine microfibrillar elements are seen as
interconnections between closely adjacent particles. The microfibrils stain
positively with silver proteinate after periodate oxidation and this contrasting
method shows that the microfibrils and particles are associated in a loose, three-
336 J.M.PETTITT
dimensional network. This microfibrillar structure continues to develop until it

completely fills the free space in the lumen of the vesicle, the fluid medium that
occupied the space gradually disappearing. As radial growth proceeds, the
density of fibrils in that part of the structure above the pollen plasmalemma
increases, the observed change being brought about at least partly by physical
compaction. Close packing of the fibrils at the perimeter of the grain establishes
the first stratum of the pollen wall. The microfibrillar component of the inner
region of this layer stains only faintly with the silver proteinate method, possibly
because the high content of largely anionic matrix polysaccharide has a masking
effect. New wall material is deposited during the period of pollen maturation
when the enclosing vesicles are no longer present and the grains are freely
suspended in what remains of the thecal periplasmodium. Early in this interval,
lamellae or short tubules, resembling fragments of membrane, can be detected
intermixed with the microfibrils at the surface of the pollen wall. Small,
amorphous, electron-opaque globular units are frequently discernible associated
with, or in some cases actually attached to, the lamellae. The evidence from the
electron microscope images points to the possibility that the globuli are formed
from granular masses which originate in the tapetal debris remaining in the
theca, contact with the lamellae at the surface of the wall inducing a change in
state. This change is electronoptically visible as conversion from a granular to an
amorphous substructure and an increase in density. In sections stained with
uranium and lead salts, the pollen wall at this period in development is resolved
as two fibrillar strata with clear demarcation between the inner and outer layers.
The outer stratum contains the compound structures as inclusions accumulated
immediately beneath the surface. The wall of the ripe pollen grain at the time of
dispersal is some 800 nm in total thickness, a basic fibrillar organization is
apparent, but stratification of the fabric is very indistinct. Direct staining shows
that the wall is fabricated from polysaccharides, and fragments of the
microfibrillar skeleton can be recovered for negative staining after digestion of
the grains with hot alkali (see Fig. 31 in Pettitt et al., 1984). With the PTA:
chromic acid post-staining procedure the presence of the subsurface zone of wall
inclusions is clearly distinguished in sections of hydrated and germinating
pollen; the chemical nature of these structures has not yet been determined. It
may be significant, nevertheless, that Ducker et al., (1978) have demonstrated
the presence of the enzyme acid phosphatase in the wall of mature, freeze-
sectioned A. antarctica pollen and McConchie et al. (1982) report a general
protein load in the wall of chemically fixed A. griffithii grains. Moreover, the
electron microscope studies show that Amphibolis is not unique; wall inclusions
have been detected in the pollen of Posidonia australis and Heterozostera
tasmanica (Pettitt et al., 1984). Again, without knowledge of their composition
and fate, speculation on the function these structures may possibly fulfil, if any,
is hardly justified.
Returning to the general substructural organization of the pollen wall, the
rather limited available information would tend to suggest that certain features may
have value as taxonomic criteria. For example, subdivision of the microfibrillar

fabric is usually quite evident in the mature filiform grains of the Zosteraceae
(H. tasmanica, Zostera capricorni and Phyllospadix torreyi) whereas this level
of complexity is not exhibited by the Posidoniaceae (Posidonia australis) nor
characteristic of the Cymodoceaceae (Amphibolis antarctica, A. griffithii and
Thalassodendron ciliatum) McConchie et al., 1982; Pettitt et al., 1984).
THE STIGMA
The stigma can be regarded as that part of the pistil or style which receives the
pollen, and as such it has a key rôle to play in angiosperm reproduction.
Compared with the information available on seagrass pollen, that for the stigma
is rather scant. Among the species where the character of the receptive surface
has been examined, an obvious and important morphological difference is
recognized. The receptive surface can be either papillate or non-papillate and
there seems to be some correlation between these two categories and pollen
shape.
In the Hydrocharitiaceae, represented by Enhalus acoroides, Thalassia
hemprichii, and Halophila decipiens, the receptive region of stigma is distinctly
papillate and the papillae are clustered into ridges (Svedelius, 1904; Pettitt 1976,
1980; see Fig. 9 between pp. 334–335). The cellulosic papilla wall in all three
species is bounded by a substantial cuticle which forms an intact, though
sometimes detached cover on the papilla. Closely overlying the cuticle, but not
physically united to it, there is a delicate and continuous pellicle layer. In
Thalassia hemprichii a viscous secretion material that is not dispersed in saline,
and which stains positively for polysaccharide and protein, if found adhering to
the papilla bases. Coomassie Blue staining has demonstrated that proteins are
associated with the pellicle layer in the three species. When mature, receptive
pistils of T. hemprichii and Halophila decipiens are incubated in a simple ester
or indoxyl substrate, non-specific esterase reaction product is found to be
uniformly precipitated on the cuticle of the stigma papillae, the superficial
localization corresponding exactly to that found in respect of general protein.
This result clearly suggests that the enzyme constitutes an important fraction of
the protein content of the papilla pellicle of these marine angiosperms.
Furthermore, cytochemical procedures for light and electron microscope
detection of acid phosphatase both reveal the presence of this hydrolase at the tips
of the stigma papillae. The precise distribution of the metallic salt precipitate
visible under the electron microscope shows the enzyme to be extracellular, but
in this case localized beneath the papilla cuticle, rather than in the pellicle layer.
Results obtained with a lectin-fluorochrome preparation have also shown that
acceptor molecules—specific sugar residues—for concanavalin A (con A) are
present on the stigma papilla in Thalassia hemprichii. The FITC (fluorescein
isothiocyanate)-con A preparation employed in this experiment was bound
specifically to the mature, receptive stigma papillae, the method of detection
338 J.M.PETTITT
Fig. 3.—Filiform pollen grains (sectioned transversely) attached to the stigma in

Posidonia australis (light micrograph, × ′ 3500).
Fig. 4.—Adhesion meniscus attaching the pollen grain to the stigma cuticle in Amphibolis
antarctica (transmission electron micrograph, ×24000: from Pettitt et al., 1980, 1983).
Fig. 5.—The surface coating containing lipid, protein and carbohydrate forming on the
pollen wall in Posidonia australis (transmission electron micrograph, × 24000).
suggesting that accessible saccharides containing residues for the lectin occur
only in the pellicle layer. The specificity of the attachment was confirmed by the
absence of any fluorescence emission attributable to FITC in stigmas pre-
incubated in the competitive sugar ′ -methyl-D-mannoside and then treated with
con A-FITC in the presence of the competitive inhibitor (Pettitt, 1976, 1980).
[To face page 334]
Fig. 6.—Nearly mature filiform pollen grains of Zostera muelleri (sectioned transversely)
before release from the anther (transmission electron micrograph, × 8000).
Fig. 7.—Pollen tube in Amphibolis antarctica growing from the grain: the tip is making
contact with the stigma surface (scanning electron micrograph, × 3000; from Pettitt et al.,
1983).
340 J.M.PETTITT
Fig. 8.—Filiform pollen grains attached to the receptive region of the stigma in Zostera
capricorni (scanning electron micrograph, × 100).
Fig. 9.—Stigma papillae in Thalassia hemprichii: the pellicle layer overlying the cuticle
has wrinkled during perparation of the specimen (scanning electron micrograph, × 650;
from Pettitt, 1976).
Fig. 10.—A pollen tube passing through the epidermal wall of the stigma branch in
Amphibolis antarctica (transmission electron micrograph, × 5000; from Pettitt et al., 1983).
On the other hand, the receptive region of the stigma in the Zosteraceae,
illustrated by Zostera marina (de Cock, 1980), Z. capricorni and Heterozostera
tasmanica (Pettitt et al., 1983; see also Fig. 8), the Cymodoceaceae, illustrated
by Amphibolis antarctica (Ducker & Knox, 1976; Ducker et al, 1978, Pettitt et
al., 1980, 1981, 1983) and Thalassodendron ciliatum (Pettitt, 1976) and the
Posidoniaceae, represented by Posidonia australis (see Fig. 3), is essentially non-

papillate, the receptive cells being flat or slightly bullate. While the taxonomic
range of the survey is perhaps inadequate for a broad generalization, a correlation
between a non-papillate stigma surface and a filiform pollen grain is clearly
indicated by these findings. Of the species listed, the receptive region in
Amphibolis antarctica has been examined in greatest detail and the structural and
morphological features in this plant are probably general for the
Cymodoceaceae, although not necessarily typical of non-papillate seagrass
stigmas as a whole. Pettitt et al. (1983) have shown that the epidermal cells in
the receptive regions of the stigma branches in A. antarctica are covered by a
substantial cuticle. The stigma cuticle is constructed of separate globular units or
rodlets, presumably composed of cutin, with an amorphous embedding substance
between. Electron microscope staining methods demonstrate that
polysaccharides are present in the interstitial substance and that it extends to the
surface of the cuticle where it is continuous with, or possibly forms, a thin layer
of secretion. This secretion layer covering the cuticle in the receptive region of
the stigma branch in Amphibolis corresponds to the pellicle in the
Hydrocharitaceae and has the same basic properties. It does not disperse in
saline, has an affinity for general protein stains and, furthermore, during the
receptive period, exhibits an intense reaction for the enzyme non-specific
esterase (Ducker & Knox, 1976).
POLLINATION
POLLINATION IN ZOSTERA MARINA

Pollination in eelgrass was a subject of fairly intensive study in the last century,
principally by German and French botanists, Hofmeister (1852) and Clavaud
(1878) among them. In more recent times various aspects of the process have
been investigated by de Cock (1980) in plants of the annual ecophenotype
which, since they do not maintain clones, have a limited existence in time. In the
absence of vegetative propagation, within these populations, sexual reproduction
is cardinal for survival. Many of de Cock’s findings have been mentioned in a
previous section in relation to flowering and a summary of the development
timing is presented in Figure 1 (p. 320). To complete the description of the
events here we can consider some of the observations in de Cock’s account
concerned specifically with pollination.
Stylar exsertion is a necessary condition for pollen reception, and once the
grains are attached, the styles begin to reflex. Pollination, geitonogamous if an
alternative is not achieved, determines this behaviour. Notice too (Fig. 1), that
stigma abscission is consequent upon pollination and takes place 7 h or more
after the event, while the first morphological changes associated with seed
development can be discerned about one week later. The spread of the pollen
342 J.M.PETTITT
shadow was found to be negligible in the absence of water movement and some
turbulence is required to ensure dispersion during the period the grains remain
viable. In this connection it is interesting to note that cyclosis had generally
ceased in 90% of the grains 20 h after their liberation, but a few still showed
activity and were presumably viable 48 h after release. The pollen is shed from
the anther passively, not explosively. Apart from these observations, the matter of
pollen longevity in relation to precision of transfer in the seagrasses has never
been examined. What seems clear, however, is that in the marine environment,
as in any other, economical transfer must demand a degree of precision.
Relevant to this, Cox (1983) has presented a mathematical evaluation which
suggests that the filiform shape of the grain greatly increases the search
efficiency.
It appears, however, from de Cock’s studies that in Zostera marina pollen
transfer can, in some circumstances under certain conditions, be within an
inflorescence, or between inflorescences on the same individual, as well as
between individuals. For a population of the perennial form transfer must also be
within and between clones, and since two or more developmentally different
individuals can be identical genetically, the success of any outbreeding
behaviour may well be determined by a factor such as the range of the pollen
shadow. There is evidently no physiological impediment to geitonogamy;
experimental transfer between inflorescences on the same flowering shoot
resulted in seed development. But in none of these instances was the possibility
of pseudogamy investigated (de Cock, 1980).
In a previous study, de Cock (1978) recorded the development of pollen tubes
up to 100 μ m in length from grains attached to Z. marina stigmas. The number of
tubes formed from each grain was extremely variable—from one to as many as
20–and where there were many, there was no consistent pattern of emergence.
The sites were randomly distributed, concentrated towards the middle of the
grain, or localized at one end. Germination was seldom observed in ripe pollen
incubated in artificial sea water at 18–20°C for 3 h, but short tubes, 5–10μ m in
length, were produced from grains exposed to full-strength natural sea water, and
to natural sea water diluted to 50% and 75%, at this temperature. Germination
was not induced in ripe pollen incubated in a medium containing a saccharose
(de Cock does not say which) and boron, or the sugar and yeast extract. A
medium consisting of 50, 75 or 100% artificial sea water containing 10% sugar
and 25 ppt of an extract obtained from Z. marina pistils, however, stimulated
pollen germination, whereas media prepared from the same percentage
concentrations of natural sea water with identical amounts of sugar and pistil
extract were found to enhance pollen tube growth. These results are taken as
providing direct evidence for the presence of an organic substance in the pistil
which has a promotional effect on pollen tube development. The physiological
basis of the response is not known, and the nature of the influence on the
metabolic machinery can hardly be guessed at, nor, unfortunately, is it known
whether the observed effect is limited to conspecific grains. Consequently, it is
not possible to say whether the pistil fraction includes a molecule or molecules
with a specific part to play in determining compatibility reactions.
POLLEN-STIGMA INTERACTION IN AMPHIBOLIS

ANTARCTICA
A study of the normal mechanical events of pollen-stigma interaction in a marine
angiosperm has been made by Pettitt et al. (1980, 1981, 1983) using Amphibolis
antarctica. Mature, flowering specimens of the seagrass were maintained in
tanks of aerated sea water at 14 and 22°C and as the pollen was released it was
collected and applied to the submerged receptive stigmas on the gynoecious
plants. Cytological information was obtained concerning three consecutive
stages in pollination; pollen attachment, pollen germination, and pollen tube
penetration.
Pollen attachment
All the pollen grains captured by the stigma were firmly attached to the receptive
regions of the branches. Microscopical examination of the pollinated stigmas
showed that a meniscus had developed at every point of pollen-stigma contact
and that the two surface components are involved. The meniscus is formed by
coalescence of the proteinaceous coating on the pollen wall and the surface
secretion, or pellicle, covering the stigma cuticle (see Fig. 4 facing p. 334). Such
bonding indicates that the surface materials have waterproof adhesive properties
and requires that they remain physically mobile, at least up to the time of
combining. While adhesion may well necessitate localized alteration in the
chemical properties of the two components which could serve to increase the
efficiency of the bond, no such change could be detected cytochemically. Some
coiling of the filiform grain round the stigma branches typically occurs during
natural and experimental pollination. Clearly, one consequence of this is to
increase the frequency of points of mutual contact and, thereby, the strength of
pollenstigma cohesion.
Pollen germination
Germination begins very soon after the grains are attached to the stigma
branches. First there is slight expansion of the grain and swelling of the pollen
wall, changes believed to be related to hydration. With general slackening of the
pollen wall fabric the basic microfibrillar component becomes difficult to discern
electron-optically but the compound inclusions become clearly visible. It appears
that the modifications in the state of the wall are a prelude to germination since
they are quickly followed by differentiation of the germinal apertures. The
apertures are initiated in positions near to, but never exactly in register with, the
points of pollen-stigma adhesion. The process begins with gelation of the pollen
344 J.M.PETTITT
wall over a small, well-circumscribed area. In light microscope preparations the

further change in the physical aspect of the wall at the incipient aperture is
clearly revealed by a difference in staining characteristics; there is, for example,
a diminished affinity for general polysaccharide stains in these regions. The
nature of the conditions clearly suggests that glycosidases are involved in
localized wall lysis. Moreover, the fact that the aperture never forms at a point of
pollen-stigma contact implies that the enzymes involved in the lytic process are
synthesized and mobilized from within the pollen grain, rather than being
secretion products of the stigma cells. Ultrastructural examination of the
germinating grain at this stage reveals that a large lens of electron-grey,
amorphous polysaccharide materials has been deposited immediately beneath the
future aperture. Germination continues as the weakened zone of the wall is
pushed outwards to form a low surface prominence which then elevates to
resemble a papilla as the sub-apertural lens of polysaccharide moves into
position and likewise hydrates. It is evident that the lax wall offers little or no
elastic resistance to impede the outward movement and this soon disperses, the
lens remaining as a balloon of gel at the apertural perforation. At first, of course,
this apertural feature is without intrinsic rigidity—manifest by the tendency to
burst or collapse—but with the passage of the cytoplasm through the aperture
pollen tube development proper begins and there is strengthening of the wall
which encloses it. Increasing rigidity would be expected if, as seems likely,
microfibrillar cellulose was being inserted into the extending regions to provide
structural reinforcement. Thereafter a tubular growth pattern is established.
Pollen tube penetration

The pollen tube tip grows towards the stigma surface and eventually makes
contact with the secretion layer on the cuticle (see Fig. 7 between pp. 334–335).
Contact must have been followed by enzymic erosion of the cuticle in the
proximity of the tube tip. Although the erosion was not directly observed, the
process is an indispensable pre-requisite for tube penetration into the underlying
stigma tissue. Once the tube has successfully penetrated the stigma cuticle in the
receptive region, it enters the superficial tissue of the stigma branch and can be
readily traced on its course through the outer layer of the epidermal wall (see
Fig. 10 between pp. 334–335) and as it passes inwards between the epidermal
cells on the way to the ovary. Entry of the pollen tubes into the epidermal wall
and their subsequent growth through the epidermal tissue of the stigma branch
leads to a dissolution of the wall fabric and causes a marked alteration in the
ultrastructural appearance of the epidermal cell cytoplasm. The evidence, as far
as it goes, clearly suggests that the tubes release a variety of enzymes the primary
function of which is to facilitate their passage through the stigma.
CONCLUDING REMARKS
The work reviewed in this survey indicates that, the habitat difference
notwithstanding, there are no insuperable technical difficulties to investigating
the reproductive biology in the marine species in the same way as has been
adopted for the land-based flowering plants. The advantage of laboratory
cultivation for such studies is obvious. Now that the conditions for maintaining
mature specimens of seagrasses are known and the factors necessary to induce
flower development determined for many species, the way is open for detailed
analysis of all aspects of sexual behaviour in the groups, This is likely to be the
direction in which future work will proceed. And, from the evolutionary point of
view, of special interest will be the studies expressly designed to extend our
existing knowledge of the mechanical and physiological aspects of submarine
pollination.
The pollen grain is attached to the conspecific stigma in seagrasses by an
adhesion meniscus that is formed by the merging of the pollen and stigma
surface materials the instant these come together (see Figs. 3, 4 facing p. 334).
This exactly parallels the situation in the terrestrial angiosperms (Dickinson &
Lewis, 1973; Heslop-Harrison, Knox, Heslop-Harrison & Mattsson, 1975;
Heslop-Harrison, 1977; Heslop-Harrison, 1978b). It would appear, however, that
the two classes of materials have different qualities. The adhesive in the seagrass
system is insoluble and, as might be expected, the mode of bonding highly
developed for an aqueous medium. By contrast, the stigma pellicle in terrestrial
species generally contains a saline-soluble component and brief exposure of the
stigma to detergent solutions disrupts the layer. Furthermore, such treatments are
also found to affect adversely the ability of the stigma to bind compatible pollen
(Heslop-Harrison & Heslop-Harrison, 1975; Knox et al., 1976; Stead, Roberts &
Dickinson, 1980). Various methods of assay have revealed that the pellicle
components in the terrestrial flowering plants include proteins and glycoproteins
together with glycolipids and carbohydrates, as well as the enzyme non-specific
esterase (Heslop-Harrison, 1975a, 1976, 1978a; Heslop-Harrison et al., 1975;
Knox et al., 1976; Clarke, Gleeson, Harrison & Knox, 1979; Roberts, Stead,
Ockendon & Dickinson, 1979, 1980; Clarke & Gleeson, 1981). Here, again,
there is a feature in common; in the seagrasses the presence of esterase activity is
found to be a distinguishing feature of the stigma secretion or pellicle during the
receptive period. Stead, Roberts & Dickinson (1979) have found that in one land-
based angiosperm incompatible pollen is less firmly bound to the stigma than is
compatible pollen, but structural differences at the points of adhesion are not
electron-optically discernible in these instances (Dickinson & Lewis, 1973).
Similarly, experiments with the marine angiosperms have revealed that within
the diclinous species, geitonogamous pollination (interfloral-intraplant) in
Zostera capricorni and ‘cross-pollination’ (interplant but possibly intraclonal) in
Heterzostera tasmanica leads to the formation of a stable adhesion meniscus at
the points of pollen-stigma contact (Pettitt et al., 1983). This shows that if either
346 J.M.PETTITT
of these species has the capacity to discriminate against the particular association
tested, then however the control is exercised, it clearly does not prevent adhesion.
As was mentioned at the beginning, studies in the land-based flowering plants
have demonstrated the importance of the stigma pellicle layer in the process of
cuticle erosion. Experiments have shown that a compatible pollen tube will not
penetrate the stigma if the properties of the pellicle are impaired (Heslop-
Harrison & Heslop-Harrison, 1975; Knox et al., 1976; Heslop-Harrison, 1977)
and that pollen wall exudates containing hydrolases are not by themselves
capable of causing cuticle lysis; interaction with the pellicle is necessary before
they are effective (Heslop-Harrison, 1976; Heslop-Harrison, 1977). This
discovery has been incorporated in a hypothesis which imputes a rôle for the
cytochemically detectable esterase activity of the stigma pellicle in the digestive
process (Heslop-Harrison, Heslop-Harrison & Barber, 1975; Heslop-Harrison et
al., 1975). Observations satisfy the basic proposition. Significantly, attachment
of compatible pollen to the stigma brings about an increase in surface esterase
activity, and the level is also noticeably enhanced in the vicinity of the tube tip
where this encounters the pellicle (Heslop-Harrison, 1977; Heslop-Harrison, &
Heslop-Harrison, 1981). As an extension of this, it seems entirely possible that
the esterase present in the stigma pellicle and the hydrolases in the pollen wall of
the marine angiosperms signify the same mechanism of cuticle erosion. Of
course, contained in this explanation is the assumption that the mechanism would
provide the same means of regulating fertilizaton (Heslop-Harrison, 1975a, b;
Clarke & Knox, 1978).
It will be apparent from this conspectus that much remains to be learned about
pollination in the marine angiosperms, particularly about pollen-stigma
interaction, and whether this includes any intimate recognition responses
comparable with those that are involved in the control of breeding behaviour in
the land-based relatives.
REFERENCES
Bhatti, E.L., Chambers, R.E. & Clamp. J.R., 1970. Biochim. Biophys. Acta, 222,
339–347.
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ADDENDUM
Since this review was prepared, R.C.Phillips & T.W.Backman (Aquat. Bot., 17,
85–90, 1983) have found that annual Zostera marina growing in the area of
Bahia Kino, Sea of Cortez, Mexico, enters and completes the reproductive phase
before the water temperatures reach 30°C, the lethal upper limit for the species.
The authors conclude that the reproductive pattern of eelgrass at this locality is
probably not an induced one, but a true annual habit, an ultimate response to the
thermal conditions. In another study, R.C.Phillips, W.S.Grant & C.P.McRoy
(Aquat. Bot., 16, 1–20, 1983) have investigated differences in the effectiveness
of sexual reproduction (such as flowering frequency, seed production) in eelgrass
populations on the Pacific coast of North America and relate these differences to
habitat differences. At the southern margin of the range (the Gulf of California)
the plant grows only subtidally, is an annual, and all the individuals flower. The
high water temperatures in summer are lethal, and the eelgrass of each
succeeding year originates entirely from seedlings. At the northern margin of the
range (the Bering Sea), where there is winter mortality, the species is limited to
subtidal areas or intertidal pools. Perennial plants persist and the sexual
reproductive effort was found to be greater than that of subtidal populations in
the central, more temperate part of the range. Here, in the central region, the
species exhibited two methods of reproduction in response to fluctuations in
salinity associated with habitat. In subtidal areas, where such fluctuation is
minimal, dense stands of perennial plants reproduce vegetatively. On the other
hand, annual growth and a high incidence of flowering are found in intertidal
habitats having periodic fluctuations in salinity, where the germination
requirement of the seeds, low salinities, is seasonally provided.

FEEDING IN THE CHAETOGNATHA
DAVID L.FEIGENBAUM and ROBERT C.MARIS
Department of Oceanography, Old Dominion University, Norfolk,
Virginia 23508 U.S.A.
INTRODUCTION
The phylum Chaetognatha consists of some 52 species arranged in seven genera
(Alvariño, 1965). Though fairly similar to one another, chaetognaths are
phylogenetically isolated from other animals and their origin is obscure (Hyman,
1959). All species are either marine or estuarine (Alvariño, 1965) and are strictly
carnivorous (Fig. 1). There are both benthic and planktonic chaetognaths, but it
is the latter which are important in marine food webs. The benthic species, all of
the genus Spadella, are small and minor constituents of their ecosystems. Interest
in Spadella lies principally in the fact that they are easily maintained and studied
in the laboratory (e.g., John, 1933; Parry, 1944; Feigenbaum, 1976) and can help
us understand the behaviour and physiology of their more delicate planktonic
relatives. In the plankton, chaetognaths are often second only to copepods in
numerical abundance. By weight their contribution is even greater (Reeve,
1970a). Chaetognaths are food for a wide variety of larger organisms (Busch,
1851; Bigelow, 1924; David, 1955; Reeve, 1966; Reeve & Walter, 1972a; many
others) and, therefore, occupy a central position in planktonic food webs. Some
species are highly cannibalistic and function at more than one trophic level
(Pearre, 1982).
Major reviews of the phylum have been made by Hertwig (1880), Grassi
(1883), Ritter-Zahony (1911), Kuhl (1938), Hyman (1959), de Beauchamp
(1960), Alvariño (1965), and Ghirardelli (1968) but as most species proved
difficult to keep in the laboratory these provide little information about feeding.
In recent years, significant advances have been made in collecting and
maintaining planktonic chaetognaths in the laboratory. Procedures have also
been developed for estimating feeding rates of natural populations. The result
has been a spate of new studies of chaetognath feeding. These data are presented
here along with the methodology. We hope that bringing this information
FEEDING IN THE CHAETOGNATHA 351
Fig. 1.—Generalized chaetognath.
together will not only prove useful, but also indicate areas worthy of future
research effort.
HISTORICAL BACKGROUND
Historically, living chaetognaths have been difficult to study because they lack a
carapace or other protective covering and are easily damaged in plankton tows
352 DAVID L.FEIGENBAUM AND ROBERT C.MARIS
(Burfield, 1927; Parry, 1944). Darwin (1844) was one of the first to report
observations of living specimens, including movement of the jaws. Even Lebour
(1923) was unable to keep chaetognaths alive for more than a day, although she
used a large (50 l) “plunger jar” which was successful with many other types of
zooplankton. Burfield (1927), despite great care, could not keep Sagitta alive for
more than 24 h, nor could John (1933), although he cultured the benthic Spadella.
Scott (1893) observed one chaetognath eating another half its size, perhaps the
earliest description of a feeding act. Grey (1930) also described a similar event.
Parry (1944) provided the first report of feeding in the laboratory other than by
chance observation. Though he found Sagitta setosa Müller difficult to keep in
the laboratory, he was able to report on the difference between day and night
feeding. Mironov (1960) was also unsuccessful in keeping planktonic
chaetognaths alive. He believed that, like some young fish in captivity, they died
from exhaustion due to extreme movement. The first report of controlled
laboratory feeding was by Reeve (1964) working with S. hispida Conant in
Miami, Florida. Reeve fed Artemia nauplii to Sagitta hispida in small plastic
compartments and presented estimates of the daily ration and weight specific
daily ration for the species. Later, Reeve (1970b) reported the complete cycle of
development in the laboratory for a planktonic species for the first time.
Additional information about feeding in this hardy species was provided in these
and subsequent papers by Reeve, his students and co-workers. About the same
time, Murakami (1966) successfully kept S. crassa Tokioka alive for 34 days
indoors in glass jars and for 106 days outdoors in large concrete tanks.
Protozoans were provided as food for young chaetognaths, and small copepods
for the adults. In recent years, the knowledge gained by the Miami group has
allowed other workers to collect and maintain several planktonic species in the
laboratory.
One of the earliest reports of the chaetognath diet was by Krohn (mentioned in
Busk, 1856). In their guts he found fragments of minute fish, crustaceans and
other chaetognaths. In another early report, Scott (1892) noted that Sagitta lives
on larval and postlarval fishes, copepods and small amphipods. Scott (1893) also
observed that Sagitta is “not fastidious providing the object is of convenient size
to suit the capacity of its jaws”. Although we agree with this comment today, this
view was not always held in the intervening years.
Other early reports of chaetognath feeding come from Shipley (1901), who
included diatoms and infusorians in the diet; Steuer (1910) who presented a
sketch of S. lyra Krohn eating an amphipod, and Lebour (1922, 1923), who made
extensive observations on the gut contents of S. bipunctata Quoy & Gaimard
(probably S. setosa). Lebour recognized the problems caused by feeding in the
net or cod-end jar. Her report that chaetognaths were probably responsible for
the many herring larvae found cut in two or decapitated is, however, probably in
error. Her often-reproduced figures of Sagitta grabbing prey may represent
artifacts of net feeding, because the chaetognaths did not live in the laboratory.
Writing on the plankton of the Gulf of Maine, Bigelow (1924) said, “Sagittae are
strictly carnivorous and so active, fierce, and well armed that it is no wonder they
are recorded as feeding on things as far apart as tintinnids, crustaceans, other
Sagittae, and young fish”.
Wimpenny (1936) made the first attempt to analyse systematically the gut
contents of chaetognaths. He looked at the percentage of S. setosa and S. elegans
Verrill containing food by location and time of year in the south-west North Sea.
He was, however, misled by “green matter” in the guts of young chaetognaths
and believed diatoms were a direct source of food. He concluded that diatom
patches were nursery areas and centres of reproduction for S. setosa and tried to
correlate his feeding data with algal concentrations.
In recent studies the gut contents of chaetognaths have been quantitatively
analysed to allow for estimation of the daily ration and energetic considerations.
These, as well as recent studies on the chaetognath diet are reported in later
sections.
DETECTION OF FOOD
Chaetognaths detect and locate prey by sensing vibrations via sensory hairs
(Horridge & Boulton, 1967; Newbury, 1972; Feigenbaum & Reeve, 1977). They
feed in the dark as well as light (Parry, 1944; Reeve, 1964) and are not visual
feeders (Reeve, 1966). The two ‘eyes’ on the dorsal side of the head have been
examined with both the light (Hertwig, 1880; Grassi, 1883; Burfield, 1927; and
others) and electron microscope (Eakin & Westfall, 1964; Ducret, 1975) and
generally found to lack a lens, necessary for image formation. In most species
these eyes have their sensory cells divided into five parts by opaque pigment
which allows the animal to detect the intensity of light and its general direction
(Burfield, 1927). Phototactic responses can be observed in the laboratory
(Feigenbaum, pers. obs.) and the eyes probably function in vertical migration
(Michael, 1911; Reeve, 1966) and control the vertical distribution in the day-
time (Murakami, 1959, cited in Ghirardelli, 1968). There is also some evidence
that pressure, not light, causes upward movement in S. setosa (Singarajah, 1966).
Alvariño (1962) reported that the eyes of some deep water species (Eukrohnia
fowleri Ritter-Zahony and E. bathypelagica Alvariño) have a central area
“covered with a large number of hexagonal lenses”. She found this structure
reminiscent of the compound eyes of arthropods. If true, these species could be
visual feeders. Newbury (1972), however, took the absence of pigment in these
deep water species as an indication of the relative unimportance of visual
perception. Additional information on the structure of the chaetognath eye is
given in another section (see p. 354).
Three species, all of which feed readily in small Petri dishes, have been shown
to attack a glass and/or metal vibrating probe (Boulton, 1965; Horridge &
Boulton, 1967; Feigenbaum, 1977; Feigenbaum & Reeve, 1977). Attacks were
made to low frequency vibrations (9–20 Hz, Spadella cephaloptera (Busch),
Horridge & Boulton, 1967; 8–150 Hz, S. cephaloptera and S. schizoptera Conant
and 8–500 Hz, Sagitta hispida, Feigenbaum, 1977) from a relatively short
distance (less than 3 mm). Attacks were quite accurate and, in experiments, best
initiated when the probe was near the chaetognath head. Parry (1944) observed
Spadella cephaloptera attacking prey above its head and speculated that the
corona ciliata played a rôle in sensory perception. Chaetognaths can,
however, attack a probe when it is more than halfway down the body. A
vibrating probe near the posterior part of the body will either be ignored or evoke
a fright reaction (unpubl. obs.). Figure 2 shows the attack response curves of the
chaetognaths tested to date superimposed on a background of the reported range
of copepod vibrations.
Fraser (1969) attempted to duplicate Horridge & Boulton’s vibrating probe
experiments using Sagitta elegans, but only succeeded in evoking fright
reactions. He was also unable to get this species to feed in the laboratory. S.
hispida used by Feigenbaum & Reeve (1977), although planktonic, frequently
attached to the sides of its container and was undoubtedly more “comfortable” in
the small dishes used in vibrating probe work. Vibrating probes are physically
difficult to employ with species which will not feed in small dishes. If this
research direction is to be pursued new experimental methodology will have to
be devised.
From the probe experiments it can be seen that the prey most susceptible to
detection, and therefore capture, are those which make a distinct beat in the
water. In this category lie copepods, barnacle nauplii and in particular,
appendicularians (Feigenbaum, 1982). Fish larvae seem to be detected by the tail
beat and the same may be true for the detection of other chaetognaths, although
Feigenbaum & Reeve (1977) found that S. hispida also exhibited a strong
response to lateral motion.
The chaetognath diet is discussed more fully in a later section (p. 361).
Mechanoreception, however, precludes recognition of potential prey which are
not actively moving. This eliminates non-motile algae, eggs, and detritus (Reeve,
1966). Organisms which swim smoothly—such as naked ciliates— also seem to
avoid detection. Reeve & Walter (1972a) found that S. hispida would not grow
on a diet of large ciliates even though the prey were large enough for capture and
handling. Reeve (1966) and Kuhlmann (1977) found that chaetognaths would
not attack fish eggs (Kuhlmann, 1977) or Artemia eggs (Reeve, 1966), even
when swirled in the water. Chaetognaths can be induced to attack an object
pressed against their side and this may account for the occasional instances when
polystyrene pellets (Carpenter et al., 1972), eggs, and dead plankton (Reeve,
1966) have been found in their guts.
The chaetognath sensory hairs are arranged in fan-like arrays in an orthogonal
pattern over the chaetognath body surface (Feigenbaum, 1978). This pattern
permits the organism to respond to vibrations in any direction and, through
triangulation, to know how far the prey is from its body. A large chaetognath
such as S. elegans or S. enflata Grassi has several hundred fan arrays. Hairs
along the length of a 20 mm individual serve to increase its detection range
Fig. 2.—Response of chaetognaths to a vibrating probe: A, Spadella cephaloptera (′ )

from Boulton, 1965), S. cephaloptera (′ ) and S. schizoptera (′ , from Feigenbaum, 1977);
B, Sagitta hispida; the entire figure is from Feigenbaum (1977).
because those on the head alone cannot detect prey that far back. Newly hatched
chaetognaths contain sensory hairs which are proportionally very long (Reeve &
Cosper, 1975; Feigenbaum, 1978). The larvae begin feeding as soon as they have
a functional gut, 2–3 days in S. hispida, S. helenae Ritter-Zahony and S. enflata
(Reeve & Cosper, 1975) and 5 days in Spadella schizoptera (Feigenbaum,
1976).
The sensory hairs have an internal ciliary structure and respond to the ‘near
field’ (particle displacement of water molecules) effect of vibrating objects, not
the pressure wave (Horridge & Boulton, 1967). In this, the sensory hairs act
much like the lateral line of fish and differ significantly from ‘hearing’ type
mechanoreceptors. Unlike pressure waves, near field detection is limited to short
distances because the signal is attenuated very rapidly (Bergeijk, 1964). On
theoretical grounds it can be shown that the signal produced by the feeding
appendages of a 1-mm copepod will be undetectable beyond 2–3 mm. This has
been confirmed by both the vibrating probe trials and by feeding experiments
designed for the purpose (Feigenbaum & Reeve, 1977). Earlier reports of
chaetognaths moving one or two body lengths to attack a prey are, therefore,
inaccurate. Chaetognath sensory hairs were originally considered tangoreceptors
Fig. 3.—The chaetognath head with hooks extended: ventral view; from Reeve (1971).
(touch receptors) (Gegenbaur, 1870; John, 1933; and many others) responding to
physical contact. Though the hairs respond only from a distance, the chaetognath
body itself is sensitive to touch. Both Sagitta hispida and S. elegans will attack
small forceps if they are ‘grabbed’ along their trunk. A touch on the posterior
part will evoke an escape response (Feigenbaum, unpubl. obs.).
Other behavioural observations of a sensory nature were made by John
(1933), who directed a small jet of water against the body surface of
[To face page 348] Spadella cephaloptera after first making the animal
inactive with hyposaline water. With the jet directed at the corona ciliata the
chaetognath attempted to shift its position. John also noted that the corona ciliata
structures of mating individuals often touched. He hypothesized that this
structure was the most sensitive region of the body and functioned as a tactile
organ. He supposed that because the numerous hair tufts had a similar structure
they too would be tangoreceptors. (These hypotheses were not borne out by
probe experiments or morphological examinations and have been discounted by
Horridge & Boulton, 1967).
Bieri (1966b) touched different parts of Pterosagitta draco (Krohn) with a
needle and also observed that Sagitta sp. reacted to a glass rod when it was
moved in the water, but not above it. He was the first to conclude that
chaetognath sensory hairs are not touch receptors, but could respond to
vibrations.
Chemoreception has not been well studied in chaetognaths. In vibrating probe
experiments (Feigenbaum & Reeve, 1977), chaetognaths that grabbed the probe
attempted to ingest it, displaying a clear lack of gustatory sense. Also, neither the
addition of water decanted from a beaker of swimming copepods nor the addition
of crushed copepods into the test vessel enhanced the response of S. hispida
Fig. 4.—Scanning electron micrograph of the anterior teeth of Sagitta hispida: from
Cosper & Reeve (1970).
(unpubl. data). These latter experiments were preliminary, and the possibility
that chaetognaths use chemoreception to bring themselves to the vicinity of prey
has not been examined. The ability to detect pheromones must be considered
likely, because cross fertilization takes place in at least some species
(Ghirardelli, 1968; Reeve & Walter, 1972b).
FEEDING MORPHOLOGY
HOOKS AND TEETH

The name Chaetognatha or “bristle-jaws” derives from the imposing armature of
the chaetognath head, particularly the large grasping spines (Figs 3 and 5). These
spines (or hooks) move individually to grab and entrap prey. The teeth are much
smaller than the hooks, point toward the mouth, have associated vestibular pits
(Burfield, 1927), and may possibly be hollow (Cosper & Reeve, 1970) (Figs 4 &
5). Hertwig (1880) summarized previous knowledge of the hooks and teeth, from
which the following historical comments are taken. Even though the hooks are
obvious, Slabber (1775) overlooked them and they were illustrated as striped
palps surrounding the mouth by Quoy & Gaimard (1827). Darwin (1844)
discovered the small teeth at the entrance of the mouth while Leuckart (1854)
proposed the name Chaetognatha.
In a resting position, the hooks are folded so that the sides touch each other,
with the concave border clinging close to the head and the pointed ends lying
Fig. 5.—Scanning electron micrograph of the head of Sagitta friderici showing the hooks
(H), teeth (T), vestibular pits (VP), and mouth (M): the hood is drawn back; photograph
by courtesy of Belinda Stovall.
near the oral opening. When ready to grasp prey, the small teeth near the mouth
turn outwards and the hooks are extended (Fig. 3). A hood consisting of two
large folds of skin covers most of the head when the animal is not feeding and
folds backward during hook action (Hertwig, 1880). The hooks are supported by
three pairs of plates on the head and elaborate associated musculature (John,
1931). Teeth, hooks, and plates are all made of cuticular products of the
epidermis (Hertwig, 1880; Hyman, 1958). Major studies of the feeding apparatus
were made by Krumbach (1903) and Kuhl (1932).
Cosper & Reeve (1970) were the first to provide electron micrographs of the
chaetognath head region. They identified a papillate vestibular ridge which runs
to the anterior end of the mouth immediately behind the second row of teeth. The
finger-like processes of the papillae resemble sensory hairs on the body and,
Cosper & Reeve believed they may perform a sensory function during ingestion.
Head armature has frequently been used for species identification in
chaetognaths (Ghirardelli, 1968; Nagasawa & Marumo, 1973, 1979; Moreno,
1979; many others).
DIGESTIVE SYSTEM
Anatomy
The alimentary canal of chaetognaths consists of an oesophagus, intestine and
rectum. The centre of the ventral head surface is turned in as a vestibule, lined by
Fig. 6.—Cross section of the intestine of Sagitta: DM, dorsal band of trunk muscles; EP,
epidermis; GC, glandular cells; I, intestine; LM, lateral band of trunk muscles; M,
mesentery; MI, muscle layer of intestine; VM, ventrai band of trunk muscles; redrawn
from Burfield (1927).
a thick cuticle, and leads to the mouth (Hyman, 1959). When feeding, the
vestibule is evaginated with the slit-like or oval mouth assuming an anterior
terminal position (Fig. 5). Following the mouth is a narrow oesophagus that
expands into a bulb-like swelling. The posterior part of the oesophagus forms a
valve that may prevent regurgitation from the intestine (Parry, 1944). The
intestine is a straight, undifferentiated tube. Anteriorly it may send a pair of
lateral diverticula to the head-trunk septum as in Spadella cephaloptera or the
diverticula may be absent as in Sagitta setosa. The intestine is circular to
elliptical in cross section with a narrow but expandable lumen (Fig. 6) (Parry,
1944). Posterior to the intestine is a short tube, the rectum, which leads to the
anus. During defaecation, an entire copepod skeleton can be accommodated
(Parry, 1944). The anus is an oval opening reported to lack sphincter muscles
(Burfield, 1927; Hyman, 1959).
Krohn (1844) and Wilms (1846) provided the earliest anatomical descriptions
of chaetognaths. Hertwig (1880) summarized the digestive structures and
reviewed all previous reports on the phylum. Doncaster (1902) discussed
embryonic development of the digestive system. Burfield (1927), Meek (1928),
and John (1933) provided further studies of the digestive system. Parry’s (1944)
study is the most complete description of the structure and function of the
chaetognath gut. Dallot (1970) studied the intestinal anatomy of 40 species and
classified them according to their arrangement of epithelial cell types.
Histology
Oesophagus. Parry (1944) described two types of cells in the oesophagus of
Spadella cephaloptera (granular and vacuolated) and three types in the
oesophagus of Sagitta setosa (granular, vacuolated, and compound granular)
(Fig. 7). Stovall (1980) studied S. friderici Ritter-Zahony with the transmission
electron microscope and found cells similar to those reported by Parry for S.
setosa. She further divided the granular cells into two types: lateral granular
(Type I) and dorsal granular (Type II). Type I cells were smaller, homogeneous
and contained nucleoid granules. Type II cells were large and fibrous. Stovall
found the vacuolated cells each contained a large vacuole with numerous
partitions made of aggregated vesicles and matrix material. The compound
granular cells could be distinguished by their numerous discrete vacuoles.
Parry (1944) believed both types of cells in the Spadella oesophagus were
secretory. The granular cells were more abundant near the mouth, and he
believed they released a glutinous secretion which entangles the prey and
lubricates the gut. Parry hypothesized that the vacuolated cells liberated a
digestive secretion.
Intestine. Burfield (1927) and Parry (1944) noted two kinds of epithelial cells
in the intestine of Sagitta setosa (Burfield called it S. bipunctata)— glandular
and absorptive (Fig. 7). Parry found the glandular cells similar to the compound
granular of the oesophagus, but Stovall (1980) distinguished between them in S.
friderici, under high magnification. Parry described the glandular cells as being
vacuolated and noted that their exact appearance changed during the digestion
process. These cells were more numerous in the anterior part of the intestine and
he believed they secreted digestive enzymes. Parry found the absorptive cells
were ciliated and most abundant in the posterior part of the intestine. He
hypothesized these absorbed the digestive product and also acted as storage
cells. The cilia maintained a current in the gut lumen, possibly for the removal of
dissolved excretory matter or for respiration. Stovall confirmed the presence of
both types of intestinal cells in S. friderici, but found them distributed uniformly
over the length of the intestine.
Rectum. Parry (1944) found the rectal cells of Spadella were columnar bearing
short cilia. Stovall (1980) found similar cells lining the rectum of Sagitta friderici
with intestinal-type glandular cells scattered intermittently.
NERVOUS SYSTEM
Chaetognaths have a relatively large and differentiated nervous system (Fig. 8).
There are cerebral and ventral ganglia and a circumoesophageal connective, plus
several outlying ganglia. Sensory hairs and body musculature are connected
through a nerve plexus (Bullock & Horridge, 1965).
Krohn (1844) discovered the nervous system of chaetognaths and described it
in great detail. Wilms (1846) confirmed the cerebral ganglion and the optic
nerves, but made some errors. Busch (1851) believed that the ventral ganglion
did not belong to the nervous system at all, but Krohn M (1853) remained
sceptical. Hertwig (1880) summarized the debate which arose among Leuckart
(1854), Meissner (1857), Keferstein (1862), and Kowalevsky (1871) regarding
the function of this structure. Langerhans (1878) provided an extensive
Fig. 7.—Cells of the digestive system of chaetognaths: A-C, oesophagus; D-E, intestine;
A, granular; B, vacuolated; C, compound granular; D, glandular; E, absorptive; redrawn
from Parry (1944).
examination of the nervous system describing various new features. His
description basically holds today, though details have been added by Hertwig
(1880), Grassi (1883), Ritter-Zahony (1908), Burfield (1927), John (1933), Kuhl
(1938), de Beauchamp (1960), Bullock & Horridge (1965), and Huguet (1968).
THE EYE
The chaetognath eye consists of photosensitive cells divided into five parts
(cupulae or cups) by opaque pigment (Fig. 9). Of the five cups, the largest faces
laterally and the four smaller face inward, two above and two below. The nerves
of the visual cells of each cup branch to the optic nerve (Burfield, 1927;
Ghirardelli, 1968). Newly hatched larvae of S. elegans have no visible eye
pigments. The pigments first appear after hooks form from the septum, but
before the anterior fin develops (Kotori, 1975a, b). Eyes were observed and
depicted in newly hatched larvae of S. hispida, but not in S. enflata or Spadella
schizoptera (Feigenbaum, 1978). The eyes were the first observed sense organs
in chaetognaths, having been noted by Quoy & Gaimard (1827, cited in Hertwig,
Fig. 8.—Generalized chaetognath nervous system: A, side view; B, plan; cc, corona
ciliata; cic, circumoesophageal connective; cg, cerebral ganglion; en, oesophageal nerve;
fc, frontal commissure; np, nerve plexus; pc, pharyngeal commissure; pg, pharyngeal
ganglion; shf, sensory hair fan; vg1, ventral ganglion; vg2, vestibular ganglion; redrawn
from de Beauchamp (1960) and Bullock & Horridge (1965).
Fig. 9.—The chaetognath eye (after Burfield, 1927): A, dorsal view; B, lateral view.
1880). There have been many studies of the eye, reviewed by Hertwig (1880),
Hyman (1959), and Ghirardelli (1968).
Eakin & Westfall (1964) were the first to examine the chaetognath eye
(Sagitta scrippsae Alvariño) under the electron microscope and detail its ultra
fine structure. They found the photoreceptors to be of the ciliary type, which has
phylogenetic implications. Ducret (1975) compared the eye structures of Sagitta
and Eukrohnia using the electron microscope and found two basic types:
cupulian eyes in Sagitta and ommatidian eyes in some species of Eukrohnia.
Deeper living specimens of Eukrohnia in the tropics showed a smaller number of
ommatidia than surface specimens from colder areas. Photoreceptors of Sagitta
enflata were the ciliary type like those of S. scrippsae (Eakin & Westfall, 1964),
but S. tasmanica Thomson and S. serratodentata Krohn appeared to have
rhabdomeric photoreceptors. Pigment granule migrations occurred in both S.
setosa and Eukrohnia fowleri with pigmented area enlargement during the night
to facilitate diurnal migration.
SENSORY HAIRS
Fans of fine hairs project from the chaetognath body surface in an orderly
arrangement of transverse and longitudinal rows (Fig. 10). The hair-fans,
previously called tangoreceptors (Feigenbaum, 1978), are immobile in contrast to
those of the corona ciliata, and their function was thought to be tactile. It is now
accepted to be distance mechanoreception (Horridge & Boulton, 1967).
Feigenbaum (1978) illustrated the external hairs for larvae and adults of three
planktonic and two benthic species and reviewed the literature. He found the hair
patterns to be species specific, but generally quite similar. The hair fans are aligned
in rows that run the length of the chaetognath body or in circumferential rings.
Newly hatched larvae have hair fans which are long in relation to their length. In
Sagitta, as the chaetognath grows, fans are added by adding more circumcentric
rings. In Spadella, the number of fans changes little between juvenile and adult.
Instead, the space between rings increases with growth. Hair fans are also found
on the head (except in older Sagitta enflata), caudal fin and extremities of the
second lateral fins (or the one pair in Spadella). Pterosagitta draco has a unique
pair of extremely long and delicate hair fans. These are photographed in Fig. 11
for the first time.
Chaetognaths give the appearance of having two types of sensory hairs
because, when viewed under a light microscope, the transversely orientated hair-
fans appear as single stout hairs, while those orientated longitudinally appear as
delicate fans composed of many hairs (Feigenbaum, 1977; Nagasawa & Marumo,
1978). Most previous illustrations of hairs depict the more obvious transverse
fans (Conant, 1895; Doncaster, 1902; Grey, 1930; Tokioka, 1939; Huguet, 1968;
and many others), although some longitudinal fans have been illustrated (e.g.,
Busch, 1851; Hertwig, 1880; Tokioka & Bieri, 1966). Sensory spots—areas on
the chaetognath body where hairs were lost in preservation—have also received
mention (e.g., Aida, 1897; Alvariño, 1978).
Horridge & Boulton (1967) discovered two distinct types of hairs on the
benthic chaetognath Spadella cephaloptera using electron microscopy. Only one
type, having a ciliary structure, was sensory. The other, termed “bristles”, had an
unknown function. The cilia were finer than the bristles and tended to be
overlooked in living specimens, but preserved better and were usually the hairs
Fig. 10.—Some hair fan patterns in the Chaetognatha: A, Sagitta hispida, 2nd day; B,
Sagitta enflata; C, Sagitta hispida; D, Spadella cephaloptera; B–D all dorsal views of
adults; from Feigenbaum (1978).
studied histologically. Neither type was found consistently orientated in a single

direction. Bone & Pulsford (1978) also described the arrangement of the ciliary
sense organs in S. cephaloptera using electron microscopy. Histological
examination confirmed that the sensory structures were closely packed arrays of
cilia and that all ciliary cells on the body sent axons to the ventral ganglion. Bone
& Pulsford also found that the cilia aligned across the body were twice as
numerous and longer than the cilia parallel to the long axis. This arrangement
facilitates response to movements by the chaetognath’s longitudinal trunk
muscles.
A second type of ciliated cell was found on the ventral surface of the head of
Spadella. The “enclosed ciliary slit receptor” was interpreted by Bone &
Pulsford as a possible chemoreceptor. Still a third type of receptor was isolated
on the tail-fin and caudal region. These large cilia arise singly or in pairs from
surface pits. Bone & Pulsford (1978) believed these cilia to be a second type of
vibration receptor. Small bunches and non-sensory, irregularly distributed
epidermal bristles (not cilia) were also found scattered on the body.
Nagasawa & Marumo (1978) have also studied the ciliary sense organs of
Sagitta nagae Alvariño using the scanning electron microscope. Spero, Hagan &
Vastano (1979) devised a special sedation and handling procedure for electron
microscopic examination of chaetognaths. The process preserved surface
microstructures, including the sensory hairs, and produced fixed specimens in
better condition than had previously been possible.
OTHER POSSIBLE SENSE ORGANS
Corona Ciliata
The corona ciliata (ciliary loop or “wheel organ”) is on the dorsal region of the
body, either entirely on the head or neck or extending to a large part of the trunk.
It is believed to have a sensory function (John, 1933; Parry, 1944) but, except for
a reproductive rôle in Spadella cephaloptera (Ghirardelli, 1968), it is little
understood. Since its discovery, the corona ciliata has also been thought to be
olfactory (Hertwig, 1880) and excretory (Reisinger, 1934). Ghirardelli (1968)
provided a good recent review of the subject.
The name “corona ciliata” is attributed to Grassi (1883), along with the first
detailed description. He observed that the ciliary loop in S. cephaloptera seemed
to be made of two concentric ellipses separated by a median line. According to
Ghirardelli (1968), between the rings in Spadella there is a thin annular canal
that gathers excretory products from granular cells of the inner ring. The outer
ring cells are provided with vibratile cilia and are believed to be sensory. All
pelagic chaetognaths studied to date are missing the glandular part of the corona
ciliata.
Retrocerebral Organ
The retrocerebral organ consists of a pair of club-shaped sacs in the posterior
part of the cerebral ganglion (first noticed by Grassi, 1883), separated from the
nervous tissue by a membrane (Bullock & Horridge, 1965). Although described
by John (1933) and several early workers its function is still unknown. Scharrer
(1965) examined the retrocerebral organ of Sagitta using the electron
microscope. The glomeruli-like mass of presumably glandular follicles
composing the organ were found to be masses of microvilli. Similarities were
noted between the retrocerebral organ of chaetognaths and the cerebral ganglion
of Leptodora kindtii Focke (Cladocera).
THE FEEDING PROCESS

In planktonic chaetognaths, once a prey has been detected the attack is initiated
by a sudden flick of the tail and a flex of the body towards the prey. The prey are
grabbed by the grasping spines which entrap, but do not pierce. These chitinous
‘hooks’ move individually, acting like rigid fingers (Parry, 1944, called them
“prehensile spines”). The lateral plates, to which the hooks are attached, can be
extended from the head, and the chaetognath can actually stuff prey down its
“throat” (Parry, 1944; Feigenbaum, pers. obs.). In Spadella schizoptera the lateral
plates and musculature take on the appearance of a forearm when the
chaetognath is feeding (Feigenbaum, pers. obs.).
The benthic Spadella only swims when disturbed, spending most of the time
attached to surfaces by ventral adhesive papillae on the posterior surface of the
trunk (John, 1933; Parry, 1944; Feigenbaum, 1976). When a copepod swims
above Spadella, the chaetognath makes a rapid upward and backward jerk. At the
same time, the hood is thrown back and the hooks extended. The animal
maintains a firm position on the substratum and does not chase food (Parry,
1944).
Once caught, rigid prey such as copepods are manipulated longitudinally and
eaten endwise (Parry, 1944; see Reeve, 1971). Therefore, prey found in the gut
head first were not necessarily swimming toward the chaetognath when
captured. Softer prey, such as other chaetognaths or elongate fish larvae, may be
grabbed in the middle and doubled over (see Kuhlmann, 1977), but often they
too are ingested endwise. If the prey is too long for the gut it will stick out until
gradually brought in through softening and digestion (see Fig. 14). John’s (1933)
observation that the posterior part of a long prey will be cast off is not in
agreement with our observations. Mironov (1960) noted that the chaetognath
feeding apparatus is not adapted for chewing or biting off prey.
The minimum sized prey which can be eaten is determined by the ability of
the hooks to grasp it. Very small prey such as protozoans and small copepods are
not eaten by larger chaetognaths and they probably do not attack the prey.
Maximum prey size is governed by the mouth opening, which is greater than the
unexpanded head width of the chaetognath (Kuhl, 1938; Sullivan, 1980; Pearre,
1980).
Chaetognaths have one or two rows of small teeth, first noted by Darwin
(1844). The function of these teeth is still conjectural. They appear to be hollow
in electron photomicrographs (see Fig. 5) (Cosper & Reeve, 1970) and have
vestibular pits behind them (see Fig. 4) (Burfield, 1927; Nagasawa, pers. comm.).
Darwin (1844), John (1933), Parry (1944), Hyman (1959), and others believed
that the teeth served to help hold the prey, but this is unlikely, because prey are
easily held by the hooks. Furnestin (1977) suggested that the anterior teeth of
Sagitta hexaptera D’Orbigny could be used not only for gripping of prey, but
also their catch. Burfield (1927) suggested that the vestibular pits were secretory
and could pour a toxin on prey. If so, such a toxin might be injected into the prey
through the hollow teeth. Further support for this hypothesis comes from
observations that copepods stopped struggling and appeared paralysed once
ingested by Spadella cephaloptera (Parry, 1944) and Sagitta hispida
(Feigenbaum, pers. obs.). In preliminary trials, S. hispida were quickly forced to
drop captured prey when the chaetognaths were dashed into a dry dish. In
approximately half the trials, the chaetognaths released the copepods and, in all
cases, these prey were immobile. Other copepods picked up inadvertently by the
pipette were not immobilized. Parry (1944) also found that in Spadella
cephaloptera, while a captured copepod is not dead, if relinquished it is unable to
move away. The paralysing of spiny prey, such as copepods, would prevent
damage to the gut lining of the chaetognath.
Once ingested, prey are wrapped in a peritrophic membrane in at least some
species (Sagitta hispida, Reeve, Cosper & Walter, 1975; S. elegans, Sullivan,
1977; Peters, 1967) and passed to the posterior part of the gut by peristaltic
movements of the gut wall (Parry, 1944). This procedure may take from a few
seconds (Reeve et al., 1975) to more than 30 min (Feigenbaum, 1982) depending
on the species and the temperature.
In some species, such as S. hispida, the prey is moved back and forth within
the gut during the digestive process (Reeve et al., 1975). In others (S. elegans, S.
enflata, and S. tenuis Conant) the prey remains near the anus until defaecation
(Canino, 1981; Feigenbaum, pers. obs.). Grey (1930) reported movement of a
prey back and forth in the gut of S. enflata. S. hispida wraps its prey in a
relatively thick peritrophic membrane whereas S. elegans and S. enflata appear to
secrete much thinner ones. A membrane of this nature may function to protect
the gut lining from the sharp spines of crustacean prey (Sheader & Evans, 1975).
After a copepod has been swallowed by Spadella cephaloptera the
chaetognath gulps water. Parry (1944) suggested the water could carry digestive
secretions liberated by cells of the oesophagus down to the prey. During the
digestive process soft-bodied prey are rendered unrecognizable unless they have
refractory parts. Prey chaetognaths can be recognized by their hooks (Nagasawa
& Marumo, 1979)—the size of the prey can be established from a hook length-to
total length regression, if the hooks are distinctive or only one species is present.
The latter is often the case in high latitudes (see Pearre, 1981). Chaetognath
lateral plates can also be counted
[To face page 358] (Nagasawa & Marumo, 1979). Appendicularian faecal
pellets also resist digestion and Shelbourne (1962) found that the size of at least
one species of Oikopleura could be determined from the size of its pellets.
Copepods, the most common prey, can be identified to species and sometimes
even stage from hard parts such as the mandibles (Sullivan, 1977). In an
advanced state of digestion, the carapace is telescoped or compacted, making
estimates of prey size difficult. Fish larvae are difficult to identify if they lack
pigmented eyes or other dark marks. Kuhlmann (1977) found the digestion time
to be far greater for pigmented species than for clear ones. This would seem to be
an artifact of the observation process.
In Sagitta hispida, the undigested portion of a prey, in its peritrophic
membrane, is defaecated as a single soft ‘pellet’. Chaetognaths that have more
than one prey in their guts at a time usually defaecate them together, the
peritrophic membrane coalescing or connecting in some manner (Reeve et al.,
Fig. 11.—Photomicrograph of Pterosagitta draco showing the very delicate, long hair
fans: ventral view, the dark spots on the head are hooks.
1975) (Fig. 12). In some instances this has been observed even when one prey
was ingested some time later than the other (Feigenbaum, pers. obs.). The
question of whether such prey are digested equally well has not been addressed.
Immediately after defaecation S. setosa swallowed water, thereby distending the
gut anterior to the prey (Parry, 1944). Reeve & Cosper (1975) found that, for S.
hispida feeding on at least three copepods at a time, digestive efficiency was 80%
(54–97%). They used a gravimetric method—feacal pellets were collected and
compared with the weight of food ingested—to obtain this estimate. The
Conover Ratio Method yielded much lower efficiencies (mean, 43%).
Typically, chaetognaths with food have just one prey item in their gut at any
given time. Sullivan (1977) analysed the frequency of multiple encounters in
Eukrohnia hamata Möbius and Sagitta elegans and found that for Eukrohnia the
instances of two, three and other multiple prey numbers were not different than
that predicted by a random distribution. For S. elegans, half the statistical tests
were significantly different than a Poisson distribution, suggesting that either the
prey distributions were patchy or the feeding behaviour of the chaetognath was
more directed than random. Further analysis by Sullivan showed that the longer
the time between feeding events, the more likely that a different species would
be eaten. Given the opportunity, hungry chaetognaths will eat several prey in
rapid succession (Cosper & Reeve, 1975; Feigenbaum, 1982) and a priori it
seems that if most feeding chaetognaths contain only a single prey they are not
often feeding in dense patches.
Fig. 12.—Faecal pellet of Sagitta hispida containing the remains of three copepods: a,
anal sphincter; p, pellet; scale bar is 200 μ m; from Reeve et al. (1975).
METHODS FOR COLLECTING AND MAINTAINING
CHAETOGNATHS IN THE LABORATORY
The history section documents the difficulty early workers had in keeping
planktonic chaetognaths alive in the laboratory for more than 24 h. For successful
maintenance, chaetognaths must be collected in near-perfect condition. Whereas
benthic species are hardy and can be collected by a plankton sled (Feigenbaum,
1976) or shaken from macroalgae (John, 1933), planktonic species will generally
not survive a typical plankton net tow. S. hispida is an exception, which
contributed to the early success of the Florida studies.
Ideally, delicate species should be collected by direct entrapment either by
dipping water from a boat, dock or by hand collection underwater using SCUBA
or snorkeling (Reeve, 1977). This is not always possible or feasible, but has been
used by Kuhlmann (1977). Reeve (1977, 1981) described the net used in Florida
and British Columbia for collecting S. enflata, S. elegans and other species. A
converted 1-m diameter plankton net was modified to hold a 30 1 acrylic cod-end
by having a zipper which attached to a nylonwebbed support bag. The acrylic
tank had four small holes near the top, protected by mesh, to encourage a gentle
downward flow into the reservoir and reduce the volume of water to prevent slop
over on deck. A weight was used for ballast (Fig. 13). The net (102 μ m in some
studies, larger aperture in others) was lowered to depth and retrieved vertically at
a slow pace. Less expensive versions that can expect moderate success can be
Fig. 13.—A “Reeve Net” used to collect undamaged chaetognaths (from Feigenbaum,
1977).
made with smaller nets, using wide-mouthed plastic cannisters normally sold for
kitchen use. Using the “Reeve net”, Feigenbaum (1977) was able to collect the
extremely delicate S. enflata in healthy enough condition to get them to feed in
the laboratory for the first time.
A more sophisticated modification was described by Reeve (1981). In this
arrangement a pair of nets are attached to a vertical wire and lowered to depth.
There, a pressure release is activated and built-in flotation carries the nets slowly
Fig. 14.—Cannibalism: redrawn from photograph by Reeve (1971)

up the wire on nylon rollers. The principal advantage of this arrangement is that
the surface surging by the boat is not transmitted to the nets, keeping the tow as
Fig. 15.—Three stages of digestion of Oithona similis from Eukrohnia hamata digestive
tracts: a, early state—copepod is virtually undigested; b, intermediate state—exoskeleton
is partly compacted and tissue digested; c, advanced state—only mandible (arrow) and
setae from legs remain; from Sullivan (1977).
gentle as possible.
Reeve (1977) described methods for laboratory maintenance of delicate
zooplankton. For chaetognaths, it is often sufficient to keep them in clean water
at low densities. Small amounts of live prey may be added periodically and dead
animals and faecal pellets must regularly be siphoned from the bottom. Aeration
is not always necessary and may be harmful if too vigorous. To prevent
chaetognaths from being entrained and damaged by turbulence, air streams can
be isolated with cylindrical mesh, providing water movement is not strong
enough to draw and hold chaetognaths against it.
Handling should always be done by dipping the animals with a beaker— never
with a net or pipette. Chaetognaths tolerate temperatures lower than those during
surface collection and do better in the laboratory if kept this way. Feigenbaum
(unpubl.) has often kept chaetognaths in wide-mouthed cannisters (2·5 l) at
controlled temperatures in an incubator or low-temperature room.
For feeding experiments, chaetognaths should first be kept in the laboratory
for at least 24 h to allow those damaged during collection to be eliminated
(Reeve, 1977). It has become standard procedure to isolate individually
experimental animals without food for a day before feeding trials, because
chaetognaths are batch-feeders and cannibalistic (Feigenbaum & Reeve, 1977).
Tests should be run in the dark (although this may affect feeding rates), because
both chaetognaths and prey will typically display phototactic responses to room
lighting and aggregate in the experimental container. Most feeding experiments
have random distribution of experimental animals as an underlying assumption.
Feigenbaum & Reeve (1977) found that, even in the dark, prey would not be
randomly distributed without gentle aeration. The size of the experimental
container should be as large as feasible because this approaches natural
planktonic conditions. Reeve & Walter (cited in Reeve, 1977) found that S.
hispida grew faster in progressively larger containers. Excessive confinement
will reduce their activity levels (Reeve, 1977).
Batch-rearing procedures were described by Reeve & Walter (1972a) for the
larvae of S. hispida. Larvae were obtained from eggs laid by adults in a 30–1
aquarium. Water containing larvae was gently siphoned off through a wide (15
mm diam.) tube into a clean vessel without adults. A slow stream of single large
bubbles aerated the new container and 50% of the water was changed at least
three times a week. Live food, sized with plankton meshes, was added as needed
by visual determination. Progressively larger prey were supplied as the
chaetognaths grew.
DIET
As discussed in the section on prey detection, chaetognaths feed on actively
moving prey that transmit a distinctive signal through the water. Prey size is
limited to the range which can be handled by the feeding apparatus and the
mouth (Kuhl, 1938). Chaetognaths begin feeding a few days after hatching on
small prey that they can detect. Tintinnids, though ciliates, swim in a jerky
fashion because of their heavy lorica and are important in the diet of young
chaetognaths (Lohmann mentioned by Kuhl 1938; Mironov, 1960; Pearre,
1981). Because the lorica is readily identified in the chaetognath gut, the
proportion of tintinnids recorded in the diets of young chaetognaths is, however,
probably over-estimated compared with other soft-bodied prey (Pearre, 1981).
Rotifers are also eaten by the youngest chaetognaths (Pearre, 1981). The
mainstay of the diet in most areas, however, are probably nauplii and
copepodites of small copepod species like Oithona sp. (Reeve, 1966, 1980;
McLaren, 1969; Reeve & Walter, 1972a). McLaren (1969) found larval Sagitta
elegans ate copepod nauplii of Pseudocalanus, but the nauplii of the much
smaller Oithona did not appear to support growth in Ogac Lake, Canada.
Reeve & Cosper (1975) found the provision of suitable food a major problem
in rearing larvae of Sagitta hispida in the laboratory. Wimpenny (1936) reported
the stomachs of young S. setosa generally were composed of green matter and he
believed the larvae ate diatoms. John (1933) reported that the Spadella
cephaloptera larvae he kept in the laboratory fed on diatoms and algae after 5–7
days, when their alimentary canal was fully developed. His account of the young
feeding, however, appears confused and most of his larvae died before reaching
the fifteenth day “because they could not be properly fed”. Reeve & Walter
(1972a) found neither ciliates the size of copepod nauplii nor rotifers could
support the growth of larval Sagitta hispida in the laboratory. They hypothesized
that the ciliates swam too smoothly to be detected by the chaetognaths and that
the rotifers were too large. Reeve (1970b) reared S. hispida from the egg, feeding
the newly hatched larvae on natural microzooplankton (passed through a 75 μ m
mesh)—mostly copepod nauplii, some veliger larvae, polychaete larvae and
tintinnids. Murakami (1966) supplied protozoans for the young of S. crassa, and
Feigenbaum (1976) reared Spadella schizoptera larvae on nauplii and
copepodites of calanoid and cyclopoid (Oithona) copepods.
TABLE I
Chaetognath diets expressed as a % of total prey by number; a, number of food items; b,
mostly eaten by young chaetognaths; c, ciliates ignored; d, 0–25 m zone only; e, our
calculation; f, includes “eggs”, which may be parasites non-quantitative report.
Speci Locati . No. Frequ Cope Chaet Tintin Barna Ostrac Polyc Eupha
es on Speci ency ponds ognat ids cle ods hates usiids
mens of hs naupli
with multi i
gut ple
conte prey
nts (%)
Pter Agul 337 6·2 81·3 12·5 — — — — —
osag has
itta Curr
drac ent
o
Near — Very 96 — — — — —
Haw scarc
aii e
Sagi Agul 240 14·2 92·1 6·7 — — — — —
tta has
bipu
mens of hs naupli
with multi i
gut ple
conte prey
nts (%)
nctat Curr
a ent
West 334a 54·1 0·6 — — 0·6 — —
ern
Medi
ter-
ranea
n
Sagi Britis 5772 95·5 1·8 — — — — —
tta h
eleg Isles
ans
Bedf 442 62·1 3·0 11·9b — — 5·1 —
ord
Basi
n,
Scoti
a July
,, 786 89·7 2·5 6·1b — — 0·5 —
Dece
mber
,, Nort 536a 12·0d 99·3 0 — — — — —
Stag heast
e0 Pacif
ic
„ „ 481a 9·4d 95·6 3·1 — — — — —
Stag
e I-
III
Vine 501 98·4 0·4 — — — — —
yard
Soun
d,
Mass
achu
setts
„ 1143 com 31·6 1·4 — — — — —
mon –
79·6
Sagi Kane 944 36·6 44·8 — — — — —
tta ohe
Bay,
mens of hs naupli
with multi i
gut ple
conte prey
nts (%)
enfla Haw
ta aii
Agul 374 12·0 85·3 10·4 — — — — —
has
Curr
ent
West 214a 63·1 1·4 — — — — —
ern
Medi
ter-
renea
n
Sagi West 1071a 68·8 3·6 — — — — —
tta ern
enfla Medi
ta ter-
renea
n
Kane 1522 4·3 53·0c 8·2c — — — — —
ohe
Bay,
Flori 902 1·9 94·8 5·2 — — — — —
da
Curr
ent
Virgi 85·3 0·7 — 14·0 — — —
nia
conti
nenta
l
shelf
Sagi Easte 84·8 — — — — — —
tta rn
euxi Blac
na k Sea
Sagi Agul 41 4·9 90·2 7·5 — — — — —
tta has
fride Curr
rici ent
West 135a 63·7 2·2 — — — — —
ern
Medi
mens of hs naupli
with multi i
gut ple
conte prey
nts (%)
ter-
renea
n
Sagi Sout 45 42·2 13·3 — — — — 40·0
tta hern
gaze Ocea
llae n
Sagi Agul 107 14·4 60·7 30·9 — — — —
tta has
hexa Curr
pter ent
a
Sagi „ 42 21·4 45·2 47·6 — — — — —
tta
lyra
Sagi West 470a 78·1 0·2 — — — — —
tta ern
mini Medi
ma ter-
renea
n
„ 94a 60·6 0 — — — — —
Sagi Agul 44 6·8 77·3 22·7 — — — — —
tta has
robu Curr
sta ent
Sagi Suru 1748 98·6 1·0 — — — — 0·4
tta ga
naga Bay,
e Japa
n
Sagi Pacif
tta ic
scrip Ocea
psae n
Sagi Agul 168 3·0 98·2 1·2 — — — — —
tta has
serr Curr
atod ent
entat
a
mens of hs naupli
with multi i
gut ple
conte prey
nts (%)
Sagi Bay many scarc 59·7 2·1 5·2 5·2 — 0·8 —
tta of e
setos Seva
a stopo
l
“Ope „ „ 48·3 8·2 8·2 — — — —
n
sea”
Bay „ 5·5 0 43·5 Acartia clausi juveniles, 5·5;
of copeod
Seva
stopo
l
Britis 411 72·7 5·1 — — — — —
h
Isles
Sagi Ches 96a 0·3 0·4 — — — — —
tta apea 90·6
tenui ke
s Bay,
Virgi
nia
„ 216a 2·9,
Eukr Nort 384a 10·7d 97·9 1·3 — — — — —
ohni heast
a Pacif
ham ic
ata
Appen Cladoc Larval Dinofl Rotifie Uniden FCR NPC Comm Refere
dicular erans fish agellat rs tified ents nce
ians es or misc
— — — — — 6·2 Stone
, 1969
— — — — — 0·115 Newb
ury,
1978
— — — — — 1·2 Stone
, 1969
ians es or misc
— 26·9 2·4 0·6 Diato 12·9 — 0·196 Diet Pearr
ms, provid e,
1·5 ed by 1974
copep
od
specie
s and
chaeto
gnath
stage
0·9 0·7 — 0·8 Provi Rakus
des a a-
break Suszc
down zewsk
by i,
region 1969
and
fall vs
summ
er.
— — — — 8·2 9·6 0·199 Diet Pearr
provid e,
ed by 1973
chaeto
gnath
stage
— — — — — 1·2 0·234 „ „
— — — — — 0·7 0·372e 0·550e — Sulliv
an,
1977
— — — — — 1·3 0·296e 0·248e — „
0·2 — — — — — — 0·400 Befor Feige
e 10 nbau
March m,
1978 1982
19— — — — — — — 0·564 10 ,,
67 March
1978
— — — — — 7·2 0·429 — Appe
misc. ndicul
aria
possib
ly
under
estima
ted
ians es or misc
becau
se not
recog
nized
when
digest
ed.
57·1%
of all
prey
unide
ntified
.
11·3 — — — — 4·3 — — — Stone
, 1969
— 14·5 0·9 13·1 — 6·6 — 0·459 Diet Pearr
provid e,
ed by 1974
copep
od
specie
s and
chaeto
gnath
stage.
2·2 19·6 0·2 1·1 — 22·0f — 0·77 Data Pearr
are e,
provid 1976
ed
month
ly.
29·2c — — — — 9·6c 0·276 0·288 — Szype
r,
1976,
1978
— — — — — — — 0·295 — Feige
nbau
m,
1979
— — — — — — 0·128 0·162 Abov Bushi
e the ng &
therm Feige
ocline n
only baum,
in
press
ians es or misc
4·3 — — — — 7·4 — — April Miron
1950 ov,
1960
— — — — — 2·5 — — — Stone
, 1969
3·0 10·4 0·7 3·7 — 16·3f — 0·12 Proba Pearr
bly S. e,
setosa 1976
; data
are
provie
ded
month
ly
— — — — — 4·5 — — — David
, 1955
— — — — — 8·4 — — — Stone
, 1969
— — — — — 7·2 — — — „
— 1·1 — — — 20·6 0·070 Diet Pearr
provid e,
ed by 1974
copep
od
specie
s and
chaeto
gnath
stage
— — — — — 39·4f — 0·10 Data Pearr
are e,
provid 1976
ed
month
ly
— — — — — — — — — Stone
, 1969
— — — — — — 0·152 — — Nagas
awa
&
Maru
mo,
1972
ians es or misc
— — — — — — — — Alvar
iño,
1962
— — — — — 0·6 — — — Stone
, 1969
0·4 13·6 0·1 — — 12·9 — 0·20 Septe Miron
mber, ov,
1951 1960
20·1 14·9 — — — 0·3 — — Augus „
t,
1951
nauplii, 3·0; Oithona minuta 43·0 — — 1–2 „
adults, 5·5 Unid. mm
tarvae
only,
Septe
mber
1951
1·0 20·4 — — — 0·7 — — Provi Rakus
des a a-
break Suszc
down zewsk
by i,
region 1969
and
fall vs
summ
er
— 0·4 — — — 8·6 . Provi Canin
0·208 0·224 des o,
diet 1981
by
copep
od
size
class
for six
chaeto
gnath
sizes
— — — — — 0·8 0·353e 0·543e — Sulliv
an,
1977
Copepods are the principal component of the diet of juvenile and adult
chaetognaths by virtue of their abundance in the water column of most marine
ecosystems (Table I). A small number of chaetognaths, are however, routinely
eaten. Barnacle nauplii are frequent prey in coastal areas as are appendicularians
when available. Fish larvae are infrequently found in the guts because they are
scarce members of the zooplankton. Nevertheless, reports of chaetognaths
feeding on young fish are common in the literature (Scott, 1892; Lebour, 1922,
1923; Bigelow, 1924; Kuhlmann, 1977; Nair, 1977; and many others) perhaps
because of the potential impact to man. Cladocerans, euphausiids and
meroplankton can all be a significant part of the diet in a given locality (Table I).
In the laboratory, chaetognaths will feed readily on Artemia nauplii (Reeve,
1964).
Chaetognaths will “snap” at anything under crowded conditions and are often
preserved with their jaws open. Plankton samples are generally swirled when
formalin is added and dying chaetognaths are later found grasping the sides of
large salps, medusae and even their own tails (David, 1955; Reeve, 1970a;
Feigenbaum, pers. obs.). This has led to apparently incorrect reports of the type
of prey eaten (e.g., Massuti-Oliver, 1951, 1954; Alvariño, 1962; Della Croce,
1963), some of which were incorporated by Hyman (1959) in her prestigious
review of the phylum.
Spadella, being benthic, presumably relies on benthic crustaceans such as
harpacticoid copepods and cumaceans for a large part of the diet. John (1933)
maintained S. cephaloptera on harpacticoids, while Feigenbaum (1976, 1977)
reared both this species and S. schizoptera on natural zoo-plankton.
Sullivan (1980) pointed out that chaetognaths can use a very wide spectrum of
sizes and developmental stages of prey. She found the sizes eaten by larger
chaetognaths apparently depended on the relative frequency of prey present. The
actual diet will vary seasonally (Pearre, 1976) and annually (compare Pearre,
1974 and 1976; Piyakarnchana, 1965 and Szyper, 1978), reflecting the
availability of prey and lack of strict selectivity by the chaetognaths.
CANNIBALISM
Chaetognaths are common prey for other chaetognaths (Fig. 14), although by
number they usually comprise a small percentage of the diet (Table I). Whether
the chaetognath eaten is of the same species or not is difficult to determine in
tropical waters where many species may be present. In this review, both true
cannibalism and intraphyletic predation are loosely termed “cannibalism”.
Cannibalism in chaetognaths has been known for some time (Krohn,
mentioned in Busk, 1856; Scott, 1893) and is probably responsible for the
reputation chaetognaths attained as “voracious” predators. Undoubtedly, some of
the observations resulted from the abnormally high densities found in nets and
collecting bottles. Although Burfield (1927) believed that chaetognaths are
“probably not normally cannibalistic”, today there seems little doubt that they
are. Mironov (1960) noted cannibalism in specimens of Sagitta setosa, as small

as 2–3 mm in length, with the highest percentage of cannibalism in the diet of the
4–5 mm size class. Reeve & Walter (1972a) investigated the contribution of
cannibalism to laboratory mortality in S. hispida. They compared the survival of
two groups of newly hatched larvae over 18 days. The first group was reared in a
250-ml beaker whereas the animals of the second were individually isolated.
Dead animals were replaced from a synchronous population. After eight days,
survival of the isolated animals increased over those in the batch culture and by
the eighteenth day survival was 1·5 times higher on a daily basis. Reeve & Walter
(1972b) suggested that for S. hispida cannibalism among mature adults is
behaviourally related to copulation. This does not, however, account for
cannibalism among younger individuals.
Feigenbaum (1979) pointed out that chaetognath prey are larger than copepods
and most other prey, and by weight their contribution to the diet can be quite
significant. Assuming the prey chaetognaths in his study of S. enflata were two
thirds the length (and about half the weight) of the predators, they contributed
from 18–51% of the specific daily ration on a carbon weight basis. Likewise,
cannibalism accounted for 8·2% of the S. setosa diet in the Black Sea by number,
but 26·8% by weight (Mironov, 1960).
Pearre (1982) analysed quantitative reports of chaetognath cannibalism in the
literature. He found chaetognath head width to be the best predictor of the degree
of cannibalism in a given species and arrived at the following best fit multiple
regression for cannibalism as a function of chaetognath size and abundance:
(1)
where, Cs=arcsine transformation of the proportion of chaetognaths among the
diet items, P=chaetognath head width, and U=number of chaetognaths/m3.
Based on energy considerations, Pearre found the cost of acquiring a food item
in relation to its value unfavourable for large chaetognaths unless a considerable
portion of their diet consisted of chaetognath-sized particles. He concluded that
cannibalism may be necessary for the existence of large species.
Pearre’s theory, that larger chaetognaths are more cannibalistic than small
ones, and that cannibalism is dependent almost entirely on the size of the predator,
is not borne out by other studies. Mironov (1960) found cannibalism to be
highest in the mid-sized group of S. setosa and Szyper (1978) and Feigenbaum
(1979) both found the degree of cannibalism in S. enflata populations
independent of chaetognath size. Pearre believes, however, the lower cannibalism
of the larger size classes to be a statistical artifact and the cannibalism of young
chaetognaths to be understated because the prey are difficult to recognize.
Pearre’s model (Equation 1) assumes behavioural differences between species
can be disregarded. Yet, of the six reports for S. enflata, cannibalism averaged
11·9% (1·4–44·8%) in contrast to a mean of 2·0% (0·9–4·0%) for nine reports of
S. elegans (Table I). Even discounting the very high value found by
Piyakarnchana (1965), which has been questioned by Szyper (1978), three of the
five percentages for S. enflata are greater than all nine of those for S. elegans. S.
elegans is at least as large a chaetognath as S. enflata, but has a smaller relative
head size (Table II). S. hispida, one of the most cannibalistic of all species, was
not analysed, apparently because no diet has ever been published for natural
feeding in this species. The possibility of significant behavioural differences is,
however illustrated by the benthic Spadella, which is rarely cannibalistic (Reeve
& Walter, 1972b; Feigenbaum, pers. obs.) (although John, 1933, frequently
observed cannibalism of S. cephaloptera in his cultures when the predator was
more than twice the size of the prey).
The relative head widths of 13 chaetognath species are given in Table II.
Pearre’s (1982) model was derived to fit published data. Future studies should
test his assumptions by carefully looking at cannibalism among the smallest and
largest individuals of a population.
Piyakarnchana (1965) reported that 44·8% of the identifiable prey of Sagitta
enflata in Kaneohe Bay, Hawaii were other S. enflata. In his study, 57·1% of the
material in the guts was unidentified. Some of the latter may have been ciliates
(see Szyper, 1976) which are not true prey. Many undoubtedly were the remains
and faecal pellets of soft-bodied appendicularians which, if counted, would have
reduced the percentage of cannibalism in the diet. Still even with only the 8·2%
cannibalism found by Szyper (1978), cannibalism accounted for 17% of the daily
chaetognath population mortality.
In theory, true cannibalism may be an adaptive behaviour when food is limited,
particularly if it is behaviourly related to reproduction in mature individuals. Too
few data currently exist in the literature for a complete understanding of this
behaviour in chaetognaths. Cannibalism should be investigated seasonally at
various locations to see if it varies with the abundance of other prey.
TABLE II
Head width in relation to body length for chaetognaths (after Pearre, 1980, 1982)
Species Head width/body length ratio
Sagitta bipunctata 0·0676
Sagitta elegans 0·0517
Sagitta enflata 0·0758
Sagitta friderici 0·0710
Sagitta hexaptera 0·0619
Sagitta hispida 0·0782
Sagitta lyra 0·0745
Sagitta minima 0·0460
Sagitta robusta 0·0977
Sagitta serratodentata 0·0586
Sagitta setosa 0·0540
Eukrohnia hamata 0·0618
Species Head width/body length ratio

Pterosagitta draco 0·1169
PREY SELECTION
The question of whether chaetognaths prefer certain prey over others is difficult
to answer. Electivity indices (e.g., Ivlev, 1961) applied to natural gut contents are
of questionable value because many chaetognaths actively undergo vertical
migration and may not have fed in the layer in which they were caught. Pearre
(1973) found that electivities for S. elegans feeding on two surface-dwelling
copepods increased with depth, indicating that the chaetognaths ate near the
surface and rapidly transported the food downward. Even where electivity
indices have been applied to non-migrating stages or species, they are variable.
This reflects the difficulty of estimating the actual availability of the prey with a
tow net on a scale important to the predator (Sullivan, 1980).
Newbury (1972) compared the vibration frequency to which Spadella
cephaloptera responded (Horridge & Boulton, 1967) with the vibration rates of
swimming copepods reported in the literature and concluded that chaetognaths
could select specific copepod species on this basis. Feigenbaum & Reeve (1977)
and Feigenbaum (1977) found, however, the frequency response of S.
cephaloptera, S. schizoptera and Sagitta hispida to be much broader and less
specific than those of Horridge & Boulton (1967). Giguère & Dill (1979), though
working with Chaoborus larvae (Insecta), provided additional evidence that
predators relying on vibrations are unlikely to select prey from narrow frequency
bands. It is also noteworthy that Newbury (1972) compared the benthic Spadella
with planktonic copepods, including some species which are far too large for this
small chaetognath to consume. Also, Feigenbaum (unpubl. obs.) found no
difference in the prey preference of S. hispida on many occasions when both
Paracalanus and Acartia, two copepods which swim quite differently, were
offered as food in the laboratory. Barnacle nauplii, which produce very low
frequency signals when they swim, were also readily consumed by this
chaetognath.
Selection by species or type of prey may be more an artifact of the strength
and clarity of the prey signal or the prey’s ability to avoid capture than an
indication of preference on the part of the predator. The swimming speed and
movement pattern of the prey can, through random encounters, affect the
probability of it being eaten (Feigenbaum, 1977). Chaetognaths do not pursue
escaped prey (Parry, 1944; Nagasawa & Marumo, 1972; Feigenbaum, pers. obs.)
and many chaetognath species are mainly ambush predators. They depend on the
prey’s movements to bring it close enough for detection (see Feigenbaum &
Reeve, 1977; Feigenbaum, 1977, for models of random encounter). Sullivan
(1980) found Eukrohnia hamata of about the same size as Sagitta elegans
consumed more Oncaea than Sagitta elegans in the same layer of the water
column. This may reflect a preference for size rather than species.
Large chaetognaths tend to eat larger prey. Reeve (1966) fed S. hispida (8–9
mm) a mixture of natural zooplankton and found the chaetognaths selected the
larger crustaceans. He obtained similar results using two sizes of Artemia
nauplii. Rakusa-Suszczewski (1969) found that the larger Sagitta elegans
showed a preference for the larger prey available such as copepodites of Calanus.
The author attributed differences in the prey of Sagitta elegans and S. setosa, in
the same sample, to the size differences of the two chaetognath species.
Reeve & Walter (1972a) performed a series of food-size preference experiments
with S. hispida taken from a culture of growing animals. Food of specific sizes was
provided by sieving freshly caught zooplankton through successively finer
meshes having apertures from 50 to 500 μ m. Food of three adjacent size ranges
was offered simultaneously and food left uneaten was sized again and compared
with initial numbers. Food size ranges were increased one step when more than
50% of the largest of the three size fractions was consumed. The authors found
that newly hatched larvae preferred 88-μ m food and the preferred size increased
linearly on a log-log scale as the chaetognaths grew. Reeve & Walter also found
that the relative size of the food (as a proportion of chaetognath head width)
decreased with increasing chaetognath size. The larvae had a food width: head
width ratio of 0·7, while for adults it was only 0·3.
Feigenbaum (1979) divided the S. enflata of his Gulf Stream study into nine 1-
mm length classes and analysed the mean prey weight for each. He found the
weight of the mean prey eaten did not change with chaetognath size. Pearre
(1980) suggested this was due to a dearth of larger copepods in the study area.
The result is more probably caused by the absence of small chaetognaths in the
analysis (none<11 mm). A similar analysis for all sizes of the small form of S.
enflata in Hawaii yielded a significant relationship between prey and predator
size (Szyper, 1976) as did a study of S. elegans in Massachusetts which found
that the weight of the mean copepod eaten increased linearly with chaetognath
length (Feigenbaum, 1982).
Pearre (1980), reviewing data on the relationship between chaetognaths and
the size of their prey, found the best prediction of prey size to be an equation in
the form: H=aPb, where H=prey body width and P=chaetognath head width.
Table III lists the coefficients of this equation for six species. The coefficients
are affected by the natural availability of larger prey. For example, the
relationship is considerably steeper for S. elegans feeding around the British
Isles where large copepods are available (Rakusa-Susczcewski, 1969) than for
the same species feeding in Bedford Basin, Nova Scotia, where only small
copepods are in the plankton (Pearre, 1973). There is also a tendency to over-
estimate the prey size of smaller chaetognaths because smaller prey are more
difficult to identify and are probably digested more rapidly (Pearre, 1980). Pearre
(1980) also found that real species differences exist in the prey size relationships
of S. setosa and S. elegans. Table II, containing chaetognath head width: body
length relationships, also illustrates sizeable differences in relative head size of

the six species analysed.
Consuming larger prey often results in a shift in prey type as the chaetognath
grows. Szyper (1978) found that the largest S. enflata of his study had a greater
proportion of appendicularians in the diet because these prey were larger than the
copepod species in Kaneohe Bay, Hawaii. Rakusa-Suszczewski (1969)
graphically illustrated the change in both prey species and stage of development
with chaetognath size for S. elegans and S. setosa around the British Isles.
Cannibalism, discussed in another section (p. 364), also tends to increase with
chaetognath size and may be related to the availability of other large prey
(Pearre, 1982).
TABLE III
Prey size: predator size regressions, H=aPb: H=prey body width; P=chaetognath head
width; (after Pearre, 1980)
Species a b Location Reference
Sagitta elegans 0·622 0·766 British Isles Rakusa-Suszczewski ,
1969
„ 0·316 0·485 Bedford Basin, Nova Pearre, 1973
Scotia
Sagitta enflata 0·333 0·274 Mediterranean Pearre, 1974, 1976
Sagitta friderici 0·362 0·283 „ „
Sagitta hispida 0·282 0·602 Biscayne Bay, Florida Reeve & Walter, 1972a
Sagitta minima 0·864 0·824 Mediterranean Pearre, 1974, 1976
Sagitta setosa 0·482 0·577 British Isles Rakusa-Suszczewski,
1969
„ 0·388 0·520 Black Sea Mironov, 1960
COLOURATION IN CHAETOGNATHS
Although most chaetognaths are colourless except for the eyes and seminal
vesicles (Bieri, 1966a) colours have been occasionally reported in species
normally known to be clear. We present these records because the colours may
have derived from the diet.
Aida (1897) reported a yellowish-green epidermis and ovaries in living
specimens of Krohnitta pacifica (Aida) and Germain & Joubin (1916) reported a
green specimen of Eukrohnia hamata. Colour in the latter was, however,
possibly due to a piece of copper wire in the sample jar. The gut of orange-red
bathypelagic species such as E. fowleri were found to contain a carotenoid
pigment with many small oil droplets presumably derived from orange-red
copepods in the diet (Furnestin, 1959). Bieri (1966a) described a blue specimen
of Sagitta pacifica Tokioka. He believed either the colour was caused by
absorption of blue pigment after eating pontellid copepods, or was structural, due
to scattering of blue light by fine particles within the body. Terazaki, Marumo &
Fujita (1977) studied the pigments of S. macrocephala Fowler and Eukrohnia
fowleri by chromatographic analysis. All pigments turned out to be carotenoids,
independent of chaetognath species or habitat. Terazaki et al. inferred that the
pigments are synthesized by the chaetognaths themselves, because the pigments
were also different from the pigments in the plankton which formed the
chaetognaths’ diet. Other coloured chaetognaths have been reported by Tokioka
& Bieri (1966), Bieri (1974, 1977) and Feigenbaum (1976).
DIGESTION TIME
Digestion time, defined here as the time from the ingestion of prey until its
defaecation, is important in chaetognath biology. It allows feeding rates to be
estimated from static values obtained from the gut content analysis of preserved
samples, as described later.
Digestion time can be estimated in several ways: (1) direct observation—
getting the chaetognath to feed in the laboratory and timing the process; (2)
partial observation—collecting chaetognaths with food in their guts and using the
longest time to defaecation or an average of the five longest times as an estimate;
(3) the same as (2), but using twice the mean of all times so obtained; and (4)
Szyper’s (1978) method. In this last method groups of chaetognaths caught in
good condition are preserved at different intervals after capture. The proportion
of those with prey, p, is then regressed on the “time to preservation”. The p=0
intercept of the regression line provides the estimate. Either the chaetognaths
have to be isolated (tedious and impractical) or all potential prey removed while
waiting for preservation.
Of the above, method (1) is the most straightforward and has the advantage of
only using animals which are healthy enough to feed in the laboratory. The
difficulties faced with (1) lie in getting the chaetognaths to feed and in providing
a prey-species mix similar to a natural diet. Chaetognaths that feed in the
laboratory must be isolated to prevent them from further feeding. As a practical
matter the chaetognaths are generally starved for a day to induce them to feed on
demand. Methods (2), (3), and (4) avoid the necessity of achieving laboratory
feeding, but require the chaetognaths to be healthy enough for digestion to
proceed at its normal pace.
There are few early estimates of digestion times. Grey 1930) observed a
Sagitta enflata digest a S. friderici about half its size in 40 min and David (1955)
described a S. gazellae Ritter-Zahony ingesting a euphausiid while he watched.
Unfortunately, it died before the prey was defaecated. Parry (1944) kept Spadella
cephaloptera in the laboratory and noted its digestion time was 3–4 h. He had
more limited success in keeping Sagitta setosa and reported that its digestion
probably takes about 5 h. A shorter time was estimated by Mironov (1960) for S.
setosa, using method (2) (longest time to defaecation). Cosper & Reeve (1975)
found that it took S. hispida 3–4 h to digest copepod prey, but their observations
in support of a digestion efficiency study were always based on chaetognaths

which had eaten at least three prey in rapid succession. Table IV lists published
digestion times with as much pertinent information as was available. In recent
years, laboratory studies by Kuhlmann (1977), Szyper (1978), Feigenbaum
(1979, 1982), Reeve (1980), and Canino (1981) have provided precise estimates
for S. enflata, S. elegans, S. hispida, and S. tenuis. Data are, however, still
lacking for most species.
Szyper (1978) observed that the digestion time for large S. enflata was about
the same as for small individuals because, although larger chaetognaths can
digest prey faster, they eat larger prey which take longer to digest. Sullivan
(1980) found the same to be true for S. elegans, but Reeve (1980) presented data
showing digestion time increasing with chaetognath size. When Feigenbaum
(1982) regressed digestion time on the ratio of chaetog nath weight to prey
weight for S. elegans feeding at low temperatures, the regression coefficient was,
however, not significant. It was also not significant for the regression of
digestion time on chaetognath size. Based on current data, it appears that
digestion time is quite variable, even for the same species, and perhaps because
of this, shows little trend with chaetognath or prey size.
The few recent observations of digestion time for cannibalism (Kuhlmann,
1977; Canino, 1981) indicate that digestion may take a little longer because of
the large prey size. This warrants further study because chaetognaths are
frequent prey items, sometimes comprising a significant part of the diet (Table I;
see Pearre, 1982). Multiple prey tend to increase the digestion time and make it
still more variable (Reeve, 1980; Canino, 1981).
Mironov (1960) estimated the digestion time for S. setosa at 2 h (11·5°C) and
at 1·5 h (15·5°C). Through extrapolation he arrived at an estimate of 1 h for 20°C.
Data are also available for S. elegans at different temperatures. Kuhlmann (1977)
estimated a time of 147 min at 15°C, while Feigenbaum (1982) found it to be
614 min at 0°C. Based on these, Pearre (1981, subsequently corrected) developed
the following equation for the relationship of digestion time and temperature for
this species:
(2)
where, DT=digestion time in hours, and T=temperature in °C.
Canino (1981), who made 68 observations, compared digestion times for S.
tenuis at 21 and 25°C and did not, however, find them significantly different.
Obviously, more data are needed to understand the effect of temperature on
digestion time. Due to the fact that many chaetognaths are diurnal vertical
migrators and pass through various temperature regimes, it may be impossible to
determine accurately the digestion time applicable to a given set of samples if
temperature is significant. For a reasonable approximation, Pearre (1981)
suggests that in a given study, a mean digestion time be computed based on the
mean temperature experienced by each developmental stage during the time of
sampling.
Digestion time for S. enflata has been reported from two widely separate
populations. Szyper (1978), using method (4), estimated the digestion time of the
Kaneohe Bay, Hawaii, population at ′ 60 min, while Feigenbaum (1979) using
direct observation, arrived at an estimate of 190 min for the Gulf Stream
population. Temperatures between the two studies varied by only 2°C and
cannot account for the difference. The two populations may, however, be
physiologically distinct. The Kaneohe Bay population is the “short form” of S.
enflata while the Gulf Stream animals are much larger. The great difference in
the two estimates indicates that caution should be taken when using the data from
one population to analyse another.
GUT CONTENT ANALYSIS

It is relatively easy to count and measure the prey in the chaetognath guts,
because they swallow their prey whole and are fairly transparent. The
TABLE IV
Chaetognath digestion times: a data taken from published graph; * 95% confidence
interval; ** plus or minus 1 SD
Species Location Temperature Prey Methods
Pterosagitta — — Copepods —
draco
Sagitta crassa — — Tigriopus —
japanicus
(Copepoda)
Sagitta elegans Bedford Basin, 6 — Casual
Nova Scotia observations
Southern North 15 Copepods Observations
Sea
Sagitta elegans „ 15 Chaetognaths „
and Sagitta
setosa
„ 15 Fish larvae w/o „
pigment
„ 15 Fish larvae with „
pigment
Sagitta elegans Saanich Inlet, — — —
British
Columbia
„ — — —
Vineyard 0 Copepods Observations
Sound,
Massachusetts
Sagitta enflata Society Islands — Chaetognath (S. „
friderici)
Species Location Temperature Prey Methods

Kaneohe Bay, 24–26 Natural feeding Decrease of
Hawaii FCR with time
Florida Current 23 Copepods Observations
Sagitta Southern Ocean — Euphasiids „
gazellae
Sagitta hispida Biscayne Bay, — Copepods Casual
Florida observations
„ — „ Observations
„ 21 Natural mixture „
(mostly
copepods)
„ 21 „ „
Chesapeake 25 Copepods „
Bay, virginia
„ 21 Two copepods —
Sagitta nagae — — Copepods —
Sagitta setosa England — — —
Bay of 11·5 — Longest time to
Sevastopol, defaecation
Russia
„ 15·5 — „
„ 20 — Linear
extrapolation of
observations
Sagitta tenuis Chesapeake — 6·8 mm S. tenuis Observation
Bay, Virgina
” 21& 25 Adults and „
copepodites of
Acartia tonsa
Spadella England — — Casual
cephaloptera observations
Time to reach Digestion time Number of Comments Reference

anal area (min) (min) observations
— 165 — — Terazaki
unpubl., cited
in Nagasawa
& Marumo,
1972
— 360 — — Takano (1971)
cited in
Nagasawa &
Marumo, 1972

60 — — — Pearre, 1973
12·5±4·03** 147±47·05 12 Time to reach Kuhlmann,
anal area, 1976, 1977
combined with
S. setosa
— 200–300 — —
20·2±3·9** 55(30–90) 3 —
Combined with 314(180–480) 9 —
above
— 210 43 Mature Reeve unpubl.,
chaetognaths cited in Reeve,
1980
— 240 21 Range of sizes. Sullivan
No correlation unpubl., cited
between age in Reeve, 1980
and digestion
time
15–30 614(273–1000) 17 Independent of Feigenbaum,
chaetognath 1982
size and of
relative prey
weight. 5 of 17
were multiple
prey
8 40 1 Grey, 1930
0·5;<2 60 — Only two Szyper, 1978
observations of
time to anal
area
190·2±48.6* 13 — Feigenbaum,
1979
60 — 1 Died before David, 1955
defaecation
180–240 — At least 3 prey Cosper &
in gut for all Reeve, 1975
observations
0·13 — — — Reeve et al.,
1975
60–120 (1 mm) 250 Single prey. Reeve, 1980
(6 mm) Digestion time
increased with
chaetognath
size
— 150–240a (1 — Chaetognaths
prey)-(8 prey) 8–10 mm.

Digestion time
increased with
number of prey
— 52·8 1 Predator was Canino, 1981
10·7 mm
— 137·4 1 Predator was
10–9 mm
— 120–300 — — Terazaki
unpubl. cited
in Nagasawa
& Marumo,
1972
— 300 — — Parry, 1944
— 120 — — Mironov, 1960
— 90 — —
— 60 — —
— 145·8 1 Predator was Canino, 1981
10–4 mm
6–10 69·2(28–119) 68 Independent of
chaetognath
length.
Difference at
two
temperatures
tested not
significant.
Multiple prey
increased
variability at
25 °C
60·1 single prey
77·3 multiple
prey
2–8 180–240 — — Parry, 1944
analysis of chaetognath gut contents has been considerably refined in recent

years to provide quantitative information about feeding rates and energy flow.
The assumptions of gut content analysis when used in this manner are as
follows.
(1) That prey species are equally identifiable in the chaetognath gut. This is
probably false (Pearre, 1974) and those species which lack identifiable
features will be under-estimated in the diet.
(2) That all prey are digested at the same rate. This also seems likely to be false
(Pearre, 1974), although available data are insufficient to provide a
definitive answer. Differential digestion rates can, however, be accounted
for when digestion times are estimated.
(3) That cod-end feeding is either negligible or can be discounted in the
subsequent analysis.
(4) That the chaetognath neither regurgitates nor defaecates prey due to the
preservation process. Sullivan (1980) observed the gut contents of S. elegans
during preservation and observed no loss, but this area warrants further
investigation. Feigenbaum (1977) used cold formalin to reduce the
possibility of such preservation losses.
That digestion times measured in the laboratory are applicable to feeding
in nature (Reeve, 1980).
A number of ways have been devised to reduce the effect of (3) above, because
chaetognaths are notorious cod-end feeders. Cod-end feeding can be reduced by
increasing the mesh size or by making shorter tows and rapid preservation of the
catch. The former is, however, at the expense of losing the smaller chaetognaths.
Feigenbaum (1979) used a 1600 μ m mesh net which was sewn closed at the
bottom in his study of S. enflata in the Gulf Stream. Virtually all potential prey
passed through the mesh, but very few chaetognaths smaller than 10 mm (length)
were retained. Sullivan (1980) used a bongo arrangement with different mesh
sizes (183 and 333 μ m) in her study of feeding in S. elegans and Eukrohnia
hamata. For gut contents she analysed the chaetognaths from the larger mesh
while the smaller mesh net provided an estimate of available prey. A comparison
of the gut contents from the two nets allowed some estimate of cod-end feeding
and she found more net-feeding on small prey by Sagitta elegans than Eukrohnia
hamata. Evidently, the amount of net-feeding is also dependent on the chaetognath
species.
In addition to reducing the amount of cod-end feeding, workers have tried to
account for it by eliminating all prey found in the forward part of the digestive
tract. Sometimes called “% forward” (Pearre, 1973) or PI, (Nagasawa & Marumo,
1972, 1976), this generally accepted technique assumes that the amount of time
it would take for prey to be ingested and passed to the posterior of the gut is
greater than the mean tow plus preservation time. Table IV lists estimates of the
time it takes for prey to reach the anal area. Reeve, Cosper & Walter (1975)
observed that transfer to the rear of the gut was very rapid and a poor indicator of
cod-end feeding and Szyper (1978) agreed. Feigenbaum (1982) eliminated the
“% forward” in his study, because Sagitta elegans had been feeding at very low
temperatures and passage of prey through the gut was slow. While eliminating
prey in the “% forward” category may not account for all food eaten in the net, it
should at least improve the estimate. Table IV shows that most studies have
found passage of the prey to take minutes, not seconds as Reeve et al. (1975)
believed.
Several authors (Nagasawa & Marumo, 1972, 1976; Pearre, 1973; Feigenbaum,
1979, 1982) have divided the prey found in the gut into three groups (Fig. 15): (a)
the “% forward”, or number of prey in the forward half of the gut (PI); (b) those
prey that are in the rear of the gut and partially digested, but still recognizable
and/or measurable (PII); and (c) prey in an ‘advanced’ state of digestion, which
cannot be identified or measured (PIII).
Standard practice is to eliminate (a) from the quantitative analysis (being
attributed to cod-end feeding) and to count those prey in (c), applying
measurements of size and/or identifications from (b) to this group also. The
additional assumption is that the prey in (c) can also be represented by (b)
(Pearre, 1974).
Knowledge of the digestion time is necessary before further inferences can be
made from the categories above. For example, the “% forward” can be an
indication of the depth or time where chaetognaths are most actively feeding, if a
large mesh has been used to eliminate net-feeding. Pearre (1973) combined (a)
and (b) to obtain a “% fed” which he used as an indication of active feeding.
When the digestion time is only on the order of an hour or so, even the most highly
digested prey may still have been eaten in the layer the chaetognath was caught.
In analysing gut contents, Sullivan (1977) mounted each chaetognath (S.
elegans and Eukrohnia hamata) in glycerine and dissected out the rear gut. She
found up to 30% of the prey were not visible through the body wall. Using
copepod mandibles and chaetognath hooks, Sullivan was able to identify almost
all prey to the species level. When species identifications were not sought,
Feigenbaum (pers. obs.), working with Sagitta enflata and S. elegans, found
dissection of the gut unnecessary in most cases. In his method, several
chaetognaths were laid out on a single slide and covered with sea water for
examination. The application of cover glass pressure was sometimes helpful.
The food containing ratio (FCR) is the percentage of chaetognaths with food
in their guts, generally taken as PII+PIII. The number of prey per chaetognath
(NPC) exceeds the FCR because some predators will have multiple prey. In
general, multiple prey are not common in chaetognath guts (Table I). Newbury
(1978) found them very scarce in Pterosagitta draco in Hawaiian waters and
Mironov (1960) characterized multpile prey in Sagitta setosa of the Bay of
Sevastopol, Russia, and Black Sea as “extremely rare”. There were two or more
prey in only 1·9% of the S. enflata studied by Feigenbaum (1979) and in 4·3% of
those of Szyper (1978). Sullivan (1977), however, found multiple prey more
numerous in S. elegans and Eukrohnia hamata of the surface zone (9·4–12·0%)
and Feigenbaum (1982) found 42 instances of five prey or more in the guts of
Sagitta elegans when appendicularians (Fritillaria) were in the water column in
Massachusetts. He attributed this exceptionally high number of multiple prey to
the strong, distinctive signal produced by this larvacean, which lives outside its
house and would seem to be particularly vulnerable to predation. Tintinnid
ciliates, prey for young chaetognaths, are also consumed in quantity
TABLE V
Chaetognath feeding rates: a, maximum ingestion rate during experiments; b, data taken
from graph; c, based on our calculations using their data; GCA =gut content analysis,
LAB=laboratory feeding experiments
Species Location Temperatur Chaetognath Daily ration Specific
e (°C) length (mm) No./day daily Dry wt
basis
Pterosagitt Near 12–25 5·0–7·0 1·0 —
a draco Hawaii
Sagitta Saanich 13 16 4a —
elegans Inlet,
British
Columbia
Vineyard 0 3·5–20·5 0·53–1·33 0·465–
Sound, 0·006
Massachus (3·5mm–
etts 20·5mm)
„ 0 „ 0·7–6·0
Saanich — mature ′8 —
Inlet,
CEPEX
bags
Sagitta Southern 15 10–22 2·04c 0·062
elegans North Sea
and
Sagitta
setosa
combined
Sagitta Kaneohe 24–26 4–13 7·4
enflata Bay,
Hawaii
Florida — 12·5–20.5 2·23 0·124–
Current 0·077
(12·5mm–
20·5mm)
„ 21 17 10a —
Virginia 25·4 3·2–23·0 1·25 —
continental
shelf
Sagitta Eastern — — 2·53 —
euxina Black Sea
Sagitta Biscayne 24 8·5 40–50 —
hispida Bay,
Florida
„ 24 2·5–9·5 5–60b —
,, 24 8·5 50b 0·64
„ 16 6·9 10·8c —
Species Location Temperatur Chaetognath Daily ration Specific

e (°C) length (mm) No./day daily Dry wt
basis
„ 21 7·0 14·1c —
„ 26 6·9 23·7c —
„ 24–26 larvae — ′ 1·0
„ „ adult — ′ 0·10
Sagitta Suruga — — 0·9c 0·188c
nagae Bay, Japan
Sagitta Bay of 20 1–10 4·8c l·68–0·072c
setosa Sevastopol, (larvae-
Russia adult)
Sagitta Chesapeak 21+25 4·5–9·5 5·36 0·358
tenuis e Bay, (0·644–
Virginia 0·214)
(4·5mm–
9·5mm)
ration Carbon Nitrogen basis Phosphorus Comments Reference

basis basis
— 0·02 — GCA. Newbury, 1978
Digestion time
from the
literature for
another species
0·003–0·035b — — LAB. Varying Reeve, 1980
with food
concentration
— — — GCA. Before Feigenbaum,
appendicularia 1982
ns.
— — — GCA With „
appendicularia
ns
0·19 — — GCA Sullivan,
unpubl., cited
— — — LAB. in Reeve, 1980
Copepods and Kuhlmann,
fish larvae 1976, 1977
combined
— 0·607(2·06– 0·898(2·74– GCA Szyper, 1976,
0·253) (4mm– 0·394) (4mm– 1978
13mm) 13mm)
0·704 for 1·11 for
popula-tion population

basis basis
0·264–0·144 — — GCA. Feigenbaum,
(12·5mm-20·5 Assumed prey 1979
mm) chaetognaths
were 2/3
length of
predators
0·0025–0·105 — — LAB. Varying Reeve, 1980
with food
concentration
— — — GCA. Bushing &
Expatriate Feigenbaum,
population in press
— — — GCA. Based Mironov, 1960
on erroneous
graphic
analysis
— — — LAB. Artemia Reeve, 1964
prey. Day vs
night
— — — LAB. Artemia „
prey. DR vs
size
— — — LAB. Artemia „
prey. DR vs
density
— — — LAB Artemia Reeve, 1970a
prey
— — — „ „
— — — „ „
— — — Unpubl. data Reeve &
Walter, 1972a
— — — „ „
— — — GCA. We Nagasawa &
calculate half Marumo 1972
the rates the
authors did
— — — GCA. The Mironov, 1960
author
calculated 2·5/
day
0·412(0·809– 0·327(0·626– — GCA. Prey Canino, 1981
0·220) 0·181) 91·8%
copepods.
SDR
decreasing

basis basis
with increasing
chaetognath
size
(Mironov, 1960) and recognized by the lorica which resists digestion (Pearre,
1973).
Chaetognaths are frequently parasitized by trematodes, cestodes, gregarine and
ciliate protozoans (Nagasawa & Marumo, 1979), some of which can be confused
with prey. The protozoans are too small for larger chaetognaths to eat directly
and undoubtedly enter the chaetognath with its normal prey. Ciliates, sometimes
of substantial size, can often be seen actively swimming inside the gut of a live
chaetognath. Careful observation will show that they are also discharged with the
faecal pellet, still swimming actively. Parry (1944) noted that apostomous
ciliates enter the chaetognath while encysted on the outside of a copepod prey.
Apparently, the ciliates are activated when the copepod is damaged by the
chaetognath and they enter the copepod while it is being digested. These ciliates
were also discussed and photographed by Kuhl (1938). Szyper (1978), although
recognizing the ciliates were not digested normally, incorrectly believed that they
were prey organisms.
The equivalent of the FCR is often reported in earlier papers (e.g. Wimpenny,
1936; Mironov, 1960) and sometimes wrongfully equated with feeding rate. For
a comparison of FCR’s to be meaningful, both the chaetognath species and
temperature must be identical (see p. 380). Jakobsen (1971) compared FCR’s for
Sagitta elegans caught in epibenthic toboggen tows with FCR’s from several
water layers above the bottom in inner Oslofjord, Norway. He found the bottom
FCR’s at the two stations were comparable with those in the next deepest layer
(bottom to 20 m), providing a strong indication that the epibenthic individuals
were active and healthy.
FEEDING RATES
DAILY RATION
Bajkov (1935) seems to have been the first to recognize that daily feeding rates
could be estimated from the average amount of food in the stomach and the rate
of digestion. His formula, developed with regard to feeding in fish, is presented
here (with different symbols):
(3)
where, FRN=daily feeding rate in number of prey per day, DT=digestion time in
hours, and NPC=number of prey per chaetognath, from gut content analysis.
Mironov (1960) attempted to apply digestion times to gut contents in order to

estimate feeding rates for S. setosa, but did not understand the relationship.
Feeding rates from his data have been re-calculated in Table V.
Equation 3 was first applied to chaetognaths by Nagasawa & Marumo (1972)
who estimated feeding rates for S. nagae in Suruga Bay, central Japan. Not
having a digestion time for the species, they used a literature value (4 h) and then
incorrectly applied only half this number. Nevertheless, their use of Equation 3
paved the way for Szyper (1978), Feigenbaum (1979, 1982), Canino (1981), and
Bushing & Feigenbaum (in press) to estimate natural feeding rates in three
species (S. enflata, S. elegans, and S. tenuis).
The NPC should be a mean of at least two estimates, one for daylight
collections and the other for after dark, because chaetognaths feed more
frequently at night than during daylight hours (Reeve, 1964; Nagasawa &
Marumo, 1976; and many others). For his study of S. enflata feeding in the
Florida Current, Feigenbaum (1979) divided the day into four parts: midnight to
sunrise, sunrise to noon, noon to sunset, and sunset to midnight. Although the
difference was not statistically significant, NPC’s were higher during the hours
of darkness.
In estuarine situations it is likely that timing in relation to the tidal cycle will
also be an important consideration. A large number of samples, taken through
both tidal and day-night cycles, will be necessary to sort out the significance of
each.
Feeding rates by weight can be estimated by the application of a “mean prey
weight” to Equation 3 (Equation 4):
(4)
where, FRw=daily feeding rate by weight, and MPW=mean prey weight.
Feigenbaum (1979) divided the S. enflata of his study into nine, 1-mm size
categories and analysed the prey size of each. When the weights of the mean
copepods eaten were regressed on chaetognath length, the slope was not
significant and a pooled mean weight was used in all calculations. Because
NPC’s increased with chaetognath size, both the FRN and FRW also increased.
Figure 16 illustrates the way the daily ration typically varies with chaetognath
size.
Szyper (1978) presents a slightly different, but more confusing, formula for
calculating daily feeding rates. His equation is:
(5)
where, f=daily feeding rate=FRN, b=a “batch” factor defined as the number of
batches per hour, this is equivalent to NPC/FCR/DT, p=the per cent with
food=FCR, and d, n=subscripts which indicate day and night samples.
In the paper, f is incorrectly described as equal to b/p in two places, although
the actual calculations use Equation 5. Szyper treats day and night periods as
lasting exactly 12 h each, a simplification which will lead to errors when used in
higher latitudes. Further potential for confusion exists because Szyper’s digestion
Fig. 16.—Daily ration (—) and specific daily ration (—) for Sagitta enflata feeding in the
Florida Current: DW, dry weight; C, carbon weight; from Feigenbaum (1979).
time was exactly one hour and digestion time per se does not appear in his
calculations.
Table V lists feeding rates available from the literature. Daily rations vary
from 0·53 prey/day for young S. elegans feeding at 0°C to 60 Artemia nauplii/
day for adult Sagitta hispida feeding in the laboratory at 24°C. Most field values
fall in the 1–7 prey/day range, while laboratory values, mostly for S. hispida, are
higher. Surprisingly, there are no data available for S. hispida feeding in nature.
It would be particularly interesting to see if feeding rates in nature are
comparable with the laboratory rates reported for this species, because
chaetognaths are not superfluous feeders (Reeve, 1964). Temperature affects
feeding rates, though this has not been well studied in chaetognaths. Reeve
(1966) found laboratory feeding in S. hispida increased with temperature from
10°C to 25°C, but was lower at 30°C. At 33°C the experimental animals died
(ambient temperature was 25°C).
When feeding rates are compared using gut content analysis, caution must be
taken because digestion time decreases with increasing temperature (Pearre,
1981). Lower NPC’s at higher temperatures do not necessarily mean lower
feeding rates.
SPECIFIC DAILY RATION

The specific daily ration (SDR) is the weight of food consumed daily per unit
weight of the chaetognath. It is convenient to report the SDR in terms of dry
weight, because it is easily determined, but dry weights include a considerable
amount of salt. For this reason, SDR’s are more meaningful when determined on
a carbon, nitrogen, phosphorus, or ash-free dry weight basis. In both S. enflata
and S. tenuis, the two species where SDR’s have been reported both ways, SDR’s
based on carbon are higher than those based on dry weights (Table V)
(Feigenbaum, 1979; Canino, 1981).
A typical curve for chaetognath SDR against size is shown in Figure 16.
Larger chaetognaths tend to have higher daily rations than small individuals of
the same species, but lower SDR’s. For predictive purposes, these curves can
often be fit rectalinearly or with an exponential decay (see Feigenbaum, 1982). It
would be helpful if published graphs provided an expression of best fit, because
figures are often reduced and/or have logarithmic axes making it difficult to
obtain accurate values.
The results shown in Table V indicate that very young chaetognaths may
consume several times their weight daily (SDR’s′ l), while larger individuals
consume from <1 to 40% of their weight on a dry weight or carbon basis when
feeding on natural prey (64% for S. hispida feeding on Artemia nauplii). The
more flaccid species such as Sagitta enflata appear less active than rigid
chaetognaths like S. hispida and S. tenuis and have lower carbon-based SDR’s.
The largest S. enflata had SDR’s of 0·144 (Feigenbaum, 1979) and 0·105 (Reeve,
1980) compared with 0·220 for S. tenuis (Canino, 1981) and 0·40 for S. hispida
(Reeve, 1980). S. elegans, with a body type intermediate to these species, had a
carbon-based SDR of only 0·035 in laboratory feeding (Reeve, 1980), but 0·19 in
the CEPEX bags (Sullivan, unpubl., cited in Reeve, 1980).
Szyper (1976) found higher SDR’s than Feigenbaum (1979) for large S.
enflata, although his were on a nitrogen (0·253) and phosphorus (0·394) basis. In
addition, the largest specimens in Kaneohe Bay, Hawaii are only mid-size by
Gulf Stream standards. Szyper’s “population” SDR’s are very high because of
the predominance of young animals.
Feeding comparisons are additionally complicated by environmental factors.
Although temperature clearly affects feeding rates (Reeve, 1966), it is not the
absolute temperature, but the temperature in relation to the species’ normal range
that is significant. In addition, other stress factors must be considered.
Zooplanktonic organisms are often carried by currents into marginal
environments. These expatriate populations can sometimes comprise a significant
part of the plankton population yet behave in some stress-affected manner. Reeve
(1966) found that feeding in S. hispida increased slightly at the extremities of its
salinity range, presumably because stress increased energy demands. On the other
hand, Bushing & Feigenbaum (in press) found that the S. enflata population
feeding in the surface waters of the Virginia continental shelf fed at half the rate
of the population near Miami, Florida. In their study, none of the 42 specimens
caught below the thermocline had been feeding at all. Clearly, modellers will
have to consider the environment relative to the species’ normal range when
accounting for chaetognath feeding activities.
Pearre (1981) analysed the daily ration in terms of energy content for three
developmental stages of S. elegans in Bedford Basin, Nova Scotia, over two
different seasons. He compared these to estimated minimum energy
requirements based on respiration data from Sameoto (1972) and found general
agreement between his calculations and predicted require ments. The two stages
that fell furthest short of their energy needs (Stage III in July and Stage I in
December) appeared, from population surveys, to have been subject to heavy
mortality.
Feigenbaum (1982) similarly calculated energy requirements for two sizes of
S. elegans at 0°C using respiration rates and conversion factors from Sameoto
(1971, 1972). The no-growth SDR for small (6·5 mm) individuals was estimated
to be less than their actual feeding rates in Vineyard Sound, Massachusetts,
during the winter. The excess was presumed to have contributed towards growth.
Large individuals (20·5 mm) were found to be feeding at their minimum
requirement rate and merely maintaining themselves.
The energy content approach not only promises an increased understanding of
chaetognath nutritional requirements, but appears to have utility in population
forecasting as well.
FEEDING AND PREY DENSITY

Attempts to correlate chaetognath feeding in nature with zooplankton availability
have generally been unsuccessful for two reasons: (1) chaetognaths do not
necessarily feed at the depths caught (Pearre, 1973); and (2) we are unable to
estimate prey density on a scale important to the chaetognaths (Sullivan, 1980).
No relationship was found between FCR’s and zooplankton abundance by
Mironov (1960) for S. setosa in the Bay of Sevastopol, Russia; Nagasawa &
Marumo (1972 for S, nagae in Suruga Bay, central Japan; or Bushing &
Feigenbaum (in press) for S. enflata in the waters of the Virginia continental
shelf. Sullivan (1980) found NPC’s of Eukrohnia hamata only reflected the
abundance of prey in the upper layers of her study area where density was high.
She found no relationship between feeding and prey density for Sagitta elegans.
In the laboratory, Reeve (1964, 1980) has found that chaetognaths will
increase their daily ration with food concentration until they apparently attain
satiation. He called this food level the “critical density” and cited this as
evidence that chaetognaths are not superfluous feeders. At food levels above the
critical density Reeve found some evidence of feeding inhibition (also noticed by
Feigenbaum & Reeve, 1977). The possible existence of a lower threshhold was
also noted. Reeve’s experiments dealt with S. elegans, S. enflata, and S. hispida
from Saanich Inlet, British Columbia and Miami, Florida. Kuhlmann (1977),
working with S. elegans and S. setosa from the southern North Sea, found food
density did not influence feeding rates. His experiments were, however, more
limited than Reeve’s.
The critical densities in the laboratory lie far above the range of prey densities
in nature, yet some reported natural feeding rates are comparable with maximum
laboratory rates. For example, Feigenbaum (1979) estimated the carbon-based
SDR for adult S. enflata of the Florida Current to be 0·14 when zooplankton
abundance was <2·5/l (Reeve, unpubl., cited in Reeve, 1980) and Sullivan
(unpubl., cited in Reeve, 1980) estimated an SDR of 0·19 for S. elegans in the
CEPEX bags when there were only 10 prey/l. Both of these are comparable with
feeding rates reported by Reeve (1980) for the same species feeding at densities
of 60–100 copepods/l. Therefore, it appears that chaetognaths can achieve
satiation and maximum ingestion rates in nature, even at modest prey densities
(Reeve, 1980).
One explanation, which many adhere to, is that chaetognaths in nature depend
on localized patches of high prey density to obtain their daily requirements
(Cosper & Reeve, 1975; Reeve, 1980). On the other hand, Feigenbaum & Reeve
(1977) demonstrated with a random encounter model that S. hispida could obtain
its daily ration at natural prey densities in Biscayne Bay, Florida without needing
patch densities. Also arguing against the patch-feeding theory is the fact that
chaetognaths are seldom encountered in nature with more than a single prey in
their guts (Table I). The paradox is perhaps best explained by simply saying that
chaetognaths do not feed as readily in the laboratory, and require the inducement
of higher prey densities for maximum consumption.
FEEDING AND TIME OF DAY

Wimpenny (1936) appears to have been the first to report differences in
chaetognath feeding during day and night periods. He analysed the gut contents
of S. setosa from the North Sea and compared FCR’s. Mironov (1960) examined
S. setosa samples over a 24-h period at a station in the Bay of Sevastopol, Russia.
Although finding the highest FCR’s in the late evening, he concluded that
feeding intensity was apparently not linked with time of day because some
FCR’s from other daytime periods were comparable.
In the laboratory, Parry (1944) found that 6 of 47 S. setosa kept in the dark fed,
but none of the 27 kept in the light did. He believed that Sagitta would only feed
under conditions of low light intensity. Reeve (1964) fed a group of S. hispida
twice daily for 11 days under natural light conditions and counted the prey eaten
in each 12-h period at 1000 and 2200. After an initial period of acclimation, a
clear diurnal feeding rhythm became apparent with feeding some 40% higher at
night.
Quantitative studies of natural gut contents by Rakusa-Suszczewski (1969),
Nagasawa & Marumo (1972), Pearre (1973), Szyper (1978), Newbury (1978),
Feigenbaum (1979, 1982) and Bushing & Feigenbaum (in press) have also found
feeding greater at night than during the day, but due to the kind of variability
observed by Mironov (1960), the difference in FCR’s is often not statistically
significant (e.g., Feigenbaum, 1979; Bushing & Feigenbaum, in press).
Sullivan (1980) found the gut contents for migrating stages of S. elegans were
significantly more digested in her day samples and concluded they may have
been the remains of the previous night’s feeding. She found the NPC’s of night
samples significantly greater than for day samples for Eukrohnia hamata and the
larger, migrating Sagitta elegans, but not for the juvenile S. elegans, which
remained in the surface layers.
Pearre (1973) compared the day and night gut contents of S. elegans for July
and December in the Bedford Basin, Nova Scotia. While feeding was little
different between day and night in December, there were significant decreases in
feeding during the day in July. This could have been due to the greater light
intensity in July, leading to feeding inhibition, or the longer day length, which
provided more time for digestion of night-captured prey (Pearre, 1973).
FEEDING AND GROWTH AND REPRODUCTION

In the laboratory, food unquestionably affects growth and egg production. For
example, Reeve (1970a) found the length of S. hispida increased linearly with
prey density at food levels from 0–20 Artemia per compartment (100 ml), but
then reached an asymptote. There was little additional per cent change in
chaetognath length at higher food levels, because these animals had matured and
additional growth went into egg production. During the same experiments, the
number of animals with mature eggs increased linearly through the entire range
of food levels (0–100/compart-ment). Starved animals halt their reproductive
development and shrink (Reeve, 1966; Reeve, Raymont, & Raymont, 1970).
Gross growth efficiency, defined as chaetognath growth divided by the weight
of food intake, was also measured by Reeve (1970a). Immature animals had an
average efficiency of 34·5% (19–50%) on both a dry weight and total nitrogen
basis. Egg-producing populations were inefficient on a dry weight basis (0%), but
not on a nitrogen basis (41%). Reeve (1970a) hypothesized that mature animals
utilized stored carbon reserves for metabolism while incorporating nitrogen into
the eggs.
In nature, food does not appear to be a limiting factor for growth or
reproduction, but may affect the timing of spawning. Sameoto (1973) noted that
growth rates of Sagitta elegans were similar in the Bedford Basin and St
Margaret’s Bay, Nova Scotia, although the Basin has a greater copepod biomass.
McLaren (1969) found that estimates of S. elegans production in Ogac Lake,
Canada, did not parallel either the production or standing stock of the copepods.
Final size and, therefore, the number of eggs per chaetognath, was governed by
temperature, not food level, at least for S. elegans (Dunbar, 1962; Sameoto, 1971).
Stone (1966) examined fecundity of S. enflata in the Agulhas Current and
found that individuals from neritic waters—which contained more food, but had
lower temperatures—had more eggs than those from oceanic stations. Although
food level appeared to be the more important factor in egg production, it was
crudely measured in the study and the influence of temperature could not be
ruled out.
McLaren (1969) found the mean times of recruitment of the new S. elegans
population in Ogac Lake, Canada coincided with sharp increases in the number of
nauplii of Pseudocalanus (Copepoda) (which were also eaten by the young
chaetognaths). Noting that mature chaetognaths cannot detect prey availability
for larvae, because larger animals eat larger prey, he hypothesized that
reproductive timing was based on general seasonal indications. McLaren also
found that the number of recruits was not related to the abundance of copepod
nauplii but to the number of mature adults. From this, McLaren concluded that
timing in relation to food was more important than food level.
Others who reported that chaetognath reproduction was tied to the abundance
of small copepods were Sameoto (1973), for the Sagitta elegans population of
the Bedford Basin and King (1979) for the S. elegans population of Dabob Bay,
Washington. An exception was found by Dunbar (1962) who discovered that in
Arctic waters S. elegans had a long spawning period not accurately timed with
food availability.
STARVATION
Chaetognaths can tolerate short periods of starvation, although all but a few deep-
water species have little lipid food reserve (Lee, 1974, 1975; Mayzaud & Martin,
1975; Sargent & Lee, 1975; Mishin, 1980). Parry (1944) found Spadella
cephaloptera could be starved 3–4 days without apparent ill effect while Reeve
(1966, 1970a) and Reeve et al. (1970) found Sagitta hispida could survive two
weeks without food at 21°C although they failed to attain maturity. Over a six-
day period, S. hispida lost 4% of their dry weight/day, one half of which was
protein. Lee (1974) was unable to starve S. elegans for more than 48 h but
Feigenbaum (unpubl. obs.) held this species for days without food at low
temperatures. Kotori (1976) kept S. elegans alive for more than two weeks
without food. One individual survived 44 days at natural temperatures.
Cosper & Reeve (1975) looked at the effect of starvation on digestive
efficiency and found that for an extra day or two, starvation increased the
variability, but not the mean value. Digestive efficiency decreased when
starvation lasted more than 5 days. Animals kept much longer periods without
food were unable to digest food altogether.
ADVANTAGES AND DISADVANTAGES OF

LABORATORY AND FIELD FEEDING RATES
Chaetognath feeding rates have been obtained in two basic ways—laboratory
feeding experiments and gut content analysis (GCA) of animals which have fed
in nature (Table V). Each provides something the other cannot as explained
below. Most of the early data were provided by Reeve in the laboratory. The
recent trend is, however, towards GCA.
Laboratory feeding
Advantages. Conditions can be carefully controlled (not only temperature,
salinity and food level, but also the prior feeding history of the animals).
Observations of the feeding process and prey escape behaviour are possible.
Reeve & Baker (1975) pointed out that maximum growth rates can provide a
standard for comparison.
Disadvantages. Conditions are unnatural. These planktonic animals may sense
confinement, because of the surfaces provided by confinement. In addition, there
is a lack of normal water movement, with restriction of chaetognath movement
(e.g., no vertical migration) and constant compared with variable temperature
and salinity regimes. In the laboratory we are also unable to duplicate naturally-
occurring patchy prey distributions. N
Gut content analysis

Advantages. Chaetognaths feed on a natural-species mix under natural
conditions.
Disadvantages. It is necessary to apply a laboratory-obtained estimate of
digestion time which, at best, can only be made under temperature conditions that
approximate those experienced in nature by active migrators. GCA also suffers
from inaccuracies caused by cod-end feeding along with regurgitation and
defaecation due to handling and preservation. Other difficulties include the
identification of all prey and of estimating the weight of soft-bodied prey.
ROLE OF FEEDING IN VERTICAL MIGRATION

There is little doubt that chaetognaths come to the food-rich surface layer to feed
(McLaren, 1969; Pearre, 1973, 1974). Pearre (1973, 1979), on the basis of gut
contents, postulated that in chaetognaths satiation causes downward migration
and may account for the “midnight dip” observed in vertical migration patterns.
Pearre (1979) also hypothesized that young stages reported as being non-
migratory (e.g., Sullivan, 1980) actually do migrate, but in a smaller, less
synchronous fashion than the more powerful adults. He argued that with their small
energy reserves and high feeding rates young chaetognaths cannot obtain enough
food in the surface layer at one feeding to last the entire daylight period. Their
vertical movements go undetected with conventional sampling techniques.
THE SIGNIFICANCE OF CHAETOGNATHS IN

PLANKTON ECOSYSTEMS
Early records document the great abundance of chaetognaths in the sea. Darwin
(1844) noted they abound “in infinite numbers over the intratropical and temperate
seas”. Busch (1851) recognized their significance, pointing out that they fall prey
to most larger predators. Grassi (1883, cited in Shipley, 1901) described the
surface of the sea at Messina, Sicily as literally covered with chaetognaths on
certain days. Nor were they known only from the surface waters. Chun cited in
Shipley, 1901) collected countless numbers of chaetognaths at depths of from
100 to 1300 m.
Shipley (1901) also reported that at times chaetognaths devoured young fish
and undoubtedly did considerable damage to sea fisheries. This concern has been
expressed by other workers as well (e.g., Lebour, 1923; Bigelow, 1924;
Heydorn, 1959).
Mironov (1960) made the first quantitative estimates of chaetognath
consumption of zooplankton standing stock. He calculated that S. setosa daily
consumed 0·5% of the mean zooplankton standing stock in the Bay of
Sevastopol, Russia and S. euxina Moltschanoff about 0·2% of the standing stock
in the eastern Black Sea. Based on data from Kusmorskaya (1950, cited in
Mironov, 1960), Mironov also calculated that chaetognaths could potentially eat
half the standing stock daily in the northwest Black Sea when in maximum
abundance. He conceded, however, this estimate was probably too high.
TABLE VI
Estimates of standing stock and secondary production consumed by chaetognath
populations: a, our calculations based on author’s data.
Species Area % standing % secondary Remarks Reference
stock production
consumed consumed
daily daily
Sagitta Eastern 0·2 — — Mironov,
euxina Black Sea 1960
Sagitta Bay of 0·5 — When „
setosa Sevastopol, chaetognath
Russia density is
27/m3
Sagitta sp. Northwest almost 50 — Based on „
Black Sea data of
Kusmorskay
a (1950)
Sagitta St — 2·2–3·3 A revision Sameoto,
elegans Margaret’s of his 1972 1973
Bay, Nova estimate
Scotia
Species Area % standing % secondary Remarks Reference

stock production
consumed consumed
daily daily
St — >100 1 Dec.–1 Sameoto,
Margaret’s April only 1972
Bay, Nova
Scotia
Bedford — 36 Possibly Sameoto,
Basin, Nova over- 1973
Scotia estimated
Sagitta Card 100 — Of Reeve &
hispida Sound, zooplankton Baker, 1975
Florida retained by
64 μ m
Biscayne 23a — Of „
Bay, Florida zooplankton
retained by
64 μ m
Sagitta Kaneohe 8a — Of post Szyper,
enflata Bay, Hawaii naupliar 1976
copepods
100 — Of „
Oikopleura
caught on
330 μ m
Florida 1·9 6·9 — Feigenbaum
Current , 1977
All „ — 12 „
chaetognath
s combined
Sagitta Bering Sea 0·2 10 Summer Kotori,
elegans only 1976
Sagitta Chesapeake 1·2 — — Canino,
tenuis Bay, 1981
1–4 5–15 September „
only
Expatriate
population
Sagitta Virginia <1 — Bushing &
enflata continental Feigenbaum
shelf , in press
Reeve (1970a), deducing from the literature that chaetognaths have a biomass
equal to about 30% of the copepods in the world’s ocean, theorized that most of
the energy converted to animal biomass by copepods is distributed to higher
trophic levels via chaetognaths. He concluded that chaetognaths are the primary
carnivores of the seas.
Recently, several workers have estimated the percentage of herbivore standing
stock and/or secondary production consumed by chaetognath populations as an
extension of their analysis of feeding rates and metabolic activity. These are
listed in Table VI. The estimates range from 0·2% of the herbivore standing
stock of the eastern Black Sea to more than 100% of the secondary production
during the winter and early spring in St Margaret’s Bay, Nova Scotia. In virtually
every case, these estimates rely on significant assumptions or broad
generalizations that probably have caused them to be too low in some instances
and certainly too high in others. It is interesting that hardly any really good
quantitative estimates of the impact of chaetognath feeding exist. This is
certainly an area for further research.
CONCLUDING REMARKS
Chaetognaths are not superfluous feeders (Reeve, 1964) and their feeding rates
are low compared with gelatinous predators like ctenophores and medusae
(Fraser, 1969; Reeve, 1980). Yet they have often been called “voracious” in the
literature simply because prey have been found in their guts (e.g., Kielhorn,
1952). We cannot help but wonder what investigators expected to see in the gut
of a predator! Likewise, while chaetognaths are undoubtedly important in many
marine food webs, there are other localities where their low abundance make
them of minor significance. In preparing this review we have found authors who
seemed reluctant to admit that. For example, Kielhorn (1952) considered
Eukrohnia hamata of considerable importance to the economy of the boreo-
arctic Atlantic although it rarely occurred as more than a few per cent of the
plankton population.
Casual observations of chaetognaths in preserved samples may not detect
prey. Generally, only one prey will be found in the chaetognath gut and if the
prey is fairly well digested it will be quite transparent. Reports such as Heydorn
(1959), where no food was found in the guts of almost all the species examined,
may be in error. Table I shows that typically more than 10% of the chaetognaths
will contain food, even in the day-time.
Reeve (1977) pointed out that casual observations of feeding behaviour can
produce misleading conclusions. In Sagitta hispida, copulatory behaviour has
been mistaken for cannibalism (Reeve & Walter, 1972b) and random movement
mistaken for pursuit of prey (Feigenbaum & Reeve, 1977). If such errors of
observation can be made under ideal conditions in the laboratory, observations
made by SCUBA diving will have to be particularly scrutinized.
Our review shows that almost all studies of chaetognath feeding have been
made in bays or similar semi-enclosed bodies of water—Biscayne Bay and Card
Sound, Florida; the Chesapeake Bay, Virginia, the Bedford Basin and St
Margaret’s Bay, Nova Scotia; the Bay of Sevastopol, Russia; Kaneohe Bay,
Hawaii; Saanich Inlet, British Columbia; Suruga Bay, Japan; and Vineyard
Sound, Massachusetts. Convenience and cost have probably been responsible, but
the fact remains that we have too little information about chaetognath feeding in
major current systems or open ocean areas. As a result, we are forced to draw
conclusions about the chaetognath’s rôle in the sea from data obtained in small
bodies of water. We hope our review can help change the situation.
ACKNOWLEDGEMENTS
We thank Paul Friedhoff of Clearwater, Florida for translation of the German
papers and Yvonne Maris for expert and speedy typing of the manuscript.
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ECOPHYSIOLOGY OF MARSUPIAL
DEVELOPMENT AND REPRODUCTION
IN MYSIDACEA (CRUSTACEA)
KARL J.WITTMANN
Institut für allgemeine Biologie der Universität Wien, A-1090
Wien, Austria
INTRODUCTION
All species of the order Mysidacea lay their eggs in a brood pouch thus allowing
direct study of the development of young from oviposition to attainment of the
juvenile stage. In recent years increasing interest has been focused on the
development of young and its ecological and physiological demands and
implications. This has been accompanied by increasing efforts and success in
experimentation and the culture of the animals. Besides their traditional rôle in
fisheries biology and in food chain studies, mysidaceans have recently become
important as test organisms in work on the ecological and physiological effects
of pollutants (see review by Nimmo & Hamaker, 1982). The present review is
mainly concerned with the ecophysiological importance of incubation in
mysidaceans. This importance may be direct or indirect; it may reflect the effects
of certain factors on incubation or the implications of incubation for other
ecological or biological processes. In fact, it is shown in the following that the
duration of incubation bears more and stronger implications on reproductive and
population ecology than was previously thought. The incubation period appears
to be a key factor for the understanding of variations in the length and timing of
the breeding season, age at maturity, frequency of broods, numbers of young per
brood, egg size, and adult body size. This review may initiate search for similar
relationships in other groups of brood-protecting marine poikilotherms. These
relationships are of fundamental importance to the whole complex of
reproductive and population ecology. In this way the present study may give
valuable background information for almost any kind of study dealing with
biology, population ecology or ecophysiology in mysidaceans.
Recently Mauchline (1980) has reviewed the biology of mysidaceans and I
have drawn freely on some of the data presented in his tables. He dealt with the
broad field of the biology but did not go into so much detail as far as incubation
418 KARL J.WITTMANN
is concerned. Nevertheless, some overlap in our studies appears to be inevitable.

I have not included some important topics such as sex ratio, differential mortality
of sexes, and growth, age, and numbers of moults at sexual maturity. For these
fields of interest one should consult Mauchline’s (1980) study.
EFFECTS OF SIZE AND AMBIENT CONDITIONS ON

DEVELOPMENT AND REPRODUCTION
TEMPERATURE RELATIONS OF THE INCUBATION

PERIOD
It is well known in the comparative physiology of poikilotherms that temperature
is an important factor responsible for variations in the time of development. This
should be especially valid for the incubation periods in mysidaceans as the young
in the brood pouch do not feed. The temperature relations given below also
contain effects due to different egg sizes. In some species egg sizes vary
seasonally. Allowing for a reasonable error, egg size can be substituted by its
temperature relation, particularly because the effects of egg size are small.
The available data on the effect of temperature on the marsupial development
of nine species are summarized in Table I. All nine species originate from
temperate climates. As was shown by Wittmann (1981b) for Leptomysis lingvura,
the temperature relation of incubation periods (DI, in days) fits well to a variant
of the Arrhenius equation: where a is a constant, μ (in cal·mol−1) is
the “temperature characteristic”, R the gas constant, and 1/T the inverse absolute
temperature. The data for nine species indicate an average μ of 11 000 (range of
4000 to 17000). The Berthelot equation (in the form of ; where k is a
velocity constant and t the temperature in °C) is used in order to calculate
average Q10 values . This gives an average Q10 of 1·9 (range of 1·3 to
2·8). Due to its biochemical meaning the Arrhenius equation appears to be
theoretically better founded and thus to be the more appropriate way of reflecting
temperature effects. Nevertheless, Q10 values and, therefore, also the Berthelot
equation appear to be inevitable if one wants to use published data.
The data given by Murano (1964b) for Neomysis intermedia indicate that the
incubation period is less temperature-dependent above 21°C than expected from
the physicochemical equation. The decrease of the temperature effect with
increasing temperature has been observed in a variety of animals and caused
Krogh (1914), Bel′ hrádek(1930), and many others to be reluctant to accept a
pure and too restricted physicochemical understanding of animal development.
Schwerdtfeger (1963) states that Q10 values are usually between 2 and 3. The
temperature effect in mysidaceans is, therefore, relatively small. In the following
published data on other orders of crustaceans it is assumed that the experiments
were conducted within the approximate temperature ranges relevant to the natural
populations. McLaren, Corkett & Zillioux (1969) studied the development of
DEVELOPMENT AND REPRODUCTION IN MYSIDACEA 419
eggs of 11 species of marine copepods from different latitudes and I have

calculated the temperature coefficients from the data: (range of 2·4 to
4·9, for means for each species). Patel & Crisp (1960) report Q10 values for
embryos of eight species of balanids from European coasts in the range of 1·8 to
4·2 (mean 3·4). Wear (1974) studied the embryonic development of decapods
from British coasts. I used his data for 12 species in the range of 9 to 18°C: mean
Q10 equals 4·1 (range of 3·6 to 5·2). Steele & Steele (1973) examined the genus
Gammarus (Amphipoda) in the northwestern Atlantic: for five species the data
give Q10 values of 3·8
TABLE I
Rates of temperature acceleration of marsupial development in species of Mysidacea: the
egg size data are partly from measurements (a) of Mauchline (1973) and (b) myself on
Mediterranean species
Species Location Temperat Incubatio Temperat Q10 Egg size Reference
ure (°C) n period ure (mm) s
(days) character
istic μ
Hemimys Mediterra 12–23 12–18 6182 1·5 0·39– Macquart
is nean 0·44b -Moulin
spelunco & Patriti
la (1966)
Hemimys Mediterra 14–22 11–22 14604 2·4 0·39– Gaudy &
is nean 0·44b Guerin
spelunco (1979)
la
Leptomy Mediterra 14–26 9–20 11822 2·0 0·44–0·54 Wittmann
sis nean (1981b)
lingvura
Neomysi Northwes 10–16 13–24 16616 2·8 0·41 Pezzack
s tern & Corey
american Atlantic (1979)
a
Neomysi Baltic 11–19 15–20 7359 1·6 0·50 Kinne
s integer (1955)
Neomysi Japan 17–30 6–17 13287 2·1 0·5 Murano
s lakes (1964b)
intermed
ia
Neomysi Japan 12–30 6–17 10344 1·8 — Ishikawa
s ponds &
japonica Oshima
(1951)
Praunus Danish 16–19 20–27 11762 2·0 0·78a Blegvad
flexuosus waters (1922)
420 KARL J.WITTMANN
Species Location Temperat Incubatio Temperat Q10 Egg size Reference

ure (°C) n period ure (mm) s
(days) character
istic μ
Praunus Northeast 17–19 16–18 9210 1·7 0·78a Nouvel &
flexuosus ern Nouvel
Atlantic (1939)
inermis waters (1922)
neglectus waters (1922)
to 4·6 in the temperature range of −1·5 to 13°C. Kinne (1953, 1960) examined
two Gammarus species from temperate waters of the European Atlantic: the
average Q10 value for each of both species is 2·0 for 10 to 22°C. According to
Andersson (1969), in the limnic isopod Asellus aquaticus from Swedish lakes,
the marsupial development is accelerated by in the range of 10–21°C;
in French populations of this species according to the data given by
Henry (1976) for 11–16°C, and for 10–19°C according to Magniez
(1975). For the intertidal isopod Dynamena, Holdich (1968) reports durations of
development which give a for the range of ′ 8–18°C. This restricted
survey of the literature shows that the temperature effect in mysidaceans is
smaller than usual in Crustacea, at least in the temperate region where enough
data are available to support this conclusion.
The next step for a comprehensive study of the marsupial development in
Mysidacea is to summarize all the available data on durations of the incubation
period (Table II). For such a summary a basis has to be found to make the data
comparable. The data chosen were, therefore, those which come from periods of
intensive breeding—or of most intensive breeding if determinations at different
temperatures and/or seasons are available for a certain population. As a
conseqence of this kind of selection, most data for the temperate region represent
breeding during the spring or summer. Different populations and different ways
of assaying the data were treated like different species. In this way, 41
determinations of the time of development for a total of 26 species are available
(Table II). Species of all major geoclimatic regions, the Arctic, the temperate,
and the tropical regions are compared. The populations originate from marine
and brackish, as well as freshwater habitats. Despite this very high ecological
diversity, the time of development depends on the relation to egg size and
temperature which is equally well applicable to most of the species as is shown
in the following.
At the interspecific level (Fig. 1), the temperature relation of the incubation
period is given by ; . The slope of the regression
line gives a temperature characteristic μ =21 665± 608. (In the present article ± or
-indicates standard error of estimate; +/− or ×/÷ indicates standard
deviation about the mean; arithmetic or geometric, respectively). The Berthelot

equation gives the correlation coefficient . The resulting van’t Hoff
temperature coefficient is . Two outliers (i.e., points outside the
confidence limits) are indicated by the confidence intervals in Figure 1; these
results were not included in the calculation. The giant deep-sea species
Gnathophausia ingens is an outlier most likely because of exceptionally large
eggs; the egg size of the nearshore species Acanthomysis sculpta is unknown.
The effects of temperature are highly different when the temperature
characteristics at the intra- and the interspecific level are compared. All
acceleration rates at the intraspecific level given in Table I
are well below the lower limit of confidence (99%) for the
interspecific level. The difference is highly significant and indicates that the
temperature effects at both levels are different (but not independent) entities.
There is a small temperature effect at the intraspecific level, on the one hand, and
a much higher effect at the interspecific level, on the other. There is no doubt
that this difference is an outcome of latitudinal temperature adaptation. The
small effect at the intraspecific level indicates that there may be homeostatic
mechanisms (in the broadest sense) which regulate the time of development to a
distinct level and which keep the temperature triggered oscillations about this
level small. The position of the level itself is set by—usually genetic—adaptation
in relation to the geoclimatic distribution and is highly temperature-dependent
when different species or populations are compared.
To explain the converse patterns of temperature dependence without assuming
the involvement of regulatory phenomena would be highly unsatisfactory or at
least, would lead to quite complicated ecophysiological implications. The
question may, therefore, be asked: why are the Mysidacea better regulators than
is usual in other Crustacea? There is some information available on this point.
The duration of the marsupial period is very long. In the Arctic the animals spend
′ 35–50% of the average generation time in the brood pouch. The corresponding
duration is typically ′ 15–30% in temperate to tropical climates. The incubation
time is in most species well synchronized with the maternal moult cycle and with
the development of the eggs in the ovarian tubes. Therefore, every change in the
TABLE II
Duration of marsupial development, egg size, body size of breeding females, and number
of young per brood in species of Mysidacea in relation to ambient temperature,
geoclimatic distribution, salinity, and vertical distribution: parentheses indicates
transformed or adjusted data; the data are partly from supplementary literature (a) cited
elsewhere in this table and by my own measurements (b) on Mediterranean species;
distribution is indicated by letters; TR, tropical; ST, subtropical; T, temperate; B, boreal;
SA, subarctic; A, arctic; L, limnic; LA, limnic subalpine; BR, brackish; C, marine
coastal; MP, marine mesopelagic; BP, marine bathypelatic; the incubation period
422 KARL J.WITTMANN
Fig. 1.—Duration of marsupial development in 26 species (a total of 41 determinations)

of Mysidacea in relation to temperature and geoclimatic distribution: egg diameters are
indicated by different symbols; the continuous line was fitted by least squares fit to a
relation according to the Arrhenius equation; two outliers are indicated by the 99%
confidence intervals (dotted lines) for individual data sets; the outliers were not included
in the calculation.
indicated for Acanthomysis sculpta was roughly adjusted due to 5·6 days between
hatching and postnauplioid stage 3
Species Incuba Egg Egg wt Body Brood Tempe Distribu Referen
tion diamete (μ g) size size rature tion ces
period r (mm) (mm) (°C)
(days)
Acanth (8) — — 11 18 12 T, C Green
omysis (1970)
sculpta
Boreo 95 0.77 — — — 7 B-A, Jepsen
mysis MP (1965)
arctica
Diamy 8·9 0·40 16·3b 7 8 22·5 T, BR Ariani
sis (1981,
bahire pers.
nsis comm.)
Diamy 9·0 0·46 — 5 — 22·5 T, BR Ariani
sis (1981,
bahire pers.
nsis comm.)

(days)
Diamy 9·4 0·40 — — — 22·5 T, C Ariani
sis (1981,
bahire pers.
nsis comm.)
Gastro 21 0·45b 17·0b 9 30 15 T, C Macqu
saccus art-
lobatus Moulin
(1965)
Gastro 25 0·57 — 16 68 10·9 T, C Matsud
saccus aira et
vulgari al.
s (1952)
Gnath 530 4·0a — 145a 190 3·5 BP Childre
ophaus ss &
ia Price
ingens (1978)
Hemim 22 0·44b 12·8b 6 — 14 T, C Gaudy
ysis &
spelun Guerin
cola (1979)
Hemim 12 0·39b 9·6b 6 — 23 T, C Macqu
ysis art-
spelun Moulin
cola &
Patriti
(1966)
Lepto 14·3 0·48 32·9b 10 19 19 T, C Wittma
mysis nn
bürgii (1981b
)
Lepto 14·0 0·45 20·1 8 16 19 T, C Wittma
mysis nn
lingvur (1981
a b)
Lepto 22·5 0·66 48·0 10 15 13 T, C Wittma
mysis nn
lingvur (1981
a b)
Mesop 4 0·35 — 7 9 27 ST-TR, Nair
odopsi C (1939)
s
orienta
lis
424 KARL J.WITTMANN

(days)
Metam 10 (0·31) 5·5 6 14 18 T, C Clutter
ysidop &
sis Theilac
elonga ker
ta (1971)
Metam 5·5 0·42 — 5 13 32·5 TR, BR Quinter
ysidop o&
sis Roa
insular (1973)
is
Mysidi 6·5 0·40 — 6 6 26·5 TR, C Davis
um (1966,
columb 1967)
iae
Mysido 6·5 — — 5 8 23 ST, BR J.H.Ge
psis ntile et
bahia al.
(1982)
TABLE II—continued
Species Incubat Egg Egg wt Body Brood Tempe Distrib Referen

ion diamete (μ g) size size rature ution ces
(days)
Mysis 180 1·84 — 20 80 3 SA-A, Ladura
litorali BR ntaye
s &
Lacroi
x
(1980)
Mysis 270 (0.78) 120 12 12 0.33 A, L Lasenb
relicta y&
Langfo
rd
(1972)
Mysis 150 (0·91)a — — 15 1·5 B, L Berrill
relicta (1969)
Mysis 150 (0.76)a — — 19 2·5 B, L Fürst
relicta (1965)
Mysis 165 (0·76) 112 — 19 (3) B, L Hakala
relicta (1978)

(days)
Mysis 75 0·66 — 17 25 3·5 T, L Samter
relicta &
Weltne
r
(1904)
Mysis 150 (0·91) 200 14 12 3·6 B, L Lasenb
relicta y&
Langfo
rd
(1972)
Mysis 128 (0·9l)a — 17 14 4·5 LA Morga
relicta n
(1980)
Mysis 75 0·52a — 24 157 3 B, C Amarat
stenole unga &
pis Corey
(1975)
Neomy 21 0·40a — — — 13·5 T, BR- Berrill
sis C (1971)
americ
ana
Neomy 13 0·41 — — 45 16 B, BR- Pezzac
sis C k&
americ Corey
ana (1979)
Neomy (21·3) 0·50a — — — 15 T, BR Vlasbl
sis om &
integer Elgersh
uizen
(1977)
Neomy 14·5 0·50 — 11 26 18·5 T, BR Kinne
sis (1955)
integer
Neomy 8·5 0·5 — — 19 21·5 T, L Muran
sis o
interm (1964b
edia )
Neomy 14 — — — 18 16·8 T, BR Ishika
sis wa &
japoni Oshim
ca a
(1951)
Praun 21 0·78a — — — 13·5 T, BR- Berrill
us C (1971)
426 KARL J.WITTMANN

(days)
flexuos
us
Praun 18 0·78a — 18 — 16·8 T, C Nouvel
us &
flexuos Nouvel
us (1939)
Praun 22 0·78a — 18 (21) (17) T, C Blegva
us d
flexuos (1922)
us
Praun 27 0·67 — 13 25 12·5 T, C Mauchl
us ine
inermi (1965,
s 1973)
Praun 17 0·67a — 10 8 (19) T, C Blegva
us d
inermi (1922)
s
Praun 18 0·80a — 15 10 (19) T, C Blegva
us d
neglect (1922)
us
Schisto ′ 21 0·55 — 13 18 12·5 T, C Mauchl
mysis ine
spiritu (1967,
s 1973)
Siriella 12 0·53b 36·4b 17 30 19·5 T, C Cuzin-
armata Roudy
et al.
(1981)
incubation time should produce strong alterations within the whole complex of
reproductive and population biology. Therefore, one may expect that the
Mysidacea have a high need to regulate the seasonal effects of temperature on
breeding. Hypogean isopods have a much longer incubation period than their
epigean relatives and their development is much less, namely not or very
weakly, temperature dependent within natural ranges (Magniez, 1975; Henry,
1976). This also supports the view that there is a relation between length of
development and the need for homeostasis.
Homeostatic mechanisms in biology, and temperature response in particular,
usually have well definable ranges in which good performance occurs. There is
only scarce information available which deals with the temperature ranges of
marsupial development in mysidaceans. There are numerous experiments of B
cesco (1940) and Vlasblom & Elgershuizen (1977) which show that the adults
can survive only within certain limits of salinity and temperature. The limits
correspond well to the natural distribution of the animals. The salinity limits are
smaller for embryos than for adults.
In the Mediterranean Sea breeding is continuous in those areas where there are
small seasonal temperature differences, but this is not so where the winter
temperatures fall below 10°C (B cesco, 1940; Macquart-Moulin, 1965;
Wittmann, 1978a). The peak of summer temperatures is roughly constant
between 25 and 27°C on European coasts in the northern part of the
Mediterranean. In higher latitudes breeding occurs far below 10°C. This shows
that the cessation of breeding in winter in certain parts of the Mediterranean and
the Black Sea and adjacent brackish and freshwater areas is not caused by the
low winter temperatures per se, but by the large difference of winter and summer
temperatures. Neomysis intermedia lives in Japanese freshwater lakes at ambient
temperatures of 4–30°C; reproduction only occurs in the range of 15–30°C
(Murano, 1964a).
When the data for species and populations from different latitudes are
compared, a very steep developmental acceleration is found: 700 or
. This acceleration is interpreted as the distance between the different adaptation
levels of the various populations which breed at different temperatures and
latitudes. It is a most interesting finding that the same physicochemical equation
can be successfully used to describe the real physiological acceleration on the
intraspecific level which may even be experienced by a certain individual.
Winberg (1971) presents the results of Mednikov (1962) who summarized the
temperature relations of marine, brackish, and limnic copepods in an equation to
which a Q10 of 2·3 corresponds (for the optimal temperature for breeding in the
range of 5–28°C). From the data given by McLaren et al. (1969) for each
copepod species I have selected those results which correspond to the average
temperatures to which the animals are subjected during breeding in nature—as
far as this can be estimated from the data given by the authors. The selection
gives a range of 2–6 to 26°C. The Berthelot equation results in an average Q10 of
2·2 within the 99% confidence limits of and . There is no
doubt that the development of Copepoda, when surveyed at the interspecific
level, is much less temperature-dependent than in Mysidacea although, as
mentioned above, it is usually more temperature-dependent at the intraspecific
level. Thus, there are two groups of crustaceans which have opposite reactions to
temperature during embryonic development. The copepods are obviously
insensitive temperature conformers and, therefore, need only a slight latitudinal
adaptation to temperature. The mysidaceans are highly temperature sensitive and
consequently need to be good temperature regulators. In addition, they need
latitudinal adaptation to temperature due to the limited capacity of the regulatory
mechanisms. This agrees well with the observation that the Copepoda are more
eurythermic and more ubiquitous than the Mysidacea and most other groups of
428 KARL J.WITTMANN
poikilotherms in the sea (see extended ranges for copepods given by McLaren et
al., 1969).
For the zoogeographical distribution of mysidacean populations a relatively
high degree of stenothermy is expected but there is only sparse information
available on this point. Samter & Weltner (1904) report that Mysis relicta—a
winter-breeding species of boreo-arctic origin—breeds in the range of 0–7°C and
survives only in those German lakes where the bottom temperatures do not rise
above 14°C in summer. Because of the scarcity of data for different populations,
the thermal ranges of distribution for various species have been considered but this
information is less conclusive with regard to the degree of stenothermy in
populations. Most of the epipelagic and coastal species of Mysidacea are
confined to one or other of the major geoclimatic regions of the sea. Within these
regions, temperature is a less important zoogeographical factor, salinity and the
spatial distribution in the shelf areas and the sea basins being of greater
importance. This is obvious from the comprehensive study of Mauchline &
Murano (1977). A highly stenothermal distribution is reported for the pelagic
genus Lophogaster by Fage (1952). Worldwide distribution is known, with few
exceptions, only for the constantly cold deep-water areas in the oceans. There is
no doubt that temperature is a first-class factor in the distribution of Mysidacea
but stenothermy at the species level is equally important as in the majority of
other orders of poikilotherms in the sea (for comparison see Ekman, 1967).
Before these considerations are continued, it is necessary to have a
physiological interpretation of the intraspecific and the interspecific level at
which the data were examined. The interspecific level corresponds to a basic
adjustment of development and its metabolism which occurs in a population in
relation to its distribution and also its breeding biology (e.g., winter-breeders,
summer-breeders). The adjustment is not necessarily constant but may vary with
breeding temperature and size. The intraspecific level represents the temperature-
triggered oscillations about the point of adjustment during the various changes of
the ambient conditions during breeding.
The underlaying assumption is that duration of development in relation to
temperature is not a simple physical process but a synthesis of regulatory and
purely physicochemical processes. Otherwise, it would be very difficult to
understand that, within a group of closely related animals, temperature relations
are split into two very different levels. The importance of physicochemical
processes is supported by the fact that the Arrhenius equation can be successfully
used for both levels. In which way the regulatory mechanisms work is only
partially understood but there is undoubted evidence that they exist. Clarke
(1964) studied the locust, Locusta migratoria, and concluded “that metabolic
response to a temperature change is mediated through temperature receptors,
central nervous system, and hormonal release, followed by cellular metabolic
response”. There is evidence of homeostatic mechanisms at the enzymatic level;
Hochachka & Somero (1968) studied the adaptation of enzymes to temperature
in five species of fish from different latitudes. These authors examined the
relation of substrate affinity to temperature and assume that “these properties…

supply one mechanism by which a given reaction velocity can be held relatively
independent of temperature at least under conditions of limiting substrate”.
Hochachka & Somero (1968) assume that in evolutionary temperature
adaptation selection for enzyme affinity for substrate is a more important feature
than selection for activation energies (which are described by the Arrhenius
equation). Marked differences in enzyme activity of cytochrome c oxydase are
reported by Vernberg & Vernberg (1972) for separated populations of crabs of
the genus Uca. Genetic as well as non-genetic temperature adaptation is widely
known in the animal kingdom (Kinne, 1963). Rate of development and response
to temperature changes have a high genetic component as was shown by Moore
(1951) in hybridization experiments on amphibians, and by Spiess & Spiess
(1966) who observed genetic drifts in Drosophila under laboratory controlled
selection conditions.
Prosser (1958) proposed a system to classify the patterns of acclimation of rate
function to temperature: the curves may not shift, or shift by translation, or
rotation, or combinations of these. According to Barnes & Barnes (1976),
temperature adaptation in the embryonic development in Balanus balanoides
populations from boreal to temperate zones is mainly due to rotation. The data of
McLaren et al. (1969) indicate that in copepods translation and rotation occur
due to different latitudes. Kinne (1953, 1960) and Steele & Steele (1973) give
results for the duration of marsupial development of Gammarus species
(Amphipoda) from different latitudes; rotation and translation is indicated. There
is a preponderance of translation in the closely related Mysidacea, at least for the
temperate region. In both groups of Peracarida translation is correlated with
differences in egg size.
IMPORTANCE OF EGG SIZE FOR THE INCUBATION

PERIOD
Not only temperature but also body size is an important but less effective factor
which determines the rate of metabolism in poikilotherms (Rao & Bullock,
1954). From this well-known fact one can derive the effect of egg size on
duration of development as well as the applicability of the allometric equation to
describe this effect.
A few years ago there was an intensive discussion about the importance of the
size of invertebrate eggs to the time of development (Vance, 1973; Underwood,
1974; Steele, 1977; Strathmann, 1977). Steele (1977) demonstrated that this
relation exists in a variety of organisms including crustaceans; McLaren (1966)
found it in copepods, Wear (1974) in decapods, and Steele & Steele (1975a) in
crustaceans in general. But there are also crustaceans where this relation does not
exist as was shown by Barnes & Barnes (1965, 1976) for balanids. All these
studies were carried out by comparison of the time of development of different
populations and/or species.
430 KARL J.WITTMANN
For the mysidacean Leptomysis lingvura, I demonstrated this effect directly by

culturing, in the laboratory, eggs detached from the parent (Wittmann, 1981b). A
variant of the allometric equation was used to describe the relation of the
incubation period (DI, in days) to egg size (diameter DE, in mm):
where a and b are constants. The allometric exponent was found
for L. lingvura when egg size is expressed as egg diameter, and
when expressed as egg dry weight.
As a next step it is necessary to consider the effect of size at the interspecific
level. In this examination average egg sizes are taken as they usually appear in
field samples; this is intermediate between size at deposition and size shortly
before hatching. Some precautions have also to be made in order to separate
clearly effects of temperature from those of egg size: Steele & Steele (1973)
studied the effect of size on the development of amphipod eggs at the
interspecific level. They compared the duration of development at a distinct
temperature (10°C). Theoretically, this is a valuable method of examination but
there is still the problem of latitudinal temperature adaptation which occurs
independently of egg size. Only species with the same geoclimatic distribution
should, therefore, be compared. Furthermore, the development of animals should
be compared only at temperatures which actually correspond to periods of
intensive breeding in nature. In addition, the breeding temperature should not
correspond to the distributional limits of a species or population.
At present, for mysidaceans there are not enough data available to overcome
these problems without reservations. Nevertheless, the bias seems tolerable when
the following method is used. The data in Table II were divided into four
approximately equally spaced intervals representing breeding at 3, 10, 17, or 24°
C, respectively. The incubation periods were then corrected to the corresponding
standard temperature using the Q10’s in Table I or an average Q10 of 2. This
procedure should introduce only a small bias as the corrections are small
. The results are shown in Fig. 2. For each of the above
temperatures separate allometric equations were calculated by regression
analysis: , for breeding at 3°C (mainly boreal
to Arctic species); ; for 10°C (cold-temperate
and overwintering generations of some warm-temperate species);
, for 17°C (mainly warm-temperate species); and
, for 24°C (tropical, subtropical, and some
warm-temperate species). Significant correlations were found only for 3 and 17°
C. There is no significant difference between the diverse allometric exponents.
Because of this, an average exponent was calculated for all the data by relating
data to the means of incubation periods and sizes within each temperature
interval. This gives ; for a total of 23 species
from the tropics to the Arctic. This relation is practically the same as was found
in the laboratory for L. lingvura (Wittmann, 1981b). At present, there appears to
be no difference between the inter- and the intraspecific level as far as this
relation is concerned.
Fig. 2.—Correlation of egg size and duration of marsupial development in 23 species (a

total of 38 determinations) of Mysidacea from the tropics to the Arctic: the data are
divided into four temperature intervals as indicated; for each species the incubation period
is given corrected to its standard temperature which is indicated by different symbols; for
each standard temperature straight lines were fitted by least squares fit according to the
allometric equation; slope of dashed lines is not significant.
The relation of egg diameter and dry weight (WE, in mg) has been studied
using summer and/or winter eggs of nine species from Mediterranean waters:
Acanthomysis longicornis, Diamysis bahirensis, Gastrosaccus lobatus,
Hemimysis speluncola, Leptomysis bürgii, L. lingvura, Siriella armata, S.
clausii, and S. jaltensis (data are partly given in Table II). Mean egg diameters
were found in the range of 0·32 to 0·72 mm. The results fit the following
relation: , . This was used to calculate the
allometric relation of the incubation period to egg weight at the interspecific level:
. This is very low compared with allometric relationships of
metabolism to body weight given in the literature (Bertalanffy, 1964).
ARE THE EFFECTS OF SIZE AND TEMPERATURE

INTERDEPENDENT?
The regression lines for different temperatures and latitudes in Figure 2 are
approximately parallel. This indicates that the effects of size and temperature on
duration of development may be to a high degree mutually independent, at least
at the interspecific level. Thus, it seems justified to propose a unifying model
432 KARL J.WITTMANN
which describes the diverse diviations of development for the different species
from the tropics to the Arctic.
If it is assumed that the effects of egg size (s) and temperature (t) on development
rate (v) are independent and additive, then the following simple equation results:
. This assumption is only an approximation as size and temperature
are correlated. As derivation from this equation, the allometric and the Arrhenius
equation are combined to the following multiple linear regression:
where a is a constant and the other constants and
variables are as in the equations given above (pp. 394, 403).
The 38 data triplets (DI, DE, T) for 23 species give ,
, and . The multiple computation shows a
significantly higher correlation coefficient than the separate calculations
when the same data sets are used. The 99% confidence intervals for individual
data sets were used for outlier analysis. The length (l) of the intervals give a
rather complicate expression in the three dimensional data field:
; or one may use a rough
estimate: . All 38 data triplets lie well within these limits. This reveals
that the long incubation periods in the bathypelagic Gnathophausia ingens are
due to exceptionally large eggs.
A further argument for the applicability of the multiple computation is that it
gives an allometric coefficient ξ of 0·795 which lies close to that obtained by the
other method of determination given above (p. 403). As egg sizes increase with
increasing latitudes, there are two different estimates for the temperature effect:
is the temperature characteristic sensu lato
including indirect effects, and when the
effects due to size are excluded. The former estimate is more appropriate for
comparison with published data which usually are not related to size.
EFFECTS OF CHEMICAL FACTORS ON

REPRODUCTION
Vlasblom & Elgershuizen (1977) observed a strong effect of salinity on the
success of marsupial development in Neomysis integer. They also report a small
effect of salinity and of salinity adaptation on the duration of marsupial
development in this species. The data for duration of development surveyed in
Table II include marine, as well as brackish and limnic species. At the
interspecific level there is no apparent salinity effect. If there were effects in the
same degree as in Neomysis, they would be too small to be detected with the
methods applied. McLusky & Heard (1971) report that Praunus flexuosus can
regulate the marsupial fluid hyper- or hypo-osmotically. So far no clear
differences in egg size among populations or species have been established
which are due to a limnic, brackish, or marine mode of life.
In recent years mysidaceans have become increasingly used as test organisms
in acute and chronic toxicity tests (see review by Nimmo & Hamaker, 1982).
Nimmo, Rigby, Banner & Sheppard (1978) found delay of brood release and a
sharp decrease in the number of young due to chronic exposure to cadmium in
the estuarine Mysidopsis bahia. In the same species, increasing concentrations of
mercury lead to an increase of the brood duration (Gentile, Gentile, Hairston &
Sullivan, 1982).
EFFECTS OF NUTRITION ON REPRODUCTION

Johns, Berry & Walton (1981) fed diets of Artemia nauplii from different
geographic locations to the mysidacean Mysidopsis bahia. Due to feeding
different strains of Artemia, the mysidacean showed differences in growth, age at
attainment of sexual maturity, and numbers of young in relation to parental body
size.
Morgan (1980) studied a population of Mysis relicta in the subalpine Lake
Tahoe. In an enclosed embayment with lower biological production, the
mysidaceans needed a longer time to reach sexual maturity and produced fewer
eggs than the population in the main part of the lake. From these findings
Morgan (1980) concluded that differences in life history among populations of M.
relicta may represent a phenotypic rather than evolutionary adaptation.
My own unpublished experiments on the effect of semi-starvation were made
on 49 adult females of Leptomysis lingvura. The animals were fed a diet of
Artemia nauplii corresponding to ′ 50% satiation. They showed prolonged
intermoult periods and produced fewer and slightly smaller eggs than control
animals. All broods were aborted from the brood pouch in a premature condition
and eaten by their parents. (The breeding females were cultured individually as
described by Wittmann, 1981a, b.)
Numbers of adult females with empty brood pouch are usually small in
samples of natural populations, but this is not always so (see p. 414). They
originate from two possible sources, abortion or prolonged intermoult periods
which are longer than incubation time. Clutter (1969) observed strong variations
in the relative numbers of animals with empty brood pouch in a population of
Metamysidopsis elongata. These fluctuations showed a significant correlation
with population density. Clutter assumes this to be related to variations in food
availability.
When these findings are summarized it appears that the mysidaceans have a
strong capability of adapting reproduction to ambient food levels. Thus the
strong seasonal variations of reproduction in temperate climates are supposed to
be to a large extent due to direct responses to variations in food availability.
434 KARL J.WITTMANN
INTRASPECIFIC VARIATIONS IN BREEDING BIOLOGY
SEASONAL AND INDIVIDUAL VARIATIONS IN SIZE

AND BREEDING INTENSITY
Mauchline (1980) has given an extensive review of the literature dealing with
seasonal and other aspects of size and breeding in mysidaceans. Therefore, I
shall restrict myself to a short outline in relation to the following question: to
what extent are seasonal variations of the incubation period compensated by
variations in size and breeding intensity in iteroparous mysidaceans?
In the majority of iteroparous species in temperate climates, the adult females
reach maximum body sizes in winter to spring or early summer and minimum
sizes in summer to autumn. In mid-autumn to early winter there is a steep
increase of sizes at attainment of sexual maturity. Maximum brood sizes tend to
be in spring or early summer and, following this, to decline steadily until autumn.
Breeding then ceases or, when breeding is continuous, brood sizes tend to
increase again. At any given season, brood sizes increase with increasing body
size in almost every species so far studied. Nevertheless, seasonal patterns of
brood sizes are also apparent in many species when females of equal body size
are compared. Typical examples of such patterns are found in Leptomysis bürgii,
L. lingvura, Neomysis integer, N. intermedia, N. japonica, N. mercedis,
Paramysis intermedia, P. ullskyi, Praunus inermis, P. flexuosus, and
Schistomysis spiritus (see Blegvad, 1922; Nouvel & Nouvel, 1939; Ishikawa &
Oshima, 1951; Kinne, 1955; Murano, 1964a; Mauchline, 1965, 1967, 1971c;
Brown & Talbot, 1972; Borodich & Havlena, 1973; Wittmann, 1978a; Gaudy &
Guerin, 1979; Parker & West, 1979; Siegfried, Kopache & Knight, 1979). In
some species of temperate climates winter eggs are larger than summer eggs. At
any given season there seems to be no relation between parental size and egg
diameters (Mauchline, 1980; Wittmann, 1981b). In some species there may be no
measurable seasonal variations of egg size (Mauchline, 1980).
Some species do not conform with the above seasonal variation of breeding in
temperate climates. For example, Mauchline (1969) observed maximum brood
sizes of Leptomysis gracilis in summer to autumn. According to Brown & Talbot
(1972), fecundity undergoes no clear seasonal variations in Gastrosaccus
psammodytes.
This short outline clearly shows that temperature compensation for numbers of
young per female incubatory day (that is, the number of young/time of
incubation in days) is generally low between seasons. This is indicative that
other factors, such as seasonal variations of food supply, are at least of equal
importance. As stated above, the temperature effect on incubation periods at the
intraspecific level is generally small. Nevertheless, the above findings imply that
an average species in temperate climates must undergo strong seasonal variations
in the relative amount of body weight invested into reproduction. As there are no
published data on direct weight measurements of broods in relation to parental
weight, I am including preliminary results of a study on a population of

Leptomysis lingvura off the island of Ischia in the Gulf of Naples using samples
taken in 1979 and fixed in sea-water formalin. Dry weights of whole broods at the
‘egg’ stage and of parent animals were determined separately. Average relative
fecundity varied between a maximum of 44% body weight in March, and a
minimum of 16% in early November. Despite strong seasonal variations, at a
given season, there is no apparent correlation of body weight with relative
fecundity, and also no correlation with egg weight. There is, however, a strong
linear, but seasonally varying, relation between numbers of eggs and parental
weight. Because of these findings I recommend that brood sizes and parental
body lengths are related on a log scale rather than the linear scale which is more
commonly used in the literature.
Consequently, not only the fecundity but also the natality (birth rate) in an
average species must undergo seasonal variations in temperate climates. As
mentioned above, in most species maximum brood sizes tend to be in spring to
early summer. Due to the effect of temperature on incubation periods it is
expected that maximum natality expressed as numbers of young per female
incubatory day should be reached in late spring to summer in the majority of
species. Minima are expected in autumn to winter. This is supported by rough
estimates given by Wittmann (1978a) for L. lingvura. These estimates can be
slightly corrected using more precise estimates for incubation periods given by
Wittmann (1981b). In the North Adriatic (1973–75) maximum natality is attained
in June to July with 1·0 egg per female per day, the minimum was in November
with 0·3 egg per female per day; following this breeding ceases. In the
Tyrrhenian Sea (1967–77), the maximum is attained in May to June with 1·2
eggs per female per day and the minimum in November to December with 0·2
egg per female per day; following this natality increases again. Thus, natality is
similar in both sea areas despite the generally larger eggs and larger body sizes in
the North Adriatic. In the Tyrrhenian population maximum population densities
were observed three to four weeks following the peak of natality. These
observations are interpreted as being adaptive in relation to the winter minimum
and spring maximum of biological production in both sea areas (Wittmann,
1978a).
DURATIONS AND FREQUENCIES OF MARSUPIAL

STAGES
The durations of the different marsupial stages appear to vary considerably. On
the average, the embryonic stage, that is from oviposition to hatching from the
egg membrane, takes 25–40% of the total incubation period. The subsequent
nauplioid stage lasts another 30–45%, this is until the first larval moult which
takes place in the marsupium in all species so far studied. At this moult the
postnauplioid stage hatches which accounts for the last 15–30% until release
from the brood pouch. The second larval moult may take place shortly before
436 KARL J.WITTMANN
release in some species, or shortly afterwards in others. In certain species the

relative duration of the postnauplioid stage is shortened by an increase in
temperature (Wittmann, 1981b). Taking a bias of about 10% of the total
incubation period into account, the percentages of females carrying different
types of young in nature may be used to reflect the durations of the different
marsupial stages provided that breeding is highly asynchronous (Mauchline,
1973; Wittmann, 1981b).
MORTALITY OF BROOD POUCH YOUNG

It appears to be a usual feature in mysidaceans that the numbers of marsupial
young decrease with successive larval stages. In his study on eight Scottish
species Mauchline (1973) estimated that about 10% of young are lost in
premature condition. This was confirmed by a more detailed study of Wittmann
(1981b) on L. lingvura which loses about 11% of young. The brood pouch young
are almost immotile and helpless. Thus, almost all loss of young is assumed to
result in mortality. A small number of lost young may be captured by other
breeding females and adopted into the brood pouch (Wittmann, 1978b;
Mauchline, 1980). A minimum estimate indicates that 0.80% of the females of L.
lingvura carry one or more adopted young in natural populations in the
Mediterranean (Wittmann, 1978b). Thus, adoption appears to be of little
quantitative importance for the survival of young.
The reasons why premature larvae disappear are still unknown. For Mysis
stenolepis, Amaratunga & Corey (1975) report “that females were capable of
releasing young at any point subsequent to the first embryonic moult” that is still
in premature and almost immotile condition. Other authors did not observe the
same behaviour in other species. Due to embryonal and larval growth the broods
swell considerably in volume. This becomes compensated by enlargement of the
brood pouch by reducing the overlap of the marsupial plates. As young become
lost at any stage of development the volumetric problem may have little
quantitative importance.
A further source of the loss of young may be cannibalism. As shown above,
females of Leptomysis lingvura may eat their own offspring under conditions of
starvation in the laboratory. This was not observed in well-fed animals, nor were
signs of cannibalism found in the stomach contents of this species sampled in
nature. This was not so for Siriella jaltensis (Wittmann, 1981b). During release of
young, cannibalism was observed in some species while in others it was not
(Berrill, 1969; Wittmann, 1978b; Amaratunga & Corey, 1979).
As far as is known, a small contribution to marsupial mortality appears to be
due to parasites, especially epicaridean isopods (see Mauchline, 1980).
INTERSPECIFIC VARIATIONS IN REPRODUCTIVE

BIOLOGY
LATITUDINAL VARIATIONS OF BREEDING PERIODS

AND TIMING
Mauchline (1980) considered the population dynamics of mysidaceans from the
tropics to the Arctic. He gives the following classification: (a) species producing
<0·5, (b) 0.5, (c) 1, (d) 2, (e) 3, and (f) >3 generations per year. For details one
should consult his extensive review.
The latitudinally varying breeding cycles are very similar to those reported for
amphipods by Steele & Steele (1975b). In both orders of Peracarida length and
timing of breeding periods seem to be indicative of an adaptive behaviour in
order to ensure that the young are realeased into an environment of optimal food
supply (Steele & Steele, 1975b; Wittmann, 1978a). The underlaying concept is
that proposed by Barnes (1957) in his study on the barnacle Balanus balanoides.
Wittmann (1978a) discusses the available data on periods and timing of breeding
in mysidaceans from the tropics to the Arctic in relation to the assertions of
Dietrich & Kalle (1965), Whittaker (1970), and Odum (1971) for the timing of
biological production in aquatic ecosystems. Mysidacean species appear to be
capable of utilizing a wide variety of food (Baldo-Kost & Knight, 1975). Thus,
they should be subjected to the seasonal variations of biological production in
general. The time of breeding in any one species usually belongs to one of the
types given below.
Cold-season breeding
Cold-season breeding is typical for Arctic and boreal climates. The eggs are
deposited in autumn or winter. As a consequence of the low temperatures,
breeding continues through the long Arctic winter until the young are released in
spring or early summer into an environment where the short-lived, but intensive,
biological production has already started. The females are usually semelparous.
Under extreme Arctic and/or oligotrophic conditions the newly released young
may need two summers to reach maturity, thus the generation time is two years.
This is the case in some populations of the following species: Antarctomysis
maxima, Mysis relicta, M. litoralis, and possibly also M. oculata (Larkin, 1948;
Geiger, 1969; Fürst, 1972; Lasenby & Langford, 1972; Carpenter, Mansey &
Watson, 1974; Mauchline, 1980; Morgan, 1980). Under extreme oligotrophic
conditions the generation time may last up to four years in M. relicta (Morgan,
1980). Under less extreme temperature or trophic conditions the young mature
by the end of the same growth season as they were released and the generation
time becomes one year. This reproductive cycle was found for populations of M.
litoralis, M. mixta, M. relicta, and M. stenolepis (Apstein, 1906; Wigley &
Burns, 1971; Fürst, 1972; Lasenby & Langford, 1972; Amaratunga & Corey,
438 KARL J.WITTMANN
1975; Ladurantaye & Lacroix, 1980; Morgan, 1980; Grabe & Hatch, 1982).
Künne (1939) reports that almost all species of the southern North Sea are
winter-breeders. The southernmost record of annual breeding (in autumn) on
European coasts is given by Mauchline (1970b) for Mysidopsis didelphis from
waters off Scotland.
Pseudocontinuous breeding
The over-wintering generation of Mysis relicta after having liberated the young
in spring may produce a second brood which remains in the brood pouch through
the summer and becomes liberated in late summer to autumn. Recently, Morgan
(1980) has given evidence that the observation of summer-breeders may not be
due to biparity, but as an alternative explanation may be due to semelparity with
alternating generation cycles. The observation of summer-breeding females in
M. relicta is typical of cold-temperate lakes in Europe and North America, but may
sometimes occur in boreal waters (Samter & Weltner, 1904; Fürst, 1972;
Morgan, 1980). According to Morgan (1980), the production of a summer brood
essentially depends on the trophic state of the lake, as it does not occur in strictly
oligotrophic boreal lakes. In M. relicta, the combination of winter- and summer-
breeding may also be the outcome of complicated alternating life cycles with a
generation time of 18 months (Carpenter et al., 1974). In some Swedish lakes
two populations with different breeding times, summer- or winter-breeders, may
coexist (Fürst, 1972). Where breeding is highly asynchronous, pseudocontinuous
breeding may lead to the presence of breeding females throughout the year
(Reynolds & DeGraeve, 1972). Nevertheless, this type of breeding essentially
differs from continuous breeding as the generation time is one year or longer.
Warm-season breeding
Warm-season breeding is typical of the cold-temperate and, provided there is a
strong seasonal variation in temperature, also occurs in warm-temperate regions.
Two to four generations per year are produced. The over-wintering generation
matures and deposits the eggs into the brood pouch at the end of winter, in spring
or, more rarely, in summer. The young are released a few weeks later depending
on ambient temperatures. Where the summer temperatures are high enough two
subsequent summer generations may be produced as the generation time may be
of the order of eight weeks at 25–27°C (Wittmann, 1978a). The females usually
produce more than one brood so that the generations overlap and breeding
females are present throughout the warm season. The last summer generation
releases its young in autumn thus giving place to the over-wintering generation.
Then breeding ceases completely until late winter or spring. The cessation may be
quite abrupt causing a sharp and short-lived peak in the percentages of females
with an empty brood pouch (Wittmann, 1981a). The generation time of the over-
wintering animals is of the order of four to five months. According to Tattersall
& Tattersall (1951) this type of breeding generally occurs in northern temperate
regions. As pointed out above, it also occurs in more southerly areas of Europe
where the winter temperatures fall below about 10°C; this was found for species
from the Black Sea and bordering brackish and freshwater areas by B cesco
(1940) and Zatkutskiy (1970), for east European inland waters by Borodich &
Havlena (1973; q.v. for other references), and for the North Adriatic by
Wittmann (1978a).
The adaptive significance of warm-season breeding is quite clear. In temperate
climates there is a strong winter minimum and in addition, when there is one, a
smaller summer minimum of production in aquatic ecosystems. In contrast to the
Arctic climate, the winter temperatures are high so that the incubation periods
would be short enough to lead to a winter release following winter-breeding. To
avoid this, breeding starts later, usually at the end of winter to spring. According
to Odum (1970), the spring maximum of production is usually stronger and also
qualitatively different from the autumn maximum. In fact, most species living in
shallow waters of the Mediterranean have the maximum numbers of young in
relation to parental size during the spring months which coincides with the spring
diatom bloom. Generally speaking, breeding in temperate climates is at a high
level from spring to autumn. Not every species cited in the following completely
stops breeding in winter. There are only a few species showing a summer
minimum between maxima of spring and autumn as shown by Murano (1964a)
for Neomysis intermedia and by Zatkutskiy (1970) for Paramysis pontica. There
are, however, a few species with distinct summer maxima of breeding such as
Mysidopsis bigelowi and Neomysis americana as shown by Hopkins (1965) and
Richards & Riley (1967).
Continuous breeding
The importance of seasonal variations in temperature for biological production in
the sea decreases with decreasing latitudes (Whittaker, 1970). This is reflected by
the patterns of breeding in mysidaceans.
Continuous breeding with partial winter depression is typical for moderately
cold- to warm-temperate regions with low seasonal variation. The majority of
species in waters off Scotland (Mauchline, 1980), in the Gulf of Marseille
(Macquart-Moulin, 1965), and the Gulf of Naples (Wittmann, 1978a, unpubl.
obs.) belong to this type. Comparable observations are reported by Hodge (1963)
and Connel (1974) for three species from the Southern Hemisphere. Breeding
females are present throughout the year, but in distinctly lower numbers during
winter. At least two generations per year are produced but there may be many
more. Extrapolation of laboratory data indicates that Leptomysis lingvura
produces about six generations per year in the Gulf of Naples when the
calculation is based on the time to first brood release (Wittmann, 1978a). As the
females tend to produce more than one brood, the average number of generations
should be about four to six depending on estimates of longevity. Breeding is
440 KARL J.WITTMANN
highly asynchronous and, therefore, distinct generations cannot be identified in

the field.
Continuous breeding sensu stricto appears to be typical of tropical climates
(Goodbody, 1965; Almeida-Prado, 1973; Quintero & Roa, 1973). It is only rarely
found in temperate regions as reported for Gastrosaccus psammodytes by Brown
& Talbot (1972) and for Neomysis mercedis by Heubach (1969). The time to
first brood release in the subtropical species Mysidopsis bahia reared in
laboratory at 20–21°C is 20 to 27 days, according to Gentile, Gentile, Hairston &
Sullivan (1982) and Gentile, Gentile, Walker & Heltshe (1982). A crude
extrapolation suggests that this species produces about 10 to 15 generations per
year.
When the world fauna of epipelagic and coastal Mysidacea is seen as a whole
it appears that there are two natural groups, cold-water breeders and warm-water
breeders, which are fundamentally different. The former are semelparous or
occasionally biparous, and ususally breed intensively during the cold season at 0–
7°C, the latter are usually iteroparous and breed intensively above 10°C.
LATITUDINAL VARIATIONS OF BROOD SIZES

Available data for average numbers (N) of young are related to the temperature
at the most intensive breeding season as far as the intensity of breeding can be
estimated from the literature. The majority of temperature data were estimated
from extended ranges (mainly given by Mauchline & Murano, 1977) and from
climatological data given by Dietrich & Kalle (1965) and Ekman (1967). The
results for 96 species of warm-water breeders given in Figure 3 fit to a straight
line when expressed as a variant of the Arrhenius equation in its broadest sense:
where a=-29·18± 3·25 and ; . The
temperature characteristic μ does not significantly differ from that for the
incubation periods . This shows that the production of young per
female incubatory day has no significant latitudinal trend. An approximate
estimate for the average production of an average species can be made from the
data for warm-water breeders in Table II: this gives 1·30 young/day
. As expected there is no apparent correlation of the daily
production of young with the inverse temperature on the semilog data
. In other words, the brood size of an average warm-water
species amounts to about 1·30 times the incubation period in days, irrespective of
latitudinal distribution. This finding strongly indicates that there is an adaptive
temperature compensation between the reproduction of parent animals and the
temperature triggered interspecific variations in the development of the brood
pouch young. This compensation is probably of adaptive value for species which
have the parental reproduction synchronized with the development of young.
In the Mysidacea and in the Peracarida in general, egg-laying is coupled with
moulting. In iteroparous mysidaceans the release of fully developed young
precedes moulting, copulation, and subsequent deposition of eggs belonging to
Fig. 3.—Average numbers of young in 110 species (a total of 129 populations) of

Mysidacea in relation to temperature and geoclimatic distribution: ′ , are for 96 species
of epipelagic or coastal warm-water breeders; ′ , are for four epipelagic or coastal cold-
water breeders; *, are for five mesopelagic species; ′ , are for five bathypelagic species;
the continuous line was fitted to the data for warm-water breeders using the Arrhenius
equation; dotted lines indicate 99% confidence intervals for individual data sets.
the second or further brood. In the majority of species especially in warmer

regions these events occur within one night or occasionally two. The
synchronization is attained by moult inhibition (Wittmann, 1981b). In semi-
starved females moulting and subsequent extrusion of eggs may be delayed for
some days, but this is not so for the development of young.
So far it has not been demonstrated for any mysidaceans that the females may
be able to reduce their brood plates at moulting as is known for amphipods. In
samples from natural populations in temperate regions only a small number of
females with an empty brood pouch are found during the main breeding season
in the majority of species. In a few species, however, there are larger numbers
throughout the year (compare species examined by Macquart-Moulin, 1965;
Mauchline, 1965–1971; Wittmann, 1978a); in such species there may be less
synchronization or some of the empty brood pouches may be due to abortion. So
far a further possible explanation, maturation moult without subsequent egg-
laying, has not been demonstrated in the laboratory. According to my experience
the numbers of empty marsupia in samples are highly dependent on the methods
of sampling and conservation as young tend to fall out. Therefore, in many cases
the number may be over-estimated.
442 KARL J.WITTMANN
Such a synchronization cannot exist in semelparous species by definition, so it

is not surprising that the numbers of young in cold-water breeders do not
conform with the temperature relation shown in Figure 3. All three groups, epi-,
meso-, and bathypelagic species tend to produce smaller broods than expected
from the temperature relation. In epipelagic (including coastal) cold-water
breeders this is mainly due to smaller parental sizes in relation to temperature
(see p. 417). In contrast to that in meso- to bathypelagic species it is due to
smaller broods and larger eggs in relation to parental size as was shown by
Mauchline (1973). So far, the only bathypelagic species in which reproduction
has been investigated is the semelparous Gnathophausia ingens (Childress &
Price, 1978). Large sizes are supposed to be of adaptive significance to the
stability and low food levels in mid- and deep waters (Mauchline, 1973;
Childress & Price, 1978). Figure 3 indicates a very high diversity of brood sizes
in bathypelagic habitats. This may be partly due to loss of young from marsupia
during the long sampling procedures. If not so, one may expect a variety of life
cycles in the deep sea.
LATITUDINAL VARIATIONS OF EGG SIZES

Steele & Steele (1975a) note that in amphipods and mysidaceans the duration of
embryonic development in relation to egg size is shorter than in copepods,
barnacles, isopods, cumaceans, and decapods (the measurements of egg sizes in
these groups cannot be compared without some reservations). The results
presented in the present article for mysidaceans support this conclusion. The
difference seems to be due to larger eggs in amphipods and mysidaceans but not
to principally shorter periods of development in relation to temperature when the
results from the tropics to the Arctic are compared. For example, copepods
(McLaren, Corkett & Zillioux, 1969) develop faster, but decapods (Wear, 1974)
develop more slowly than mysidaceans when the time from deposition to release
of young is compared.
The Amphipoda and the Mysidacea have in common that the young are
released as miniature adults. Because of this, the Amphipoda have a large lower
limit of egg size: 0·25 mm according to Steele & Steele (1975a). Exactly the same
limit is found for the Mysidacea when the data in Figure 4 are compared. This
coincidence is seen within the frame of the close phylogenetic relationship of the
orders Amphipoda and Mysidacea which in part is supported by common
characteristics in embryology and brood biology (Siewing, 1951, 1953;
Wittmann, 1981b).
Figure 4 shows that egg sizes (diameters DE, in mm) increase with decreasing
temperatures or increasing latitudes. This is a well known feature in many groups
of marine poikilotherms. The data for 58 species of epipelagic (including
coastal) warm-water breeders fit to a straight line when expressed as a variant of
the Arrhenius equation: . Calculation gives and
; . The confidence intervals in Figure 4 show that
Fig. 4.—Egg sizes in 72 species (a total of 85 populations) of Mysidacea in relation to

temperature and geoclimatic distribution: ′ , are given for 58 species of epipelagic or
coastal warm-water breeders; ′ , are for four epipelagic or coastal cold-water breeders; *,
are for four mesopelagic; ′ , are for six bathypelagic species; lines are fitted as in
Figure 3.
the egg sizes of the majority of epipelagic cold-water breeders conform with this
relation. This also holds true for meso- but not for bathypelagic species. This is
due to a larger maximum of egg size in the deep sea.
When the egg diameters are substituted by their relation to dry weights (p. 404),
an approximate estimate for the relation of egg weights (in mg) to the
temperature can be made where and
. The temperature characteristic μ does not significantly differ
from that for the incubation periods . As for brood sizes this
finding is interpreted as an outcome of the interdependence of marsupial
development and reproduction of the parent. The investment of eggs with yolk
per female incubatory day obviously has no significant latitudinal trend. This
relation is quantitatively evaluated by calculation of the average production of
yolk per incubatory day from the data for warm-water breeders in Table II (egg
weights partly estimated from diameter). An average species produces 1·94 μ g
yolk·egg−1·day−1 . As expected there is no correlation with the
inverse temperature on the semilog data .
In studies of variation of egg size with latitude it is usually emphasized that
large eggs produce large young and the fitness of young in terms of survival is
often correlated with the size of young (Thorson, 1950). This seems to be of
444 KARL J.WITTMANN
special importance at higher latitudes where there is a very long unfavourable

season. Steele & Steele (1975b) assume that in amphipods the different egg sizes
at different latitudes are indicative of an adaptive method of the timing of the
release of young in relation to the seasonally varying food supply. The authors
did not numerically distinguish the effects of egg size and of latitudinal
temperature adaptation. An examination of this kind may possibly result in the
finding that egg size is only of small, but significant, importance when compared
with the temperature response as has been found for mysidaceans. An average
tropical species incubates for four days at 28°C and carries eggs with 0·35 mm
diameter. The Arctic counterpart incubates for 160 days at 1°C and the eggs
measure 0·86 mm. According to the three-variable equation above (p. 405), egg
size is responsible for a twofold increase in the incubation period between
latitudes. In contrast to that, the temperature causes a nineteenfold increase. Both
egg size and temperature response are assumed to be in part adaptive but are they
adaptive in the sense of Steele & Steele (1975b)?
This is examined by comparison of two species which breed at the same
temperature (3°C) and have adult females of comparable size (20 and 24 mm,
respectively). The first is a subarctic population of Mysis litoralis which
produces about 80 very large eggs with 1·8 mm diameter. Mainly due to egg size
the incubation period is very long, lasting over six months. According to
Ladurantaye & Lacroix (1980) the eggs are deposited in late October or early
November, and the young are released in April to May. The second is a boreal
population of M. stenolepis which produces on average 157 small eggs with 0·52
mm diameter. Mainly due to small egg size, the incubation period is short,
namely about 2·5 months. According to Amaratunga & Corey (1975) the eggs
are deposited in about February and the young are released in April to May. It is
obvious that both species liberate their young at the same season despite of
having different egg sizes and incubation periods. The properties of these two
species lead to a hypothesis which is in contrast to the assumption of Steele &
Steele (1975b) for amphipods. The main adaptation for the timing of the release
of young takes place by adjustment of the timing of copulation and subsequent
oviposition. Variations of the incubation period due to egg sizes are compensated
by adaptations in this timing.
Steele & Steele (1975a) give a list of ecological implications of egg size; four
of their six points appear to be important for mysidaceans.
(1) The size of young at release depends only on egg size and does not vary
with the temperature as was shown by Wittmann (1981a) for Leptomysis
lingvura. Between latitudes it should behave like egg sizes.
(2) The size at maturity is positively correlated with egg size as both increase
with increasing latitudes (see also p. 422).
(3) The number of eggs per brood at any given brood weight must decrease
with increasing egg size. On the interspecific level egg size (DE, in mm) and
brood size (N) are, however, positively correlated as both features increase with
parental size and with increasing latitudes. The relation is expressed as the
allometric equation: ; for 56 species which

breed above 10°C. From μ values for N and DE given above (pp. 412, 415) one
would have expected an allometric exponent , or from a values for
the relation to parental size given below (pp. 421, 422) an exponent
. The empirical value is significantly below both variants of expectation. This
indicates that the positive correlation of numbers of young and egg diameters is
superimposed by a weaker negative correlation due to species with larger eggs in
relation to parental size or latitude producing fewer young. There is no significant
correlation between numbers of young and egg sizes in epi- to bathypelagic cold-
water breeders at the interspecific level .
(4) The number of broods per unit time is largely an outcome of incubation
time in iteroparous mysidaceans. As egg size is in part responsible for variations
of the incubation time it appears to have some importance.
LATITUDINAL VARIATIONS OF BROOD WEIGHTS AND

PARENTAL SIZES
Both egg weights and numbers of young increase almost linearly with the
incubation periods (DI). Thus brood weights are supposed to increase in
proportion to . Brood weights were estimated from the data for average brood
sizes (Fig. 3) during intensive breeding seasons and from egg weights, the
majority of which were derived from diameters (Fig. 4). The temperature relation
of brood weights (in mg dry wt) in 56 species of warm-water breeders conforms
well with the Arrhenius equation where and ;
. This finding agrees well with the expectance that the
temperature characteristic μ should be about double that for the incubation
periods .
Such a steep increase of brood weights with decreasing temperature or
increasing latitudes must have marked consequences on parental size. Data on
the relation of parental body lengths (total length, L, in mm, as defined by
Mauchline, 1973) to the temperatures at intensive breeding seasons are given in
Figure 5. The data for 108 species of warm-water breeders fit well to the
Arrhenius equation where and ;
. The epipelagic (including coastal) cold-water breeders tend to have smaller
sizes than calculated from this equation. As shown by the confidence intervals in
Figure 5, the sizes of meso- and bathypelagic species conform with this relation
with only few reservations. O
Before these considerations are continued one needs to evaluate the
relationship between parental body weight (WP, in mg dry wt) and length (L, in
mm) at the interspecific level. Mauchline (1980) reviews the length-weight
relationships in mysidaceans. Additional data are given by Juday & Birge
(1927), Båmstedt (1978), Gaudy (1979), Bremer & Vijverberg (1982), and Sell
(1982). My own unpublished measurements were made on L. bürgii in the
Adriatic and the Tyrrhenian Sea
446 KARL J.WITTMANN
Fig. 5.—Body lengths of breeding females in 130 species (a total of 150 populations) of
Mysidacea in relation to temperature and geoclimatic distribution: ′ , are given for 108
species of epipelagic or coastal warm-water breeders; ′ are for five epipelagic or coastal
cold-water breeders; * are for seven mesopelagic; ′ , are for ten bathypelagic species;
lines are fitted as in Figure 3.
. According to Lasenby & Langford (1972)

there may be considerable differences between populations of the same species
(Mysis relicta). Data for 13 temperate to Arctic species with a total of 20
populations are available. At the interspecific level, the weight of adult females
excluding their broods depends on body length according to the allometric
relation: ; ; . The Mysidacea are highly
uniform in body shape when compared with other orders of Peracarida,
especially the Amphipoda and Isopoda. Therefore, this relation should be a
valuable method of estimating body weights in the present context.
The length-weight relationship is used to give a rough estimate for the
temperature relation of parental body weights (in mg) in warm-water breeders:
and ; . The μ value conforms
well to the finding for brood weights but is significantly below . For
warm-water breeders there appears to be no significant latitudinal trend in the
percentage of body weight spent in reproduction. This was improved by relating
the quotient of brood weight and parental weight to the inverse temperature on
the semilog data ; . For only four species in Table II,
Leptomysis bürgii, L. lingvura, Metamysidopsis elongata, and Mysis relicta, are
data from direct measurements available for both egg and parental weights.
These results indicate that an average of 23% body weight is

invested in reproduction for each brood.
From the data in Table II one can calculate the production of yolk (in mg dry
wt) per female incubatory day per mg parental weight; the majority of data on
weights are derived from length-weight relationships. To reduce the sources of
error, those data were selected where all results such as egg size, parental size,
number of young, incubation period, and temperature were determined for
individuals belonging to the same population. The species selected in this way
were Diamysis bahirensis, Gastrosaccus vulgaris, Leptomysis bürgii, L. lingvura,
Mesopodopsis orientalis, Metamysidopsis elongata, M. insularis, Neomysis
integer, Praunus inermis, and Schistomysis spiritus (Table II). The temperature
relation of yolk production fits well to the Arrhenius equation where
and ; . As the temperature characteristic μ is
negative, the animals appear to be more productive at higher temperatures in
spite of producing smaller eggs and the attainment of smaller final sizes.
According to Kinne (1963, 1970), this situation is typical for marine
poikilotherms in general. The μ value does not significantly differ from the
negative value for the incubation periods . This leads to an
assumption which seems to be important for the physiological understanding of
the balance between parental size, parental reproduction, and marsupial
development at the interspecific level. Yolk formation in relation to parental
weight is accelerated by a given increase in temperature in about the same way
as marsupial development.
DISCUSSION ON LATITUDINAL TEMPERATURE

COMPENSATION OF REPRODUCTION
The statements below are valid primarily for second and subsequent broods of
iteroparous mysidaceans. The eggs of the first brood are produced during two or
three moult intervals before attainment of sexual maturity in Leptomysis lingvura
(Wittmann, 1981a). These combined two to three intervals are usually of the
order of one to two times the incubation period (Clutter & Theilacker, 1971;
Wittmann, 1978a; Gaudy & Guerin, 1979; Cuzin-Roudy, Berreur-Bonnenfant &
Fried-Montaufier, 1981). According to Cuzin-Roudy et al. (1981) the first egg
clutch becomes aborted in Siriella armata. These findings indicate that the
implications below may also be of some importance for the first (non-abortive)
brood.
Reproduction of the parent is synchronized with the development of young as
in almost any other iteroparous brood protecting animals. As the development of
young is generally highly temperature sensitive in poikilotherms, this poses
strong implications for the reproductive fitness of the parent animal. A high
degree of latitudinal homeostasis is shown in mysidaceans. As the temperature
relations of incubation periods are highly different between the inter- and the
intraspecific level, it seems likely that there are complex adaptations in any
448 KARL J.WITTMANN
single species in relation to its latitudinal distribution. The factors involved are
parental weight, brood weight, number of young, egg weight, and incubation
period.
Homeostatic adaptations appear to be indicative of the finding that the
following patterns have no significant trend with latitudes or temperature: (1)
natality, expressed as the average number of young produced per female
incubatory day, (2) relative fecundity, expressed as the percentage of body
weight per brood spent for reproduction, and (3) the average amount of yolk
invested per egg per day. It is obvious that the compensation of temperature
effects on points (1) and (2) must have high adaptive significance as both directly
affect reproductive fitness. This is not so clear for point (3). It seems probable
that larger eggs are likely to lead to larger adult sizes. In this way (3) may
stabilize (1) and (2). But egg sizes also bear de-stabilizing implications due to
their importance for the incubation period. This may explain why egg sizes are
less strongly correlated with temperature than the other factors discussed above.
INTERSPECIFIC ALLOMETRIC REL ATIONSH I PS IN

BREEDING
Latitudinal temperature compensation of reproduction bears noteworthy
implications on allometric relationships between females and their reproductive
products.
Mauchline (1973) found that the volume of broods corresponds to about 10%
of the body volume of the parent. Species of all size classes, including meso- and
bathypelagic species follow this rule. The percentage agrees very well with the
above finding that about 23% of body dry weight is invested in reproduction
taking into account that eggs are much denser than bodies. According to my own
measurements on Leptomysis lingvura, eggs have a water content of about 51%,
the adult animals with empty ovaries have 82–84% or about 78% with filled
ovaries, shortly before moulting and oviposition (samples dried for two days at
80°C).
On the assumption that reproduction shows perfect temperature compensation,
it is expected that the numbers of young increase with the square root of body
weight. Thus they are supposed to increase with body length by about L(3/2) or
when the length-weight relationship given above (p. 418) is used, by
. This hypothesis is supported by the finding of Mauchline
(1973) that the maximum numbers of young in epipelagic (including coastal)
species are related to the body length raised to the third power by an allometric
exponent . As it fully supports the above assumption.
Mauchline (1973) distinguishes two natural groups, the meso- and bathypelagic
species which show no significant relation between maximum brood sizes and
body length, and the epipelagic species where a strong relation exists.
Figure 6 relates average numbers of young (N) at intensive breeding periods
directly to the body length (L, in mm). There seems to be no difference between
Fig. 6.—Relation of brood size to parental body size in 110 species (a total of 127
populations) of Mysidacea: ′ , are given for 96 species of epipelagic or coastal warm-
water breeders; ′ , are for four epipelagic or coastal cold-water breeders; *, are for five
mesopelagic; ′ , are for five bathypelagic species; the continuous line was fitted to the
data of epipelagic and coastal species using the allometric equation: the dotted lines give
99% confidence intervals for individual data sets; the dashed line was fitted to the data for
meso- and bathypelagic species; majority of data from Mauchline (1980).
epipelagic warm- and cold-water breeders. The data for 100 species give the
relation ; . The allometric exponent differs
significantly from but not so from when the scatter of the
expected value is also taken into account. In addition, the data for average brood
sizes in meso- and bathypelagic species give a significant relation with parental
body length provided those data are excluded where the brood sizes were
determined on only a single individual: ; . The
allometric exponent is significantly smaller than in the epipelagic species. As
shown by Mauchline (1973) and in Figure 6, the meso- and bathypelagic species
tend to carry smaller broods than epipelagic or coastal species.
According to the above assertions, for the relation of egg weights to parental
weights one expects an allometric exponent . Thus egg diameters should
increase with body length by about L(½), or using the allometric relations given
above (pp. 404, 418) by . Mauchline (1973) related egg
volumes to the body length raised to the third power. For epipelagic species he
found an which practically coincides with the expectation of .
For meso- and bathypelagic species he found an almost linear relation
. Figure 7 relates egg diameters (DE, in mm) to body lengths. On the basis of
450 KARL J.WITTMANN
Fig. 7.—Relation of egg size to parental body size in 72 species (a total of 83 populations)
of Mysidacea: ′ , are given for 58 species of epipelagic or coastal warm-water breeders; ′
are for four epipelagic or coastal cold-water breeders; *, are for four mesopelagic; ′ , are
for six bathypelagic species: the continuous line was fitted to the data of warm-water
breeders using the allometric equation; the dotted lines give 99% confidence intervals for
individual data sets; the dashed line was fitted to the data for epipelagic or coastal cold-
water breeders, meso- and bathypelagic species; majority of data from Mauchline (1980).
more data I have slightly modified Mauchline’s (1973) grouping. Warm-water

breeders are opposed to the combined epipelagic cold-water breeders and meso-
to bathypelagic species. The data for 58 species breeding in warm waters give
; . The allometric exponent significantly
differs from but not so from . .
The confidence intervals in Figure 7 indicate that the epipelagic cold-water
breeders conform with meso- to bathypelagic species rather than with warm-
water breeders. In agreement with Mauchline’s (1973) finding, the relation for 14
species of epi- to bathypelagic cold-water breeders is approximately linear:
; . The allometric exponent conforms with
, but significantly differs from . This difference shows that the
allometric relation a′ ½ is adaptive as it enables iteroparous species to maintain
an equilibrium between incubation periods, numbers of young, brood weights,
and body sizes. As the cold-water breeders are predominantly semelparous an
a′ ½ would have no apparent adaptive significance.
ETHOECOLOGICAL ASPECTS OF REPRODUCTION

In the order Mysidacea sperm transfer is direct as usual for Peracarida. In no
species so far studied is there anything comparable with the precopula which is
typical in the closely related Amphipoda. This is also indicated by the fact that
mysidacean males are usually slightly smaller in size than females. The problem
of attracting mating partners is solved in the following way in the Mysidacea.
Females ready to copulate may release a sexual attractant which alarms the
males in the surroundings (Nouvel, 1940; Clutter & Theilacker, 1971; Wittmann,
1982). Many species live in swarms or in similar dense aggregations during
daytime. There is the problem that copulation takes place exclusively during the
hours of darkness. This is at the time when the swarms disintegrate and the
individuals disperse over the sea bottom or migrate upwards into surface water
levels. This was found for a total of six swarming species studied by Macquart-
Moulin (1973), Wittmann (1977, 1978a, 1982), and Dauby (1980), but is not so
in Metamysidopsis elongata as is reported by Clutter (1969). In a few cases
dense aggregations of Leptomysis lingvura were found which remained close to
the sea bottom at night and occasionally remained there until the early morning
hours (Wittmann, 1982). As these aggregations contained many adults, they may
have been mating aggregations but this needs further confirmation.
At the high summer temperatures (25–27°C) in Mediterranean surface waters,
the frequency of propagative events is so high that the diurnal rhythm of release
of young, of ecdysis, and of egg laying is reflected in the frequencies of the
diverse stages and of exuviae in samples of natural populations of L. lingvura.
The release of fully developed young starts shortly before sunset. This is
followed by moulting and mating. Eggs are deposited from one to six hours after
sunset (Wittmann, 1982). These findings confirm laboratory results on this and
other species (Nouvel, 1937, 1940; Labat, 1954; Clutter & Theilacker, 1971;
Wittmann, 1978b). So far L. lingvura is the only species where a spermatophore
was found to be placed into the marsupium at copulation (Wittmann, 1982). In
all species so far studied copulation lasts only a few seconds or less. Hakala
(1978) found that males of Mysis relicta in lakes of Finland died shortly after
copulation.
In many species the adults tend to gather together to form breeding
aggregations (see species list given by Mauchline, 1980). In some species, such
as M. stenolepis and Gnathophausia ingens the females breed in deeper waters
and migrate into more shallow regions prior to liberation of fully developed
young (Amaratunga & Corey, 1975; Childress & Price, 1978). In Gnathophausia
the breeding females tend to stay apart from the residual population.
452 KARL J.WITTMANN
GENERAL CONCLUSIONS FOR THE UNDERSTANDING

OF BREEDING BIOLOGY IN MYSIDACEANS
There are two basically different groups, semelparous and iteroparous
mysidaceans. Differences are apparent not only in generation times and timing of
breeding but also in the allometric relationships between parents and young. The
latter differences appear to be due to the number of broods per se as in the case of
semelparity there is neither the necessity nor the possibility of synchronizing
development and production of subsequent broods. There is no doubt that
semelparity is of advantage in high latitudes due to the low temperatures in
combination with the short duration of the favourable season. It is, however,
known also from the giant bathypelagic species G. ingens which probably lives
in a relatively stable environment. Childress & Price (1978) discuss the possible
advantage of semelparity for this species and state” …because of the greater
stability of its habitat it can…concentrate all its reproductive effort on a single
event. This may be much more energy efficient, since the reproductive
individual can use a larger fraction of its energy in reproduction…”. This
remains speculative as long as there are no weight or energy measurements
which compare broods and breeding females. Volumetric studies of Mauchline
(1973) indicate that the meso- and bathypelagic species including G. ingens
invest on the average the same fraction of body volume in reproduction as do
epipelagic species.
In iteroparous mysidaceans the breeding biology is split into three highly
different levels which involve differences (1) between latitudes, (2) between
seasons (provided that there is a strong seasonal climate), and (3) between
individuals.
Natality and relative fecundity, as defined above, both appear to be constant
between latitudes but undergo strong seasonal variations. Natality increases with
increasing individual size but, as far as is known, relative fecundity does not
seem to vary with variations in size. Absolute fecundity expressed as numbers of
young per brood increases with increasing latitudes in relation to temperature. At
the favourable season absolute fecundity is high, but at or shortly before the onset
of the unfavourable season, fecundity is low and largely independent of seasonal
variations in body size and temperature. Brood sizes increase linearly, or
possibly less than linearly, with individual body weight. In contrast to this, brood
size increases with about the square root of weight between latitudes.
Egg weights increase with increasing latitudes in relation to temperature in
about the same way as do brood sizes. Egg sizes may not vary between seasons
in certain species or a species may produce larger winter eggs and smaller
summer eggs. There seems to be no direct relation to temperature as the
production of the larger eggs may start in early autumn at water temperatures as
high as 20–25°C, while on the other hand, the production of small summer eggs
may start in late spring at about the same temperatures (pers. obs. on Leptomysis
lingvura in the Gulf of Naples). There appears to be no correlation between egg

sizes and individual parental body sizes.
As a consequence of the foregoing, the production of yolk per egg per
incubatory day does not vary between latitudes and also not, as far as is known,
between individuals. There may, however, be strong variations between seasons.
Weight at attainment of maturity and brood weights, both increase between
latitudes almost twice as steeply with increasing temperature than do brood sizes
and egg weights. In temperate climates, summer animals are frequently smaller
than winter ones, but similar frequently maximum sizes may be reached in
spring. Similar relations may exist for brood weights. These increase about
linearly with individual body weights. The same relation was found to exist
between latitudes or species. Among seasons this relation is heavily ‘disturbed’
by variations in brood weight due to minima or maxima in breeding intensity.
The key factor for the understanding of these relationships seems to be the
temperature effect on incubation periods. It is strong between latitudes, but much
weaker between seasons. There are no visible differences in the temperature
response between individuals of L. lingvura (Wittmann, 1981b). There is a small
effect of egg size on incubation periods which is about the same between
latitudes and among individuals. Wittmann’s (1981b) results indicate that this is
also most likely between seasons. Each of three levels of breeding performance
are supposed to be indicative of different adaptive significance. Between
latitudes reproduction appears to be adaptive in order to compensate for the
strong effects of temperature on incubation periods. Among seasons the seasonal
variations of food supply and, as an outcome of these, variations of population
levels seem to be of major significance. For individuals it may be of major
importance that a given increase in body weight becomes transformed into a
corresponding increase of individual reproductive fitness, expressed as
production of young per incubatory day. This indirectly favours the capability of
adapting population levels to ambient food levels.
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COMPETITION BETWEEN MARINE
ORGANISMS: ECOLOGICAL AND
EVOLUTIONARY IMPLICATIONS
G.M.BRANCH
Zoology Department, University of Cape Town, Rondebosch 7700,
South Africa
INTRODUCTION
Few subjects have evoked as much interest and controversy as competition. In
all habitats there is a finite amount of food or space, and as populations increase
in density, competition for these resources may occur. Whether this competition
assumes a dominant rôle in structuring communities and in moulding the
evolution of the species is much debated. Although competition has long been
invoked as just such a dominant force, the drawing together of theory,
observation and experiment into what is referred to as “competition theory” owes
much of its roots to Hutchinson’s seminal paper, published in 1959. In posing the
question “Why are there so many species?”, Hutchinson put forward five major
themes, one of which addresses the question of how similar co-existing species
with overlapping requirements can be, if co-existence is to continue. This has
formed the focal point of much competition theory, leading to attempts to
quantify overlap between species and competitive impact of one species on
another— factors that are difficult to assess in real-world situations. In its extreme
form this approach has led to a preoccupation with niche differences as a means
of allowing presumed competitors to co-exist. Hutchinson himself would, I am
sure, be dismayed by the uncritical acceptance and application of his idea. Too
often competition is assumed to exist, and differences between species (and there
must be differences if one searches hard enough) are assumed to allow
‘apportionment’ of the habitat and to permit continued co-existence. These
assumptions are testable but all too often are untested before they are applied to
explain ecological phenomena.
A further development of this theme leads to the idea that current differences
between species that permit co-existence (or even separate the animals to the
extent that they do not compete at all) have their origins in the historical past—
that previous competition has forced the species apart, diverging their niches to
COMPETITION BETWEEN MARINE ORGANISMS 459
reduce competition. Competition is thus taken to be a driving evolutionary force.

The frustration of this approach is that it is unfalsifiable; one can never
manipulate the past to test it, and the dangers of tautological argument are ever
present (Peters, 1976). Heavy reliance is thus placed on circumstantial evidence,
particularly from the relative distribution and abundance of species when they
are living in allopatry (separately) or in sympatry (together).
Trends that come from such comparative studies can be important pointers to
whether competition is important or not (or has been in the past). But even
advocates of this approach, such as Schoener (1974), point out that the patterns
need to differ from those that might be expected by chance before any
significance is attached to them. There are, however, too many ‘ghosts of
competition past’ in the literature, based largely on inferences and correlations,
and the need for critical experiments of the kind outlined by Connell (1980) must
be emphasized.
In 1966 Paine published a critical paper in which he described how a
dominant predator (the starfish Pisaster) is capable of reducing the numbers of a
potentially dominant competitor (the mussel Mytilus californianus) to the point
that it cannot monopolize the environment and other species are capable of co-
existing with it. Others have built upon this idea suggesting that factors such as
physical disturbance or fluctuations of the environment may achieve the same
effect (see, e.g. Wiens, 1977; Connell, 1978). This approach has become popular
and is of course much more amenable to direct experimental manipulations
which can be used to test various ideas. By and large this approach has been
much more critically applied than the early development of competition theory.
Even so, just in the same way as early workers on competition theory were
uncritical in their acceptance of competition as a driving force, so some are now
equally uncritical in ascribing patterns of distribution or abundance to
disturbance or predation. The predation and disturbance hypotheses are not
simply new bandwagons; they too need critical testing under different
circumstances and with different kinds of organisms. I also believe that it is
important that we do not polarize the various approaches into ‘either/or’
situations. It is likely that all these approaches are valid and that in different
situations or in dealing with different animals competition may be important at
times whilst predation and disturbance are important at other times. Ecological
theory is more likely to be enriched by discovering what circumstances lead to a
dominance of each of these structuring forces than by denying that one or more
of them plays any rôle.
A distinction that must be made early in this review is the difference between
exploitation and interference. Competition by exploitation is simply the use of a
common resource, and has been aptly described as a “scramble” in which the
individuals which are quickest to the resource and use most of it are likely to be
the winners (Nicholson 1955). By contrast, interference involves an indirect
action which hinders a competitor or denies it access to a resource. This usually
involves “fighting or some directly damaging behaviour” (Pontin, 1982, p. 4).
460 G.M.BRANCH
Territorial defence is an obvious example. Much of competition theory has been

built around the concept of exploitation; but another change of emphasis that is
detectable in the literature over the past 25 years has been the shift from
considering how species manage to coexist while exploiting a resource, to a
realization that interference plays a major rôle and that exclusion by interference
is probably more frequent than niche apportionment and seems a more potent
evolutionary force.
In this review I have focused on the literature from 1960 onwards,
partly because of the switches of emphasis mentioned above and partly because
early reviews (e.g. Miller, 1967) do justice to the literature prior to this period. In
particular, Jackson (1981) pays tribute to early workers and reminds us how
relevant their ideas are to the modern interpretation of ecological theory. Many
of the concepts which were advanced over 50 years ago foreshadow the ideas that
we espouse today. Other reviews with a general approach to the subject which I
have drawn upon include those of Ayala (1972), Harger (1972c), Schoener (1974,
1982), Yodzis (1978) who deals with the concept of competition for space,
Pontin (1982), and Begon & Mortimer (1982).
One can justifiably ask why there should be a review on competition in marine
organisms. The marine world has been curiously overlooked in most earlier
reviews on the subject of competition. An examination of general texts reveals a
preponderance of terrestrial examples, and in a random search of seven texts I
found that marine examples constituted only between 2 and 14% of the cases
covered in these texts. In addition to this the marine world has a much wider
range of habitats than on land—a range that covers different types of substratum,
different degrees of stability, different sources of food and different mechanisms
of feeding, so that one might expect that competition will act in different ways
and be of different importance in different kinds of habitats in the sea. In many
ways the marine environment is the ideal one in which to test ideas of
competition.
I hesitate to burgeon the literature with further definitions and have followed
Pontin’s (1982) sense of what competition is—when two individuals have a
negative effect on one another—but I must add to this one plea: the need to
identify the resource which is being competed for and to ensure that it really is
limiting. It might seem curious to make such an obvious plea and yet one still
finds in the literature examples where competition is treated so broadly that it is
quite unfair really to call it competition, and in which there is no attempt to
identify whether there is really a limiting resource. Secondly, the term “niche
apportionment” seems to carry with it the inevitable idea that the apportioning
has been undertaken by the species with the purpose of reducing competition and
has been driven by competition in order to allow coexistence. Not only is there
the danger of circularity in this suggestion but I will argue later that this
approach is not a useful one and, furthermore, that differences between species
which may well allow them to coexist do not necessarily have their origins in a
competitive reaction—either in the past or in the present. In this review I use the
term niche apportionment simply to mean differences between species which

may allow coexistence without any implication that competition has caused the
differences.
I have not attempted to make this a complete review, but rather to compare
different types of organisms and different kinds of habitats with a view to
exploring when competition is likely to be important and what rôle it really plays
under different circumstances. I have also felt that there is a need to bring
together and to compare and contrast ecological approaches with evolutionary
viewpoints. This particular approach I have found especially illuminating
because issues which are of vital local ecological significance are not necessarily
important when viewed from a long-term evolutionary perspective, nor are
extrapolations from small-scale observations to large-scale evolutionary
implications always possible.
This review is developed in four major sections. In the first section I outline
examples of intraspecific competition. It is a curious thing that intraspecific
competition has been paid much less attention than interspecific competition and
yet if we are to understand the latter we need to comprehend the rôle of intraspecific
competition as well. In this section I also discuss possible means of reducing
intraspecific competition.
The second section of the review outlines examples of interspecific
competition. I have divided these examples into various groups depending on the
type of habitat, the mechanism of feeding, and the nature of the resources
competed for. While these groups are somewhat arbitrary they do make the
examples more manageable and allow contrasting conclusions to be emphasized.
The groups that I have divided organisms into are: benthic carnivores, benthic
herbivores, sessile forms on hard substrata, primary producers, the fauna of soft
sediments, hermit crabs, zooplankton, and finally mobile forms such as bird and
fish. Following the outline of these examples I discuss processes that may allow
the coexistence of competitors.
The third section of the review draws together various approaches which
examine competition from a different perspective. Too often it is assumed that
competition is the driving force that explains patterns that are perceived in the
field, when it is possible that other ecological processes are actually at work.
When competition theory reigned supreme many of these alternative processes
were not even contemplated, but more recently they have assumed greater
importance in ecological theory.
The final section of the review deals with competition and its rôle in
evolution. I outline the importance of distinguishing the nature of the resource
that is competed for, the mechanism of competition and the characteristics of the
species involved—distinctions that are essential if we are to distinguish when
competition is likely to play a major rôle and what effect it may have on the
evolution of species. Also discussed in this section are the factors which may
influence genetic diversity in populations, and the possible effect of competition
on genetic diversity. Finally, I outline a new concept of how niche
462 G.M.BRANCH
apportionment may evolve—even if it can never rival the elegance of the

exposition of Dr Seuss (Giesel, 1955):
“And NUH is the letter I use to spell Nutches

Who live in small caves, known as Nitches, for hutches.
These Nutches have troubles, the biggest of which is
The fact that there are many more Nutches than Nitches.
Each Nutch in a Nitch knows that some other Nutch
Would like to move into his Nitch very much.
So each Nutch in a Nitch has to watch that small Nitch,
Or Nutches who haven’t got Nitches will snitch.”
INTRASPECIFIC COMPETITION
The consequences of intraspecific and interspecific competition are very different.
For one thing, individuals belonging to the same species cannot avoid contact
with one another all their lives if they are to reproduce. On the other hand,
members of different species can avoid one another, particularly if they compete,
and it is for this reason that Connell (1980) has suggested that the niche
divergence of different species is likely to be a rare event since competitors are
very seldom tightly linked to one another for long periods. When competition
involves the exploitation of a limited resource it will normally be most intense if
conspecifics (individuals of the same species) are involved, for they will
probably have nearly identical needs. Comparable competition between different
species will vary from being slight to intense depending on how much overlap
there is in the requirements of the two species and how deep their needs are for
the resource for which they compete. The situation is very different when
competition by interference is involved, for while conspecifics will be fairly
evenly matched, individuals of different species will probably be ill-matched and
one species will often dominate over the other.
There is ample circumstantial and experimental evidence of the potency of
intraspecific competition. Intense competition appears to occur in some natural
populations. For instance, the limpet Patella cochlear reaches very high densities
of up to 1700· m−2 and is adversely affected in a number of ways (Branch,
1975a). As density increases, maximum size declines, thus decreasing mean
body weight (Fig. 1A). Growth rates also decrease, while mortality rises.
Densities are usually so high that newly-settled juveniles fail to survive unless
they settle on the shells of adults, where they cannot be grazed. The higher the
density, the larger the proportion of juveniles situated on shells. Ultimately these
juveniles must descend from their host shells and become established on rocks,
and they are then extremely vulnerable because their shells do not fit the
substratum. The resulting high mortality is restricted largely to these pre-
reproductive juveniles. Density also affects the standing stock of P. cochlear
(Fig. 1A). Increased density obviously means an increase in the total biomass, but
Fig. 1.—A, maximum length and biomass of Patella cochlear relative to density; B, P.
cochlear, effect of density on the total female gonad output per year (′ ) and on the output
per unit of biomass (′ ); (after Branch, 1975a).
once the density reaches about 400 m−2, carrying capacity is reached and
intraspecific competition must then become especially intense if density rises any
higher. Another important consequence of competition at high densities is that
the reproductive output per individual animal decreases and, in addition, the total
reproductive output of the population per unit biomass also declines.
Reproductive output per m2 initially rises with density, but peaks at a density of
about 400· m−2 and then declines sharply (Fig. 1B).
Observations such as these can be rightly criticized (see Underwood, 1979) for
the fact that environmental variables may explain the patterns rather than
density. In this instance manipulative experiments have been undertaken to
modify the density of P. cochlear, and reveal that the patterns are indeed due to
intraspecific competition although about 10% of the variation in the results
appears to be due to variation in the intensity of wave action.
There are many other examples where limpets demonstrate intraspecific
competition (Frank, 1965; Sutherland, 1970; Stimson & Black, 1976; Black,
1977; Choat, 1977; Black, Fisher, Hill & McShane, 1979; Creese, 1980; and see
review by Branch, 1981). One observation made on the limpet Patelloida
alticostata is of particular interest, for it relates to the question of habitat range.
Intraspecific competition may lead to an expansion of the range of habitat the
species occupies, for when competition is intense it could pay individuals to
occupy marginal parts of the habitat where competition is less severe.
Conversely, interspecific competition usually results in a contraction of the
species to the most favourable portion of the range. Intra- and interspecific
competition often act simultaneously. For example, increased density leads to an
expansion of the intertidal range occupied by P. alticostata, while coexistence
with competing chitons results in a decrease in range (Fig. 2). Once again we
need to be cautious about accepting that data such as these really do reflect intra-
or interspecific competition for although this is the most likely explanation
experimental proof is lacking.
464 G.M.BRANCH
Fig. 2.—Number of shore levels occupied by the limpet Patelloida alticostata increases
as its own density rises, but is reduced by the presence of chitons which presumably
compete with Patelloida (R.Black, unpubl. data).
One limpet for which rigorous experiments have been undertaken is
Notoacmea petterdi which occurs in the extreme high shore (Creese, 1980). In
this animal density declines up the shore and with this decline growth rate
increases. By manipulating densities in different regions of the shore Creese was
able to show that an increase in growth rate high on the shore occurs in spite of
the fact that there is less production of food at that level. At any given density
growth rate is actually lower high on the shore and it is only because there are so
few limpets at that level that growth rate is faster there. Another limpet which
has been intensively studied is Cellana tramoserica. Manipulative experiments
have shown that an increase in density brings about a decrease in growth and an
increase in mortality and there is a negative correlation between the density of
recruiting juveniles and that of adults (Underwood, 1978; Branch & Branch,
1980a; Underwood, Denley & Moran, 1983).
Experimental alteration of population density has very clearly shown that
increasing the density of the gastropod Nerita atramentosa (Fig. 3) sharply
reduces the growth rate of juveniles, increases the mortality of adults, and
decreases the mean tissue weight of both adult and juveniles (Underwood, 1976).
Both adults and juveniles are affected in the same way by increases of either
adult or juvenile numbers, implying very similar requirements by the two age
groups. Under these circumstances the population will tend to be self-regulating,
for high density will lower growth rates and increase mortality until a lower density
is re-established. Comparable experimental manipulations of the littorinid
Bembicium auratum (Branch & Branch, 1980b) show that increased density
reduces growth, body weight, survival of juveniles, and also suppresses the
levels of micro-algal food present on the surface of the mud. Four other
littorinids have been similarly investigated and in each case adverse intraspecific
effects were detectable although mortality remained unaffected by the density of
Fig. 3.—Influence of experimental density on growth, mortality and tissue weight of

Nerita atramentosa: A, growth of juveniles; when kept with other juveniles or with
adults; B, mortality of adults when kept with other adults or with juveniles; C, tissue
weight of both adults and juveniles; (after Underwood, 1976).
the animals (Behrens, 1971; Striven & Kuenzler, 1979; Branch & Branch, 1981).
Sea urchins also suffer from intraspecific competition as can be demonstrated by
changing their density. Ebert (1977) and Schroeter (1978) have both shown this
for Strongylocentrotus species, and Mann (1977) and Lang & Mann (1976) have
inferred that intraspecific competition is responsible for a decrease in the growth
rate and gonad weight of urchins following the collapse of kelp beds.
Competition for food is seen in animals even at opposite ends of the size
spectrum. Foraminifera decrease in size, rate of cell division, and rate of
population growth with increased crowding (Muller, 1975), and various whales
grow faster and mature earlier following culling that has reduced most
populations (May et al., 1979), although in the latter case it is difficult to
disentangle the effects of intra- versus interspecific competition since
populations of different species have been reduced simultaneously.
Turning to organisms in which competition for space or shelter is involved,
intense and aggressive interference competition may often occur between
individuals. The occupation of space may provide a protection against predators,
a physical space where feeding can take place, or an optimal position for
reproduction—and of course the same space may provide for more than one of
466 G.M.BRANCH
these functions simultaneously. As an example, Grünbaum, Bergman, Abbott &

Ogden (1978) have shown that tropical urchins aggressively defend the holes in
which they live against intrusion by conspecifics. In this case it seems as if the
holes provide a shelter against predators, but at the same time floating algae
accumulate within these depressions and the rate of accumulation of algal debris
is proportional to currents, and so the shelters also serve the function of
providing a food source (Russo, 1977). This example is an interesting one
because predation may actually intensify competition rather than alleviating it.
Because predation is intense in the tropics and because it involves forms such as
fast-moving fish and crabs which are active year-round (Menge & Lubchenco,
1981) there will be a premium on crevices and holes in which prey species can
shelter so that competition for such sites may be intense. Other animals which
aggressively defend a shelter are hermit crabs (Hazlett, 1968, 1981) mantis
shrimps (Caldwell & Dingle, 1979), and alphaeid shrimps (Schein, 1975).
All these cases clearly involve aggressive interference, but competition for
shelters can be by way of exploitation as, for example, in Littorina rudis. Emson
& Faller-Fritsch (1976) drilled holes in intertidal rocks to provide artificial
crevices for L. rudis and this increased the population by up to 800% (Fig. 4).
The number of small Littorina is usually related to the number of empty barnacle
shells which provide shelter. When the littorines become too large to occupy
these shells and have to compete for limited crevices in the rocks, heavy
mortality occurs. The eightfold increase in density which followed the provision
of artificial crevices had no effect on the body-weight or reproductive output of
the individual animals, suggesting that surplus food was actually available on the
rocks and that only a shortage of crevices limited the population.
Instances in which competition over a source of food involves aggressive
defence of a patch include the amphipod Erichthonius braziliensis (Connell,
1963) and the territorial limpets Lottia gigantea (Stimson, 1970, 1973) and
Patella longicosta and P. tabularis (Branch, 1975a, b).
In some cases territorial aggression serves largely to secure a reproductive
advantage. For example, in scarid fishes only terminal-phase mature males hold
tightly defined and rigorously defended territories, into which females are
attracted to mate (Barlow, 1975). Territorial contest is well known in the fiddler
crabs, Uca spp. (see Crane, 1975, for a review). Fights between sexually mature
males of U. pugnax and U. pugilator are aimed mainly at holding space in the
upper shore where the females most often mate with the males (Hyatt & Salmon,
1978; see also p. 449). Damselfish are renowned for their belligerent defence of
their territories (see Sale, 1980, for a review). Anemone fish, Amphiprion spp.,
not only defend their anemones against intrusion but within the small groups of
fishes associated with each anemone there is a social control of sexuality. Each
group consists of a dominant female (the largest individual), a single functional
male, and a number of sub-adults which are sexually immature. Amphiprion spp.
are protandrous hermaphrodites, and it is the social dominance of the female
over the male that prevents his transformation into a female. Similarly, the male
Fig. 4.—Abundance of Littorina rudis in control areas and in areas where artificial
crevices were provided (after Emson & Faller-Fritsch, 1976).
dominates the sub-adults and prevents them from achieving a sexual state (Fricke
& Fricke, 1977). In this case territorially is linked with social dominance,
regulating the numbers of animals associated with an anemone and their
sexuality. The idea of social control of sex change in fish was first demonstrated
by Fishelson (1970), for the protogynous fish Anthias squamipinnis.
A very different form of intraspecific competition occurs in the clam Tridacna
crocea, which burrows into coral heads (Hamner, 1978). The larvae aggregate
when they settle (which would seem maladaptive in the light of subsequent
competition for space), but orientate their bodies so that their posterior ends face
away from adjacent animals. During subsequent growth the clams can re-align
their burrows to reduce contact with other animals. In combination with the larval
orientation, this leads to a regular or random pattern of spacing in adults. Adults
also reduce larval settling in their immediate vicinity by covering part of the
substratum with the mantle. In spite of all these adaptations, intraspecific
competition is intense, and up to 40% mortality may result. T. crocea lives an
estimated 80 years, but there is a heavy mortality of 1-to 3-year old animals that
suffer from competition, being burrowed into, having their shells distorted or
eroded, or being overshaded by larger clams. Hamner points out that these clams
act like plants in terms of intraspecific competition, requiring physical space
where they can obtain sufficient light for the photosynthesis of their
zooxanthellae. Corals may face a similar problem, and Sheppard (1980) has
described how deeper stands of corals create an almost unbroken canopy,
beneath which lie smaller colonies. The bimodal size distribution of corals in
these stands may be because the large colonies which form the canopy suppress
the development of smaller individuals that lie in the understorey and only once
a gap appears in the canopy do these smaller colonies grow rapidly.
468 G.M.BRANCH
Records of intraspecific competition in marine algae yield curiously

contrasting results. Harvesting of kelp is often said to enhance the growth of
young plants growing below the canopy. Black (1974) has, for example, shown
that as the density of large Egregia laevigata increases, so the recruitment,
growth rate and survival of juveniles decrease. On the other hand, Schiel & Choat
(1980) had difficulty in finding any adverse effect of density in Ecklonia radiata
and Sargassum sinclairii. Unlike terrestrial plants, in which the 3/2 thinning law
applies (log weight is related to log density with a slope of −1·5) measurements
of algal length, biomass, and the weight of reproductive tissues revealed no sign
of thinning in denser stands and, in fact, growth was highest in dense stands. The
survival of germlings was constant at four different densities in Sargassum but
admittedly slightly depressed in Ecklonia. Schiel & Choat suggest that groups of
plants are buffered against wave action and that algae are not subjected to a
higher herbivore load when they occur in dense stands (in contrast to terrestrial
plants which are attacked proportionately more intensely as their density rises,
mainly by insects). There are, however, two additional factors that may explain
this result. First, light is diffusely scattered in the subtidal zone and canopy
plants are in continual movement, so that shading of understorey plants may be
less critical under these conditions than it is on land or in the intertidal zone.
Secondly, land plants compete for nutrients that are localized in the soil, while in
the sea nutrients are dispersed in the water and are unlikely to be locally depleted
by algae—at least in the subtidal zone where water movement continually
replenishes the nutrient. This is not to imply that nutrients are not limiting at
times but that local depletion is unlikely to be significant. If algal growth is
limited by nutrient levels, then density may have little impact on the growth of
the plants. Conversely, in situations where light is limiting, over-shading may
have an important inhibiting effect. This dichotomy may help to explain the
divergent results of Black (1974) and Schiel & Choat (1980).
Before leaving these examples of intraspecific competition, it is worth
recalling that an increase of density is not necessarily associated with adverse
competition, but may sometimes be of benefit. For instance, the breeding success
of the common guillemot (Uria aalge) increases with density (Birkhead, 1977),
the escape responses of fish may be more effective in dense shoals (Major,
1978), and the feeding of birds that capture prey by feel may be enhanced at high
densities (e.g. Goss-Custard, 1976).
MECHANISMS REDUCING INTRASPECIFIC

COMPETITION
Any reduction of intraspecific competition will have obvious value. The means
by which competition is reduced will depend on the type of resource that is
limiting, the mechanism of competition, and the nature of the species. Species
with mobile adults can move from an overcrowded habitat while sessile species
depend far more on the behaviour of their larvae at settling.
Fig. 5.—Distances between cyprids of Balanus balanoides and three species of the
nearest previously settled barnacles: the cyprids spaced themselves out from their own
species but readily settle alongside other species; (after Knight-Jones & Moyse, 1961).
Larval settling patterns

Many larvae are gregarious, settling in the vicinity of adults. In sessile species it
is essential that the larvae space out so that there is room for subsequent growth
(see Knight-Jones & Moyse, 1961, for a review). For example, Spirorbis
borealis larvae crawl in irregular circles before metamorphosing, swimming
away if they contact an irregular projection or one of their own species (Wisely,
1960). This behaviour ensures sufficient space for growth to adult size. Cyprids
of Balanus balanoides (Fig. 5) space themselves away from adults of their own
species when settling but react quite differently to other species, crowding
against them (Crisp, 1961; Knight-Jones & Moyse, 1961; Moyse & Hui, 1981).
Despite this dispersion of larvae, intense intraspecific competition may develop
in barnacle colonies, and Connell (1961b) has shown that crushing, undercutting
and overgrowth may cause up to 75% mortality in crowded barnacle beds.
Larval spacing is not universal in sessile species, for bryozoan larvae all
aggregate irrespective of the density of the settling larvae (Harvey, Ryland &
Hayward, 1976). This may be because bryozoan colonies have a labile and
indeterminate growth and stop growing or redirect their growth if they contact a
colony of their own species. Furthermore, individual zooids are the units of
sexual reproduction so that the size of the colony is not related to the ability of
the individual to reproduce. These factors may mean that avoidance of
intraspecific crowding is not critical in Bryozoa. Seed & O’Connor (1981) have,
however, suggested that this argument is shortsighted, for if space is short it willl
still be profitable for bryozoans to space themselves at settling.
The larvae of the serpulid polychaetes Spirorbis corallinae and S.
pagenstecheri and the bryozoan Scrupocellaria reptans regularly settle on
Laminaria fronds. Stebbing (1972; see also Stebbing, 1973a, b; and a review by
470 G.M.BRANCH
Seed & O’Connor, 1981) showed a striking preference by all three species for
the youngest (basal) parts of the fronds (Fig. 6). This preference has two
advantages. First, fewer other epiphytes will have settled on the youngest part of
the frond so that competition for space is reduced. Secondly, Laminaria blades
are continually growing from the base and being eroded away distally, so that
settling near the base ensures a substratum that is not on the point of
disintegrating. Quite how settling larvae determine the age of different parts of
the plant is unknown, but bacterial films that accumulate on older portions may
act as a cue (Ryland, 1976; Seed & O’Connor, 1981). In addition to selecting the
youngest parts of the frond, some Spirorbis spp. preferentially select plants that
are not already crowded with adults (O’Connor & Lamont, 1978).
Stimson (1974) has shown that the coral heads of Pocillopora meandrina are
regularly spaced out. Furthermore the sum of the diameters of adjacent heads is
correlated with the distance between these neighbours (Fig. 7): in other words,
large neighbours have larger distances between them. This pattern is very
suggestive of a competitive interaction, either the adults or the settling planulae
responding to existing coral heads. The most likely explanation for this pattern is
that the planulae select settling sites which receive maximum light, hence
spacing themselves away from the shadows of established coral heads and
consequently minimizing competition with existing corals. Avoidance of
shading may be critical in hermatypic corals which require adequate light for
their symbiotic zooxanthellae. Some corals are gregarious in their settling
patterns and do not space out. Favia fragrum and Agaricia agaricites are two
examples (Lewis, 1974). In the case of the coral Mantipora berryi, larvae of the
coral settle preferentially in holes burrowed by the bivalve Lithophaga curta in
dead Mantipora (Highsmith, 1980). It seems likely that Lithophaga and
Mantipora have co-evolved a symbiotic association. Lithophaga settles
predominantly on live Mantipora, and creates burrows which, after the death of
the Mantipora (which is unrelated to the burrowing activity of the bivalve), are
colonized by larvae of Mantipora.
These examples illustrate that in some species spacing mechanisms in settling
larvae can help reduce the adverse effects of crowding. The benefits of
dispersion, however, must be balanced against the need to aggregate for
reproduction. Sessile forms must be sufficiently gregarious to maximize the
chances of reproduction, and it is perhaps for this reason that dispersion is not
more frequently developed in the larvae of sessile species.
Dispersal of adults
Mobile animals can simply move from one area to another when food supplies
are exhausted or overcrowding occurs. For instance, Ebert (1977) adjusted the
densities of the urchins Strongylocentrotus purpuratus and S. franciscanus in the
field, either separately or together. At very high densities, algal food was
eliminated and movement of the urchins increased, leading to dispersal. Dispersal
Fig. 6.—Larval settlement of the ascidian Scrupocellaria (A) and the polychaete Spirorbis
(B) on discs cut from different regions of the stipe of Laminaria: the youngest (basal)
parts of the frond attract most larvae; (after Stebbing, 1972).
was faster in single-species groups than in mixed groups, implying that
intraspecific competition was greater than interspecific competition. Dispersal
has also been demonstrated in other echinoids (Khamala, 1971) and may
sometimes involve aggressive defence of shelter-holes (Grünbaum et al., 1978).
It also seems that echinoids may compensate for crowding by increasing the size
of Aristotle’s lantern, an adaptation exemplified in Echinometra mathaei, which
presumably allows the species to feed more efficiently in high-density
populations which are short of food (see Black, Johnson & Trendall, 1982, and
references therein).
While adult echinoids are dispersive at high densities, in at least two instances
juvenile urchins are found aggregated under adults. Juveniles of
Strongylocentrotus franciscanus obtain shelter under large individuals and
probably benefit by feeding on drifting algae which are captured by the adults
(Tegner & Dayton, 1977). Larvae of Dendraster excentricus selectively
metamorphose where adults occur, and their survival is greatest in the vicinity of
the adults because the latter’s burrowing activities reduce the number of micro-
predators such as tanaids (Highsmith, 1982).
472 G.M.BRANCH
Fig. 7.—The coral Pocillopora meandrina: correlation between sum of diameters of

nearest neighbours and the distance between the centres of these neighbours (Stimson,
1974).
Ophiuroids (Fishelson, 1971; Wilson, Holme & Barrett, 1977) and asteroids
(Mauzey, Birkeland & Dayton, 1968; Mayo & Mackie, 1976; Birkeland, 1977;
Dayton, Rosenthal, Mahen & Antezana, 1977; Sloan, 1979a; reviewed by Sloan,
1980) show avoidance behaviour when they contact members of their own
species, but at least in the case of the asteroids, since all the species are predatory
and may be cannibalistic, it is likely that the avoidance is a means of preventing
predation rather than achieving dispersal to avoid intraspecific competition.
The crabs Carcinus maenas (Vannini, 1981) and Pachygrapsus crassipes
(Bovbjerg, 1960) disperse at high densities. The amphipod Calliopiella
michaelseni, which is commensal under various Patella spp. (Branch, 1975c)
feeds on the faeces of the limpet and thus has a restricted habitat and a limited
food supply. Almost invariably the amphipods are limited to a male and female
pair per limpet (except when juveniles have recently been released from the
female and have not yet dispersed). The mechanism regulating the number of
amphipods per limpet is not known (although territorial defence is probable) but
the effect ensures dispersal of juveniles and avoids over-exploitation of a limited
food supply. Another commensal animal, the polychaete Arctonoe pulchra which
lives beneath limpets and holothurians, becomes progressively aggressive as it
grows, and this results in a similar dispersal from the host and avoids
overcrowding (Dimock, 1971).
Francis (1973, 1976) has shown that the anemone Anthopleura elegantissima
occurs in colonies of genetically identical individuals, which react aggressively
to other clones of the same species. Interactions occur mainly at the edge of
colonies where the individuals have more acrorhagi (spheres lying below the
tentacles which are used in aggression) but a slower growth rate and lower
reproductive output than individuals in the centre of the colony. Aggression
results in a spacing of colonies which is probably important in an animal such as
Anthopleura which has a very long life and low mortality, indeterminate growth,
and both sexual and asexual reproduction. Intraspecific and even interclonal
competition for space may thus be acute.
Similar aggressive interactions have subsequently been recorded for a number
of anemones. Actinia equina uses its acrorhagi to rake across the surface of
adjacent anemones and may inflict formidable wounds (Ottaway, 1978). In
Phymactis clematis and in Actinia equina there are size-dependent differences in
the threshold releasing aggression, and larger animals are more aggressive and
invariably win contests against smaller individuals, with the result that smaller
animals disperse away from large animals (Brace & Pavey, 1978; Brace, 1981).
Several other anemones form fighting tentacles (sometimes called “catch
tentacles”) when in contact with other anemones, which are larger than normal
tentacles and bear nematocysts used in aggressive encounters (holotrichs and
atrichs) in place of the normal feeding nematocysts (Williams, 1975). In the case
of Metridium senile these are used in contests against anemones of either the same
or different species, but never against clone-mates. Attacks lead to necrosis of
the tissues and even death (Purcell, 1977).
In most of these cases dispersal is the result of aggressive interactions and
Bovbjerg (1964) has proposed that density-dependent dispersal is typical of
aggressive or territorial animals. While dispersal probably is more obvious in
active aggressive species, non-aggressive animals may also disperse, usually in
response to food levels rather than to interactions between organisms or to
density per se.
Mackay & Underwood (1977) have interpreted the function of homing in
limpets as a mechanism for regulating population density. In Cellana
tramoserica some individuals return to a home site but a variable percentage of
the population moves at random. Proportionately more animals have home sites
in areas of low density, and this proportion can be decreased by experimentally
increasing the density. Fewer limpets will move into or remain in areas where
microalgal food has been experimentally removed. This suggests that homing
allows regulation of density in relation to the availability of food, reducing
intraspecific competition. This example is a particularly valuable one because it
is one of the few in which authors have been able to prove that dispersal is
primarily in response to a reduction of food at higher densities. The amount of
movement in Littorina unifasciata is inversely proportional to the level of food
(Branch & Branch, 1981) and this, too, will lead to dispersal from areas where
food is limited.
The oyster drill, Urosalpinx cinerea, has a complex pattern of dispersal and
aggregation which improves the chances of feeding. Specimens are attracted to
water which has passed over satiated individuals, but are repelled from water
coming from starved animals (Pratt, 1976). There is a twist to this tale, for
Urosalpinx is also cannibalistic and has the ability to distinguish the size of other
individuals by distance chemoreception. When larger animals detect smaller
ones, they attempt to capture them, leading to cannibalism or to copulation
474 G.M.BRANCH
depending on the sex of the individual. Conversely, detection of a larger animal

results in a rapid escape by the smaller individual (Snyder & Snyder, 1971).
Limited dispersal of sessile organisms is possible in terms of the direction they
grow. Overgrowth of conspecific bryozoans is usually prevented by cessation of
growth at the point of contact between two colonies and a redirection of growth
(Seed & O’Connor, 1981). In the compound ascidian Botryllus schlosseri
colonies may fuse on contact or they may repel one another. Fusion only takes
place between genetically related colonies, and recognition appears to depend on
the two colonies sharing at least one allelle at a particular locus (Sabbadin, 1978).
Several colonial species which are epibiotic on algae grow towards the
youngest part of the plant, where there will be at least competition from
established colonies. Examples include bryozoans (Ryland & Stebbing, 1971;
Ryland, 1976) and hydroids (Katô, Nakamura, Hirai & Kakinuma, 1961). Norton
(1973) has analysed the growth of Membranipora and shown that while it
normally grows towards the proximal parts of the fronds (and thus towards the
youngest parts) it also grows proximally on the stipe and thus towards old tissues.
Norton suggests that growth is rheotactic, leading to growth in a proximal
direction, and this must cast doubts on whether the growth pattern really is an
adaptation minimizing competition for space, or whether the directed growth
serves some other function.
Dispersal along an environmental gradient

If juveniles settle in a particular habitat and then progressive migration occurs
away from this site as the animals age, there is always the possibility that
intraspecific competition can be reduced by lessening overlap between different
age groups. Figure 8 summarizes the relationship between body size and
intertidal zonation for eight gastropods, showing that in each case the juveniles
occur above or below the adult population. Other examples include the
gastropods Littorina unifasciata (Branch & Branch, 1981), Bembicium auratum
(Branch & Branch, 1980b), Conus spp. (Leviten & Kohn, 1980), the mole crab
Hippa pacifica (Haley, 1982), and a large number of fish (reviewed by Helfman,
1978). It must be stressed that such distribution patterns do not necessarily
reduce competition, nor can we assume that they are caused by it. In the case of
Patella granularis (Fig. 8B) manipulations of density in the field and
measurements of growth rates in experimental and control populations
(G.M.Branch, P.Britz & P.Hockey, unpubl. data) show that upward migration of
larger limpets takes them into a zone where food levels are reduced but where
they grow faster because of the lower densities of grazers. On the other hand, the
size gradients in Conus spp. appear to be the result of catastrophic mortalities of
smaller individuals in the high shore, following heavy rains (Leviten & Kohn,
1980), with no hint that the resulting size gradient either alleviates or is caused
by intraspecific competition.
Fig. 8.—Relationship between tidal height and shell length in various gastropods: A,
Olivella biplicata (after Edwards, 1969); B, Patella granularis (after Branch, 1975b); C,
Acmaea digitalis (after Breen, 1972); D, Littorina littorea (after Gendron, 1977); E, Thais
lamellosa, T. emarginata; F, T. canaliculata, Searlesia disa (after Bertness, 1977).
Vermeij (1972) has reviewed the occurrence of size gradients in gastropods

and suggests that their main advantage is to place pre-reproductives where
mortality is lowest. Thus high-shore species which are presumed to suffer
increased stress higher on the shore should increase in size up the shore, as is the
case in Patella granularis and P. granatina (Branch, 1975b), and Acmaea
digitalis (Breen, 1972). On the other hand, low and mid-shore species probably
suffer more from biotic factors which are more intense low on the shore, and the
476 G.M.BRANCH
Fig. 9.—Model of the behavioural control of the intertidal distribution of Thais spp: the
interaction of photokinesis and geotaxis (which may change with light intensity) will tend
to separate the size groups and species (after Bertness, 1977).
small pre-reproductives should thus occur higher on the shore. This does occur in
a number of species including Searlesia disa, Thais spp. (Bertness, 1977), Tegula
funebralis (Paine, 1969), and Littorina littorea (Gendron, 1977). There are,
however, exceptions such as L. africana knysnaensis (McQuaid, 1981) and
Oxystele variegata (McQuaid, 1982) which are discussed below in terms of
mechanisms controlling their zonation.
Most of these size gradients are maintained by migration up or down the shore
and the cues controlling the movement have been analysed for some species.
Olivella biplicata responds differentially to light: small animals are more active
in bright conditions and this photokinesis moves them into deeper water where
they become less active in the dimmer light. Large animals have the reverse
response and hence tend to accumulate higher up on the shore (Edwards, 1959).
Littorina littorea also migrates seasonally up and down the shore, resulting in
size gradients. When dislocated up or down the shore it migrates in the direction
of the preferred shore level, and Gendron (1977) has suggested that this species
uses wave movement as its cue for orientation. Considering the turbulence of the
intertidal zone it is questionable whether the direction of wave movement is a
useful cue.
Size gradients in Thais emarginata and T. lamellosa may be established by
geotaxis and photokinesis according to Bertness (1977). Small T. emarginata
occur highest on the shore because they are most active in the dark, and hence
move most when covered by water (which reduces light intensity). In addition,
they are geonegative under both light and dark conditions (Fig. 9). Large T.
emarginata predominate in the mid-shore. They are only negatively geotactic in
the dark so that as they move into the higher regions of the shore they are less
often covered by water (and hence exposed to brighter light for longer periods)
and consequently lose their negative geotaxis and tend to maintain a fixed
position on the shore. Small T. lamellosa occur in the mid-shore (where eggs are
deposited and hatch). They remain there because they are alternately geonegative
(in the dark) and geopositive (in the light). Larger T. lamellosa are more active in
the light, hence tending to accumulate lower on the shore. This downward
movement is encouraged by a positive geotaxis in the light (Fig. 9). It may,
however, be unnecessary to invoke this complex mechanism, for size gradients in
the thaids may be a direct response to the availability of suitable prey (see below,
p. 553).
Littorina africana knysnaensis is an extreme high-shore inhabitant on South
African shores and displays a size gradient the reverse of that predicted by
Vermeij (1972), juveniles occurring highest on the shore, adults in the zone
below. McQuaid (1981) has shown that this pattern is restored very soon after
animals are transplanted up or down the shore. If the animals are tethered in
different zones, juveniles lose weight in the lower zone and larger animals in the
highest zone.
Measurements show that food is more abundant in the lower zone, but because
the small animals lack the tenacity to tolerate the higher wave action experienced
there, they are confined to the top of the shore. As the littorinids increase in size
they migrate downshore to the richer feeding grounds. In this instance there seems
a secure case for reduced intraspecific competition associated with the
downshore migration.
Quite a different cause can be ascribed to the size gradients in the gastropod
Oxystele variegata, which is restricted to the low shore in early life because of the
intolerance of juveniles to desiccation. As the winkles increase in size they
migrate upshore. Individuals that are experimentally transplanted up or
downshore very quickly migrate back to the zone from which they were taken,
covering up to 30 m in a single tidal cycle to do so (McQuaid, 1982; see also
Byers & Mitton, 1981, regarding comparable movements in Tegula funebralis).
Initially it was assumed that up-shore migration in Oxystele variegata reduced
intraspecific competition. Underwood (1979) has previously hypothesized that
zonation patterns may be explained by a negative geotaxis which is suspended
when the animal reaches an area of appropriate food. But when adult O.
variegata were caged in the high and low shore they gained weight in the low
shore, where the productivity of their food was also shown to be greatest. On the
other hand, the survival of tethered adults was far higher in the high shore,
apparently because of more intense predation by the whelks, Burnupena spp., in
the low shore. It seems that movement upshore is thus primarily a means of
avoiding predation. This is an important example, for it illustrates the need to
avoid jumping to the conclusion that dispersal along an environmental gradient is
driven by the need to reduce intraspecific competition.
In the case of Hippa pacifica, small animals occur in the upper half of wave-
washed shores (Haley, 1982). This may not be so much a means of avoiding
competition but rather a consequence of competitive dominance of large animals
over smaller individuals in the lower shore, since large mole-crabs are capable of
excluding their small counterparts from food (which comprises animal debris
that is washed up by the waves). In laboratory experiments Haley showed that
478 G.M.BRANCH
small animals accumulate in the upper half of sloped surfaces, but that this
response is abolished when water that has contained large females is run over the
surface—presumably a dispersive effect to avoid contact with the competitively
superior adults.
Dispersion patterns
Species which have restricted habitats and limited powers of dispersal cannot
simply migrate away from areas in which food or space are in short supply. They
can, however, develop dispersion patterns which maximize distances between
individuals. Examples in which settling larvae establish such patterns have
already been discussed, but adults of more mobile species may achieve the same
effect. For example, Patella cochlear is restricted to a narrow band at low tide. As
mentioned above, juveniles are mainly confined to the shells of adults because of
grazing pressure, and as these juveniles can feed on the encrusting algae growing
on their host shell, this two-tiered arrangement reduces competition between
adults and juveniles. Adult P. cochlear feed by rotating on their scars so that
their feeding range is confined to a narrow band around each limpet, in which
grow ephemeral red algae which seem to form the main part of the diet of P.
cochlear. These algae are dependent on the limpets, soon disappearing if the
limpets are removed. P. cochlear territorially defends its feeding area and in
consequence spaces out in a remarkably regular pattern, minimizing contact
between the individuals. A minimum distance is always maintained between
individuals but decreases at higher densities. The regularity of this pattern
ensures minimum contact between individuals (Branch, 1975a, b). P. longicosta
is another territorial limpet, defending its “gardens” of Ralfsia expansa against
other limpets, and its pattern of dispersion is random in sparse populations but
becomes progressively more regular in dense populations, once again
minimizing contact between individuals (Fig. 10) (Branch, 1975a, b).
Terebellid polychaetes also achieve a regular dispersion on mud flats, thus
reducing interference between the feeding tentacles of adjacent individuals
(Anderson & Kendziorek, 1982) but the mechanism achieving this pattern is
uncertain. In the case of the spionid polychaete, Pseudopolydora
paucibranchiata, a remarkably regular dispersion is apparent in the arrangement
of the tubes of the worms which project from the surface of sand flats. This
dispersion is brought about in two ways. First, during larval settling cannibalism
occurs on the larvae and ensures that they do not settle within a certain minimum
distance from established worms. The spacing is then enhanced by interreactions
between adults, involving palp fighting and biting—the first recorded instance of
territoriality in a spionid polychaete (L.A.Levin, 1981). The need for dispersion
in this polychaete revolves around its method of feeding, for it is a depositfeeder
which uses its palps to scour the surface of the sediment, collecting particles both
for feeding and for tube construction. The tube-building amphipod Erichthonius
braziliensis has regularly dispersed tubes, partly because newly settled larvae
Fig. 10.—Relationship between dispersion coefficient (R) and density of Patella

longicosta (after Branch, 1975b).
require a minimum space in which to establish their tubes and partly because of
subsequent territorial fighting which maintains a minimum feeding area around
each animal (Connell, 1963).
Animals which are aggressively territorial and occur in crowded colonies are
very likely to show dispersion. An obvious example is the fiddler crab Uca.
Connell (1963) has shown that the holes of U. pugilator are regularly spaced out.
Zucker (1977) has further analysed the patterns of dispersion in Uca and shown
that sexually mature displaying males are more distinctly spaced out and defend
larger territories than females or males which are only involved in feeding.
Dominant males display to adjacent individuals, and if their holes are too close
they will pull out the owners and fill in the P holes. Feeding males which are not
sexually active never do this. Dominant sexual males are most likely to act
aggressively to other males, but although they are more tolerant of females, they
will also attack them if their holes are too close. The actively courting males
occur mainly in the high shore (Hyatt, 1977), despite the fact that this zone has
less food and so males must leave their holes to feed in the low shore. Hyatt
suggests the crabs operate on a lek system, for the females show a strong
preference for males that occur in the high shore. It seems clear that the
aggressive defence of space around each male’s hole (and hence the dispersion
of the crabs) is maintained more to achieve sexual success than to maintain a
food supply.
Highly mobile organisms seldom show regular spatial patterns, but some
consideration has been given to why mobile animals should (or should not) feed
480 G.M.BRANCH
in aggregations. Amongst birds that feed in the intertidal zone, Goss-Custard

(1976) has suggested that those which feed by sight should be dispersed, since in
such birds the efficiency of feeding may decline as density increases—due to the
interference between the birds, distraction, and disturbance of prey. Birds feeding
in flocks are more likely to feed by feel, probing the mud to detect prey. In this
case group-feeding may enhance the ability to detect local concentrations of prey.
Goss-Custard was able to observe redshank (Tringa totanus) feeding under
various conditions and showed that the success rate of feeding declined with
density when the birds were feeding by sight, and that when they were forced by
environmental circumstances to feed in tightly packed groups, that their diet
changed and they sought mainly prey that could be detected by feel.
Predatory fish are more successful when attacking schooling fish if they
operate in schools themselves, while isolated individuals have a higher success
rate when pursuing individual fish. Major (1978) has experimentally shown this
to be the case for the jack (Caranx ignobilis) which is a facultative schooling
predator, and suggests that prey species have evolved schooling as a means of
reducing predation, while schooling of predators has been co-evolved to counter
this.
Thus, the degree of dispersion different species develop is a function of several
factors, including their mobility, mode of feeding and nature of food, the degree
of territoriality, and the functional need for space. It is most clearly seen only in
territorial species which defend a fixed space.
A voidance or ritualization of combat

For species that are highly aggressive, particularly those which have the ability to
inflict damage on their opponent, ritualization is an important means of avoiding
escalation of intraspecific contests to the point where one of the contestants is
damaged or killed. Ritual displays are clearly seen in mantis shrimps which
ferociously defend their burrows against other intruding mantis shrimps, and
which have the potential to inflict lethal wounds. Caldwell & Dingle (1979) have
shown that in Gonodactylus viridis contests are usually won by the larger of a
pair of individuals. During contests, the larger animal is more likely to attack, the
smaller to avoid contact or retreat. Small animals indulge in extensive ‘meral
displays’, spreading the raptorial maxillipeds, antennules and antennal scales to
increase their apparent size. When two mantis shrimps meet while out in
the open, a contest may ensue, but it is always very mild; when defence of the
burrow, however, is involved, aggression is often escalated and the lethal dactyl
spine used to stab the opponent, with loss of appendages or even death being
possible. Caldwell (1979) describes how G. festai begins contests with meral
displays, which may be enough to repel an intruder, but as the contest gets more
aggressive, it strikes out and produces a clicking noise (by striking the side of the
cavity) and these actions serve as a second level of ritualized combat before all-
out physical battle begins. Individuals which are ejected from burrows
subsequently react differently to other burrows depending on whether they are

inhabited or not. Empty cavities are readily entered; cavities which contain water
in which another shrimp has been kept are entered more cautiously in an
exploratory manner; while if the burrow contains water that has housed the
victor of the previous encounter, it is avoided altogether. Thus, the behaviour of
the shrimp is mediated by chemical recognition of water that has housed other
shrimps— not merely on the basis of presence or absence, but allowing
individual recognition of the animal and whether it was a recent victor or not.
Carcinus maenas, an aggressive species in which dispersal is related to
density, reduces its level of combat when kept at high densities, and Vannini
(1981) has shown this reduction of aggression is caused by water-borne
nitrogenous wastes from the crabs. Snapper shrimps, Alphaeus spp., use their
large chela during agonistic defence of their burrows. The snapping of the chela
directs a jet of water, travelling at about 4 m·s−1 and accompanied by a loud click,
at intruders. The size of the chela is proportional to the sound intensity of the
click, so that contestants have a clue as to their relative sizes, and contests
between animals of very different sizes are avoided (Schein, 1975). Snapper
shrimps are solitary except during reproduction when pairs of animals of
opposite sexes share a burrow. Reproductive pairs are always similar in size,
leading Schein to suggest that there is an ‘agonistic balance’ between the two
which can be gauged by the sound intensity and possibly also the intensity of the
jet produced by chelar clicks. Since males have larger chelae than females
(relative to their body size) the sexual pairs nearly always consist of animals with
similar size chelae but in which the body size of the female is larger than that of
the male. Thus, the male secures a female which is larger than him and capable of
producing more offspring than a small female.
Frequent battles occur between fiddler crabs for the possession of burrows
(see Crane, 1975, for a review). Hyatt & Salmon (1978) analysed the incidence
and intensity of intraspecific contests in two species—Uca pugnax and U.
pugilator. U. pugnax lives in firm mud, which makes the burrows difficult to
construct but very stable and long-lived. In most colonies there is an excess of
burrows, so that the loss of a burrow to an intruder, or the lack of success in
attempts to win a burrow from a resident, are not critical. Consequently, in this
species fights are brief, of low intensity, and involve fewer acts per fight.
Animals which are wandering around seeking a hole are indiscriminate in
selecting an opponent to fight for a burrow. In U. pugilator the situation is
different, for this species lives in sand, where burrows collapse easily and need
continual (but low cost) maintenance. There are no surplus burrows in the colony
since they collapse quickly if not maintained. As a result, the burrow is a more
valuable commodity in this species than in U. pugnax, and U. pugilator remains
close to its burrow. Wandering individuals which have lost their burrows attack
residents more persistently and intensely, fight for longer periods, and are more
likely to be very selective in their choice of opponents, never choosing to fight a
larger animal (which can be expected to win the fight) and usually choosing an
482 G.M.BRANCH
animal which is only slightly smaller than themselves so that if they do

successfully eject the resident they will scarcely need to modify the burrow to
allow occupation.
There are occasions when ritualization of contests involves different species
which share a common shelter. For example, Lassig (1977; see also Coles, 1980)
has shown that symbiotic crabs, shrimps and fish that coinhabit coral heads are
very aggressive to intruders—of the same or different species—but tolerate one
another’s presence after a period of acclimation, after which they may even co-
operate in defending their coral heads against intruders.
Hermit crabs are renowned for their fights over shells and the frequency with
which they exchange shells. Since each hermit crab will have a particular sized
shell that fits it best, there is always the possibility that intraspecific ‘contests’
actually benefit both participants (see Hazlett, 1981, for a review). Abrams
(1982) has shown that shells are exchanged in 70 to 72% of ‘fights’ if both
animals benefit from the exchange, or if one benefits considerably and the other
either suffers no loss or only loses very slightly. Where neither animal benefits,
shell exchange never occurs, and when one animal stands to lose substantially,
then the exchange of shells only takes place in less than 10% of the fights.
Aggressive interactions have also been shown to be restricted because an animal
will normally only attack a smaller individual, and then only if that individual
has a shell that is superior in terms of the attacker’s own needs (Bertness,
1981a). Where only one animal benefits, it is always that individual that initiates
the fights; but in such cases, exchange only occurs if the initiator is the larger of
the two crabs (Hazlett, 1978). In some species the initiator of a fight taps its shell
on the substratum, which may impart information about the nature of the shell to
the opposite animal (Hazlett, 1981). All these findings suggest that both
participants glean information about the ‘quality’ of the respective shells and that
‘fighting’ between conspecific hermit crabs is more likely to lead to a mutualistic
exchange benefiting both animals than to a competitive situation where one animal
loses. There are even cases where the use of shells by hermit crabs facilitates
their subsequent use by other hermits. An example is the terrestrial Coenobita
compressus which preferentially occupies Nerita shells. Each individual slowly
modifies the shell, enlarging the mouth and eliminating the columella to broaden
the internal space. So important is this function that a large proportion of
sexually mature hermit crabs would be unable to find shells which were large
enough if it were not for this process of shell modification (Abrams, 1978).
Thus in many instances contests between conspecifics are ritualized,
escalations of aggression are minimized, and apparently aggressive interractions
may even be of mutual benefit.
Differences in diet
Intraspecific competition may be reduced if different sized animals feed on
different sized prey, although in most of such cases it remains to be proved that
Fig. 11.—Relationship between predator and prey size: A, Conus ebraeus, size of
polychaete prey measured as size of mandible or maxilla (after Kohn & Nybakken, 1975);
B, Pisaster ochraceus (after Menge, 1974).
Fig. 12.—Relationship between body length of Pectinaria gouldii and depth of feeding (A)
and length of average sized particle ingested (B) (after Whitlatch, 1974).
intraspecific competition is the cause of this differentiation. Correlations between

body size and prey size are well known for a number of species including the
rock lobster Jasus lalandii (Griffiths & Seiderer, 1980), starfish Pisaster
ochraceus (Fig. 11B), gastropods Acanthina punctulata (see Fig. 44, p. 549)
(Menge & Menge, 1974), Thais lamellosa and T. emarginata (Bertness, 1977)
and several species of Conus (Fig. 11A, Kohn & Nybakken, 1975; Leviten,
1976). In some cases the necessary spectrum of prey sizes can only be attained
by feeding on a range of species, with overlapping sizes. For example, small C.
ebraeus feed largely on Nereis jacksoni, medium sized animals on Perinereis
singaporiensis, and large individuals only on Palola siciliensis (Kohn &
Nybakken, 1975). This has the effect of further separating the diets of different
sized individuals.
Deposit-feeders may select different sized particles. The polychaete Pectinaria
gouldii lives in a tapering tube, positioned just below the surface of the sand with
484 G.M.BRANCH
the head of the worm downwards. Whitlatch (1974) has shown that the depth at
which feeding occurs is related to the size of the worm (Fig. 12A) so that
apportionment by depth occurs. In addition, small worms preferentially select
small particles (Fig. 12B), further subdividing food resources between the size
classes, as Walter (1973) has also recorded for sipunculids.
Warwick (1982) has compared the sizes of successive instars of various
marine nematodes and shown a ratio which consistently approximates 1:1·3.
Hutchinson (1959) has suggested that this is the minimum difference that must
exist between the sizes of different species within a feeding guild if they are to
continue co-existing. In fact, there seems to be no limit to the similarity of body
size between coexisting competitors (Pontin, 1982), but Warwick’s application
of this idea to an intraspecific situation is an interesting one, for body size in
nematodes is closely correlated with prey size. This implies that ecological
isolation (in terms of diet) may occur between age groups of nematodes and, for
that matter, age groups of any other organisms which maintain a constant body
size between moults. Of course there is nothing magic about differences in body
size—let alone a particular minimum difference of 1·3–unless it can be linked to
differences in food and unless food is limiting. One would never claim
ecological isolation for successive instars of caterpillars even though they
conform almost exactly to a ratio of 1:1·3!
It is more difficult to conceive how herbivores feeding on macroalgae may
partition their food between different sized classes. Patella longicosta is one of
the few herbivores showing clear-cut differences in the diet of different sized
classes (Branch, 1975b). Small individuals are almost completely limited to the
shells of other gastropods where they feed on the encrusting alga, Ralfsia
expansa. Increase in size forces the limpets to relinquish their host-shells and to
settle on rocks. Here they are excluded from Ralfsia, for almost all of this alga
occurs in the territorial ‘gardens’ of other larger Patella longicosta. Initially
these intermediate sized limpets are thus prevented from feeding on Ralfsia and
they settle on Lithophyllum and use this as their main food source. Only in their
third or fourth year do they establish their own Ralfsia ‘gardens’ by means still
not elucidated. Consequently, all large Patella longicosta are found on such
Ralfsia ‘gardens’ which they territorially defend against other invading limpets.
Other species of algae are grazed away from the perimeter of the ‘garden’ and
any spores settling within the ‘garden’ itself are also eliminated. The Ralfsia
itself is grazed by cutting paths through the alga thus avoiding its elimination. As
Ralfsia grows fastest at its edge, these paths increase the growing edge and hence
the growing rate of the alga. Thus, there are very sharp changes in diet related to
body size in Patella longicosta (Branch, 1981).
Fish frequently change their diets as they age (e.g. Collette & Talbot, 1972;
and see review by Helfman, 1978). Hobson & Chess (1976) have compared both
diet and feeding rhythms of fish of different ages and shown that juveniles of
reef fish are usually predatory and diurnal but adults are more specialized, more
often herbivorous and usually nocturnal. Olla, Bejda & Martin (1974) discuss
how the adults and juveniles of various species occupy different habitats, and
suggest that both predation and competition are reduced as a result. In each of
these cases the real significance of these differences in reducing intraspecific
competition between adult and juvenile fish remains an open question because no
tests have been undertaken to show whether there would be an increase in
competition in the absence of these presumed adaptations.
One final aspect of differential diets that may alleviate competition within
species is that of intersexual differences. Such differences are only likely to be
effective when pairs of animals feed in the same area, and have frequently been
suggested to occur in birds. A clear example is the African black oystercatcher,
Haematopus moquini, which occurs in territorial pairs. The sexes overlap in bill
size, but within any given pair the female always has the longer, more pointed
bill. This is associated with differences in the diet of the two sexes, males taking
a greater proportion of whelks and limpets and females of polychaetes and small
unshelled prey (Hockey & Underhill, 1984). An unresolved question in this
example—and in other comparable cases—is whether food is ever sufficiently
limiting to demand sexual dimorphism as a means of reducing intraspecific
competition.
Thus there exists a variety of mechanisms whereby intraspecific competition
may be reduced, but the accent remains on the “may” because, apart from a few
experimental tests, little has been done to establish whether these mechanisms
really are efficient means of reducing competition. There is clearly a need for
more research on intraspecific competition. In particular, when tests are
undertaken for interspecific competition experiments should be designed so as to
test simultaneously the intensity of intraspecific competition in the participating
species, for the short- and long-term response of a species to an interspecific
competitor may depend on how intense is its own intraspecific competition.
COMPETITION BETWEEN SPECIES

The consequences of interspecific competition are likely to vary with the nature
of the species involved, the means of competition, the kind of resource competed
for and the amount of overlap in the niches of the species. In extreme cases
competition can result in the exclusion of the weaker competitor from the area
occupied by the dominant. In the long term, extinction of the subordinate species
is a possibility—although this is a more debatable consequence and one that is
extremely difficult to prove. More often the weaker species will be forced to
withdraw from part of its potential niche (referred to as its ‘fundamental niche’)
to a smaller part of its range (its ‘realized niche’), often being confined to
suboptimal areas in the process. During evolutionary time it is possible that the
dominant species only becomes dominant because it evolves greater efficiency at
exploiting the resource that is being competed for, or because it develops
methods of interfering with its competitor. This possibility is discussed further in
the concluding section of the review. An alternative viewpoint is that over time
486 G.M.BRANCH
competing species will diverge in their use of resources, reducing competition

and often increasing the specialization of the species in the process.
In this section I discuss examples of interspecific competition, drawn from a
range of contrasting communities in which different kinds of resources are
competed for in different ways; and I follow this with a discussion of various
proposals put forward to explain continued coexistence of competitors.
EXAMPLES AND CONSEQUENCES OF INTERSPECIFIC

COMPETITION
Sedentary benthic carnivores

Starfish play a major rô1e in many intertidal and subtidal communities, and
potential competition between species has been analysed in a number of
instances. One example is the comparison of two closely related species,
Astropecten aranciacus and A. bispinosus which coexist despite having very
similar prey (Ribi, Scharer & Ochsner, 1977). When they occur separately the two
starfish have very similar body sizes (Fig. 13A) but when living together their
body sizes are displaced (Fig. 13B). Character displacement such as this was
first described by Brown & Wilson (1956), who suggested that competition
forces species to diverge, reducing overlap in the process. In this instance,
displacement reduces overlap in the size range of prey eaten by the two starfish.
According to competition theory (see MacArthur & Levins, 1967; MacArthur,
1972) the distance between the mean values of the prey sizes of the two species
(d) should exceed the functional width (w) of prey sizes for each species if
coexistence is to continue. The standard deviation (ξ ) is often taken in place of
w. Figure 13C illustrates the size composition of one important prey species
(Echinocardium cordatum) eaten by both starfish, and shows that d exceeds ξ ,
conforming to the theoretical prediction for two coexisting species. Further
displacement is suggested by the fact that when the animals occur sympatrically
they have different daily rhythms of activity. Astropecten aranciacus also tends
to occur in deeper water and on coarser sediments than A. bispinosus
(FerlinLubini & Ribi, 1978), partially separating their habitats.
At first sight, analyses such as this are very satisfying, the data fitting the
predictions of competition theory very closely. However, a number of
unanswered questions remain. One is that no allowance is made for animals of
different ages (and hence sizes). If displacement of adult body size is necessary
for coexistence, how do younger (smaller) individuals of the larger species
manage to coexist with the smaller species, with which they must overlap in size
at some stage? Another problem is that competition is assumed to be reduced
because different sized prey are eaten. But if the two species are simply taking
different size groups of the same species of prey (e.g. Fig. 13C) then the smaller
Fig. 13.—Size-frequency composition of the starfish Astropecten aranciacus and A.

bispinosus: A, when they occur separately; B, when they coexist; C, displacement of body
size in coexisting Astropecten aranciacus and B. bispinosus results in a displacement of
prey size, as shown for Echinocardium cordatum; the difference between the means (d) is
greater than standard deviation (ξ ) for the size composition of each lot of prey; (after Ribi
et al., 1977).
species will still deprive the larger of food, by consuming the prey before it
reaches the size at which the larger predator consumes it.
Further difficulties beset attempts to quantify the minimum overlap that can be
tolerated by competitors. The ratio between d and w discussed above, for which
a minimum value of 1 is proposed for stable coexistence, depends on three
assumptions: first, that only a single resource is important and that it can be
measured in a unidirectional manner (e.g. body size of prey); secondly, that the
utilization of the resource by both competitors is approximately similar in
intensity and variability (i.e. their ‘utilization curves’ are similar); and thirdly,
that the resource that has been chosen for analysis really is the one that is
limiting in terms of competition between the organisms. These conditions are
488 G.M.BRANCH
Fig. 14. Changes in mean wet weight of the starfish Leptasterias at a control site and at
sites where Pisaster was removed or added (Menge, 1972).
probably not often met, and even if they are it is difficult to falsify the model, for
if the ratio of d:w is less than 1, it is always possible to claim that some other
resource is being used differentially by the species and thus separating them
ecologically (see Begon & Mortimer, 1982 for a succinct summary and
references).
The concept of character displacement has also been criticized by Grant
(1972) who (at least up to that date) could find no examples in which the
displacement was convincingly linked to a reduction in competition, was
repeatable from one locality to another, and could be proved to have a genetic
basis. The possible case of character displacement in the two Astropecten spp. is
clearly worthy of further investigation, bearing these problems in mind, before it
is accepted as meeting the criteria set down by Grant. Other cases of character
displacement are discussed below (p. 559), at least one of which meets most of
these criteria.
A more complex interreaction occurs between the starfish Pisaster ochraceus
and Leptasterias hexactis. After altering the density of Pisaster by removal in
one area and addition in a second area, Menge (1972) demonstrated that
Leptasterias, respectively, increased and decreased its mean body weight in these
two areas (Fig. 14). This is one of the few experimental demonstrations of
competition between carnivorous marine invertebrates. Pisaster and Leptasterias
have very similar distribution patterns and simultaneous peaks of feeding in mid-
summer. Their diets are very similar in terms of both the numbers of prey species
(Fig. 15B) and the size composition of prey (Fig. 15A). When the food,
however, is analysed in terms of caloric intake, the starfish obtain most of their
energy from quite different prey sizes and species (Fig. 15C) (Menge, 1974). The
failure of Pisaster and Leptasterias to subdivide their resources in a simpler way
may have a number of explanations: prey are not predictably or continually
available and large prey are relatively scarce so that apportionment by prey
species or size is not possible, and scarcity of food in winter prevents seasonal
segregation of feeding activities (Menge, 1974).
Fig. 15.—Overlap in the diets of the starfish Pisaster and Leptasterias in terms of prey
size (A), prey species (B) and calories obtained from different prey species (C) (after
Menge, 1974).
In addition to this exploitative competition, Pisaster attacks Leptasterias with

its pedicellaria, causing a reduction in the feeding rate of Leptasterias. Such
interference competition is unusual in a predator such as Pisaster which holds no
490 G.M.BRANCH
fixed territory. Leptasterias survives this interference because it is smaller,

finding refuge in deep crevices, is more mobile and forages more efficiently, and
reproduces at a much smaller size. Pisaster also repels the starfish Pycnopodia
(Wobber, 1975), and similar dominance by Crossaster papposus over Asterias
rubens has been recorded by Sloan (1979a).
Menge (1979) has come to quite different conclusions in comparing two
coexisting almost identical species of Asterias. Electrophoretic protein analyses
indicate their very close relationship and they have been referred to as “semi-
species”, the suggestion being that they probably evolved in allopatry during the
mid- to late Pleistocene (Schopf & Murphy, 1973). Ecologically the two species
share many characteristics. Their diets, times and seasons of maximum activity,
and their distribution patterns are very similar—at least in the area where Menge
worked. Furthermore, their body sizes are positively correlated when
comparisons are made between different areas, and the starfish have no adverse
effect on one another’s growth when held together in the laboratory at either high
or lower food levels. Menge (1979) suggests the two coexist not because of
differences between them, but because they are held below equilibrium densities,
by periodic diseases, storms and possibly cannibalism, at population levels too
low for competition to take its toll. This explanation fits the observations made in
the field, but it still seems peculiar that the animals have no adverse effect upon
each other when held in the laboratory and given only low food levels. Menge
also proposes that the relatively variable environment of New England is the
reason why the two Asterias spp. have not evolved the competitive mechanisms
found in Pisaster, which occurs in the relatively constant environment of the
Pacific north west.
A detailed analysis of habitat and food overlap between Conus species has
been undertaken by Kohn and his co-workers. This mainly tropical genus is often
represented by a large number of coexisting species. These may be zoned
differentially across intertidal platforms or have different habitats, and most of
the species are separated by very specialized diets, many feeding on specific
polychaetes, fewer on gastropods and a small number on fish (Kohn, 1959,
1968). For example, C. sponsalis and C. abbreviatus have very similar
distribution patterns and feed exclusively on polychaetes, but eunicids comprise
68% of the diet of C. abbreviatus while nereids make up 52% of the diet of C.
sponsalis. In food-choice experiments the two species also show a preference for
these respective polychaetes. Kohn (1959) concluded that the 18 Hawaiian
Conus spp. he examined were sufficiently ecologically different that
interspecific competition does not limit their population densities, and he
suggested that the lack of overlap between the species was a result of earlier
competition. Comparable differences in diet have been described for other
coexisting gastropods (Paine, 1962, 1963; Taylor, 1976). The differential
zonation of various Conus spp. probably has little to do with competition.
Leviten & Kohn (1980) have shown that high-shore species such as C. ebraeus
are most tolerant of harsh conditions and survive catastrophic rainfall that kills
less tolerant species. Zonation thus reflects tolerance to a physical stress.
On the other hand, dietary specializations may well allow the coexistence of
species. In one interesting comparison, Kohn (1966) contrasts the dietary
specialization of the many Hawaiian Conus spp. with the very generalized diet of
C. californicus, the only member of the genus in California. This dietary difference
is to be expected if competition has resulted in specialization. Recently Kohn
(1978) has made an important comparison between an isolated population of C.
miliaris on Easter Island and populations elsewhere in the Indo-West Pacific
which coexist with other members of the genus. On Easter Island the density of
C. miliaris is far greater and its diet includes a greater diversity of prey species,
suggesting an increase of numbers and an expansion of diet in the absence of
other competitors in the genus. This is convincing circumstantial evidence that
competition usually restricts the populations of C. miliaris. Particularly
significant is the finding that many of the prey species that are added to the diet
of C. miliaris on Easter Island are eaten by competing Conus spp. in other areas.
Kohn also shows that larger C. miliaris feed on larger polychaete species,
resulting in a separation of the diets of different sized cones and, at least,
potentially reducing intraspecific competition.
It does not always follow that species richness is correlated with dietary
specialization. In a comparison of the Conus spp. from the Maldives and Chagos
islands with those of Hawaii, Kohn (1968) could find no greater specialization in
the animals from the Maldive and Chagos islands, despite there being almost
twice as many species there. His comparison of intertidal and subtidal species
also shows greater specialization in the intertidal zone where fewer species
coexist. Kohn explains this on the basis that the intertidal represents a uniform
habitat allowing freer movement and greater access to prey, so that specialization
is possible. This is an interesting point, for it shifts the emphasis away from
competition and towards the nature of the habitat to explain dietary
specialization.
Figure 16 combines measures of habitat overlap and food overlap for the very
diverse Conus assemblages from Thailand and Indonesia, revealing that there are
very few species that are not separated by substantial differences in their habitat
or food (Kohn & Nybakken, 1975). Figure 16 also indicates that those species
with considerable overlap in habitat usually overlap very little in diet and vice
versa. Kohn (1971) has calculated the overlap (ξ ) in habitat and food of various
Conus assemblages and has predicted the theoretical number of species which
can be packed into each region. Basing his calculation solely on the microhabitat
differences between the species, the number of species actually present always
exceeds the predicted maximum species packing. Habitat apportionment is thus
inadequate to explain existing diversity. A similar calculation based on dietary
differences between the species predicts numbers of species which are very close
to or slightly lower than the observed numbers. Thus, specialized feeding habits
more closely predict the diversity of Conus Only when microhabitat and food
492 G.M.BRANCH
Fig. 16.—Conus spp.: relationship between habitat overlap and dietary overlap; with few
exceptions those species with high dietary overlap have low habitat overlap while high
habitat overlap is associated with low dietary overlap (after Kohn & Nybakken, 1975).
requirements are combined do the predicted number of species always equal or

exceed the actual number. Schoener (1974) has pointed out that as the number of
species in a competitive system increases, so they will need to partition more
dimensions of the environment to allow them to share the habitat. Food, space,
and time may all be segregated between the members of a complex community
while one of these dimensions would be adequate to keep members of a simple
community apart. Nevertheless, Kohn (1971) has suggested that, in general,
cooccurring predators are likely to possess differences in diet as a means of
allowing coexistence of competitors; while deposit-feeders will more often
specialize in terms of the microhabitats they use.
Kohn & Nybakken (1975; and see Kohn, 1967) have found that heterogeneity
of the environment is related to the number of coexistent species. The
topographically more simple intertidal areas support fewer Conus species than
the more complex and patchy subtidal reefs. Abele (1974, 1976) and Biernbaum
(1979) have demonstrated a similar relationship between species diversity and
habitat complexity for crustaceans. This leads to an important generalization:
that the more complex the topography of a habitat is, the more species we can
expect to be supported. This is often presumed to be because each species can
afford to be more specialized to a specific portion of the habitat, and hence less
likely to overlap the needs of other species. Another interpretation is that
heterogeneous habitats provide more refuges from physical stress and predation.
Kohn & Leviten (1976) and Leviten & Kohn (1980) have shown a correlation
between species diversity and the occurrence of refuges, and ascribe it to
increased protection from wave action.
Spight (1981) has sought differences between three Thais spp. which might
explain their coexistence. They are zoned differently, and make maximum use of
barnacles (their major food) at different times of the year. In spring, the
barnacles are confined to the high shore, and the two high- to mid-shore thaids
grow faster during this period. The low-shore Thais lamellosa reaches its peak
growth in summer after the annual settling of fresh batches of barnacles. Spight
suggests the three Thais spp. are not clearly separable in terms of habitat, food or
time of peak growth, but that all three factors combined allow sufficient
differences in their niches for coexistence. Connell (1970) has speculated that the
main reason the west coast of North America supports three species of Thais is
because the recruitment of barnacles is very predictable in time and space so that
the three species can specialize on different regions of the shore. By contrast, the
erratic settling of barnacles in Scotland sustains only a single Thais (Connell,
1961b).
The analyses of Kohn and his co-workers constitute an important and
impressive set of data in which patterns of resource usage (principally in terms
of diet) consistently conform to those that would be predicted by competition
theory. The more species that coexist the finer they appear to partition resources,
the more specialized they are, and the more dimensions of the habitat they
appear to utilize to achieve ecological differences between the species. It is still
necessary to question whether these differences are really due to competition. In
no case has competition between diffferent species been demonstrated. This does
not deny that its past action may have led to ecological divergence, but if this is
so, it once again leaves a sense of frustration because it is impossible to test for
such effects; and there may be other causes of specialization in Conus spp. which
are unrelated to competition (see below, p. 551).
A different approach by Kent (1983) based on experimental manipulations,
has yielded concrete evidence of competition between the gastropods Busycon
contrarium and B. spiratum. The two are different in size, B. contrarium being
substantially larger, and Kent has addressed the question whether competition
occurs between juveniles of B. contrarium and comparably sized adult B.
spiratum. Removal of small B. contrarium from sea grass beds does result in an
increase of B. spiratum, demonstrating that competition normally takes place,
but this result is not achieved on oyster beds, where predation by crabs annually
eliminates the thinner-shelled B. spiratum. A comparison of the two species
reveals no difference in their habitats nor in seasonal or daily peaks of activity.
Their diets are, however, very different, B. spiratum eating ‘active’ bivalves
which are mobile but thin-shelled, and B. contrarium ‘passive’ bivalves which
are sedentary and thick-shelled. B. contrarium has a thick shell itself, and a
narrow foot and shell-mouth which allow it to chip the shells of the passive
bivalves to open them. The inability of B. spiratum to do this, and its smaller
size, originally prompted Paine (1962) to suggest that B. contrarium is the
superior competitor. Kent (1983), however, has demonstrated in laboratory
experiments that B. contrarium prefers active bivalves but is normally prevented
494 G.M.BRANCH
from feeding on them in the field, partly by the greater efficiency of B. spiratum
(due to its broader foot, wider shell and faster movement) and partly by
aggressive attacks that B. spiratum makes on B. contrarium. Thus, it is the
smaller B. spiratum which is the dominant competitor, forcing the other species
to rely on less preferred prey. In the light of its greater exploitative efficiency and
its ability to interfere aggressively, it is interesting that B. spiratum still suffers
from the presence of B. contrarium (as evidenced by the consequences of
removing B. contrarium) presumably because B. contrarium exploits some of the
bivalves normally eaten by this animal. It is a great pity that the experiments
undertaken by Kent did not also include the reverse manipulation—removal of
B. spiratum—nor did they test for the relative effects of intra- and interspecific
competition, but even so the results are of great interest. For one thing, they show
that the difference in diet between the two species is a consequence of
competition and not a means of reducing competition. For another, it appears
that there is a trade-off of benefits arising from the different shells of the two
species. B. contrarium, with its thick heavy narrow-mouthed shell, is inefficient
at feeding on active bivalves and a poor competitor, but can withstand predation
from crabs more efficiently, while the reverse is true for B. spiratum. Paine
(1962) has pointed out that in other areas different but comparable pairs of thick-
and thin-shelled Busycon spp. co-exist.
This example has its counterpart in a very different pair of animals, the
intertidal spiders Desis formidabilis and Amaurobioides africanus. Both are air-
breathing, possess physical gills that allow survival during submergence, and
build nests under empty shells in which they pass the high-tide period. Although
they have similar tolerances to desiccation, Amaurobioides is restricted to the
upper shore while Desis dominates the lower regions. Since density is governed
by the availability of suitable shells, aggressive intraspecific competition takes
place for nesting sites, particularly between females. Interspecific fighting is very
marked at the overlap boundary between the two species. In laboratory
experiments, Desis always outfights and often kills Amaurobioides, its
superiority stemming from its more aggressive nature and the far larger size of
its fangs (Lamoral, 1968). Thus, it seems that aggressive interference confines
Amaurobioides to the inferior upper-shore zone where food is scarcer; but
Lamarol could not identify the factor limiting Desis to the low shore.
Thus, in the case of sedentary benthic carnivores there exists abundant
circumstantial evidence of competition and its consequences, but with the
exceptions of the work of Menge (1972), Kent (1983), and Lamoral (1968), little
experimental proof of its rôle. It is significant that all three examples include
elements of interference competition, notably absent in all the cases in which
niche divergence and apportionment are inferred.
Sessile carnivores
Niche apportionment on the basis of diet seems inprobable in sessile carnivores
which must depend on water movement or wave action to make prey available.
Forms such as anemones seem totally opportunist in what they consume (e.g.
Dayton, 1973a). On the other hand, they depend absolutely on holding space and
have evolved a bewildering array of mechanisms towards this end.
The aggressive nature of intraspecific interreactions between anemones has
already been mentioned. Comparable interspecific contests take place, different
species using acrorhagi or specialized fighting tentacles to overcome neighbours
(Francis, 1973; 1976; Williams, 1975; Purcell, 1977; Brace & Pavey, 1978;
Bigger, 1980). Anemones also overgrow adjacent low-growing competitors, and
because of their ability to form clones, can spread over the substratum.
Aggression never occurs between clone-mates. Intensity of aggression is species-
specific and also size-specific and, at least in the Carribean, correlates with the
permanency of the substratum each species normally occupies. Species living on
fragile corals are non-aggressive, those on rubble or sand are moderately
aggressive, while those on stable massive corals are so aggressive that they even
destroy the coral polyps in the immediate vicinity (Sebens, 1976).
The last ten years have seen the birth of a new literature on coral interactions.
While it has long been assumed that corals compete passively by over-shading
competitors (see Connell, 1978; Sheppard, 1982, for reviews) the discovery by
Lang (1971) of aggressive interactions has opened new possibilities. While fast-
growing species may overgrow others, those with slower growth rates are more
aggressive and can extrude their mesenteries and digest away less aggressive
species. Lang (1973) demonstrated a persistent hierarchy of aggressive
dominance, allowing the massive and often encrusting species to prevent or at
least slow down overgrowth. Working in a different area, Sheppard (1979)
confirmed the aggressive mesenterial digestion of corals, but did not find the
inverse relationship between growth rate and aggression that Lang described.
Hydrozoans can also prevent overgrowth by producing toxins that inhibit growth
of other hydroids (Katô, Hirai & Kakinuma, 1967).
While some species of coral may gain temporary ascendancy by use of
mesenterial digestion, subordinate species may ultimately win the contest by a
secondary defence—the development of long sweeper tentacles which reverse
the dominance (Richardson, Dunstan & Lang, 1979; Wellington, 1980; Bak,
Termaat & Dekker, 1982). As a variation on this theme, Goniopora spp. develop
elongate “sweeper polyps” which kill adjacent species that fall within their reach
(Sheppard, 1982). A further complication is that immunological responses
between different individuals may lead to cell damage and even death. The effect
is most dramatic and one-sided in intergeneric contacts, while with conspecifics
or congeneric interactions both parties suffer and sustain bleaching (Hildemann
et al., 1977a, b). A final twist to the tail is that symbiotic crustaceans influence
the outcome of contests. For instance, the crab Domecia which lives in crevices
496 G.M.BRANCH
that it causes to form in the host coral, will kill the tissues of adjacent corals,
causing up to 60% mortality on the surface of corals which grow close to its
host, and thus tip the competitive balance in favour of its host (Bak et al., 1982).
Despite the aggressive defences of corals, at least one soft coral (Nephthea
brassica) has the ability to overgrow the stony coral Acropora hyacinthus (La
Barre & Coll, 1982; see also Benayahu & Loya, 1981). The coral deposits a flat
plate of aragonite beneath the advancing soft coral— seemingly to reduce
contact with it—leaving trails marking the passage of the Nephthea over the
surface of the coral. Acropora is able to prevent colonization of most organisms
but Nephthea has obviously overcome its defences and enjoys a habitat which is
free from competition by other organisms. In a comparable situation, the
hydrocoral Millepora not only overgrows gorgonians but is capable of detecting
the presence of gorgonians which are suitable as a substratum and of directing its
growth towards these colonies (Wahle, 1980).
The complexity of biotic interactions in determining the outcome of
competition between corals is well illustrated by the work of Wellington (1982a;
see also Vine, 1974; Potts, 1977). Wellington argues that zonation of corals is
due to differential mortality from predators and that the community structure of
corals is due to interactions between mobile and sessile species. He shows that
damselfish (Eupomacentrus acapulcoensis) kill areas on corals, particularly
massive corals, to create algal gardens in their territories. The damselfish
concentrate in shallow waters where the topography provides abundant holes and
crevices for them to shelter from predators. There they destroy most of the
massive corals such as Pavona while having relatively little effect on forms such
as pocilloporids which have branching colonies that are difficult for the small
fish to graze and make a poor substratum for the gardens. The overtopping of
other corals by pocilloporids is thus enhanced by the activity of the damselfish.
Furthermore, the damselfish protect corals within their territories by chasing
away grazers such as surgeon fish and parrotfish. In deeper waters, the
topography is less complex and there are few damselfish. Here grazers
selectively attack and eliminate pocilloporids, which are very vulnerable to
grazing by large fish. The result of this interreaction between various fish and the
corals themselves is that pocilloporids are concentrated in shallow waters while
in deeper waters there exists a much sparser cover of corals consisting mainly of
Pavona.
Working on the assumption that it is possible for corals to apportion the
environment between them, Porter (1976; see also Maguire & Porter, 1977) has
developed a model of how competition may have moulded the evolution of
colony structure and mechanisms of nutrition in corals. Most corals contain
symbiotic zooxanthellae, which require light. Porter suggests this is reflected in
their branching plant-like growth forms which maximize surface area for capture
of the multi-directional scattered light. Some corals also capture zooplankton. As
polyp diameter is correlated with tentacle length it is a useful indicator of the
ability to capture zooplankton. The relative abilities to photosynthesize or to
Fig. 17.—Relationship between polyp diameter and the ratio of surface area to volume in
corals: corals with large polyp diameters have long tentacles and may depend more on
capturing zooplankton, while those with large surface areas possibly depend more on
autotrophic production by their symbiotic zooxanthellae (after Porter, 1976).
capture zooplankton are reflected in the relationship between the ratio of surface
area to volume and polyp diameter. Figure 17 shows the dichotomy between
forms which are presumed to rely more on their zooxanthellae, and those which
depend on the zooplankton capture (Porter, 1976). No two species overlap in
their position on a curve which plots surface area/volume against polyp
diameter, suggesting niche separation (Fig. 18). Even the major coral families
occupy discreet portions of the curve, hardly overlapping with other families.
The families which are geologically oldest occupy the largest area, implying that
niche separation has increased over geological time (Porter, 1976). It is thus
possible to have a canopy of predominatly autotrophic species with high surface
area to volume ratios, shading an understorey of more heterotrophic species with
large polyps and a low surface area.
For this model to have any validity, competition must be a dominant force in
the evolution of corals (and thus, by implication, in the structuring of modern
communities), and different species should show differences in their relative
dependence on zooplankton and zooxanthellae. It is true that some corals have a
dominating competitive rôle and do exclude many species where they occur
densely. Two examples are Acropora palifera (Sheppard, 1979; but see
Sheppard, 1981) and Monastrea annularis (Scatterday, 1977). Furthermore,
when corals are experimentally shaded, those species with small polyps
(presumably least dependent on plankton) leach first, while those with largest
polyps are least affected (Rogers, 1979). Partial support for Porter’s model also
comes from Wellington’s (1982b) work in which he screened and/or shaded
corals; massive species with larger tentacles did utilize zooplankton more than
branching, small tentacled species. Even so, all the corals that were tested were
primarily dependent on light, and Wellington concluded that the differences
between the various species in terms of their use of light and zooplankton were
inadequate to explain observed patterns of zonation. The discovery that various
species can compensate for low light (Wethey & Porter, 1976; Falkowski &
Dubinsky, 1981) also casts doubts on the possibility of niche apportionment of
498 G.M.BRANCH
Fig. 18.—Plotting coral species on a graph of log (polyp diameter) versus the ratio of
surface area to volume shows that families occupy discrete portions of the graph,
suggesting that competition is reduced because the families differ in their dependency on
autotrophy and zooplankton: 1, Astrocoeniidae; 2, Siderasteridae; 3, Poritidae; 4,
Acroporidae; 5, Agariciidae; 6, Pocilloporidae; 7, Oculinidae; 8, Faviidae; 9,
Meandrenidae; 10, Caryophyllidae; 11, Mussidae; (after Porter, 1976).
trophic demands. Bradbury & Young (1983) analysed the spatial arrangement of
corals and, despite finding a few species that were negatively correlated, concluded
that large-scale patterns of zonation could not be explained by the small-scale
spatial arrangements of species—in other words, that coral interactions play little
part in structuring communities.
It is possible that these seemingly divergent views are reconcilable. The
sophistication and diversity of competitive mechanisms argue for an intensely
competitive situation almost suggestive of an evolutionary race, adaptation
countering adaptation. Paradoxically, this very complexity may prevent
competitive interactions per se from dictating community structure in coral reefs.
While Lang (1973) found regular transitive hierachies of competitive ability (in
which A out-competes B, B out-competes C, and so on), the variety of
competitive mechanisms and the reversals of dominance that are now known
(reviewed by Sheppard, 1982) make it less likely that there will ever be a clear
winner and a regular order of competitive ability. It would be naïve to assume
that competition alone can explain all the patterns of coral distribution and it
seems that more profit will be gained by exploring the different conditions under
which competition does seem dominant compared with those in which factors
such as wave surge, predation and periodic disturbances are important. Depth,
productivity, incidence of predation, and biotic interactions may dictate the
relative importance of competition.
Sedentary rocky-shore herbivores

Because the densities of relatively immobile herbivorous animals are easy to
manipulate, and their food supply can be altered experimentally, there exists an
extensive literature testing whether competition exists between such herbivores.
Limpets in particular, being dominant organisms on most shores, have received a
lot of attention. For instance, the coexisting limpets Acmaea digitalis and A.
scabra compete for food (Haven, 1973). Experimental removal of either species
results in a more rapid growth of the other. The diets of these two species are
very similar, and they may continue to coexist because of microhabitat
differences: A. digitalis is more common on vertical rocks, A. scabra on
horizontal surfaces; A. digitalis extends higher on the shore and is
proportionately more common in areas of strong wave action. Haven’s
experiments have been criticized by Underwood (1979) because of the failure to
distinguish the relative impact of intra- and interspecific competition but, as
Hawkins & Hartnoll (1983) comment, they remain a valid indication of the
effects of two species upon each other.
Underwood (1978) has examined the competitive interactions between three
herbivorous gastropods which are common on the southeastern coast of
Australia. By caging these animals in the field at different densities and in
different combinations of species, he measured their interactions in terms of
survival and change of body weight. Cellana tramoserica proved competitively
superior to Bembicium nanum and Nerita atramentosa to both. A similar
comparison of the competitive ability of Cellana tramoserica and the pulmonate
limpets Siphonaria spp. shows that Cellana tramoserica always has an adverse
effect on the survival of the pulmonates while they in turn have no impact on C.
tramoserica. The difference is predictable, for while C. tramoserica digs deep
into the substratum with its radula and removes most of the food in its path, the
Siphonaria spp. skim superficially over the rock or feed on macroalgae thus
failing to interfere with the major food source of the other limpet (Underwood &
Jernakoff, 1981; Creese & Underwood, 1982).
Far more complex interactions occur between some limpets. Stimson (1973)
has described territorial behaviour in Lottia gigantea, which pushes other
herbivores (and potential competitors for space) forcefully off its patches of
algae. Experimental removal of Lottia from these patches results in an invasion of
Acmaea spp. while, conversely, instalment of Lottia rapidly reduces the numbers
of Acmaea (Fig. 19). Because of its large size (and hence larger radula) Lottia
leaves behind more alga when it grazes so that it does not eliminate its algal
500 G.M.BRANCH
Fig. 19.—Number of Acmaea spp. occurring in the territories of Lottia gigantea when
Lottia were left on their territories (A), Lottia were removed (B), and Lottia were installed
in vacant territories (C) (after Stimson, 1970).
patch. By contrast, Acmaea spp. are much smaller and crop the alga close to the
rock and would eliminate it if it were not for the territorial defence by the Lottia.
Branch & Branch (1980a) have shown that the limpet Cellana tramoserica
adversely affects the herbivorous starfish Patiriella exigua, which grows less (or
even loses weight) in the presence of the limpet. This seems partly because the
two compete for food and partly because Cellana interferes with the starfish,
repelling it on contact. Field observations show that the limpets C. capensis and
Patella concolor overlap broadly in distribution, zonation and food, but
differences exist in their microhabitats, Cellana capensis preferring dry rocks
and avoiding sand-covered rocks, while Patella concolor predominate in damp
areas, often where sand scours or forms a film over the rocks (Branch, 1976).
These differences may simply be due to different preferences and can be
interpreted as a means of permitting two competitors to coexist, but in the light
of the discovery of an interference mechanism in Cellana tramoserica, the
possibility exists that Patella concolor avoids areas occupied by Cellana
capensis. Further work is needed to distinguish which possibility is correct.
Interference takes place between the chiton Mopalia muscosa and the limpet
Collisella pelta, competitors for the same food source. Mopalia pushes
aggressively against the limpet, which disperses away from Mopalia (Connor,
1975). Since interference is involved, this is one of the few cases where
differences in activity rhythms may facilitate coexistence of competitors, for
while both animals are active at night, Mopalia moves around only when
submerged and Collisella pelta when it is exposed to air or awash. Competition
between different species of urchin has been suggested by various authors, but in
cases where manipulative experiments have been undertaken, remarkably little
effect of one species on another has been detected (Ebert, 1977; Schroeter, 1978).
Possible reasons for this are discussed below (p, 545). Only when interference is
involved—the aggressive defence of shelter-holes—do urchins succeed in
influencing the local distribution of other species of urchins (Grünbaum et al.,
Fig. 20.—The effect of removing Acmaea (Collisella) digitalis on the vertical zonation of
other Acmaea spp: A.(C.) paradigitalis responds by extending its range upwards; (after
Choat, 1977).
1978). Urchins often eliminate foliose macroalgae leaving only encrusting

corallines to coat the rocks (e.g. Paine & Vadas, 1969) and it has been inferred
that the restriction of Haliotis ruber to zones above and below the zone
dominated by the urchin Centrostephanus is due to competition for algae
(Shepherd, 1973b).
One particularly important demonstration of the effects of competition has
been described by Choat (1977). He was able to show that experimental removal
of a high-shore limpet, Collisella digitalis, allows the species occupying the zone
immediately below (C.strigatella, described in Choat’s paper as Acmaea
paradigitalis) to expand its vertical range and move upwards to occupy part of
the zone previously dominated by Collisella digitalis (Fig. 20). This remains one
of the few proven cases in which one herbivore excludes another from a habitat
without the use of interference. Another example involves Littorina unifasciata,
which is zoned immediately above Nodilittorina australis. Removal of Littorina
unifasciata allows upward expansion of Nodilittorina australis, increasing its
niche breadth; the reciprocal experiment in which N. australis is removed allows
Littorina unifasciata to expand its zonation down the shore (D.Ayre et al.
unpubl. data, cited in Branch & Branch, 1981).
Niche differences have frequently been sought as a means of explaining the
continued coexistence of herbivores that have similar requirements. For
example, Hines (1982) compared the biology of five coexisting species of spider
crabs (Majidae). He found differences in their diets, depths, zonation,
microhabitats, and body sizes. No single factor was sufficient to separate all the
species and Hines concluded that several dimensions of the niches of the species
were necessary to separate the species ecologically (see Schoener, 1974). He did
not, however, demonstrate that any of the niche dimensions he explored could be
limiting or that competition was taking place between the crabs. Since predation
and winter storms were the factors most likely to control the crab populations, it
502 G.M.BRANCH
seems unnecessary to seek differences between species that could explain their
coexistence.
There have been suggestions that herbivores are relatively indiscriminate
feeders. While predators are often very specialized in their diets and appear to
partition the environment on the basis of differences in diet (Kohn, 1971),
hervivores may achieve this less readily and be more likely to apportion the
habitat on the basis of differences in their microhabitats. It is true that suites of
grazing limpets feed indiscriminately on microalgae (e.g. Nicotri, 1977). Creese
1978, 1982) has addressed the question of how Cellana tramoserica and
Patelloida latistrigata can coexist when both feed apparently indiscriminately on
microalgae. Experiments show that Cellana tramoserica out-competes
Patelloida latistrigata unless there are barnacles present. Being much larger,
Cellana is presumably hindered while feeding amongst barnacles, while
Patelloida latistrigata is small enough to be unaffected by the barnacles and
even feeds on the surface of the barnacles, and hence finds a refuge from Cellana
in amongst the barnacles. Figure 21A shows that mortality of Patelloida
latistrigata is increased if half or all the barnacle cover is experimentally
removed, because Cellana tramoserica then invades the area. This interaction is
further complicated by a common predatory gastropod, Morula, which attacks
barnacles. Following an increase in the numbers of Morula, Creese (1978)
recorded a decrease in barnacle cover, which led to a dramatic decline in
Patelloida latistrigata as Cellana tramoserica immigrated into the area.
Subsequent recruitment of Patelloida latistrigata also failed due to heavy
mortality of juveniles in the area where barnacles had been depleted (Fig. 21B).
Since recruitment of Cellana tramoserica is decreased by the presence of
barnacles, and immigration of adults increased, while Patelloida latistrigata
predominates among barnacles (Underwood, Denley & Moran, 1983), differences
in the preferred microhabitats of these two species prevent exclusion of the
inferior competitor.
Two remarkably similar urchins, Echinometra oblongata and E.
mathaei coexist on Hawaiian reefs. Both live in holes in the reef, in which algal
debris accumulates. In both species mean size is correlated with increasing
waterflow over the reef (a function of increased deposition of algal debris in the
holes). The only difference that can be detected between the two is that E.
oblongata has spines with a slightly larger diameter; the greater strength of these
spines allows E. oblongata to dominate in areas of rough water while E. mathaei
is restricted to slightly calmer areas. Again, differences in microhabitats separate
the species rather than differences in diet. Since aggressive defence of holes is
known in various tropical urchins (Grünbaum et al., 1978), the possibility exists
that the differences in microhabitat reflect exclusion of one of the species from
the preferred habitat of the other.
These three examples all indicate microhabitat differences between
herbivores, rather than differences in diet. On the other hand, there are
herbivores that are very specialized in their diets. On South African shores there
Fig. 21. A, mortality of the limpet Patelloida latistrigata, following experimental removal
of barnacles; B, decline in the density of adult Patelloida latistrigata and failure of
juvenile recruitment following elimination of barnacles by the predatory gastropod
Morula; (after Creese, 1978).
are eleven Patella spp. Four occur in the mid- to upper-shore and are all
generalized browsers, feeding on any available macroalgae as well as diatoms, or
even organic spume deposited by the waves. Their niche breadths (B) can be
quantified and are large in terms of both zonation and diet. It is logical that the
upper-shore species should have catholic tastes (and hence a broad niche) for
their food supply is unpredictable and often restricted. These species all compete
by non-selective exploitation, and there are firm theoretical grounds suggesting
that this can also yield broadened food niches (Schoener, 1974).
By contrast, the low-shore and subtidal species have narrow niches, may have
selective diets, and are territorial (Branch, 1975b, 1976). Of these species,
Patella longicosta and P. tabularis territorially defend Ralfsia ‘gardens’ against
other limpets. Patella cochlear occurs densely at low tide, where individuals rotate
504 G.M.BRANCH
on their scars, feeding on a narrow band of algae around the scar, and they too
defend this area against intruders. P. cochlear is so dense that it excludes
virtually all algae except encrusting lithothamnia and fringing gardens of
filamentous red algae which seem to be its main food. The elimination of most
other algae prevents other limpets from encroaching into the P. cochlear zone.
To achieve this P. cochlear must exist at a density exceeding 400·m−2, which is
sufficient to exclude Ralfsia and hence also P. longicosta (Fig. 22). P. longicosta
is confined to areas above and below the P. cochlear zone, the intrusive niche of
P. cochlear incising into that of P. longicosta (Branch, 1976; and see Black,
1979 for another example of an intrusive niche in limpets). A correlation exists
between the number of coexisting limpets and their average specialization
(Fig 23) which parallels the findings of Kohn (1966, 1971) for Conus spp.; it is
discussed further in the concluding section of this review in relation to the possible
mechanisms giving rise to such correlations (see p. 575).
Hervibory is, therefore, not necessarily linked to an inability to partition the
environment by differential diets. Steneck (1982) has put forward a useful model
which predicts that specialized plant-herbivore relationships (and hence
specialized diets) are most likely to evolve in herbivores that are relatively
immobile and which feed on plants that are large relative to themselves.
Microalgal feeders are thus likely to be indiscriminate and mobile forms such as
fish are unlikely to be tightly associated with a particular species of alga. The
restriction of herbivores to particular habitats is not necessarily due to
competitive restraints. Shepherd (1973a) has argued that the microhabitats
selected by five coexisting Haliotis spp. are more a reflection of their relative
susceptibility to predation than of competitive interactions. Ayal & Safriel
(1982) have used similar reasoning in explaining the zonation and microhabitats
of five cerithiid gastropods. Unfortunately in neither case have experiments been
undertaken to test the rival merits of predation and competition in explaining the
selection of particular microhabitats.
There is thus abundant experimental and observational evidence of
com petition between sedentary herbivores on rocky shores. This competition
manifests itself in the form of reduced growth rates, reduced reproductive output,
increased mortality, reduction of niche breadth and exclusion from particular
habitats. With the exception of cases where interference is involved there are,
however, very few instances of competition leading to the local exclusion of one
species by another.
Sessile filter-feeders
It is generally held that exploitative competition for food is unimportant in filter-
feeders. Their food is unpredictable, fluctuates widely in time and space, and its
availability is more a function of water movements than competition between
suspension-feeders. Furthermore, planktonic organisms undergo rapid seasonal
changes and successions so that feeding on a particular prey is unlikely
Fig. 22.—Relationship between Patella cochlear density and per cent cover of the alga
Ralfsia (A) and density of Patella longicosta (which feeds on Ralfsia) (B): the histogram
gives the per cent frequency for P. cochlear densities; (after Branch, 1975a).
Fig. 23.—Relationship between the number of Patella spp. coexisting at any particular
point on the coast of southern Africa, and the mean dietary or habitat (zonational)
specialization of those species (Branch, 1981).
(Levinton, 1972). On the other hand, intense competition for space frequently
occurs between suspension-feeders, often with the consequence that one or a few
species dominate filter-feeding communities. Warwick (1982) has commented on
the instability of such communities, variations in the recruitment of the dominant
species leading to wide fluctuations in numbers. Schoener (1974) has predicted
that organisms with very small prey will seldom segregate their niches in terms of
food type but are more likely to apportion the habitat spatially. Despite these
generalizations, filter-feeders are at times able to eliminate food sufficiently
rapidly and efficiently that competitors are left without any food. As an example,
506 G.M.BRANCH
Reiswig (1971) has described how shallow-water sponges filter the water so
efficiently that they remove almost all suspended particles.
Other authors have sought and found differences in the size-range and nature
of food ingested by suspension- and particle-feeders. For instance, different
species of sponges have ostia of different diameters and oscular papillae of
different lengths, and may ingest particles of different sizes (Hartman, 1957). A
similar argument has been advanced for particlefeeding caprellid amphipods,
which feed at different heights from the substratum or on particles of different
sizes (Caine, 1977). In neither case, however, has competition for food actually
been demonstrated.
In contrast, intense competition for space regularly occurs between sessile
suspension-feeders, frequently leading to the exclusion of the inferior
competitor. The classical and often quoted work by Connell (1961a, b, 1970) on
barnacles still constitutes one of the best examples. Amongst the earliest of
workers to apply critical experiments to test for competition in marine organisms,
Connell (1961a) showed that Balanus balanoides consistently out-competes
Chthamalus stellatus in the mid-shore, smothering, under-cutting or pushing
Chthamalus off the rocks. As a result Chthamalus is limited to a high-shore band
above the tolerance limits of B. balanoides. Experimental removal of B.
balanoides increases the survival of Chthamalus in the mid-shore, where it
achieves a faster growth than in its high-shore refuge. On New Zealand shores
the barnacle Chamaesipho brunnea is similarly restricted to the high-shore by a
combination of competition from other barnacles and predation (Luckens, 1975).
Competition between barnacles may involve more than the mere attainment of
space on a rock face, for crevices, which ensure lower mortality because they
provide greater protection from wave action and physical battering, are often at a
premium (Connell, 1961a).
Mussels are renowned for their competitive ability, often dominating intertidal
and shallow-water communities to the extent that they substantially reduce the
diversity and influence the abundance and zonation patterns of other species.
Interactions between pairs of mussel species have received particular attention.
Suchanek (1978) describes how Mytilus edulis is confined to a band above M.
californianus, its lower limits of zonation being set by competition, although it
can settle in empty patches where M. californianus has been torn free by storms.
In a contrasting observation that is particularly interesting because it is unusual,
Hoshiai (1964) has shown that the upper limits of M. edulis may be set by
competition with a highshore mussel, Septifer virgatus. This remains the only
example where the upper limit of zonation of one filter-feeder is set by
competition with another.
The competitive interactions between Mytilus edulis and M. californianus
have been elucidated in a series of papers by Harger (1968, 1970a, b, c, 1972a, b,
summarized in Harger, 1972c). M. edulis predominates in quiet water and M.
californianus in exposed situations, but there is a substantial area of overlap
between the species. The growth of adult M. edulis is lower in mixed species
clumps and mortality is higher because the faster growing M. californianus has a
stronger shell and outgrows or crushes competitors. Small M. edulis, however,
grow faster in mixed species populations while small M. californianus become
smothered. The competitive superiority of M. californianus in wave-washed areas
is due to its greater powers of attachment, while M. edulis is more mobile and
better able to crawl free of silt in quieter waters where M. californianus is
smothered. Thus extremes of water movement favour one or the other species
and under these conditions single-species populations occur, but recruitment
continues to maintain completely mixed populations under intermediate
conditions. Overlapping niches such as this permit the continued coexistence of
species because neither species can gain ascendency over the other throughout its
entire range. In those parts of the coast where M. californianus is absent, M.
edulis is not confined to sheltered regions but expands to occupy wavebeaten
shores, so that its habitat shifts when one compares coastal areas with and
without M. californianus. This research is all the more valuable because Harger
(1972a, c) was able to show that there are differences in shell shape between
animals from sympatric and allopatric populations which are maintained even
after animals are transplanted between sites, suggesting a genetic basis for the
differences. Furthermore, when M. californianus is removed from wave-beaten
shores, although M. edulis expands to fill some of the area that is left vacant, it is
incapable of totally filling the niche vacated by M. californianus. In these
respects, the mussels conform to the conditions laid down by Connell (1980)
when he stipulated the kinds of responses expected of competitors which coexist
because of differences in their fundamental niches.
Overgrowth of one species by another is a frequent method of competition in
sessile filter-feeders. It occurs commonly in bryozoans, ascidians, and sponges,
but has also been recorded for bivalves, gastropods, tube-forming polychaetes,
barnacles, hydroids, and corals (see for example Rützler, 1965; Gordon, 1972;
Stebbing, 1973a; Karlson, 1978; and a review by Jackson, 1977). Most
organisms die if they are overgrown, but epizoism of sponges regularly occurs
without harm to either of the participants (Rützler, 1970; Sará, 1970). In fact,
some sponges are normally found under other species. They survive by
extending their turrets through the uppermost sponge or by forming channels
between the two, through which feeding and respiratory currents can be drawn.
Vance (1978) has shown that epizoites overgrowing the sessile clam Chama
pellucida decrease the chances of the clam being detected by the predatory
starfish Pisaster gigantea; while the epibionts benefit because Chama grows in
positions where sea-urchin grazing is less likely. Thus, although overgrowth can
lead to competitive exclusion, there are instances where it is beneficial.
Sessile filter-feeders are not restricted to competing with animals at the same
trophic level. For example, the presence of barnacles has a detrimental effect on
the limpet Patella granularis, decreasing its growth rate (and hence mean size)
and its reproductive output (Branch, 1976). This case is complicated by the fact
that P. granularis juveniles survive better in the presence of barnacles, thus
508 G.M.BRANCH
increasing the density of limpets and leading to intraspecific competition. Mean

size and gonad output are also decreased because of this intraspecific
competition, but over and above this barnacles exert their effect on growth and
reproduction (Fig. 24). The barnacles diminish the area over which the limpets may
feed effectively, so that competition is primarily for space.
The limpet Cellana tramoserica suffers reduced recruitment, growth and
survival of juveniles and decline of adult body weight at higher barnacle
densities. In turn, the limpet has an adverse effect on barnacles (see Denley &
Underwood, 1979, and references therein); but its impact on barnacles varies
with circumstances. In the mid-shore, high densities of limpets reduce settling
and increase mortality of newly settled barnacles; but when limpets are absent
the barnacles suffer from intense competition with algae, which smother the
shore if unchecked by grazing. Maximum survival of barnacles thus occurs at
intermediate levels of limpet grazing. Further down the shore, where algae grow
faster, higher densities of limpets are favourable to the barnacles, because the
faster growing algae present a greater competitive threat than the limpets
(Underwood et al., 1983). Petraitis (1983) describes a similar triangle of
competition involving barnacles, Littorina and algae. Interactions between
organisms may thus modify or even reverse competitive relationships.
Competition across trophic boundaries is also revealed by the field experiments
of Denley & Underwood (1979) which show that the barnacles Tesseropora
rosea and Tetraclitella purpurascens are capable of settling and growing in
experimental clearings low on the shore but are soon out-competed by
macroalgae or the polychaete Galeolaria which overgrow the barnacles.
These examples serve to emphasize an important point. Intensity of
competition is not necessarily linked with taxonomic or even trophic similarity
between organisms, contrary to the view espoused by many workers (see Ayala,
1972, and references therein for examples). This is particularly true when space
is the resource being competed for (see Yodzis, 1978).
Competition can be more subtle than the direct overgrowth described above.
Both sponges (Amade, Pesando & Chevolot, 1982) and bryozoans (Al-Ogily &
Knight-Jones, 1977) produce antibiotic compounds which suppress the growth of
micro-organisms and probably reduce settling of larvae on top of their colonies.
Homogenates of various sponges and ascidians are allelopathic and inhibit the
growth of bryozoans. Not all species have this capacity, and in those that do, it is
specific to particular species of Bryozoa. No solitary organisms are affected by
the allelopathic chemicals, an interesting feature, since they represent no
competitive threat to the sponges or ascidians (Jackson & Buss, 1975). Allelo-
chemicals and antibiotics have now been demonstrated in many sponges and
ascidians (Burkholder, 1973; Stoecker, 1980; and a review of sponges in Buss,
1976). Some ascidians have the additional ability to slough off their tunic surface
to shed epibionts and competitors (Jackson, 1977). Green (1977) discusses how
the toxicity of sponges increases towards the equator where predation is more
intense, and is most virulent in species that grow in habitats where they are
Fig. 24.—A, influence of barnacles on the mean length of the limpet Patella granularis at
various densities of the latter; both increased limpet density (intraspecific competition)
and increased barnacle cover (interspecific competition) reduce mean size of the limpets;
B, gonadal output of Patella granularis declines at high limpet densities but is also
reduced by increasing barnacle cover; (Branch, 1976).
exposed to fish predation. The presence of ‘tunic acids’ in ascidians is associated

with a lack of epibionts; but accumulation of vanadium (a metabolic poison) is
not correlated with an ability to avoid overgrowth by epibionts. Both tunic acid
and vanadium, however, do reduce palatability of ascidians to fish. Whether the
same toxins serve as an all-purpose defence against predators as well as
achieving immunity to overgrowth by specific competitors is not known.
While contact between bryozoan colonies may result in overgrowth, it can also
cause a redirection of growth, so that overgrowth is avoided and a ‘stand-off’
develops at the point of contact. This situation is promoted in many bryozoans by
an elevation of the edge of the colony at the point of contact, or by the erection
510 G.M.BRANCH
of a barrier of spines or an increase in the number of avicularia—all making

overgrowth more difficult (Gordon, 1972; Stebbing, 1973b). Sponges may
produce additional and unusually long spicules and sessile predators such as
hydroids, anemones, and corals generate additional tentacles and nematocysts to
avoid overgrowth (as described above, p. 465). Karlson (1978, 1980) proposes
that different degrees of competition will select for different responses to the
threat of overgrowth. In intensively competitive situations where space is very
limited, the ability to overgrow other organisms is of paramount importance. But
where disturbance is more frequent, thus making space available and reducing
competition, selection will favour mechanisms promoting ‘stand-offs’, for the
colonies can without detriment simply redirect their growth upon contact.
One particularly interesting adaptation reducing overgrowth is the aggregate
settling of the upright bryozoan Bugula turrita. Despite intra-specific
competition, which reduces the growth rate of B. turrita, it pays the organism to
settle gregariously because groups are able to resist overgrowth by a common
coexistent competitor, Schizoporella (Buss, 1981). This is a clear example of the
rival forces of intra- and interspecific competition, the balance between the two
determining whether selection will favour group-living or not.
Sessile epibiotic animals growing on algae have received considerable
attention (reviewed by Seed & O’Connor, 1981). In part, their coexistence is
achieved by differential zonation along the fronds, by selection of opposite faces
of the frond, or by selective occurrence on different parts of the plant (Ryland,
1974; O’Connor, Seed & Boaden, 1979, 1980; Bernstein & Jung, 1979). Despite
this, there is sufficient overlap for competition to occur (Stebbing, 1973a, b;
O’Connor, Boaden & Seed, 1975). In general terms it is possible to rank the species
in a competitive hierarchy, but very seldom does any one species achieve total
ascendancy over all the other competitors (Wood & Seed, 1980). In several cases
habitat shift of one or both competitors takes place when they occur on the same
plant. For example, the ascidian Didemnum normally occurs basally on the alga
Fucus serratus, but is displaced distally when it coexists with the sponge Scypha
compressa; similarly, Polyclinum is displaced along the fronds by Didemnum,
while the numbers of the latter are reduced (Boaden, O’Connor & Seed, 1976).
Unfortunately, all these shifts are clouded by the complication that samples of
sympatric and allopatric populations were collected in different localities, so that
the possibility of environmental induction of the habitat shifts cannot be
discounted. O’Connor et al. (1975) have tested whether niche width in four
bryozoans (as measured by the range of segments that they occupy on the algae
Fucus serratus) changes in the face of competition. They demonstrated that as
density rises the range of segments that are occupied increases, i.e. niche breadth
increases in response to increased intraspecific competition. On the contrary, the
niche breadths for each of the four species decreased in the presence of other
species, shrinking in response to interspecific competition.
A particularly detailed analysis of interactions between various epibiotic
species that grow on Macrocystis (Bernstein & Jung, 1979) has uncovered
remarkable interaction and co-evolution between the species. Membranipora, the

commonest species on young fronds, is dominant over two other bryozoans,
Hippothoa and Lichenopora, and over the polychaete Spirorbis, mainly because
of its rapid and indeterminate growth. It does not, however, occupy the fronds of
Macrocystis perennially. During summer its larvae lose their normally
photopositive response and settle on another alga, Pterygophora, which grows on
the sea floor beneath the Macrocystis canopy. Furthermore, even in winter it is
not spread uniformly through the kelp beds, but occurs predominantly on the
outer, seaward, edge of the beds. This latter effect is partly due to the circulation
of water through the kelp beds, the kelp plants filtering out settling larvae on the
seaward edge; when offered a choice, the larvae themselves preferentially select
plants that have grown on the outer edge of the kelp bed. During winter the
larvae of the subordinate species settle preferentially on the plants that grow on
the inner edge of the kelp bed and on older blades—thus minimizing competition
with Membranipora. During summer the subordinates expand their range to
occupy the younger upper parts of Macrocystis, filling the habitat left vacant by
the movement of Membranipora to other algae. This niche expansion is brought
about by the abolishment or even reversal of the normal larval preferences for
older fronds. Furthermore, one of the subordinates, Spirorbis, occupies
Pterygophora during winter (when Membranipora is associated with
Macrocystis) but settles on Macrocystis in summer.
Thus, the niches occupied by Membranipora and its subordinates are
complementary to a remarkable degree, and remain so, despite seasonal changes
in the preferences of all the species involved. The subordinates compete little
between themselves, for while Spirorbis and Lichenopora settle in the troughs
that ripple across the blades of Macrocystis, Hippothoa selects the ridges, and
this distinction is maintained throughout life. Spirorbis, a small solitary animal,
presents no threat to Lichenopora. It, in turn, may overgrow Spirorbis, but the
polychaete can re-orientate its tube to keep the mouth free from the bryozoan,
and thus suffers minimally. This well-documented analysis is one of only a few
in which the complementary niches of competitors can convincingly be
explained as the outcome of coevolution, the subordinate species developing
adaptations which minimize the competitive impact of the superior competitor.
Despite the dominant rôle of direct interference (overgrowth) in competition
between sessile filter-feeders, we cannot assume that competition for Q food is
unimportant. While it is unlikely to be the major means whereby one species
excludes another, it can tip the balance between species. This situation occurs in
two encrusting bryozoans, Onchoporella and Antropora (Buss, 1979a).
Onchoporella is fractionally taller than Antropora (900 μ m compared with
600μ m) but this is sufficient for its tentacles to overreach those of Antropora and
create a ‘feeding shadow’. As a consequence when the two colonies meet, the
growth of Antropora is slowed. Antropora normally grows faster than
Onchoporella, but at the point of contact Onchoporella grows faster and is,
512 G.M.BRANCH
therefore, able to overgrow the other species. Thus, competition for food and
space are inter-dependent.
Since size plays a major rôle in determining whether an animal is overgrown or
not, growth rate can be important. As an example, the compound ascidian
Aplidium pallidum overgrows the alcyonacean Alcyonium siderium when it is
small but once the latter achieves a diameter of 16mm it is immune to
overgrowth by the ascidian. This escape in size can only be achieved if growth is
fast enough and, once again, this is influenced by food availability (Sebens, 1982).
Many sessile suspension-feeders are colonial, and Jackson (1977) and Buss
(1979b) have drawn attention to the predominance of colonial forms amongst the
subtidal fauna. A number of characteristics make colonial organisms superior
competitors for space. Their growth is indeterminate, allowing them to occupy
space throughout their lives by lateral expansion; the growth rate of colonies also
increases exponentially throughout their lives while that of solitary animals
decreases exponentially. Both features make it more likely that colonies will
overgrow solitary organisms than vice versa. Colonial organisms are also more
successful at preventing overgrowth and larval settling on their surfaces. If they
are attacked by a predator, regrowth of the colony can take place from fragments
that are left, while solitary organisms are likely to be killed by the attack.
Colonial forms have an indeterminate reproductive output, so that they can
colonize newly-available surfaces more easily than solitary forms which often
have clearly defined annual reproductive periods.
Despite all these advantages, colonial forms fail to dominate the intertidal
zone in the same way they do in the subtidal. Mussels, barnacles, tube-worms,
oysters, anemones, and solitary ascidians replace colonial organisms in the
intertidal. Although solitary, many of these aggregate or even form tightly bound
units, some becoming fused together; in the case of anemones they can divide to
form clones. Presumably the physiological stress is too great in the intertidal
zone for truly colonial organisms to exist there. The solitary forms all possess
protective external coverings in the form of shells, tests or tubes. Some intertidal
anemones cover their bodies with sand grains and shell fragments to reduce
water loss. The zoanthids, which are the only colonial organisms to have
successfully occupied the intertidal, may also embed sand grains in their tissues.
Thus solitary (but often aggregating) sessile species, because of their superior
tolerance to physical stress, dominate the intertidal; but in the subtidal zone they
are replaced by colonial forms which are competitively superior.
This summary of competitive reactions between sessile suspensionfeeders
serves to emphasize that competition for space is an important force. In some
cases it is a dominant force structuring communities but, in other instances, field
experiments such as those by Dayton (1971), Paine (1971, 1974), and Menge
(1976) have uncovered different interactions.
Working on New England rocky shores, which are dominated by Balanus
balanoides at high levels and Mytilus edulis in the midshore, Menge, (1976) used
cages to exclude or include various predators or competitors from experimental
Fig. 25.—Recruitment of Balanus balanoides and Mytilus edulis to experimentally

cleared sites on a New England rocky intertidal shore: the control was left to develop
naturally; “roof”, excluded only large predators such as Pisaster; “exclusion”, excluded
the predator Thais; A, high shore; B, mid-shore, exposed to wave action; C, mid-shore,
sheltered site; (after Menge, 1976).
plots which had previously been cleared of all organisms. In this way the
influence of any particular organism on the settling or survival of Mytilus or
Balanus could be analysed. In the high shore (Fig. 25A), only Balanus could
tolerate the harsh conditions and became the dominant. In this situation physical
conditions alone dictated the structure of the community. In midshore areas
which were exposed to strong wave action (Fig. 25B) initially Balanus colonized
bare spaces, but was soon overgrown by Mytilus. Only if Mytilus was
experimentally removed did Balanus survive. The absence of any difference
between control sites and sites where predators were excluded suggests that
predation had little effect in this community which was primarily ordered by
competition between the two dominant filter-feeders.
At sheltered midtidal levels the experimental sites developed differently
(Fig. 25C). Predators played a far more important rôle, by reducing the number of
Mytilus to the point where Balanus could coexist with Mytilus. Under these
conditions exclusion of predatory snails and starfish again resulted in a
monopolization of space by Mytilus. If the predators and Mytilus were removed
then Balanus again comprised the solitary dominant. Comparable work by
Dayton (1971) has shown that competitive elimination of Chthamalus dalli by
Balanus glandula is also prevented by Thais which preferentially preys on B.
glandula. In these cases predation regulates the nature of the community,
preventing one competitor from monopolizing the area. Like Menge (1976),
Peterson (1979a) was able to show that on exposed shores competition between
filter-feeders is a predominant feature, predators being excluded by the wave
514 G.M.BRANCH
action. Here, the mid- and low shore are almost completely covered by mussels,
and the high shore by barnacles. In more sheltered areas, predators become more
effective and competition less intense: as a result, the communities are more
diverse.
The rôle of predators has been highlighted by Paine (1974). After removal of
Pisaster ochraceus he demonstrated a downward expansion of the range of
Mytilus edulis, with a consequent decrease in the diversity of the community.
Similar monopoly by Perna canaliculatus followed removal of the starfish
Stichaster australis (Paine, 1971). These results suggest that predation may
increase community diversity by preventing competitive exclusion and thus
relegate competition to having a minor rôle in structuring communities. Whether
this is a general phenomenon or one specific to certain situations or animals still
needs to be established, as discussed further in the concluding section of this
review.
Marine algae
Plants are often regarded as being qualitatively different from animals, because
they require only four basic resources—light, water, carbon dioxide, and
nutrients—seemingly discreet entities that cannot be par titioned among
competing species (see Begon & Mortimer, 1982). This view is, however,
oversimplified.
Light, for example, alters as it passes through water, different wavelengths
being filtered out differentially and blue-green light penetrating furthest. Certain
algal groups have evolved auxiliary pigments (such as fucoxanthins in brown algae
and phycobilins in red algae) which enable the algae to absorb light of different
wavelengths at different depths. Red algae tend to predominate in deeper waters
where they can make use of blue-green light that other algae cannot absorb. That
auxiliary pigments were evolved as a response to competition in shallower
waters is pure speculation, but the possibility of partitioning light by wavelength
is clearly a potential means of reducing competition.
A more concrete example concerns nutrients. Titman (1976) has elegantly
demonstrated a partitioning of nutrients between two planktonic algae,
Asterionella formosa and Cyclotella meneghiniana. Both are potentially limited
by phosphate and silicate, Asterionella being limited by phosphate at ratios of
silicate:phosphate exceeding 97, and by silicate at lower ratios; Cyclotella is
more usually limited by phosphate, only becoming limited by silicate at ratios
below 5·6. As a result, there exists a wide range of nutrient ratios over which the
two algae are limited by different nutrients and can coexist. Only above ratios of
97, or below 5·6, do they compete, one species excluding the other (Fig. 26).
Despite these examples, space is the resource most often competed for by
benthic algae, and in numerous instances the abundance, zonation and
distribution of algae have been shown to be controlled by competition for space.
As an example, the factors controlling fucoid zonation on Scottish shores have
Fig. 26.—Coexistence and competition between two species of phytoplankton,

Asterionella and Cyclotella, in relation to nutrient ratios (modified from Titman, 1976).
been discussed by Schonbeck & Norton (1978). Four clearly defined bands of
algae develop on these shores, Pelvetia canaliculata highest, followed by Fucus
spiralis, then a mixed band of F. vesciculosus and Ascophyllum nodosum, and
finally a lowermost zone of F. serratus. With the exception of Ascophyllum
nodosum (which may be distasteful to grazers and thus have other attributes
allowing it to live with Fucus vesciculosus), the growth rates of the species
progressively increase from the high-shore Pelvetia to the low-shore Fucus
serratus. The implication behind this is that the species occurring lowest on the
shore is the best competitor and thus prevents the next highest species from
extending further down the shore. Schonbeck & Norton did not test this
hypothesis for all the species but they did show that experimental elimination of
strips of F. spiralis allowed Pelvetia canaliculata to extend down the shore, and
that if P. canaliculata and Fucus spiralis were transplanted to experimentally
cleared patches lower on the shore than they normally occur, they thrive there
and can grow faster than in their normal zones. Clearly each alga is limited to
how far down the shore it occurs by competition from lower-shore faster-
growing competitors.
A comparable example is the restriction of down-shore colonization of two
Laminaria spp. by Chondrus crispus in New England (Lubchenco, 1980). Further
north, where Chondrus is heavily grazed by limpets or scoured by ice, its
abundance is reduced, and here Fucus serratus coexists with it low on the shore.
Chondrus has two competitive advantages over Fucus serratus. First, it seems to
inhibit the settling and development of Fucus sporelings (although, once
established, adult Fucus can survive in mixed stands with Chondrus); and
secondly, it develops an extensive crustal covering on the rocks, which can
survive grazing and overgrowth by other algae, and can perennate at any stage to
allow rapid recolonization.
516 G.M.BRANCH
Dayton (1975b) has shown that the removal of one dominant intertidal alga,
Hedophyllum sessile, allows opportunistic ‘fugitive’ species to colonize zones
where they are normally rare but, at the same time, the obligate understorey flora
that normally lives beneath Hedophyllum disappears once deprived of this alga.
Other cases where competition between species of algae restricts abundance or
sets limits to zonation are described by Hruby (1976), Emerson & Zedler (1978),
Sousa (1978a, b), Hodgson (1980) and Montalva & Santelices (1981). The
competitive dominance of one species, Codium dimorphum, fluctuates
seasonally, at least in Chile, where summer bleaching of this algae coupled with
grazing of bleached plants allows other species which are normally confined to
the high shore to penetrate the low shore during hotter months, only to be
displaced by regrowth of the Codium in autumn and winter (Santelices, Montalva
& Oliger, 1981).
In the subtidal zone, overshading by dominant algae such as Macrocystis may
reduce algal diversity (Foster, 1975). It is not, however, the obviously large
plants which necessarily dominate. By manipulating the densities of various
species Dayton (1975a) showed that the largest of the offshore algae, Alaria fistula,
is a fugitive and is competitively inferior to Laminaria spp., and even to the low-
growing red algae, Agarum spp. The latter species are also subordinate to
Laminaria spp. Amongst the Laminaria spp., L. longipes seems to have an
advantage over its congeners in areas where disturbance is high because its
extensive rhizoidal holdfast allows rapid regeneration after the uppermost
sections of the plant have been torn away in storms; its lower canopy may,
however, place it at a disadvantage in quiet waters where disturbance is
infrequent.
A different form of competition may occur between algae and sessile animals.
Colonial animals overgrow slow-growing perennial plants, while algae may
smother barnacles (see Underwood et al., 1983, and references therein) or
prevent the settling of spat or survival of adults by whiplash of the fronds
(Menge, 1976; Grant, 1977). Jackson (1977) suggests this action may favour
solitary encased animals over soft-bodied colonial forms. Velimirov & Griffiths
(1979) have shown the importance of whiplash in the establishment of clumps of
Laminaria pallida. Adult plants clear a swathe around them, excluding grazers
and filter-feeders and allowing kelp sporelings to settle and establish.
Allelopathy has been demonstrated in several benthic macroalgae and in both
benthic and planktonic microalgae. Ralfsia is amongst several algae which have
an antagonistic effect on other algae in cultures, and inhibits epibiotic organisms
from settling on it (Russell & Fielding, 1974; Fletcher, 1975). Exudates from
Ascophyllum nodosum have an antibiotic effect and suppress growth of the
zoospores of Laminaria hyperborea (Walker & Smith, 1948) and may contribute
to the success of Ascophyllum nodosum on fucoid-dominated shores (see above).
Laminaria and Himanthalia produce antibiotics, but this ability is limited to the
photosynthesizing tissues. Thus, epiphytic organisms are largely restricted to the
non-photosynthesizing tissues of both species (Al-Ogily & Knight-Jones, 1977).
In culture, the crustose germlings of Chondrus crispus can totally prevent the
development of diatoms in their vicinity, although the sporelings of Gigartina
stellata lack this ability (Khfaji & Boney, 1979).
In several instances diatoms and dinoflagellates have proved to inhibit the
growth of other species of phytoplankton in cultures (e.g.. Kayser, 1979; Sharp,
Underhill & Hughes, 1979) but Chan, Anderson, Le Blanc & Harrison (1980)
have questioned that this inhibition is due solely to allelotoxins, pointing out that
nutrient depletion may have contributed to the results. To overcome this problem,
they grew plates of diatoms and subjected them to extracts from various
phytoplankton to test for the effect of allelotoxins. Six out of six diatoms and four
out of five dinoflagellates proved to have either intracellular or extracellular
compounds suppressing the growth of the plated diatoms, but Chan et al. caution
against extrapolating these results to field conditions. This reservation is a valid
one and applies to all the above examples. There is an urgent need to test the rôle
of allelotoxins in the field or at least under more realistic conditions than are
possible in cultures.
The impact that grazers have on algae and, in particular, on competition
between algae, will depend on the mode of grazing, the selectivity of the grazer,
the relative size of the grazer and alga, and on the competitive ability of the algae
attacked. Recent reviews summarize grazer-algal interactions (Branch, 1981 on
limpets; Lubchenco & Gaines, 1981; Gaines & Lubchenco, 1982; Hawkins &
Hartnoll, 1983). The effect that grazers have on algal diversity is illustrated by
Lubchenco’s (1978) analysis of the impact of Littorina littorea. In tide-pools
Littorina preferentially feeds on Enteromorpha intestinalis, the competitive
dominant, reducing it and allowing a perennial red alga, Chondrus chrispus, and
several ephemeral algae to coexist with it. A plot of algal diversity against
Littorina density reveals maximum diversity at intermediate densities,
presumably because Enteromorpha dominates and competitively excludes other
species when grazing is limited, while with intense grazing many of the algae are
eliminated by the Littorina. The relationship between Littorina and
Enteromorpha is complicated by the fact that the crab Carcinus maenas is more
abundant in pools canopied by Enteromorpha (sheltered there from attacks by
gulls) and eliminates Littorina. Thus Enteromorpha-dominated pools tend to
persist.
On emergent rocks which dry out at low tide the competitive dominance of
algae changes and Fucus spp., Ascophyllum nodosum, and Chondrus crispus are
competitively superior to most other algae. Since these species are least preferred
by Littorina, the snail concentrates on the subordinate ephemeral algae.
Consequently, its effect here is to reduce diversity of algae in direct proportion to
its abundance. Thus, depending on whether a grazer preferentially attacks algae
that are competitively dominant or subordinate, it will, respectively, increase or
decrease the chance of algal competitors coexisting—a result forecast by Paine
(1969).
518 G.M.BRANCH
Other grazers capable of either increasing or decreasing algal diversity are the
urchins Strongylocentrotus spp. (Paine & Vadas, 1969). In areas where these
urchins are rare, Chondrus reigns as the dominant, reducing species diversity,
but where the urchins are common they can increase diversity by eliminating
species that otherwise monopolize space (Lubchenco & Menge, 1978). Algae
such as Agarum spp. which are subordinate but distasteful to urchins may thrive
where Laminaria spp. are controlled by urchins (Dayton, 1975a). On the other
hand, high densities of urchins often eliminate most algae, leaving only “the
barrens” of encrusting corallines (Paine & Vadas, 1969; Shepherd, 1973a; Lang
& Mann, 1976; Mann, 1977; Ayling, 1981). The impact of urchins and other
grazers on algal diversity is partly because they may feed on competitively
dominant species, but in some areas they increase diversity by non-selectively
grazing in random patches, thus promoting patchiness (e.g. Paine & Vadas,
1969; Sousa, 1979a).
Limpets which are indiscriminate microalgal grazers depress the diversity of
diatoms (Nicotri, 1977) or reduce macroalgal diversity by eliminating sporelings
before they can establish themselves (see Hawkins & Hartnoll, 1983, for
examples). A few limpets actively maintain specific algae in their territories
(Stimson, 1970, 1973; Branch, 1975b, 1976). Patella longicosta, for instance,
grazes away other algae that grow at the perimeter of its territory, thus
preventing the competitive elimination of the encrusting Ralfsia expansa that
comprises its ‘garden’ (Branch, 1976). Some algae seem largely dependent on
the activities of grazers, and Steneck (1982; see also Paine, 1980) has produced
clear evidence that at least one encrusting coralline has co-evolved with grazers.
In the absence of grazing by limpets and chitons, Clathromorphum is killed by
epiphytic algae and diatoms. Encrusting corallines have even been shown to
release chemicals which induce Haliotis larvae to settle on them (Morse,
Hooker, Duncan & Jensen, 1979), and the chiton Tonicella lineata is known to
settle preferentially on coralline crusts (Barnes & Gonor, 1973).
Herbivorous fish appear to decrease both algal biomass and diversity
(Stephenson & Searles, 1960; Day, 1977) although intermediate levels of grazing
by scarids is associated with maximum algal diversity (Brock, 1979) and
diversity of algae is higher inside pomacentrid territories—mainly because of
protection against more voracious herbivores (Brawley & Adey, 1977). Until
recently, large herbivores such as the sea cow (Hydrodamalis gigas) must have had
a substantial impact on algal beds, and Dayton (1975a) has speculated that in the
near absence of these animals in modern times substantially different competitive
interactions may now be taking place.
Hay (1981) has investigated why some algal species form tightly-packed turfs.
These mixed turfs have lower productivity than individual plants, photosynthesis
being much reduced in the lower layers of the turf due to shading. Balanced
against this, turfs are more resistant to desiccation and to grazing, and they occur
in areas where heavy grazing or physical stress exclude more productive solitary
species that would otherwise out-compete them. Lubchenco & Gaines (1981)
have postulated that competitive ability in algae (which they link with growth
rate) is inversely related to the ability to resist grazing. If this is true, then grazers
may promote succession and diversity by preferentially eliminating the fast-
growing early colonizers, allowing other species to become established. Several
papers testify to this effect (Jones & Kain, 1967; John & Pople, 1973; Vadas,
1977; Estes, Smith & Palmisano, 1978; Lubchenco, 1978), but in some instances
preference is shown by herbivores for late successional species (Sousa, Schroeter
& Gaines, 1981, cited in Lubchenco & Gaines, 1981).
The algal succession studied by Sousa (1979a, b; and see review of successional
mechanisms by Connell & Slatyer, 1977) on boulder fields is particularly
instructive in terms of competitive interactions between algae at different stages
of succession. On stable boulders there is a predictable succession, Ulva being
first to colonize, then a group of perennial red algae, and finally Gigartina
canaliculata forming a persistent climax. Maximum diversity occurs on boulders
of intermediate size, not so small that regular disturbance prevents colonization
of most species, and not so large that succession proceeds to a climax in which
competitive exclusion eliminates most species (Sousa, 1979a). Areas in which
seals haul-out yield similar results (Boal, 1980), primary colonizers and tough
compact algae being the only species to grow where haul-out activities are
intense. Some species are actually more common in areas where hauling-out
occurs, presumably because the disturbance prevents dominance of species
which would normally exclude these algae. The traditional explanation of
Sousa’s results has been that algae developing later in the succession are superior
competitors and slowly replace earlier less dominant species. Sousa has shown
that this is not the case. In fact, the early colonizer Ulva inhibits the red algae,
and it is only due to grazing of Ulva by the crab Pachygrapsus crassipes that
patches are created in which the red algae settle. The secondary colonizers also
inhibit development of the climax species, Gigartina canaliculata, but they are
more susceptible to desiccation and overgrowth by epiphytes, and so they are
eventually replaced by the climax species. Clearly the earlier colonizers are not
replaced because they are inferior competitors but because of their greater
vulnerability to grazing or physical stress (Sousa, 1979b). Once Gigartina is
established it can maintain itself and hold space, preventing the invasion of other
algae, but only at this stage is it competitively superior. The way it attains space
in the first place has little to do with the relative competitive abilities of the
various species. Ulva is not displaced primarily by competition, as Northcroft
(1948) pointed out earlier.
It is thus evident that marine algae, far from being different from animals, bare
striking similarities to sessile animals, particularly colonial forms. Their asexual
and largely indeterminate growth allows expansion across rocks and promotes
the ability to overgrow other organisms; they produce allelotoxins to suppress
competitors; they normally compete for space; and their competition can be
alleviated by grazers or physical disturbance much in the same way that
predators may permit coexistence of competing sessile animals. In terms of
520 G.M.BRANCH
competitive mechanisms and abilities, the two groups of organisms share more
common features than they have differences between them.
The fauna of soft sediments

Three assumptions are often made about the fauna inhabiting soft sediments:
first, that they are not short of food (e.g. Woodin & Jackson, 1979); secondly,
that because most of the infauna is made up of deposit-feeders they are incapable
of selective ingestion and, hence, of partitioning food resources; and finally that
space is not limiting. None of these assumptions is entirely true.
With respect to the availability of food, Levinton (1979) has argued that food
is often short, and points to the correlations between density and levels of food,
and between diversity and food availability (see also Whitlatch, 1980, 1981). In
support of this, there are several experimentally proved cases of resource
depression in soft sediments (e.g. Striven & Kuenzler, 1979; Branch & Branch,
1980b), and Tenore (1977) has shown that while the absolute amount of organic
detritus in sediments often seems superabundant, much of this potential food
source is inadequate because of its low nitrogen content. Levinton (1979) has
also pointed to the niche divergence between the food requirements of coexisting
species as an indication that food is short. This is, of course, a circular argument,
for differences in food requirements do not necessarily prove that competition is
taking place or has caused the divergence. Nevertheless, it is a pointer.
It is true that in soft sediments space is not competed for with the same
intensity that it is on hard substrata, and that food is more constantly and
predictably available than it is for filter-feeders. On purely theoretically grounds,
Levinton (1972) has argued that these two factors promote diversity and stability
in soft-bottom communities, and subsequent work has yielded data supporting
these contentions (see Warwick, 1982, for a summary). Furthermore, at higher
trophic levels—for instance fish and shrimps feeding on the fauna of sediments—
analyses of the production of food indicate that food is never short (Evans, 1983).
On the other hand, there are several cases in which competition appears to take
place. For instance, Peterson (1977), in comparing the vertical stratification of
organisms in a Californian lagoon, found that only the species that overlap
vertically (Fig. 27A) have any adverse effect on one another. The numbers of the
sand prawn Callianassa californiensis and the bivalve Sanguinolaria nuttallii are
negatively correlated (Fig. 27B) suggesting that one normally displaces the
other. Peterson analysed the vertical distribution of species in an area where
Callianassa has been removed by human exploitation and found that Tagelus and
Sanguinolaria had increased in abundance, filling the niche vacated by
Callianassa. Furthermore, after experimental elimination of Callianassa,
recruitment of Sanguinolaria and Dendraster increased markedly although other
species were unaffected. Peterson suggests that this community is structured
largely by competitive interactions, resulting in a vertical stratification.
Fig. 27.—A, depth stratification of the dominant species in a sandy lagoon; B,

Callianassa californiensis and Sanguinolaria nuttallii are the only species sharing the
same depth range and their numbers are negatively correlated, suggesting competitive
exclusion of one by the other; (after Peterson, 1977).
Levinton (1977) has described competition between three bivalves, Nucula

proxima, Yoldia limatula, and Solenomya velum, in which direct interference,
exploitation of food and sediment re-working all play a rôle. As a consequence
of this, the distribution of two of the species, Nucula and Yoldia, is largely
mutually exclusive. The tube-building polychaete Axiothella rubrocincta reduces
the numbers of spionid polychaetes which coexist with it. Axiothella places
heavy demands on organic-mineral aggregates as a food source and competes
with the spionids for these. In areas where the aggregates are abundant, it has no
effect on the spionids, but where they are limiting Axiothella has an adverse
effect on the worms, decreasing their density, survival, and larval recruitment.
The mechanism of competition is an interesting one, particularly in the manner it
applies to the spionid Pseudopolydora paucibranchiata. When Axiothella
reduces the organic-mineral aggregates, Pseudopolydora is forced to reach far
from its tube to glean the aggregates, and in doing so it falls ready prey to
flatfish. Thus competition is supplemented by predation in bringing about the
decline of Pseudopolydora (Weinberg, 1979).
The numbers of another spionid, Pygiospio elegans are negatively correlated
with those of Pseudopolydora kempi, which led Wilson (1983) to suspect
competition between the two species. In areas of sympatry in the field, Pygiospio
is more likely to have a conspecific as a neighbour than a Pseudopolydora—
more often than expected by chance—suggesting an avoidance of
Pseudopolydora. In the laboratory Pseudopolydora decreases the survival of
Pygiospio, inhibits its reproduction and increases its rate of emigration. Despite
this convincing evidence of competition, when Wilson manipulated the densities
of the two species in the field with the object of testing for density-dependent
competition, neither of the species had any influence on the other, although both
converged on ambient densities. The lack of density-dependent competition may
have been because water movements in the field supply adequate food for both
species, or because the avoidance reaction of Pygiospio is sufficient to minimize
contact with Pseudopolydora.
522 G.M.BRANCH
The colonization of disturbed sediments by opportunistic species has long

been held to reflect competitive interactions: the opportunists only being able to
colonize an area once the established fauna of superior competitors is eliminated,
and later being replaced by the return of these competitive dominants. In fact,
such changes need not necessarily be due to a release from interspecific
competition, but may be a direct response by opportunistic species to resources
that are made available by disturbance (see Thistle, 1981, for a review). For
instance, experimental organic enrichment of sediments often allows
opportunistic forms, such as the polychaetes Capitella capitata and Strebliospio
benedicti, to invade an area (Young & Young, 1978), suggesting that these
species thrive only where organic matter is present in high concentrations. Such
concentrations are often the result of disturbance, but their subsequent depletion
(and the associated decline in the numbers of opportunistic species) seems to be
due to the opportunists themselves, rather than to other species. Intraspecific
competition thus appears to be of more importance than interspecific interactions
in explaining the disappearance of opportunistic species (Peterson, 1979b).
A clear example of the influence of disturbance per se, unrelated to
competition, comes from the work of Van Blaricom (1982) on the feeding
activities of rays. When they shuffle into the sediments to feed, rays create pits.
Early invaders of these disturbed areas are mobile swimming species such as
tanaid and amphipod crustaceans, which aggregate in pits to feed on the organic
debris that collects there. The use of simulated feeding pits, housing a normal
fauna, and of filled-in defaunated pits allowed Van Blaricom to separate the
effects of competition and accumulation of organics and leaves no doubt that the
presence or absence of potentially competing infaunal organisms has no effect on
these opportunists, which are responding solely to the organic matter in the pits.
Similarly, Thistle (1980) has described how two harpacticoid copepods are
specifically associated with the faecal casts of acorn worms.
One could argue that these examples are unusual in that feeding pits and
faecal casts are temporary phenomena, too short-lived to allow interspecific
competition to enter the picture, but large-scale disturbances also allow access to
resources that are not normally available. Mass mortalities following red tides
(Dauer & Simon, 1976a, b), catastrophic low salinities due to storms (Boesch,
Diez & Virnstein, 1976), and pollution (see reviews by Pearson & Rosenberg,
1978; Gray, 1979) all lead to an enrichment of the sediments as a consequence of
the death of benthos. Even the experimentally defaunated cores of sediment that
have been used to test for the effects of competition or to measure rates of
recolonization (Grassle & Grassle, 1974; Grassle, 1977; McCall, 1977) are
organically enriched by the bodies of the dead animals in the sediment. This is an
inevitable consequence of defaunating the sediment by freezing it—leaving the
dead organisms to rot in the cores. Thus, in each of these cases, colonization of
defaunated areas by opportunists need not reflect competitive release but rather a
response to the provision of a new resource—high organic concentrations.
Reviewing the subject, Thistle (1981) suggests that opportunists appear because
disturbance makes organic material available, and disappear when it is exhausted

—and that intraspecific depletion of the resource, or depletion by physical
factors, are more important in this process than interspecific competition. Thus,
it is still not clear whether “the mere relaxation of competition for background
resources” (Thistle, 1981, p. 227) is important or not, and future experiments
should be designed to distinguish between competitive release and the simple
provision of a resource independent of interspecific competition.
The clearest examples of competition in soft sediments involve direct
interference. For instance, Pseudopolydora paucibranchiata is territorial, and by
means of palp-fighting and biting prevents other spionids from living near to it
(L.A.Levin, 1981). Other spionids are known to pull different species out of their
tubes if they build their tubes within reach (Whitlatch, 1976). Streblospio
benedicti shifts its tube to avoid interacting with Paraspionospio pinnata (Dauer,
Maybury & Ewing, 1981). Nereid polychaetes react aggressively to other nereids
(Reish & Alosi, 1968; Woodin, 1974), the intensity of fighting being greater in
intrageneric than in intergeneric contests, but least in intraspecific meetings
(Evans, 1973). Interactions of this kind may lead to the local exclusion of one
species by another, resulting in horizontal partitioning, one species dominating in
one area, the other in a different area.
This pattern is even more obvious in species which fight aggressively. One
case involves the grass shrimps Palaemonetes vulgaris and P. pugio which occur
in estuaries where both feed on detritus. When alone they prefer shelly substrata
to mud, as the shell offers a refuge from predation by fishes (Thorp, 1976). When
the two occur together P. vulgaris interfers with P. pugio, snapping at it and
displacing it onto muddy substrata. In experimentally mixed populations which
were subject to predation by Fundulus, Palaemonetes pugio suffered higher
mortality than when it was alone. Thus interference competition results in a
spatial partitioning of the environment, which in turn reduces the energy used in
agonistic interaction but forces P. pugio into a sub-optimal area where mortality
from predation is higher.
In a similar manner, Palaemon floridanus aggressively excludes Palaemonetes
vulgaris from red algae, forcing it to occupy the less preferred sea-grass beds,
and thus depriving it of optimal cover and exposing it to greater predation (Coen,
Heck & Abele, 1981). The freshwater crayfish Orconectes virilis aggressively
displaces O. immunis from the mutually preferred pebble substratum of fast-
flowing streams (where crevices provide shelter from predators and turbulent
waterflow), compelling it to live in stagnant ponds (Bovbjerg, 1970). Mantis
shrimps are particularly ferocious in their defence of burrows (see above in
relation to intraspecific competition): Cloridopsis scorpio dominates
Oratosquilla inornata and can exclude it completely from mud and sandbanks
when abundant (Dingle & Caldwell, 1975); and Haptosquilla glyptocercus—
despite its smaller size—prevents Gonodactylus incipiens from living in coral
rubble and compels it to occupy an adjacent refuge in a nearby habitat where
Haptosquilla is rare (Dingle, Highsmith, Evans & Caldwell, 1973).
524 G.M.BRANCH
In an equivalent interaction involving crabs, Pachygrapsus crassipes not only

displaces Hemigrapsus oregonensis from the high shore, but it takes over the
burrows dug by Hemigrapsus and does not dig its own holes. Hemigrapsus has a
wide tolerance of physical factors and thus has refuges beyond the habitat
occupied by Pachygrapsus, but the width of its zonation is reduced when the two
live together (Willason, 1981). Jeffries (1966) has suggested that two Cancer spp.
continue to coexist because they partition the estaurine environment by their
different substratum preferences, but produces no evidence that they do in fact
compete.
A common pattern occurs in these examples of aggressive domination. In each
case the species compete for shelter, and one of the species dominates the other
by an interference interaction, restricting the weaker competitor to a less
preferred habitat, where it survives because the dominant species does not occur
there. The dominant thus has a narrower niche which is included in the broader
niche of the weaker competitor. Such a system is costly for the dominant in
terms of energy expended on agonistic reactions and costly for the weaker
species because it foregoes its optimal habitat. The interac tion can only be
maintained if the dominant benefits sufficiently to offset its costs.
It is possible that deposit-feeders which require similar kinds of food may
coexist if their needs are sufficiently different. Such differences are usually
detectable. Holothurians ingest particles of different sizes and organic content
(Sloan, 1979b), differences that can be correlated with the size and structure of
tentacular nodules (Roberts, 1979). Coexistent polychaetes from the continental
shelf of Texas almost all feed on different kinds of food (Flint & Rabalais,
1980). But what significance these differences have in permitting coexistence
remains unknown. Flint & Rabalais even found two coexistent species that were
so similar in their trophic requirements and habitats that they were ecologically
inseparable, and they comment that there “may be something present in their
ecology that further distinguishes their niches”. This remark epitomizes the
frustration of seeking differences between species to explain coexistence. In the
first place, there is no certainty that the two species are competing, but even if
they are, the discovery of a difference between them is no reason to assume that
this particular difference is what allows the two animals to coexist.
Whitlatch (1980) has provided a more penetrating analysis of niche
differences between intertidal deposit-feeding polychaetes. He found that the
surface-feeders divided their food resources more finely than burrowers, their
use of feeding tentacles allowing finer selectivity of ingested particles.
Burrowers were more diverse and partitioned the habitat both by particlesize of
the food and by depth—another example of the use of more than one
environmental dimension to segregate the niches of species in diverse
communities (cf. Schoener, 1974). In areas where the organic content of the
sediment was high, species with similar trophic needs coexisted, but only
dissimilar species lived together in areas of low organic content. The
implications behind this are, first, that food is limiting in these soft-bottom
communities, and secondly, that competition is greatest between species with

similar needs. Comparing different areas, Whitlatch showed that as diversity
increases, so does the average overlap between the species (Fig. 28A). This
stands in direct contradiction to the generally accepted rule that as communities
become more diverse, so the mean overlap between species will reduce, and
appears to be related to the fact that higher food levels sustain more diverse
communities in these soft-bottom polychaete communities, permitting greater
overlap. When these polychaete species are ranked in order of abundance
(Fig. 28B), it is the rarer species that have highest niche overlaps with other
species, and it is these species that are eliminated first when food levels decline
and the community becomes less diverse. Since no particular species seems
responsible for excluding any of these rarer species, Whitlatch suggests this is an
example of “diffuse competition”, the cumulative effect of several species
resulting in the exclusion of the rarer animals. Whitlatch’s results are strongly
suggestive of competition, and the patterns revealed are significantly different
from those expected by chance. This does not prove that competition causes the
patterns, although Whitlatch’s arguments for competition-induced
nicheapportionment are convincing. Experimental manipulations on this
community would be a welcome complement to Whitlatch’s work.
526 G.M.BRANCH
Fig. 28.—Relationships between the average resource overlap between deposit-feeding

burrowing polychaetes which coexist and the number of coexisting species (A); B, the
abundance rank of the species; (after Whitlatch, 1980).
Particle selection has been demonstrated in a number of deposit-feeders such
as Pectinaria gouldii (Whitlatch, 1974 see p. 454), Abarenicola pacifica and A.
vagabunda (Hylleberg, 1975a). A detailed comparison between the amphipod
Corophium volutator and the mud snail Hydrobia ulvae (Fenchel, Kofoed &
Lappalainen, 1975) shows the former selects fine particles (Fig. 29A) and also
feeds on much smaller diatoms (Fig. 29B). Because of this, the diet of H. ulvae
contains far more diatoms and that of Corophium has proportionately more
bacteria. Using radioactively labelled bacteria, Fenchel et al. (1975) showed that
Corophium is almost incapable of feeding on bacteria unless they adhere to fine
particles (Fig. 29C). Similar labelling of several strains of diatoms demonstrate
that Hydrobia ulvae is more efficient at feeding on diatoms than Corophium
(Fig. 29D). Growth of another mud snail, Hydrobia ventrosa is linearly related to
the biomass of large diatoms but is unaffected by the mass of small diatoms
(Fenchel & Kofoed, 1976), showing that it feeds preferentially on larger
diatoms.
A comparison of the deposit-feeding gastropods Ilyanassa obsoleta and
Hydrobia totteni (Bianchi & Levinton, 1981) shows that both species depress
blue-green algae and diatoms in the sediments they feed upon, but only Ilyanassa
has any effect on coccoid blue-green bacteria. Their contrasting effects on
coccoid bacteria may be due to differences in their digestive enzymes, or in gut
Fig. 29.—Separation of the diets of Corophium and Hydrobia ulvae on the basis of
particle size (A) or size of diatoms (B); C, uptake of bacteria by Corophium is only possible
in the presence of silt and clay; D, the relative uptake of radioactively labelled diatoms by
Hydrobia ulvae and Corophium volutator; (after Fenchel et al., 1975).
residence times, or in the greater concentration of extracellular carbohydrases in

Ilyanassa. When the two animals are kept together Ilyanassa depresses the
growth of Hydrobia totteni, while the latter has no effect on Ilyanassa. Bianchi &
Levinton propose that the high-shore distribution of Hydrobia totteni is due to it
being confined there by an “interference response to competition with Ilyanassa
and other deposit-feeders found lower in the intertidal”.
A more challenging problem has been the detection of processes allowing
coexistence of the closely related Hydrobia spp. in Europe. Fenchel (1975a)
reviews the distribution of the three species in northern Jutland. Salinity is the
most important factor relating to their distribution, H. ulvae occurring in high
salinities approaching those of sea water, H. ventrosa being more abundant at
about 16‰ and H. neglecta being intermediate. The first two are the commonest
and Fenchel points out that H. neglecta is often absent where one would expect
to find it, suggesting it is squeezed out by competition with the other two
528 G.M.BRANCH
Fig. 30.—Relative enzyme activities in three species of Hydrobia (after Hylleberg, 1976).
species. Hylleberg (1975b) has measured the egestion rates of the three species
at various combinations of temperature and salinity, using egestion as a simple
measure of activity. H. ulvae has an optimum of 30°C and 30‰ , H. neglecta at
20 to 25°C and 25‰ , while H. ventrosa is tolerant of a much wider range of
conditions although peaking at 30°C and 20‰. Hylleberg suggests that because
different combinations of temperature and salinity favour different species,
fluctuating environmental conditions prevent one species from gaining a
permanent advantage over the other, so that there are wide areas of coexistence.
The assimilation efficiency of H. ventrosa is uniformly high for most bacteria
(75% efficiency) and diatoms (60–71%) and only some blue-green algae (8–50%)
are less efficiently assimilated. This initially led Fenchel (1975a) to suggest that
differential utilization of ingested organisms can only play a modest rôle in
partitioning food by Hydrobia species. Hylleberg’s (1976) analysis of hydrolytic
enzymes reveals, however, distinct differences between the species (Fig. 30). H.
ulvae has a high activity of ξ rather than ξ glucosidases suggesting a greater
importance of green algae and diatoms in the diet. H. neglecta exhibits a low
enzymic activity to many substrates and is evidently more specialized than the
other species. It has the highest lysosome activity, possibly indicating a
specialization on grampositive bacteria. H. ventrosa has a high level of activity
for most carbohydrases and seems the most generalized species (as its
temperature and salinity tolerances also indicate). It has relatively higher ξ
glucosidase and trypsin activity, possibly correlated with the digestion of
diatoms, fungi, and bacteria. Low lysosome activity may imply that H. ventrosa
preferentially digests gram-negative bacteria in contrast to H. neglecta.
Hylleberg is cautious in interpreting these differences as a way of reducing
competition between the species, for even if certain ingested elements are not
digested, they are packaged into faecal pellets which are then too large for the
other species to eat. Feeding may be affected, however, by the different
Fig. 31.—Character displacement of Hydrobia ulvae and H. ventrosa, which are

respectively larger and smaller than usual when the two coexist (A) but are similar sized
when they occur separately (B): as a result their diets diverge in coexisting populations (C)
although they are usually very similar in separate populations (D, E); (after Fenchel,
1975b).
enzymatic potentials of the three species and may increase the chances of
coexistence in a patchy or variable environment.
H. ulvae and H. ventrosa are usually very similar in size, but Fenchel (1975b)
has described character displacement of body size in coexisting populations,
where H. ulvae is larger than normal and H. ventrosa smaller (Fig. 31A, B).
Similar, but less obvious displacement occurs in H. neglecta when it coexists
with either or both of these species. As body size is related to the median particle
size which is selectively ingested, differences in body size will also displace the
particle sizes which are eaten (Fig. 31C-E) and hence reduce competition.
Fenchel & Kofoed (1976) have shown that increase in snail density decreases
530 G.M.BRANCH
Fig. 32.—A, effect of snail density on the growth of Hydrobia ulvae when this species is
grown with its own species or with H. neglecta; B, per cent survival of H. ventrosa is
greater when this species is grown with large H. ulvae than with small H. ulvae; C, effect
of snail density on photosynthetic production by diatoms in the sediment; (after Fenchel &
Kofoed, 1976).
growth (Fig. 32A) and survival, and that the difference between single and mixed
species colonies are negligible: implying that interspecific competition is as
intense as intraspecific competition. When small H. ventrosa are grown together
with large H. ulvae their survival, however, is much greater than when they are
grown with H. ulvae of a similar size (Fig. 32B). This is the first experimental
proof that character displacement has a real effect in reducing competition.
Fenchel & Kofoed (1976) have measured the effects of Hydrobia density on
the photosynthetic activity of the sediment (Fig. 32C). High densities reduce
photosynthesis, indicating that exploitative consumption substantially reduces
diatoms. Interestingly moderate densities actually increase photosynthesis,
because the snails stir the sediment and disrupt the mats of blue-green algae
which would otherwise compete with the diatoms for light. As a partial test of
whether character displacement can reduce competition in Hydrobia, Levinton
(1982) grew H. totteni with sediment particles of two different sizes. Since
differences in growth could not be detected in the animals grown on the different
particles, Levinton has questioned how effective size displacement can be. This
is, however, a coarse test, since Levinton worked with a different species from
any of those used by Fenchel, used sediment particle size rather than size of
diatoms, and grew the animals in isolation without any congeneric competitors.
All of these factors could have influenced the outcome of his experiment and
may explain the difference between his results and those of Fenchel (1975).
As with all cases where character displacement is held to reduce competition

between species, the question of overlap between juveniles of the larger
Hydrobia and adults of the smaller species must be raised. In this instance this is
not an issue, since the Hydrobia spp. have a sharply defined breeding season
once a year, and so the size difference between sympatric species can be
maintained year-round. Furthermore, reproductive displacement occurs in areas
of sympatry, the larger species breeding earlier than usual and the smaller ones
later, so that the size difference between them is emphasized (Fenchel, Frier &
Kolding, 1977). Thus a range of interesting factors allows the three European
Hydrobia species to coexist, including different environmental optima, differing
enzymes, and displacement of body size leading to separation of feeding niches.
Gray (see Gray & Johnson, 1970) has shown that various meiofaunal species
(harpacticoids, archiannelids, and gastrotrichs) occur in dense local patches.
They are attracted there by specific bacterial strains and their numbers can be
correlated with the density of these bacteria. This suggests that meiofauna also
have very narrow requirements which may allow partitioning of food.
Differences in the diets of coexisting harpacticoids (Rieper, 1978, 1982) do
exist. Foraminiferans are known to suffer adversely from interspecific
competition and to undergo shifts in diet in the face of competition (Muller,
1975). Comparing four predatory nematodes that occur in the Exe Estuary,
Devon, Warwick (1982) recorded size differences between the species, with
consistent ratios of 1–28 between the sizes of successively larger species. While
this again conforms to the size ratio suggested by Hutchinson (1959) for
coexistence of competitors, considerable overlap must occur between juveniles
and adults of the four species. Warwick suggests that juveniles may have
different diets from the adults. In the Lynher Estuary, Cornwall, there are only
two predatory nematodes, and these differ so radically in size that even the
smallest instars of the larger species do not overlap the size range of the smaller
species. There are also examples of coexistent meiofaunal species with
seemingly identical food. For instance, amongst the harpacticoid copepods, two
sibling pairs of Tisbe (Van den Berghe & Bergmans, 1981) and Enhydrosoma
(Ivester & Coull, 1977) are inseparable ecologically and yet they coexist
persistently. As a result, although differences in the diets of coexisting
meiofauna can be demonstrated, it would be premature to assume that they are
related to competition or are the reason species can coexist. Only in the case of
the foraminiferans has convincing evidence of competition been put forward
(Muller, 1975).
Infaunal species occupying soft sediments have another option open to them to
achieve habitat partitioning: in addition to differences in their horizontal
distribution, vertical apportionment of the sediment is possible. In several cases
differences in horizontal distribution separate different species. For instance
Nucula proxima occurs in sediments with a silt and clay content of less than 50%,
while N. annulata lives in fine ooze with greater than 90% silt and clay
(Levinton, 1977). Similarly, two sibling ampeliscid amphipods are separated by
532 G.M.BRANCH
Fig. 33.—Segregation of haustauriid amphipods by horizontal zonation up the beach (A)

and vertical depth in the sediment (B): 1, Neohaustorius schmitzi; 2, Parahaustorius
longimerus; 3, Lepidactylus dytiscus; 4, Haustorius canadensis; 5, Acanthohaustorius
millsi; (after Croker, 1967).
differences in their substratum preferences (Mills, 1967; see also Biernbaum,

1979). It is not known whether this segregation is either linked to, or reduces,
competition in these organisms. N. proxima does shun areas where Yoldia
limatula is abundant, presumably a means of avoiding competition (Levinton,
1977), as may be the changes of areal distribution of five species of gammarid
amphipods in regions of sympatry (Fenchel & Kolding, 1979). Rees (1975)
describes how two intertidal isopods, Gnorimosphaera oregonensis and
Exosphaeroma amplicauda have very similar preferences for substratum particle
size when they are alone, but that their preferences are narrowed and displaced
when the animals occur together in the field (Fig. 34). In experimentally mixed
populations, the amount of displacement is related to the proportion of the two
species. A 3:1 ratio of Gnorimosphaera:Exosphaeroma approximates that in
natural populations and the amount of displacement then also closely approaches
that found in the field (Fig. 34). While it is tempting to term this “behavioural
character displacement” and suggest that mutual displacement allows
coexistence of these two species, Rees’s data show that Exosphaeroma is far
more displaced than Gnorimosphaera, so that this may be a simple case of one
species excluding the other from their mutually preferred habitat, probably by
interference.
Differences in the depth at which coexisting species occur in the sediment
(vertical partitioning) do occur. As an example Croker (1967) describes the
ecology of the many haustoriid amphipods which occur together on Georgia
beaches. Of the five most abundant species Neohaustorius schmitzi and
Haustorius canadensis occur together high on the shore, Parahaustorius
longimerus and Acanthohaustorius millsi lower down, while Lepidactylus
dytiscus is sandwiched between these (Fig. 33A) and shifts its zone up or down
depending on the abundance of the upper or lower group of species and only
becomes abundant when either of these groups is absent. The pairs of species
which share zones occupy different depths in the substratum (as do coexisting
Bathyporeia congeners—Nicolaisen & Kanneworf, 1969). They also differ in
body size (which may influence the size of particles on which they feed). The
breeding seasons of those pairs of species which share zones are also staggered
so the juveniles of one species dominate when populations of the other consist
mainly of mature adults. This increases the difference in body size and also
ensures that peaks of population size do not coincide. Whether size differences
do promote coexistence remains unproven. Acanthohaustorius and Haustorius
occur at the same depth in the sediment, but their numbers are negatively
correlated, Acanthohaustorius always occurring lower on the shore and
following the seasonal movements of Haustorius up and down the shore. Their
horizontal segregation is most marked in brooding females and juveniles, and
Croker & Hatfield (1980) have shown that in the laboratory Acanthohaustorius
females experience high mortalities and low reproductive output if they are kept
with Haustorius.
Vertical partitioning of the sediment occurs in modern bivalves and appears to
have occurred in Silurian communities, judging by the layering of fossil deposits
(Levinton & Bambach, 1975). Peterson & Andre’s (1980) experimental analysis
of interactions between bivalves shows that a shallow-living species, Protothaca
staminea, has no effect on three deeper-dwelling species (and vice versa) but that
interactions occur between the three deeper species which occupy a common
stratum. To illustrate, the growth of Sanguinolaria nuttallii is depressed by as
much as 80% by Tresus nuttallii and Saxidomus nuttalli and it avoids areas
where they are common. Since all three have long siphons that extend to the
surface, it seems unlikely that they are competing for food, but rather for space.
To test this idea, Peterson & Andre planted dead shells of Saxidomus and Tresus
amongst Sanguinolaria, and found that the growth of the latter was depressed.
The amount of the depression was, however, not as great as that caused by living
individuals of these bivalves, so it appears as if, in addition to competition for
space, interference or competition for food may take place.
Despite this, we cannot assume that species living at the same depth are
necessarily competing. Peterson’s (1982) long-term experimental analysis of
534 G.M.BRANCH
Fig. 34.—Substratum selection by two isopods, Gnorimosphaera oregonensis (black

shading) and Exosophaeroma amplicauda (white) when they are alone (A), or tested
together in various experimental ratios of 1:1 (B) or 3:1 (C): substratum selection in field
samples where the species coexist in a 3:1 ratio is given in (D); (after Rees, 1975).
interactions between two bivalves, Chione undatella and Protothaca staminea,

produced no evidence of interspecific competition, despite the fact that these
species live at the same depth in the sediment and that intense intraspecific
competition can be demonstrated—as evidenced by decreased growth, reduced
gonadal mass and (in the case of Protothaca) increased emigration at higher
densities. Peterson was forced to conclude that this intraspecific effect is due to
competition for food rather than space (because competition for space would
almost certainly involve an interspecific effect) and that the two species have
partitioned their food requirements so that they do not compete.
Stratification of species in the sediment is commoner in deposit-feeders and
suspension-feeders than in tube-builders, but Mangum (1964) has described a
vertical stratification of coexisting maldanid polychaetes. Comparing five

species, Mangum found differences in their preferences for certain types of
sediment, and in the depth at which they occurred. Only two species were
frequently sympatric, but of these, one (Clymenella zonalis) feeds at a depth of 8
to 15 cm and the other (C. torquata) at about 20 cm. Another interesting
difference is that C. torquata is dimorphic, having orange and green forms. Only
the green form coexists with C. zonalis (which is always orange) and Mangum
proposes that the green colour is due to C. torquata being able to feed on blue-
green algae. If this source of food is unique to the species, it may provide a
further avenue for coexistence of the two species.
The possibility of vertical stratification of meiofauna has been overlooked
until recently, largely because of the difficulty of examining strata on a small
enough scale. Having achieved this, Joint, Gee & Warwick (1982) showed clear
vertical partitioning by harpacticoid copepods in the top 20 mm of sediment.
Interestingly, the nematodes (which have very specialized modes of feeding that
differ from species to species) were not stratified. The only exception to this
latter generalization was two species of epigrowth-feeders with the same mode
of feeding and the same body size: they were clearly stratified into different
vertical zones.
That microhabitat differences between existing species can be due to character
displacement of body size is suggested by the work of Frier (1979a, b; and see
Fenchel & Christiansen, 1977, for a review) on two isopods. Sphaeroma hookeri
and S. rugicauda are similar in size when they occur allopatrically, but in
sympatry their sizes are displaced, S. hookeri always being the smaller of the two.
Unfortunately the changes in relative size follow an environmental gradient up a
fjord, and further data are needed to separate competitive and environmental
effects on body size. The two species also show signs of having their
reproductive periods displaced when they live together, increasing the size
difference between the two, but the amount of displacement of the reproductive
periods is fairly small—a matter of days. Frier’s (1979b) explanation for the
cause of size displacement is that both species accumulate in the shallows to
breed, and seek shelter in small holes in rocks. Since the size of the hole is
correlated with body size, and animals that choose holes that are too large can be
forcibly evicted, the displacement of body size may reduce interference between
the species. This explanation can only be sustained if interspecific effects are
greater than intraspecific effects, or there would be no reason for either species to
reduce effectively the range of hole sizes that they could occupy.
Thus, vertical stratification, differences in microhabitats, and apportionment
of food resources do occur in a wide range of soft-bottom organims and, at least
in some cases, there is solid evidence indicating that these effects contribute
towards reducing competition between species. Despite the several examples
given above of competitive exclusion resulting from overlaps in food or habitat,
the most clear-cut illustrations of ‘competitive’ interactions are the result of
amensalism, in which one species has an adverse effect on the other but is itself
536 G.M.BRANCH
not affected by that species. One of the major developments in understanding the
functioning of sedimentary communities has been the comprehension that such
amensalistic interactions often operate through indirect effects on the
substratum. Gray (1974) and Rhoads (1974) have reviewed animal-sediment
interactions, but many examples have appeared since then. Two key features in
understanding such indirect amensalistic effects are the impact organisms have
on the hydrodynamics of the sediment, and the effects that adults have on larvae.
Burrowing organisms increase the water content of sediments and decrease the
particle size, destabilizing and encouraging the resuspension of surface
sediments. This has two adverse effects, particularly on filter-feeders. First, a
high load of suspended inorganic matter tends to clog their gills and to smother
them if they are not mobile. Secondly, it inhibits settling of larvae because they are
liable to be swept away in the resuspended sediments. Very early on, Segerstråle
(1962) pointed out that the amphipod Pontoporeia reduces larval settling of
Mytilus. Conversely, filter-feeders, tube-builders and rooted plants stabilize the
sediments, making it difficult for burrowing organisms to penetrate the
sediments (Young & Young, 1978) and filter-feeders also tend to exclude
settling larvae by filtering them out of the water column. Even surface-feeding
deposit-feeders such as the bivalve Nuttalia and the polychaete Neanthes
influence the nature of the sediment, reducing organics and keeping the Eh high
(Tsuchiya & Kurihara, 1980).
Rhoads & Young (1970; see also Rhoads, Allen & Goldhaber, 1977) were the
first to develop these ideas, with specific reference to suspension-feeders versus
deposit-feeding burrowers, and they referred to the interaction as “trophic group
amensalism”. This draws attention to the fact that groups of species,
taxonomically unrelated, act as functional units, and adversely affect other
groups that are trophically different (Woodin & Jackson, 1979). Thus corals,
algae and sea grass stabilize sediments and are adversely affected by burrowers,
and in particular by the sand prawn Callianassa which increases the suspension
of sediments (Aller & Dodge, 1974; Suchanek, 1983). Tube-building
polychaetes inhibit deposit-feeders, and their experimental removal leads to an
increase in burrowing deposit-feeders (Woodin, 1974, 1977). Large burrowers
adversely affect small surface-dwelling deposit-feeders but have less effect on
larger species. Thus Arenicola pacifica dramatically reduces the numbers of
Pygiospio elegans but has little or no effect on a slightly larger polychaete
Pseudopolydora kempi. Conversely, Pygiospio and Pseudopolydora reduce the
numbers of Arenicola by ingesting its larvae and settling juveniles, but they are
too small to have any impact on adult Arenicola (Wilson, 1981). Clearly size
plays a major rôle in determining which functional group is dominant.
The effect of roots and tubes on the activities of burrowers has been quantified
by Brenchley (1982) who has shown that burrowers take two to ten times longer
to penetrate sediment consolidated by tubes, and three to 37 times longer in
sediment bound by roots of sea grass. Large animals with inflexible bodies
proved most susceptible to the stabilization of sediments, and were largely

excluded from sea-grass beds and areas with tubeworms.
Although, as a generalization, burrowing deposit-feeders and tube-builders act
antagonistically, there are exceptions. There are times when tubes destabilize the
sediment rather than stabilizing it, causing local scour by deflecting water
towards the sea bed (Eckman, Nowell & Jumars, 1981). Furthermore, large tubes
such as those of Diopatra cuprea may provide protection from predators, with a
consequent increase of diversity in the immediate vicinity (Woodin, 1981).
Similarly, sea-grass beds provide considerable protection to infaunal species
against predators, so the disadvantages of having to burrow through stable
sediments may be offset by added protection (Young, Buzas & Young, 1976;
Young & Young, 1978). Thus, the influences of one functional group on another
are not as simple as they might at first sight have appeared.
The effects of such amensalistic interactions are obviously density-dependent
(Rhoads, 1974), but the members of a particular group tend to create conditions
that favour other members of their own group. For instance, infaunal deposit-
feeders decrease particle size and increase oxygen levels in the sediment,
enhancing microbial growth, thus generating more food for the deposit-feeders
and encouraging an increase in their numbers (Driscoll, 1975). They will also act
in concert to undermine tube-builders and to increase the ease of burrowing, so
that the members within one functional group are indirectly mutualistic, via their
effects on the sediment and on other organisms (Brenchley, 1978, 1981).
Since sediment deposition and suspension are determined partly by currents,
which also influence the availability of different kinds of food, the balance
between deposit-feeding burrowers and tube-dwellers or suspension-feeders is
often set by the combined ef fects of the stability of the sediment and current
speed. Calm depositing areas favour deposit-feeders, current-swept but stable
sediments (usually coarse and with a lower organic content) favour suspension-
feeders (Warwick, 1982).
One final facet of competitive interactions between soft-sediment organisms is
the possible rôle of predation in preventing competitive monopolization.
Peterson (1979b; and see Peterson, 1980, for a critique of methods) has provided
a penetrating comparison of the rôle of predators in sediments in comparison
with their impact on the communities of rocky substrata. In every case where
predators have been experimentally excluded from soft-bottom communities
their absence has led to an increase in biomass and diversity (e.g. Virnstein,
1977; Berge & Valderhaug, 1983; and see Woodin, 1978 for the effects of
disturbance). This occurs in spite of the fact that birds feeding on soft bottoms
may capture the most common prey species more often than expected on the
basis of their abundance (Schneider, 1978), and is in direct contrast to the
situation on rocky shores where predators are considered to hold potentially
competing populations below the level at which exclusion is likely to occur, and
hence increase community diversity (see Paine, 1971, 1974). Peterson suggests
this difference has a number of explanations. First, lethal interference
538 G.M.BRANCH
competition by means of crushing or undercutting is difficult to imagine in

sediments where competitors will have no firm purchase against which they can
act. Secondly, overgrowth is equally unlikely in sediments because animals are
free to move up and down, and the instability of the sediment will occlude
colonial forms which so effectively overgrow other organisms on rocky substrata.
Thirdly, potential competitors can partition the environment in three dimensions,
vertical partitioning being a means of reducing competition, while on rocky
shores this third dimension is not available. Fourthly, interactions between adults
and juveniles may maintain populations at relatively low levels, at which
competition is not likely to be acute. Finally, most invertebrates are sufficiently
plastic in their growth to survive even if food is limiting, and are unlikely to
starve to death. The latter two arguments apply equally well to many
communities living on hard substrata. Nevertheless, it appears that competition
in soft-bottom communities is less likely to lead to competitive exclusion, but
rather to co-existence under sub-optimal conditions.
In contrast to the suppositions outlined at the beginning of this section, soft-
sediment organisms do compete, can be short of food, and do partition both food
resources and vertical space. Indirect competition by way of modification of the
sediment, and adult-larval interactions may, however prove to be of much
greater importance in the organization of these communities than more
conventional forms of competition for food and space.
Hermit crabs
Because hermit crabs depend on gastropod shells for protection, and because
they only rarely attack living gastropods to obtain these shells, their populations
are usually limited by the availability of empty shells. Shells constitute an easily
quantified resource, and the suitability of different kinds and sizes of shells can
be determined, so hermit crabs are model animals that have been used in various
ways to test competition theory, as discussed by Hazlett (1981) in a review of
hermit crab behavioural ecology. Several authors have deduced that competition
for suitable shells limits hermit crab numbers (Grant & Ulmer, 1975; Bach,
Hazlett & Rittschof, 1976; Fotheringham, 1976a, b; Kellogg, 1976), but few
have followed Vance’s (1972a) lead in supplying shells to field populations to
test whether shell availability really is limiting. Vance’s provision of 1,000 shells
per month to a population of Pagurus hirsutiusculus did indeed result in an
increase in the population. Another approach, which has been used to assess
whether shells are limiting, has been to supply hermits (which are held in
aquaria) with a wide range of shells of different sizes and, from the selection
made by the crabs, to deduce whether they normally occupy optimal shells.
Almost invariably the animals choose shells larger than those they have been
able to glean in the field, suggesting a shortage of optimalsized shells. In fact,
when they are given a free choice of shells, animals from populations where
shells are in short supply ‘overcompensate’ and select for larger shells than do
members of the same species living in areas where shells are more freely
available (Scully, 1979). Although it is seldom possible to calculate the rate of
shell supply needed to sustain a hermit crab population, Spight (1977) has
managed to do this for Pagurus granosimanus, determining that it requires 0·8
shells per crab per month. Because the acquisition of a suitable-sized shell is
important, hermit crabs may aggregate at sites where the mortality of gastropods
is high, and are attracted to gastropods that have just been killed, relying on
chemical cues (McLean, 1974), probably peptides (Rittschof, 1980a, b), to locate
gastropods that have fallen prey to predators.
Shells serve a number of functions for hermit crabs; they are a defence against
predators (Rossi & Parisi, 1973), the efficiency of this defence improving if the
shell fit is good (Vance, 1972b), but shell-shape also influences how effective the
defence is (Bertness, 1981c; and see below). Various symbionts growing on
shells may improve the defensive function of the shell (as reviewed by Ross,
1967). For instance, Octopus joubini is repelled by Calliactis tricolor when
attacking hermit crabs that house this anemone on their shell (McLean, 1983)
and Octopus vulgaris is repulsed by Calliactis parasitica (Ross, 1971). In similar
vein, predation on hermit crabs by the crabs Cancer irroratus and Callapa
flammea is largely or partially prevented by, respectively, Hydractinia echinata
(Grant & Pontier, 1973) and Calliactis tricolor (McLean & Mariscal, 1973) on
the shells of the hermit crabs.
It is thus not surprising that many hermit crabs actively choose shells with
particular symbionts on them (Mercando & Lytle, 1980) and that particular
species are associated with specific symbionts (Conover, 1976; Jensen, 1970;
McLean, 1983). Dardanus gemmatus actively transfers Calliactis onto its shell
(Ross, 1970) and has evolved specific tactile signals which elicit particular
behavioural responses in the anemones, making the transfer easier (Ross &
Sutton, 1968). Dardanus arrosor ceases to transfer anemones onto its shell if
held in predator-free situations, but the urge to acquire anemones immediately
increases if the hermit crab is exposed to even the odour of an Octopus (Ross &
von Boletzky, 1979). Clearly certain epibionts make shells more effective as a
means of reducing predation, and at least in one species, Dardanus arrosor,
dominant crabs steal anemones from subordinate animals, adding a new
dimension to competition between hermit crabs (Mainardi & Rossi, 1969).
Crabs with better-fitting shells also win more fights with other hermit crabs,
and seldom relinquish their shells to other animals (Hazlett, 1980). Once again,
the presence of symbionts is of importance in that they can tip the balance
between competitors. For instance, Clibanarius vittatus is dominant over Pagurus
pollicaris when contesting a shell, but if the P. pollicaris has a hydroid growing
on its shell, Clibanarius vittatus is repelled because of the sting it receives.
Pagurus spp. are not stung by the hydroids and frequently house them (Wright,
1973). P. longicarpus is another member of the genus gaining competitive
superiority because of hydroid symbionts (Mercando & Lytle, 1980). Thus, as a
540 G.M.BRANCH
secondary function, the shell and its epibiota can modify the competitive ability
of hermit crabs.
Shell size and shape also influence the growth and reproductive potential of
hermit crabs, both being increased in optimal shells (Fotheringham, 1976a).
Since there is an inverse relationship between the ratio of animal size to shell
size and the size of egg clutches produced by female hermit crabs, animals which
are obliged to occupy sub-optimal shells due to competition with other hermit
crabs cannot achieve their full reproductive potential. This has been shown to
occur in Clibanarius tricolor, which occupies smaller shells when living
sympatrically with a superior competitor, C. tibicen, than when it lives alone
(Bach et al., 1976). Interspecific competition thus has a direct impact on
reproductive success. It has also been suggested that the reproductive periods of
coexisting hermit crabs are displaced to reduce competition between the larvae
for food (Reese, 1968), but there is no evidence to suggest that hermit crab larvae
do compete for food.
The final function of shells is to protect the animal against physical stresses,
and shell shape and size influence the tolerance of hermit crabs to factors such as
desiccation. An illuminating comparison of shell preferences in three coexisting
species illustrates this point. One of the species, Pagurus sp., inhabits the low
shore and preferentially selects narrow-mouthed heavy shells. Such shells have a
small internal space and house little water, so Pagurus sp. has a low tolerance to
desiccation. On the other hand, these shells are ideal protection against
predators, which are more likely to be a problem in the low shore than
desiccation. Two mid- to high-shore species, Clibanarius albidigitus and
Calcinus obscurus, select shells with wide mouths and thin walls, which have a
large water-holding capacity and increase the resistance of these animals to
desiccation, but are a poor means of deterring predators. To compensate, both
species have well-developed escape responses. Of the three species, Clibanarius
albidigitus occurs highest on the shore, partly because of competitive
interactions with Calcinus obscurus lower down the shore, and has a higher
physiological tolerance to water loss (Bertness, 1981c). Thus, there are
conflicting advantages to different types of shell (Bertness, 1981d).
McLean (1983) has described a “habitat web” revolving around the use of
empty gastropod shells as a resource. Hermit crabs function as key organisms in
this habitat web, preventing shells from being rapidly lost, crushed or buried.
Various symbionts grow on the hermit-inhabited shells and depend on the hermit
to retain the shell and prevent burial. Apart from hermit crabs, other animals may
shelter in the shells. An example is the goby, Gobiosoma robustum, which
broods its eggs in gastropod shells and most often uses shells that are less
preferred by hermit crabs. This minimizes the potential disturbance from hermit
crabs, which have no difficulty in ejecting gobies. The hermit crabs are preyed
on by Octopus which does not destroy the shell in the act and may even occupy
it if the shell is large enough. Hermit crabs are also hunted by predatory crabs
and by spiny lobsters, both of which destroy the shell in the process and thus
eliminate it from the habitat web. The central rôle of the hermit crabs in this web
emphasizes that they have no serious contenders for empty shells apart from
other hermit crabs. Interspecific competition for shells tends to be viewed in
three different ways by different authors. First, there is the view that coexistent
species have diverged in shell preferences to the point that apportionment takes
place and competition is minimal. Secondly, the opposite argument is that
differences between species are due to competition rather than a means of
reducing it. Finally, recent work lays emphasis on the mutualistic nature of many
shell ‘fights’.
Certainly differences in shell preferences and in habitat do exist between
species (Vance, 1972a; Grant & Ulmer, 1975; Mitchell, 1975; Bach et al., 1976)
and are usually inferred to allow coexistence. As one example Abrams (1980)
has shown that in sympatry Calcinus obscurus, Clibanarius albidigitus, and
Pagurus sp. occupy different zones on the shore, differ in size, and utilize
different kinds and sizes of shells. Abrams concluded that the three species were
partitioning the environment and the shells between them and that they probably
competed very little. Almost simultaneously, Bertness (1981a, b) undertook a
study of the same three species, but reached a quite different conclusion. He
demonstrated that Clibanarius is a superior exploiter of new shells, but that
Calcinus is competitively dominant in fights and soon usurps the shells that
Clibanarius has acquired. This point is worth stressing as it is one of the few
cases where the rival merits of exploitation and interference can be quantitatively
compared. Of course, the shell is an unusual resource in that it is not consumed
by its use, so the generality of this comparison is limited. Because of its
dominance by means of interference, Calcinus actually benefits from the
association with Clibanarius because the latter minimizes loss of new shells.
That Clibanarius suffers from interactions with Calcinus can be confirmed by
comparing “shell adequacy indexes” of Clibanarius which are coexisting with
Calcinus with those in allopatry: the Clibanarius which are not coexisting with
Calcinus always have superior shells. There is thus good evidence that the two
species do compete for shells. Furthermore, Clibanarius occurs above Calcinus
on the shore and also only occupies the edges of pools inhabited by Calcinus, while
when it occurs alone it lives further down the shore and is spread throughout
pools. Clibanarius has a well-developed escape response when in contact with
Calcinus (Bertness, 1981b) and this is probably responsible for its high-shore
and pool-edge distribution when in sympatry with Calcinus. Thus, the differential
distribution of the two species and their use of different shells are the outcome of
competition and not a means of preventing it (yet another example of the
inadequacy of “overlap indices” as measures of the degree of competition
between two species). Even the smaller size of Clibanarius may partly be due to
competition, for being restricted to less-preferred shells its growth is likely to be
stunted. It is not, however, possible to reject the concept of resource partitioning
in hermit crabs altogether, for while Pagurus sp. is inferior to both Clibanarius
and Calcinus in its ability to compete for shells, it does have different needs, as
542 G.M.BRANCH
discussed above, for it uses narrow-mouthed heavy shells which reduce mortality
due to predation, while the other two species prefer lighter shells that maximize
water storage.
Clearly, competition for shells does take place between different species. Early
work has shown that contests between different sized animals usually end in the
larger animal winning and forcing a shell exchange. The more inadequate the
larger animal’s shell is, the greater the chance of it evoking an exchange of shells
(Vance, 1972b). Results such as these have prompted the view that shell
exchange depends largely on the size and aggressiveness of the initiator of a
fight (Hazlett, 1970). Since then it has become apparent that shell exchange is
rare when the smaller animal possesses a shell that fits it ideally, and that
mutualistic exchanges, where both individuals benefit, are frequent (Hazlett,
1978, 1980). Much of the ‘fight’ involved in shell exchange is ritualized, and in
several species it includes a rapping of the shell on the substratum (Hazlett,
1972) which may impart information about the respective shells, facilitating
exchange when it is mutually beneficial. Hazlett (1981) has reviewed several
features of the shell, as a resource, which makes mutualism feasible. First,
different species transfer shells from one area to another, making them accessible
in areas where they would not otherwise be available. Secondly, if a hermit crab
does not take residence in a shell shortly after the death of its gastropod owner, it
is likely that the shell will be buried or damaged and hence lost. Thirdly, it is
possible for hermits to ‘trade-up’ or ‘trade-down’ with benefit, for shells can be
too large or too small; thus the opportunity for mutually beneficial exchanges
does exist. Fourthly, the resource is not consumed by its use in the way that food
or nutrients are consumed; in fact in some species the shell is modified by use,
making it more suitable for subsequent occupation by other hermit crabs.
Finally, potential information on the quality of the shells is available to both
participants.
The possibility of mutualistic shell exchange does not imply that competition
between different species does not exist: quite clearly differences in the ability to
compete by interference result in competitive dominance by some species. But
mutualism is likely to blunt the intensity of interspecific competition and is far
more likely a reason for continued coexistence than niche apportionment. Even
in cases where differences in shell preference can be demonstrated, they appear
to be adaptive in terms of selective agents such as predation and desiccation
rather than in terms of reducing competition.
Zooplankton
Planktonic organisms occupy what is arguably the most homogeneous habitat in
the sea, and Hutchinson (1961) has drawn attention to the “paradox” that there
are so many coexistent species while there are fewer than usual avenues open for
these species to partition the environment between them. Despite this, there are
hints that some species may partition food resources. For instance, the 18 species
of chaetognathes recorded by Stone (1969) in the Agulhas Current differ in terms

of their prey species and the size of their prey as well as having different patterns
of horizontal and vertical distributions. Although Schoener (1974) uses this
example as an instance of habitat apportionment, Stone himself places little
emphasis on these differences as a means of avoiding competition and, indeed,
there is no evidence that the chaetognathes compete with one another. It is true
that size (width) of prey is related to the width of the head in various species of
chaetognathes (Pearre, 1980) but although the relationship is species-specific,
there are large overlaps in the food items of most species.
Indian Ocean candacid copepods provide a more convincing example
(Lawson, 1977). Species which are closely related (and presumed to have similar
food requirements) do not coexist, and species which recurrently occur together
are exceptionally different in body size and have different feeding and sexually-
adapted appendages. Lawson suggests this avoids competition for food, a newly
evolving species being displaced in terms of feeding and sexual characters to
allow continued coexistence, or adapting physiologically to occupy other areas
and avoiding sympatry with possible competitors. Although Lawson has no
experimental proof that differences between coexisting species are sufficient to
prevent competition, or that species that are more similar would compete
sufficiently to affect them detrimentally, his data do suggest that coexistent
species are more different (in terms of size) than would be expected by chance.
Far more critical work has been done on competition in freshwater
zooplankton. While it is true many earlier authors simply assumed that
competition takes place in these organisms, and that differences between species
(such as the timing of annual appearance, the depth of occurrence and the nature
of food) are means of avoiding competition and allowing coexistence (e.g.
Sandercock, 1967), more recent work has experimentally demonstrated
competition and explored the consequences. It would be inappropriate to review
the extensive literature on competition in freshwater zooplankton, but some of
the concepts emerging from this research are relevant.
Neill’s (1975) analysis of competition in micro-crustaceans is particularly
revealing. He created experimental microcosms with various crustaceans,
introducing 12 species into the cultures and allowing time for them to interact
under conditions of food shortage. Ceriodaphnia became the dominant in each
case, and only three other species succeeded in coexisting with it. When the fish
Gambusia (which preferentially feeds on the larger Ceriodaphnia) is introduced
into the cultures, it reduces Ceriodaphnia to the point that two of the other
species (Alonella and Simocephalus) increase in density, and a further three
species are able to colonize and maintain themselves in the cultures (Fig. 35A).
This is reminiscent of Paine’s (1971, 1974) results on rocky shores (see above, p.
484). Neill’s results also show R that as Ceriodaphnia declines, the diets of
Alonella and Simocephalus change, and they make more use of the particle sizes
previously dominated by Ceriodaphnia (Fig. 35B). One of the new recruits
(Pseudopsida) also steps into the same feeding niche (Fig. 35B). Neill also
544 G.M.BRANCH
Fig. 35.—A, the influence of introducing a predatory fish on the structure of a

microcrustacean community: numbers of Ceriodaphnia decline, permitting Alonella and
Simocephalus to increase and three other species to colonize the culture. B, when
Ceriodaphnia are reduced by predation, the diets of Alonella and Simocephalus shift and,
together with a new colonizer Pseudopsida, they use the food particles previously
monopolized by Ceriodaphnia; (after Neill, 1975).
revealed that Daphnia was excluded from the cultures only because its juveniles
required the same food as Ceriodaphnia. Adult Daphnia feed on larger particles
and do not compete with Ceriodaphnia, but cannot establish themselves because
of the competitive bottle-neck affecting the juveniles. This is an important result
that has implications for the concept of character displacement. If two species
diverge in size to avoid competition, how do they avoid the bottle-neck when the
juveniles of the larger species are the same size as the smaller species?
While conceding that freshwater lakes are very different from the open sea, it
is evident that much fruitful experimental work along these lines could be done
on marine zooplankton. This is very much an open field in need of critical
research. We have very little direct evidence that competition takes place
between members of the marine zooplankton, nor do we know what processes
permit continued coexistence if they do compete. Niche divergence in terms of
diet has proved inadequate to explain coexistence (Poulet, 1978). Even in very
constant water masses such as the North Pacific Central Gyre, where copepods
are organized into definable groups at different depth zones (McGowan &
Walker, 1979) the maintenance of these groups, and coexistence within them,
cannot be accounted for by either niche apportionment or by selective predation.
Vertebrates: birds and fish

Despite not being aquatic, birds play a significant rô1e in the sea, and they and
the fish and marine mammals constitute the most important marine vertebrates.
These groups share several features. They are active and mobile and can cover
wide distances. Only in the case of territorial forms is competition for space
likely to be an issue. Their mobility also decreases the chances that they will be
obliged to coexist with competitors and, in turn, this reduces the chances that co-
evolutionary divergence will occur because of competition.
Many of the sea birds constitute an interesting exception to this last
generalization. Because they are obliged to return to land to roost and to nest, sea
birds coexist at concentrated focal points such as islands. Intense competition for
nesting space may occur and different species tend to specialize on different
kinds of nesting sites. Even so, their feeding activities, particularly during the
breeding season may be a heavy drain on food resources. Cody’s (1972) analysis
of sea-bird communities shows that many of the Alcidae (auks) overlap
extensively in their fish diets although in both the north Pacific and north
Atlantic up to six species may coexist on islands. The species differ in where
they obtain their fish, feeding at progressively greater distances from the island
and thus partitioning the available feeding area while feeding on similar species
of fish (Fig. 36). The parallel patterns in two different oceans are striking, and
are most readily interpreted as means of reducing competition, more mobile
species dispersing furthest to feed and avoiding competition with species that
are obliged to feed in the vicinity of the island. There is, however, no direct
proof that competition is the cause of these patterns. Interpretative work of this
kind has been criticized by various authors (e.g. Connor & Simberloff, 1979)
who question whether the distribution of feeding birds has been analysed
rigorously enough to distinguish between biologically meaningful patterns and
chance. A re-analysis of data for Alaskan sea-bird colonies (Whittam & Siegal-
Causey, 1981) shows that there are significant patterns of association between
species but, interestingly, most of these are positive associations between pairs
of species, suggestive of mutualism. Furthermore, a ranked measure of resource
overlap between the species was not correlated with the magnitude of the
interactions between the species. This also suggests that competition is of minor
importance in this sea-bird community.
An analysis of the five species of terns coexisting on Christmas Island reveals
differences in their diets, which can be linked with differences in bill size and
body size of the birds. There are also differences in the distances the five species
fly to feed, but these are of secondary significance in separating them. The two
species most similar in size feed at different times of the day (Ashmole, 1968).
Schoener (1974) has attached significance to these differences as means of
permitting coexistence between potential competitors, although Ashmole himself
regards them as adaptive for different reasons and considers competition to be of
little importance.
546 G.M.BRANCH
Fig. 36.—Zonation of the fishing grounds in two alcid bird communities: shading
indicates the major areas fished by each species; (after Cody, 1972).
Mobile species have an additional option in that they may apportion a resource
temporally as well as spatially. For instance A. Crowe (pers. comm.) has shown
that in southern Africa the white-fronted sandplover (Charidrius marginatus)
feeds largely in the upper zones of sandy shores, nesting above high tide and
territorially defending a feeding area. The sanderling (Calidris alba) feeds in the
lower regions of the shore. This spatial segregation is enhanced because the
sanderling (of necessity) feeds during the low-tide period while the sandplover
feeds at high-tide. The two birds only coexist during the southern summer, the
sanderling migrating to the northern hemisphere between June and August.
During this latter period the sandplover partially fills the vacant niche, spreading
its feeding over more of the shore and feeding for a much longer period over
each tidal cycle (Fig. 37). Since territoriality is involved, it seems that this
summer contraction of the area and time available for the sanderling to feed in is
due to interference competition with the sandplover.
A comparative study of six species of migratory sandpipers shows that they
are optimally adapted to their wintering grounds. It is here that they go through a
lean period for food, yet they overlap one another’s niches less during this time
than when conditions are more favourable (Baker & Baker, 1973). Schoener
(1982) amplifies on this and has developed the hypothesis that during lean times
“strong directional selection resulting from interspecific competition produces in
each species adaptations most suited for resources used relatively exclusively by
the species” (Schoener, 1982, p. 591). Conversely, when there is no shortage of
food, it may pay to use other resources because of their abundance, even if this
means an increase in the overlap with other species. Schoener gives several
examples in support of this argument. In the marine context, there is an
important lesson to be learnt from this concept: that long-term analyses of
potential or actual competition are necessary if we are to understand fully the
implications of resource utilization by coexisting species. Thus far very few
Fig. 37.—Niche shifts in the feeding grounds and time of feeding of the sandplover
(Charidrius marginatus) when faced with competition from the sanderling (Calidris
alba): sanderling are migratory and only occur on southern African beaches in the austral
spring and summer (as exemplified here by October); in their absence in winter (e.g.
August) the sandplovers feeding is prolonged and covers a wide range of shore levels;
(A.Crowe, unpubl. data).
studies on marine organisms have been run sufficiently long to test ideas such as
those of Schoener.
Most pelagic fish are highly mobile and cover considerable distances in their
life time. Frequently they are also associated with regions of upwelling,
notorious for their fluctuations. Hence, it is no surprise that considerable
controversy exists as to whether interspecific competition between pelagic fish is
important. For several species which are harvested commercially, long-term
records of stock-size are available. Unfortunately most of these assessments
depend on catch-related statistics, the interpretation of which is fraught with
problems because they reflect the availability to, and preferences of, the fishery,
rather than absolute sizes of the fish populations. Nevertheless, large-scale
‘manipulative experiments’ in the form of commercial exploitation do allow the
opportunity to test for competitive effects between species.
Daan (1980) has reviewed the literature and concludes that there are two cases
in which increases in the numbers of one species can convincingly be linked with
reductions of those of another, presumably competitive, species. The first
concerns the Californian anchovy-pilchard species-pair, Sardinops caerulea and
Engraulis mordax. Complementary changes do seem to occur in these fish, one
increasing when the other declines, and the initial increase in E. mordax seems
associated with the over-exploitation of Sardinops caerulea. The second example
is a more indirect one, in which declines in pelagic fish in the North Sea have
been correlated with increases in some benthic species. More particularly, the
Norway pout (Trisopterus esmarkii) has increased greatly, presumably as a result
of access to food released by the reduction in herring and mackerel stocks
(Anderson & Ursin, 1978).
548 G.M.BRANCH
Other comparable pelagic fisheries do not, however, show equivalent

replacement of one species by another (Daan, 1980). In the case of the southern
African anchovy-pilchard fishery, fishing on the two species has varied in
intensity and has also been regulated by catch-quotas, so that commercial
landings cannot be used as a fair reflection of possible complementary changes
in the populations of the two species, Sardinops ocellata and Engraulis capensis.
The two species do have very similar requirements for food and occupy the same
water masses (King & McLeod, 1976) so that competition between them can be
anticipated. An indirect measure of their combined stocks can be obtained from
figures for the annual accumulation of guano on bird islands that sustain fish-
eating birds. These records show that guano production declined dramatically
when Sardinops ocellata was depleted by over-fishing. If Engraulis capensis had
increased as a result of competitive release following the decline of Sardinops
ocellata, one would have anticipated a constant production of guano (Crawford &
Shelton, 1978).
The most convincing case of competitive replacement of one pelagic species
by another comes from Skud’s (1982) analysis of changes of population size in
various pilchard-anchovy pairs in response to temperature. For instance, in the
case of Clupea harengus and Scomber scomber he showed that whichever species
was numerically dominant responded positively to an increase in temperature,
further increasing its population; while the other, numerically subordinate
species, declined in numbers, not as a direct response to the increased
temperature but because of the rise in the population of the dominant species.
Exactly the same pattern can be demonstrated for the Californian pilchard-
anchovy pair.
In spite of the long-term records available, controversy continues about the
rôle of competition between pelagic fish. This is to be expected, given the nature
of the species and the inevitable lack of controls against which the impact of
commercial fisheries can be gauged. Declines in another commercially harvested
group of species, the whales, seem to have led to an increase in penguins and
crab-eater seals, which have presumably benefited from an increase in the
availability of krill (May et al., 1979), but similar criticisms can be made about
this interpretation. Competition does seem likely to take place between pelagic
fish, and between other pelagic organisms, but its effects may normally be
masked by environmental variability.
MacPherson (1981) has adopted a different approach in examining demersal
species in the Mediterranean. Determining the amount of overlap between the
species and measuring their niche breadths, he found little overlap between the
species, particularly in terms of food. Even those species which did overlap only
did so in a few size groups. In addition, those species which shared similar food
and occurred at the same depths tended to be abundant at different times of the
year or to have different diel patterns of activity.
Shallow-water fish may occupy different zones with respect to depth
(Fig. 38A) and Gibson (1973) suggests this may reduce competition, although
the species overlap considerably. Several of the species Gibson worked on are
zoned by size, smaller animals occurring in shallower water, so that the larger
individuals of one species tend to overlap spatially with the smaller specimens of
the species in the zone below. If size affects prey selection, this may further
reduce competition between the species. More remarkably, most of the fish
migrate up the shore each tidal cycle, and in doing so, the relative positions of
the species are maintained and the size gradient within the species is also
maintained (Fig. 38B). Intertidal pool-inhabiting fish often occupy different
zones on the shore, and when they co-occur they differ in their selection of
microhabitats (Gibson, 1972, reviewed by Gibson, 1982). Helfman (1978)
reviews other instances of differential zonation, particularly in subtidal species,
and discusses the possibility that diel feeding patterns separate suites of fish
which specialize on either nocturnal or diurnal feeding (see also Ebeling & Bray,
1976). This dichotomy develops to a peak in reef fish, in which there is an
orderly “replacement set”, of nocturnal and diurnal species (e.g. Collette &
Talbot, 1972), which Helfman suggests is probably based “on historic avoidance
of competition”.
As with all the above examples of ecological differences between coexisting
demersal or benthic fish, we need to be cautious of laying the blame for these
differences at the door of competition. A multitude of other factors, such as
physical stress, wave action, and predation, may have a bearing on the manner
the species ‘apportion’ the habitat. In none of these cases has competition been
proven and, in fact, many of the authors who have described differences between
the species do not attach undue significance to the rôle of competition in
explaining these differences.
In contrast to the indirect and sometimes debatable evidence of competition
between these fish, many territorial fish provide clear-cut evidence of intra- and
interspecific competition and, in some instances, of competitive exclusion.
Territoriality has been linked to the defence of a food source, shelter or
reproductive site (or some combination of these requirements) and described for
many species (e.g. Rasa, 1969; Clarke, 1970. 1971; Low, 1971; Sale, 1972a, b;
Barlow, 1975; Thresher, 1976; A.H.Williams, 1978, 1979, 1980; Kohda, 1981;
and reviews by Sale, 1980 on reef fish; and Choat, 1982 on temperate fish).
An example is the interaction between Embiotica lateralis and E. jacksoni
(Hixon, 1980, 1981), species which are very similar in body form, morphology,
methods of feeding and diets. Embiotica lateralis occurs in shallow waters,
feeding on invertebrates that it picks from the algal mats that are abundant in the
shallow waters. E. jacksoni lives in deeper waters when sympatric with E.
lateralis but when allopatric it occupies both deep and shallow waters and, in
areas where the two species coexist, experimental removal of E. lateralis also
allows it to move into shallow waters. Conversely, the elimination of E. jacksoni
has no effect on E. lateralis, unless the algae in the shallows are simultaneously
experimentally removed; this dual treatment causes E. lateralis to move into
deeper waters. Thus, it appears that the aggressive superiority of E. lateralis
550 G.M.BRANCH
Fig. 38.—A, the depth distribution of common fish species; from left to right, Limanda
limanda (dab), Agonus cataphractus, Gadus morhua (cod), Pomatoschistus minutus,
Pleuronectes platessa (plaice), Myoxocephalus scorpius, and Psetta maxima (turbot);
(after Gibson, 1973). B, changes in the size of plaice caught at a fixed site over a tidal
cycle, showing that different sized fish maintain different fixed depths over the tidal cycle
(after Gibson, 1973).
allows it to dominate the inshore region, where algae grow most prolifically,
competitively relegating E. jacksoni to an inferior habitat.
A parallel example is provided by two species of Sebastes (Larson, 1980), and
choice of habitat is modified by the occurrence of a congener in two Gobiosoma
spp. (Hoese, 1966). Pomacentrus lividus excludes P. albofasciatus from heads of
the coral Acropora, but the two continue coexisting because Pomacentrus
albofasciatus can occupy a wider habitat (Belk, 1975). Other instances of
territorial dominance in pomacentrids are described by Williams (1978), Sale
(1978) and many other authors cited in Sale’s (1980) review. Sale (1975)
discusses the interactions between three pomacentrids which have essentially the
same requirements for space, taking over one another’s territories
indiscriminately when a territory holder disappears or is removed. Since space
seems in short supply for these fish, territories are rapidly refilled when left
vacant. Of the three species, Eupomacentrus apicalis and Plectroglyphidodon
lachrymatus are co-dominant, and Sale could detect no differences between them
that allowed one an advantage over the other. Both are dominant over
Pomacentrus wardi, which is more likely to lose its territory to one of these
species but is a superior colonizer and occupies a greater range of habitats.
A common pattern appears from all these examples. Territorially dominant
species hold optimal habitats, but because subordinate species can live in a wider
range of habitats they can persistently coexist. Territorial aggression leads
primarily to a rearrangement of existing individuals rather than effecting their
total abundance. Indirectly, however, subordinates may suffer from having to
occupy an inferior habitat where food is less available or predation more intense.
A different approach to interspecific territoriality has been to ask whether the
level of aggression displayed is correlated with the degree of threat an intruding
competitor poses. For example, Myrberg & Thresher (1974) measured how close
intruding fish were allowed to approach the territories of the damselfish,
Eupomacentrus planifrons, before they were attacked. This distance was greatest
for conspecific fish, less for congeners and least for more distantly related
species (Fig. 39). Aggression must cost time and energy and, if it is to be
selected for, this must be balanced by the gain of expelling a potential
competitor. If intensity of competition is correlated with the closeness of the
relationship between any two fish, then aggression should be most marked
towards closely related fish. Seasonal changes also occur in this pattern, the
maximum distance of attack increasing in the reproductive season. This suggests
that defence of a food supply is not the only function of territoriality. Other
advantages include the protection of a nest site and the eggs. Moran & Sale
(1977) similarly quantified the distance intruders were allowed to penetrate the
territory of the pomacentrid Parma microlepis. They could find no correlation
between this distance and dietary overlap of the species. They found, however, a
strong correlation with the overlap of space usage. Ebersole (1977) has related the
incidence of aggression by Eupomacentrus leucosticus to the potential
competitive impact of different intruding fish (Fig. 40). This again shows that the
effort of aggression can only be justified if the intruder really is a threat.
The inference behind many of these findings is that the communities in
question are “dominance controlled” (Yodzis, 1978) by the superior competitors.
The traditional view of such communities is that they are at equilibrium and
saturate the environment. The corollary to this is that only by sufficient niche
diversification can competitors continue to coexist. This explanation has been
espoused by many, particularly by Smith & Tyler (1972, 1973). Roughgarden
(1974) compared the fish populations in different areas and showed an inverse
correlation between species with comparable resource requirements. Conversely,
even closely related coexisting species can be shown to differ in their niches
(Luckhurst & Luckhurst, 1978). Juvenile recruitment of siganids can at times be
so high that food is demonstrably limiting (Tsuda & Bryan, 1973), and resident
adults of various species are held to influence the success of recruits, both
positively and negatively (Smith, 1978). Artificial reefs of differing
552 G.M.BRANCH
Fig. 39.—Maximum distances of attack by the territorial Eupomacentrus planifrons

against intruding males of several species, including conspecifics, congeners, and non-
congeners (after Myrberg & Thresher, 1974).
Fig. 40.—The relationship between potential competitive impact of an intruder and the
intensity of the agonistic response by the territory holder Eupomacentrus leucosticus: the
regression is for 140 different intruding species; (after Ebersole, 1977).
constructions do attract some species differentially, indicating habitat

preferences (Talbot, Russell & Anderson, 1978).
These threads of evidence all support the idea that fish populations are at
equilibrium, and competition can be taken as the driving force maintaining the
differences between the species. The evidence, however, is not always as robust
as one would like. A case in point is the analysis by Anderson et al. (1981) of
changing patterns of chaetodontid communities along a transect from open-ocean
islands to shallow inshore stations. They interpret their data as showing that (a)
coexistent species always differ in their niches, either in terms of food or use of
space, and (b) that there is geographic replacement of species with similar niches
as one moves shorewards. This approach is criticized by Sale (1977), and Sale &
Williams (1982) attack the specific conclusions that Anderson et al. draw from
their data. Sale & Williams simulated the data to test if the patterns were
anything but a random outcome, and found that the actual patterns were
indistinguishable from those that could be generated randomly. This re-
emphasizes the need to search for patterns that differ significantly from those
that occur purely by chance, before ascribing patterns to a deterministic cause,
let alone assuming that competition is the cause. As Sale & Williams (1982, p.
125) facetiously remark “perhaps polar bears and penguins have excluded one
another?”
Gladfelter & Johnson (1983), in accepting this challenge, have shown that
overlap in the diets of six coexisting holocentrids is significantly less than would
be expected in random groups of species which were free from competition.
They conclude that the evolution of the holocentrids has been influenced by
competitive interactions, even although they suggest that competition need not
be structuring the modern communities—that “differences in food utilization
permit competition free coexistence”. This is a moot point. If the environment is
saturated and the populations at equilibrium, what stops the species from
overlapping if the competitive force that drove the species apart in historical
times is now non-existent? If intraspecific competition ever occurs—as it must
do if the species are saturating the environment—then expansion of niches is
likely to occur and is liable to lead to overlap between the species unless
interspecific competition remains an issue and the adverse effects of interspecific
competition are greater than those of intraspecific competition.
Clearly many doubts exist about the application of traditional competition
theory to explain the coexistence of fish in communities that are often very
diverse. Even authors who do find differences between coexisting species
question whether these are sufficient to allow continued coexistence if they alone
are to be responsible for preventing competitive exclusion (e.g. Clarke, 1977).
Sale & Dybdahl (1975, 1978), while finding differences between coral-reef
assemblages conclude that most of the fish in these communities are very
generalized and overlap one another substan tialy in their use of space and food.
While some of the differences of opinion are semantic (what is ‘generalized’,
how different do species have to be to coexist?) the doubts expressed above have
generated two more recent concepts, in opposition to the traditional view of
niche divergence as a means of coexistence.
The first of these has been championed by Sale and his coworkers, who
maintain that while coral-reef fish communities are at equilibrium and that
competition does occur, that the outcome of competition for territories is
determined largely by priority (or “founder-control”); the first fish to establish
themselves in territories becoming sufficiently dominant by virtue of their
position to maintain their territories in the face of competition from subsequent
arrivals. Equal competitive ability of all the species is thus assumed, once the
fish hold a territory, and it is true that fish gain both a psychological and a size
advantage once in possession of a territory (Phillips, 1971; Myrberg, 1972).
More important, Sale looks to chance (particularly the chanciness of recruitment)
to explain which species arrives first and, again, all species are assumed to have
554 G.M.BRANCH
an equal chance of recruitment. This has become known as the “lottery

hypothesis” (Sale, 1975, 1977, 1978, 1980, 1982; Sale & Dybdahl, 1975, 1978)
or the “equal chance” hypothesis (Connell, 1978).
The absence of linear correlations (or even any correlations) between adult
stock-size and recruitment (Sale, 1982), the enormously high reproductive output
and massive mortality of larvae, the inability of resident adults to influence the
relative ability of different species to recruit (Williams & Sale, 1981; Doherty,
1983), the almost total absence of negative correlations between the species (Sale
& Dybdahl, 1975, 1978; Talbot et al., 1978) and the broad habitats of most
species (Sale & Dybdahl, 1975) all point to communities in which competition is
not the primary force regulating species composition, but in which the variability
and unpredictability of recruitment are of major importance. Thus chance events
determine which species settle, but once the adults are established they may
saturate the environment and hold their habitats against intruders, limiting the
immigration of other adults or juveniles, as has been shown for pomacentrids (Sale,
1976), blennies (Stephens, Johnson, Key & McCosker, 1970), and for various
species already mentioned above (Hoese, 1966; Belk, 1975; Williams, 1978;
Hixon, 1980, 1981; Larson, 1980).
Advancing from this concept of a lottery other authors have suggested an
additional explanation of high diversity in coral-reef fishes: that they are not at
equilibrium and do not saturate their environment. Various reasons are proposed
to explain why fish populations may fail to fill their habitats. Inadequate
recruitment is one reason (Sale, 1977; D.McB.Williams, 1980; Stephens &
Zerba, 1981; Doherty, 1983). Russell, Anderson & Talbot (1977) describe ten-
fold variations in recruitment from year to year, and Talbot et al. (1978)
document substantial seasonal variations in numbers (although they also record
that recruitment to empty artificial reefs is greater than to those occupied by
adult fish). Predation (Talbot et al., 1978) and unusual water temperatures
(Bohnsack & Talbot, 1980) may also keep fish numbers below the carrying
capacity of the environment.
In a test of whether space for shelters limits the populations of coral-reef fish,
Robertson, Hoffman & Sheldon (1981) removed coral containing the territorial
mats of a damselfish, Eupomacentrus planifrons, or eliminated all of the coral in
half the habitat. Both treatments resulted in a concentration of the fish in the
remaining shelters, but despite being concentrated, the fish did not decline in
size, fat content or mass of ovaries. Consequently Robertson et al. concluded
that E. planifrons does not normally live at the carrying capacity of the
environment. Similarly Robertson & Sheldon (1979) added fish or reduced
shelters by blocking them up, but found no evidence that the shelter-holes were
in short supply. Removal of adult pomacentrids (D.McB.Williams, 1980) or of
Pomacentrus wardi specifically (Doherty, 1983) has no effect on the settling of
larvae from the plankton, the major avenue of recruitment in these fish. Again, this
suggests non-equilibrium conditions, as do the high variation in density and the
high rate of turnover recorded by Talbot et al. (1978) in a 3½-year study of

artificial reefs.
In summary, there are three views of how diversity is maintained in tropical
reef fish: the competition hypothesis (requiring that the species segregate their
niches because of competition and that the fish are in equilibrium); the lottery
hypothesis (in which random larval recruitment is a major factor dictating
community structure, even although equilibrium and competition between adults
may occur); and the non-equilibrium hypothesis (that the fish are held below
levels at which they saturate their habitats and competition is of little
significance in structuring the communities). These approaches are conflicting,
but they are not necessarily irreconcilable. The major prononents of all three
hypotheses show signs of softening their views to accommodate aspects of the
other hypotheses. For instance, Sale (1979, 1980) now recognizes that some
species are probably held below equilibrium levels, and Smith (1978) concedes
an element of randomness in larval recruitment. This merging of views can be
crystallized by focusing on three questions. (a) Do differences in scale and
duration explain different results? (b) Are results locality-specific? (c) Are there
differences between the mechanisms controlling adults and settling larvae?
Many of Sale’s critics suggest that he and his co-workers have worked on too-
small a scale or for too-short a time to allow equilibrium conditions to be
established. It is true that even two years after Doherty (1983) experimentally
eliminated one species from isolated reefs that recovery was very limited and
only between 27 and 48% of the original numbers had become re-established, so
criticisms such as this may be justified. Large-scale patterns (Anderson et al.,
1981), long-term temporal constancy (Ogden & Ebersole, 1981), and
predictable, seemingly deterministic recovery after disturbance over wide areas
(Brock, Lewis & Wass, 1979), all point to apparently stable community structure
which can be contrasted with Sale’s small-scale short-term stochastic patterns.
However, as Sale (1980, 1982) discusses, the lottery hypothesis also predicts
large-scale and long-term constancy—in fact, if it did not, a few species would
eventually come to dominate. He also points out that if experimental results are
to be accounted for, conventional competition theory seems inadequate. Sale’s
great strength is that he has based his conclusions on the outcome of experiments.
It is inevitable that such experiments are based on relatively small areas, for
purely logistic reasons, but at the same time, experiments of longer duration
would be welcome (if tedious). Helfman (1978) suggests that the contrasting
views may reflect real differences in the manner in which communities in
different localities are regulated. The Caribbean, where Smith’s school undertook
most of their work, may have communities that are “more deterministic” and
influenced by competition, while those of the Indo-Pacific, including the Great
Barrier Reef where Sale works, may be more influenced by chance events. Most
of Sale’s work was centred at the extreme southern tip of the Great Barrier Reef
where recruitment is most likely to be stochastic.
556 G.M.BRANCH
The final question is the most interesting for there do seem to be differences
between the ways in which adults and settling larvae are regulated. One specific
result is worth recalling. Doherty (1983), deliberately working on isolated-patch
reefs to preclude immigration of juveniles and adults, could detect no differences
in larval recruitment whether adult P. wardi were present or not. In contrast, Sale
(1976) concluded that adults of the same species inhibited colonization—but his
sites were not isolated and so colonists were mainly juveniles that immigrated
from adjacent patches rather than larvae which settled from the plankton. This
paradox is solved if larval recruitment is independent of existing adults, while
the adults may saturate sufficient of the habitat to suppress immigration of
juveniles. When larvae recruit to a population they are so small that territorial
fish do not take aggressive action against them. Even as they grow, they remain
small enough to shelter in small holes where they are safe from the threat of
larger residents. Sale, Doherty & Douglas (1980) refer to this as “topographic
deception”, and suggest that residents will have little choice but to habituate to
these small fish, even within their territories.
Smith (1978) ascribes to a similar view in discussing a compromise between
the conflicting hypotheses. He visualizes three successive “sieves”: (a) an
environmental sieve by which physical conditions select for certain suites of
fish; (b) a recruitment sieve in which chance plays a rôle in the arrival and
survival of larvae; and (c) a biological sieve which is deterministic and by way
of competition and mutualism sets limits on which species can coexist. Whether
chance or determinism plays the major rôle depends largely on whether the
larvae or the adults are more important in the establishment of populations, i.e.
the balance between the second and third “sieves”. This, in turn, partly depends
on how long-lived the adults are, and partly on factors such as predation and
physical conditions which may keep the adult populations at sub-saturation
levels. Talbot et al. (1978) calculated a 17 to 39% turnover of species per month,
and under such high rates of replacement chance events of larval recruitment
become of paramount importance.
Even in populations which are below the carrying capacity of the
environment, territorial defence is adaptive. From each adult’s point of view,
saturation is measured at the level of the defended shelter, where sufficient food
and shelter from predators can be attained. In the face of intense predation, to
leave or be ousted from a territory is potentially lethal. Thus intra- and
interspecific defence against intruders and grazers is logical even if all the
shelters are not saturated.
Clearly, in some fish territorial competition is of major importance, leading to
local exclusion and thus dictating community structure, while in coral-reef fish it
seems of much less importance, except in terms of the maintenance of individual
territories, with chance playing a dominant rôle in shaping overall community
structure. Rather than polarizing different hypotheses, we are likely to learn more
by focusing on the characteristics of different species and communities which
make one or other element more important. In determining whether species exist
at equilibrium or not, the rôle of predation is likely to be a key feature, and one
that has not been fully explored in most of the hypotheses. Certainly the view of
assuming competition as the dominant force structuring communities and
shaping the evolution of species is no longer tenable.
MECHANISMS OF COEXISTENCE
The preceding examples establish quite clearly that interspecific competition is
often an important controlling factor, influencing population size and structure,
growth rate, reproductive potential, and distribution. Equally clear is the fact that
competition is not the all-pervasive force it was once assumed to be. Competitors
or potential competitors often coexist without any sign that one species will ever
displace the other. In this section I review processes that permit coexistence,
drawing largely on examples discussed above. Broadly speaking, three types of
processes exist: (1) those that occur in populations which are at equilibrium and
saturate the environment; (2) those which prevent competitors from attaining
equilibrium densities and hold them below the carrying capacity of the
environment, thereby ameliorating competition, and (3) those which rely largely
on chance events which are unpredictable. These can be further subdivided as
follows.
(1) Equilibrium populations: (a) intra- versus interspecific competition, (b)

resource partitioning, (c) refuges in time or space, (d) changing
circumstances, and (e) intransitive networks.
(2) Sub-saturation populations: (a) predation, (b) other competitors, and (c)
disturbance.
(3) Rôle of chance: (a) variations in larval recruitment, (b) historical events, and
(c) interactions between populations.
These processes can be complementary and can function in parallel, but often
one prevails in a particular environment or in competition between particular
kinds of organisms.
Intraspecific versus interspecific competition in equilibrium

populations
When two species compete by exploitation it is usually true that intraspecific
competition will be more intense than interspecific competition, for the needs of
conspecifics are more similar than those of different species. This fact is of
fundamental importance for it means that as a species increases in density it will
affect members of its own species more than those of its competitor.
In comparing three gastropods, Underwood (1978) was, for instance, able to
show that an increase in the density of the dominant species, Nerita atramentosa,
had a far more radical effect on that species than it did on two other species,
558 G.M.BRANCH
Cellana tramoserica and Bembicium nanum. Similarly, although Cellana

tramoserica is dominant over Siphonaria spp. (Creese & Underwood, 1982), the
effect of intraspecific competition on Cellana tramoserica exceed its effects on
Siphonaria spp. In these two instances, the consequences of intraspecific
competition are so severe, that they lead to mortalities at high densities,
preventing the dominant species from ever attaining densities at which it could
exclude the subordinate. Thus, competitors can coexist at equilibrium providing
the effects of intraspecific competition are greater than interspecific competition.
This condition is rarely satisfied if species compete by interference, when
conspecifics are likely to be equally matched but interspecific duals often occur
between illmatched individuals. Thus interference more regularly leads to
exclusion, as discussed in more detail below.
While intraspecific competition will favour range expansion to reduce the
consequences of competition, interspecific competition is more likely to cause a
contraction of range (e.g. O’Connor, Boaden & Seed, 1975, exemplified above,
p. 481). The balance between inter- and intraspecific competition will thus
determine the range the species occupies. A species will only contract its range
until the intensity of intraspecific competition exceeds that of interspecific
competition (see, for example, Fig. 2. p. 434).
Resource partitioning
The most conventional view of coexisting competitors is that competition in the
past has caused the competitors to evolve niches which are sufficiently different
that they can continue to coexist. Schoener (1974) has reviewed this approach
and concludes that most species (55%) partition their physical habitats, while
fewer (40%) partition their food resources, and only a small proportion (5%)
partition time (by season or by diel differences) to avoid competition. A
comparable break-down exists in marine organisms if one analyses the examples
discussed in the preceding section: 49% partition their habitats, 40% their food
resources, 10% partition by time, and 1% by using different proportions of
nutrients.
To illustrate, marine organisms partitioning their physical habitats include
epifaunal species living on algae, which use different portions of the plant
(reviewed by Seed & O’Connor, 1981; and see Bernstein & Jung, 1979); limpets
and littorinids which occupy different regions of the shore (e.g. Choat, 1977;
Black et al., 1979), birds which feed in different parts of the shore or at different
distances out to sea (e.g. A. Crowe, pers. comm., see Fig. 37, p. 516; Cody,
1972, see Fig. 36, p. 515), and bivalves that occur at different depths in the
sediment (Peterson & Andre, 1980). Species that may use different food
resources to reduce competition include the gastropods Conus spp. (e.g. Kohn,
1966, 1978), Hydrobia spp. (Fenchel, 1975b), Patella spp. (Branch, 1976), and
the sunfish (Werner & Hall, 1976, 1977). Apportionment of time is easy to
imagine in species that become abundant or more active at different times of the
year (e.g. Paine, 1962, 1963; Wells, 1970; Spight, 1981), or which occupy the
same habitat but at different times of the year, as do some epiphytic species
living on kelp (Bernstein & Jung, 1979; Seed, Elliott, Boaden & O’Connor,
1981). Diel differences in the time of feeding may reduce overlap between birds
(e.g. A. Crowe, pers. comm., see Fig. 37, p. 516; Ashmole, 1968), and fish
(Ebeling & Bray, 1976; reviewed by Helfman, 1978). Many other possible cases
of resource partitioning are given in the preceding section of this review.
Before accepting that such differences are either caused by past competition or
achieve ecological differences that are required to avoid competitive exclusion,
several key questions need to be answered. First, is competition occurring?
While it is possible that competition which has occurred in the historical past
drives species apart and reduces niche overlap, I do not believe that this process
will ever lead to a total elimination of competition. For one thing, what will
continue the process of divergence once competition becomes of little
significance? For another, what maintains differences between the species once
competition is non-existent? Niche expansion due to intraspecific competition is
almost certain to bring the two species together again if the only reason for their
initial divergence was interspecific competition. Thus, I believe it is imperative
that at least mild competition be documented between species before
competitioninduced divergence is invoked, or differences between species
assumed to exist as means of avoiding competition.
Secondly, are differences between the species such as to alleviate competition
for limiting resources? Most differences are a simple reflection of the fact that
species have their own unique characteristics, and these do not necessarily have
to be adaptive in terms of competition but may be moulded by a wide range of
other selective agents. It is also necessary to guard against regarding differences
as a means of avoiding competition when they may be the outcome of
competition. For example, when subordinate species are excluded from part of
their fundamental habitat by a dominant species (e.g. Kinzie, 1968; Choat, 1977;
Hixon, 1980, 1981; Bertness, 1981a, b), the lack or reduction of niche overlap
reflects intense competition, not that an evolutionary process has led to its
reduction.
Thirdly, are the differences between the species heritable or phenotypic
responses to prevailing conditions? Phenotypic differences may still be of
survival value and, I believe, can reduce competition, but they cannot be part of
an evolutionary change leading to divergence if they have no genetic basis. This
issue is amplified in the concluding section of this review (p. 574).
Connell (1980) has raised similar issues in discussing the ‘ghosts of
competition past’ and outlines tests whereby valid cases of niche apportionment,
arising from past competition, can be distinguished. These include experimental
removal of a presumed competitor (to test for competitive release, thereby
demonstrating competition); and transplants of both competitors, with suitable
controls (to test for heritability of characteristics). A different approach is to
supply the organisms with increased amounts of the resource that is presumed to
560 G.M.BRANCH
be limiting and to determine if this reduces competition in the short term or leads
to an increase in the populations of one or both species. In cases where
experimental manipulations are not possible, patterns of apparent resource
partitioning need to be statistically analysed to ensure that they are not simply
random events.
In the literature summarized above, there are 65 cases in which resource
partitioning may play a rôle in reducing competition or has been invoked to
explain coexistence. In 72% of these cases there is no evidence that the presumed
competitors are actually competing. Of course, competition may still be
occurring although it has not been proven; even so, only 36% of the examples
are based on ecological differences which could feasibly provide means of
coexistence. Six of the cases involved character displacement which seems to be
linked to competition, only appearing in sympatric populations of competitors,
and these are worth isolating and examining further.
Fenchel’s (1975b) description of consistent displacement of body size in
coexisting Hydrobia spp. (p. 500) is most convincingly linked to reduction of
competition. Competition does occur between the species, is linked to similarity
of body size, and has been demonstrated to be reduced by differences in body
size (Figs 31 & 32 see p. 499). There is, however, little evidence that the
displacement is genetically controlled, apart from a hint that displacement of
reproductive seasons in sympatric populations may, to a limited extent, persist
when the animals are held in isolation (Fenchel, Frier & Kolding, 1977).
The displacement of body size in coexistent populations of Sphaeroma spp.
(p. 505) has been related to a shortage of shelter-holes of a size corresponding to
the body size of the two species, but although this is a plausible explanation of
the reason for shifts in body size, there is no proof that the species are
competing, or that the differences in body size are genetically controlled (Frier,
1979a, b). Similar reservations can be expressed about the divergence of body
size in sympatric populations of the starfish Astropecten spp. (Ribi, Schaser &
Ochsner, 1977) described above (p. 457, Fig. 13). Fossil radiolarians provide one
of the few examples in which displacement of body size can be followed in time
(Kellogg, 1975) and shows that one species, Eucyrtidium calvertense decreased
in size during a period of sympatry with E. matuyamai, shifting its body size
away from that of this species, but remaining unchanged in size before the period
of sympatry and after E. matuyamai became extinct. It would be unfair to expect
evidence of genetic control in this case, but it would strengthen the argument if
modern radiolarians could be shown to compete in a manner that is reduced by
differences in body size.
Evidence of genetic differences between sympatric and allopatric populations
of two Mytilus spp. does exist (Harger, 1972c, and see p. 477) but these
differences seem related to differences in physical conditions rather than to the
presence or absence of a competitor. Even the characteristics which allow one of
these species to dominate in sheltered areas and the other on wave-beaten shores
are unlikely to have evolved in response to competition, even although they are
responsible for continued coexistence in intermediate areas. One case in which

divergence between coexisting species is certainly genetically controlled is the
shift of frequencies of eight alleles controlling the enzyme leucine
aminopeptidase (Lap) in acmaeid limpets (Murphy, 1976). This case is discussed
in more detail below (p. 570) in relation to genetic variability but, for the
present, it must be stressed that although character displacement clearly occurs in
sympatric populations, and is genetically controlled, we have no idea of what
significance the various Lap alleles have in reducing competition between the
species, or even what the ecological significance of the different alleles is.
Other examples of ‘character displacement’ involving shifts of
behaviour, such as a displacement of preferences for certain particle sizes (see p.
504, Fig. 34) or changes of habitat ‘preferences’, I believe, are more likely to
reflect competitive exclusion from a preferred habitat than true character
displacement. Thus, as Grant (1972, 1975) concluded for earlier examples, there
is no single case of character displacement which satisfies one that it is
repeatable, does effectively reduce competition, is induced by competition rather
than other selective agents, and is heritable. This does not mean that we should
discard the concept. First, the lack of evidence in certain areas is partly due to a
failure to seek for the evidence, not necessarily that it does not exist. Secondly,
even if ‘character displacement’ proves to be phenotypic in some instances, this
does not deny its ecological significance as a means of reducing competition.
Even with these provisos, it is evident that the case for niche apportionment,
as a competition-driven means of reducing competition, is not nearly as strong as
much ecological theory implies it to be. Connell (1978) has argued forcibly that
because competitors do not depend on each other that co-evolution between them
is far less likely to occur than, for instance, between predators and prey, parasites
and hosts, or mutualistic species, which are obliged to coexist or which benefit
from living together. On this basis, character displacement will be an infrequent
event. It is most likely to occur (or to have occurred) in organisms which are
relatively sedentary, which share resources that are localized, and which are
isolated from other populations. Possible examples are Hydrobia spp. (Fenchel,
1975b), Conus spp. (Kohn, 1966, 1978; Kohn & Nybakken, 1975, and see p. 460),
Patella spp. (Branch, 1981; and see Fig. 23 and p. 575), the starfish Astropecten
spp. (Ribi et al., 1977), the radiolarians Eucyrtidium spp. (Kellogg, 1975) and the
isopods Sphaeroma spp. (Frier, 1979a, b).
Refuges in time or space

Even if a species is sufficiently dominant to exclude totally a subordinant from
its habitat, it presents no long-term threat to the survival of that species unless
the inferior competitor has a habitat that falls wholly within that of the dominant.
Refuges beyond the reach of a dominant competitor allow persistence and
continued invasion of the habitat held by the superior competitor. Several
examples have been given above. For instance the limpet Patelloida latistrigata
562 G.M.BRANCH
shelters amongst barnacles which prevent the invasion of a dominant competitor,

Cellana tramoserica (Creese, 1982), and another limpet, Patella longicosta, is
subordinate to P. cochlear but has a wider zonation, occurring above and below
P. cochlear (Branch, 1976). Many cases of aggressive interference and
territoriality allow the dominant to hold a narrow niche while the subordinate
survives in a refuge beyond this habitat, as exemplified in fish (e.g. Sale, 1975;
Hixon, 1980, 1981), mantis shrimps (Kinzie, 1968; Dingle et al., 1973; Caldwell
& Dingle, 1979), shrimps (Thorp, 1976; Coen, Heck & Abele, 1981), and
freshwater crayfish (Bovbjerg, 1969). High-shore refuges allow barnacles
(Connell, 1961a) and mussels (Suchanek, 1978) to survive beyond the reach of
species that are capable of overwhelming them. Jackson (1976) has suggested
that in coralreef ecosystems small surfaces provide refuges, for once a species has
covered a small area it will preclude further settling and will be immune
to overgrowth by lateral expansion of adjacent competitors. On larger areas,
there is a greater chance that another colony will settle close to an individual and
ultimately overwhelm it by lateral growth. Osman (1977) could not, however,
detect any larval preferences for small substrata, although larvae may avoid
substrata already bearing competitors (Grosberg, 1981).
Paine & Levin (1981, see also Levin & Paine, 1974; Levin, 1981) have argued
that spatial heterogeneity, generated by disturbance in intertidal communities,
allows opportunistic species to colonize empty patches amongst otherwise
continuous bands of dominant competitors. They even suggest that the life cycles
of the fugitive species are geared to allow settling during the period when storms
are most likely to provide fresh patches for colonization.
Thus refuges may be temporally and spatially dynamic, depending on the
disturbance of superior competitors, or there may be areas which are
permanently beyond the reach of dominant competitors.
Changing circumstances
Competitive supremacy can be fickle, conditions reversing the rôle of dominant
and subordinate. The interaction between the mussels Mytilus edulis and M.
californianus demonstrates this: the former is supreme in quiet waters, the latter
gains ascendency in exposed areas (Harger, 1972c). Both species, therefore, have
refuges in which they dominate and from which they can continue to recruit into
areas which are predominantly occupied by the other species—an instance of
reciprocal niche overlap. Similarly, competition between the reef worm
Phragmatopoma californica and the anemone Anthopleura elegantissima is
tipped in favour of the latter by exposure to desiccation or by inundation with
sand (Taylor & Littler, 1982). Three Hydrobia spp. have different tolerances and
salinity optima, so that fluctuations in estuaries may allow them to dominate at
different times of the year or in different parts of the estuary (Fenchel, 1975a).
Hutchinson (1961) has argued that short-term changes in conditions are important
in preventing competitive exclusion in zooplankton.
Arguments such as these are two-edged for, as Wiens (1977) has pointed out,
if the environment fluctuates widely in time, competition will only occur during
‘crunches’ when conditions deteriorate and resources become limiting. This
approach pre-supposes, however, that populations do not respond to favourable
conditions quickly enough to expand and become limited by competition, even
although resources are more abundant.
The impact of a competitor may also depend on biological interactions. As an
example, limpets normally have an adverse effect on barnacles (and vice versa)
but their presence is essential to the barnacles in the low- and mid-shore if algae
are to be prevented from dominating and eliminating the barnacles (Underwood,
Denley & Moran, 1983). In a similar manner, grazing by urchins has a negative
effect on some corals but in the absence of grazing, some corals are out-
competed by algae while others do better. Since damselfish reduce the grazing of
urchins within their territories, a number of factors can combine to determine
which coral species thrive (Sammarco, 1980; Sammarco & Williams, 1982).
Furthermore, the damselfish themselves attack different species of corals
differentially, protecting and allowing pocilloporids to dominate in the shallows
while massive corals are more abundant in deeper waters where the damselfish
are scarce (Wellington, 1982a and see p. 446).
Competition between the ascidian Styela and the bryozoan Schizoporella
favours the latter if it settles first, or if fish graze away the Styela, but if Styela
settles beneath a colony of Tubularia it is protected from grazing and dominates
over Schizoporella (Sutherland, 1974, 1978). Isopods mediate in competitive
interactions between bryozoans and encrusting coralline algae (Woodin &
Jackson, 1979). The hermit crab Clibanarius is competitively dominant over
Pagurus, but the rôles are reversed if Pagurus carries hydroids on its shell
(Wright, 1973).
There are thus many instances in which competitive domination depends on the
presence or absence of a third party—a theme that is expanded in more detail
below, in relation to the rôle of predators.
Intransitive competitive networks

While species can sometimes be ranked in a transitive competitive hierarchy in
which one species is out-competed by a second, which is subordinate to a third
and so on, Buss & Jackson (1979) and Buss (1980) have described several
intransitive situations in which species A out-competes B, and B out-competes
C, but C is dominant over A. Their examples are drawn from coral-reef
environments and are based on cryptic sessile species in widely different
taxonomic groups, which compete principally by overgrowth or by the
production of allelopathic chemicals. Connell (1978) could, however, detect no
such circular competitive pathways between 12 species of corals which he
investigated over a period of nine years.
564 G.M.BRANCH
Corals exhibit an array of competitive mechanisms, one mechanism frequently

countering the advantages temporarily gained by another (see Sheppard, 1982
for a review). High growth rate may be countered by mesenterial digestion (Lang,
1973), mesenterial digestion by the development of sweeper tentacles
(Richardson, Dustan & Lang, 1979), overgrowth by allelochemicals (Jackson &
Buss, 1975), and rapid growth and superior competitive ability may be balanced
against higher reproductive output and better colonizing ability (Bak & Engel,
1979). Circular competitive interactions could in theory lead to perpetual
coexistence, no single species ever attaining total ascendancy. In practice, most
interactions are more complex than this, forming networks of a few species that
are more dominant than others, but without any one species ever becoming the
overall winner. The epifauna of large algae exemplifies this situation (O’Connor,
Seed & Boaden, 1979; Seed & O’Connor, 1981).
Furthermore, the strength of competitive dominance at each step in transitive
networks may vary and can even be reversed. The angle at which colonies
approach as they grow together (Jackson, 1979; Rubin, 1982), the relative
thickness (Buss, 1980) or growth rates of two colonies (Sebens, 1982) can all
determine which colony gains supremacy. The extraordinary variety of
competitive mechanisms, the intransitive nature of many interactions, and the
number of factors that can reduce or reverse dominance all make it extremely
difficult to predict the outcome of such competition. Buss & Jackson (1979)
originally suggested that intransitive rings and networks may prevent
competitive exclusion, but later Buss (1980) concedes that they will only slow
down the process of exclusion, thereby reducing the importance of other factors,
such as predation and disturbance, which prevent dominant species from
monopolizing particular habitats.
The rôle of predators

All the processes outlined above, which may reduce the impact of interspecific
competition, occur in populations at equilibrium, which are living at or near the
carrying capacity of the environment, but predators or disturbance may hold
competitors at lower levels where competitive exclusion is unlikely. Paine’s
(1971, 1974) very dramatic experiments show that the experimental exclusion of
starfish may lead to the monopolization of the lower shore by mussels with
consequent competitive elimination of several species and a reduction in
diversity. The convincing nature of these results have made it a paradigm that
rocky shore communities are regulated more by predators preventing competitive
exclusion than by competition. There is a danger of accepting this concept
uncritically, and several authors have blindly fitted their data to this model
without testing whether predation does play such a rôle in the particular
communities with which they have worked.
It is true that there are many examples of predation preventing competitive
exclusion, and of herbivory fulfilling the same rôle among plants. Predatory
starfish may account for the high diversity of sponges in benthic Antarctic
communities (Dayton, Robilliard, Paine & Dayton, 1974), and biological
disturbance, including predation, may account for the surprisingly diverse
communities in the deep sea (Dayton & Hessler, 1972). The epifauna growing
within coral-reef caves (Day, 1977) and on experimental plates (Russ, 1980;
Mook, 1981) declines in diversity due to competitive exclusion if predators are
prevented from grazing on these surfaces. Crabs (Kitching, Sloane & Ebling,
1959; Peterson, 1979a), starfish (Paine, 1971, 1974; Menge, 1976), and
predatory gastropods such as Thais (Connell, 1961b, 1970; Dayton, 1971;
Menge, 1976; Lubchenco, 1980) can all be responsible for preventing particular
organisms such as mussels and barnacles from dominating the intertidal zone,
and predators can transform subtidal mussel beds into areas in which red algae
and a variety of cryptofauna abound (Lubchenco & Menge, 1978). Coral
diversity seems to be increased by moderate fish or urchin grazing (Wellington,
1982a; Sammarco, 1982).
There are also particular species that depend on grazing or predation for their
existence. Grazing by the urchin Arbacia promotes the hydroid Hydractinia
(Karlson, 1978), and Macrocystis sporelings are smothered by sessile colonial
animals unless these are preyed upon (Foster, 1975). Amongst algae, early
colonizers may maintain themselves and inhibit succession unless grazed by
organisms such as crabs (Sousa, 1979b). Algal turfs are inferior competitors but
survive where most other algae are eliminated by grazing or desiccation, because
they are more resistant (Hay, 1981). Encrusting coralline algae are particularly
susceptible to overgrowth and smothering by other algae unless they are grazed
(Paine, 1980) and some of them have co-evolved with their grazers (Steneck,
1982).
On the other hand, predators sometimes have no effect on the diversity
(Sutherland & Karlson, 1977; Keough & Butler, 1979), and in many instances
they reduce diversity as, for example, in the cases of algae grazed by fish and
urchins (Stephenson & Searles, 1960; Paine & Vadas, 1969; Day, 1977) and soft-
bottom communities preyed upon by fish and other organisms (reviewed by
Peterson, 1980). Some groups of organisms respond ambivalently to predation,
sometimes increasing in diversity, sometimes decreasing, as is the case in algae
(Jones & Kain, 1967; Paine & Vadas, 1969; Lubchenco, 1978; Brock, 1979;
Brawley & Adey, 1981; reviewed by Lubchenco & Gaines, 1981, and discussed
above p. 487), and corals (Porter, 1972, 1974; Glynn, Stewart & McCorker,
1972; Glynn, 1976, 1980, 1983; Glynn, Wellington & Birkeland, 1979).
Predictions of the effect of predation on competition are made more difficult
by ‘cascade effects’. For example, predation by otters or lobsters restricts urchin
numbers, urchins sometimes attack competitively dominant algae, permitting
fugitive species to thrive (Estes & Palmisano, 1974; Duggins, 1980; Breen,
Carson, Foster & Stewart, 1982), but sometimes eliminate all available algae
(Paine & Vadas, 1969; Mann & Breen, 1972). Even this cascade ignores the
possible rôle that sea otters must have played in this system before they became
566 G.M.BRANCH
virtually extinct (Dayton, 1975a). Similarly, the crab Carcinus maenas shelters in
pools filled with Enteromorpha and preys upon Littorina, which feeds upon the
Entermorpha, preventing its competitive exclusion of subordinate algae and thus
maintaining high algal diversity in pools—but only provided the activities of the
crabs are not sufficient to reduce the littorines (Lubchenco, 1978). Furthermore,
predators may exert their effect by merely altering the behaviour of prey species,
as Bernstein, Williams & Mann (1981) have shown for urchins preyed upon by
lobsters, so their effect can be disproportionately greater than their direct
influence on prey numbers. Predation may also increase competition rather than
reduce it if the limiting resource is space in which to shelter. This often seems
the case in the tropics where predation is intense (Menge & Lubchenco, 1981)
and where, for instance, urchins (Grünbaum et al., 1978) and fish (Smith &
Tyler, 1972) shelter in crevices and coral heads.
Thus the effect of predation on competition and species diversity is not a
straightforward one. Analysis of 38 examples cited in this review, in which the
impact of predators has been experimentally tested, reveals that predation
increases diversity in 58% of the cases, but decreases it in 21%, while in 16% it
decreases or increases diversity depending on circumstances, and in 5% of the
cases it has no effect on diversity.
Several authors have developed generalized models to try and explain when
predation will supplant competition as a dominant force structuring
communities. Menge & Sutherland (1976) suggest that at high trophic levels
competition will be more important, as there are fewer predators (or even none)
capable of keeping down the numbers of top predators, which consequently are
more likely to be limited by food. Possible examples include fish-eating sea
birds, starfish, and whales. On the other hand, they argue that populations of
primary consumers are more likely to be restricted by predators. Reference to
Table I shows, however, that the impact on species diversity is not linked in any
obvious way with trophic level. This is confirmed by analysing the kinds of
organisms which are regulated by
TABLE I
The impact of predators in increasing or decreasing the diversity of communities, in
relation to the dominant functional group in each community: the number of cases
investigated in each instance is given (n), and the data given as the percentage of cases in
each category.
Functional group n % increased Diversity % unchanged % decreased
Algae 25 40 0 60
Corals 7 57 0 43
Mussels 8 100 0 0
Other sessile filter-feeders 10 80 20 0
Zooplankton 2 100 0 0
Fauna of soft sediments 10 0 30 70
predators in such a way as to prevent their competitively excluding other species

—i.e. predation brings about an increase in diversity. Fifty per cent of these
organisms are sessile filter-feeders, 33% are algae, 13% are sessile carnivores
such as corals, 4% are planktonic particle-feeders, while none are mobile deposit-
feeders, herbivores or carnivores. From this it appears that the nature of the
resource that is being competed for is more important than trophic level. With
the exception of the few planktonic forms, all the species regulated by predators
in the manner outlined above are competing for space, while most of these
groups in which predators have never been shown to influence diversity are
mobile and more likely to compete for food. This issue is raised again below.
Various patterns emerge in Table I. Sessile filter-feeders have the capacity to
monopolize space, and almost invariably predation increases diversity in
communities of filter-feeders by breaking this monopolization and creating
patches or zones that are free for other organisms to colonize.
Algae sometimes increase and sometimes decrease in diversity when grazed.
Lubchenco & Gaines (1981) have proposed that the outcome depends on
whether the dominant or the subordinate species are preferentially grazed. They
also suggest that in many algae competitive ability is inversely related to the
ability to resist grazing, although they do record exceptions. A similar argument
can be made for corals, on which substantial predation takes place (Glynn et al.,
1972, 1979), although the impact of predators on coral diversity is not as well
documented. Porter (1972, 1974) records an increase in diversity due to
predation by the starfish Acanthaster (although this is due to a change in the
proportion of corals—evenness— and not to the appearance or disappearance of
species, since sites with or without Acanthaster have the same species
composition). Coral diversity is also increased by intermediate levels of grazing
by urchins, but this is due to the elimination of algae that would otherwise
smother the corals (Sammarco, 1982). On the other hand, Glynn (1976, 1980,
and see 1983) has shown that symbiotic crustaceans living in the heads of a
dominant coral, Pocillopora, protect the coral against attack by Acanthaster.
Under these conditions diversity decreases due to the predator switching to
massive corals which are less efficient competitors and do not support symbionts.
This may be a rather special case but, as in the algae, it illustrates that the rôle
predators play depends on whether they attack competitive dominants or
subordinates.
In soft-bottom communities, predators have little effect on the diversity of
organisms associated with sea-grass beds, the rooted plants evidently providing
protection against predators. But in areas lacking plant cover predators reduce both
biomass and diversity (as reviewed by Peterson, 1979b, and outlined in more
detail above, p. 507). In essence this is because competitive exclusion and
monopolization are far more difficult to achieve in soft sediments, so that
predators are not required to prevent these effects. Thus, communities dominated
by particular groups of organisms respond in different ways to predators.
568 G.M.BRANCH
Menge & Sutherland (1976) also propose that complex communities with
many trophic links are more probably regulated by predators, and simple
communities by competition. This may be true, but the more important question
is why some communities are simple and others complex. Menge & Sutherland’s
example of a simple community, for instance, is a wave-beaten shore dominated
by filter-feeders. The stress of wave action will exclude most organisms, and
particularly mobile predators, but dense beds of sessile filter-feeders thrive under
these conditions and may experience intense competition. Quiet waters permit a
much wider range of organisms and allow predators to live and feed effectively,
reducing competition (Ebling, Kitching, Muntz & Taylor, 1964; Menge, 1976;
Peterson, 1979a). Thus the rôle of predators is influenced primarily by the
physical stress of the habitat, not the complexity of the community per se.
Connell (1975) has developed a model of the rôles of competition and
predation, which incorporates both prey size and physical stress (Fig. 41). Prey
that are very large or very small (relative to their predator) are likely to escape
predation. Predation will also probably decline in physically more harsh habitats,
where death of the prey is more often due to physical factors. Under stressful
physical conditions large body size will reduce mortality. Thus, we have an
interplay of body size and physical stress suggesting that, on the one hand,
predators are likely to regulate populations in benign habitats and when the prey
is intermediate in size, while, on the other, physical factors keep numbers low in
harsh habitats and particularly if the species is small. In between these extremes
is a region of lower mortality in which competition is likely to be more
important, and it is clear on the basis of this model that large prey are most likely
to compete.
Size has a further important consequence not predicted by Connell’s model.
Predators that consume prey very much smaller than themselves are normally
indiscriminate feeders and are more likely to eliminate certain species and reduce
diversity than selectively to attack dominant competitors and thereby increase
diversity. Furthermore, they may feed on the juveniles of organims that would
attain a large size (and often relative immunity to predation) were they not
eliminated at an early stage. Grazers such as limpets and chitons, which can
totally prevent recruitment of algae by removing all sporelings, are good
examples of this effect (Hawkins & Hartnoll, 1983). Table II shows that very
small prey do tend to have their communities impoverished by predation, while
an increase in diversity is more likely to be caused by predation on large prey.
Thus a variety of factors impinges upon whether predation or competition
plays a dominant rôle, including physical stress, relative size of the organisms,
nature of the substratum, and possibly trophic level but more likely the nature of
the resource competed for. One final point is that
TABLE II
The effect of predators in increasing or decreasing the diversity of communities, in
relation to the size of the prey relative to the predator: prey were ranked as 1 (larger or
Fig. 41.—Connell’s (1975) model relating size of prey to the intensity of predation under
different degrees of physical stress: in benign environments predation is more intense
(contours—predation 1–3) while in physically harsh habitats death due to physical stress
is increasingly more likely (contours—stress 1–3); the shaded area shows intermediate
conditions where perhaps competition is more intense.
equal to size of predator), 2 (smaller than predator but not <5% size of predator), or 3 (<5%
size of predator) and the data averaged for each functional group; the number of data in
each category is given by n.
Average ranked size of prey
Functional group Diversity increased Diversity decreased
Algae 1·36 (n=11) 2·36 (n=15)
Corals 1·00(n=4) l·33(n=3)
Sessile colonial filter-feeders l·75(n=8) —
Mussels 1·87 (n=8) —
Fauna of soft sediments — 2·70(n=7)
Overall mean 1·54 (n=31) 2·33 (n=25)
predation does reduce competition and increase diversity in many instances, but
it can also reduce competition even when it is reducing diversity. It is the
intensity of predation that is important, not whether it increases or decreases
diversity.
Other competitors
It is possible that a competitor can play the same rôle as a predator in mediating
between two competing species. The only concrete case in which this has been
shown involves the interaction between two coral-reef urchins, Diadema
antillarum and Echinometra viridus. Experimental removal of either urchin leads
to an increase in the numbers of the other (Williams, 1981), demonstrating
competition between them. If damselfish (Eupomacentrus planifrons) are
570 G.M.BRANCH
excluded from a reef there is a rapid increase in the numbers of Diadema, which
move into the damselfish territories within a matter of days and eliminate most
of the algae previously defended there. Since the damselfish interact much more
aggressively with Diadema than Echinometra (Williams, 1979) the latter can
occur in the upper coral branches within damselfish territories, but the former is
excluded. Thus, the damselfish may be responsible for spatial partitioning of the
environment between the two competing urchins, and in this sense is a “non-
carnivorous key-stone species” (A.H.Williams, 1978, 1980). Other examples like
this are likely to come to light now that we are aware of the possibility, but will
probably only function in this manner if two species are competing by
exploitation of a common resource but are kept apart by a third competitor that
competes in a different manner—say by territorial interference—and for a
different resource.
Physical disturbance
Disturbance may act in the same way as predation, maintaining nonequilibrium
conditions under which competition is reduced and exclusion unlikely. A wide
range of factors can achieve this. Battering of intertidal shores by logs (Dayton,
1971), the scraping of seals over rocks at their hauling-out sites (Boal, 1980),
unusually heavy rainfall (Leviten & Kohn, 1980), burial by sand (Taylor &
Littler, 1982), the rolling of boulders (Osman, 1977, 1978; Sousa, 1979a), storms
(Glynn et al., 1972; Dayton, 1973b; Grigg & Maragos, 1974; Levin & Paine,
1974; Connell, 1976, 1978; Grant, 1977; Paine, 1979; Menge, 1979; Porter et
al., 1981; Paine & Levin, 1981; S.A.Levin, 1981), and unusually low tides
(Fishelson, 1973; Loya, 1976; Benayahu & Loya, 1981; Seapy & Littler, 1982)
are all largely unpredictable events which can decimate communities or sections
of communities, often reducing diversity initially but allowing less competitively
able species to occupy areas cleared of dominants. In some instances disturbance
causes compensatory mortality. For example, Connell (1978) found that corals
ranking highest in the competitive hierarchy suffered most from hurricanes,
principally because they are upright branching forms that grow above other
corals. Thus, the competitive inadequacies of low-ranking species are
compensated for by their greater survival in the face of storm damage.
In several of the above cases intermediate levels of disturbance are associated
with maximum diversity. Sousa’s (1979a, b) work on boulder beaches shows
highest algal diversity occurs on boulders of intermediate size, which are neither
so unstable as to preclude most species nor so stable as to permit a low-diversity
climax community developing, in which most opportunistic species are
excluded. The same pattern is displayed by the epifauna growing on boulders
(Osman, 1977). Prolonged and repeated exposure to air kills many species,
reducing diversity (Seapy & Littler, 1982). More moderate or intermittent
exposure increases diversity in coral reefs, but perpetually submerged coral
communities are not subject to this disturbance and have a high cover of corals
Fig. 42.—Relationship between diversity of coral species and per cent cover of corals: the
dashed line is for samples in 1972 after hurricanes had damaged some slopes (′ ) but left
some undamaged (′ ); the solid arrowed lines and (′) indicate changes occurring from
year to year over 10 years; (after Connell, 1978).
but a lower diversity—presumably due to competitive exclusion of some species

(Connell, 1978).
Results such as these have led to the intermediate disturbance hypothesis
(Connell, 1978, 1979; Fox, 1979) that highest diversity is maintained at
intermediate levels of disturbance. At least three elements determine what can be
regarded as intermediate: the frequency of disturbance, the time since the last
disturbance, and the intensity of disturbance. To exemplify this, Connell (1976,
1978) has summarized the diversity of corals (number of species per sample) at
Heron Island on the Great Barrier Reef in relation to the per cent cover of live
corals—which is some indication of the level of disturbance experienced at
different sites (Fig. 42). Intermediate levels of coral cover are associated with
highest diversity. Furthermore, Connell has followed the fate of corals within
marked quadrats over nine years, including two years in which hurricanes
occurred. One such site is shown in Figure 42, and reveals that coral diversity
rises rapidly after a disaster has eliminated most of the coral, but that the rate of
increase falls as coral cover rises, and diversity even shows some sign of
declining at high densities.
Thus, some critical level of disturbance achieves maximum diversity. Above
this level conditions are too harsh for some species, but below it competition
plays a rôle in dictating community structure. Huston (1979) has combined both
elements into a single model (Fig. 43). His concept is that diversity is determined
by two groups of factors.
(1) Factors determining the rate at which species can displace one another by
competition. If physical conditions are very benign, the environment
uniform, nutrient levels high, productivity high, and if the reproductive
potential of the populations is great, then one (or a few) species is likely to
win the competitive scramble, and the rate of displacement will be high, or
early colonizers will grow so profusely that they will perpetually out-
compete late successional species normally regarded as better competitors
572 G.M.BRANCH
Fig. 43.—A, the relation between rate of environmental disturbance and species
diversity; B, influence of rate of species replacement on species diversity; C, three-
dimensional plot showing the combined effect of disturbance rate and replacement rate
on species diversity; lines A and B show the curves plotted in Fig. 43A and B.
(Birkeland, 1977). Competitive monopolization will be reduced by poorer

conditions, a more heterogeneous environment, and slower rates of growth.
Diversity will thus rise. Of course, there reaches a limit below which any
further deterioration of physical factors will lead to a decline in diversity as
fewer species can tolerate the harsher conditions (Fig. 43B).
(2) Factors that disturb the community. Increased predation rate, increased
herbivory of plants, or physical instability of the habitat may continually
disturb the community, reducing numbers and preventing a climax state.
This can prevent a dominant species from ever monopolizing the habitat,
thus increasing diversity. Conversely, if biological or physical disturbance is
too frequent, then very few species can colonize and grow before the next
disturbance. Between the two extremes there is a happy medium where
diversity is greatest (Fig. 43 A).
These two suites of factors act in concert. For instance, in a very unproductive
habitat stable conditions will be needed to sustain life, for frequent disturbance will
prevent the slow-growing organisms from establishing themselves. Conversely,
in very productive environments a high rate of disturbance will be necessary to
prevent monopolization of the habitat by the dominant competitors.
The interplay between these two aspects can be visualized by plotting both
against diversity in a three-dimensional graph (Fig. 43C). Competition is likely
to be the dominant force when physical conditions permit high productivity (high
rates of displacement), and when rates of disturbance are low (low predation,
infrequent environmental changes).
The rôle of chance: lotteries of larval recruitment

Whether species are living in equilibrium or at levels below the carrying capacity
of their habitats, larval dispersal and recruitment introduce an element of chance
into the local persistence of populations. Fluctuations in recruitment can be
considerable (e.g. Hawkins & Hartnoll, 1982) and may shift the competitive
dominance from one organism to another, sometimes leading to cyclic changes
in communities (Hawkins & Hartnoll, 1983). Furthermore, even when it is
possible for one competitor to oust completely a subordinate locally, it is very
unlikely that it will ever do so at all localities, so that by colonizing refuges
where a dominant is absent or reduced in numbers, an inferior competitor can
perpetuate itself and even continue to invade areas largely controlled by the
dominant (Underwood, 1978, 1979). The greater the reproductive output of a
species and the longer its larval life, the more recruitment at a particular site will
be unpredictable from year to year.
This fact has been elaborated by Sale (1978) in advancing his lottery
hypothesis: that the maintenance of high diversity in coral-reef fish is due to
chance events of recruitment, coupled with an equal ability of established adults
of all species to hold their territories against invaders and to resist predators and
physical stress. These latter provisos are necessary if there is not to be a
progressive ousting of inferior competitors in communities where space is
limiting. Sale (1982) has good evidence of wide fluctuations in larval
recruitment and that it is independent of adult stocks at any particular locality, but
the existence of equal competitive ability in adults is doubtful. Even Sale himself
records inequality between species (Sale, 1975).
The essential part of Sale’s hypothesis—random recruitment—is as applicable
to non-equilibrial communities as to space-limited equilibrial communities.
Evidence is accumulating that coral-reef fish are not always limited by the
availability of suitable space (Robertson & Sheldon, 1979; D. McB.Williams,
1980; Bohnsack & Talbot, 1980; Robertson et al., 1981; Doherty, 1983), a point
that Sale (1979, 1980) now concedes for some species. In fact, the lottery
hypothesis is more viable when applied to nonequilibrial situations. Fluctuations
and periodic failure of recruitment are in fact likely to be one of the causes of
non-equilibrium conditions (Russell et al., 1977; Talbot et al., 1978; Doherty,
1983; and see p. 523).
Historical events
Early colonizers may influence the subsequent establishment of later arrivals in a
number of ways. Connell & Slatyer (1977, and see Connell, 1972) have reviewed
574 G.M.BRANCH
the mechanisms that may cause succession in communities: (1) the “facilitation”
model in which early species make it easier for later species to colonize; (2) the
“tolerance” model, that later species are not influenced by the primary colonizers,
simply being late successional species because they arrive later and/or grow
more slowly; and (3) the “inhibition” model in which early colonizers hinder or
prevent the establishment of later arrivals. Elements of all three models can be
found in different examples. For instance, Dean & Hurd (1980) showed that
some of the species settling on experimental plates laid in estuaries only settled
on bare surfaces; while others, such as Mytilus preferred to settle where organisms
were already established, their recruitment being facilitated by earlier arrivals
(see also Poore, 1968). Plates with ‘mimic’ barnacles or tunicates are favoured
by Mytilus edulis and the ascidean Molgula, in preference to flat plates without
mimics (Dean, 1981).
Inihibition of subsequent arrivals by early colonizers has been recorded
several times. Sousa (1979a) has shown how Ulva settles early on bare surfaces
and inhibits succession; burrowing organisms modify the sediment and make it
less suitable for suspension-feeders (Rhoads & Young, 1970), while the latter
filter out larvae and hinder recruitment (Woodin, 1976); sheet-like colonial
organisms, once they cover a substratum, prevent the settling of larvae (Goreau &
Hartman, 1966; Sutherland, 1974, 1978; Jackson, 1977; Sutherland & Karlson,
1977).
Some communities, such as the fouling epifauna documented by Sutherland &
Karlson (1977) achieve no stable climax. Sutherland & Karlson contrast this
situation with the rather predictable succession known in many terrestrial
communities. They suggest that the difference is because, first, early colonizers
in fouling communities do not modify the substratum (although they may
themselves serve as a shelter or substratum). Secondly, colonization in the sea
relies on larval recruitment which is relatively unpredictable, in contrast to the
development of dormant ‘seeds’ on land. Finally, the adults of fouling
communities are short-lived compared to the plants which have been studied in
terrestrial climaxes.
Sutherland & Karlson (1977) argue that the communities which develop at any
time or place depend largely on historical events, preceding species determining
what may or may not develop in the community, and that “multiple stable
points” exist in many communities (Sutherland, 1974) dependent on the history
of the community. The use of the word “stable” is perhaps unfortunate, for most
of the examples Sutherland & Karlson provide are characterized by instability
and low longevity of the participants. The availability of larvae at different
seasons (Osman, 1977, 1978; Chalmer, 1982), the order of larval settling
(Sutherland, 1978), the presence or absence of consumers (Sutherland, 1974;
Lubchenco & Menge, 1978), and the rate of colonization and turnover (Schoener,
Long & De Palma, 1978) may all determine what type of community develops.
The greater the variability in each of these elements, the more difficult it will be
to predict what community materializes. On the other hand, some
marine communities proceed predictably to a climax irrespective of the history

of a site. Examples are the subtidal banks of solitary tunicates described by Poore
(1968), the total coverage of experimental plates by mussels (Dean & Hurd,
1980), and the domination of stable rocks by Gigartina canaliculata (Sousa,
1979b).
It is possible that purely methodological differences explain the divergence of
these results. A wealth of information has come from the use of experimental
settling plates, but because these are small and isolated they restrict lateral
overgrowth, and limit the development of large, long-lived organisms, so that
one would expect instability and unpredictable communities on these substrata.
At the same time, some communities do seem more deterministic than others.
Key biological features that may explain such differences are the longevity of
adults, their relative competitive ability and susceptibility to predation, and the
predicability of recruitment.
Interactions between organisms

Part of the reason why communities can be unpredictable is the intricacy of
interactions between species. As a simple example, in competition between the
bryozoan Schizoporella and the ascidian Styela, fish-grazing favours the former,
while the hydroid Tubularia reduces fish-grazing and favours the latter
(Sutherland, 1974). Thus, the outcome depends on previous settlings of
Tubularia, on the intensity of fish-grazing, and on the relative settling rate of the
two competitors. The more species interacting in this manner, the greater the
chance that history and chance events play a rôle.
The point is made more forcibly by Underwood et al. (1983). They have
analysed the individual interactions of the major organisms on rocky shores of
New South Wales: algae, two species of limpets (Cellana tramoserica and
Patelloida latistrigata), the barnacle, Tesseropora rosea, and the predatory
gastropod, Morula marginalba. At high densities Cellana reduces its own
recruitment, growth and survival, and decreases barnacle densities by crushing
small barnacles and grazing settled cyprids. On the other hand, where barnacles
are dense, Cellana immigration increases, its recruitment declines and growth
and survival of its juveniles are lower; but survival of Patelloida is higher
because of the exclusion of its competitive dominant, Cellana. At lower densities
Cellana promotes recruitment and/or survival of the barnacles because it
prevents macroalgae from pre-empting the rock surface and smothering or
restricting the settling of barnacles. Morula decreases settling and survival of
barnacles, but ‘switches’ to eating Patelloida when it is available. Algae may
supply shelter for Morula, increasing its density, but may also protect the
barnacles from being drilled by it. The web of interactions is thus a complex one
in which competitive domination of one species over another will change, and
may even be reversed, depending on which species are present and even on their
576 G.M.BRANCH
relative densities. Variations in recruitment—both in time and in space—play a

major rôle in altering the densities of these species from year to year.
Thus, both deterministic and random processes play a rôle in permitting the
long-term coexistence of organisms, even when competition between them is
intense.
ALTERNATIVE EXPLANATIONS
Coexisting species with similar needs are often assumed to compete, and
differences between species are assumed to permit coexistence, or at least, a
reduction in competition. Neither assumption is always valid, and other
explanations can be advanced. These include facilitation between species with
similar requirements, enhancement of a resource by one or both participants,
apostatic selection as an alternative to competition and, perhaps most important,
the possibility that differences between species and specialization are unrelated
to competition but simply characteristics of the species which have been evolved
for different reasons.
CO-OPERATION BETWEEN SPECIES

Species may coexist and share resources without having any adverse effect on
one another. Dayton (1973a) describes such an interaction between three
predators, the starfish Pisaster ochraceus and Pycnopodia helianthoides and the
anemone Anthopleura xanthogrammica. Pisaster feeds primarily on barnacles
and mussels while Pycnopodia specializes on an echinoid, so the two starfish
scarcely compete. Anthopleura, however, overlaps the diets of both starfish. If
they are competing with it, increasing the numbers of either starfish should affect
the diet of Anthopleura, decreasing those prey which it shares with the starfish. A
decrease in starfish density should have the opposite effect. Contrary to these
expectations, Dayton (1973a) showed that doubling the density of Pisaster
greatly increased the number of mussels and barnacles eaten by Anthopleura
while removal of Pisaster reduced the numbers eaten. The explanation is that when
Pisaster feeds it dislodges or loosens some of its prey, which are tumbled about
in the waves and often captured by Anthopleura. In a similar way Pycnopodia
increases the number of echinoids eaten by Anthopleura because the urchins
retreat from Pycnopodia, often losing grip and being dislodged by waves and,
again, frequently being swept into Anthopleura patches and captured. Thus, in
Anthopleura feeding is facilitated by both starfish and competition does not
occur.
Ayling (1981) has shown that the numbers of several subtidal grazing
gastropods are directly correlated with those of the herbivorous urchin,
Evechinus chloroticus. Far from competing with the urchins, these gastropods
seem to depend on them to clear away macroalgae, or prevent their
establishment, creating a suitable grazing surface for the gastropods. In a similar
manner, the chiton Tonicella and the limpet Acmaea mitra, species that graze
encrusting coralline algae, are more abundant beneath the urchin
Strongylocentrotus purpuratus than elsewhere, and the grazing of this urchin
eliminates foliose algae and promotes the corallines (Paine, 1980). The limpet
Cellana tramoserica similarly prevents macroalgae from developing and
enhances the survival of barnacles (Underwood et al., 1983) and may provide a
surface which is easier for the starfish Patiriella exigua to graze on (Branch &
Branch, 1980a). Its positive influence on these two species is interesting, for it
also competes with them and has a detrimental effect on them.
Other examples of facilitation include teleosts that may benefit by picking up
organisms shuffled from the sediment by feeding rays (van Blaricom, 1982).
Adult labrid fish feed on benthic animals disturbed by foraging parrotfish
(Hobson, 1968). Predatory fish drive small fish to the surface where birds can
capture them (Zaret & Paine, 1973). In some cases facilitation may be more
indirect. For example, the oystercatcher Haematopus moquini reduces limpet
numbers, promoting the growth of algae which, in turn, sustain a cryptofauna on
which smaller waders can feed (P.A.R.Hockey & G.M.Branch, in prep.).
Even congeneric coexisting urchins may facilitate one another’s existence
rather than compete. Duggins (1981) describes how Strongylocentrotus
franciscanus, S. purpuratus, and S. droebachiensis have a similar subtidal
zonation with peak densities in the same zones, and all share the same food—
mainly drifting algae. A positive correlation exists between the numbers of S.
franciscanus and the numbers of the other two species. With such a close
association and overlap, competition between the species could easily be
assumed, but when Duggins increased the density of S. franciscanus this had no
effect on the numbers of the other two species, and their gonad indices either
remained constant or increased, while the gonad index of S. franciscanus
dropped. Thus, intraspecific competition in S. franciscanus is an issue, but
competition between it and the other two species seems negligible. This is
because S. franciscanus, the largest of the three species, is most successful at
capturing and holding down drifting algae, and the other two species can
capitalize on this, feeding on the trapped fronds. S. franciscanus thus facilitates
their feeding. Furthermore, a major urchin predator, the seastar Pycnopodia
helianthoides avoids clusters of urchins containing Strongylocentrotus
franciscanus while readily preying on S. purpuratus and S. droebachiensis.
Aggregates containing only S. purpuratus or only S. droebachiensis are unstable
because the seastar converges on them and causes the groups to break up; but
clusters containing S. franciscanus are stable. Thus, the two smaller species also
gain protection from the association. One unanswered question is whether S.
franciscanus suffers from the presence of the other species. Certainly it is losing
food but, as Duggins points out, until recently urchin populations would have
been held at low levels by otters, and perhaps competition for food was not a
problem under those conditions.
578 G.M.BRANCH
A more intricate interaction concerns the three tubificid worms Tubifex tubifex,
Limnodrilus hoffmeisteri, and Peloscolex multisetosus which frequently coexist
in dense populations in organically polluted freshwater systems. Frequent attempts
have been made to elucidate why one species does not out-compete the others,
but the only detected difference between them is that different species of bacteria
pass through their guts undigested: Acromonas sp. and Pseudomonas fluorescens
in the case of Peloscolex; Micrococcus sp. in Limnodrilus, and Pseudomonas sp.
in Tubifex. The discovery that mixed populations of the worms grow faster and
respire at slower rates than pure cultures suggests that the species are not
competing but co-operating (Chua & Brinkhurst, 1973; Brinkhurst, Chua &
Kaushik, 1972). Co-operation revolves around the passage of different bacteria
through the guts of the three species so that the faeces of any particular species
contain a concentration of bacteria which can be digested by the other species.
Thus, aggregation may develop by mutual attraction of S different species.
Solitary species may be more active as they search for food or for members of
the other species, consequently elevating their oxygen consumption. Conversely,
worms in mixed aggregates may be less active and reduce their respiration. In
support of this, Brinkhurst (1974) has shown that the faeces of Tubifex are more
than twice as attractive to Limnodrilus than its own faeces and five times as
attractive than control mud which lacks faeces. Thus mutual enhancement of
growth and reduction of metabolic losses can explain the coexistence of the
tubificids, and the search for differences allowing coexistence between these
presumed competitors has been misdirected.
The association of the hydroids Xanclea spp. with the bryozoans Celloporaria
brunnea and Schizoporella spp. is a case of co-operation not competition, despite
the fact that other species of both groups of organisms are frequent contestants
for space. Celloporaria forms a calcified fortification over Xanclea, protecting it,
while Xanclea improves the competitive ability of Celloporaria, allowing it to
overgrow poriferans, colonial polychaetes, and other bryozoans which would
otherwise out-compete Celloporaria. It also improves the survival of
Celloporaria by reducing the numbers of a predatory flatworm and by repelling a
nudibranch (Osman & Haugsness, 1981). In a similar manner the bryozoan Bugula
simplex preferentially settles in clumps of its own species or with B. turrita, in spite
of suffering slower growth in such clumps, because joint tufts of the two
congeners are large enough to prevent overgrowth by Schizoporella (Buss,
1981).
ENHANCEMENT OF FOOD SUPPLY

The activities of some animals modify conditions and enhance the growth of
their food supply. For instance, numbers of Macoma balthica are correlated with
the number of bacteria in the sediment, and Tunnicliffe & Risk (1977) suggest
the faecal pellets of Macoma are an attractive substrate for bacterial growth, so
that the bivalves encourage growth of their own food supply. It seems unlikely,
however, that Macoma benefits directly from this as the faeces are re-suspended.
The faeces of Hydrobia ulvae rapidly increase in nitrogen content, presumably
due to growth of microorganisms. Re-ingestion of these faeces by Hydrobia
results in a fall in the level of nitrogen, implying digestion of the micro-organisms
(Newell, 1965).
Abarenicola pacifica forms U-shaped burrows which it irrigates by passing
water down the tail shaft. Small particles drawn in with the water are filtered out
in the sand pocket at the head of the worm. The circulating water also sorts the
sediment in the head shaft, heavier particles accumulating at the bottom, and the
oxygen levels are increased by the irrigation. The activities of the worm thus
locally change particle size, raise the oxygen level and enrich the sediment.
Conditions are ideal for growth of bacteria: nematodes, flagellates and ciliates
are attracted and increased in number, becoming 10 to 15 times more
concentrated than in the surrounding sediment. This whole community is
ingested by Abarenicola. The worm’s faeces contain a higher proportion of
organic matter and fine particles than the sediment, indicating selective feeding.
Diatoms, bacteria attached to sand grains, and decaying algae pass undigested
through the gut, while all ciliates, flagellates, most bacteria and motile diatoms
are digested. Thus, Abarenicola ‘gardens’ its food supply (Hylleberg, 1975a),
locally enriching the sediment rather than simply competing for available food
resources. Nematodes and at least one harpacticoid copepod release mucus which
attracts micro-organisms. In the case of the nematode Praeacanthonchus
punctatus this ‘gardening’ is selective and results in monocultures of the
nematode’s preferred food, Tetraselmis (Warwick, 1981).
The grass shrimp Palaemonetes pugio has an important influence on the
turnover of detritus, supporting its own food requirements in the process (Welsh,
1975). Palaemonetes shreds detritus, reducing it to finer particles on which
bacteria and diatoms attach and multiply; and also increases the particulate organic
carbon in the water column. Shredded detritus and the attached microflora are
ingested and digested. The shrimp releases copious faeces and dissolved organic
matter which supersede its own biomass production by a factor of seven.
Together with the dissolved organic matter, excretion of large quantities of
ammonia and phosphate probably fertilizes the heavy growth of microflora on
the shredded detrital fragments. In a similar way the amphipod Orchestia grillus
ingests detritus from Spartina but only digests the micro-organisms attached to
the detritus. The grazing activity of the amphipods stimulates microbial activity
so that the biomass of micro-organisms increases. This increase may be
associated with ammonia excretion and with elevated diffusion due to the
movement of the amphipods, but the action of grazing itself seems to be the
major agent promoting microbial growth (Lopez, Levinton & Slobodkin, 1977).
Thus, these species increase their food by their activities, and may incidentally
enhance the food of other species as well, rather than competing with them.
580 G.M.BRANCH
APOSTATIC SELECTION
The possibility that differences between species may be maintained by apostatic
selection by predators has been raised by Knight-Jones, Knight-Jones & Al-
Ogily (1975) in relation to the coexistence of different species of spirorbid
worms. Small organisms such as mites and flatworms are major predators on
spirorbids and Knight-Jones et al. suggest that they may become conditioned to
feeding on the most abundant species. Should this species become rare, predators
would then be likely to switch their attentions to another more abundant species.
Under these conditions, coexisting spirorbids should gain some protection from
being distantly related, reducing the chances that the predator will recognize them
when switching from one prey species to another. Thus, species with overlapping
habitats would be expected to be distantly related; this is indeed often the case.
For instance, three spirorbids may coexist on the shells of the mussel Aulacomya
ater: Paralaeospira levinseni predominates in the light, occupying the outer-lip
of the shell, Paralaeospira patagonica in the dark beneath the shell, while a
distant relative, Pileolaria sp., occupies an intermediate position on the shell and
overlaps both of the other species.
Apostatic selection may thus provide an alternative to competitive exclusion
as an explanation of the fact that coexisting spirorbids are seldom closely related.
There is, however, no evidence that apostatic selection does take place in
spirorbids, and experiments on these polychaetes and their micro-predators need
to be undertaken before this concept is accepted.
Another possibility is that prey species have different advantages in different
environments, in relation to predation. An intraspecific example is the differential
survival of colour morphs of Crepidula convexa on different substrata (Hoagland,
1977). Operating at an interspecific level this could allow species to coexist but
to dominate in different habitats. Predators could also compel potential
competitors to occupy different microhabitats, as Shepherd (1973a) suggests for
sympatric species of abalone, Haliotis spp.
OPTIMAL FEEDING
Some animals have specialized diets not because of competition with other
species but to optimize the balance between risk and gain or to maximize yield
(as reviewed by Pyke, Pulliam & Charnov, 1977; and Hughes, 1980). Thus, they
select the most profitable prey species or size range of prey. The specificity of such
selection is often dictated by the abundance and predictability of the prey. As an
example, prey selection and time of feeding have been analysed by Menge &
Menge (1974) for the predatory whelk Acanthina punctulata. The whelk’s search
for prey takes about 5% of its foraging time, 95% being spent on drilling through
the prey’s shell and eating the prey. Acanthina normally shelters in crevices
during high tide, risking being swept away by the surf if it moves around at high
tide. Feeding time, however, normally exceeds the duration of low tide and as
Acanthina cannot move its prey it is forced to spend at least one high tide sitting
on its prey. The risk it incurs must be balanced against the gain of energy.
Acanthina can minimize risk by starting to forage as soon as it is exposed at low
tide, making maximal use of the safe period. It can also select the prey yielding
maximum biomass in relation to handling time, so that feeding can at worst be
confined to a single high tide. Its four major prey are the winkles Littorina
scutulata and L. planaxis, and the barnacles Chthamalus fissus and Balanus
glandula. The winkles yield a much higher biomass. In theory they should be
preferred and, in practice, there is a strong preference for them. There is also a
change in the behaviour of Acanthina as low tide progresses. Early in the low
tide, more littorines are selected, but later on more barnacles are eaten
(Fig. 44A). This suggests that Acanthina searches first for the preferred
littorines, but later becomes less selective, settling for the less-preferred
barnacles rather than returning to a crevice without feeding.
The two littorines also differ in handling time relative to the biomass they
yield (Fig. 44B) and Littorina planaxis should be, and is, preferred. It is eaten
more often in the field, has a higher electivity coefficient (number eaten relative
to availability) and, in choice experiments, is eaten nearly three times as often as
L. scutulata. Larger littorines obviously yield more biomass but may take longer
to drill or feed on. Larger Acanthina should be able to handle larger littorines more
efficiently and a relationship between Acanthina size and prey size can be
predicted and does occur (Fig. 44C). This relationship may incidently ease
competition between different size classes of Acanthina. Acanthina also shows a
strong preference for Balanus glandula over B. cariosus, although they provide
the same yield per unit time. This is because B. glandula takes only three hours
to eat, while B. cariosus takes 14 hours. The longer the time a whelk must spend
feeding on a single prey, the greater the chance that other whelks will accumulate
and share the meal, reducing the yield to the animal which originally spent time
drilling through the barnacle shell (Emlen, 1966 cited by Hughes, 1980, p. 447).
Thus, Acanthina appears to rnaximize yield and minimize risk by selecting
‘optimal’ prey species and prey sizes and by timing its foraging to minimize
exposure at high tide. It is not inflexible, however, in its behaviour, selecting less
suitable prey if the preferred species are not encountered within a certain time.
There is, however, still no evidence of how Acanthina can actually ‘assess’ the
suitability of different prey items.
The dietary specialization of Conus spp. is well established (e.g. Kohn, 1959,
1966, 1978; Nybakken, 1969; and see above, p. 460, for a more detailed outline)
and there is good evidence of dietary shifts and of increased specialization in
areas where many species coexist. These responses accord well with competition
theory, but Leviten’s (1976) analysis of worm-eating Conus spp. casts new light
on specialization in the genus. In developing his ideas, Leviten makes two
assumptions about predator-prey size relationships. (1) There is a minimum size
of prey below which the predator will not feed for energetic considerations, and
this should increase with increasing predator size. (2) There is a maximum size
582 G.M.BRANCH
Fig. 44.—A, numbers of barnacles and littorines eaten by Acanthina in relation to the time
Acanthina has been exposed by the receding tide; B, relationship between size of
Acanthina and the relative cost (time spent drilling per mg of food obtained) of feeding on
Littorina planaxis and L. scutulata; C, correlation between size of Acanthina and size of
prey (Littorina planaxis); (after Menge & Menge, 1974).
of prey the predator can feed on, due to morphological or behavioural limitations;
this also should increase with increasing size of predator.
These assumptions are supported by data for Conus spp. (Fig. 45) and for
many other species (e.g. Fig. 12B, see p. 453, and Fig. 44). Leviten also analyses
the frequency of different sized worms which are present in the field (Fig. 46).
Both small and large worms are rare and represented by a low diversity of
species. Consequently, the number and diversity of worms which are available
for very small or very large Conus are restricted (Fig. 46A, C). Furthermore, the
maximum size of worms that are available probably falls well below the upper
size limit that large Conus can handle, while the lower limit is set by energetic
considerations. Consequently, the larger the Conus is, the narrower the size range
Fig. 45.—Relationship between size of six predatory Conus spp. and their polychaete prey
for subtidal reefs (A), and intertidal beaches (B): volumes are in mm3; (after Leviten 1976).
Fig. 46.—The relative frequency of worms of different sizes at Kwajalein in the Indo-
Pacific: shaded areas are the fractions available to Conus spp. which are (A) small (<10
mm), (B) medium-sized (10–27 mm), and (C) large (>27 mm); (modified from Leviten,
1976).
of worm that can profitably be eaten (Fig. 45A, B). In the intertidal zone, worms
are smaller, making this stricture even more severe (Fig. 45B). No such
restriction exists for medium-sized Conus (Fig. 46B) which feed at the peak of
prey frequency and diversity. As a result it can be predicted that the dietary niche
breadth of small and large Conus must be narrow, while that of medium-sized
Conus may be much wider. Figure 47A shows this to be true, increased body size
resulting in specialization of diet, and (although the data are sparse) very small
body size also decreasing breadth of diet. A similar effect can be shown for other
carnivorous gastropods (Fig. 47C, D) and even within species (see Menge, 1974).
Thus, in the case of vermivorous Conus, dietary specialization may be a function
of the availability of suitable sized prey, and not a consequence of competition
between Conus species. The larger Conus spp. have higher total metabolic costs,
their prey density is lower and they can be expected to forage over a wider area
and hence probably over a wider variety of microhabitats, and Figure 47B
shows that body size is significantly correlated with microhabitat niche breadth
(Leviten, 1976).
584 G.M.BRANCH
Fig. 47.—Relationship between size of predatory gastropods and the diversity of their
prey or microhabitats: A, size of Conus spp. and prey diversity; B, size of Conus spp. and
habitat diversity; C, size of various bivalve-eating gastropods and their prey diversity; D,
size of fasciolarid gastropods and their prey diversity; (after Leviten, 1976).
The predictability of prey will also dictate how specialized a predator may
become. Bertness’s (1977) analysis of Thais spp. from Puget Sound shows that T.
lamellosa occurs low on the shore and T. emarginata above it. Both species
decrease in size with increasing tidal height (see p. 446), a size gradient
parallelled by their main prey, Balanus glandula and B. cariosus. This places
size classes of the thaids in close proximity to the prey size classes which they
can most efficiently utilize and are their preferred prey (Emlen, 1966, cited by
Bertness, 1977). Size gradients and selection of particular size classes of prey
may thus reduce both intra- and interspecific competition in the thaids. Connell
(1970) suggests that the very predictable annual settlement of these barnacles has
allowed the smaller thin-shelled T. emarginata to evolve as a specialist feeding
on the smaller high-shore barnacles, while T. lamellosa feeds on larger barnacles
of the lower shore where its larger size and thick shell allow it to survive
predation by crabs.
In the ascoglossan molluscs, which feed by puncturing the cells of algae and
sucking out the cell contents, different species specialize on particular algae. The
diameter of the foot of each species is correlated with the diameter of the
filamentous alga on which it feeds, and there is also a correlation between cell
size and the length of the leading radular tooth of each species. Such correlations
presumably reflect the fact that each species can feed most efficiently on a
particular alga, with consequent specialization of diet (Jensen, 1983). Urchins
prefer particular algae when given a choice, and the algae they select are those
which they can absorb with greatest efficiency and yield highest growth and
gonad production (Vadas, 1977; Larson, Vadas & Keser, 1980). Under field
conditions the algae that are eaten are a compromise between the preferences of
the urchins and the availability of different kinds of algae. Thus, urchins are not
highly specialized but do have preferences which correlate with energetic gains.
Steneck (1982) has developed a conceptual model of herbivore-plant
specialization, proposing that specialization occurs when the herbivore is small
relative to the plant, is non-mobile, and requires little energy. Thus, the high
degree of specialization in ascoglossans and some limpets can be anticipated,
while urchins will be selective but not specialized, and herbivorous fish will be
generalized.
Elner & Hughes (1978) have measured the prey value (energy content/
handling time) of different sized Mytilus edulis for the predatory crab Carcinus
maenas. Large mussels are difficult to crush, while small mussels yield little
energy for the time expended on opening and eating them: optimal prey size
increases with the size of the crab (Fig. 48A). When offered unlimited prey,
crabs selected mussels close to the predicted optimum (Fig. 48B). Optimal sized
mussels are always eaten as they are encountered but a series of encounters is
required before mussels of suboptimal size will be eaten. Thus, depending on the
size range of mussels available, crabs either feed immediately on optimal prey or
can adjust rapidly to accepting prey of lower quality. Crayfish (Jasus lalandii)
similarly select mussels of optimal size (Griffiths & Seiderer, 1980). Carcinus
maenas also selects Littorina rudis in preference to L. nigrolineata and small snails
in preference to large: both choices yielding higher returns of energy per unit of
handling time (Elner & Raffaeli, 1980). Thus, dietary specialization extends not
only to selection of particular species of prey but to particular sized individuals of
a given prey.
Competition may affect the realization of an optimal diet, as Werner & Hall
(1976) have shown for two competing sunfish. The bluegill Lepomis marochirus
prefers to feed on large prey (insects and crustaceans) in vegetation at the edge
of freshwater ponds, but is displaced into open water where it feeds on the less-
preferred zooplankton when the green sunfish L. cyanellus is present.
Experimentally confining the two species together decreases the growth of the
bluegill but hardly affects the larger more aggressive sunfish. Overlap in diet is
586 G.M.BRANCH
Fig. 48.—A, the value of prey eaten by Carcinus maenas (energy derived per unit
handling time) in relation to prey size; B, the frequency with which C. maenas feeds on
mussels of different sizes when offered a choice; (after Elner & Hughes, 1978).
asymetrical (Fig. 49A), the green sunfish overlapping the bluegill’s diet by 83%
while the reverse overlap is only 64%. This partly explains why the bluegill
suffers most when the fish coexist. For both species the relative ‘cost’ of food
(time spent handling prey: biomass gained) varies with prey size, optimal prey
size being greater for the green sunfish than the bluegill (Fig. 49B). The most
frequent prey sizes in the diets of each species (Fig. 49A) closely approach the
predicted optimal sizes (Fig. 49B). When the bluegill is competitively displaced
into open waters, its prey size decreases threefold. This increases prey handling
time but, as searching time decreases, the actual ‘cost’ of the food is little
affected (see dashed line in Fig. 49B). If the green sunfish, however, were to
expand its habitat to occupy open waters, the increase in relative cost of prey
would be much greater, and in fact the bluegill would probably gain more from
the open-water zooplankton than the green sunfish (see Fig. 49B, points B and
G), possibly reversing the normal superiority of the green sunfish. The bluegill
thus enjoys a refuge from competition in the open water, while the green sunfish
is competitively superior in its narrow niche in the vegetation at the edge of
ponds, aggressively defending these feeding grounds where the larger prey are
concentrated.
Thus, specialization may reflect the degree to which a species can optimize its
diet by balancing energetic gains against the cost of time or risk. Competition is
not necessarily involved in such specialization, although overlap in diet between
and within species may incidentally be reduced by specialization, and
competition may still effect the realization of an optimal diet, as Werner & Hall
(1977) have shown for the two competing sunfish. Viewed in this way,
specialization increases the efficiency with which an animal utilizes its
Fig. 49.—A, bluegill and green sunfish; size-frequency composition of their diets, and
dietary overlap in terms of prey size. B, the effect of prey size on cost (handling time/
biomass obtained) for the bluegill and the green sunfish. The circle and star indicate the
actual size of food most often selected by each species, and the dashed line and points G
and B indicate the changes in cost that would occur if both species were forced to feed in
open waters where prey size is smaller; under these circumstances the bluegill would
actually have a higher yield (spend less time to obtain a given biomass); (modified from
Werner & Hall, 1977).
resources, and it is not always necessary to invoke competition to explain

specialized dietary requirements.
COMPETITION AND EVOLUTION

Interspecific competition has an undeniable effect on the populations of a wide
range of species, but the link between competition and evolutionary processes is
more difficult to prove. There are four ways in which competition may influence
evolution: by the extinction of species; by causing reduction in niche breadth; by
selecting for improved competitive ability; and by influencing speciation.
Figure 53 (see p. 576) summarizes six ways in which competing species may
interact, two of which (Figs. 53A, B) are associated with genetic changes, and
four with phenotypic responses or short-term shifts in habitat. Three different
aspects of competition affect the rôle it plays and the kind of evolutionary
responses that can be anticipated: (a) the nature of the resource being competed
for; (b) the nature of the species participating, particularly their mobility, size
and mode of dispersal; and (c) the mechanism of competition, whether it is by
exploitation or interference.
588 G.M.BRANCH
THE NATURE OF RESOURCES AND SPECIES

Mobile and sessile species are intrinsically different in the way they compete and
the manner in which they are regulated (Table III). Mobile species are almost all
herbivores, deposit-feeders, carnivores or scavengers, and when competition
occurs between them it is most often for food , although some
compete for space in the form of shelters. Conversely, sessile species,
comprising attached macroalgae, filter-feeders, and carnivores such as anemones
and corals, compete most often for space , although competition
for food, or overshading in the case of algae and autotrophic corals, also takes
place (Table IV).
Mobile organisms also respond differently to predators, for they have the
capacity to hide, escape or even retaliate, avenues largely closed to sessile
species which can only escape in size or develop toxins. Furthermore, mobile
species can recruit either by larval settling or by immigration or adults; sessile
forms rely on larval recruitment, which is frequently limited to certain periods of
the year. Both points suggest that predators will be far more important in
regulating the local density of sessile organisms than of mobile species.
Turning to the nature of resources (Table V) Underwood (1978, 1979) and
Yodzis (1978) draw attention to the contrasts between space and food as limiting
resources. Space is often an absolute requirement in that species must have space
in which to live. Furthermore, space is not readily partitioned between species,
although in soft-sediment communities three-dimensional apportionment of
space eases this stricture (Peterson, 1979b). Food, on the other hand, is a relative
requirement, for most marine animals (and in particular invertebrates) are plastic
in their growth and can exist on limited quantities of food although, obviously,
there is a limit below which starvation leads to death. In addition, food is self-
renewing and often becomes available rapidly after it has been used, particularly
in the case of algae consumed by herbivores; space does not renew itself, and
once it has been occupied by a sessile organism it only becomes available again
with the
TABLE III
Comparison of the contrasting characteristics of mobile and sessile species.
Mobile Sessile
Usual method of nutrition Herbivorous, carnivorous, Filter-feeding, autotrophic
deposit-feeding,
scavenging
Most frequent limiting Food Space
resource
Effect of predators Limited; prey can escape, Considerable: prey easily
hide or retaliate attacked, and only defence
is size or toxins
Mobile Sessile
Recruitment Both larval recruitment and Larval recruitment only
adult immigration (often seasonal)
Effect of elimination Short-lived Potentially long-lived
(unless larvae happen to be
settling at the time)
TABLE IV
Synopsis of the resources competed for by organisms in different trophic groups and with
differing mobility: data are percentages; n=number of species
Organisms
Sessile Mobile
Resource Algae Filter- Carni- Deposit- Herbi- Carni- Incidence
s feeders vores feeders vores vores of
exclusion
Space 74 96 90 36 22 29 38
Food — 4 10? 63 78 71 14
Light 26 — 10? — — — —
n 39 48 21 30 60 31
TABLE V
Comparison of consequences of competition for food and space: percentages are
incidences of each event, based on numbers of species, and drawn from the literature
included in this review
Food Space
Requirements by Relative Absolute
competitors
Renewability Rapid Slow or even non-
renewable
Most frequent mode of Exploitation (68%) Interference (82%)
competition
Usual consequence of Coexistence (90%) (often Exclusion (37%) or
competition with depression of growth). depression of numbers
Exclusion unusual (10%)
Impact of predators or Limited, short-lived, Important, longer-lived,
disturbance decreases (64%) or has no usually increases diversity
effect on diversity (30%) (66%)
Evolutionary consequences Exclusion unlikely. Niche Exclusion likely, extinction
apportionment possible if possible unless prevented
long-term coexistence by disturbance or
occurs predation.
Apportionment difficult;
improved competitive
590 G.M.BRANCH
Food Space
ability evolved by
interference
death of that organism. In some cases the persistence of the empty shells or tests
of dead organisms prevent re-occupation of space even after death. One
exception to the rule that space is non-renewable is when organisms settle on the
surface of algae, which by virtue of their growth continually provide new space
(Seed & O’Connor, 1981). As a result algae house a disaproportionately large
number of fugitive species.
Competition for space leads to exclusion more than twice as often as
competition for food (Table IV). Consequently, predation and disturbance play a
more significant rôle in preventing competition in sessile communities (see
above, p. 533), than in communities dominated by mobile species. Their
immediate impact is higher, longer lasting in its effects, and more important in
reducing competitive monopolization of space, thereby allowing a higher
diversity to be maintained. Mobile species, competing for food, are less
vulnerable to predators and more difficult to eliminate. In addition, because they
most often compete for food and seldom exclude one another, their communities
respond differently to predators, which either have no effect on the species
composition or cause a reduction in diversity (Yodzis, 1978).
Thus, competition for space is most likely to lead to exclusion unless predation
or disturbance maintains the competitors at sub-equilibrium levels; but when
food is a limiting resource competitors are much less likely to exclude one
another, and predators are less significant in controlling their numbers. Since
competition for food does not normally lead to exclusion, species which compete
for food can coexist for prolonged periods, during which niche apportionment
may evolve.
THE MECHANISM OF COMPETITION

The two contrasting modes of competition, exploitation and interference, have
different ecological and probably evolutionary consequences. While interference
often leads to the localized exclusion of one species, exploitation rarely does and
is linked with the possibility of niche divergence as a means of reducing
competition (Fig. 53A see p. 576). This latter view is advocated by prononents of
the niche theory and considerable intellectual thought invested in the concept
(see, for example, Hutchinson, 1959; Ayala, 1972; Schoener, 1974, 1982;
Pontin, 1982, and references therein). Despite this, recent doubts have been
voiced as to whether competition is capable of causing niche divergence (e.g.
Wiens, 1977; Connell, 1980). To confirm that competition is the driving force
responsible for differences in the niches of coexistant species requires more than
the mere demonstration of differences between species. The species must
compete, the differences between the species must provide a means of reducing
that competition, and genetic inheritance of the characteristics must be proved.
If niche divergence is caused by competition, it is only likely in species that
consistently coexist under limiting conditions. For this reason alone, Connell
(1980) queries whether it is a regular phenomenon, for competitors are seldom
obliged to coexist and are thus unlikely to co-evolve—and the unlikelihood of co-
evolution increases with the diversity of species in a community. It is most likely
in species with low mobility and restricted habitats, which share a limiting
resource that can be feasibly apportioned— such as food.
Character displacement or niche divergence can only be of benefit if, while
allowing separation of the niches of two species, they do not increase overlap of
either participant with a third species. Again, low-diversity communities, which
offer opportunities for species to fill vacant niches, are likely candidates; they are
also the communities in which competition will occur relatively seldom. Genera
such as Hydrobia (see p. 500 and Fig. 31) and Sphaeroma (Fenchel, 1975b; Frier,
1979a, b) do display character displacement in estuaries, where fluctuating and
sub-saturation conditions may allow divergence of closely related species without
the danger of overlap with other species.
The concept that species become more specialized in highly diverse
communities because of competition must also explain what advantage
specialization brings the species, for while it may decrease interspecific
competition it will also incur increased intraspecific competition. To use a
concrete example, Conus spp. appear more specialized in diverse communities
(Kohn, 1966, 1971) and one species, Conus miliaris, broadens its diet when it
occurs in isolation (Kohn, 1978), presumably a consequence of release from
competition. But in sympatry with other species it makes no sense for C. miliaris
to narrow its niche, by-passing prey which it would otherwise eat, simply
because other species make use of them. It is more likely that the other Conus
spp. are more efficient at capturing some of its prey species, leaving few for C.
miliaris, so that its diet appears more specialized. If this interpretation is correct,
‘specialization’ is caused by exclusion from a fraction of the diet normally used
by C. miliaris, not by a competition-induced genetically inherited contraction of
niche breadth with the purpose of avoiding competition.
Character displacement of body size raises another problem. Difference in
body size may well reduce competition as, for instance, it seems to do in
Hydrobia spp. (Fenchel, 1975b). But the species which becomes smaller in
sympatry than it is in allopatry almost certainly suffers from decreased
reproductive potential, size being linked to reproductive output in most
invertebrates. For that matter, if the other species can achieve a size that is greater
than normal when it is in sympatry, what stops it from increasing in size (and
elevating its reproductive output) in allopatry? There are examples of coexistent
congeners of different sizes in which different benefits accrue to the two species.
For instance, the gastropod Busycon contrarium is large and thick-shelled and
resists predation, while its smaller congener B. spiratum is more efficient at
592 G.M.BRANCH
capturing prey. But in Hydrobia, as in Astropecten (Ribi, Scharer & Ochsner,

1977; and see p. 456 and Fig. 13) and Sphaeroma (Frier, 1979b) no obvious
reasons present themselves—other than avoidance of competition—for size
displacement. Which leaves us with the queries raised above. Presumably the
disadvantages of small size in the smaller of the two coexistent species are offset
by the advantage of reduced competition, and presumably the larger species only
attains unusually large size in sympatry because in allopatry there is no selective
advantage to being larger; but neither explanation is satisfying.
One final question relating to differences between species which may reduce
competition, is whether divergence in areas of sympatry is genetically controlled
or not. Connell (1980) concluded that no properly controlled experiments had
ever been undertaken to demonstrate genetic control. As discussed above (p.
477) Harger (1972c) has aescribed differences between sympatric and allopatric
populations of Mytilus spp. which may be genetic, and the different allele
frequencies of sympatric and allopatric populations of acmaeid limpets are
certainly genetic (Murphy, 1976). All other instances of character displacement
discussed above (p. 529) are more likely to be phenotypic—although proof of
this is still lacking.
A different viewpoint is that rather than driving species apart and minimizing
competition, exploitation of a common resource leads to improved competitive
ability in one or both participants. This can occur either by increasing the
efficiency with which they exploit the resource, or by the development of
interference mechanisms. Hairston (1980) is one of the few authors to have
tested this viewpoint, using terrestrial salamanders—no work of a comparable
nature having been undertaken on marine organisms. Hairston compared two
species (Plethodon glutinosus and P. jordani) in two localities: in the Smoky
Mountains where they scarcely overlap one another’s vertical range and where
strong competition occurs; and in the Balsam Mountains where the two overlap
substantially and where competition between them is relatively mild.
Transplanting P. jordani from the Smokies to Balsam, revealed that it had a
greater effect on the P. glutinosus there than the resident P. jordani has, and it
has a greater competitive effect on these P. glutinosus than on the P. glutinosus
from the Smokies. These results suggest that the animals from the Smokies have
both evolved an increased competitive ability, which now keeps the two species
virtually separated. Conversely, transplanting Balsam P. jordani to the Smokies
led to an increase in the numbers of P. glutinosus from the Smokies compared
with animals kept with native P. jordani, indicating that Balsam P. jordani have
less competitive effect on P. glutinosus from the Smokies than do resident P.
jordani. The implication is that means of reducing competition have evolved in
the Balsams, perhaps by an alteration of the requirements of each species to
reduce the resources that they share—just as would be predicted by the
conventional niche diversification theory.
Hairston suggests that in the two areas selection has proceded in diametrically
opposed directions, reducing competition and allowing considerable vertical
overlap of the two species in the Balsams, but intensifying it in the Smokies with
resultant vertical separation of species. The process heightening competitive
ability in both species in the Smokies is not known, but it could be improved
exploitative ability or the evolution of interference mechanisms. The only
problem with this interpretation is that there is no knowledge of what
interactions originally occurred between the two species. It is equally possible to
argue that the two were originally mild competitors (as they still are in the
Balsams) but have become more aggressively competitive in the Smokies, that
the original situation was the highly competitive one that is now muted in the
Balsams, or that the initial condition was intermediate and has evolved in
opposite directions in the two localities, as suggested by Hairston. In spite of this
hesitation, Hairston’s example is an important one, for in many ways the
evolution of improved competitive ability makes more sense than a reduction of
competition by niche divergence, bringing with it, as it does, the implication of
increased specialization and the risk of increasing intraspecific competition.
Of the 192 examples of competition reviewed in this paper, 154 (80%) involve
interference—by territoriality, aggressive fighting, overgrowth, allelopathic or
antibiotic chemicals, external digestion, immunological responses, inhibition of
settling, or by indirect interference involving alteration of the nature of the
substratum to make it less suitable for competitors. Interference is obviously the
predominating form of competition in the sea, a finding that contrasts with
earlier synopses, such as that of Reese who, in reviewing the ethology of marine
animals in 1964, recorded only eight instances of interference. Furthermore, of
the 62 examples summarized in the present review in which competitive
exclusion occurs, 58 (93·5%) involve interference; exploitation very seldom
achieving exclusion (Table VI). Interference is also most likely to be involved
when species compete for space; while food is most frequently competed for by
exploitation (Table VI).
In discussing types of resources and the nature of species above (p. 556 and
Tables IV and V), space was identified as an absolute resource, which
TABLE VI
Analysis of the occurrence of interference and exploitation in interspecific competition, in
relation to the nature of the resource: data given as percentages; n=number of species (or
functional groups of species, in some instances)
Limiting resource
Mode of n Spacea Food Light Nutrients Otherb Incidenc
competiti e of
on exclusio
n (%)c
Interfere 154 82 8 4 1 5 38
nce
Exploita 38 23 64 0 ?8 5 10
tion
594 G.M.BRANCH
Limiting resource
Mode of n Spacea Food Light Nutrients Otherb Incidenc
competiti e of
on exclusio
n (%)c
a Including space used as a shelter against predators, or for general purposes (e.g. by
barnacles, attached algae) but excluding areas defended only for the food they
contain, which are classed under “Food” (e.g. territorial areas, defended by
limpets)
b Includes shells for hermit crabs
c Defined as total or partial exclusion (>50% reduction) of the subordinate species from
that part of its fundamental niche occupied by the dominant species, and
measured in terms of its spatial or temporal use of a given resource.
is difficult to partition, so that competition for space leads to competitive

exclusion more frequently than competition for any other resource. Thus, it is
not surprising that competition for space is linked with interference, which
allows one species to exclude another without loss of the resource; while food,
which is a relative requirement and more easily partitioned, is competed for by
exploitation. Therefore the nature of the resource and the mode of competition
reinforce one another, increasing the likelihood of exclusion in a space-limited
interaction and increasing the chances of coexistence when food is competed for,
opening the way for apportionment.
Murray (1981), in reviewing interspecific territoriality, has posed two
questions: is it adaptive, and does it have adaptive origins? These questions can
be broadened to include other forms of interference. There seems little doubt that
interference is adaptive. For instance, limpets maintaining territorial gardens and
defending them against other grazers benefit from a rich predictable food supply
(Stimson, 1970, 1973) and individuals which lack territories have slower growth,
lower body weights and gonad weights, and a high ash content (G.M.Branch,
unpubl.). Territorial fish similarly maintain algal beds that are rapidly eliminated
by other grazers in their absence (e.g. Brawley & Adey, 1977; Williams, 1981).
Interference (including territoriality) also enhances reproductive potential (e.g. in
fish: Clarke, 1970, 1971), survival (e.g. in shrimps: Thorp, 1976; Coen, Heck &
Abele, 1981), prevents overgrowth (in sponges: Amade, Pesando & Chevolot,
1982; and ascidians; Jackson & Buss, 1975; Bakus, 1981), and increases access
to food (e.g. in whelks: Kent, 1983). Many other examples of species benefiting
from interference with competitors are given in the earlier sections of this review.
Furthermore, it is difficult to explain why fish should vary the intensity of their
attacks on intruders in proportion to the competitive threat they pose (Myrberg &
Thresher, 1974; Ebersole, 1977; Moran & Sale, 1977) if their behaviour is not
adaptive.
The second question is more difficult to answer, for while interference may be
adaptive it does not follow that its evolutionary origins are due to interspecific
competition. It may originate as an intraspecific device, in response to predators,

or as a means of capturing prey, and only later assume a secondary function in
countering an interspecific competitor. Thus, the origins of interspecific
interference may be adaptive or pre-adaptive.
To distinguish these options is fundamental to our understanding of whether
or not interspecific competition influences the evolution of species-specific
characteristics. Murray (1981) offers several conditions as an aid to
distinguishing the two alternatives, proposing that an adaptive origin can be
inferred (a) if interference displayed between different species is absent between
conspecifics, (b) if the dominant species displays the interference and not the
subordinate (which would suffer from attempting to interfere with a dominant),
(c) if the species possessing an interference mechanism succeeds in preventing a
competitor using mutually required resources, and (d) when a subordinate
species evolves a means of minimizing the dominant’s aggression or countering
its interference. None of these tests is adequate, but because one is dealing with
historical events that shape current happenings no completely satisfactory test
can be devised.
Some cases of interference are clearly pre-adaptive. For instance, the mantis
shrimp Gonodactylus falcatus fights aggressively with Pseudosquilla ciliata and
displaces it from its normal habitat in coral heads on Hawaiian reefs, but since
the former was only recently introduced to Hawaii, its method of competition
must have been evolved for other purposes (which could, of course, have been
interspecific competition in its native grounds).
On the other hand, many examples of interference do conform to the guidelines
suggested by Murray (1981) for an adaptive origin. There are many instances of
a dominant excluding a subordinate form its habitat, including crayfish
(Bovbjerg, 1969), shrimps (Thorp, 1976; Coen et al., 1981), fish (Hixon, 1980,
1981; Larson, 1980), limpets (Stimson, 1970, 1973; Branch, 1976), whelks
(Kent, 1983), spiders (Lamoral, 1968), corals (Scatterday, 1977; Sheppard,
1979), urchins (Grünbaum et al., 1978), mussels (Harger, 1972c; Suchanek,
1978), ascidians (Sebens, 1982), algae (Dayton, 1975a, b; Fletcher, 1975;
Schonbeck & Norton, 1978; Santelices, Montalva & Oliger, 1981), crabs
(Willason, 1981), anemones (Williams, 1975; Purcell, 1977), and mantis shrimps
(Dingle & Caldwell, 1975). Other examples are also given earlier in this review.
In all these cases, interference is not uniquely interspecific, so that it may have
originated as an intraspecific device and only inadvertently valuable in
combating other competitors.
Even in those cases where interference is confined to interspecific encounters,
its origin may still be explicable in other ways. As an example, the limpet
Cellana tramoserica competes with the starfish Patiriella exigua by exploiting
its food, but also interferes with it by extending its mantle—which is laden with
mucus glands—causing the starfish to retreat. The same reaction is, however,
used to repel predators, and is more likely to have evolved for this reason
(Branch & Branch, 1980a). The starfish Pisaster interferes with its competitor
596 G.M.BRANCH
Leptasterias by attacking it with its pedicellaria (Menge, 1974). This, too, is

likely to be primarily a means of defence against predators, as are the toxins
produced by ascidians (Stoecker, 1980) and sponges (Bryan, 1973; Green, 1977;
Bakus, 1981). The use of mesenterial digestion and sweeper-tentacles by corals
is nearly always interspecific (Sheppard, 1982) but may have its origins in the
attainment of nutrition rather than as a means of competition (Lang, 1980, cited
in Sheppard, 1982). On the other hand, allelopathic chemicals produced by algae
are remarkably specific to those tissues which most need to be kept free of
fouling organisms (Al-Ogily & Knight-Jones, 1977) and the allelopathy of some
ascidians and sponges is species-specific, and has no effect on conspecifics or on
other species (including all solitary organisms) which present no competitive
threat (Jackson & Buss, 1975). In fact, allelopathic chemicals probably present
one of the most likely cases where an interference mechanism has been evolved
for the specific purpose of interspecific competition.
Even so, all these examples must have a question mark appended to their
origins. Some may indeed have been adaptive in origins as well as adaptive in
current function, but we have no way of determining this with certainty. My own
feeling is that most, but not all, cases of interspecific interference have their
origins in some other function, and that most often this will have been an
intraspecific function, but to produce concrete evidence of this is another matter.
There are many instances in which subordinate species counter or reduce the
aggression of a dominant. Acmaeid limpets have a ritualized response to
territorial Lottia gigantea, withdrawing immediately on contact, so that they
avoid potentially dangerous contacts (Wright, 1982; and see Branch, 1981).
Parrotfish make use of schooling to thwart the territorial defences of damselfish
(Robertson, Sweatman, Fletcher & Cleland, 1976). Urchins capitalize on the
inactivity of the damselfish at night to invade their territories (Williams, 1981).
Bryozoans erect barriers of spines to prevent overgrowth (Seed & O’Connor,
1981), and corals use sweeper-tentacles to counter mesenterial digestion (as
reviewed by Sheppard, 1982). Once again, these examples can be explained as
adaptive processes which arose pre-adaptively for other reasons, or even as
incidental effects, but the data provided by Wright do convincingly link the
ritualized responses of acmaeid limpets with the specific threat posed by
territorial Lottia.
One final point is worth making with respect to different modes of
competition. If niche apportionment is to arise in response to a common
exploitation of a resource by two species, it will be a response which is species-
specific, permitting two particular species to continue to coexist by reducing
overlap between them. Thus, the two species must be intimately associated to co-
evolve in this manner. As mentioned above, this in itself will make the event a rare
one. But interference is a different matter. Not only can it arise as an intraspecific
function or as a defence against predators, and later serve to combat interspecific
competitors, but it is a generalized adaptation which will aid the organism against
a wide range of competitors. This remains true even if it arises as an adaptive
response to a particular interspecific competitor. Every instance of interference

explored so far acts against at least several, and often many, species. Thus, the
evolution of interspecific interference is easier to realize, as borne out by its
prevalence in competitive interactions between marine organisms.
EXTINCTION
Both the fossil record and the impact of invasive introduced species can be used
to guage the possibility that interspecific competition may cause extinction.
Based on fossil records, Stanley (1973) has compared the low rates of radiation
and extinction in bivalves with the much higher rates exhibited by mammals, and
attributes the differences to the relatively intense and sophisticated interspecific
competition typical of mammals. It is true that bivalves have low rates of
phylogenetic turnover, their genera having an average longevity of 78 million
years compared with about 8 million years for mammalian genera (Simpson,
1944, 1953, cited by Stanley, 1973). And it is also true that free-living bivalves
which inhabit soft sediments compete relatively little (Levinton & Bambach,
1975; Peterson, 1979b, 1982; Peterson & Andre, 1980) although a certain amount
of competition has been demonstrated in some cases (Levinton, 1977; Peterson &
Andre, 1980). Part of the reason why interactions between bivalves are restricted
is that competition for space is eased in soft sediments (see Peterson, 1979b);
another reason is that bivalves—like most invertebrates— can tolerate long
periods of near starvation, while mammals cannot. Bivalves also have primitive
means of interacting, simple inflexible behaviour, generalized diets, and are often
limited by predation. Conversely, Stanley argues that the mobility of mammals,
their high demand on food to sustain their body temperatures, and their evolution
of aggressive interactions and territoriality all point to intense competition, as do
the limitation of many populations by food and the high degree of dietary
specialization in mammals.
Stanley supports his argument that intensity of competition can be linked with
rates of turnover and radiation, by pointing to groups of marine invertebrates in
which competition was, or is, intense. The rudist bivalves (Hippuritacea), reef-
forming animals of the Cretaceous period, appear to have competed intensely for
space, as do the hermatypic corals; and both groups have displayed rapid
radiation and high extinction rates. This reflects back on the contrast between
space and food as limiting resources, discussed above (p. 556).
Factors other than competition may also have affected the rates of extinction
and radiation in bivalves and mammals. The physical constancy of the sea, the
relative ease with which terrestrial populations can be isolated from one another,
the wide dispersal of bivalve larvae and the ease of reproductive isolation in
animals with internal fertilization and sophisticated mating systems may all have
had an influence.
Stanley & Newman (1980) have also proposed that competition between
balanoid and chthamaloid barnacles has been responsible for the decline in
598 G.M.BRANCH
chthamaloids and their frequent occurrence in the extreme high shore, beyond
the reach of balanoids. They point to Connell’s (1961a) experiments which
demonstrate that Chthamalus stellatus is largely confined to the high shore by
competition with Balanus balanoides. They regard balanoid barnacles as being in
the midst of “a rampant adaptive radiation”, having evolved about 273 species
since their appearance in the Eocene, approximately 15 million years ago. In
contrast, the chthamaloids now comprise only 53 living species, 40 of which are
restricted to high-shore refugia—presumably because of competition with
balanoids—and the rest exist only in small relict populations in isolated parts of
the world. The key feature in the competitive superiority of the balanoids is
considered to be the evolution of a tubiferous shell, allowing faster growth, more
rapid occupation of free space, and the possibility of overgrowing other, slower-
growing, barnacles. Stanley & Newman’s proposition is challenged by Paine
(1981) who suggests that factors other than competition may be more useful in
explaining current patterns of chthamaloid distribution. He concedes that
chthamaloids will normally be the losers in competition with balanoids but
points out that small size in the genus Chthamalus may have distinct advantages,
allowing settling and growth in protected crevices, early sexual maturity, a
reduction in attractiveness to at least some predators (such as the larger species
of thaid whelks) and an increased resistance to the bulldozing effect of grazers.
Paine recounts instances where chthamaloids occur lower on the shore that
balanoids, and suggests that this will occur when invertebrate predation, grazing
by herbivorous invertebrates, or physical disturbance are important, putting the
larger balanoids at a disadvantage. He agrees that the restriction of chthamaloids
to the high shore can be caused by competition with balanoids, but only when
these factors are minimized. High-shore zonation of chthamaloids can also be
explained by extensive grazing of mobile fish as occurs in the tropics. A further
explanation is preferential grazing of smaller thaids on small rather than large
barnacles, as seems to be the case in southern Africa (G.M.Branch, unpubl.
data).
Despite a reply by Newman & Stanley (1981), Paine’s (1981) basic point
remains valid: that competition is probably not the only process confining
chthamaloids to a largely high-shore distribution, and that it is unlikely that a
single mechanism can be invoked to explain this zonation pattern. A more
serious problem with Stanley & Newman’s (1980) suggestions is the absence of
a sufficiently good fossil record to trace the rates of radiation and increase or
decline in the two barnacle groups. Stanley & Newman have been forced, of
necessity, to rely on inferences drawn from the current geographic distribution
and diversity of the two groups. The chthamaloids may in fact be conservative
and slow in evolving, rather than declining in the face of competition from
balanoids (Paine, 1981). These reservations must make one cautious of accepting
that the chthamaloids are the “clearest example…of long-term evolutionary
decline resulting primarily from competitive exclusion” (Stanley & Newman,
1980, p. 181).
Turning to invasive species, there are several records of introduced marine

organisms competing with indigenous species, but no case in which competition
has eliminated, or seems about to eliminate, any of the native species.
The introduction of various algae to Britain is summarized by Farnham (1980).
Colpomenia peregrina has had little effect on the local flora. Sargassum muticum,
a recent arrival, is causing more concern because of its aggressive ability to
establish itself and to smother other algae. The introduction of Codium fragile
from the Pacific to southwestern Ireland in 1808 has led to a reduction in C.
tomentosum at a number of sites, as C. fragile has spread to many areas in Britain
(Ramus, 1971; Farnham, 1980). C. fragile was also introduced to the Atlantic
North American coast in 1957, and has vigorously expanded down that coastline.
Crepidula fornicata, accidentally introduced to Britain and to Europe, now
smothers and has largely excluded oysters, so prolific has it become (Elton, 1958).
One clear case of competitive exclusion of a native species by an alien has been
recorded by Kinzie (1968): the mantis shrimp Gonodactylus falcatus, first
recorded in Hawaii in 1954, has displaced the indigenous Pseudosquilla ciliata
from its previously dominant position in coral heads, restricting it to areas of
mud and sand—a less preferred habitat for both species.
The progressive spread of the barnacle Elminius modestus in Britain and
Europe has been well-documented (see Barnes, Barnes & Klepal 1972, and
references therein). Elminius competes successfully with Balanus balanoides
over the whole of the littoral zone. Part of the reason for its success is that it has
multiple broods throughout summer and grows very fast, while B. balanoides
only breeds once a year in the spring. In the cooler northern regions Elminius
also out-competes Chthamalus stellatus, but in France, near its southern limit, it
is restricted to a belt below that occupied by Chthamalus. Barnes et al. suggest
that this restriction is due to competition with Chthamalus, but increased thermal
stress may also explain this pattern. The continuing spread of Elminius in Britain
suggests it has the ability to out-compete local barnacles, although winter
temperatures are occasionally low enough to destroy it in some places so that it
will never completely displace the local species. Curiously, no experimental
work has been undertaken to test the relative competitive ability of Elminius and
the indigenous barnacles, or to assess the impact that the species have on each
other when they coexist. Such experiments could be very valuable, particularly if
conducted under conditions of differing thermal stress.
A significant feature of all these examples is that competition is for space and
by means of interference, either by direct attack, smothering or overgrowth,
reinforcing the suggestion made above that spatial competition and interference
are more likely to lead to exclusion than exploitative competition for food.
In none of these cases does extinction of the subordinate species seem likely in
the near future. Even in the long term, the existence of refuges and the rôle of
disturbance and/or predation make it questionable whether competition alone
will result in extinction. But as Stanley & Newman (1980) remark, we must not
assume that total exclusion is necessary for competition to have an evolutionary
600 G.M.BRANCH
impact, for if a newly evolved, or newly arrived, competitor even reduces the
numbers of pre-existing species, extinction by other agents becomes more
probable.
GENETIC DIVERSITY AND NICHE BREADTH

Experimental or natural changes in the environment often lead to a range
expansion by some of the species in the community. This has been shown
following the removal of herbivores (Branch, 1981; Hawkins & Hartnoll, 1983),
predators (Paine, 1971, 1974; Dayton, 1971; Menge, 1976 or competitors
(Connell, 1961a; Hoshiai, 1964; Dayton, 1975a; Menge, 1976; Hruby, 1976;
Suchanek, 1978; Schonbeck & Norton, 1978; Emerson & Zedler, 1978; Larson,
1980; Hixon, 1980, 1981; Lubchenco, 1980; Hodgson, 1980; Montalva &
Santelices, 1981); or after death of some species in a community due to pollution
(e.g. Grassle & Grassle 1974; Pearson, 1975) or red tide (Dauer & Simon,
1976a, b). In some cases range expansion occurs into seemingly less favourable
conditions. For instance, removal of Acmaea digitalis (Fig. 20 see p. 471) results
in an upward movement of A. paradigitalis into an apparently more hostile
environment higher on the shore (Choat, 1977). Examples such as this suggest
that many species are capable of expanding their range if biological constraints
are lifted. This implies that they are not narrowly adapted to their environment
but have the genetic variability or phenotypic flexibility which will allow
extension into other, even physically more demanding, environments. Wolcott
(1973) suggests that species living on the border of a physically stressful but
unexploited environment probably live at the limits of their physiological
tolerance and should be capable of expanding their range if conditions improve,
capitalizing on the unexploited resource without hindrance from competitors. On
the other hand, species in more equable environments may suffer from intense
competition and will gain less from range expansion because this involves
movement into an area already occupied by a competitor. He argues that
selection will favour behavioural patterns restricting these species to the most
suitable parts of their range. This dichotomy will influence the nature of the
selective pressures imposed on an animal, and the intensity of competition it is
likely to face.
At least in part, the amount of genetic variability in a population will constrain
the adaptability of a species in responding to changing conditions, including
changes in the intensity of competition. Competition has, in turn, the potential to
influence the genetic composition of a population. It may cause a reduction of
genetic variability if particular genotypes suffer most from competition, and if it
persists for long enough it may result in ‘character displacement’ of sympatric
species, which may or may not reflect changes in genotypic composition. Thus,
any link between competition and genetic variability is of importance in trying to
guage the extent to which competition can influence the genetic composition of a
population.
Genetic variability exists in all populations, the amount of variability being

related to the population size, the selective pressures acting on the population and
the degree of isolation (see Gooch, 1975 for a review). One general hypothesis is
that genetic variability should be greatest in environments which are physically
unstable or variable. A wide range of genotypes is regarded as an insurance,
increasing the chances that at least some variants will survive fluctuations in the
environment. Levinton (1973) has shown for some bivalves that genetic
variability decreases in subtidal species that occur in deep waters, and in
intertidal or shallow-water species which burrow deeper into the sediment. He
assumes that increases of water depth, or depth within the substratum, will
decrease environmental variability; and he relates this to the reduction of genetic
variation. On the other hand, examining six bivalves which vary greatly in the
constancy of their environments, Wilkins & Mathers (1974) could find no
relationship between environmental and genetic variability. Gooch (1975) also
describes considerable genetic variability in deep-sea species, which are usually
considered to have an extremely constant environment. Ayala & Valentine (1977)
also discard variability of the physical environment as a cause of genetic
diversity, pointing to the very constant environmental conditions of the tropical
clam Tridacna maxima and the Antarctic brachiopod Liothyrella, which,
respectively, have very high and very low genetic variability in their populations,
and to the phoronid Phoronopsis, a temperate intertidal species which has a more
variable environment but only moderate genetic variability. No pattern appears in
these examples, and it seems that genetic and environmental variability are not
necessarily related.
An alternative suggestion is that the genetic variation of a species is correlated
with niche breadth. Comparing six species of Macoma, Levinton (1975) found
subtidal species did not have any less genetic variability than intertidal species
(in contradiction to the environmental-genetic variability hypothesis); but he did
find that variability at the G.P.I. locus (glucose phosphate isomerase) was
significantly correlated with niche breadth (Fig. 50).
Niche breadth is determined partly by the mode of dispersal a species has.
Crisp (1978) argues that species with long-lived pelagic larvae will disperse
widely and colonize very different environments. This will result in a similarity
of genetic composition between populations in different areas, but high genetic
variability within populations, permitting survival in widely different localities.
Species with restricted powers of dispersal are more likely to be specialized to
local conditions, with consequent low genetic variability, but with large genetic
differences between sites.
To test the niche-breadth hypothesis, Wilkins (1977) examined a number of
loci in Patella vulgata and P. aspera. P. vulgata has a far wider littoral
distribution than P. aspera and occupies shores with a much wider range of
conditions, but despite its wider habitat breadth, only at one out of nine was P.
vulgata more variable. At higher temperatures one of these loci (G.P.I.) was
much more stable in P. vulgata than in P. aspera. This relates to the higher
602 G.M.BRANCH
Fig. 50. Relationship between niche breadth and the effective number of alleles at the
glucose phosphate isomerase locus, for subtidal Macoma spp. at San Juan (A), and at
Moresby Island (B) (after Levinton, 1975).
temperatures which P. vulgata experiences high on the shore and Wilkins suggests
that selection has maintained the single phenotype which tolerates these
conditions, with the virtual elimination of the other alleles at this locus; although
Badino & Sella (1980) could detect no greater thermostability or lower
variability in the G.P.I. locus of a high-shore limpet in the Mediterranean than in
a low-shore species, and in both species the tolerance of all allozymes to high
temperatures (up to 55°C) far exceeded normal environmental conditions.
Fenchel & Christiansen (1977) have argued that the variance of realized niche
breadths will be reduced by interspecific competition. Such a response does occur
in several species, but can either be a short-term phenotypic response which is
reversed in the absence of a competitor, or a long-term genetic adjustment
involving the elimination of some genotypic variants or even a shift of
genotypes. Beardmore & Morris (1977) have tested this on Littorina spp. living
in sympatry, in allopatry or in intermediate conditions. They found significant
negative regressions between measures of heterozygosity (i.e. genetic variability)
and the extent of overlap between the Littorina spp. They suggest that
coexistence leads to a reduction of niche width, and that by way of normalizing
selection this may reduce genetic variability.
Murphy (1976) has found that in Acmaea the frequencies of eight alleles of the
leucine aminopeptidase (Lap) locus are influenced by the presence of other
Fig. 51.—A, frequency distribution of leucine aminopeptidase (Lap) alleles in six Acmaea
spp. which coexist and have overlapping habitats; B, in three Acmaea which have
specialized habitats and do not overlap congeners, the alleles have a central distribution
and are not displaced away from the alleles of other species; C, when Acmaea scabra and
A. digitalis coexist, their Lap alleles are displaced further apart (dotted lines) than in samples
taken from allopatric populations of the two species; (after Murphy, 1976).
Acmaea spp. In species which commonly coexist (Fig. 51A) the frequencies of
these eight alleles are displaced so that the species are quite different. Murphy
postulates that this divergence is due to character displacement, reducing
ecological overlap between the species. In support of this, he has also examined
three Acmaea spp. which have narrow isolated habitats, living, respectively, on
laminarian kelps, the alga Egregia, and on shells of live Tegula funebralis. In
these acmaeids the Lap alleles have much broader distributions with central
tendencies and no obvious displacement of the frequencies (Fig. 51B). Murphy has
also compared the allele frequencies in isolated and coexisting populations of
various species. For example, in allopatric Acmaea digitalis and A. scabra
populations the allele frequencies are more similar than in coexisting populations
(Fig. 51C). This may be taken as further evidence of character displacement
although it may also be due to differential survival of individuals with different
allele combinations. Murphy has been unable to examine the geneotypes of
newly settled individuals to determine which of these alternatives is more likely.
Another feature of Murphy’s study is that the three species with narrow niche
breadths have a greater mean number of alleles (6·3) than the more generalized
604 G.M.BRANCH
species (5·0) which also contradicts the niche-breadth genetic-diversity

hypothesis.
Valentine & Ayala (1977) have produced a generalized model (Fig. 52) in
which they suggest that temporal stability, and particularly stability of food
supply, is the key factor determining genetic variability; and they produce
evidence for this by comparing the trophic stability of Antarctic, temperate, and
tropical Euphausia spp. and showing that it is correlated with genetic diversity.
The low genetic variability of the Antarctic brachiopod Liothyrella, and the high
variability displayed by the tropical clam Tridacna maxima also conform to this
pattern, trophic stability being, respectively, low and high in these two species
(Ayala & Valentine, 1977; see also Battaglia, Bisol & Fava, 1977).
Valentine & Ayala (1977) argue that if conditions fluctuate widely in time,
species will have few alleles but these will have a broad functional range, so that
they can operate over a wide range of conditions. Fluctuating conditions will also
demand that species be flexible and have broad niches, perhaps leading to a low
diversity of species due to competitive exclusion. Species with broad niches will
perceive the environment as being ‘fine-grained’ in that they will range over a
variety of habitat types, and individuals will experience a variety of conditions,
both in time and in space. This will reinforce the need for them to have alleles
with wide functional ranges and, correspondingly, a limited number of different
alleles (low genetic variability). The larger and more mobile a species is, the
more likely it will perceive the environment as being fine-grained, and thus the
greater the chance of it having low genetic variability (Fig. 52). Conversely,
Valentine & Ayala propose that if conditions (particularly in terms of food
supply) are constant in time, high genetic variability and narrow functional
ranges of alleles are more likely to be selected for. Since constant environments
can accommodate a large number of species, competition may cause reductions
of niche width, leading to specialization. Such specialization is only possible in a
constant environment with a predictable source of food, and correlations between
stability and specialization have been found in a number of cases. Similarly,
correlations exist between species diversity and genetic variability and between
environmental heterogeneity and genetic variability (see Valentine & Ayala,
1977, and references therein). Specialized species will perceive the environment
as ‘coarse-grained’ and heterogeneous, with only certain patches being suitable
for occupation. This is particularly true for species that are small and relatively
immobile. Again, a patchy coarse-grained environment will favour the retention
of genetic variability, alleles being selected differentially in different ‘patches’ of
the environment and having a narrow functional range (Fig. 52).
Thus, constant conditions are associated with high species diversity, narrow
specialized niches, a coarse-grained environment, high genetic variability, and
possibly niche apportionment. Fluctuating conditions are linked with low species
diversity, broad niches and flexible responses to changing conditions, a fine-
grained environment, and low numbers of alleles with broad functional ranges.
Fig. 52.—Synopsis of the views of Valentine & Ayala (1977) on the relationship between
environmental constancy, niche breadth, species diversity and genetic variability within
populations.
Many of the links in Valentine & Ayala’s model are well-established, but
based on correlations. What is cause and what is effect is debatable in some of
these links. For instance, one can argue that when species diversity is high,
competition may cause specialization, permitting the larger number of species to
coexist. But an alternative view is that in a stable environment specialization may
be adaptive in its own right if it results in more efficient use of resources. Thus,
specialization could arise independently of whether competition occurs or not,
and might incidentally reduce competition. In similar vein, Valentine & Ayala
suggest that environmental inconstancy selects for broad niches, which increase
the overlap between species and lead to competitive exclusion, so that species
diversity is low. But the instability of the environment may itself be sufficient to
explain the low number of species, without recourse to competition, or in
addition to competition.
Work on genetic diversity is still in its infancy and there is contradictory
evidence for all of the general hypotheses advanced. The possible association
between trophic stability, narrow niches and greater genetic variability is
intuitively appealing, but in several of the examples described above individual
selective pressures such as thermal stress or competition may be of greater
importance in explaining allelic frequencies in particular cases. The limited
evidence we have suggests that interspecific competition does reduce niche
breadth and genetic diversity, but more extensive data are needed before
generalizations such as this can be made with confidence.
606 G.M.BRANCH
COMPETITION AND SPECIATION

Competition between species may follow different pathways under different
circumstances, and Fig. 53 summarizes, in hypothetical form, six prevalent
views of how competitors interact.
(1) The niche divergence hypothesis (Fig. 53A): competition will select for
divergence and specialization which reduce competition, allowing the
species to coexist. Competition is most likely to be by exploitation.
(2) The competitive elimination hypothesis (Fig. 53B): the superior competitor
eliminates the subordinate from most or all of the dominant’s habitat. In
time, the subordinate may evolve a narrow niche which overlaps little with
the dominant’s niche, which remains unaltered by the interaction.
Competitive dominance is most likely to involve interference.
(3) The disturbance hypothesis (Fig. 53C): the superior competitor has the
potential to prevent the subordinate from occupying its habitat, but physical
disturbance or predation prevent the dominant from occupying the whole of
its habitat so that the subordinate can coexist with it whenever and wherever
its numbers are reduced.
(4) The exclusion hypothesis (Fig. 53D): the superior species continually
excludes the inferior from its habitat, but the inferior species can survive
because it has a refuge beyond the habitat of the dominant. Ultimately, the
inferior species will depend upon disturbance to prevent total exclusion from
the niche of the superior species, or it will eventually evolve a narrower
niche, so that this hypothesis caters only for short term interactions between
a dominant and inferior species.
(5) The lottery or ‘equal chance’ hypothesis (Fig. 53E): chance events
determine which species establishes itself first, and priority grants this
species supremacy over later arrivals. Since dominance is only retained by
possession, death of an occupant opens the way for another chance recruit to
establish itself. Global stability and continued existence of all the species is
maintained, although locally one species may dominate another temporarily
and exclude it from most of its habitat.
(6) Changing circumstances hypothesis (Fig. 53F): one species may be dominant
and exclude another from part of its potential niche, but short-term changing
circumstances may reverse the rôles of the species.
Hypotheses (1) and (2) require genetic change to explain long-term coexistence
in equilibrium populations; hypotheses (3) to (6) do not, relying on disturbance,
refugia, chance or changes in dominance to explain continued coexistence.
Evidence exists for all six hypotheses, but only the first two are of relevance to
the question of whether interactions between competitors mould the evolution of
species, since they involve genetic changes. There is a good deal of
circumstantial evidence that divergence occurs when similar species coexist (see
Schoener, 1974, for a review). This evidence takes the form of niche expansion
in the absence of a competitor, as in Conus miliaris (Kohn, 1978), or of character
displacement in areas of sympatry, for example in Hydrobia spp. and Sphaeroma
spp. (Fenchel, 1975b; Frier, 1979a, b), or of increasing specialization in areas
where a number of congeners coexist, as happens in Conus spp. (Kohn, 1966,
1968, 1971) and Patella spp. (Branch, 1981). On the other hand, many
reservations have been expressed about the prevalence or even the existence of
competition-induced niche divergence (e.g. Connell, 1980) as a genetically based
process of evolutionary significance. The reasons for these reservations have
already been outlined in this review (pp. 456 and 528). If we are to discard
competition as a selective agent causing niche divergence, or regard this as a rare
event, we are left with the situation that certain phenomena, best explained as the
outcome of competition, have no ready explanation.
I believe that two different processes are in operation, one affecting the nature
of the species, the other affecting only the character of localized populations of
the species. Character displacement is likely to fall into the latter category. In
only one case reviewed in this paper (that of Lap alleles in acmaeid limpets,
Murphy, 1976) does character displacement have a proven genetic basis; and
even in this case it is likely to be due to the selective elimination of certain
genotypes and not to a true divergence involving the generation of new
genotypes which further displace the participating competitors. The other
examples of character displacement seem to be phenotypic responses.
Ecologically, such local divergence of competing species may be of significance
in reducing competition. But even if we were to accept that it is genetically
controlled, it is unlikely that such character displacement could ever be
transmitted to an entire species, for it will have no selective value in allopatric
populations that occupy geographic regions where competition between the two
species does not occur. Furthermore, as Connell (1980) has stressed, long-term
and wide-ranging coexistence between competitors will be unusual because
competitors are not obliged to coexist, making co-evolutionary divergence
difficult. Co-evolution that is sufficiently sustained and widespread to transmit
niche divergence throughout all the populations of a given species is even less
likely.
Thus, we are left with having to explain why some species are
characteristically specialized throughout their ranges, and the phenomenon that
specialized species tend to occur in areas where several congeners coexist.
Figure 23 (see p. 475) exemplifies one such situation: the average specialization
of southern African Patella spp. (in terms of both diet and habitat) increases in
proportion to the number of species that coexist. Amplifying this result gives
some clue as to how the situation may arise. The specialization of each of the ten
species involved in this analysis remains almost unchanged throughout their
geographic ranges. They do not become more specialized in areas where there
are more congeners. The increase in T specialization is attained because as one
moves round the coast of southern Africa, from Angola down the west coast to
608 G.M.BRANCH
the southern extremity of South Africa, the number of Patella species increases,
and the species which are added are those more specialized in terms of having very
restricted diets or zonation patterns. Thus, an increase in species involves the
addition of more specialized species, increasingly elevating the average
Fig. 53.—Contrasting views of how hypothetical competing species may influence one
another: in each figure, one species (A) is assumed to occupy allopatrically a certain
portion of a limiting resource, and a second species (B), with overlapping requirements, is
introduced to the community at a later stage and coexists with A; there are six possible
outcomes (A—F) (see text for amplification); dashed lines indicate those portions of the
potential niche of either species which is unrealized due to the pressure of competitors,
predators, physical disturbance or chance events.
specialization exhibited by the genus as a whole. The reverse pattern can be

recorded in moving up the east coast of South Africa towards Moçambique: a
610 G.M.BRANCH
reduction of limpet diversity and of average specialization.

This may explain the correlation between species diversity and specialization,
but not its origins, particularly as it seems unlikely that character displacement
can ever spread throughout an established species if it arises in a localized
population. On the other hand, if competition is one of the selective agents
influencing the species at its inception, it could fix a speciesspecific
specialization in the genetic make-up of the species at that stage. The modern
view of speciation is that it is likely to occur in small populations which are isolated
from their parental stock. This being so, an incipient species could have its niche
constrained by the presence of a competitor during the speciation process. In a
similar manner, competition could act as a ‘sieve’, screening out species during
the speciation event, preventing populations with the potential to radiate from
doing so because competition is too intense.
Such a process could have yielded the pattern recorded for Patella species in
southern Africa. In areas where only one species occurs it is generalized with
broad diet and habitat. Should a second species develop in sympatry with it, its
characteristics could be moulded by the pre-existing species, either by the
elimination of these genotypes overlapping the niche of the existing species (the
competitive elimination hypothesis, Fig. 53B) or, in a more neutral manner, by
having no effect on the development of a new species if it is sufficiently
different that it does not overlap at all with existing species. For instance, the
evolution of a kelp-dwelling specialist, P. compressa, yielded a species which
overlaps not at all with the other Patella species, and which would have lain
beyond the competitive sieve of pre-existing species. While there is no reason
why such a specialized animal could not evolve without competition taking
place, I would contend that the likelihood of its evolution is increased by a
competitive sieve of other species. Thus, the addition of more and more species
towards the southern tip of South Africa would demand increasing specialization
of each addition. In the process, no narrowing or divergence of the niches of
existing species would be necessary, and the evidence suggests it did not take
place, for the generalized species have the same specialization index in areas
where there are several congeners as they do where there are few congeners or
where they are allopatric (Branch, 1984).
If this interpretation of the rôle of competition in influencing the specialization
of species is correct, one would expect that geologically older species will be
those with broadest niches. As yet the fossil record for southern African Patella
spp. is too fragmentary to draw such conclusions. Porter (1976), in comparing
the trophic relationships of different corals (see Fig. 18, p. 467) was able,
however, to show that the earliest coral families to evolve are those with
broadest niches. while later additions to the fauna which appear in the more
recent fossil record are more specialized for either autotrophy or the capture of
zooplankton, and the variety of their body forms is much more restricted.
Indirect evidence that this may be true for southern African Patella spp. comes
from the fact that the geographic range of each species is inversely correlated
with its index of specialization. A further pointer is that the single patellid
occurring on the geologically youthful Marion Island, Nacella delesserti is very
generalized with an exceptionally broad niche in terms of both habitat (zonation)
and diet. As the only limpet species on the island, this endemic species has had to
contend with no other competitors (W.A.Blankley & G.M.Branch, in prep.).
Another interesting feature of the Patella spp. is that interference competition
is evolved in three of them—P. longicosta, P. tabularis and P. cochlear (Branch,
1975b, 1976) and intraspecific territoriality in a fourth species, P. compressa,
and these four are amongst the most specialized of the Patella spp. As the
diversity of the genus rises, so the incidence of interference competition
increases. As a partial test of whether specialization in these Patella spp. is
genetic or simply a phenotypic response to the presence of competitors,
manipulative experiments have been undertaken (Branch, 1984). In no case did
the removal of any of the generalized species have any impact on the diets of the
specialized species, despite several potential food sources becoming available as
a result, indicating genetic control of the diet of these species. On the other hand,
removal of two territorial species (P. cochlear and P. longicosta) did allow other
species to invade areas normally dominated by these limpets. Thus, zonation of
these other species, which are less specialized and non-territorial, is determined
partly by exclusion from the zones occupied by the territorial limpets. These less
specialized species therefore have the potential to live beyond their normal zones,
in the absence of dominant competitors (a result similar to that recorded by Choat,
1977, for acmaeid limpets).
I have earlier argued that competition for space will often lead to exclusion (p.
558), particularly if interference is involved (cf. Fig. 53D), but that competition
for food is more likely to lead to coexistence and perhaps the evolution of dietary
specialization (cf. Fig. 53B). Specializations of diet or habitat are only likely to
evolve in relatively constant, predictable environments; and it is also in such
environments that the long-term coexistence of competitors is likely, and that
populations will live in equilibrium. Thus, it is no coincidence that all the
specialized limpets in southern Africa have evolved in the low shore and subtidal
zone; the mid- and upper shore being occupied by three species with very
generalized habits (Branch, 1976, 1981). The patterns displayed by these Patella
spp. are what gave rise to the hypothesis I have advanced above: that competition
can mould the evolution of species, but that it is most likely to influence the
character of a species at the time of the speciation event, when species-wide
characteristics are genetically fixed in a species.
It should also be remembered that the evolution of mechanisms improving the
competitive ability in a species, such as interference, is another avenue to
counter competition. Such mechanisms could also be evolved at the inception of
a species, in response to competition; but as discussed above (p. 562), I believe
that they are more likely to have evolved pre-adaptively in response to other
selective agents, including intraspecific competition. Thus, competition will have
different evolutionary consequences dependent on whether (a) it acts at the
612 G.M.BRANCH
inception of the species and thus influences the character of the species
throughout its range, or (b) it acts on localized populations of an already
established species. In the latter case even phenotypic responses may be adequate
to counter short-term competition, but localized genetic changes may take place
if the competition is sustained.
ACKNOWLEDGEMENTS
As always, the loving support of my wife Margo has been the most important factor
allowing me to complete this work; and she also completed all the illustrations.
God bless you Margs. Many people have shared their ideas with me, especially
Bob Black, Adrian Craig, Rob Crawford, Bob Creese, Rob Day, Lev Fishelson,
John Gray, Charlie Griffiths, Pat Hulley, Wynn Knight-Jones, Paul Leviten, Ken
Mann, Hugh Paterson, Peter Sale, Frank Talbot, and Richard Warwick; but very
particular thanks are due to Bob Paine and Tony Underwood whose work
provided much stimulus and who so willingly gave of time to mull over ideas.
The long haul of typing the manuscript was gracefully and competently
undertaken by Leonora Fox. My warmest thanks to all.
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ADDENDUM
Since going to press, two important reviews have appeared. T.W.Schoener (1983,
Am. Nat., 122, 240–285) has summarized field experiments, and a whole number
of American Naturalist (Vol. 122, No. 5) has been devoted to essays on
competition.
AUTHOR INDEX
References to complete articles are given in heavy type; references to pages are
given in normal type; references to bibliographical lists are given in italics.
Abbott, D.P. See Grünbaum, H., 436; 585 See Knight-Jones, E.W., 547; 586
Abbott, M.R., 126, 128, 141; 160 Alosi, M.C. See Reish, D, J., 494; 589
Abele, L.G., 462; 580 Alp, P.R., 299; 305
See Coen, L.D., 494, 530, 562; 582 Alvarino, A., 343, 346, 356, 363, 364; 389
Abrams, P., 452, 510; 580 Amade, Ph., 478, 562; 580
Achituv, Y., 289; 305 Amann, H. See Mustaffi, Z., 196; 209
Acton, F.S., 112; 121 Amaratunga, T., 399, 409, 410, 416, 423;
Adams, J.A.S. See Horn, M.K., 181; 190 425
Addy, S.K., 173; 186 Amiel, A.J., 196, 200, 202, 203, 204, 205;
Adelseck, C. See Borella, P.E., 170; 187 208
Adey, W.H. See Brawley, S.H., 489, 534, Anderson, D.J., 448; 580
562; 581 Anderson, E.R. See Munk, W.H., 133; 164
Aida, T., 356, 369; 389 Anderson, F. See Hovis, W.A., 96
Akaka, L. See Hildemann, W.H., 585 Anderson, G.C. See Jamart, B.M., 122
Akaka, L.K. See Hildemann, W.H., 585 See Winter, D.F., 137; 168
Akerboom, T.P.M. See Groen, A.K., 308 Anderson, G.s.V., 522, 524; 580
Alcock, G.A., 36; 51 Anderson, G.R.V. See Russell, B.C., 523;
Alexander, J.E., 206; 208 590
Allan, T.D., 82; 96 See Talbot, F.H., 522; 592
Allen, B.L. See Hofer, H.W., 269; 309 Anderson, K.P., 517; 580
Allen, C.M., 146; 160 Anderson, R.J. See Chan, A.T., 487; 582
See Simpson, J.H., 146; 166 Anderson, S.J. See Carpenter, E.J., 389
Allen, J.S., 29, 149; 51, 160 Andersson, E., 396; 425
See Enfield, D.B., 157; 162 Andre, S.V. See Peterson, C.H., 503, 527,
Allen, R.C. See Rhoads, D.C., 506; 589 565; 589
Aller, R.C., 173, 178, 506; 186, 580 Andrews, J.E. See Boyland, D.B., 198; 209
Almeida-Prado, M.S.de, 412; 425 Anonymous, 179; 186
Almy, C.C. See Harriss, R.C., 195, 196, Ansell, A.D., 294, 298; 305
200, 201, 202, 204; 209 See Blackstock, J., 297; 306
Al-Ogily, S.M., 478, 487, 564; 580 Antezana, T. See Dayton, P.K., 442; 585
628
AUTHOR INDEX 629
Apel, J.R., 82; 96 Bailey, M. See Perkins, E.J., 32; 53

Apstein, C., 410; 425 Bainbridge, A. See Corliss, J.B., 188
Argote-Espinoza, M.L. See Simpson, J.H., Bajkov, A.D., 378; 389
123 Bak, R.P.M., 465, 532; 580
Ariani, A.P., 398; 425 Baker, A.E.M. See Baker, M.C., 516 580
Ármannson, H. See Kidd, R.B., 183; 190 Baker, E.T. See Hovis, W.A., 96
Armstrong, P.B. See Lyons, W.B., 191 Baker, K.S., 62; 96
Arnold, G.P. See Harden-Jones, F.R., 32; See Smith, R.C., 59, 132; 97, 167
51 Baker, L.D. See Reeve, M.R., 385, 387;
Arnoldus, M.J.H. See van de Weijden, 391
C.H., 178; 194 Baker, M.C., 516; 580
Arrhenius, G.O.S. See Goldberg, E.D., Bakke, T. See Skjoldal, H.R., 273; 312
179, 181; 190 See Widdows, J., 313
Ashmole, N.P., 515, 527; 580 Bakus, G.J., 562, 564; 581
Aspden, K.R. See Seliger, H.H., 166 Baldauf, J.G. See Gardner, J.V., 179; 189
Aston, S.R., 176; 186 Baldo-Kost, A.L., 409; 425
See Boyden, C.R., 178; 186 Bale, A.J. See Morris, A.W., 176, 178; 192
See Chester, R., 179, 181; 188 Balistrieri, L., 169, 173; 186
See Hirst, J.M., 178; 190 Ball, D. See Hovis, W.A., 96
Atkinson, D.E., 266, 272, 273; 305 Ballard, R.D. See Corliss, J.B., 188
See Klungsøyr, L., 272; 309 Balzer, W., 176; 186
See Ramaiah, A., 272; 311 Bambach, R.K. See Levinton, J.S., 503,
See Shen, L.C., 273; 312 565; 587
Atkinson, L.P., 154; 160 Båmstedt, U., 212, 214, 215, 245, 291,
See Paffenhofer, G.A., 155; 165 294, 295, 418; 260, 305, 425
Augenfield, J., 288, 289; 305 See Skjoldal, H.R., 273, 295; 312
Augustinsson, K.B., 212; 260 Banke, E.G. See Smith, S.D., 38; 53
Austin, J. See Raymont, J.E.G., 294; 311 Banner, L.H. See Nimmo, D.R., 405; 427
Austin, M.J. See Denman, K.L., 162 Bannister, T.T., 59; 96
Austin, R.W. See Hovis, W.A., 96 Banse, K. See Jamart, B.M., 105; 122
Avise, J.C., 280; 305 See Winter, D.F., 137; 168
Awapara, J. See Simpson, J.W., 287; 312 Barber, J. See Heslop-Harrison, J., 339;
See Stokes, T.M., 287; 312 341
Ayal, Y., 474; 580 Barber, R.J., 149, 150; 160
Ayala, F.J., 280, 293, 431, 478, 559, 569, Barber, R.T. See Huntsman, S.A., 136,
571; 305, 580 151; 163
See Valentine, J.W., 571, 572, 573; 592 See Packard, T.T., 144; 165
Ayling, A.M., 488, 544; 580 See Sunda, W.G., 173; 193
Ayres, P. See Jones, K.J., 122 Bardawill, C.J. See Gornall, A.G., 212; 261
Barilotti, D.C. See Blackman, T.W., 319;
Baas Becking, L.G.M., 170; 186 340
B cesco, M., 400, 411;425 Barlow, G.W., 437, 519; 581
Bach, C., 508, 509, 510; 580 Barnard, L.A., 196, 202; 208
Backman, T.W. See Phillips, R.C., 342 Barnes, H., 32, 212, 286, 294, 402, 409,
Backus, R.H., 75; 96 567; 51 260, 305, 306, 425, 581
Bacon, M.P., 176; 186 See Achituv, Y., 289; 305
Badino, G., 570; 580 See Heath, J.R., 294; 309
Barnes, H.L. See Crerar, D.A., 169; 188
630 OCEANOGRAPHY AND MARINE BIOLOGY
Barnes, J.R., 488; 581 Bender, M.L., 172, 177, 179, 181, 182, 183;
Barnes, M. See Achituv, Y., 289; 305 186, 187
See Barnes, H., 294, 402, 567; 305 See Froelich, P.N., 189
425, 581 See Graham, W.F., 178; 190
Barnevik, F.W. See Walsh, J.J., 168 See Honnorez, J., 190
Barrett, R.L. See Wilson, J.B., 442; 593 See Klinkhammer, G.P., 172, 178; 191
Barrett, T.J., 184; 186 See Luedtke, N.A., 178; 191
See Honnorez, J., 190 Bennett, R., 270; 306
Barron, J.L. See Bewers, J.M., 172; 187 Benninger, L.K. See Aller, R.C., 173, 178;
Bassett, H., 32; 51 186
Battaglia, B., 280, 571; 306, 581 Benson, A.A., 199; 205
Battelle, B.-A., 268; 306 Berge, J.A., 507; 581
Battey, J.F. See Porter, J.W., 589 Bergeijk, W.A.van, 348; 389
Baxter, G.C., 19; 51 Berger, E.M., 280; 306
Baxter, M.S. See McKinley, I.G., 33; 52 Berger, W.H., 179; 187
Baylor, E.R. See Sutcliffe, W.H., 137; 167 Bergman, G. See Grünbaum, H., 436; 585
Bayne, B.L., 264, 278, 303; 306 Bergmans, M. See Van den Berghe, W.,
See Gabbott, P.A., 264; 308 501; 592
See Koehn, R.K., 281; 309 Berlind, A. See Lemos, J.R., 268; 310
See Livingstone, D.R., 294; 310 Bernal, P.A., 156; 160
See Moore, M.N., 310 See Chelton, D.B., 156; 161
See Widdows, J., 313 Berner, R.A., 170; 187
Beales, F.W. See Wolf, K.H., 195; 210 Bernicard, A. See Thébault, M.-T., 277;
Beardall, J. See Richardson, K., 60; 97 312
Beardmore, J.A., 570; 581 Bernstein, B.B., 480, 481, 527, 534; 581
See Battaglia, B., 280; 306 Bernstein, R.L., 154; 161
Beardsley, R.C., 19, 28, 30, 142; 51, 160 Berreur-Bonnenfant, J. See Cuzin-Roudy,
Beauchamp, P.de, 343, 354; 389 J., 399, 419; 426
Becker, K. See Honnorez, J., 190 Berrill, M., 399, 409; 425
Beddington, J.R. See May, R.M., 436; 587 Berry, R.J., 281; 306
Bedwell, J.A. See Baxter, G.C., 19; 51 Berry, W.J. See Johns, D.M., 406; 426
See Horwood, J.W., 44; 52 Bertalanffy, L.von, 404; 425
Begon, M., 431, 458, 485; 581 Bertness, M.D., 445, 446, 447, 452, 453,
Behrens, S., 436; 581 509, 510, 511, 528, 553; 581
Beiles, A. See Nevo, E., 282; 310 Betzer, P.R. See Bolger, G.W., 184; 187
Beis, I., 274, 298; 306 Beustel, O. See Samain, J.F., 311
See Zammit, V.A., 275, 298; 313 Bewers, J.M., 172; 187
Bejda, A.J. See Olla, B.L., 455; 588 See Yeats, P.A., 176, 178; 194
Belderson, R.H., 27; 51 Beyth, M. See Bonatti, E., 187
B′ lehrádek, J., 394; 425 Bhatti, E.L., 327; 340
Belk, M.S., 520, 523; 581 Bianchi, T.S., 496, 497; 581
Bell, T.H., 141; 160 Bienfang, P., 108, 109; 121
Bellan, G., 300, 303; 306 Bienfang, P.K., 130; 161
Bellan-Santini, D. See Bellan, G., 300; 306 Bieri, R., 349, 369; 389
Benayahu, Y., 465, 538; 581 See Tokioka, T., 356, 369; 392
Bender, M. See Elderfield, H., 178; 189 Biernbaum, C.K., 462, 502; 581
See Klinkhammer, G., 184; 191 Bigelow, H.B., 142, 343, 345, 364, 386;
See McCaffrey, R.J., 192 161, 389
AUTHOR INDEX 631
Bigger, C.H., 465; 581 See Lynn, D.C., 179; 191

Biggley, W.H. See Seliger, H.H., 166 Bonaventura, C. See Mangum, C.P., 310
See Swift, E., 75; 97 See Weber, R.E., 288; 313
Bignell, R.D., 184, 185; 187 Bonaventura, J. See Mangum, C.P., 310
Biggs, D.B. See Krone, M.A., 207; 209 See Weber, R.E., 288; 313
Billen, G. See Duinker, J.C., 178; 189 Bone, Q., 356; 389
See Wollast, R., 178; 194 Boney, A.D. See Khfaji, A.K., 487; 586
Birge, E.A. See Juday, C., 418; 426 Bonner, W.A., 87; 96
Birkeland C., 442, 540; 581 Boral, L.L. See Orput, P.A., 320; 341
See Glynn, P.W., 534; 584 Borchert, H., 174; 187
See Mauzey, K.P., 442; 587 Borella, P.E., 170; 187
Birkhead, T.R., 439; 581 See Honnorez, J., 190
Biscaye, P. See Bender, M.L., 187 Borne, M.M. See Samain, J.F., 311
Bischoff, J. See Li, Y.-H., 173; 191 Borodich, N.D., 407, 411; 425
Bischoff, J.L., 173, 180, 183; 187 Borole, D.V. See Moore, W.S., 175; 192
Bishop, J.M. See Morgan, C.W., 154; 164 Borstad, G.A., 132; 161
Bisol, P.M. See Battaglia, B., 571; 581 Boström, K., 176, 179, 183; 187
Bitterman, D.S. See Joyce, T.M., 159; 163 Boucher, J., 278; 306
Black, R., 434, 438, 439, 442, 474, 527; See Samain, J.F., 311
581 Boudreau, B.P., 181; 187
See Stimson, J., 434; 591 Bougis, P., 127; 161
Blackburn, M., 144; 161 Boulton, P.S., 346, 347; 389
Blackman, T.W., 319; 340 See Horridge, G.A., 346, 347, 348,
Biackstock, J., 263–313; 264, 270, 273, 349, 354, 356, 367; 390
283, 293, 295, 296, 297, 299, 302; 306 Bovbjerg, R.V., 443, 494, 530, 563; 581
See Achituv, Y., 289; 305 Bowden, K.F., 12, 14, 15, 16, 32; 51
See Barnes, H., 212; 260 Bowen, V.T. See Goldberg, E.D., 308
See Pearson, T.H., 264, 283, 301; 311 See Livingston, H.D., 12; 52
Blasco, D. See Margalef, R., 108; 122 Bowers, D. See Simpson, J.H., 105; 123
See Packard, T.T., 144; 165 Bowman, M.J., 107, 108, 118, 137, 142,
Blegvad, H., 395, 399, 407; 425 147, 148, 153; 121, 161
Bligh, E.G., 212; 260 See Pingree, R.D., 153; 165
Boaden, P.J.S., 480; 581 Bowser, C.J., 180; 187
See O’Connor, R.J., 480, 527, 532; 588 See Callender, E., 172, 173, 174, 175;
See Seed, R., 527; 591 188
Boal, J., 489, 538; 581 Boyden, C.R., 178; 187
Boalch, G.T. See Russell, F.S., 157; 166 Boyer, J.F., 280; 306
Bocchi, G. See Morten, L., 192 Boyland, D.B., 198; 209
See Rossi, P.L., 183; 193 Braarud, T. See Gran, H.H., 100, 135; 121,
Boesch, D.F., 493; 581 163
Bohnsack, J.A., 523, 541; 581 Brace, R.C., 443, 465; 581
Bohrer, R. See Fournier, R.O., 143; 162 Bradbury, R.H., 468; 581
Boicourt, W.C., 142; 161 Bradford, M.M., 258, 259; 260
See Mooers, C.N., 142; 164 Bradstreet, R.B., 212; 260
See Beardsley, R.C., 28, 30; 51 Branch, G.M., 429–593; 433, 434, 435,
Boje, R., 149; 161 436, 437, 443, 444, 445, 446, 448, 449,
Bolger, G.W., 184; 187 454, 469, 471, 472, 474, 475, 478, 479,
Bonatti, E., 179, 182, 183, 184, 185; 187
487, 488, 490, 527, 530, 544, 563, 564, See Brown, O.B., 156; 161
566, 567, 575, 578, 579; 581 Brujevicz, S.W., 173; 188
Branch, M.L. See Branch, G.M., 435, 436, Bruland, C.W. See Landing, W.M., 172;
444, 469, 472, 479, 490, 544, 564; 581 191
Brand, I.A. See Soling, H.D., 269; 312 Brunfelt, A.O. See Morten, L., 192
Brand, L.E. See Waterbury, J.B., 68; 97 Bryan, P.C., 564; 582
Brannon, A.C. See Rao, K.R., 311 Bryan, P.G. See Tsuda, R.T., 522; 592
Brawley, S.H., 489, 534, 562; 581 Buat-Menard, P., 173; 188
Bray, R.N. See Ebeling, A.W., 518, 527, Buddemeier, R.W., 196, 198, 202, 203; 209
528; 583 Bullock, A.M. See Jones, K.J., 122
Breaker, L. See Bernstein, R.L., 154; 161 Bullock, T.H., 352, 353, 354, 357; 389
Breen, P.A. 445, 446, 534; 582 See Rao, K.P., 402; 427
See Mann, K.H., 534; 587 Bulnheim, H.-P., 280; 306
Bremer, P., 418; 425 Burdick, D.B. See Gagnon, P.S., 318; 340
Brenchley, G.A., 506, 507; 582 Burdige, D.J., 173; 188
Brewer, P.G., 172, 176; 187, 188 Burfield, S.T., 345, 346, 349, 350, 351,
See Bacon, M.P., 186 353, 354, 358, 364; 389
See Balistrieri, L., 169; 186 Burkholder, P.R., 479; 582
See Murray, J., 169; 192 Burman, J.-O. See Boström, K., 176; 187
See Spencer, D.W., 176, 177; 193 Burns, B.R. See Wigley, R.L., 410; 428
Bricaud, A., 55; 96 Burns, R. See Moore, W.S., 192
Brichet, E. See Lalou, C., 183; 191 Burns, V.M. See Moore, W.S., 192
Bridges, K.W. See Phillips, R.C., 321; 342 Buroker, N.E., 280; 306
Bricker, O.P. See Holdren, G.R., 173; 190 Burton, J.B. See Moore, R.M., 178; 192
Bright, T.J. See Thompson, Jr, J.H., 196, Burton, R.S., 281; 306
207; 210 Busch, W., 343, 352, 356, 386; 389
Brink, K.H., 152; 161 Bushing, M., 363, 377, 379, 381, 382, 383,
Brinkhurst, R.O., 545, 546; 582 387; 389
See Chua, K.E., 545; 582 Busk, G., 345, 364; 389
Briscoe, M. See Gregg, M, 138; 163 Buss, L. See Jackson, J.B.C., 479, 532, 562,
Briscoe, M.G., 138; 161 564; 586
See Haury, L.R., 140; 163 Buss, L.W., 479, 480, 482, 532, 533, 546;
Brock, R.E., 488, 524, 534; 582 582
Broecker, W. See Bender, M.L., 187 Bustamante, A. See Zuta, S., 144; 168
Broecker, W.S., 169, 172, 173, 179; 188 Butler, A.J. See Keough, M.H., 534; 586
See Bender, M.L., 181; 187 Butler, E.I. See Knox, S., 191
Brooks, R.R. See Presley, B.J., 173; 192 See Russell, F.S., 157; 166
Brown, A.C., 407, 412; 425 See Southward, A.J., 157; 167
Brown, B.E., 196, 198, 203, 204; 209 Butler, L.W. See Scott, M.R., 193
See Howard, L.S., 195–210 Buzas, M.A. See Young, D.K., 507; 593
Brown, D.T. See Swift, E., 75; 97 Byers, B.A., 447; 582
Brown, M.B. See Dixon, W.J., 216; 261
Brown, O.B., 156; 161 Cacchione, D., 139; 161
Brown, R.M. See Borstad, G.A., 161 Caine, E.A., 476; 582
Brown, W.L., 456; 582 Calabrese, A. See Vernberg, F.J., 265; 312
Brubaker, J.M. See Caldwell, D.R., 139; Caldwell, D.R., 139; 161
161 Caldwell, J. See Gaines, M.S., 280; 308
Bruce, J.G., 156; 161
AUTHOR INDEX 633
Caldwell, R., 451; 582 Charnov, E.L. See Pyke, G.H., 548; 589
Caldwell, R.L., 436, 450, 530; 582 Chase, R.L. See Grill, E.V., 183; 190
See Dingle, H., 494, 563; 583 Chatfield, C., 113; 121
Callender, E., 172, 173, 174, 175; 188 Chelton, D.B., 156, 157; 161
See Bowser, C.J., 180; 187 Chess, J.R. See Hobson, E.S., 454; 586
See Robbins, J.A., 175; 193 Chesson, P., 128; 161
Calvert, S.E., 173, 178; 188 Chesselet, R. See Buat-Menard, P., 173;
See Duchart, P., 173; 189 188
See Price, N.B., 173; 193 See Sundby, B., 176, 181; 194
Campbell, C.A., 280; 306 Chester, R., 179, 180, 181; 188
Campbell, J.A., 173; 188 Chet, I. See Mitchell, R., 197, 206; 209
Campbell, J.W., 80; 96 Cheung, G. See Hildemann, W.H., 585
Campbell, L., 83; 96 Cheung, G.P. See Hildemann, W.H., 585
Campbell, P.N., 260; 260 Chevolot, L. See Amade, Ph., 478, 562;
Canino, M.F., 358, 363, 370, 371, 373, 377, 580
379, 381, 387; 389 Chew, K.K. See Buroker, N.E., 280; 306
Cann, J.R., 183; 188 Childress, J.J., 213, 217, 218, 398, 414,
Cantelmo, A.C. See Rao, K.R., 311 423, 424; 260, 426
Carhart, J.A. See Mangum, C.P., 287; 310 See Felbeck, H., 184; 189
Carpenter, E.J., 348; 389 Chilingar, C.V. See Wolf, K.H., 195; 210
See Campbell, L., 83; 96 Chisholm, S.W. See Olson, R.J., 83; 97
Carpenter, G.F., 410; 426 Choat, J.H., 434, 471, 519, 527, 528, 568,
Carpenter, R., 169; 188 579; 582
Carpenter, R.H., 174; 188 See Schiel, D.R., 438, 439; 590
Carr, R.F. See Mottl, M.J., 183; 192 Chornesky, E. See Woodley, J.D., 168
Carr, R.S., 302, 303; 307 Christiansen, F.B. See Fenchel, T., 505,
See Reish, D.J., 303; 311 570; 584
Carroll, J.W. See Chambers, J.E., 307 Christie, W.W., 213, 225, 245, 252; 260
Carson, R.M. See Allen, C.M., 146; 160 Cnua, K.E., 545; 582
Carson, T.A. See Breen, P.A., 534; 582 See Brinkhurst, R.O., 545; 582
Cartwright, D.E., 24; 51 Churchill, A.C., 317, 318; 340
Cassie, R.M., 113; 121 Clamp, J.R. See Bhatti, E.L., 327; 340
Clancy, R.M. See O’Brien, J.J., 165
Ceccaldi, H.J. See Trellu, J., 277; 312 Clark, C.W. See May, R.M., 436; 587
Cerling, T.E., 174; 188 Clark, D.K. See Gordon, H.R., 71; 96
Chaisson, R.E., 280; 307 See Hovis, W.A., 96
Chalmer, P.N., 542; 582 Clarke, A., 235, 239, 246; 260
Chambers, J.E., 294; 307 Clarke, A.E., 339, 340; 340
Chambers, R.E. See Bhatti, E.L., 327; 340 See Knox, R.B., 341
Chan, A.T., 487; 582 Clarke, A.J. See O’Brien, J.J., 165
Chan, H.L. See Edmond, J.M., 189 Clarke, K.U., 401; 426
Chandler, I.M. See Laxen, D.P.H., 175; Clarke, R.D., 522; 582
191 Clarke, T.A., 518, 562; 582
Chao, T.T., 174; 188 Claus, T.H., 269; 307
Chapnick, S.D., 175; 188 Clavaud, A., 335; 340
Charnell, R.L. See Schumacher, J.D., 142; Cleland, M.G. See Robertson, D.R., 564;
166 590
Clifford, P. See Woodley, J.D., 168
Clutter, R.I., 398, 406, 419, 423; 426 Corliss, J.B., 183, 184; 188
Coachman, L.K., 143; 161 See Edmond, J.M., 189
See Kinder, T.H., 142; 163 Cormick, R.K. See Crerar, D.A., 169; 188
Cobb, J.S., 127; 161 Cosper, T.C., 349, 350, 358, 359, 370, 373,
Codispoti, L.A. See Smith, S.L., 156; 167 383, 385, Fig 4 (Feigenbaum & Maris)
Cody, M.L., 514, 515, 527; 582 facing p. 350; 389
Coen, L.D., 494, 530, 562, 563; 582 See Reeve, M.R., 348, 358, 359, 361,
Coffino, P., 279; 307 374, 375, Fig. 12 (Feigenbaum &
See Steinberg, R.A., 279; 312 Maris) facing p. 358; 389
Cohen, P., 267; 307 Cottam, G.L. See Hall, E.R., 270; 305
Coil, J.A. See Leigh-Abbott, M.R., 143; Coull, B.C. See Ivester. M.A., 501; 586
164 Cox, P.A., 336; 340
Colebrook, J.M., 157; 161 Crabtree, B., 269; 307
Coles, S.L., 452; 582 See Newsholme, E.A., 269; 310
Coll, J.C. See La Barre, S., 465; 587 Craig, H. See Lupton, J.E., 191
Collette, B.B., 454, 518; 582 Crane, J., 437, 451; 583
Collier, R. See Edmond, J.M., 189 Crane, K. See Corliss, J.B., 184; 188
Collins, C.A., 143; 161 Cranston, R.E. See Emerson, S., 178; 189
See Mooers, C.N., 132, 143; 164 Crawford, R.J.M., 517; 583
Collins, M.B. See Hammond, T.M., 19; 51 Creese, R., 472, 473; 583
Comely, C.A., 294; 307 Creese, R.G., 434, 435, 469, 472, 527, 530;
Conant, F.S., 355; 389 583
Conklin, P.J. See Rao, K.R., 311 Crepon, M. See O’Brien, J.J., 165
Connel, A.D., 412; 426 Crepon, M.R., 29; 51
Connell, J.H., 430, 433, 437, 439, 449, Crerar, D.A., 169; 188
463, 465, 476, 477, 489, 523, 528, 530, Cresswell, G.R., 154, 155; 161
532, 533, 536, 537, 538, 539, 542, 553, Cripps, R.A., 264, 283; 307
559, 560, 565, 568, 575; 582, 583 Crisp, D.J., 439, 569; 583
Connor, E.F., 515; 583 See Flowerdew, M.W., 280; 308
Connor, M.S., 471; 583 See Patel, B., 394; 427
Conover, M.R., 509; 583 Croker, R.A., 502, 503; 583
Conover, R.J., 211; 260 Cronan, D.S., 178, 179, 182, 183, 184; 188
Conte, F.P. See Hand, S.C., 279; 309 See Bignell, R.D., 184; 187
Cook, P.A., 268; 307 See Moorby, S.A., 169; 192
See Gabbott, P.A., 268, 294; 305 See Shearme, S., 184; 193
Coombs, S.H. See Colebrook, J.M., 157; See Smith, P.A., 184, 185; 193
161 See Sozanski, A.G., 174; 193
Copland, D. See Sholkovitz, E.R., 175, 178; See Tooms, J.S., 171; 194
193 See Varnavas, S.P., 184; 194
Corcoran, E.F. See Alexander, J.E., 206; Cross, F.A. See Evans, D.W., 177; 189
205 See Wolfe, D.A., 178; 194
Cordes, E.H. See Mahler, H.R., 264, 268; Csanady, G.T., 28, 30, 127; 51, 161
310 Culkin, F. See Morris, R.J., 213; 261
Corey, S. See Amaratunga, T., 399, 409, Cullen, D. See Froelich, P.N., 189
410, 416, 423; 425 See McCaffrey, R.J., 192
See Pezzack, D.S., 395, 399; 427 Cullen, J.J., 130; 161
Corkett, C.J. See McLaren, I.A., 394, 414; See Lewis, M.R., 164
427 Cunnington, H.M., 327, 328; 340
AUTHOR INDEX 635
Curl, H.C. See Iverson, R.L., 136; 163 Deakin, M.A.B., 117, 118; 121
Curtis, A. See Woodley, J.D., 168 Dean, T.A., 542, 543; 583
Currie, R.I. See Swallow, J.C., 118, 142; Dean, W.E., 174, 175; 189
123, 167 See Gardner, J.V., 179; 189
Currie, R.W., 278; 307 See Moore, W.S., 175; 192
Cushing, D.H., 118, 127, 130, 157, 264; Debro, J.R., 253; 261
121, 161, 307 De Cock, A.W.A.M., 318, 319, 320, 335,
Cutshall, N.H. See Evans, D.W., 177; 189 336; 340
Cuzin-Roudy, J., 399, 419; 426 Defant, A., 23; 51
DeGraeve, G.M. See Reynolds, J.B., 410;
Daan, N., 517; 583 427
Dales, R.P., 287, 288, 289, 290, 294; 307 Deibel, D. See Paffenhofer, G.A., 155; 165
See Warren, L.M., 287; 313 de Jorge, F.B., 294; 307
See Wells, R.M.G., 288; 313 Dekker, R. See Bak, R.P.M., 465; 580
Dallmeyer, D.G. See Porter, J.W., 589 Delaney, J.R. See Jones, C.J., 184; 190
Dallmeyer, M. See Woodley, J.D., 168 Della Croce, J., 364; 389
Dallot, S., 351; 389 Demers, S., 130, 135; 161
Dalziel, J. See Bewers, J.M., 172; 187 Den Hartog, C., 316, 317; 340
Daniel, J.Y. See Samain, J.F., 278; 311 Denley, E.J., 478; 583
Daniel, R.J., 32; 51 See Underwood, A.J., 435, 472, 531;
Danielsson, L.-G., 185; 188 583
Danielsson, L.G., 206; 209 Denman, K.L., 125–168; 91, 114, 128,
Darnell, J.E., 278; 307 133, 134, 135, 137, 138, 139, 140, 152,
Darwin. C., 345, 349, 358, 386; 389 156, 160; 96, 121, 161
Darwin, J.H. See Glasby, G.P., 179, 180; See Freeland, H.J., 152, 153, 156; 162
190 See Gower, J.F.R., 91, 132; 96, 163
Dauby, P., 423; 426 See Herman, A.W., 76, 141, 143; 96,
Dauer, D.M., 493, 494, 568; 583 163
Dauphin, J.P. See Heath, G.R., 170; 190 See Platt, T., 77, 110, 128, 135, 160; 97,
Dauphin, P. See Froelich, P.N., 189 123, 166
Davey, E. See McCaffrey, R.J., 192 De Palma, J.R. See Schoener, A., 542; 590
David, M.M. See Gornall, A.G., 212; 261 Derenbach, J.B., 89; 96
David, P.M., 343, 363, 364, 370, 373; 389 de Szoeke, R.A., 132, 144; 162
Davies, A.M., 22, 23, 32; 51 Devol, A.H. See King, F.D., 102, 136; 122,
Davies, J.I. See Zaba, B.N., 294; 313 163
Davies, J.M. See Lee, R.F., 309 de Vooys, C.G.N., 290, 294; 307
Davis, C.C., 398; 426 de Zwaan, A., 270, 271, 272, 273, 274, 275,
Davis, R.E. See Chelton, D.B., 157; 161 276, 286, 287, 294; 307
Davison, W., 175; 188 See Ebberink, R.H.M., 269, 270, 274,
Day, R.W., 488, 533, 534; 583 275, 287; 307
Dayal, R. See Wilke, R.J., 178; 194
Davey, E. See McCaffrey, R.J., 192 See Livingstone, D.R., 274, 276; 310
Dayton, L.B. See Dayton, P.K., 533; 583 See Wijsman, T.C.M., 274; 313
Dayton, P.K., 442, 464, 484, 486, 488, See Zandee, D.I., 294; 313
489, 533, 534, 538, 544, 563, 568; 583 Dickie, L.M. See Klawe, W.L., 295; 309
See Mauzey, K.P., 442; 587 Dickinson, H.G., 339; 340
See Tegner, M.J., 442; 592 See Roberts, I.N., 339; 342
See Stead, A.D., 339; 342 See Brink, K.H., 161

Dickson, A.G. See Knox, S., 191 Duggins, D.O., 534, 545; 583
Dickson, F.W. See Bischoff, J.L., 183; 187 Duinker, J.C., 178; 189
Dickson, R.R. See Cushing, D.H., 130, 157; See Wollast, R., 178; 194
161 Dunbar, D.S. See Murthy, C.R., 29; 52
Dietrich, G., 409, 412; 426 Dunbar, M.J., 384, 385; 390
Diez, R.J. See Boesch, D.F., 493; 581 Duncan, C.J., 275; 307
Dill, L.M. See Giguère, L.A., 367; 390 Duncan, H. See Morse, D.E., 488; 588
Dillon, C.R., 318; 340 Dunstan, W.M. See Paffenhofer, G.A.,
Dillon, T.M., 133; 162 155; 165
Dimock, R.V., 443; 583 Durako, M.J. See Moffler, M.D., 320; 341
Dingle, H., 494, 530, 563; 583 Durbin, E.G., 89; 96
Dingle, J. See Caldwell, R.L., 436, 450, Durbin, P.A. See Mellor, G.L., 133; 164
530; 582 Dustan, P. See Richardson, C.A., 465, 532;
Dixon, W.J., 218; 261 589
Dodge, R.E., 195, 207, 208; 209 Duursma E.K., 61; 96
See Aller, R.C., 506; 580 Duval-Jouve, J., 318; 340
Doherty, P.J., 523, 524, 525, 541; 583 Dwyer, R.L., 160; 162
See Sale, P.F., 525; 590 Dybdahl, R. See Sale, P.F., 522, 523; 590
Dolbeare, F.A., 84; 96 Dyer, W.J. See Bligh, E.G., 212; 260
Doncaster, L., 351, 355; 390 Dymond, J., 183, 184, 185; 189
Donkin, P. See Moore, M.N., 310 See Corliss, J.B., 184; 188
See Widdows, J., 313 See Moore, W.S., 192
Dooley, H.D., 105; 121 Dyrssen, D. See Danielsson, L.-G., 185;
Dorsey, T.E., 212; 261 188
Dortch, Q. See Yentsch, C.M., 97
Doty, J.E. See Marsh, Jr, J.A., 196; 209 Eakin, R.M., 346, 354; 390
Douglas, D. See Harrison, W.G., 122 Eaton, A., 178; 189
Douglas, W.A. See Sale, P.F., 525; 590 Ebberink, R.H.M., 268, 269, 270, 273,
Doyle, D. See Schimke, R.T., 277; 312 275, 287; 306
Drinkwater, K. See Sutcliffe, W.H., 156; See Wijsman, T.C.M., 274; 313
167 See de Zwaan, A., 271; 307
Drinkwater, K.F. See Sutcliffe, W.H., 156; Ebeling, A.W., 518, 527, 528; 583
167 Ebersole, J.P., 520, 521, 563; 583
Driscoll, E.G., 507; 583 See Ogden, J.C., 524; 588
Droop, M.R., 105, 116; 121 Ebert, T.A., 436, 442, 471; 583
Drummond, G.I., 268; 307 Ebling, F.J., 536; 583
Dubinsky, Z. See Falkowski, P.G., 468; See Kitching, J.A., 533; 586
584 Eckman, J.E., 507; 583
Dubois, D.M., 111, 112, 151; 121, 162 Edden, A.C. See Cartwright, D.E., 24; 51
Dubois, M., 327; 340 Edelsten, D.J. See Simpson, J.H., 166
Duchart, P., 173; 189 Edmond, J.M., 183, 184, 185; 189
Ducker, S.C., 330, 332, 333, 335; 340 See Corliss, J.B., 188
See McConchie, C.A., 331; 341 Edwards, A. See Simpson, J.H., 123, 166
See Pettitt, J.M., 330, 332; 341 See Tett, P., 99–123
Ducret, F., 346, 354; 390 Edwards, D.C., 445, 446; 583
Dugdale, R.C., 102, 103, 104, 105, 108; Ehrlich, A.H. See Anderson, G.s.V., 580
121
AUTHOR INDEX 637
Ehrlich, P.R. See Anderson, G.s.V., 580 Evans, S.V. See Widdows, J., 313
Eisler, R., 264, 298; 307 Ewing, M. See Addy, S.K., 173; 186
Eisma, D. See Sholkovitz, E.R., 178; 193 Ewing, R.M. See Dauer, D.M., 494; 583
Ekman, S., 401, 412; 426
Ekman, V.M., 133; 162 Fage, L., 401; 426
El-Bastavizi, A.M., 213; 261 Fager, E.W., 131; 162
Elderfield, H., 173, 178, 179, 181, 183, Falkowski, P. See Harrison, W.G., 122
185; 189 Falkowski, P.G., 135, 468; 162, 584
Eleftheriou, A. See Pearson, T.H., 264; 311 See Malone, T.C., 164
Elgershuizen, J.H. B.W. See Vlasblom, Falk-Petersen, S., 294; 308
A.G., 399, 400, 405; 428 Fall, L. See Atkinson, D.E., 272; 305
Eliassen, J.-E., 239; 261 See Klungsøyr, L., 272; 309
Ellington, W.R., 288; 308 See Shen, L.C., 273; 312
Elliot, M.N. See Seed, R., 527; 591 Faller, A.J., 137; 162
Ellis, A.J., 183; 189 Faller-Fritsch, R.J. See Emson, R.H., 436,
Elner, R.W., 553, 554; 583 437; 584
El-Sayed, S.Z. See Hovis, W.A., 96 Farnham, W.F., 566, 567; 584
Elsberry, R. See O’Brien, J.J., 165 Farr, A.L. See Lowry, O.H., 212; 261
Elton, C.S., 567; 584 Farrington, J.W. See Goldberg, E.D., 308
Emerson, S., 178; 189 Fasham, M.J.R., 106, 113, 114, 128, 136;
See Jacobs, L., 176, 178; 190 121, 162
Emerson, S.E., 486, 568; 584 Fava, G. See Battaglia, B., 571; 581
Emery, K.O., 131; 162 Fearnhead, P.G., 146; 162
Emson, R.H., 436, 437; 584 Feigenbaum, D. See Bushing, M., 363,
Enfield, D.B., 157; 162 377, 379, 381, 382, 383, 387; 389
Engel, M.S. See Bak, R.P.M., 532; 580 Feigenbaum, D.L., 343–392; 343, 346, 347,
Engström, L., 270; 308 348, 349, 354, 355, 357, 358, 359, 360,
Eppley, R.W., 136, 141; 162 361, 363, 364, 365, 366, 367, 368, 369,
See Cullen, J.J., 130; 161 370, 371, 373, 374, 375, 377, 378, 379,
See Smith, R.C., 132; 167 380, 381, 382, 383, 387, 388, Fig. 13
Erhlich, P.R. See Anderson, G.s.V., 580 (Feigenbaum & Maris) between pp. 358
Esaias, W.E., 55, 76; 96 and 359; 390
Esaias, W.E. See Bowman, M.J., 108, 118, Felbeck, H., 184, 287; 189, 308
137, 142, 147, 153; 121, 161 Fenchel, T., 496, 497, 498, 499, 500, 501,
See Campbell, J.W., 80; 96 505, 527, 529, 530, 531, 559, 560, 570,
See Owens, O.V.H., 127; 165 575; 584
See Pingree, R.D., 153; 165 Fenchel, T.M., 502; 584
See Walsh, J.J., 168 Ferguson, A., 281; 308
Estes, J.A., 489, 534; 584 See Murdock, E.A., 280; 310
Estrada, M. See Margalef, R., 108; 122 Ferlin-Lubini, V., 456; 584
Evans, D.W., 177, 178; 189 Février, M. See Hekinian, R., 183, 184; 190
Evans, E.C., 206; 209 Fielding, A.H. See Russell, G., 487; 590
Evans, F. See Sheader, M., 358; 392 Fields, J. See Hochachka, P.W., 287; 309
Evans, G.T., 134, 136, 138; 162 Fields, J.H.A. See Guderley, H.E., 271; 308
Evans, K.E. See Dingle, H., 494; 583 Finkel, R.C. See Berger, W.H., 179; 187
Evans, R.H. See Brown, O.B., 156; 161 Finlayson, D.M. See Barnes, H., 286, 294;
Evans, S., 490; 584 305, 306
Evans, S.M., 494; 584
Fishelson, L., 196, 438, 442, 538; 209, 584 Fricke, S. See Fricke, H., 438; 584
Fisher, D.E. See Bonatti, E., 179; 187 Friedman, G.M., 196; 209
Fisher, K. See Black, R., 434; 581 See Amiel, A.J., 196, 200, 202, 203,
Fix, G.J., 21; 51 204, 205; 208
Flagg, C.N. See Beardsley, R.C., 142; 160 Fried-Montaufier, M.C. See Cuzin-Roudy,
See Mooers, C.N., 142; 164 J., 399, 419; 426
Flather, R.A., 23; 51 Friedrichsen, H. See Barrett, T.J., 184; 186
See Davies, A.M., 22; 51 Frier, J.O., 505, 529, 530, 559, 560, 575;
Fleer, A.P. See Brewer, P.G., 172; 188 584
Fleet, A.J., 185; 189 Frier, J.-O. See Fenchel, T., 501, 529; 584
Fletcher, E.A. See Robertson, D.R., 564; Fritsch, H.A.R., 268; 308
590 Froelich, P. See McCaffrey, R.J., 192
Fletcher, R.L., 487, 563; 584 Froelich, P.N., 170, 171, 173; 189
Flick, R.E. See Inman, D.L., 152; 163 Fujita, Y. See Terazaki, M., 369; 392
Flint, R.W., 495; 584 Fujiyoshi, R. See Kitano, Y., 178; 190
Flowerdew, M.W., 280; 305 Fuller, S.L.H. See Hart, C.W., 265; 309
Folch, J., 212, 213, 214, 215, 216, 219, Furnestin, M.-L., 358, 369; 390
221, 223, 224, 225, 229, 230, 232, 234, Fürst, M., 399, 410; 426
235, 236, 239, 245, 246, 247, 250, 252, Fyfe, W.S., 183; 189
253, 257, 258, 259; 261
Folkard, A.R. See Jones, P.G., 17; 52 Gaardner, T., 100; 121
Fonselius, S.H., 206; 209 Gabbott, P.A., 264, 268, 294; 308
Forbes, E.A., 169; 189 See Bayne, B.L., 303; 306
Ford, E.B., 281; 305 See Cook, P.A., 268; 307
Ford, G. See Georghiou, L., 196; 209 See Gade, G., 274; 308
Foret, J.P. See Bellan, G., 303; 306 See Zaba, B.N., 294; 313
Forster, G.R. See Pingree, R.D., 103, 146; Gade, G., 274; 308
122, 165 Gagnon, P.S., 318; 340
Förstner, U., 180; 189 Gaimard, P. See Quoy, J., 349, 354; 391
Foster, J.B. See Breen, P.A., 534; 582 Gaines, M.S., 280; 308
Foster, M.S., 486, 533; 584 Gaines, S.D., 487; 584
Fostie, W.G. See Seliger, H.H., 75; 97 See Lubchenco, J., 487, 489, 534, 535;
Fotheringham, N., 508, 509; 584 587
Fournier, R.O., 143, 155; 162 Gallegos, C.L., 135; 162
Fox, F.R. See Rao, K.R., 311 See Platt, T., 135; 166
Fox, J.F., 539; 584 Gamble, E. See Goldberg, E.D., 308
Francis, L., 443, 465; 584 Gammelsrod, T. See O’Brien, J.J., 165
Frank, P.W., 434; 584 Gardner, J.V., 179; 189
Frankel, S.L. See Olson, R.J., 83; 97 Gardner, W.S. See Lee, R.F., 278; 310
Fraser, J.H., 347, 388; 390 Gargett, A.E. See Denman, K.L., 134, 135,
Freed, J.M., 270, 273; 305 138; 161
Freeland, H.J., 152, 153, 156; 162 Garlick, R.L., 287; 308
See Denman, K.L., 162 Garrett, C., 129, 138, 143, 146, 155; 162
Freeman, H.C. See Lee, R.F., 309 See Loder, J.W., 157; 164
Frenkeil, L. See Ansell, A.D., 294; 305 Garrett, C.J.R. See Young, W.R., 152; 168
Gartner, S. See Boström, K., 179; 187
Fricke, H., 438; 584 Garvine, R.W., 148; 162
AUTHOR INDEX 639
See Stevenson, M.R., 144; 167 Goldberg, E.D., 117, 179, 181, 264; 121,
Garwood, R.W., 133; 162 190, 308
Gatien, M.G., 142; 162 Goldhaber, M.B. See Rhoads, D.C., 506;
Gaudette, H.E. See Lyons, W.B., 177, 178; 589
191 Goldhammer, A.R., 269; 305
Gaudy, R., 395, 398, 407, 418, 419; 426 Golding, T.J. See Cresswell, G.R., 154,
Gavis, J. See Pasciak, W.J., 159; 165 155; 161
Gee, J.M. See Joint, I.R., 505; 586 Goldman, J.C., 116, 159; 121, 163
Gegenbaur, C., 348; 390 See McCarthy, J.J., 159; 164
Geiger, S.R., 410; 426 Gonor, J.J. See Barnes, J.R., 488; 581
Gendron, R., 445, 446; 584 Gooch, J.L., 568, 569; 584
Gentile, J.H., 398, 406, 412; 426 See Snyder, T.P., 280; 312
See Gentile, S.M., 412; 426 Goodbody, I., 412; 426
Gentile, S.M., 412 426 Goodley, E.F.W. See Barnes, H., 32; 51
See Gentile, J.H., 398, 406, 412; 426 Gordeev, V.V. See Bolger, G.W., 184; 187
Georghiou, L., 196; 209 Gordon, D.C. See Sutcliffe, W.H., 137; 167
Germain, L., 369; 390 Gordon, D.P., 477, 480; 585
Ghirardelli, E., 343, 346, 349, 350, 354, Gordon, H.R., 71, 82; 96
356; 390 See Hovis, W.A., 96
Ghosh, S.K. See Dean, W.E., 174, 175; 189 Gordon, L.I. See Corliss, J.B., 188
Giam, C.S., 264, 265; 308 See Edmond, J.M., 189
Gibbs, R.J., 178; 189 Goreau, N.I. See Goreau, T.F., 198; 209
Gibson, R.N., 518, 519; 584 Goreau, T. .F, 198, 542; 209, 585
Giese, A.C., 239, 293, 294; 261, 308 Goreau, T.J., 196, 198, 200, 202, 203, 204,
Giesel, T.S., (Dr. Seuss), 432; 584 205; 209
Gieskes, J.M., 173, 174; 189 Gornall, A.G., 212, 213, 214, 215, 219,
See Burdige, D.J., 173; 188 230, 236, 245, 246, 250, 251, 252, 253,
Giguère, L.A., 367; 390 258; 261
Giles, I.G. See Munday, K.A., 271; 310 Gornitz, V. See Bender, M.L., 187
See Poat, P.C., 271; 311 Gosling, E.M., 280; 308
Gill, A.E., 127; 162 Goss-Custard, J.D., 439, 450; 585
See Swallow, J.C., 118, 142; 123, 167 Gould, E., 302; 308
Gilles, K.N. See Dubois, M., 340 Gould, W.J., 19; 51
Giovando, L.F. See Tully, J.P., 133; 167 Gower, J.F.R., 91, 132; 96, 163
Gladfelter, W.B., 522; 584 See Borstad, G.A., 161
Glasby, G.P., 163–194; 169, 171, 172, Grabe, S.A., 410; 426
179, 180, 181, 182; 189, 190 Graham, D.W. See Klinnhammer, G.P.,
See Cronan, D.S., 188 173; 191
See Meylan, M.A., 180, 183; 192 Graham, W.F., 178; 190
Gleeson, P.A. See Clarke, A.E., 339; 340 Gran, H.H., 100, 135; 121, 163
Glynn, P.W., 534, 535, 536, 538; 584 See Gaardner, T., 100; 121
Goddard, J. See Bacon, M.P., 186 Granéli, A. See Danielsson, L.-G., 185; 188
Godfrey, J.S. See Hamon, B.V., 155; 163 Grant, B. See Edmond, J.M., 189
Goering, J.J. See Dugdale, R.C., 102, 103, Grant, P.R., 458, 530, 538; 585
104, 105, 108; 121 Grant, W.C., 508, 509, 510; 585
See Iverson, R.L., 143; 163 Grant, W.S., 487; 585
Gogate, S.S. See Sreekumaran, C., 200, See Phillips, R.C., 342
202; 210
Grassi, B., 343, 346, 354, 356, 357, 386; See Marchig, V., 170, 182, 183, 185;
390 191
Grassle, J.F., 280, 283, 293, 493, 568; 308, Gunnlaugsson, E. See Elderfield, H., 183;
585 189
See Grassle, J.P., 296; 308
Grassle, J.P ., 296; 308 Hacker, P.W. See Boicourt, W.C., 142; 161
See Grassle, J.F., 280, 283, 293, 493, Hagan, D. See Spero, H., 356; 392
568; 308, 585 Hageman, J.H. See Klungsøyr L., 272; 309
Gray, J.S., 263, 301, 493, 501, 506; 308, Hairston, N.G., 560; 585
585 See Gentile, J.H., 398, 406, 412; 426
See Pearson, T.H., 301; 311 Hakala, I., 399, 423; 426
Green, G., 479, 564; 585 Hale, S.M. See Van Kley, H., 258, 259;
Green, J.M., 398; 426 261
Green, K. See Corliss, J.B., 188 Haley, S.R., 446, 448; 585
Greenberg, D.A. See Garrett, C., 146; 162 Hall, C. See Zeeman, E.C., 123
Gregg, M., 138; 163 Hall, D.J. See Werner, E.E., 527, 554, 555;
Greig, M.A. See Hamon, B.V., 155; 163 592
Grey, B.B., 345, 355, 358, 370, 373; 390 Hall, E.R., 270; 308
Grey, W.F., 320; 340 Halliwell, A.R., 32, 43; 51
See Moffler, M.D., 320; 341 Halliwell, G.R., 154; 163
Grieshaber, M., 274; 308 Halpern, D., 19, 20, 144; 51, 163
Grieshaber, M.K. See Felbeck, H., 287; See Jones, B.H., 151; 163
308 Hamaker, T.L. See Nimmo, D.R., 393,
Griffiths, C., 453, 553; 585 405; 427
Griffiths, C.L. See Velimirov, B., 487; 592 Hamilton, J.K. See Dubois, M., 340
Griffiths, D.K. See Pingree, R.D., 23, 24, Hamming, R.W., 112; 121
27, 44, 103, 146; 53, 122, 165 Hammond, D. See Froelich, P.N., 189
Grigg, R.W., 538; 585 Hammond, G.L., 278; 309
Grill, E.V., 178, 183; 190 Hammond, T.M., 19; 51
Grimaud, D. See Michard, G., 173; 192 Hamner, W.M., 438; 585
Groen, A.K., 266, 267; 308 Hamon, B.V., 155; 163
Groenendaal, M., 288, 290; 308 Hand, S.C., 279; 309
Gronvik, S. See Hopkins, C.C.E., 261 Hannan, P.J., 199; 209
Grosberg, R.K., 531; 585 Hansen, S.W.F., 212; 261
Gross, M.G., 126; 163 Harden-Jones, F.R., 32; 51
Grünbaum, H., 436, 442, 471, 473, 534, Hardy, A.C., 113, 128; 121, 163
563; 585 Harger, J.R.E., 431, 477, 529, 531, 560,
Grundmanis, V. See Murray, J.W., 173; 563; 585
192 Hargraves. B. See Parsons, T.R., 125, 135;
Guderley, H.E., 271, 282; 308 165
Guérin, J.-P., 277; 308 Hargreaves, N.B. See Fournier, R.O., 143;
Guerin, J.P. See Gaudy, R., 395, 398, 407, 162
419; 426 Hariya, Yu, 183; 190
Guillard, R.R.L. See Hulburt, E.M., 129; Harlin, M.M. See Cobb. J.S., 127; 161
163 Harris, B.G. See Hofer, H.W., 269; 309
See Waterbury, J.B., 68; 97 Harris, G.P., 126, 127, 130, 135; 163
Gundlach, H., 173, 185; 190 Harrison, P.J. See Chan, A.T., 487; 582
AUTHOR INDEX 641
See Turpin, D.H., 128; 168 Head, R.N. See Pingree, R.D., 146; 165
See Zeeman, E.C., 123 Heaps, N.S., 22, 23, 28, 30, 32, 43, 44, 46,
Harrison, S. See Clarke, A.E., 339; 340 49; 52
See Knox, R.B., 340 See Flather, R.A., 23; 51
Harrison, W.G., 102, 116, 159; 122, 163 Heard, V.E.J. See McLusky, D.S., 405; 427
See Eppley, R.W., 136; 162 Heath, G.R., 170; 190
Harriss, R.C., 195, 196, 200, 201, 202, See Bischoff, J.L., 180; 187
204; 209 See Froelich, P.N., 189
Hart, C.W., 265; 309 Heath, J.R., 294; 309
Hart, R.A., 183; 190 Heaton, M.J. See Tipping, E., 176; 194
Hart, S.R. See Staudigel, H., 183; 193 Heburn, G.W. See Brink, K.H., 161
Hartman, B. See Froelich, P.N., 189 Heck, K.L. See Coen, L.D., 494, 530, 562;
Hartman, W.D., 476; 585 582
See Goreau, T.F., 542; 585 Hedgecock, D. See Nelson, K., 280, 293;
Hartmann, M., 173, 176; 190 310
Hartnoll, R.G. See Hawkins, S.J., 469, 487, See Tracy, N.L., 312
488, 537, 541, 567; 585 Heggie, D.T. See Klinnhammer, G.P., 173;
Harvey, G. See Goldberg, E.D., 308 191
Harvey, G.R. See Carpenter, E.J., 389 Heitz, J.R. See Chambers, J.E., 307
See Sunda, W.G., 173; 193 Hekinian, R., 183, 184; 190
Harvey, H.W., 102; 122 Helfman, G.S., 446, 454, 518, 525, 528;
Harvey, J.G., 32; 51 585
Harvey, P.H., 439; 585 Hellerman, S., 43; 52
Harwood, J.P. See Drummond, G.I., 268; Heltshe, J.F. See Gentile, S.M., 412; 426
307 Henderson, E.W. See Steele, J.H., 105; 123
Haskin, L. See Schofield, A., 200; 210 Helz, G.R. See Sigleo, A.C., 178; 193
Hastings, J.W., 77; 96 Hempel, G., 118; 122
Hatch, E.R. See Grabe, S.A., 410; 426 Henry, J.-P., 396, 400; 426
Hatfield, E.B. See Croker, R.A., 503; 583 Herman, A.W., 76, 141, 143; 96; 163
Hathaway, J.A. See Ramaiah, A., 272; 311 See Denman, K.L., 137, 139, 140; 162
Haugen, E. See Yentsch, C.M., 97 Hermannsen, A. See Hopkins, C.C.E., 211–
Haugsness, J.A. See Osman, R.W., 546; 261
588 Hers, H.-G. See Van Schaftingen, E., 269;
Haury, L.R., 91, 140, 141; 96, 163 312
Haven, S.B., 469; 585 Hershberger, W.K. See Buroker, N.E., 280;
Havlena, F.K. See Borodich, N.D., 407, 306
411; 425 Hertwig, O., 343, 346, 349, 350, 351, 354,
Hawkins, S.J., 469, 487, 488, 537, 541, 356; 390
567; 585 Herzenberg, L.A. See Bonner, W.A., 87; 96
Hay, M.E., 489, 533; 585 Heslop-Harrison, J., 316, 332, 339, 340;
Hayes, W.B. See Carpenter, R.H., 174; 188 340, 341
Haymon, R. See Lupton, J.E., 191 Heslop-Harrison, Y., 339, 340; 341
Haymon, R.M., 184; 190 See Heslop-Harrison, J., 339; 341
Hayward, P.J. See Harvey, P.H., 439; 585 Hess, J., 178; 190
Hazel, J., 277; 309 Hessler, P.R. See Dayton, P.K., 533; 583
Hazlett, B. See Bach, C., 508; 580 Hesterberg, L.K., 269; 309
Hazlett, B.A., 436, 452, 508, 509, 511; 585 Hetherington, J.A., 11; 52
Head, E.J H. See Gabbott, P.A., 294; 308 Heubach, W., 412; 426
Heydorn, A.E.F., 386, 388; 390 Holley, M.C. See Brown, B.E., 196, 200,
Heye, D., 182; 190 203, 204; 209
Hickey, B.M., 156; 163 Holliday, L.M., 178; 190
Hickman, P.E. See Weidemann, M.J., 269; Holligan, P.M. See Fasham, M.J.R., 136;
313 162
Highsmith, R.C., 442; 585 See Pingree, R.D., 103, 146, 147; 122,
See Dingle, H., 494; 583 165
Hildemann, W.H., 465; 585 Holme, N.A. See Wilson, J.B., 442; 593
Hill, A. See Black, R., 434; 581 Holm-Hansen, O. See Eppley, R.W., 141;
Hill, H.W., 35; 52 162
See Ramster, J.W., 34, 35; 53 Holt, S.J. See May, R.M., 587
Hill, S.H. See Denman, K.L., 162 Holwerda, D.A. See Zandee, D.I., 294; 313
Hillebrand, M.T.J. See Duinker, J.C., 178; Holyer, R.J. See Gower, J.F.R., 91, 132; 96,
189 163
Hines, A.H., 472; 585 Honnorez, J., 184; 190
Hirai, E. See Katô, M., 444, 465; 586 Hooker, N. See Morse, D.E., 488; 588
Hirata, S., 178; 190 Hopkins, C.C.E., 211–261; 213; 261
Hiroki, K. See Theede, H., 288; 312 See Seiring, J.V., 212; 261
Hirst, J.M., 178; 190 Hopkins, T.L., 411; 426
Hixon, M.A., 519, 523, 528, 530, 563, 568; Hopkins, T.S. See Malone, T.C., 164
585 Horan, P.K., 82; 96
Hoagland, K.E., 548; 585 See Yentsch, C.M., 97, 98
Hoar, W.S., 258; 261 Horn, M.K., 181; 190
Hobson, E.S., 454, 545; 586 Horne, E.P., 143, 154; 163
Hochachka, P.W., 274, 277, 282, 287, 402; See Garrett, C., 143; 162
309, 426 See Lewis, M.R., 164
See Guderley, H.E., 271; 305 Horne, R.A., 175; 190
See Moon, T.W., 277; 310 Horridge, G.A., 346, 347, 348, 349, 354,
See Storey, K.B., 270, 274; 312 356, 367; 390
Hockey, P.A.R. 455; 586 See Bullock, T.H., 352, 353, 354, 357;
Hodge, D., 412; 426 389
Horwood, J.W., 23, 44; 52
Hodgson, L.M., 486, 568; 586 Hoshiai, T., 477, 568; 586
Hoese, H.D., 520, 523; 586 Hoshika, A., 178; 190
Hofer, H.W., 269; 309 See Shiozawa, T., 178; 193
Hoffman, R.J. See Nicklas, N.L., 280; 311 Hovis, W.A., 81; 96
Hoffman, S.G. See Robertson, D.R., 523; See Gordon, H.R., 71; 96
589 Howard, L.S., 195–210
Hoffman, K.-H., 271, 275; 309 Howarth, M.J., 11–53; 20, 36, 44; 52
Hofmeister, W., 335; 341 See Alcock, G.A., 36; 51
Hohnke, L., 294; 309 Howe, S.O., 105, 118; 122
Hohnke, L.A., 295; 309 See Walsh, J.J., 168
Højerslev, N.K., 62; 96 Howland, R.J.M. See Morris, A.W., 176,
Holdren, G.R., 173; 190 178; 192
Holdich, D.M., 396; 426 Hruby, T., 486, 568; 586
Holland, D.L. See Bayne, B.L., 303; 306 Hsieh, W.W. See Mysak, L.A., 157; 165
Holland, H.D. See Mottl, M.J., 183; 192 Hsueh, Y., 152; 163
Hu, V.J.H., 198; 209
AUTHOR INDEX 643
Hubbard, J.A.E.B., 203; 209 Immerman, F.W. See Koehn, R.K., 280,
See Swart, P.K., 202; 210 281, 282; 309
Hubberten, H.-W. See Honnorez, J., 190 Ingram, R.G., 142, 148; 163
Hudson, A. See Edmond, J.M., 189 See Legendre, L., 135; 164
Hudson, J.H., 195, 207, 208; 209 Ingri, J. See Boström, K., 176; 187
See Shinn, E.A., 207; 210 Inman, D.L., 152; 163
Hue, L. See Van Schaftingen, E., 269; 312 Irvine, R. See Murray, J., 173; 192
Huff, L.C. See Beardsley, R.C., 51 Isaacs, J.D., See Soutar, A., 131; 167
Hughes, D.G. See Simpson, J.H., 103, 146; Ishikawa, M, 395, 399, 407; 426
123 167 Ishikawa, T., 268, 270; 309
Hughes, D.J. See Sharp, J.H., 487; 591 Ivanovici, A. See Lee, R.F., 309
Hughes, G.M., 265; 309 Ivanovici, A.M., 264, 273; 309
Hughes, M.J. See Chester, R., 180; 188
Hughes, R.N., 548, 549; 586 Iverson, R.L., 136, 137, 143; 163
See Elner, R.W., 553, 554; 583 See Bowman, M.J., 148; 161
Huguet, D., 354, 356; 390 Ivester, M.A., 501; 586
Hui, E. See Moyse, J., 439; 588 Ivlev, V.S., 367; 390
Hulburt, E.M., 129, 159; 163 Iwayama, Y. See Ishikawa, T., 268; 309
Hulett, K.R. See Bonner, W.A., 87; 96
Hull, C.J. See Hildemann, W.H., 585 Jack, W. See McKinley, I.G., 33; 52
Hunt, C.D., 172; 190 Jackson, G.A., 116, 159; 122, 163
Hunt, G.J., 11, 33; 52 Jackson, J. See Woodley, J.D., 168
Hunt, J.L. See Glasby, G.P., 179, 180; 190 Jackson, J.B.C., 431, 477, 479, 482, 487,
Hunter, J.R., 23, 44; 52 530, 532, 542, 562, 564; 586
See Simpson, J.H., 103, 108, 146; 123 See Buss, L.A., 532; 582
167 See Woodin, S.A., 490, 506, 532; 593
Huntsman, S.A., 136, 151; 163 Jacobs, L., 176, 178; 190
See Sunda, W.G., 173; 193 See Emerson, S., 189
See Walsh, J.J., 168 Jacobs, R.P.W.M., 317, 318, 319; 341
Hurd, L.E. See Dean, T.A., 542, 543; 583 Jakobsen, T., 378; 390
Huston, M., 539; 586 Jamart, B.M., 105; 122
Hutchings, P.A., 295; 309 James, I.D., 105, 146; 122, 163
Hutchinson, A. See Peterson, W.T., 144; Jangaard, P.M., 212, 224, 235; 261
165 Jannasch, H.W., 184; 190
Hutchinson, G.E., 107, 108, 119, 429, 454, See Karl, D.M., 184; 190
501, 512, 531, 559; 122, 586 Jassby, A.D. See Platt, T., 135, 160; 166
Huthnance, J.M., 30, 31; 52 Jefferies, D.F., 33; 52
Huyer, A., 156; 163 See Hetherington, J.A., 11; 52
Hyatt, G., 437, 451; 586 See Kautsky, H., 12, 33; 52
Hyatt, G.W., 450; 586 Jeffries, H.P., 494; 586
Hylleberg, J., 496, 498, 547; 586 Jehanno, C. See Lalou, C., 183; 191
Hyman, L.H., 343, 350, 351, 354, 358, Jenkins, G.M., 113; 122
364; 390 Jennings, C.D. See Wolfe, D.A., 178; 194
Jensen, K., 509; 586
Iacono, I.J. See Campbell, L. 83; 96 Jensen, K.R., 553; 586
Ichimura, S. See Shimura, S., 59, 60; 97 Jensen, L. See Morse, D.E., 488; 588
Imbrie, J. See Turekian, K.K., 179; 194 Jepsen, J., 398; 426
Jerlov, N.G., 61, 62; 96 Kakinuma, Y. See Katô, M., 444, 465; 586
Jermy, A.C. See Pettitt. J.M., 329, 332; 341 Kalhorn, S. See Emerson, S., 189
Jermyn, M.A., 327; 341 Kalle, K., 61; 96
Jernakoff, P. See Underwood, A.J., 469; See Dietrich, G., 409, 412; 426
592 Kamenkovich, V.M. See Monin, A.S., 128;
Joensuu, O. See Bonatti, E., 179; 187 164
Johannes, R.E., 195; 209 Kamykowski, D., 129, 140, 141; 163
Johannessen, P.J. See Pearson, T.H., 301; Kanamori, N. See Kitano, Y., 203; 209
311 Kanneworf, E. See Nicolaisen, W., 503;
John, C.C., 343, 345, 348, 350, 351, 354, 588
356, 357, 358, 359, 361, 364, 366; 390 Kaplan, I.R. See Baas-Becking, L.G.M.,
John, D.M., 489; 586 170; 186
Johns, B., 22; 52 See Presley, B.J., 173; 192
Johns, D.M., 406; 426 Karato, S. See Honnorez, J., 190
Johnson, D.R., 150; 163 Kariya, T. See Matsudaira, C., 398; 427
Johnson, H.P. See Jones, C.J., 184; 190 Karl, D.M., 184; 190
Johnson, J.A., 144; 163 Karlson, R., 477, 480, 533; 586
Johnson, K.S., 170; 190 Karlson, R.H., 480; 586
Johnson, M.S. See Black, R., 442; 581 See Sutherland, J.P., 534, 542; 592
Johnson, R.K. See Stephens, J.S., 523; 591 Kasten, F.H., 66; 96
Johnson, R.M. See Gray, J.S., 501; 585 Kastner, M. See Haymon, R.M., 184; 190
Johnson, W.R. See Johnson, D.R., 150; 163 Katô, M., 444, 465; 586
Johnson, W.S. See Gladfelter, W.B., 522; Kaufman, L. See Woodley, J.D., 168
584 Kaushik, W.K. See Brinkhurst, R.O., 545;
Johnston, J.H. See Meylan, M.A., 183; 192 582
Joiner, B.L. See Ryan, T.A., 218; 261 Kausik, S.B., 327, 328; 341
Joint, I.R., 505; 586 Kautsky, H., 12, 33; 52
Jones, B.H., 151; 163 Kay, R. See Bender, M.L., 187
See Brink, K.H., 161 See Bonatti, E., 185; 187
Jones, C.J., 184; 190 Kayser, H., 199, 487; 209, 586
Jones, J.E. See Heaps, N.S., 44, 46; 52 Kazakov, V.K. See Plisetskaya, E., 268;
See Howarth, M.J., 20; 52 311
Jones, K. See Simpson, J.H., 123 Keddy, C.J., 318; 341
Jones, K.J., 118; 122 Keeley, J.R. See Garrett, C., 146; 162
Jones, N.S., 489, 534; 586 Keene, D.F. See Pearcy, W.G., 144; 165
Jones, P.G., 17; 52 Keferstein, W., 354; 390
Jones, S.C. See Honnorez, J., 190 Kelley, J.C. See Walsh, J.J., 168
Joubin, L. See Germain, L., 369; 390 Kellogg, D.E., 529, 530; 586
Joyce, T.M., 159; 163 Kellogg, L.W., 508; 586
Juday, C., 418; 426 Kelly, M.G. See Tett, P.B., 75; 97
Jumars, P.A. See Eckman, J.E., 507; 583 Kendziorek, M. See Anderson, D.J., 448;
Jung, G.N. See Bernstein, B.B., 480, 481, 580
527; 581 Kent, B.W., 463, 464, 562, 563; 586
Jupp, B. See Woodley, J.D., 168 Keough, M.H., 534; 586
Kerambrun, P. See Guérin, J.-P., 277; 308
Kaeini, M.R. See Hofer, H.W., 269; 309 Kerr, S.R., 77; 96
Kain, J.M. See Jones, N.S., 489, 534; 586 Keser, M. See Larson, B.R., 553; 587
Key, G.S. See Stephens, J.S., 523; 591
AUTHOR INDEX 645
Khamala, C.P.M., 442; 586 Knight, A.W. See Baldo-Kost, A.L., 409;
Khan, M.A., 32, 36; 52 425
Khfaji, A.K., 487; 586 See Siegfried, C.A., 407; 427
Kidd, R.B., 183; 190 Knight-Jones, E.W., 439, 440, 547; 586
Kiefer, D.A., 66; 96 See Al-Ogily, S.M., 478, 487, 504; 580
Kielhorn, W., 388; 390 Knight-Jones, P. See Knight-Jones, E.W.,
Kierstead, H., 109, 110, 114, 152; 122, 163 547; 586
Kilham, P., 119, 129; 122, 163 Knowlton, N. See Woodley, J.D., 168
See Tilman, D., 128; 167 Knox, R.B., 339; 341
Kilham, S.S. See Kilham, P., 119, 129; 122, See Clarke, A.E., 339, 340; 340
163 See Ducker, S.C., 330, 335; 340
See Tilman, D., 128; 167 See Heslop-Harrison, J., 339; 341
Killingley, J.S. See Berger, W.H., 179; 187 See McConchie, C.A., 331; 341
Kimura, M., 281; 309 See Pettitt, J.M., 330, 332; 341
Kinder, T.H., 142; 163 Knox, S., 178; 191
See Schumacher, J.D., 142; 166 Knudsen, M., 32; 52
King, D.P.F., 517; 586 Kobayashi, J. See Teraoka, H., 178; 194
King, F.D., 102, 136; 122, 163 Koehl, M. See Woodley, J.D., 168
King, K.R., 384; 390 Koehl, M.A.R., 159, 160; 164
Kinne, O., 395, 396, 399, 402, 407, 419; Koehn, R.K., 280, 281, 282; 309
426 Kofoed, L.H. See Fenchel, T., 496, 499,
Kinzie, R.A., 528, 530, 567; 586 500; 584
Kirby, R. See Smith, T.J., 11; 53 Kohda, T., 519; 586
See Williams, S.J., 13; 53 Köhler, G., 268; 309
Kirk, B.L. See Rust, B.W., 157; 166 Kohn, A.J., 453, 454, 460, 461, 462, 474,
See Van Winkle, W., 156; 168 527, 530, 551, 559, 575; 586, 587
Kirk, C.R. See Freed, J.M., 270, 273; 308 See Leviten, P.J., 444, 446, 461, 463,
Kitano, Y., 178, 203; 190, 209 538; 587
See Sakata, M., 178; 193 Kolbuch-Braddon, M.E. See Weidemann,
Kitching, J.A., 533; 586 M.J., 269; 313
See Ebling, F.J., 536; 583 Kolding, S. See Fenchel, T., 501, 529; 584
Klawe, W.L., 295; 309 See Fenchel, T.M., 502; 584
Klepal, W. See Barnes, H., 567; 581 Kolla, V. See Bonatti, E., 183; 187
Klinkhammer, G.P., 170, 172, 173, 178, Kono, N., 269; 309
183, 184; 191 Kopache, M.E. See Siegfried, C.A., 407;
See Bender, M.L., 172, 177, 183; 187 427
See Froelich, P.N., 189 Korner, A. See Debro, J.R., 253; 261
See Graham, W.F., 178; 190 Kort, V.G. See Monin, A.S., 128; 164
See Lupton, J.E., 191 Kotori, M., 354, 385, 387; 390
Klise, D.H. See Gardner, J.V., 179; 189 Kowalevsky, A., 354; 390
Klungsøyr, L., 272, 273; 309 Kowalik, Z. See Ramming, H.G., 21; 53
Kluytmans, J.H., 294; 309 Kraemer, T. See Bonatti, E., 182; 187
See Zandee, D.I., 294; 313 See Boström, K., 179; 187
See Zurburg, W., 287; 313 Krasnov, E.V. See Polyakov, D.M., 200;
Knauer, G.A. See Martin, J.H., 172, 173, 210
174; 191, 192 Kraus, E.B., 133; 164
Knedler, K.E. See Cronan, D.S., 188 See Niiler, P.P., 133; 165
See Meylan, M.A., 183; 192 Krauss, W., 138; 164
Kravitz, E.A. See Battelle, B.-A., 268; 306 Landini, F. See Morten, L., 192
Krawiec, R.W. See Durbin, E.G., 89; 96 Lang, C., 436, 488; 587
Krebs, H.A., 272; 309 Lang, J., 465, 468, 532; 587
Kremling, K., 173, 176; 191 See Richardson, C.A., 465, 532; 589
Krishnaswami, S., 180, 181; 191 See Woodley, J.D., 168
See Moore, W.S., 175; 192 Langerhans, P., 354; 390
Krogh, A., 394; 426 Langford, R.R. See Lasenby, D.C., 399,
Krohn, A., 351, 352, 364; 390 410, 418; 426
Kroll, J., 155; 164 Langmuir, I., 137; 164
Krom, M.D., 173; 191 Lapota, D. See Losee, J.R., 76; 97
Krone, M.A., 207; 209 Lappalainen, A. See Fenchel, T., 496; 584
Krumbach, T., 350; 390 Larkin, P.A., 410; 426
Kruth, H.S., 82; 96 Larson, B.R., 452; 587
Ku, T.-L. See Bender, M.L., 181; 187 Larson, R.J., 520, 523, 563, 568; 587
See Bischoff, J.L., 173; 187 Lasenby, D.C., 399, 410, 418; 426
Ku, T.L. See Lalou, C., 183; 191 Lasker, R., 137; 164
Lassen, H.H., 280; 309
See Moore, W.S., 192 Lassig, B.R., 452; 587
Kuenzler, E.J. See Striven, A.E., 436, 490; Lassus, P. See Trellu, J., 277; 312
591 Laurec, A. See Boucher, J., 278; 306
Kuhl, W., 343, 350, 354, 358, 361, 378; Lavie, B., 282; 309
390 Lavergne, D. See Michard, G., 173; 192
Kuhlmann, D., 348, 357, 359, 360, 364, Laws, E. See Bienfang, P., 108; 121
370, 371, 373, 377, 382; 390 Laws, R.M. See May, R.M., 587
Kullenberg, G., 63, 64; 97 Lawson, T.J., 512; 587
Kullenberg, G.E., 134; 164 Laxen, D.P.H., 175; 191
Kumbalek, S.C. See Meylan, M.A., 180; Le Blanc, M.J. See Chan, A.T., 487; 582
192 LeBlond, P.H., 127, 138; 164
Kundu, P.K., 133; 164 Lebour, M.V., 345, 364, 386; 390
Künne, C., 410; 426 Le Coz, J.R. See Samain, J.F., 278; 311
Kuo Yang, R.T. See Quinn, W.H., 157; 166 U
Kurihara, Y. See Tsuchiya, M., 506; 592 Lee, C.K. See Shinn, E.A., 207; 210
Kusakabe, M. See Tsunogai, S., 173; 194 Lee, J.C. See Hesterberg, L.K., 269; 309
Kusmorskaya, A.P., 387; 390 Lee, R.F. 265, 278, 385; 309, 310, 391
See Sargent, J.R., 385; 392
Labat, R., 423; 426 Lee, S.L., 178; 191
La Barre, S., 465; 587 Lees, M. See Folch, J., 212, 221, 247; 261
Lackner, R. See Weiser, W., 271; 313 Le Gal, Y. See Thébault, M.-T., 277; 312
Lacroix, G. See Ladurantaye, R.de, 399, Legeckis, R., 142; 164
410, 416; 426 Legendre, L., 87, 105, 115, 135; 97, 122,
Ladurantaye, R.de, 399, 410, 416; 426 164
Lai, Y.-K. See Hammond, G.L., 278; 309 See Demers, S., 130, 135; 161
Lalou, C., 183; 191 See Yentsch, C.M., 97
Lam, R.K. See Jamart, B.M., 122 Legendre, P. See Legendre, L., 87; 97
Lamont, P. See O’Connor, R.J., 440; 588 Leibovich, S., 138; 164
Lamoral, B., 464, 563; 587 Leibson, L.G. See Plisetskaya, E., 268; 311
Landing, W.M., 172; 191 Leigh-Abbott, M.R., 143; 164
AUTHOR INDEX 647
Leinen, M., 179; 191 See Bayne, B.L., 264; 306

Leinen, M. See Bischoff, J.L., 180; 187 See Ebberink, R.H.M., 269; 307
Lemos, J.R., 268; 310 See Moore, M.N., 310
Leopold, M. See Livingstone, D.R., 276; See Widdows, J., 313
310 See de Zwaan, A., 274; 307
Lesicki, A., 270, 295; 310 Loder, J.W., 31, 157; 52, 164
Leuckart, R., 349, 354; 391 Loftus, M.E., 66; 97
Leverne, C. See Honnorez, J., 190 Long, E.R. See Schoener, A., 542; 590
Levi, S. See Honnorez, J., 190 Longhurst, A.R., 127; 164
Levin, L.A., 449, 493; 587 Longuet-Higgins, M.S., 30; 52
Levin, S.A., 128, 531, 538; 164, 587 Lonsdale, P., 183; 191
See Paine, R.T., 531, 538; 589 Lonsdale, P.F. See Fyfe, W.S., 183; 189
Levins, R. See Macarthur, R.H., 456; 587 Lopez, G.R., 547; 587
Levinton, J., 476, 490, 568; 587 Lorenzen, C.J., 66, 113; 97, 122
Levinton, J.S., 127, 275, 280, 490, 492, Losee, J.R., 76; 97
500, 502, 503, 565, 569; 164, 310, 587 Lot-Helgueras, A., 320; 341
See Bianchi, T.S., 496, 497; 581 Lott, J.N. See Harris, G.P., 135; 163
See Lopez, G.R., 547; 587 Loucks, R.H. See Sutcliffe, W.H., 156; 167
Leviten, P.J., 444, 446, 453, 461, 463, 538, Love, R.M., 213, 239; 261
550, 551, 552, 553; 587 Lovegrove, T., 213; 261
See Kohn, A.J., 462; 587 Lovett, M.B. See Nelson, D.M., 12; 52
Levy, Y., 202; 209 Low, R.M., 519; 587
Lewis, C. See Brock, R.E., 524; 582 Lowe, D.M. See Bayne, B.L., 303; 306
Lewis, D. See Dickinson, H.G., 339; 340 See Moore, M.N., 310
Lewis, J.B., 198, 442; 209, 587 See Widdows, J., 313
Lewis, J.K. See Hochachka, P.W., 277; 309 Lowry, O.H., 212, 216, 259, 260; 261
Lewis, L. See Chambers, J.E., 307 Loya, Y., 538; 587
Lewis, M.B. See Daniel, R.J., 32; 51 See Benayahu, Y., 465, 538; 581
Lewis, M.R., 135; 164 Lubchenco, J., 486, 487, 488, 489, 533,
Leyendekkers, J., 61; 97 534, 535, 542, 568; 587
Li, Y.-H., 169, 173, 181; 191 See Gaines, S.D., 487; 584
Liddicoat, M.I. See Knox, S., 191 See Menge, B.A., 436, 534; 588
Lighthill, J., 138; 164 Lucchini, F. See Rossi, P.L., 183; 193
Lindl, T. See Köhler, G., 268; 309 Luckens, P.A., 476; 587
Linford, E. See Raymont, J.E.G., 294; 311 Luckhurst, B.E., 522; 587
Liss, P.S., 176; 191 Luckhurst, K. See Luckhurst, B.E., 522;
See Emerson, S., 178; 189 587
See Holliday, L.M., 178; 190 Luedtke, N. See Elderfield, H., 178; 189
Littler, M.M. See Seapy, R.R., 538, 539; See McCaffrey, R.J., 192
591 Luedtke, N.A., 178; 191
See Taylor, P.R., 531, 538; 592 See Froelich, P.N., 189
Livingston, H.D., 12; 52 Lupton, J.E., 184; 191
Livingston, H.O., 195, 196, 198, 200, 201, Lyle, M., 182, 183; 191
202, 204, 205; 209 See Corliss, J.B., 184; 188
Lyle, M.W. See Moore, W.S., 192
Livingstone, D.R., 274, 276, 278, 282, Lyne, V.D., 160; 164
287, 294, 297, 298; 310 Lynn, D.C., 179; 191
Lyons, W.B., 173, 177, 178; 191
Lytle, C.F., See Mercando, N.A., 509; 588 Marchalonis, J.J. See Knox, R.B., 341
Marchig, V., 170, 182, 183, 185; 191
Macarthur, R.H., 456; 587 See Berger, W.H., 179; 187
MacDonald, K.C. See Lupton, J.E., 191 See Gundlach, H., 173, 185; 190
MacDonald, R.D. See Grill, E.V., 183; 190 See Heye, D., 182; 190
MacDougall, J.D. See Moore, W.S., 192 Marcus, N.H., 280; 310
MacIntyre, I.G. See Barnard, L.A., 196, Mardell, G.T. See Pingree, R.D., 103, 147;
202; 205 122, 165
MacIntyre, R.J., 278; 310 Margalef, D.R., 129; 164
Mackas, D.L., 131; 164 Margalef, R., 108; 122
See Denman, K.L., 91; 96, 162 Maris, R.C., See Feigenbaum, D.L., 343–
Mackay, D.A., 443; 587 392
Mackie, A.M. See Mayo, P., 442; 588 Mariscal, R.N. See McLean, R.B., 509; 588
MacPherson, E., 518; 587 Markert, C.L. See Hammond, G.L., 278;
Macquart-Moulin, C., 395, 398, 400, 412, 309
414, 423; 426, 427 Marra, J., 126, 128, 135, 141; 164
MacVean, M. See O’Brien, J.J., 165 Marra, J. See Fournier, R.O., 143; 162
Maddock, L. See Pingree, R.D., 22, 31, Marriage, H. See Zeeman, E.C., 123
137, 153; 53, 165 Marsh, Jr, J.A., 196; 209
Maggi, P.See Trellu, J., 277; 312 Marshall, N.F. See Shepard, F.P., 152; 166
Magniez, G., 396, 400; 427 Marshall, S.M., 100, 159; 122, 164
Mague, F.C. See Yentsch, C.M., 98 Marszalek, D.S., 196; 209
Maguire, L.A., 466; 587 Marteijn, E. See Livingstone, D.R., 276;
Mahen, L.C. See Dayton, P.K., 442; 583 310
Mahler, H.R., 264, 268; 310 Martin, A.D. See Olla, B.L., 455; 588
Maier-Reimer, E. See Radach, G., 105; 123 Martin, J.H., 172, 173, 174, 178, 198; 191,
Mainardi, D., 509; 587 192, 209
Major, P.F., 439, 450; 587 See Goldberg, E.D., 308
Malmestein, A.D., 320; 341 Martin, J.-L.M. See Mayzaud, P., 385; 391
Malone, T.C., 148; 164 Martin, J.-M. 178; 192
Mandelli, E.F. See Zeitoun, M.A., 196; 210 Marumo, R. See Nagasawa, S., 350, 355,
Mangini, A. See Müller, P.J., 170; 192 356, 358, 359, 363, 367, 373, 374, 375,
Mangum, B. See Edmond, J.M., 189 377, 378, 379, 382, 383; 391
Mangum, C.P., 264, 287, 288, 291, 505; Marumo, R. See Terazaki, M., 369; 392
310, 587 Massutí-Oliver, M., 364; 391
See Sassaman, C., 288, 289; 311 Mathers, N.F. See Wilkins, N.P., 568; 593
Manheim, F.T., 170, 178; 191 Matisoff, G. See Holdren, G.R., 173; 190
Mann, K.H., 436, 488, 534; 587 Matsudaira, C., 398; 427
See Bernstein, B.B., 534; 581 Matsumoto, E. See Sakata, M., 178; 193
See Lang, C., 436, 488; 587 Matthews, J.B. See Mungall, J.C.H., 23; 52
See Platt, T., 117, 211; 123, 261 Matthews, J.B.L. See Båmstedt, U., 294;
Mansey, E.L. See Carpenter, G.F., 410; 426 305
Mansour, T.E., 267, 269; 310 Mathieu, G. See Li, Y.-H., 173; 191
See Stone, D.B., 269, 270; 312 Mattsson, O. See Heslop-Harrison, J., 339;
Mantoura, R.F.C. See Morris, A.W., 178; 341
192 Mauchline, J., 11, 12, 393, 395, 399, 401,
Maragos, J.R. See Grigg, R.W., 538; 585 406, 407, 408, 409, 410, 412, 413, 414,
AUTHOR INDEX 649
417, 418, 420, 421, 422, 423, 424; 52, McLean, R., 509, 510; 588
427 McLean, R.B., 509; 588
Mauzey, K.P., 442; 587 McLeod, P.R. See King, D.P.F., 517; 586
May, B. See Gagnon, P.S., 318; 340 McLoughlin, P.A. See Shepard, F.P., 152;
May, R.M., 160, 436; 164, 587 166
Mayo, P., 442; 588 McLusky, D.S., 405; 427
Maybury, C.A. See Dauer, D.M., 494; 583 McMillan, C., 321, 322, 323, 324; 341
Maynard, V. See Froelich, P.N., 189 See Phillips, R.C., 321; 342
Mayzaud, P., 385; 391 McMurtry, G.M., 183, 185; 192
McArthur, J.M., 172; 192 McQuaid, C.D., 446, 447; 588
McAuliffe, C.D. See Monaghan, P.H., 196, McRoy, C.P., 317; 341
207; 209 See Phillips, R.C., 342
McCaffrey, R.J., 173; 192 McShane, P. See Black, R., 434; 581
See Elderfield, H., 178; 189 Measures, C. See Edmond, J.M., 184; 189
McCall, P.L., 493; 588 Medler, K.J. See Ramster, J.W., 36; 53
McCarthy, J.J., 159; 164 Mednikov, B.M., 400; 427
McCarthy, J.J. See Goldman, J.C., 116, Meek, A., 351; 391
159; 121, 163 Meissner, G., 354; 391
McCave, I.N. See Goldberg, E.D., 117; 121 Melamed, M.R., 82; 97
McConchie, C.A., 331, 332, 333, 334; 341 Mellor, G.L., 133; 164
See Pettitt, J.M., 330, 332; 341 Mendelson, M.L. See Melamed, M.R., 82;
McCorker, J.E. See Glynn, P.W., 534; 584 97
McCorkle, F.M. See Chambers, J.E., 307 Menge, B.A., 436, 453, 458, 459, 460,
McCosker, J.E. See Stephens, J.S., 523; 464, 483, 484, 487, 533, 534, 536, 538,
591 548, 549, 552, 564, 568; 588
McCullough, J.R. See Beardsley, R.C., 51 See Lubchenco, J., 488, 533, 542; 587
McCully, J. See Hall, E.R., 270; 308 Menge, J.L. See Menge, B.A., 453, 548,
McDonald, A.K. See Traganza, E.D., 155; 549; 588
167 Menzel, D.W. See Steele, J.H., 59; 97
U* See Sutcliffe, W.H., 137; 167
McDonald, P.W. See Dorsey, T.E., 212; See Yentsch, C.S., 66; 98
261 Menzel, W., 263; 310
McDougall, J.C. See Cronan, D.S., 188 Mercando, N.A., 509; 588
See Meylan, M.A., 180; 192 Mero, J.L., 170; 192
McDuff, R.E. See Edmond, J.M., 184; 189 Meurs, C.J. See van de Weijden, C.H.,
McElroy, W.D. See Seliger, H.H., 75; 97 178; 194
McGowan, J.A., 131, 514; 164, 588 Meybeck, M. See Martin, J.-M., 178; 192
See Chelton, D.B., 156; 161 Meylan, M.A., 180, 183; 192
See Fager, E.W., 131; 162 Michael, E.L., 346; 391
See Haury, L.R., 91; 96 Michard, G., 173, 181; 192
McIlhenny, W.F. See Zeitoun, M.A., 196; Middel, V. See Bender, M.L., 187
210 Migdisov, A.A. See Honnorez, J., 190
McKenzie, R.M., 169; 192 Miklas, H.P. See Carpenter, E.J., 389
McKinley, I.G., 33; 52 Milkman, R., 281; 310
McKinley, K.R. See Seliger, H.H., 166 Millard, R.C. See Voorhis, A.D., 143, 154;
McLaren, I.A., 361, 384, 386, 394, 400, 168
401, 402, 414; 391, 427 Miller, C.B. See Peterson, W.T., 144; 165
Miller, D.S. See Amiel, A.J., 196, 200, Moore, R.M., 178; 192
202, 203, 204, 205; 208 Moore, S.L. See Widdows, J., 313
Miller, R.S., 431; 588 Moore, T.C. See Heath, G.R., 170; 190
Mills, B.A. See Bowser, C.J., 180; 187 Moore, W.S., 175, 182, 185; 192
Mills, E.L., 502; 588 See Bonatti, E., 183; 187
Mironov, G.N., 345, 357, 361, 363, 364, See Chapnick, S.D., 175; 188
365, 369, 370, 371, 373, 375, 377, 378, See Dean, W.E., 175; 189
382, 383, 386, 387; 391 See Hess, J., 178; 190
Mirza, F.B. See Gray, J.S., 301; 308 Moran, M.J., 520, 563; 588
Mishin, V.L., 385; 391 See Underwood, A.J., 435, 472, 531;
Mitchell, K.A., 510; 588 592
Mitchell, P.H., 221; 261 Morel, A. See Bricaud, A., 55; 96
Mitchell, R., 197, 206; 209 See Sathyendranath, S., 81; 97
Mitterer, R.M, 203, 204, 205; 209 Moreno, I., 350; 391
Mitton, J.B. See Byers, B.A., 447; 582 Moreth, C.M., 62; 97
See Koehn, R.K., 280; 309 Morgan, C.W., 154; 164
Miyake, M. See Denman, K.L., 133, 134; Morgan, M.D., 399, 406, 410; 427
162 Morgan, P.W. See Malmestein, A.D., 320;
Moal, J. See Samain, J.F., 278; 311 341
Moffler, M.D., 320; 341 Mork, M., 105; 122
See Grey, W.F., 320; 340 Morris, A.W., 176, 178; 192
Möller, P. See Marchig, V., 185; 191 Morris, N.C. See Simpson, J.H., 146; 166,
Monaghan, P.H., 196, 207; 209 167
Monin, A.S., 128; 164 Morris, N.C.G. See Simpson, J.H., 103;
Monk, J.D. See Garvine, R.W., 148; 162 123
Montalva, S., 486, 568; 588 Morris, R.J., 213, 294; 261, 310
See Santelices, B., 486, 563; 590 Morris, S.R. See Beardmore, J.A., 570; 581
Montgomery, R.B. See Rossby, C.G., 133; Morrison, G. See McCaffrey, R.J., 192
166 Morrison, G.K. See Pingree, R.D., 146; 165
Mooers, C.N., 132, 142, 143, 150; 164 Morse, D.E., 488; 588
Mooers, C.N.K. See Brink, K.H., 161 Morse, J.W. See Van Valin, R., 180; 194
See Collins, C.A., 161 Morten, L., 183; 192
See Halliwell, G.R., 154; 163 Mortimer, M. See Begon, M., 431, 458,
Mook, D.H., 533; 588 485; 581
Moon, T.W., 277; 310 Moser, C. See McMurtry, G.M., 183; 192
Moorby, S.A., 169; 192 Moss, D.W., 277, 281; 310
See Cronan, D.S., 182; 188 Mottana, A. See Morten, L., 192
See Honnorez, J., 190 Mottl, M.J., 183; 192
Moore, D. See Baas-Becking, L.G.M., 170; See Seyfried, W.E., 183; 193
186 Moueza, M. See Ansell, A.D., 294; 305
Moore, J.A., 402; 427 Moyse, J., 439; 588
Moore, K.A. See Silberhorn, G.M., 317; See Knight-Jones, E.W., 439, 440; 586
342 Mueller, J.L. See Gordon, H.R., 71; 96
Moore, M.N., 278; 310 See Hovis, W.A., 96
See Bayne, B.L., 264; 306 Muench, R.D. See Pearson, C.A., 20; 53
See Koehn, R.K., 281; 309 Muir, B.S. See Sutcliffe, W.H., 156; 167
See Lee, R.F., 309 Muir, L.R. See Williams, P.J. L., 116; 123
See Widdows, J., 313 Muirhead, K. See Yentsch, C.M., 97, 98
AUTHOR INDEX 651
Mullaney, P.F. See Melamed, M.R., 82; 97 Nair, V.R., 364; 391
Müller, P.J., 170; 192 Nakada, H.I. See Bennett, R., 270; 306
See Hartmann, M., 173; 190 Nakamura, K. See Katô, M., 444; 586
Mullen, W.A., 436, 501; 588 Nakanishi, K. See Tsunogai, S., 182; 194
Mulligan, T.R. See Borstad, G.A., 161 Nalwalk, A.J. See Scott, M.R., 193
Mullin, M.M. See Hastings, J.W., 77; 96 Neal, V.T. See Caldwell, D.R., 139; 161
Munday, K.A,, 271; 309 Nealson, K.H. See Chapnick, S.D., 175;
See Poat, P.C., 271; 311 188
Mungall, J.C.H., 23; 52 See Dean, W.E., 175; 189
Munk, W. See Garrett, C., 138; 162 See Emerson, S., 189
Munk, W.H., 133, 141; 164 Neff, J.M. See Carr, R.S., 302; 307
Muntz, L. See Ebling, F.J., 536; 583 Neigel, J. See Woodley, J.D., 168
Murakami, A., 345, 346, 361; 391 Neigel, J.E. See Porter, J.W., 589
Murakami, H. See Ishikawa, T., 268; 309 Neill, W.E., 513, 514; 588
Murano, M., 394, 395, 399, 400, 407, 411; Nelson, D.M., 12; 52
427 Nelson, K., 280, 293; 310
See Mauchline, J., 401, 412; 427 See Tracy, N.L., 312
Murdock, E.A., 280; 310 Nestor, D.A. See Traganza, E.D., 155; 167
Murphy, L.S. See Schopf, T.J.M., 460; 591 Neudecker, S., 195, 196; 210
Nevo, E., 282; 310
See Yentsch, C.M., 97 See Lavie, B., 282; 309
Murphy, P.G., 529, 560, 570, 571, 575; Newbury, T.K., 346, 363, 367, 375, 377,
588 383; 391
Murray, B.G., 562, 563; 588 Newell, R.C., 546; 588
Murray, C.N. See Kautsky, H., 12, 33; 52 Newman, W.A., 566; 588
Murray, J., 173, 179; 192 See Stanley, S.M., 565, 566, 567; 591
Murray, J.W., 169, 173; 192 Newsholme, E.A., 266, 267, 269, 272; 310
See Bacon, M.P., 186 See Alp, P.R., 299; 305
See Balistrieri, L., 169; 186 See Beis, I., 274, 298; 306
See Balistrieri, L.S., 169; 186 See Crabtree, B., 269; 307
See Grill, E.V., 183; 190 See Underwood, A.H., 268; 312
See Sawlan, J.J., 173; 193 See Zammit, V.A., 269, 275, 298; 313
Murray, S.P. See Roberts, H.H., 152; 166 Nicholson, A.J., 430; 588
Murthy, C.R., 29; 52 Nicklas. N.L., 280: 311
Mustafa, T. See Hochachka, P.W., 287; Nicolaisen, W., 503; 588
309 Nicotri, M.E., 472, 488; 588
Mustaffi, Z., 196; 209 Nihoul, J.C.J., 111, 115, 118, 151; 122, 165
Muzzarelli, R.A., 205, 206; 210 Niiler, P.P., 133; 165
Myers, A.C. See McCaffrey, R.J., 192 See Kroll, J., 155; 164
Myrberg, A.A., 520, 521, 523, 563; 588 Nimmo, D.R., 393, 405; 427
Mysak, L.A., 30, 149, 157; 52, 164, 165 Nolting, R.F. See Duinker, J.C., 178; 189
See LeBlond, P.H., 127, 138; 164 Nordstrom, C.E. See Inman, D.L., 152; 163
Normark, W.R. See Lupton, J.E., 191
Nagasawa, S., 350, 355, 356, 358, 359, Northcroft, R.D., 490; 588
363, 367, 373, 374, 375, 377, 378, 379, Norton, T.A., 444; 588
382, 383; 391 See Schonbeck, M., 485, 486, 563,
Nair, K.B., 398; 427 568; 590
Noshkin, V.E. See Levy, Y., 202; 209
Nouvel, H., 395, 399, 407, 423; 427 Osborn, T.R., 139; 165
Nouvel, L. See Nouvel, H., 395, 399, 407; Oshima, Y. See Ishikawa, M., 395, 399,
427 407; 426
Nowell, A.R.M. See Eckman, J.E., 507; Osman, R., 538, 542; 588
583 Osman, R.W., 531, 538, 539, 542, 546; 588
Nozaki, Y. See Brewer, P.G., 172; 188 Ottaway, J.R., 443; 588
Nybakken, J., 127, 551; 165, 588 Owen, R.W., 142, 155; 165
Nybakken, J.W. See Kohn, A.J., 453, 454, Owens, O.V.H., 127; 165
461, 462, 530; 587
Nyholmen, O. See Hopkins, C.C.E., 211– Packard, T.T., 144; 165
261 Paffenhofer, G.A., 155; 165
Paine, R.T., 430, 446, 461, 463, 464, 471,
Oakey, N.S. See Lewis, M.R., 164 484, 488, 507, 513, 527, 531, 533, 534,
O’Brien, J.J., 105, 137, 150, 160; 122, 165 538, 544, 566, 568; 588, 589
See Preller, R., 152; 166 See Dayton, P.K., 533; 583
See Goldberg, E.D., 117; 121 See Levin, S.A., 531, 538; 587
See Wroblewski, J.S., 110; 123 See Zaret, T.M., 545; 593
Ochsner, P. See Ribi, G., 456, 529, 560; Pak, H. See Spinrad, R.W., 70; 97
589 Palmisano, J.F. See Estes, J.A., 489, 534;
Ockelmann, K.W., 295; 311 584
Ockendon, D.J. See Roberts, I.N., 339; 342 Papaioannov, J. See Varnavas, S.P., 183;
O’Connor, R.J., 440, 480, 481, 527, 532; 194
588 Paradies, H.H. See Goldhammer, A.R.,
See Boaden, P.J.S., 480; 581 269; 308
See Seed, R., 439, 440, 444, 480, 527, Pardee, A.B. See Yates, R.A., 271; 313
532, 558, 564; 591 Parisi, V. See Rossi, A.C., 509; 590
Odum, E.P., 409, 411; 427 Park, Y.-A. See Yearn, K.W., 178; 194
Ogden, J.C., 524; 588 Parker, M. 407; 427
See Grünbaum, H., 436; 585 Parker, P.L. See Goldberg, E.D., 308
Okabe, S. See Takematsu, N., 182; 194 Parker, R.L., 169; 192
Okamoto, J. See Hildemann, W.H., 585 Parker, W.R. See Smith, T.J., 11; 53
Okubo, A., 110, 111, 115, 128, 134, 152; See Williams, S.J., 13; 53
122, 165 Parks, G.A., 169; 192
See Bowman, M.J., 143; 161 Parry, D.A., 343, 345, 346, 350, 351, 352,
See Denman, K.L., 152; 162 356, 357, 358, 359, 367, 370, 373, 378,
See Shigesada, N., 126; 166 385; 391
Olafsson, J., 185; 192 Parslow, J.S. See Turpin, D.H., 128; 168
Oliger, P. See Santelices, B., 486, 563; 590 Parsons, T.R., 125, 127, 128, 135; 165
Olla, B.L., 298, 455; 311, 588 See Mysak, L.A., 157; 165
Olley, J. See Hansen, S.W.F., 212; 261 See Sheldon, R.W., 77; 97
Olson, R.J., 83, 84; 97 Parvathy, K., 294; 311
Onken, R. See Woods, J.D., 106, 109; 123 Pascasio, J.F., 325, 327; 341
Orput, P.A., 320; 341 Pasciak, W.J., 159; 165
Orr, A.P. See Marshall, S.M., 100, 159; Pashinski, D.J. See Schumacher, J.D., 142;
122, 164 166
Orr, M.H. See Haury, L.R., 140; 163 Pastan, I., 279; 311
Orth, R.J. See Silberhorn, G.M., 317; 342 Patel, B., 394; 427
AUTHOR INDEX 653
Patouillet, C. See Hannan, P.J., 199; 209 Peterson, C.H., 484, 490, 491, 492, 493,
Patriquin, D.G. See Keddy, C.J., 318; 341 503, 504, 507, 527, 533, 534, 536, 556,
Patriti, G. See Macquart-Moulin, C., 395, 565; 589
398; 427 Peterson, M.N.A. See Boström, K., 183;
Pattullo, J.G. See Collins, C.A., 161 187
Pavey, J. See Brace, R.C., 443, 465; 581 Peterson, W.T., 144, 150; 165
Pearcy, W.G., 144; 165 Petraitis, P.S., 478; 589
Pearre, S., 512; 589 Petrie, B., 155; 165
Pearre, Jr, S., 343, 358, 361, 363, 364, 365, Pettitt, J.M., 315–342; 324, 325, 326, 327,
366, 367, 368, 369, 371, 373, 374, 375, 328, 329, 330, 331, 332, 333, 334, 335,
378, 380, 381, 382, 383, 384, 386; 391 337, 339, Figs 4, 7 and 10 (Pettitt)
Pearse, A.G.E. See Fritsch, H.A.R., 268; between pp. 334 and 335; 341
308 See Ducker, S.C., 330; 340
Pearse, J.B., 264; 311 See McConchie, C.A., 331; 341
Pearson, C.A., 20; 53 Pezzack, D.S., 395, 399; 427
Pearson, M. See Woodley, J.D., 168 Phillips, A.W., 32; 53
Pearson, T.H., 263, 264, 283, 290, 300, Phillips, O.M., 138; 165
301, 493, 568; 311, 589 Phillips, R.C., 317, 320, 321, 342; 341, 342
See Blackstock, J., 296, 299; 306 Phillips, R.R., 523; 589
See Gray, J.S., 301; 308 Phinney, D.A. See Yentsch, C.M., 97
Pearson, W.H. See Olla, B.L., 298; 311 See Yentsch, C.S., 91; 98
Peavey, D. See Goldman, J.C., 116; 121 Piatigorsky, J. See Barnes, H., 286; 306
Peavey, D.G. See Goldman, J.C., 159; 163 Pickard, G.L. See Pond, G.S., 127; 166
Peck, B.B. See Carpenter, E.J., 389 See Pond, S., 106; 123
Pedersen, T.F., 170; 192 Pielou, E.C., 113; 122
Pedlosky, J., 127; 165 Pierce, J., 259; 261
Peng, T.-H. See Broecker, W.S., 169, 172, Pierce, J.W. See Barnard, L.A., 196, 202;
173; 187 208
Pennycuick, L. See Southward, A.J., 157;
167 Pierson, E.S. See Jacobs, R.P.W.M., 317,
Pequegnat, W.E. See Malmestein, A.D., 318, 319; 341
320; 341 Pieters, H. See Kluytmans, J.H., 294; 309
Perez, K.T. See Dwyer, R.L., 160; 162 See Zandee, D.I., 294; 313
Perez-Leclaire, H. See Lalou, C., 183; 191 Pietrafesa, L.J. See Atkinson, L.P., 154;
Perkins, E.J., 32; 53 160
Perl, T. See Nevo, E., 282; 310 Pilkis, S. See Claus, T.H., 269; 307
Perlman, R.L. See Pastan, I., 279; 311 Pillsbury, R.D. See Halpern, D., 19; 51
Perrin, D.D., 169; 192 See Walsh, J.J., 168
Perry, M.J. See Ward, B.B., 83; 97 Pilson, M.E.Q., 198; 210
See Yentsch, C.M., 97 Pingree, R.D., 22, 23, 24, 27, 31, 44, 103,
Pesando, D. See Amade, Ph., 478, 562; 580 104, 105, 107, 108, 118, 137, 146, 147,
Peters, R.H., 429; 589 153; 53, 122, 165
Peters, W., 358; 391 See Simpson, J.H., 146; 167
Peters, W. See Wilfert, M., 205; 210 Pionetti, J.-M., 264; 311
Petersen, H. See Kremling, K., 173, 176; Piper, D.Z. See Moore, W.S., 192
191 Piyakarnchana, T., 364, 365, 366; 391
Petersen, J.A. See de Jorge, F.B., 294; 307
Platt, T., 77, 110, 113, 114, 115, 117, 119, See Addy, S.K., 173; 186
127, 128, 135, 160, 211; 97, 123, 166, See Trefry, J.H., 177, 181; 194
261 Preston, A. See Jefferies, D.F., 33; 52
See Denman, K.L., 114, 128, 152, 160; Pressick, M.L. See Tracy, N.L., 312
121, 162 Price, M.H. See Childress, J.J., 398, 414,
See Gallegos, C.L., 135; 162 423, 424; 426
See Lewis, M.R., 164 Price, N.B., 170, 173, 179; 193
See Silvert, W., 77; 97 See Calvert, S.E., 173, 178; 188
See Wroblewski, J.S., 110; 123 Price, N.B. See Duchart, P., 173; 189
Plisetskaya, E., 268; 311 See Pedersen, T.F., 170; 192
Poat, P.C., 271; 311 See Sholkovitz, E.R., 178; 193
See Munday, K.A., 271; 310 Price, W.S. See Lewis, J.B., 198; 209
Pocock, Y.P. See Hubbard, J.A.E.B., 203; Prieur, L. See Bricaud, A., 55; 96
209 Pritchard, R.G. See Cann, J.R., 183; 188
Pollard, R.T., 133, 137, 138; 166 Proctor, R., 22, 23, 24, 30, 36, 43, 44, 46,
Polyakov, D.M., 200; 210 47, 48, 49; 53
Pomponi, S.A. See Yentsch, C.M., 97 Prosser, C.L., 402; 427
Ponat, A. See Theede, H., 288; 312 See Hazel, J., 277; 309
Pond, G.S., 127; 166 Proudman, J., 21, 22, 23; 53
Pond, S., 106; 123 Pugh, D.T., 24; 53
Pontér, C. See Boström, K., 176; 187 Pugh, P.R., 77; 97
Pontier, P.J. See Grant, W.C., 509; 585 See Fasham, M.J.R., 106, 114, 136;
Pontin, A.J., 430, 431, 454, 559; 589 121, 162
Poore, G.C.B., 542, 543; 589 See Pingree, R.D., 103, 146; 122, 165
Pople, W. See John, D.M., 489; 586 Pulliam, H R. See Pyke, G.H., 548; 589
Porter, J. See Woodley, J.D., 168 Pulsford, A. See Bone, Q., 356; 389
Porter, J.W., 466, 467, 468, 534, 535, 538, Purcell, E.M., 159; 166
578; 589 Purcell, J.E., 443, 465, 563; 589
See Maguire, L.A., 466; 587 Pyke, G.H., 548; 589
See Wethey, D.S., 468; 592
Posner, A.M. See Forbes, E.A., 169; 189 Quinby-Hunt, M.S., 172; 193
Potts, D.C., 466; 589 Quinn, W.H., 157; 166
Poulet, S.A., 514; 589 Quintero, C.R., 398, 412; 427
Poulin, M. See Legendre, L., 135; 164 Quirk, J.P. See Forbes, E.A., 169; 189
Powell, C.A. See Drummond, G.I., 268; Quoy, J., 349, 354; 391
307
Powell, T.M. See Abbott, M.R., 126, 128, Rabalais, N.N. See Flint, R.W., 495; 584
141; 160 Radach, G., 105; 123
See Dillon, T.M., 133; 162 Raffaeli, D.G. See Elner, R.W., 554; 583
See Leigh-Abbott, M.R., 143; 164 Raison, R.L. See Hildemann, W.H., 585
Prada, K.E. See Joyce, T.M., 159; 163 Rakhmanov, V.P. See Varentsov, I.M., 170;
Prakash, A. See Sheldon, R.W., 77, 128, 194
129; 97, 166 Rakusa-Suszczewski, S.J., 363, 367, 368,
See Sutcliffe, W.H., 137; 167 369, 383; 391
Prandle, D., 22; 53 Ramaiah, A., 272; 311
Pratt, D.M., 444; 589 Ramming, H.G., 21; 53
Preller, R., 152; 166 Ramster, J.W., 32, 34, 35, 36, 43; 53
Presley, B.J., 173; 192
AUTHOR INDEX 655
See Hill, H.W., 35; 52 Reynolds, J.B., 410; 427

Ramus, J., 567; 589 Rhines, P.B. See Pollard, R.T., 133; 166
Randall, R.J. See Lowry, O.H., 212; 261 See Young, W.R., 152; 168
Ranier, S.F. See Ivanovici, A.M., 264; 309 Rhoads, D.C., 506, 507, 542; 589
Rankin, P.C. See Glasby, G.P., 179, 180; Ribi, G., 456, 457, 529, 530, 560; 589
190 See Ferlin-Lubini, V., 456; 584
Rao, K.P., 402; 427 Richards, F.A., 149; 166
Rao, K.R., 302; 311 Richards, S.W., 411; 427
Rao, P.K.V. See Kausik, S.B., 328; 341 Richardson, C.A., 465, 532; 589
Rasa, O.A.E., 518; 589 Richardson, K., 60; 97
Raven, J.A. See Richardson, K., 60; 97 Richerson, P.J. See Abbott, M.R., 126,
128, 141; 160
Raymont, J.E.G., 294; 311 See Leigh-Abbott, M.R., 143; 164
See Reeve, M.R., 384; 392 Richman, J.G. See de Szoeke, R.A., 132,
Raymont, J.K.B. See Reeve, M.R., 384; 144; 162
392 Rieper, M., 501; 589
Rebers, P.A. See Dubois, M., 340 Rigby, R.A. See Nimmo, D.R., 405; 427
Rees, C.P., 502, 504; 589 Rigg, E. See Davison, W., 175; 188
Rees, D.A., 278; 311 Riley, J.P., 171, 172; 193
Reese, E.S., 510, 561; 589 Riley, G.A., 59, 100, 102, 105, 135, 136;
Reeve, M.R., 343, 345, 346, 348, 349, 357, 97, 123, 166
358, 359, 360, 361, 364, 365, 366, 367, See Richards, S.W., 411; 427
368, 369, 370, 371, 373, 374, 375, 377, Riner, M.R. See Churchill, A.C., 317, 318;
379, 380, 381, 382, 383, 384, 385, 388, 340
Fig. 3 (Feigenbaum & Maris) facing p. Riseborough, R.W. See Goldberg, E.D.,
348, Fig. 12 (Feigenbaum & Maris) 308
facing p. 358, Fig. 14 (Feigenbaum & Risk, M.J. See Tunicliffe, V., 546; 589
Maris) between pp. 358 and 359; Ritter-Zahony, R., 343, 354, 370; 392
See Cosper, T.C., 349, 350, 358, 359, Rittschof, D., 509; 589
370, 373, 383, 385, Fig. 4 (Feigenbaum See Bach, C., 508; 580
& Maris) facing p. 350; 389 Rivera, T. See Zuta, S., 144; 168
See Feigenbaum, D.L., 346, 347, 348, Rivken, R.B. See Seliger, H.H., 166
349, 360, 367, 382, 383, 388; 390 Roa, E.Z.de See Quintero, C.R., 398, 412;
Reid, P.C. See Colebrook, J.M., 157; 161 427
Reid, R.O. See Zeitoun, M.A., 196; 210 Roach, P.J., 21; 53
Reish, D.J., 263, 290, 300, 303, 494; 311, Roberts, D., 495; 589
589 Roberts, H.H., 152; 166
See Bellan, G., 303; 306 Roberts, I.N., 339; 342
See Carr, R.S., 303; 307 See Stead, A.D., 339; 342
See Cripps, R.A., 264, 283; 307 Roberts, J., 138; 166
Reisinger, E., 356; 392 Roberts, R.J. See Jones, K.J., 122
Reiswig, H.M, 476; 589 Robertson, A.H.F., 185; 194
Renard, A.F. See Murray, J., 179; 192 See Fleet, A.J., 185; 189
Renger, E.H. See Eppley, R.W., 136; 162 Robertson, D.R., 523, 524, 541, 564; 589,
Reynolds, C.S. See Walsby, A.F., 109, 590
130; 123, 168 Robertson, W. See Goldberg, E.D., 308
Reynolds, G.T., 75; 97 Robbin, D.M. See Hudson, J.H., 195, 207,
208; 209
Robbins, J.A., 175; 193 Russell, G., 487

Robilliard, G.A. See Dayton, P.K., 533; Russo, A.R., 436; 590
583 Rust, B.W., 157; 166
Robinson I.S., 17, 23, 24, 31; 53 See Van Winkle, W., 156; 168
Rockstein, M., 274; 311 Rutgers, S. See Boyland, D.B., 198; 209
Roden, G.I., 142; 166 Rützler, K., 477; 590
Rodi, W., 106; 123 Ryan, B.F. See Ryan, T.A., 218; 261
Roed, L.P. See O’Brien, J.J., 165 Ryan, T.A., 218; 261
Roels, O.A. See Dorsey, T.E., 212; 261 Rydell, H. See Bonatti, E., 182, 185; 187
Roesijadi, G., 204; 210 Rydell, H.S. See Bonatti, E., 179; 187
Rogers, C.S., 468; 590 Ryland, J.S., 440, 444, 480; 590
Rona, P.A., 183, 184, 185; 193 See Harvey, P.H., 439; 585
See Cronan, D.S., 184; 188 Rylaarsdam, K. See Woodley, J.D., 168
See Scott, M.R., 193 Ryther, J.H., 125, 144; 166
See Shearme, S., 184; 193 See Hulbùrt, E.M., 159; 163
Ronday, F. See Nihoul, J.C.J., 111; 122
Ronday, F.C., 151; 166 Sabbadin, A., 444; 590
See Nihoul, J.C., 151; 165 Sachs, P.L. See Spencer, D.W., 176; 193
Rooney, M. See Woodley, J.D., 168 Saffe, F. See Theede, H., 288; 312
Rosebrough, N.J. See Lowry, O.H., 212; Safriel, U.N. See Ayal, Y., 474; 580
261 St John, B.E., 195, 196, 198, 200, 201,
Rosenberg, O., 329, 330, 331; 342 202, 203, 204; 210
Rosenberg, R. See Pearson, T.H., 263, 290, Sakata, M., 178; 193
300, 301, 493; 311, 589 Sakshaug, E., 87; 97
Rosenthal, R.J. See Dayton, P.K., 442; 583 Sale, P.F., 437, 519, 520, 522, 523, 524,
Ross, D.M., 509; 590 525, 530, 541; 590
Rossby, C.G., 133; 166 See Moran, M.J., 520, 563; 588
Rossi, A.C., 509; 590 See Williams, D.McB., 523; 593
See Mainardi, D., 509; 587 Salimans, M. See Ebberink, R.H.M., 268;
Rossi, P.L., 183; 193 307
Rosson, R.A. See Emerson, S., 189 Salkeld, P. See Bayne, B.L., 306
Roughgarden, J., 521; 590 Salmon, M. See Hyatt, G., 437, 451; 586
Roughgarden, J.D., 128; 166 Samain, J.F., 278; 311
See Anderson, H.s.V., 580 See Boucher, J., 278; 306
Rowe, G. See Harrison, W.G., 122 Sameoto, D.D., 381, 382, 384, 387; 392
Rowe, G.T. See Malone, T.C., 164 Sammarco, P.W., 531, 533, 536; 590
Roy, S., 170; 193 Samter, M., 399, 401, 410; 427
Rozanov. A.G., 179; 193 Sand, O., 269; 311
See Volkov, I.I., 179; 194 Sandercock, G.A., 513; 590
Rubey, W.W., 181; 193 Sanders, J.G., 178; 193
Rubin, J.A., 532; 590 Santelices, B., 486, 563; 590
Rüdenberg, L. See Stewart, J.G., 330, 331; See Montalva, S., 486, 568; 588
342 Santos, J.K. See Pascasio, J.F., 325, 327;
Russ, G.R., 533; 590 341
Russell, B.C., 523, 541; 590 Sará, M., 477; 590
See Anderson, H.s.V., 580 Sargent, J.R., 213, 235, 239, 246, 385; 261,
See Talbot, F.H., 522; 592 392
Russell, F.S., 157; 166
AUTHOR INDEX 657
See Campbell, P.N., 260; 260 Schroff, G., 287; 312

See Hopkins, C.C.E., 261 Schultz, C. See Bender, M.L., 179; 187
Sassaman, C., 288, 289; 311 Schumacher, J.D., 142; 166
Sastry, A.N., 303; 311 See Pearson, C.A., 20; 53
Satchell, D.G., 268; 312 Schweder, T. See Hopkins, C.C.E., 261
Sathyendranath, S., 81; 97 Schwerdtfeger, F., 394; 427
Sato, Y. See Takematsu, N., 182; 193 Scott, J. See Beardsley, R.C., 51
Saugen, J.L. See Iverson, R.L., 136; 163 Scott, J.T. See Walsh, J.J., 168
Savidge, G., 146; 166 Scott, M.R., 183; 193
See Simpson, J.H., 123 See Boudreau, B.P., 181; 187
Sawlan, J.J., 173; 193 Scott, R.B. See Scott, M.R., 193
Scatterday, J.W., 468, 563; 590 Scott, T., 345, 364; 392
Scharer, R. See Ribi, G., 456, 529, 560; Scully, E.P., 508; 591
589 Seapy, R.R., 538, 539; 591
Scharrer, E., 357; 392 Sears, M. See Bigelow, H.B., 142; 161
Schaudinn, J. See Theede, H., 288; 312 Searles, R.B. See Stephenson, W., 488,
Scheer, B.T., 286, 290; 312 534; 591
See Hohnke, L.E., 294; 309 Sebens, K., 482, 532, 563; 591
Schein, H., 436, 451; 590
Schiel, D.R., 438, 439; 590 Sebens, K.P., 465; 591
Schimke, R.T., 277; 312 Seed, R., 439, 440, 444, 480, 527, 532, 558,
Schlater, F.R. See Edmond, J.M., 189 564; 591
Schleser, R.A. See Tracy, N.L., 312 See Boaden, P.J.S., 480; 581
Schley, F See Marchig, V., 185; 191 See Murdock, E.A., 280; 310
Schlieper, C. See Theede, H., 288; 312 See O’Connor, R.J., 480, 532; 588
Schmidt, G., 259; 261 See Wood, V., 480; 593
Schneider, D., 507; 590 Segerstråle, S.G., 506; 591
Schneider, E. See Goldberg, E.D., 308 Seiderer, J.L. See Griffiths, C., 453, 553;
Schneider, R.C., 202; 210 585
See Buddemeier, R.W., 198; 209 Seiring, J.V., 212; 261
Schnier, C. See Gundlach, H., 173; 190 See Hopkins, C.C.E., 211–261
Schnitzer, M.B. See Bowman, M.J., 108, Seliger, H.H., 75, 148; 97, 166
137, 147; 121, 161 See Loftus, M.E., 66; 97
Schoener, A., 542; 590 See Tyler, M.A., 141, 148; 168
Schoener, T.W., 430, 431, 462, 472, 474, Sell, D.W., 418; 427
476, 495, 512, 515, 516, 527, 559, 575, Sella, G. See Badino, G., 570; 580
593; 590 Serunian, L.A. See Chaisson, R.E., 280;
Schofield, A., 200; 210 307
Schole, J., 267, 279; 312 Setchell, W.A., 317, 318; 342
Scholl, A. See Bulnheim, H.-P., 280; 306 Seyfried, W.E., 183; 193
Schonbeck, M., 485, 486, 563, 568; 590 Shapiro, H.M. See Olson, R.J., 83; 97
Schopf, T.J., 460; 591 Shapland, P. See Zeeman, E.C., 123
Schopf, T.J.M., 280; 312 Sharaf el Din, S.H., 34, 36; 53
See Chaisson, R.E., 280; 307 Sharp, J.H., 487; 591
Schöttler, U., 287, 291, 292, 299; 312 Sheader, M., 358; 392
See Schroff, G., 287; 312 Shearme, S., 184; 193
Schrader, E.L. See Honnorez, J., 190 See Cronan, D.S., 184; 188
Schroeter, S.C., 436, 471; 591
Shelbourne, J.E., 359; 392 Singer, J.J. See Atkinson, L.P., 154; 160
Sheldon, J.M. See Robertson, D.R., 523, Singer, S.C. See Lee, R.F., 278; 310
524, 541; 589, 590 Skellam, J.G., 109; 123
Sheldon, R.W., 77, 128, 129; 97, 166 Skjoldal, H.R., 273, 295; 312
See Sutcliffe, W.H., 137; 167 See Båmstedt, U., 291, 295; 305
Shelton, P.A. See Crawford, R.J.M., 517; Skornyakova, N.S., 179, 180; 193
583 Skud, B.E., 517; 591
Shen, L.C., 273; 312 Slabber, M., 349; 392
Shepard, F.P., 152; 166 Slagstad, D. See Tande, K.S., 278; 312
Shepherd, S.A., 471, 474, 488, 548; 591 Slatyer, R.O. See Connell, J.H., 489, 542;
Sheppard, C.R.C., 438, 465, 468, 532, 563, 583
564; 591 Sleep, N.H. See Wolery, T.J., 183; 194
Sheppard, J.M. See Nimmo, D.R., 405; 427 Sloan, N.A., 442, 460, 495; 591
Shigesada, N., 126; 166 Sloane, J.F. See Kitching, J.A., 533; 586
Shiozawa, T., 178; 193 Sloane Stanley, G.H. See Folch, J., 212,
See Hirata, S., 178; 190 247; 261
See Hoshika, A., 178; 190 Slobodkin, L.B., 109, 111, 119; 123
Shimura, S., 59, 60; 97 See Kierstead, H., 109, 110, 114, 152;
Shinn, E.A., 207; 210 122, 163
See Hudson, J.H., 195, 208; 209 See Lopez, G.R., 547; 587
See Thompson, Jr, J.H., 196, 207; 210 Smayda, T.J., 130; 167
Shipley, A.E., 345, 386; 392 See Durbin, E.G., 89; 96
Sholkovtiz, E.R., 175, 178; 193 Smethie, W.M. See Murray, J.W., 173; 192
See Krom, M.D., 173; 191 Smirnova, G.A. See El-Bastavizi, A.M.,
Short, K.S. See Quinn, W.H., 157; 166 213; 261
Sides, E. See Woodley, J.D., 168 Smith, C.L., 521, 522, 524, 525, 534; 591
Siebenaller, J.F. See Koehn, R.K., 281, 282; Smith, F. See Dubois, M., 340
309 Smith, G.J. See Porter, J.W., 589
Siegel-Causey, D. See Whittam, T.S., 515; Smith, G.M. See Lyons, W.B., 191
593 Smith, I.R., 106; 123
Siegfried, C.A., 407; 427 Smith, M.M. See Walker, F.T., 487; 592
Siewing, R., 415; 427 Smith, N.S. See Estes, J.A., 489; 584
Sigleo, A.C., 178; 193 Smith, P. See Knox, R.B., 341
Silberhorn, G.M., 317, 318, 319; 342 Smith, P.A., 184, 185; 193
Silverberg, N. See Sundby, B., 176, 181; Smith, P.C., 154, 155; 167
194 See Petrie, B., 155; 165
Silvert, W., 77; 97 Smith, R.C., 59, 132; 97, 167
Simberloff, D. See Connor, E.F., 515; 583 See Baker, K.S., 62; 96
Simon, J.L. See Dauer, D.M., 493, 568; Smith, R.E. See Dolbeare, F.A., 84; 96
583 Smith, R.L., 144, 150; 167
Simpson, J.H., 15, 103, 105, 107, 108, 117, See Barber, R.J., 149, 150; 160
118, 146, 147; 53, 166, 167 See Collins, C.A., 161
See Allen, C.M., 146; 160 See Huyer, A., 156; 163
See Swallow, J.C., 142; 167 See Mooers, C.N., 132, 143; 164
Simpson, J.H.S. See Swallow, J.C., 118;
123 Smith, S.D., 38; 53
Simpson, J.W., 287; 312 Smith, S.L., 156; 167
Singarajah, K.V., 346; 392
AUTHOR INDEX 659
See Boucher, J., 278; 306 See Ryland, J.S., 444; 590
Smith, S.V. See Buddemeier, R.W., 198; Steele, A.K. See Jefferies, D.F., 33; 52
209 See Kautsky, H., 12, 33; 52
See Schneider, R.C., 202; 210 Steele, D.H., 394, 402, 403, 409, 414, 415,
Smith, T.J., 11; 53 416, 417; 428
See Williams, S.J., 13; 53 Steele, J.H., 59, 102, 105, 108, 115, 117,
Snyder, H.A. See Snyder, N.F.R., 444; 591 128, 129, 136; 97, 167
Snyder, N.F.R., 444; 591 See Goldberg, E.D., 117; 121
Snyder, T.P ., 280; 312 Steele, V.J. See Steele, D.H., 394, 402, 403,
Sobey, E.J. See Huyer, A., 156; 163 409, 414, 415, 416, 417; 428
Sokolov, V.S. See Volkov, I. I., 179; 194 Steemann Nielsen, E., 207; 210
Soling, H.D., 269; 312 Stegeman, J. See Lee, R.F., 309
Soltitskaya, L. See Plisetskaya, E., 268; Steinberg, R.A., 279; 312
311 Steneck, R.S., 474, 488, 533, 553; 591
Somero, G.N., 277; 312 Stephen, D., 294; 312
See Felbeck, H., 184; 189 Stephens, G.C. See Van Pilsum, J.F., 274;
See Hochachka, P.W., 274, 277, 282, 312
402; 309, 426 Stephens, C.V. See Davies, A.M., 23; 51
See Walsh, P.J., 280, 281, 284; 313 Stephens, J.S., 523; 591
Sousa, W.P., 486, 488, 489, 533, 538, 539, Stephenson, W., 488, 534; 591
542, 543; 591 Stern, C. See Bonatti, E., 183; 187
Soutar, A., 131; 167 Steuer, A., 345; 392
Southward, A.J., 157; 167 Stevenson, M.R., 144; 167
See Russell, F.S., 157; 166 See Brink, K.H., 161
Sozanski, A.G., 174; 193 See Collins, C.A. 161
Spencer, D.W., 176, 177; 193 Stewart, E.A. See Breen, P.A., 534; 582
See Bacon, M.P., 186 Stewart, J.G., 330, 331; 342
See Bender, M.L., 172, 177, 183; 187 Stewart, R.H. See Glynn, P.W., 534; 584
See Brewer, P.G., 172, 176; 188 Stimson, J., 434, 437, 440, 441, 469, 470,
Spencer, R. See Cartwright, D.E., 24; 51 488, 562, 563; 591
Spero, H., 356; 392 Stoecker, D., 479, 564; 591
Spiess, E., 402; 428 Stoffers, P. See Förstner, U., 180; 189
Spiess, L.D. See Spiess, E., 402; 428 Stokes, T.M., 287; 312
Spight, T.M., 463, 508, 527; 591 Stommel, H., 185; 193
Spinrad, R.W., 60, 70, 71; 97 Stone, D.B., 269, 270; 312
See Yentsch, C.M., 97 Stone, J.H., 363, 384, 512; 392, 591
Sreekumaran, C., 200, 202; 210 Storey, K.B., 270, 273, 274, 275; 312
Stakes, D. See Leinen, M., 179; 191 See Guderley, H.E., 271; 308
Stanley, S.M., 565, 566, 567; 591 Storm, B. See Hovis, W.A., 96
See Newman, W.A., 566; 588 Stovall, J.B., 351, 352; 392
Start, C. See Newsholme, E.A., 266, 267, Strathmann, R.R., 402; 428
272; 310 Strickland, J.D.H., 66; 97
Staudigel, H., 183; 193 See Eppley, R.W., 141; 162
Stavn, R.H., 138; 167 Strickler, J.R. See Koehl, M.A.R., 159, 160;
Stead, A.D., 339; 342 164
See Roberts, I.N., 339; 342 Stride, A.H. See Belderson, R.H., 27; 51
Stebbing, A.R.D., 264, 265, 266, 440, 441, Striven, A.E., 436, 490; 591
480; 312, 591 Stuart, D.W. See Brink, K.H., 161
Studholme, A.L. See Olla, B.L., 298; 311 Szyper, J.P., 363, 364, 365, 366, 368, 370,
Suchanek, T.H., 476, 506, 530, 563, 568; 371, 373, 374, 375, 377, 378, 379, 381,
591 383, 387; 392
See Levinton, J.S., 280; 310
Suelter, C.H. See Pierce, J., 259; 261 Tabata, S., 156; 167
Suess, E., 170; 193 Tager, J.M. See Groen, A.K., 308
See Müller, P.J., 170; 192 Takahasti, M. See Parsons, T.R., 125, 135;
Suhayda, J.N. See Roberts, H.H., 152; 166 165
Sullivan, B. See Mangum, C.P., 310 Takematsu, N., 169, 170, 180, 182; 194
See Weber, R.E., 288; 313 Takimura, O. See Hirata, S., 178; 190
Sullivan, B.K., 358, 359, 363, 364, 367, See Hoshika, A., 178; 190
370, 374, 375, 377, 381, 382, 383, 386, See Shiozawa, T., 178; 193
Fig. 15 (Feigenbaum & Maris) facing p. Talbot, F.H., 522, 523, 524, 525, 541; 592
359; 392 See Anderson, G.s.V., 580
See Gentile, J.H., 398, 406, 412; 426 See Bohnsack, J.A., 523, 541; 581
Sullivan, G.G. See Shepard, F.P., 152; 166 See Collette, B.B., 454, 518; 582
Summerhayes, C.P. See Tooms, J.S., 171; See Russell, B.C., 580
194 Talbot, M.S. See Brown, A.C., 407, 412;
Summons, R.E. See Benson, A.A., 199; 425
205 Tande, K. See Hopkins, C.C.E., 261
Sun, S.-S. See Bender, M.L., 187 Tande, K.S., 278; 312
Sunda, W.G., 173; 193 Tanimoto, T. See Shiozawa, T., 178; 193
Sundby, B., 176, 177, 181; 193, 194 Tarver, H. See Debro, J.R., 253; 261
See Yeats, P.A., 176; 194 Tattersall, O.S. See Tattersall, W.M., 411;
428
Surholt, B., 274, 291, 292; 312 Tattersall, W.M., 411; 428
Sutcliffe, W.H., 137, 156; 167 Taylor, C.M. See Ebling, F.J., 536; 583
See Sheldon, R.W., 128, 129; 166 Taylor, D. See Riley, J.P., 171, 172; 193
Sutcliffe, Jr, W.H. See Sheldon, R.W., 77; See Van Pilsum, J.F., 274; 312
97 Taylor, D.L., 206; 210
Sutherland, J.P., 434, 532, 534, 542, 543; Taylor, F.J.R. See Evans, G.T., 138; 162
591, 592 Taylor, G.I., 23; 53
See Menge, B.A., 534, 536; 588 Taylor, J.D., 461; 592
Sutton, L. See Ross, D.M., 509; 590 Taylor, P.R., 531, 538; 592
Svedelius, N., 327, 328, 334; 342 Tebro, B.M. See Emerson, S., 189
Sverdrup, H.U., 100, 101, 106, 111, 135; Tee, K.T., 31, 151, 153; 53, 167
123, 167 Tegner, M.J., 442; 592
Swallow, J.C., 118, 142; 123, 167 Tenore, K.R., 490; 592
Swart, P.K., 200, 202; 210 See Lee, R.F., 278; 310
Sweatman, H.P.A. See Robertson, D.R., Teraoka, H., 178; 194
564; 590 Termaat, R.M. See Bak, R.P.M., 465; 580
Sweeney, B.M. See Hastings, J.W., 77; 96 Terazaki, M., 369; 392
Sweet, R.G. See Bonner, W.A., 87; 96 Terwilliger, R.C. See Garlick, R.L., 287;
Swift, E., 75; 97 308
Szmant-Froelich, A. See Dodge, R.E., 195, Tett, P., 99–123; 104, 108, 118; 123
208; 209 See Jones, K.J., 122
Szyper, J. See Bienfang, P., 108; 121 Tett, P.B., 75; 97
AUTHOR INDEX 661
See Simpson, J.H., 123, 166 Tracy, N.L., 280; 312

Thannhauser, S.J. See Schmidt, G., 259; Traganza, E.D., 61, 155; 97, 167
261 Travis, D.F., 293; 312
Thébault, M.-T., 277; 312
Theede, H., 288, 289, 290; 312 Trefry, J.H., 177, 181; 194
Theilacker, G.H. See Clutter, R.I., 398, 419, Trellu, J., 277; 312
423; 426 Trendall, J.T. See Black, R., 442; 581
Theobald, P.K. See Chao, T.T., 174; 188 Trevallion, A. See Ansell, A.D., 294; 305
Thijssen, T. See Glasby, G.P., 169, 182; Truax, D. See Borstad, G.A., 161
190 Truesdale, V.W. See Elderfield, H., 189
Thistle, D., 492, 493; 592 Tsuchiya, M., 506; 592
Thomas, R.E. See Tillery, J.B., 196; 210 Tsuda, R.T., 522; 592
Thompson, G. See Livingston, H.O., 195, Tsuda, T. See Matsudaira, C., 398; 427
196, 198, 200, 201, 202, 204, 205; 209 Tsunogai, S., 173, 178, 182; 194
Thompson, J.A., 207; 210 See Uematsu, M., 178; 194
Thompson, J.D., 144; 167 Tully, J.P., 133; 167
See O’Brien, J.J., 164 Tunnicliffe, V., 152, 546; 167, 592
Thompson, Jr, J.H., 196, 207; 210 See Woodley, J.D., 168
Thompson, K.R., 49; 53 Turano, F.J. See Lassen, H.H., 280; 309
Thompson, R.J. See Ebberink, R.H.M., Turekian, K.K., 172, 179, 181; 194
269; 307 See Quinby-Hunt, M.S., 172; 193
See Livingstone, D.R., 274; 310 See Veeh. H.H., 195, 200, 202, 204,
Thompson, R.O.R.Y. See Pollard, R.T., 205; 210
133; 166 Turner, D.R. See Knox, S., 178; 191
Thompson, R.T. See de Zwaan, A., 274; Turner, J.S., 138; 168
307 See Kraus, E.B., 133; 164
Thomson, J. See Cronan, D.S., 188 Turner, R.R. See Cerling, T.E., 174; 188
Thorhaug, A., 320; 342 Turpin, D.H., 128; 168
Thornton, I. See Boyden, C.R., 178; 187 Tutin, T.G., 317; 342
Thorp, J.H ., 494, 530, 562, 563; 592 Twarog, B.M., 268; 312
Thorpe, S.A., 141; 167 See Satchell, D.G., 268; 312
Thorson, G., 416; 428 Tyler, J.C. See Smith, C.L., 521, 534; 591
Thresher, I.E., 519; 592 Tyler, M.A., 141, 148; 168
Thresher, R.E. See Myrberg, A.A., 520,
521, 563; 588 Uematsu, M., 178; 194
Thurberg, F.P. See Vernberg, F.J., 265; 312 See Tsunogai, S., 178; 194
Tillery, J.B., 196; 210 Ulanowicz, R.E. See Platt, T., 117, 211;
Tilman, D., 128; 167 123, 261
Tipping, E., 169, 176; 194 Ulmer, K.M. See Grant, W.C., 508, 510;
Titman, D., 485; 592 585
Tokioka, T., 356, 369; 392 Umbarger, H.E., 271; 312
Tomczak, M. See Boje, R., 149; 161 Underhill, L. See Hockey, P.A.R., 455; 586
Tomlinson, P.B., 320; 342 See Sharp, J.H., 587; 591
Tont, S.A., 155, 156, 157; 167 Underwood, A.H., 268; 312
Tooms, J.S., 171; 194 Underwood, A.J., 402, 434, 435, 436, 447,
See Bignell, R.D., 184; 187 469, 472, 478, 487, 526, 531, 541, 543,
Toth, J.R., 183; 194 544, 556; 428, 592
Toulmond, A. See Pionetti, J.-M., 264; 311
See Creese, R.G., 469, 527; 583 Verity, P.J. See Swift, E., 75; 97
See Denley, E.J., 478; 583 Vermeij, G.J., 446, 447; 592
See Mackay, D.A., 443; 587 Vernberg, F.J., 265, 300, 303; 312
Ursin, E. See Anderson, K.P., 517; 580 See Vernberg, W.B., 402; 428
Uthe, J.F. See Lee, R.F., 309 Vernberg, W.B., 402; 428
Uyeda, K. See Kono, N., 269; 309 See Vernberg, F.J., 265, 300, 303; 312
Vidal, J. See Harrison, W.G., 122
Vadas, R.L., 489, 553; 592 Vijverberg, P. See Bremer, P., 418; 425
See Gagnon, P.S., 318; 340 Vine, P.J., 466; 592
See Larson, B.R., 553; 587 Virnstein, R.W., 507; 592
See Paine, R.T., 471, 488, 534; 589 See Boesch, D.F., 493; 581
Vahl, O. See Eliassen, J.-E., 239; 261 Vivas, A.M. See Gaines, M.S., 280; 308
See Ockelmann, K.W., 295; 311 Vlasblom, A.G., 399, 400, 405; 428
Valderhaug, V.A. See Berge, J.A., 507; 581 Vogt, P.R. See Moore, W.S., 183; 192
Valentine, J.W., 131, 571, 572, 573; 168, Volkov, I.I., 179; 194
592 von Boletzky, S. See Ross, D.M., 509; 590
See Ayala, F.J., 293, 569, 571; 305, 580 Von Brand, T., 286; 312
X Von Damm, K. See Edmond, J.M., 183;
van Andel, Tj. H. See Corliss, J.B., 188 189
Van Blaricom, G.R., 493, 545; 592 Von Damm, K.L. See Edmond, J.M., 184;
Vance, R.R., 402, 477, 508, 509, 510, 511; 189
428, 592 von Herzen, R.P. See Corliss, J.B., 188
Van de Hulst, H.G., 64, 66; 97 See Honnorez, J., 190
Van den Berghe, W., 501; 592 Voorhis, A.D., 143, 154; 168
van der Meer, R. See Groen, A.K., 308
van Det, M. See Fournier, R.O., 143; 162 Wadley, V.A. See Ivanovici, A.M., 264;
van de Weijden, C.H., 178; 194 309
van Grieken, R. See Sholkovitz, E.R., 178; Wahle, C. See Woodley, J.D., 168
193 Wahle, C.M., 466; 592
Van Kley, H., 258, 259; 261 Wainwright, S.A., 199, 203, 205; 210
Van Leer, J.C. See Brink, K.H., 161 Wakefield, S.J., 180; 194
Vannini, M., 443, 451; 592 See Elderfield, H., 183; 189
Van Noorden, S. See Fritsch, H.A.R., 268; Waldichuck, M., 263; 313
308 Walker, F.T., 487; 592
Van Pilsum, J.F., 274; 312 Walker, J. See Gentile, S.M., 412; 426
Van-Praet, M., 198; 210 Walker, M.G. See Harden-Jones, F.R., 32;
Van Schaftingen, E., 269; 312 51
Van Valin, R., 180; 194 Walker, P.W. See McGowan, J.A., 514;
Van Winkle, W., 156; 168 588
See Mangum, C.P., 287; 310 Walsby, A.E., 109; 123
Varentsov, I.M., 170; 194 Walsby, A.F., 130; 168
Varnavas, S.P., 183, 184; 194 Walsh, J.J., 118; 123
Vassie, J.M. See Cartwright, D.E., 24; 51 See Coachman, L.K., 143; 161
Vastano, A. See Spero, H., 356; 392 See Cushing, D.H., 127; 161
Veeh, H.H., 195, 200, 202, 204, 205; 210 Walsh, P.J., 125, 127, 131, 136, 150, 151,
See McMurtry, G.M., 183; 192 280, 281, 284; 168, 313
Velimirov, B., 487; 592
AUTHOR INDEX 663
Walter, M.A. See Reeve, M.R., 343, 348, Wells, A.F., 199; 210
349, 358, 361, 364, 365, 366, 368, 374, Wells, F.E., 527; 592
377, 388; 392 Wells, R.M.G., 288; 313
Walter, M.D., 454; 592 See Warren, L.M., 288; 313
Walton, G.M. See Atkinson, D.E., 272; 305 Welsh, B.L., 547; 592
See Shen, L.C., 273; 312 Weltner, W. See Samter, M., 399, 401,
Walton, W. See Johns, D.M., 406; 426 410; 427
Wanders, R.J.A. See Groen, A.K., 308 Werner, E.E., 527, 554, 555; 592
Wangersky, B.J., 179; 194 West, B. See Parker, M., 407; 427
Ward, B.B., 83; 97 Westerhoff, H.V. See Groen, A.K., 308
Warren, B.A., 127; 168 Westfall, J.A. See Eakin, R.M., 346, 354;
Warren, L.M., 287, 288; 313 390
See Dales, R.P., 287; 307 Wethey, D.S., 468; 592
Warren, L.M. See Wells, R.M.G., 288; 313 Wheeless, Jr, L.L. See Horan, P.K., 82; 96
Warwick, R.M., 454, 476, 490, 501, 507, White, F.P. See Currie, R.W., 278; 307
547; 592 Whitfield, M. See Knox, S., 191
See Joint, I.R., 505; 586 Whitlatch, R.B., 453, 454, 490, 493, 495,
Wass, R.C. See Brock, R.E., 524; 582 496; 592
Waterbury, J.B., 68; 97 Whitledge, T.E., 159; 168
Watson, N.H.E. See Carpenter, G.F., 410; See Iverson, R.L., 143; 163
426 See Malone, T.C., 164
Watson, S.W. See Waterbury, J.B., 68; 97 See Walsh, J.J., 168
Watts, D.G. See Jenkins, G.M., 113; 122 Whittaker, R.H., 119, 409; 123, 428
Wear, R.G., 394, 402, 414; 428 Whittam, T.S., 515; 593
Webb, D.C. See Voorhis, A.D., 143, 154; Whittle, K. See Sargent, J.R., 235, 239,
168 246; 261
Webb, S., 195; 210 Whittle, M.A. See Gabbott, P.A., 268, 294;
Weber, R.E., 288; 313 308
See Warren, L.M., 288; 313 Whritner, R. See Bernstein, R.L., 154; 161
Wedepohl, K.H., 171, 177, 179, 181, 182, Widdows, J., 264, 302, 303; 313
183; 194 See Bayne, B.L., 264, 303; 306
Weeda, E. See Gade, G., 274; 308 See Moore, M.N., 310
Weidemann, M.J., 269; 313 Wiebe, P.H., 128; 168
Weiler, R.R., 175; 194 See Haury, L.R., 91; 96
Weinberg, J.R., 492; 592 Wiens, J.A., 128, 430, 531, 559; 168, 593
Weinhausen, G. See Schöttler, U., 287, 299; Wigley, R.L., 410; 428
312 Wigsman, T.C.M., 274, 291, 292; 313
Weiser, W., 271; 313 See Ebberink, R.H.M., 274; 307
Weiss, F.T. See Monaghan, P.H., 197, 207; Wilfert, M., 205; 210
209 Wilke, R.J., 178; 194
Weiss, R.F., 184; 194 Wilkins, N.P., 568, 570; 593
See Klinnhammer, G.P., 184; 191 See Gosling, E.M., 280; 305
See Lupton, J.E., 191 Willason, S.W., 494, 563; 593
Wellershaus, G. See Duinker, J.C., 178; Williams, A.H., 519, 520, 523, 538, 562;
189 593
Wellington, G.M., 466, 468, 532, 533; 592 See Sammarco, P.W., 531; 590
See Glynn, P.W., 534; 584 Williams, B.E. See Bernstein, B.B., 534;
Wellington, W., 465; 592 581
Williams, B.R.H. See Perkins, E.J., 32; 53 Wolf, K.H., 195; 210
Williams, D. See Corliss, J.B., 188 Wolfe, D.A., 178; 194
Williams, D.McB., 523, 524, 541; 593 See Evans, D.W., 177; 189
See Sale, P.F., 522; 590 Wollast, R., 178; 194
Williams, E.O., 443, 465, 563; 593 See Duinker, J.C., 178; 189
Williams, J., 65; 97 Wood, M. See Yentsch, C.M., 97
Williams, P.J.L., 116; 123 Wood, V., 480; 593
Woodcock, A.H. See Faller, A.J., 137; 162
Williams, P.J.leB. See Derenbach, J.B., 89; Woodin, B.R. See Mangum, C.P., 310
96 Woodin, S.A., 490, 494, 506, 507, 532,
See Moore, R.M., 178; 192 542; 593
Williams, P.T. See Elderfield., 183; 189 Woodley, J.D., 153; 168
Williams, S.J., 13; 53 See Porter, J.W., 589
Williamson, D.I., 32, 36, 44; 53 Woods, J.D., 106, 109, 119; 123
See Khan, M.A., 32, 36; 52 Woof, C. See Davison, W., 175; 188
Wilms, R., 351, 352; 392 Wool, D. See Nevo, E., 282; 310
Wilson, E.A. See Brown, W.L., 456; 582 Wright, H.O., 509, 532; 593
Wilson, J.B., 442; 593 Wright, W.G., 564; 593
Wilson, J.S. See Fournier, R.O., 143; 162 Wright, W.R., 142; 168
Wilson, K.M. See Lyons, W.B., 191 Wrigley, R.C. See Hovis, W.A., 96
Wilson, T.R.W., 14, 32; 53 Wroblewski, J.S., 110, 144, 145, 150, 156;
Wilson, W.H., 492, 506; 593 123, 168
See Hovis, W.A., 96 See O’Brien, J.J., 105, 137, 160; 122,
Wimpenny, R.S., 346, 361, 378, 383; 392 165
Winant, C.D., 28, 139; 53, 168 Wulff, J. See Woodley, J.D., 168
Winberg, G.G., 400; 428 Wunsch, C., 138; 168
Wing, A. See Backus, R.H., 75; 96 See Cacchione, D., 139; 161
Winter, C.K. See Cann, J.R., 183; 188 See Warren, B.A., 127; 168
Winter, D.F., 137; 168 Wyatt, B. See Stevenson, M.R., 144; 167
See Jamart, B.M., 105; 122 Wyatt, T., 111; 123
Winterhalter, B., 174; 194 Wyrtki, K., 157; 168
Wirick, C.D. See Falkowski, P.G., 135; 162
See Walsh, J.J., 168 Yamada, M. See Tsunogai, S., 182; 194
Wirick, C.D. See Whitledge, T.E., 159; 168 Yamashita, T., 330, 331; 342
Wirsen, C.O. See Jannasch, H.W., 184; 190 Yanchinski, S., 195; 210
See Karl, D.M., 184; 190 Yarbrough, J.D. See Chambers, J.E., 307
Wisely, B., 439; 593 Yates, R.A., 271; 313
Wittman, K.J., 393–428; 394, 395, 398, Yearn, K.W., 178; 194
400, 403, 406, 407, 408, 409, 411, 412, Yeats, P.A., 176, 178; 194
414, 415, 417, 419, 423, 425; 428 See Bewers, J.M., 172; 187
Wium-Anderson, S. See Steemann See Campbell, J.A., 173; 188
Nielson, E., 207; 210 Yentsch, C.M., 55–98; 84; 97, 98
Wobber, D.R., 460; 593 See Yentsch, C.S., 66; 98
Woernle, C.H. See Horne, R.A., 175; 190 Yentsch, C.S., 59, 60, 62, 66, 68, 82, 91; 98
Wolcott, T.G., 568; 593 See Backus, R.H., 75; 96
Wolery, T.J., 183; 194 See Hovis, W.A., 96
Wolf, J. See Prandle, D., 22; 53 See Moreth, C.M., 62; 97
AUTHOR INDEX 665
See Yentsch, C.M., 55–98; 98 See Kluytmans, J.H., 294; 309

Yeow, Y.M. See Jermyn, M.A., 327; 341 See Zandee, D.I., 294; 309
Yodzis, P., 431, 478, 521, 556, 558; 593 Zuta. S., 144; 168
Yonemaru, I. See Tsunogai, S., 173; 194
Yoshioka, S. See Kitano, Y., 203; 209
Young, D.K., 492, 506, 507; 593
See Rhoads, D.C., 506, 542; 589
Young, M.L. See Moore, R.M., 178; 192
Young, M.W. See Young, D.K., 492, 506,
507; 593
Young, P.C. See Bradbury, R.H., 468; 581
Young, S.D., 203, 205; 210
Young, W.R., 152; 168
Zaba, B.N., 294; 313

Zahuranec, B.J. See Yentsch, C.M., 97
Zammit, V.A., 269, 275, 298; 313
See Alp, P.R., 299; 305
Zandee, D.I., 294; 313
See Ebberink, R.H.M., 268; 307
See Kluytmans, J.H., 294; 309
See de Zwaan, A., 287, 294; 307
Zanevald, J.R.V. See Spinrad, R.W., 70; 97
Zar, J.H., 218; 261
Zaret, T.M., 545; 593
Zatkutskiy, V.P., 411; 428
Zebe, E., 286, 287, 289; 313
Zedler, J.B. See Emerson, S.E., 486, 568;
584
Zeemann, E.C., 118; 123
Zeitlin, H. See Boyland, D.B., 198; 209
Zeitoun, M.A., 196, 206; 210

Zentara, S.J. See Kamykowski, D., 141;
163
Zerba, K.E. See Stephens, J.S., 523; 591
Zerbi, M. See Bonatti, E., 185; 187
Zieman, J.C., 195; 210
Zillioux, E.J. See McLaren, I.A., 394, 414;
427
Zimmerman, J.T., 152; 168
Zimmerman, J.T.F., 31; 53
Zopf, D.O. See Quinn, W.H., 157; 166
Zucker, N., 449; 593
Zurburg, W. 287; 313
See de Zwaan, A., 276; 307
See Ebberink, R.H.M., 269, 273; 307
SYSTEMATIC INDEX
References to complete articles are given in heavy type

Abarenicola, 546, 547 Agonus cataphractus, 519
„ pacifica, 496, 546 Alaria fistula, 486
„ vagabunda, 496 Alcidae, 514
Acanthaster, 535, 536 Alcyonium siderium, 482
Acanthina, 548, 549, 551 Alonella, 513, 514
„ punctulata, 453, 548 Alphaeus, 451
Acanthohaustorius, 503 Amaurobioides, 464
„ millsi. 502, 503 „ africanus, 464
Acanthomysis longicornis, 404 Amphibolis, 330, 331, 332, 333, 335
„ sculpta, 396, 398 antarctica, 330, 331, 332, 333, 334,
Acartia, 367 335, 337, Figs 4, 7 and 10 (Pettitt)
„ tonsa, 372 between pp. 334 and 335
Acmaea, 469, 470, 471, 570 griffithii, 331, 332, 333, 334
„ (Collisella) digitalis, 471 Amphipoda, 394, 402, 414, 415, 418, 423
„ „ paradigitalis, 471 Amphiprion, 437
Acmaea digitalis, 445, 446, 469, 568, 570, Amphitrite johnstoni, 294
571 Anodonta cygnea, 268
„ mitra, 544 Antarctomysis maxima, 410
„ paradigitalis, 471, 568 Anthias squamipinnis, 438
„ scabra, 469, 570, 571 Anthopleura, 443, 544
Acromonas, 545 „ elegantissima, 443, 531
Acropora, 203, 205, 466, 520 „ xanthogrammica, 544
„ cervicornis, 206, 207 Antropora, 482
„ hyacinthus, 465 Aplidium pallidum, 482
„ palifera, 468 Arbacia, 533
Acroporidae, 200, 203, 467 Arctonoe pulchra, 443
Actinia equina, 198, 443 Arenicola, 291, 506
Agaricia, 205 „ marina, 274, 288, 290, 291, 292 294
„ agaricites, 207, 442 „ pacifica, 506
Agariciidae, 467 Artemia, 345, 348, 364, 367, 377, 379, 381
Agarum, 486, 488 384, 406
666
„ salina, 278, 279 „ californiensis, 289, 490, 491

Ascaris suum, 269 Calliopiella michaelseni, 443
Ascophyllum nodosum, 485, 486, 487, 488 Cancer, 494
Asellus aquaticus, 396 „ irroratus, 509
Asterias, 460 Capitella, 283, 296
„ rubens, 460 „ capitata, 283, 284, 288, 290, 296, 297,
Asterionella, 485 298, 299, 302, 492
„ formosa, 485 Caranx ignobilis, 450
Astrangia, 205 Carcinus maenas, 288, 289, 443, 451, 488,
Astrocoeniidae, 467 534, 553, 554
Astropecten, 458, 529, 530, 560 Cardium edule, 288, 289
„ aranciacus, 456, 457 Caryophyllidae, 467
„ bispinosus, 456, 457 Cellana, 469, 472, 543
Aulacomya ater, 547 „ capensis, 469, 471
Axiothella, 492 „ tramoserica, 435, 443, 469, 471, 472,
„ rubrocincta, 492 478, 526, 527, 530, 543, 544, 563
Celloporaria, 546
Balanus, 484 „ brunnea, 546
„ balanoides, 289, 294, 402, 409, 439 440, Centrostephanus, 471
476, 483, 484, 566, 567 Ceratium, 157
„ balanus, 294 Ceriodaphnia, 513, 514
„ cariosus, 548, 549, 553 Chaetognatha, 343–392; 343, 349, 355
„ glandula, 484, 548, 549, 553 Chama, 478
Bathyporeia, 503 „ pellucida, 478
Bembicium auratum, 436, 444 Chamaesipho brunnea, 476
„ nanum, 469, 526 Chaoborus, 367
Boreomysis arctica, 398 Charidrius marginatus, 515, 516
Botryllus schlosseri, 444 Chione undatella, 504
Bryozoa, 439, 478 Chondrus, 486, 488
Bugula simplex, 546 „ crispus, 486, 487, 488
„ turrita, 480, 546 Chthamalus, 476, 566, 567
Burnupena, 448 „ dalli, 484
Busycon, 464 „ fissus, 548
„ contrarium, 463, 464, 560 „ stellatus, 476, 565, 567
„ spiratum, 463, 464, 560 Cladocera, 357
Clathromorphum, 488
Calanus, 367 Clibanarius, 511, 532
„ finmarchicus, 278 „ albidigitus, 510
„ marshallae, 144 „ tibicen, 509
Calcinus, 511 „ tricolor, 509
„ obscurus, 510 „ vittatus, 509
Calidris alba, 515, 516 Cloridopsis scorpio, 494
Callapa flammea, 509 Clupea harengus, 517
Calliactis, 509 Clymenella torquata, 505
„ parasitica, 509 „ zonalis, 505
„ tricolor, 509 Codium, 486
Callianassa, 492, 506 „ dimorphum, 486
„ fragile, 567
„ tomentosum, 567 Drosophila, 402

Coelentrata, 280 Dunaliella tertriolecta, 90
Coenobita compressus, 452 Dynamena, 396
Collisella digitalis, 471, 472
„ pelta, 471 Echinocardium cordatum, 456, 457
„ strigatella, 471 Echinodermata, 280
Colpomenia peregrina, 566 Echinometra, 538
Conus, 444, 446, 453, 460, 461, 462, 463, „ mathaei, 442, 472, 473
474, 527, 530, 550, 551, 552, 559, 560, „ oblongata, 472, 473
575 „ viridis, 538
„ abbreviatus, 460 Ecklonia, 438
„ californicus, 461 „ radiata, 438
„ ebraeus, 453, 461 Egregia, 570
„ miliaris, 461, 559, 560, 575 „ laevigata, 438
Conus, sponsalis, 460 Elminius, 567
Copepoda, 372, 384, 400, 401 „ modestus, 567
Corophium, 496, 497 Embiotica jacksoni, 519, 520
„ volutator, 496, 497 „ lateralis, 519, 520
Crangon crangon, 288, 289 Engraulis capensis, 517
Crassostrea virginica, 270, 275 „ mordax, 137, 517
Crepidula convexa, 548 Enhalus, 325, 328
„ fornicata, 567 „ acoroides, 327, 334
Crossaster papposus, 460 Enhydrosoma, 501
Crustacea, 393–428; 146, 280, 289, 293, Enteromorpha, 488, 534
294, 295, 298, 396, 397 „ intestinalis, 487
Cyclotella, 485 Erichthonius braziliensis, 437, 449
„ meneghiniana, 485 Euchaeta norvegica, 295
Cymodocaceae, 329, 330, 334, 335 Eucyrtidium, 530
Cymodocea rotundata, 322, 324 „ calvertense, 529
„ serrulata, 322, 323, 324 „ matuyamai, 529
Cyprina islandica, 288, 289 Eukrohnia, 354, 359
„ bathypelagica, 346
Daphnia, 514 „ fowleri, 346, 354, 369
Dardanus arrosor, 509 „ hamata, 359, 362, 366, 367, 369, 374,
„ gemmatus, 509 375, 382, 383, 388 Fig. 15 (Feyenbaum
Dendraster, 492 & Maris) facing p. 359
„ excentricus, 442 Eunicea tourneforti, 204
Desis, 464 Euphausia, 571
„ formidabilis, 464 „ pacifica, 155
Diadema, 538 Eupomacentrus acapulcoensis, 466
„ antillarum, 538 „ apicalis, 520
Diamysis bahirensis, 398, 404, 419 „ leucosticus, 520, 521
Didemnum, 480 „ planifrons, 520, 521, 524, 538
Diopatra cuprea, 507 Evechinus chloroticus, 544
Diploria, 204 Exosphaeroma, 503
Domecia, 465 „ amplicauda, 502, 504
Donax vittatus, 297
Fasciola hepatica, 269 Haloclava producta, 289

Fovia, 205 Halodule, 330, 331
„ fragrum, 442 „ pinifolia, 330
Faviidae, 200, 203, 467 „ uninervis, 324, 330
Fritillaria, 375 „ wrightii, 321, 322
Fucus, 486, 488 Halophila, 328, 329
„ serratus, 480, 481, 485, 486 „ decipiens, 332, 334
„ spiralis, 485, 486 „ engelmanni, 321, 322
„ vesciculosus, 485, 486 „ ovalis, 324
Fundulus, 494 „ ovata, 328
Fungia, 205 „ stipulacea, 323, 328, 329, 332
Fungiidae, 200 Haptosquilla, 494
„ glyptocercus, 494
Gadus morhua, 239, 519 Haustorius, 503
Galeolaria, 478 „ canadensis, 502, 503
Gambusia, 513 Hedophyllum, 486
Gammarus, 394, 396, 402 „ sessile, 486
Gastrosaccus lobatus 398, 404 Helix pomatia, 271
„ psammodytes, 407, 412 Hemigrapsus, 494
„ vulgaris, 398, 419 „ nudus, 295
Gigartina, 489 „ oregonensis, 494
„ canaliculata, 489, 543 Hemimysis speluncola, 395, 398, 404
„ stellata, 487 Herpolitha, 205
Glycera, 295 Heterozostera tasmanica, 332, 333, 334,
„ alba, 270, 283, 284, 291, 295, 296, 298, 335, 339
299, 302 Himanthalia, 487
„ americana, 288 Hippa pacifica, 446, 448
„ dibranchiata, 291 Hippopus, 199
Gnathophausia, 423 Hippothoa, 481
„ ingns, 396, 398, 405, 414, 423, 424 Hippuritacea, 565
Gnorimosphaera, 503 Hydractinia, 533
„ oregonensis, 502, 504 „ echinata, 509
Gobiosoma, 520 Hydrobia, 497, 498, 500, 501, 527, 529,
„ robustum, 510 530, 531, 546, 559, 560, 575
Gondactylus falcatus. 563, 567 „ neglecta, 498, 499, 500
„ festai, 451 „ totteni 496, 497, 500
„ incipiens, 494 „ ulvae, 496, 497, 498, 499, 500, 546
„ viridis, 450 „ ventrosa, 496, 498, 499, 500
Goniopora, 465 Hydrocharitaceae, 325, 328, 334, 335
Gymnodinium splendens, 199 Hydrodamalis gigas, 489
Gyrodinium aureolum, 118
Insecta, 367
Haematopus moquini, 455, 545 Ilyananssa, 496, 497
Haliotis, 474, 488, 548 „ obsoleta, 496
„ ruber, 471 Isopoda, 418
„ rufescens, 270
Haliplanella luciae, 288 Jasus lalandii, 453, 553
Krohnitta pacifica, 369 „ berryi, 442

Meandrenidae, 467
Laminaria, 440, 441, 486, 487, 488 Meganyctiphanes norvegica, 295
„ hyperborea, 487 Melinna cristata, 295
„ longipes, 486 „ palmata, 294, 295, 296, 298, 299
„ pallida, 487 Membranipora, 444, 481
Lepidactylus dytiscus, 502, 503 Mesodinium rubrum, 144
Lepomis cyanellus, 554 Mesopodopsis orientalis, 398, 419
„ marochirus, 554 Metamysidopsis elongata, 398, 406, 419,
Leptaslerias, 458, 459, 460, 564 423
„ hexactis, 458 „ insularis, 398, 419
Leptodora kindtii, 357 Metridium senile, 284, 443
Leptomysis bürgii, 398, 404, 407, 418, 419 Micrococcus, 545
„ gracilis, 407 Millepora, 466
„ lingvura, 394, 395, 398, 403, 404, 406, Molgula, 542
407, 408, 409, 412, 417, 419, 420, 423, Mollusca, 280
424, 425 Monodonta turbiformis, 282
Lichenopora, 481 „ turbinata, 282
Limanda limanda, 519 Montastrea, 204, 205
Limnodrilus, 545, 546 „ annularis, 203, 207, 468
„ hoffmeisteri, 545 Montipora, 203
Liothyrella, 569, 571 „ verrucosa, 206
Lithophaga, 442 Mopalia, 471
„ curta, 442 „ muscosa, 471
Lithophyllum, 454 Morula, 472, 473, 543
Littorina, 437, 478, 487, 488, 534, 570 „ marginalba, 543
„ africana knysnaensis, 446, 447, Mussidae, 467
„ littorea, 445, 446, 487 Myoxocephalus scorpius, 519
„ nigrolineata, 553 Mysidacea, 393–428; 393, 395, 396, 397,
„ planaxis, 548, 549 398, 400, 401, 402, 404, 412, 413, 414,
„ rudis, 436, 437, 553 415, 418, 421, 422, 423
„ scutulata, 548, 549 Mysidium columbiae, 398
„ unifasciata, 444, 472 Mysidopsis bahia, 398, 405, 406, 412
Lobophyllia, 205 „ bigelowi, 411
Locusta migratoria, 401, 402 „ didelphis, 410
Lophogaster, 401 Mysis litoralis, 399, 410, 416
Lottia, 469, 470, 564 „ mixta, 410
„ gigantea, 437, 469, 470, 564 „ oculata, 410
„ relicta, 399, 401, 406, 410, 418, 419, 423
Macoma, 546, 569 „ stenolepis, 399, 409, 410, 416, 423
„ balthica, 546 Mytilus, 264, 268, 274, 484, 506, 529, 542,
Macrocystis, 481, 486, 533 560
Madracis, 207 „ californianus, 270, 430, 477, 531
„ mirabilis, 207 ,, edulis, 268, 269, 272, 274, 278, 281, 282,
Majidae, 472 288, 289, 290, 291, 292, 297, 476, 477,
Mallotus villosus, 212, 224 483, 484, 531, 542, 553
Mantipora, 442
Nacella delesserti, 579 Pachygrapsus, 494

Neanthes, 506 „ crassipes, 443, 489, 494
„ arenoceodentata, 283 Pagurus, 509, 510, 511, 532
Neohaustorius schmitzi, 502, 503 „ granosimanus, 508
Neomysis, 405 „ hirsutiusculus, 508
„ americana, 395, 399, 411 „ longicarpus, 509
„ integer, 395, 399, 405, 407, 419 „ pollicaris, 509
„ intermedia, 394, 395, 399, 400, 407, 411 Palaemon elegans, 282
„ japonica, 395, 399, 407 „ floridanus, 494
„ mercedis, 407, 412 „ serratus, 277
Nephthea, 466 Palaemonetes, 547
„ brassica, 465 „ pugio, 494, 547
Nereis, 290, 291, 292, 299 „ vulgaris, 494
„ diversicolor, 288, 290, 291, 292, 294 Palola siciliensis, 454
„ jacksoni, 453, 454 Palythoa, 198
,, pelagica, 288, 290, 291, 292 Pandalus, 221, 222, 224
„ virens, 288, 290, 291, 292, 294 „ borealis, 212, 219, 221, 222, 223, 224,
Nerita, 452 229, 239, 248
„ atramentosa, 434, 469, 526 Paracalanus, 367
Nodilittorina australis, 472 Parahaustorius longimerus, 502, 503
Notoacmea petterdi, 435 Paralaeospira levinseni, 547
Nucula, 492 „ patagonica, 547
Nucula, annulata, 502 Paralithodes camtschatica, 270
„ proxima, 492, 502 Paramysis intermedia, 407
Nuttalia, 506 „ pontica, 411
„ ullskyi, 407
Octopus, 509, 510 Paraspionspio pinnata, 494
„ cyanea, 271 Parma microlepis, 520
„ joubini, 509 Patella, 443, 474, 475, 527, 530, 575, 578,
„ vulgaris, 509 579
Oculina, 205 „ aspera, 570
Oculinidae, 467 „ cochlear, 433, 434, 448, 474, 475, 530,
Oikopleura, 359, 387 579
Oithona, 361 „ compressa, 578
„ similis, Fig. 15 (Feigenbaum & Maris) Patella, concolor, 469, 471
facing p. 359 „ granatina, 446
Olivella biplicata, 445, 446 „ granularis, 445, 446, 478, 479
Oncaea, 367 „ longicosta, 437, 448, 449, 454, 474, 475,
Onchoporella, 482 488, 530, 579
Oratosquilla inornata, 494 „ tabularis, 437, 474, 579
Orchestia grillus, 547 „ vulgata, 570
Orconectes immunis, 494 Patelloida, 434, 543
„ limosus, 270, 295 „ alticostata, 434
„ virilis, 270, 494 „ latistrigata, 472, 473, 530, 543
Owenia fusiformis, 288, 289 Patiriella exigua, 469, 544, 563
Oxystele variegata, 446, 447, 448 Pavona, 466
Pectinaria gouldii, 453, 454, 496
Peloscolex, 545
„ multisetosus, 545 Pseudocalanus, 361, 384

Pelvetia, 486 Pseudomonas, 545
„ canaliculata, 485, 486 „ fluorescens, 545
Peracarida, 402, 409, 413, 418, 423 Pseudopolydora, 492, 506
Perinereis singaporiensis, 454 „ kempi, 492, 506
Perna canaliculatus, 484 „ paucibranchiata, 449, 492, 493
Phoronopsis, 569 Pseudopsida, 513, 514
Phragmatopoma californica, 531 Pseudosquilla ciliata, 563, 567
Phyllospadix torreyi, 330, 332, 334 Pterosagitta draco, 349, 355, 362, 366,
Phymactis clematis, 443 372, 375, 376, Fig. 11 (Feigenbaum &
Pileolaria, 547 Maris) facing p. 358
Pisaster, 430, 458, 459, 460, 483, 544, 564 Pterygophora, 481
„ gigantea, 478 Pycnopodia, 460, 544
„ ochraceus, 453, 458, 484, 544 „ helianthoides, 544, 545
Placopecten magellanicus, 274, 299 Pygiospio, 492, 506
Platygyra, 206 „ elegans, 492, 506
Plectroglyphidodon lachrymatus, 520
Plethodon glutinosus, 560, 561 Ralfsia, 454, 474, 475, 487
„ jordani, 560, 561 „ expansa, 448, 454, 488
Pleuronectes platessa, 519
Pocillopora, 199, 203, 205, 536 Sagitta, 345, 349, 350, 354, 355, 357, 383,
„ damicornis, 205, 206 387
„ meandrina, 440, 441 „ bipunctata, 345, 351, 362, 366
„ verrucosa, 198 „ crassa, 345, 372
Pocilloporidae, 200, 203, 467 „ elegans, 346, 347, 348, 354, 358, 359,
Polyclinum, 480 360, 361, 362, 365, 366, 367, 368, 369,
Pomacentrus albofasciatus, 520 370, 371, 372, 374, 375, 376, 378, 379,
„ lividus, 520 381, 382, 383, 384, 385, 387
„ wardi, 520, 524, 525 „ enflata, 348, 354, 355, 358, 360, 362,
Pomatoschistus minutus, 519 365, 366, 368, 369, 370, 371, 372, 374,
Pontoporeia, 506 375, 376, 379, 380, 381, 382, 384, 387
Porites, 203, 205 „ euxina, 362, 376, 386, 387
„ astreoides, 207 „ friderici, 351, 352, 362, 366, 369, 370,
„ divaricata, 207 372, Fig. 5 (Feigenbaum & Maris)
„ furcata, 207 facing p. 349
Poritidae, 200, 203, 467 „ gazellae, 362, 370, 372
Posidonia australis, 332, 333, 334, 335, „ helenae, 348
Figs 3 and 5 (Pettitt) between pp. 334 „ hexaptera, 358, 362, 366
and 335 „ hispida, 345, 346, 347, 348, 349, 354,
Posidoniaceae, 329, 331, 334, 335 355, 358, 359, 361, 365, 366, 367, 368,
Praeacanthonochus punctatus, 547 369, 370, 372, 376, 379, 380, 381, 382,
Praunus flexuosus, 395, 399, 405, 407 383, 384, 385, 387, 388, Fig. 4
„ inermis, 395, 399, 407, 419 (Feigenbaum & Maris) facing p. 348,
„ neglectus, 395, 399 Fig. 12 (Feigenbaum & Maris) facing p.
Prorocentrum mariae-lebouriae, 148 358
Protothaca, 504 „ lyra, 345, 362, 366
„ staminea, 503, 504 „ macrocephala, 369
Psetta maxima, 519
„ minima, 362, 366, 369 „ schizoptera, 346, 347, 348, 354, 357, 361,
„ nagae, 356, 362, 372, 376, 378, 382 364, 367
„ pacifica, 369 Spartina, 547
„ robusta, 362, 366 Sphaeroma, 530, 559, 560, 575
„ scrippsae, 354, 362 „ hookeri, 505
„ serratodentata, 354, 362, 366 „ rugicauda, 505
„ setosa, 345, 346, 350, 351, 354, 359, Spirorbis, 440, 441, 481
361, 362, 363, 364, 365, 366, 367, 368, „ borealis, 439
369, 370, 371, 372, 375, 376, 378, 382, „ corallinae, 440
383, 386, 387 „ pagenstecheri, 440
Sagitta, tasmanica, 354 Stichaster australis, 484
„ tenuis, 358, 362, 370, 371, 372, 376 379, Strebliospio benedicti, 492, 493
381, 387 Strongylocentrotus, 436, 488
Sagittae, 345 „ droebachiensis, 545
Sanguinolaria, 492, 503 „ franciscanus, 442, 545
„ nuttallii, 490, 491, 503 „ purpuratus, 442, 544, 545
Sardinops caerulea, 517 Styela, 532, 543
„ ocellata, 517 Symplectoteuthis oualaniensis, 270, 274
Sargassum, 438 Syringodium filiforme, 322, 323, 324
„ muticum, 566 „ isoetifolium, 323, 324
„ sinclairii, 438
Saxidomus, 503 Tagelus, 492
„ nuttalli, 503 Tegula funebralis, 446, 447, 570
Schistomysis spiritus, 399, 407, 419 Telepsavus costarum, 294
Schizoporella, 480, 532, 543, 546 Tesseropora rosea, 478, 543
Scolelepis fuliginosa, 277, 299 Tetraclitella purpurascens, 478
Scomber scomber, 517 Tetraselmis, 547
Scrupocellaria, 441 Thais, 446, 447, 463, 483, 485, 553
„ reptans, 440 „ canaliculata, 445
Scypha compressa, 480 „ emarginata, 445, 446, 453, 553
Searlesia disa, 445, 446 „ lamellosa, 445, 446, 447, 453, 463, 553
Sebastes, 520 Thalassia, 325, 328
Septifer virgatus, 477 „ hemprichii, 324, 325, 326, 327, 328, 334,
Siderasteridae, 467 Fig. 9 (Pettitt) between pp. 334 and 335
Simocephalus, 513, 514 „ testudinum, 320, 321
Siphonaria, 469, 527 Thalassodendron, 330, 331
Siriella armata, 399, 404, 419 „ ciliatum, 324, 330, 331, 334, 335
„ clausii, 404 Tigriopus japanicus, 372
„ jaltensis, 404, 409 Tisbe, 501
Skeletonema, 113, 114 Tonicella, 544
„ costatum, 112, 113 „ lineata, 488
Solenomya velum, 492 Tresus, 503
Spadella, 343, 345, 351, 352, 355, 356, „ nuttallii, 503
357, 364, 366, 367 Tridacna, 199
„ cephaloptera, 346, 347, 349, 350, 351, „ crocea, 438
355, 356, 358, 361, 364, 366, 367, 370, „ maxima, 569, 571
372, 385 Tringa totanus, 450
Trisopterus esmarkii, 517

Tubastrea, 205
Tubifex, 545, 546
„ tubifex, 211, 275, 545
Tubularia, 532, 543
Turbinaria, 205
Uca, 402, 437, 449

„ pugilator, 437, 449, 451, 452
„ pugnax, 437, 451, 452
Ulva, 489, 490, 542
Unio pictorum, 268
Upogebia puttegensis, 289
Uria aalge, 439
Urosalpinx, 444
„ cinerea, 444
Xanclea, 546
Yoldia, 492
„ limatula, 492, 502
Zostera, 330
„ capensis, 323
„ capricorni, 332, 334, 335, 339, Fig. 8
(Pettitt) between pp. 334 and 335 marina,
317, 318, 319, 320, 329, 331, 332, 335,
336, 342
„ muelleri, 332, Fig. 6 (Pettitt) between pp.
334 and 335
Zosteraceae, 329, 330, 331, 334, 335
SUBJECT INDEX
References to complete articles are given in heavy type; references to sections of

articles are given in italics; references to pages are given in normal type.
Aanderaa (RCM4) current meter, 19, 20, Alanine in corals, 204
35, 36, 41, 42, 43 Alaska, primary production, 137
Absorption of light, 58 „ sea level and steric anomales, 157
Acclimation, acclimatization and enzyme Alaskan sea-bird colonies, 515
induction, 275–280 Albumin, a natural carrier in serum, 253
Acid hydrolases in intine layer of pollen Aleutian low pressure system over
wall, 315 northeast Pacific Ocean, 156
Acid phosphatase in pollen wall, 333 Amazon estuary, manganese, 178
Acidic springs on ridge crests and Americium 11, 241
manganese, 184 „ in North Minch, 12
Adenine nucleotide in muscle tissue, 298 AMF Vector Averaging current meter, 41,
Adenosine-5′-monophosphate (AMP), 270, 42
272 Amino acids in corals, 204
„ complex, 268 Amphibolis antarctica, pollen and stigma
Adenosine-5′-phosphate(AMP), 270, 272, interaction, 337–338
273 „ pollen attachment, 337
„in mussels, 291, 292 „ pollen germination, 337–338
Adenylate energy charge (A.E.C.), 272, „ pollen tube penetration, 338
273, 274, 295 Amylase, 278
„ effect of anoxia, 290, 291, 292 Anaerobic succinate pathway of
Adriatic Sea, mysids, 408, 411, 418 carbohydrate catabolism, 298, 299
African black oystercatcher, 455 Anchovy-pilchard fishery, California, 517
Agulhas Current, chaetognaths, 362, 384, „ southern Africa, 517
512 Anemone fish, 437
Airborne Oceanographic LIDAR (AOL), Anemones, fighting tentacles, 443
77, 78, 79, 80, 94 „ holotrichs and atrichs used in aggression,
Aircraft as platforms for instruments, 79 443
Aircraft Loran C system for positioning Anglesey, currents, 25, 36, 39, 40, 44
aircraft, 80 Antarctic euphausiids, 128
Alabandite, manganese sulphide, 170 Anther surface layer, carbohydrate, 332
675
„ lipid, 332 Barrow-in-Furness, currents, 34

„ protein, 332 „ tides, 24, 25
Anthesis, 329 BATFISH, undulating towed vehicle, 140
,, in pollen, 331 Bay of Fundy, hydroelectric tidal barriers,
„ Syringodium filiforme, 322 146
„ Thalassia hemprichi, 324 „ model of eddies, 151
„ Zostera marina, 317, 318 „ primary production, 135, 136
Antimony in corals, 200 „ tides, 129
Apomictic cycle, 323 Bay of Sevastopol, Russia, chaetognaths,
Arabinogalactans in marine angiosperm 362, 372, 376, 382, 383, 386, 387, 388
pollen, 327 Beam attenuation transmissometry, 70–72
Arabinose in pollen, 328 Bedford Basin, Nova Scotia 388
Aragonite, 199, 201, 203, 204, 205 „ chaetognaths, 362, 368, 369, 372, 381,
„ in corals, 197 383, 384, 387
Aragonites, organic materials in Beer's Law, 59
framework, 203, 204 Bering Sea, chaetognaths, 387
Arctic Basin, sediment cores, 173 „ internal waves, 139
„ mysids, 396, 397, 410, 416 „ manganese related to last glaciation, 179
„ water, chaetognaths, 385 Bilirubin and biuret reaction, 245, 253
Arginine phosphate, 270, 271, 274, 275 Biochemical metabolic regulatory
Arsenic in corals, 198, 199 responses of marine invertebrates to
„ invertebrates, Great Barrier Reef, 199 natural environmental changes and
Arthropodin, 205 marine pollution, 263–313
Ascidians, ‘tunic acids’ reduce palatability Biological monitoring, concept of, 263,
to fish, 480 264
„ vanadium, reduced palatability to fish, „ oxygen demand (B.O.D.), 287
480 „ processes, light emitted by, 66–69
Aspartic acid in corals, 204 „ properties measured by optical
Asterias, cannibalism, 460 instrumentation, 55–98
Atlantic Ocean, manganese, 179 „ the time-space dilemma, 55–57
„mysids, 395 Bioluminescence, 68
,, tidal constituents, 24 „ early measurement of, 75
Atlantic shelf off Nova Scotia, water „ emission, 68–69
transport, 154 Bioluminescent photometers, 75–76
Atlantis II Deep, Red Sea, manganese, 184 Bioturbation of sediments, 11
„ metalliferous sediments, 195 Birds, effects of feeding in flocks, 450
Auks, fish diets, 514 Biscayne Bay, Florida, chaetognaths, 369,
Australia, gastropods, 469 372, 376, 383, 387, 388
Black Sea, chaetognaths, 362, 369, 376,
Balsam Mountains, salamanders, 561 386, 387, 388, 400
Baltic Sea, authigenic manganese „ manganese, 176, 177
carbonate and sulphide, 170 „ stratified waters, 174
„ mysids, 395 Bluegill, optimal prey size, 554, 555
Barium in corals, 200, 201, 202 Boothbay Harbor, Maine, flow cytometric
„ input to sediments from oil plat forms, analysis of natural populations, 86
196 Bottom current winnowing as method of
,, sulphate in drilling muds, 207 transfer of manganese from
hydiothermal vents, 185
SUBJECT INDEX 677
„ currents in canyons, 152 Canada, eastern, shelf break fronts, 142

Breeding biology, intraspecific variations Canary Current upwelling system, 118, 119
in mysids, 406–409 Cannibalism in chaetognaths, 364–366
Britain, introduction of algae, effect on Capelin, factors influencing lipid values,
local flora, 566, 567 224-228
British Columbia, chaetognaths, 360 Capes and headlands, 153-154
„ commercial fish populations, 157 Carbohydrate catabolism, 302
„ submarine canyon, 153 „ and moulting, 294, 295
„ Isles, chaetognaths, 362, 368, 369, 372 „ and reproductive cycle in worms, 296
„ frontal regions, 146, 147 „ effects of environmental perturbations,
„ oscillatory tidal motions, 28 294
„ tidal model, 103 „ in polychaetes, 286
British Nuclear Fuels Ltd, Sellafield Carbohydrate catabolism, integrative
(Wind- scale), 11 regulation of, 271–275
Brittainy, eelgrass beds, flowering, 318 „ regulation of, 293
Carbohydrates in pollen, 315
Cadmium effect on mysids, 405 „ surface layer of anthers, 332
„ in copepods, 198 Card Bay, Florida, chaetognaths, 387, 388
„ corals, 200, 201, 202 Cardigan Bay, Irish Sea, 12
„ sea water, 172 Cariaco Trench off Venezuela, manganese,
„ input to sediments from oil platforms, 176
196 Caribbean, mining and dredging
„ sulphide in Atlantis II Deep sediments, operations, 195
195 „ regulation of fish community, 525
Caesium 134, 11, 34 137, 11 „ Syringodium filiforme, 322
„ Baltic, 12 Carotenoids, 58, 59, 60, 74, 369
„ Irish Sea, 33, 34 Cell-quota model, 105
„ North Sea, 12 Celtic Sea, 13, 24
„ Norwegian coast, 12 „ shallow sea fronts, 146
„ use in predictions of flow in Irish Sea, CEPEX bags, 376, 381, 382
32, 46 Cerium 144, 11
Calcite, 199, 201 Chaetognatha, feeding in 343–392
Calcium in corals, 200, 201, 202 Chaetognaths, alimentary canal, 350
„ substitution by metals in aragonite, 199– „ anatomy of digestive system, 350–351
203 „ batch rearing, 361
California, Conus sp., 461 „ cannibalism, 364–366; 343, 368, 371,
„ Current, 156 388, Fig. 14 (Feigenbaum & Maris) bet-
„ boundary of region, 131 ween pp. 358 and 359
„ eddies, 155 „ carotenoids, 369
„ system, 154 „ cells of digestive system, 351, 352
„ shelf, nutrient-rich water, 156 „ chemoreception, 349, 356
Californian anchovy-pilchard relationships „ colouration in, 369
517 „ Conover Ratio Method of determining
„ coast, feeding of larval anchovy, 137 digestive efficiency, 359
Callose in pollen, 330, 331 ,, corona ciliata, 356–357; 346, 349, 354
„ (1, 3-ξ -glucan) in pollen of Thalassia „ daily ration, 378–380
hemprichii, 326 „ detection of food, 346–349
„ diet, 361–369; 345
„ difficulty of keeping alive in laboratory, „ methods of collection and laboratory

359, 360 maintenance, 359–361
„ digestion, 370–371; 372, 373, Fig. 15 „ methods of determining digestive time,
(Feigenbaum & Maris) facing p. 359 370
„ digestive system 350–357 „ nervous system, 352–354
„ effect on sea fisheries, 386 „ number of prey per chaetognath (NPC),
„ effect on zooplankton standing stock, 375, 378, 379, 380, 382, 383
386, 387 „ observed by SCUBA diving, 388
„ electron micrograph of anterior teeth, „ oesophagus, 351
Fig. 4 (Feigen- baum & Maris) facing p. „ origin of, 343
348 Chaetognaths, paralysing of prey, 358
„ estimates of standing stocks, 387 „ parasites of, 378
„ estimation of digestive time, 370 „ pigments of, 369
„ eye, 354; 346, 353 „ phototactic responses, 346
Chaetognaths, faecal pellet, 359, 360, Fig. „ possible sense organs, 356–357
12 (Feigenbaum & Maris) facing p. 358 „ prey and predator sizes, 369
„ fed on protozoans, 345 „ prey selection, 367–369
„ feeding and prey density 382–383 „ reaction to vibrating probe, 346, 347
„ and time of day, 383–384 „ rectum, 352
„ apparatus, 350 „ “Reeve net” for collecting of, 360, Fig.
„ experiments, 360, 361 13 (Feigenbaum & Maris) between pp.
„ growth and reproduction, 384–385 358 and 359.
„ historical background, 343–346 „ response to vibrations, 367
„ morphology, 349–350 „ retrocerebral organ, 357
„ process, 357–359 „ rôle of feeding in vertical migration, 386
„ rates, 378–386; 376, 377 „ sensory hairs, 354–356; 348
„ food containing ratio (FCR), 375, 378, „ significance of in plankton ecosystems,
379, 382, 383 386 388
„ food for many organisms, 343 „ specific daily ration, 380–382
„ generalized drawing, 344 „ starvation, 385
„ generalized nervous system, 353 „ tangoreceptors (touch receptors), 348,
„ gut content analysis, 371–378, 386 349, 354
„ hair fan patterns, 355, Fig. 11 „ true cannibalism, 364
(Feigenbaum & Maris) facing p. 358 „ vertical migration, 346
„ head, hooks and teeth, 349–350; Figs 3 „ vibration receptor, 356
and 5 (Feigen- baum & Maris) facing p. Chagos Islands, Conus sp., 46
348 and p. 349 Challenger Expedition, 179
„ head width and body length, 366 Chelated iron, effect on flowering of
„ histology of digestive system, 351–352 Halophile stipulacea, 323
„ in Agulhas Current, 512 Chemical effluents, effect on coral reefs,
„ intestine, 351; 350 195
„ intraphyletic predation, 364 Chesapeake Bay, Virginia, chaetognaths,
„ laboratory and field feeding rates, 385– 362, 372, 376, 387, 388
386 „ estuarine plume front, 148
„ laboratory cultures, difficulties, 343, 345 „ flow pattern, 148
„ laboratory feeding, 385 „ flowering of Zostera marina 317, 318
„ lack of carapace, 343 Chiatura, U.S.S.R., sedimentary
„ mechano-receptors of food, 348, 354 manganese ores, 170
SUBJECT INDEX 679
Chile, Codium dimorphum, 486 Concanavalin A in stigma papilla, 334

Chitin, a polymer of N-acetyl-ξ - Connecticut River, estuarine plume front,
glucosamine, 205 148
„ in anthropods, 205 Convergence of plankton, 137
„ metal-binding properties, 205 Coomassie Brilliant Blue G-250 protein-
Chlorophyll, 58, 59, 60, 61, 62, 66, 67, 69, binding, analytical value, 259
71, 72, 73, 74, 77, 78, 79, 80, 81, 82, 83, Copper, effects on phosphoglucose
84, 89, 90, 91, 109, 113, 114, 132, 139, isomerase genotypes, 282
140, 143, 144, 146, 147, 148, 153 „ in chitin, 205
Christmas Island, terns, 515 „ copepods, 198
Chromium in corals, 200 „ corals, 200, 201, 202, 203
„ drilling muds, 207 „ manganese nodules, 181, 182
Circadian rhythms, 131 „ sea water, 172
Citrate synthase, 298, 299 „ input to sediments from oil platforms,
Citric acid cycle, 272 196
„ enzymes associated with, 298 „ sulphide in Atlantis II Deep sediments,
Coastal planktonic ecosystems, 128 195, 196
Coastal Zone Colour Scanner (CZCS) 81– „ toxic effects on corals, 206, 207
82; 55, 61, 71, 92, 94, 132 Coral physiology, effect of heavy metals,
„ phytoplankton pigment image off 206–208
Charlotte Islands , Canada, Fig. 11 Coral-reef ecosystems and hurricane-
(Denman & Powell) facing p. 154 induced waves, 153
Cobalt in chitin, 205 „ fish communities “lottery hypothesis”,
„ copepods, 198 523, 524, 541
„ corals, 200, 201, 202 „ grooves, ambient currents, 152
„ manganese nodules, 181 Coral reefs and heavy metals, 195–210
Colouration in chaetognaths, 369 „ effect of chemical effluents, 195
Common guillemot, 439 „ desalination plant discharges, 195
Compensation depth, definition, 134, 135 „ drilling muds, 195
Competition and evolution, 556–580 „ power plant discharges, 195
„ speciation, 574–580 „ sewage effluent, 196
„ apostatic selection, 547–548 Coral Sea, 204
„ between marine organisms, ecological „ skeletons and heavy metals, early studies,
and evolutionary implications, 429–593 195
„ between species, 455–543 „ as palaeo-environmental recorders of
„ co-operation between species, 544–546 metal in sea water, 196, 197
„ effect of other competitors, 538 „ incorporation of heavy metals, 199–206
„ enhancement of food supply, 546–547 Coral species, dichotomy of, 467
„ exploitation defined, 430 „ tissues, incorporation of heavy metals,
„ extinction, 565–567 197–199
„ for food and space, summary of Corals and chitin, 205, 206
consequences, 558 „ effects of a chrome ligno-sulphate (FCLS)
„ groups considered, 432 drilling mud, 207
„ interference defined, 430 „ effects of metals on physiology of, 197
„ intraspecific, 432–455 „ feeding mechanisms, 198
„ mechanism of, 559–565 „ pathways by which heavy metals are
„ optimal feeding, 548–555 incorporated, 196, 197
„ what is meant by it, 431
„ production of mucus as a stress response, „ system of chaetognaths, 356–357

207 Dinoflagellates, effect of mercury on a
„ due to copper, 206, 207 culture of, 199
„ uptake of heavy metals, 196–206 Dioecious sea-grasses species, 316
Coriolis parameter, 31, 131 Divergence of plankton, 137
Coulter electronic particle counter, 73, 76, Doubling time and particle size,
77 relationship between, 128, 129, 130
Courtown, Eire, tides, 24 Drilling muds as a source of metal
Crab-eater seals, 518 enrichment, 196
Crabs cytochrome c oxydase, 402 „ effect on coral reefs, 195
Creatine phosphate, 274 „ toxic effect on corals, 207, 208
Cretaceous period, reef-forming animals, Dublin, low frequency current, 32
565
Critical depth, definition of, 135 East Australian shelf, surface currents, 155
Current meters, Irish Sea, 18–20 East Pacific Rise, manganese, 185
Currents in eastern Irish Sea, 11–53 „ metalliferous sediments, 183
Cutin in stigma cuticle of Amphibolis Easter Island, Conus sp., 461
antarctica, 335 Ecological and evolutionary implications
Cutinase in pollen, 315 of competition, between marine
Cyanobacteria, 59, 68, 69, 74, 89, 90 organisms, 429–593
Cylic-AMP, 279 Ecological energetics from total lipid and
„ dependent protein kinases, 267, 268, 269, total protein, fact and artifact using a
270, 271 gravimetric method for lipid and a biuret
Cymodocea serrulata enzyme systems, 323 method for protein, 211–261
„ cultures, 322, 323 Ecology and sensitivity to environment,
Cytochemical analysis of pollen, 328 302–304
„ of stigma surface, 334 Ecophysiology of marsupial development
„ examination of marine angiosperm and reproduction in Mysidacea
pollen, 326 (Crustacea), 393 428
Ecosystems, planktonic, effect of physical
Dabob Bay, Washington, chaetognaths, processes in coastal oceans, 125–168
385 Effluents from desalination plants as a
Damselfish., 437 520, 531, 532, 538, 564 source of metals in ionic form, 196
Damselfish, effect on corals, 466 Ekman transport, 144, 149
Danish waters, mysids, 395 El Niño, 157, 158
Deception Island, Antarctic, manganese, Electivity indexes, 367
185 Electrophoretic protein analyses, 460
Deep Sea Drilling Project cores, „ separation of enzyme variants, 280, 281
rhodochrosite, 170 „ protein variants, 281
„ manganese, 178–183 Embden-Meyerhof glycolytic pathway, 287
Density, Irish Sea, 13–17 Emission spectra, 69
Department of the environment, U. K., 11 ′ -emitters in corals and atomic tests, 202
Desalination plant discharges, effect on English Channel, 31
coral reefs, 195 „ catches of young fish, 157
Diatom blooms off Scripps pier, 155 „ phosphate, 157
Diffusivity of phytoplankton, 130, 136 English Channel, planktonic catches, 146
Digestive enzymes, 278
SUBJECT INDEX 681
Environmental change and metabolic „ vertical migration in chaetognaths, 386

regulatory responses 265–285 „ in the Chaetognatha, 343–392
„ effect on habitat, 286–293 „ morphology, chaetognaths, 349–350
„ stress on marine fauna, time related „ process in chaetognaths, 357–359
sequence of effects, 267 „ rates, chaetognaths, 378–386
Enzyme activation, surface of stigma, 316 Ferromanganese concretions in fresh
„ heterogeneity, 281 water, 174, 175
„ systems in Zostera marina, 318 Fertilization as an apomictic pathway, 315
„ variants as genetic markers, 280 Feulgen-positive nuclei in marine
Eocene, barnacles, 566 angiosperm pollen, 327
Epifluorescence microscope, 83 Firth of Clyde, Scotland, phytoplankton
Epinephrine, effect of invertebrate muscle, biomass, 100
268, 269 „ sewage sludge dumping ground, 301
Esterase activity in pollen, 329 Fish kills and red tides, 118
„ stigma secretion, 339, 340 Fish protecting their algal patches, 562
„ in marine angiosperm pollen, 327 Fisheries Research Laboratory, Lowestoft,
„ isoenzyme, 277 U.K., 19, 35
„ reaction in stigma cuticle of Amphibolis Fishguard, U.K., mean sea level, 49
antarctica, 335 Fishing grounds, coastal, 151
„ product on stigma papillae of marine Florida, chaetognaths, 359, 360
angiosperms, 334 „ Current chaetognaths, 362, 372, 376,
„ stigma surface, 334 379, 380, 382, 387
Esthwaite Water, U.K., manganese in, 175 „ Syringodium filiforme, 322
Estuarine plume fronts, 148–149; 142 „ Zostera marina cultures, 321
Eukaryotic cells, genome of, 277, 278 Flow cytometer, 91, 92, 93
„ metabolic complexities of, 267 „ optical components of, 82, 83
Eulerian-continuum models, 106, 117 „ cytometric analysis of a natural
Euphotic zone, 136, 150, 152 population, 86
„ definition of, 134 „ chlorophyll, 90
„ eastern tropical Pacific, 102, 103 „ cytometry, 82–87
Europe, freshwater ferromanganese, „ early uses, 82
concretions, 174 „ techniques, 86
European estuaries, manganese, 178 Flowering and pollination in marine
Europium in corals, 201 angiosperms, 315–342
Evolution and competition, 556–580 Fluorescein, 67
Excitation spectra, 69 Fluorescence, 61, 62, 66, 68
„ wavelengths of argon ion laser and „ early discovery, 66, 67
phytoplankton pigments, 84 „ emission by phytoplankton, 66–68
Exe estuary, U.K., nematodes, 501 „ microscope, 67
Exine layer, marine angiosperm pollen, „ microscopy of pollen, 326
326, 327, 328, 331, 332 Fluorescent-activated cell-sorting, 87–91
„ of pollen, 315 „ instrumentation, basic arrangement, 88
„ of terrestrial pollen, 332 „ stains used in flow cytometry, 85
Eye of chaetognaths, 354 Fluorespar, 66
Fluorochromes, 67
Feeding and prey density in chaetognaths, Fluorometers, 91, 92, 93
382–383 Fluorometry, 113
„ and pumping systems, in vivo, 72–73
„ in situ, 73 Groote Eyland, Australia, sedimentary

Fluorosensor, 77 manganese ores, 170
Fructose-1, 6-bisphosphatase, 268 Guano production, indirect indication of
Fucoxanthin, 58, 59, 67, 69, 73, 74, 83, 84 overfishing, 517
Gulf of Caribbean, Syringodium filiforme,
Galactose in pollen, 328 324
Galapagos Rift, hydrothermal systems, 184 „ Maine, chaetognaths, 345
„ manganese, 184 „ chlorophyll, 139
‘Gardening’ of food supplies by „ commercial fishing, 156, 157
organisms, 547 „ emission spectra, 68
Gas and oil field operations as source of „ excitation spectra, 68
enrichment of trace metals, 196 „ fluorometry, 72
Gause’s exclusion principle, 107, 119 „ primary production, 135, 136
Geitonogamy in sea grasses, 316 „ salinities and temperatures, 156
„ Zostera marina, 319, 320, 335, 336, 339 „ temperature, 72
Gelbstoff, yellow substance, 58, 60, 61, 62, „ tides, 129
70, 71 „ transmissometry, 72
Genetic diversity and niche breadth, 567– „ Marseille, mysids, 412
574 „ Mexico, effect of hurricane on primary
,, heterogeneity, 280 production, 137
George’s Bank, primary production, 136 „ manganese, 177
GEOSECS programme, 172, 185, 186 „ Syringodium filiforme, 322
German lakes, mysids, 401 Gulf of Naples, mysids, 412
Glucose in pollen, 328 „ St Lawrence, Canada manganese, 176,
Glucose-6-phosphate dehydrogenase, 278 177
Glucose phosphate isomerase (G.P.I.) locus Gulf Stream, 137, 143, 152
and niche breadth, 569, 570 „ chaetognaths, 368, 381
Glutamic acid in corals, 204 „ eddies, 155
Glycine in corals, 204 „ off mid-Atlantic Bight, 154
Glycogen metabolism, control of, 268 „ statistical study of, 154
Glycogen phosphorylase activity and Gut content analysis of Chaetognaths, 371–
moulting, 295 378, 386
Glycogen synthetase in mussels, 268
Glycolysis, end-products of, 299 Halodule wrightii, flowering in culture,
„ in molluscs, 268 322
Glycolytic degradation of glucose-6-phos- Halophila engelmanni, salinity and
phate, 268 reproductive behaviour, 321
Glycoproteins in marine angiosperm „ stipulacia, flowering of, 323
pollen, 327 Hardy recorders, 92
„ pollen, 315 Hawaii, Conus sp., 460, 461
Glycosidases in pollen germination in „ corals, 206
Amphibolis antarctica, 337 Hawaiian reefs, coral heads, 563
Great Barrier Reef, 199 Headland plumes, 149
„ regulation of fish community, 525 Heavy metal pollution in tropical
Great South Bay, New York, flowering of environments, 195–196
Zostera marina, 317, 318 „ metals and coral physiology, 206–208
Green sunfish, optimal prey size, 554, 555 coral reefs, 195–210
SUBJECT INDEX 683
„ incorporation into coral skeleton, 199– Inorganic particles, light absorptions by,
206 60–61
„ tissues, 197–199 Instant Ocean, effect on flowering of
„ uptake by corals, 196–206 seagrasses, 324
Heimaey Island, Iceland, manganese, 185 Institute of Oceanographic Sciences,
Hermit crabs, 436 Bidston, Birkenhead, U.K., 19, 36, 40
„ chemical cue to locate gastropods, 508, Instrumentation in combination, 95
509 Insulin-like hormones in mussels, 268
„ exposed to odour of Octopus, 509 Interactions between organisms, 543
Heron Island, Great Barrier Reef, coral Interdisciplinary oceanography, 100, 109,
diversity, 539 117, 120
Heterozygosity, 281, 293 Internal waves, 133
Holyhead, low frequency currents, 32 „ and planktonic ecosystems, 138–141
Homeostatis, 271, 275, 400, 402, 420 International Council for the Exploration
„ definition of, 265, 266 of the Sea (ICES), 265
Hormonal control in marine invertebrates, Interspecific competition, birds and fish,
267–271 514-526
„ effects on carbohydrate catabolism, 279 „ changing circumstances, 531–532
Hudson Bay, stratification, 135 „ examples and consequences, 456–526
Hudson River plume and upwelling frontal „ fauna of soft sediments, 490–508
systems, 148 „ hermit crabs, 508–512
Hudson Shelf valley, wind-driven shelf „ historical events, 542–543
currents, 152 „ intransitive competitive net-works, 532–
Hydration of pollen, 315, 316 533
Hydrolases in pollen wall of seagrasses, „ marine algae, 484–490
339, 340 „ mechanisms of co-existence, 526–543
Hydrothermal activity at axes of mid-ocean „ other competitors, 538
ridge systems, 183 „ physical disturbance, 538–541
„ manganese deposits in Pacific, 183 „ refuges in time or space, 530–531
„ systems, fossil analogues, 185 „ resource partition-ing, 527–530
„ vents, manganese, 183–185 „ rôle of chance, 541
„ rôle of predators, 533–538
Iceland, depressions, 28 Interspecific competition, sedentary
Immuno-fluorescent probes, 83 benthic carnivores, 456–464
Impinging eddies and plankton „ sedentary rocky shore herbivores, 469–
ecosystems, 154–155 475
Incorporation of metals into coral skeleton, „ sessile carnivores, 464–468
rôle of organic materials, 203–206 „ sessile filter-feeders, 476–484
Index of refraction, 60, 64, 65 „ zooplankton, 512–514
Indian Ocean, candacid copepods, 512 Intine layer in marine angiosperm pollen,
„ manganese, 179, 182 327
Indonesia, Conus sp., 461 Intraspecific competition, 432–455
„ mining and dredging operations, 195 „ avoidance or ritualization of combat,
Indo-Pacific, regulation of fish community, 450–453
525 „ differences in diet, 453–455
„ West Pacific, Conus sp., 461 „ dispersal along an environmental
gradient, 444–448
„ dispersal of adults, 442–444
„ dispersion patterns, 448–450 „ topography, 12–13

„ larval settling patterns, 439–442 „ winds, 37, 38, 41
„ mechanisms reducing, 439–455 Iron in chitin, 205
„ versus interspecific competition in „ copepods, 198
equilibrium populations, 526–527 „ corals, 200, 201, 202, 203, 208
Irish Sea, bathymetry, 14 „ sediments, 181
„ bottom drifters, 35 Ischia, Gulf of Naples, mysids, 407
„ caesium 137, 44 Island mixing zones on continental
„ current vector, Eulerian, 30 shelves, 118
„ Lagrangian, 30, 31, 32, 34 Islay, Scotland, elevation nodes, 24
„ currents, 11–53 Isle of Man, 12, 13, 14, 17, 24, 25, 27, 32,
„ density, 13–17 36
„ drift bottles, 32 „ currents, 39, 40, 44, 46, 49
„ flow from, to Norway and Baltic, 33 Isocitrate dehydrogenases, 298, 299
„ Liverpool Bay, 17 Isoenzymes, 277, 278, 279
„ low frequency currents, 28–49, 50
„ driving forces, 28–31 Japan, mysids, 395, 400
„ Eulerian current meters, 34–44 Japanese estuaries, manganese, 178
„ horizontal density gradients, 29–30 Jerlov’s water types, 70
„ Lagrangian, 31–34 Juan de Fuca Ridge, manganese, 184
Irish Sea low frequency currents,
meteorological forces, 28–29 Kaneohe Bay, Hawaii, chaetognaths, 362,
„ numerical models, 44–49 366, 368, 372, 376, 381, 387, 388
„ observation of, 31–44 Kenya, Cymodocea rotundata, 322
„ pressure gradients, 30 „ Cymodocea serrulata, 322, 323, 324
„ tidal, 30–31 „ Halophila stipulacea, 323
„ Morecambe Bay, 22, 23 „ seagrasses, 324
„ movement of radioactive waste, 50 Kenya, Thalassia hemprichii, 325
„ North Channel currents, 44 „ flowering rhythm, 326
„ numerical models, 20–23 „ Zostera capensis, 323
„ physical oceanography, 12–17 Kilindini Harbour, Mombasa, tidal range,
„ plutonium, 50 325
„ recording current meters, 18–20 Korean estuaries, manganese, 178
„ river discharge to, 13 k-strategists, 119
„ salinity, 13–17 k-theory model, 133
„ shallow sea fronts, 146 Kwajalein, Indo-Pacific, Conus, 551
„ speeds of tidal currents, 17
„ stormdriven currents, 39, 50 Lactate dehydrogenase, 277, 283
„ storm surges, 46 Lagrangian-ensemble, 106, 107, 117
„ storms, 28, 29, 39, 40, 44, 46 Lake Michigan, manganese, 175
„ surface salinity, 15 „ Ontario, manganese, 175
„ sea surface temperature, 16 „ Windermere, U.K., manganese, 175
„ suspended sediments, 61 Lakes, manganese, 174–178
„ temperature, 13–17 Langmuir circulation, 137, 138
„ tidal currents, 25–27, 49 Lanthanides in corals, 200
„ tidal elevations, 24–25 Larval recruitment lotteries, 541
„ tidal energy, 18, 19 Laurentian Trough, manganese, 176
„ tides, 23–27
SUBJECT INDEX 685
Lead in copepods, 198 Lipid determination, effect of NaCl with

„ corals, 200, 201, 202 varying amounts of sample, 232–234
„ input to sediments from oil platforms, ,, washings with chloroform:methanol,
196 223–224
„ sulphide in Atlantis II Deep sediments, „ extraction, amount of
195 chloroform:methanol to use, 239–248
Lectin in pellicle layer of stigma, 334 „ in marine angiosperm pollen, 327
Leucine aminopeptidase (Lap) in acmaeid „ in pollen, 315
lim pets, 529 „ in surface layer of anthers, 332
„ alleles in acmaeid limpets, 575 „ optimum extraction of, 237–238
„ locus in Acmaea spp., 570, 571 Lithium in corals, 200
„ in mussels, 281, 282 Liverpool Bay, U.K., currents, 32, 34, 35,
Light absorption by dissolved yellow 36, 40, 43, 49, 50
substances, 61–62 „ tides, 25, 27
„ inorganic par-ticles, 60–61 Loch Creran, U.K., diatom abundance,
„ of, 58 112, 113, 114
„ and flowering of Zostera marina, 319, „ Eil, U.K., polychaetes, 295
320 „ Fyne, U.K., rhodochrosite, 170
„ and pollen release in Zostera marina, 319 „ sediment cores, 173
„ Detection and Ranging (LIDAR), 77, 78, „ Striven, U.K., spring increase, 100
79 Longhurst-Hardy recorders, 92
„ flurosensing, 77–79; 92, 94 Long Island Sound, nitrate and
„ emitted by biological processes, 66–69 chlorophyll, 153
„ scattering by particles, 64–66 „ phytoplankton, 108
„ by water, 62–63 „ plankton, 147
„ coefficient compared with wavelength, Lotka-Volterra equations of population
65 biologists, 111
Limitations and advantages of various Luciferase, 68
optical instruments, 93, 94 Luciferin, 68, 69, 74, 83
Limpets, algal “gardens”, 448, 454, 562 Luminescene, 68
„ homing of, 443, 444 Lynher estuary, U.K., nematodes, 501
Lipid, amount lost during determination,
228–229 Magnesium in copepods, 198
„ of extracting solvent associated with, 228 „ corals, 200, 201, 202, 203, 205
Lipid and protein, amount of material to Magnetite particles taken up by a zoanthid
use, 219–221 198
„ basic methods of determination of, Malate dehydrogenase, 283, 302
214−216 Malaysia, mining and dredging operations
„ determination, amounts of material to use, 195
229–232, 234–236 Maldives, Conus sp., 461
„ important points, 236–237 Malin Shelf Sea, 13, 24
„ number of replicates necessary, 255–257 Manganese, analysis in sea water, 171, 172
„ statistical analysis of values obtained „ as ferromanganese oxide concretions, 169
with different amounts, of samples, 234 „ as micronutrient, 173
„ ecological energetics, fact and artifact, „ concretions in lakes, 174, 175, 176
211–261 „ deep sea, 178–183
,, tests with capelin material, 224–248 „ hydrothermal vents, 183–185
„ Pandalus, 219–224
„ in chitin, 205 „ mysids, 395, 400, 408, 423

„ copepods, 198 „ phytoplankton, 128
„ corals, 200, 201, 202 Mercury, effect on mysids, 406
„ estuaries, 178 „ in corals, 201
„ pore waters, 173 Messina, Sicily, chaetognaths, 386
„ sediments, 173 Metabolic regulatory responses, 284–285
„ the marine environment, 169–194 „ substrates and syntheses of gametes,
„ input to oceans from atmospheric 294
particulate matter, 173 Metal-binding properties of chitin, 205
„ input to sediments from oil platforms, „ protein, 204, 205
196 Metals in coral skeletons, concentrations
„ lakes, 174–178 of, 200
„ micronodules, 170, 180 Meteorological Office, daily weather
„ nearshore environments and lakes, 174– reports, 36
178 Mexico, Zostera marina cultures, 321
„ nodules, 169, 170, 171, 178, 181, 182, Miami, Florida, chaetognaths, 381
198 „ first feeding experiments with
„ growth of, 181, 182 chaetognaths, 345
„ oxide concretions, 170 Microbial oxidation, 62
„ oxides as scavengers of transition metal Microbomb calorimetry, 245
ions, 169 Microzones round zooplankton, 116
„ sea water and pore water, 171–174 Mid-Atlantic Bight, water transport, 154
Mannose in pollen, 328 „ Ridge, manganese, 184
MANOP programme, U.S.A., 82 Ministry of Agriculture, Fisheries and
Mantis shrimp, 436 Food, 11
„ meral displays, 450, 451 Mississippi delta, manganese, 177
Marine angiosperms, aspects of flowering, Mixed function oxygenase (M.F.O.)
317–325 system, 278
„ flowering and pollination, 315–342 Mixing and plankton, an interdisciplinary
„ pollen, 325–334 theme in oceanography, 99–123
„ pollen and stigma, 325–335 „ symbols, definitions and dimensions, 120,
„ pollination, 335–338 121
„ stigma, 334–335 Models, prediction of physical conditions
„ environment, manganese, 169–194 in shelf seas, 103
„ invertebrates, behaviour and Molecular and genetic regulatory responses
environmental conditions, 298–300 to environmental stress, generalized
„ distribution of populations of, 300–302 scheme, 285
Marine invertebrates, hormonal control, Monoecious seagrass species, 316
267–271 Monomorphic species with monoclinous
„ regulation by adaptation, 280–284 species of seagrass, 316
„ pollution, definition of, 263 Monosaccharides, in thecal slime of marine
„ system, impact of pollutant, 263 angiosperm pollen, 327, 328
Marsupial development and reproduction Monterey submarine canyon, currents, 152
ecophysiology of in Mysidacea, 393–428 Morecambe Bay, U.K., currents, 32, 40
Massachusetts Bay, internal waves, 140 Moresby Island, Macoma spp, G.P.I. locus,
Mediterranean, chaetognaths, 362, 369 569
„ demersal fish, 518 mRNA, production of, 277, 278
„ flowering of seagrasses, 318
SUBJECT INDEX 687
Muir Seamount, energy in internal wave „ variations of breeding periods and

activity, 138 timing, 409–412
Mull of Galloway, U.K., weather reports, „ of brood sizes, 412–414
36, 38 Mysids, latitudinal variations of brood
Multichannel fluorometer in situ, 74–75 weights and parental sizes, 417–419
Mysidacea, ecophysiolopy of marsupial „ of egg sizes, 414–417
development and reproduction 393–428 „ loss of young from brood pouch, 409
Mysids, abortion, 406,419 „ marsupial development and temperature,
„ are effects of size and temperature 394, 395
interdependent? 404–405 „ mortality due to parasites, 409
„ as test organisms for pollutants, 393 „ mortality of brood pouch young, 408–409
„ average number of young, 413 „ natality, 407, 408, 424
„ body lengths of breeding females, 418 „ pseudocontinuous breeding, 410
„ brood size and parent size, 421 „ rôle in fisheries biology, 393
„ cannibalism, 409 „ seasonal and individual variations in size
„ cold-season breeding, 410 and breeding intensity, 406–408
„ continuous breeding, 411–412 „ stenothermy, 401
„ development, egg sizes, body sizes and „ temperature relations of the incubation
temperature, 398, 399 period, 394–402
„ direct study of young in brood pouch, 393 „ understanding of breeding biology, 424–
„ duration of marsupial development, 397 425
„ duration and frequency of marsupial „ use in toxicity tests, 405
slopes, 408 „ warm-season breeding
„ effect of cadmium, 405
„ chemical factors on reproduction, 405– Nadir-viewing components, 80
406 Nantucket Shoals, chlorophyll estimates,
„ mercury, 406 79, 80
„ of nutrition on reproduction, 406 Narrow focus single cell instruments, 82–
„ of size and ambient condi-tions on 91
development and reproduction, 394–406 NASA, 81
„ egg sizes, 415 „ Goddard Wallops Flight Station, 77
„ and incubation period, 402–404 „ system, 78
„ and marsupial development, correlation NATO workshop on coastal oceanography,
of, 404 99, 120
„ and parent size, 422 Natural physiological rhythms in marine
„ ethoecolopical aspects of reproduction, invertebrates, 293–298
423 Navier-Stokes equations, 20, 21
„ in food chain studies, 393 Negative feedback control of enzyme
„ interspecific allometric relationships in activity, 271, 272
breeding, 420–423 Nervous system of chaetognaths, 352–354
„ variations in reproductive biology, 409– Netherlands, flowering of Zostera marina,
423 319, 320
„ intraspecific variations in breeding New England, algal zonation, 486
biology, 406–409 New South Wales, Australia, rocky shores,
„ laboratory culturing, 403 543
„ latitudinal temperature compensation of New York Bight, phytoplankton, 136
reproduction; 419–420 New Zealand, estuaries, manganese, 178
Newport River estuary, N. C., manganese, Nova Scotian Shelf, current fluctuations,
177 155
Nexine layer in marine angiosperm pollen, Numerical models, Irish Sea, 20–23
326, 328 Nutrients, effect of shelf break fronts, 143
Niche breadth and genetic diversity, 567–
574 Ocean colour scanners, 82
Nickel in chitin, 205 „ fronts and plankton ecosystems, 141–149
„ copepods, 198 „ types of, 141–142
„ corals, 200, 201, 202 Oceanographic regimes and plankton
„ manganese nodules, 181, 182 ecosystems, 155–158
„ sea water, 172 Ogac Lake, Canada, chaetognaths, 361,
Nicotinamide-adenine dinucleotide 83, 384
270, 274 Oneida Lake, New York, manganese in,
Nicotinamide-adenine dinucleotide 175
phosphate, 83 Onslow Bay, bottom waters, 155
Nikopol, U.S.S.R., sedimentary manganese „ eddy exchanges, 154
ores, 170 Optical instrumentation for measuring
NIMBUS Experimental Team (NET), 81 biological properties, 55–98
„ satellite, 71, 81 „ instruments for whole population, 70–77
Nitrate uptake by phytoplankton, 136 „ in combination, 76–77
Nitrogen circulation in euphotic zone, 102 „ large scale, 77–82
„ controlling primary production, 102 „ summary, 91–95
„ cycling in middle Atlantic Bight, 116 Optical instruments time and space
Nontronite, an iron-silicate, 184 problems, 57
North America, freshwater ferromanganese Oregon, episodic winds and currents, 144
concretions, 174 „ upwelling, 143, 145
„ west coast, biological regime, 156 Otters and sea urchin population, 545
„ Atlantic, auks, 514 Oystercatcher, feeding, 545
„ manganese concentrations, 171, 172 Oyster drill, cannibalism, 444
„ Carolina, flowering of Zostera marina,
318 Pacific Ocean, manganese, 172, 179, 180,
„ Channel, Irish Sea, 12, 13, 14, 24, 25, 25, 182
32, 33 „ manganese nodules, 170
„ Pacific auks, 514 „ use of a “bottom lander” to measure
„ Central Gyre, copepods, 514 fluxes to sediment, 182
„ high pressure, 156 „ sediments, pore water profiles, 171
„ Sea biological chemical zones, 151 Palau Islands, Cymodocea rotundata, 322,
„ chaetognaths, 346, 376, 382 324
„ closed eddies, 151 „ Cymodocea serrulata, 323
„ pelagic fish, 517 Panama Basin, eastern Pacific,
„ phytoplankton colour index, 157 rhodochrosite, 170
„ southern bight plankton, 111 Parrotfish, foraging of, 545
„ temperature and chlorophyll profiles, 77 „ schooling of, 564
Norway pout, increase due to reduction of Particle counter, 92, 93
herring and mackerel stocks, 517 Penguins, 518
Nova Scotia, chlorophyll, 139 Peridinin, 58, 59, 67, 69, 73, 74, 83, 84
„ flowering of Zostera marina, 318 Peru, continental shelf ecosystems, 157
SUBJECT INDEX 689
„ upwelling, 144, 157 „ compensation depth, 100, 101

„ and anchovies, 158 „ continuous recording instruments, 113
Peruvian anchovy fishery and El Niño, 158 „ critical depth, 100, 101
„ vagaries of, 157 „ dispersion, patchiness and scales, 109–
Philippines, offshore oil drilling effect on 116
corals, 208 „ ecosystems, significance of chaetognaths,
Phosphoarginine, 275 386–388
Phosphoenolpyruvate, 270, 272, 274 „ heterogeneity, (patchiness), 128
„ carboxykinase, 274 „ horizontal turbulent diffusion, 153
Phosphofructokinase (PFK), 268, 269, 270, „ red fluorescence in blue light, 113
273, 275, 282, 291, 293, 294, 295, 296, „ swimming speeds, 138
297, 298, 299, 302 Planktonic ecosystems and ocean fronts,
Phosphoglucomutase (PCM) isoenzymes, 141–149
282 „ residual circulation, 151–152
Phosphoglucose isomerase, 282 „ upwelling, 149–151
„ mutase, 282 „ capes and headlands, 153–154
Phospholombricine, 275 „ impinging eddies and changing oceano-
Phosphotaurocyamine, 274 graphic regimes, 154–158
Phosphorylase, 298 „ in coastal ocean, and physical process,
Phosphorylase a, 268 125–168
Phosphorylase b, 268 „ internal waves, 138–141
Phosphorylase kinase, 268 „ longer time scales, 154
Phosphorylation-dephosphorylation „ shelf edge canyons and bumps, 152–153
reactions, 267, 268, 269 270, 271 „ temporal and spatial scales, 128–132
Photogrammetry, 80 „ topographic influences, 151–154
Photo-oxidation, 62 „ upper ocean processes, 132–138
Phycobilins, 84 Plessey current meter, 19, 20, 35, 41, 42,
Phycocyanin, 58, 69, 73, 74, 83, 90 43
Phycoerythrin, 58, 59, 68, 69, 73, 74, 78, Pleistocence and evolution of Asterias, 460
83, 89, 90 Plutonium 211, 238, 239 and 240, 11
Physical and ecological processes, coupling Plutonium in North Minch, 12
of, 126 Point Conception, 131
Physical processes, effects on planktonic Polar marine organisms ‘loss’ of protein in
ecosystems in the coastal ocean, 125– analysis of, 253
168 Pollen adhesion to stigma, differences
Phytoplankton biomass near fronts, 143 between terrestrial and aquatic species,
Phytoplankton, characterized to taxonomic 339
group on pigments, 58, 66 „ and stigma, chemical interaction, 315
„ definition of, 99 „ interaction in Amphibolis antarctica,
„ diffusivity, 130, 136 337–388
„ fluorescence emission by, 66–68 „ marine angiosperms, 325–335
„ growth zones and mixing regimes, 104 „ anthesis, 331
„ passive sinking, 130 „ attachment in Amphibolis antarctica, 337
„ patchiness, 141, 152 „ callose, 330, 331
„ status in a mixed water column, 100, 101 „ (1, 3-ξ -glucan) in Thalassia hemprichii,
„ subtropical, 108 326
Plankton, and mixing, 99–123 „ carbohydrates, 315
„ discussion, 116–120 „ cutinase, 315
„ cytochemical analysis, 328 „ responses of marine biota at different

„ germination, in Amphibolis antarctica, levels of organization, 263
337–338 Polymorphic dioecious seagrass species,
„ Zostera marina, 336 316
„ glycoproteins, 315 „ esterases, 282
„ grain longevity in seagrasses, 336 Polysaccharides in aragonite, 203
„ grains, Figs 3, 4, 5, 6 and 8 (Pettitt) „ corals, 205
between pp. 334 and 335 „ pollen, 331
„ hydration of, 337 „ stigma surface, 334
„ intine polysaccharide, 332 Pore water, manganese, 171–174
„ lipids, 315 Portpatrick, mean sea level, 49
„ marine angiosperms, 325–334 Potassium in corals, 200, 202
„ acid phosphatase in the intine, 327 Power plant discharges, effect on coral
„ acidic polysaccharides, 326, 327 reefs, 195
„ cytochemical examination, 326, 327 Predators, summary of impact on
„ exine layer, 326, 328, 331, 332 communities, 535, 537
„ intine layer, 327 Prey selection, chaetognaths, 367–369
„ nexine layer, 326, 328 Primary production and vertical mixing,
„ sexine bacula, 326 100–109
„ RNase, 327 „ catastrophe theory, 117, 118
„ shape and size, 327, 328 „ in turbulent waters, 135
„ ultrastructural examination, 326 Probes useful in flow cytometers, 85
„ mother cells, 326 Productivity of sea, global, 125, 126
„ polysaccharides, 331 Prograde fronts defined, 142
„ proteins, 315 Protandry described, 316
„ release and temperature in Zostera Protein and lipid determination, amounts of
marina 319 material to use, 219–221, 229–232, 234–
„ shape and size, 329, 330, 331, 333, 334 236
„ tube, Figs 7, 10 (Pettitt) between pp. 334 „ basic methods 214–216
and 335 „ important points 236–237
„ penetration, Amphibolis antarctica, 338 „ number of replicates necessary, 255–257
„ tubes in Zostera marina, 336 „ statistical analysis of values obtained
„ length of, 336 with different amounts, 234
Pollen ultrastructure, 328, 329, 330, 332, Protein and ecological energetics, fact and
333 artifact, 211–261
„ of germination, 338 „ tests with capelin material, 224–248
„ wall organization as a taxonomic „ Pandalus, 219–224
criterion, 333, 334 „ determination, effects of different
„ structure of, 331, 332, 333, 334 treatment of samples, 221–223
Pollination and flowering in marine „ extinctions, pigment that interferes, 245
angiosperms, 315–342 „ in marine angiosperm pollen, 327
„ in Zostera marina, 335–336 „ pollen, 315, 329
„ marine angiosperms, 335–338 „ stigma surface, 334
Pollution and environment, effect on „ surface layer of anther, 332
biochemical metabolic regulatory „ loss when treating with chloroform:
responses in marine invertebrates, 263– methanol, 248–254
313 „ standard curve, construction of, 216–217
„ indicator species, 300, 302 Proteins in aragonite, 203, 204
SUBJECT INDEX 691
„ corals, 205 Rossby radius, 131, 143

„ metal-binding properties of, 204, 205 „ waves, 30, 155
Puget Sound, Washington, flowering of r-strategists, 119
Zostera marina, 317 Rubidium in corals, 200
„ coastal ecosystem model, 137 Russell cycle of climatic variation, 157
Pyruvate kinase, 270, 271, 272, 274, 275, Ruthenium, 11, 106
278, 282, 294, 295, 296, 298, 299, 302
Saanich Inlet, B.C., chaetognaths, 372, 376,
Quinine, 66 382, 388
St. Bees Head, currents, 32
Radioactivity in surface and coastal waters St. Croix, Virgin Island, Zostera marina
of British Isles, 11 cultures, 321
Radionuclides in corals, 203 St. George’s Channel, Irish Sea, 12, 13, 14,
Radium in corals, 201 24, 25, 33
“Radius ratio” in aragonite structure, 199 St. Lawrence River estuary, estuarine
,, calcite structure, 199 front, 148
Raman scattering, 62, 78, 79 „ phytoplankton, 130, 131
Rate-controlling enzymes, 273, 275 „ stratification, 135
Rayleigh scattering, 62 „ variations in outflow, 156
Recording current meters and numerical St. Margaret's Bay, Nova Scotia,
models, 18–23 chaetognaths, 384, 387, 388
Red Sea brines, manganese, 185 Salamanders, 560, 561
„ corals, 206 Salinity, Irish Sea, 13–17
„ mine tailings discharged into, 196 Sanderling, southern Africa, 516
Redshank feeding of, 450 Sandpipers, wintering grounds, 516
Red-tide dinoflagellates, 147 San Juan Island, Washington, glycogen in
Red tides and fish kills, 118 polychaetes, 289, 290
Regulatory influences of rate-controlling „ Macoma spp., G.P.I. locus, 569
reactions of carbohydrate catabolism, Santorini, Aegean Sea, manganese, 184
276 Sardine eggs, distribution of, 155
Remote sensing, SEASAT, 55 Sargasso Sea, an oceanic desert, 156
Resources, nature of and species, 556–559 „ phytoplankton, 129
Retrograde fronts, defined, 142 Satellite images of surface temperature and
Reynolds stress terms, 151 phytoplankton pigments, Vancouver
Rhamnose in marine angiosperm pollen, Island, Fig 3 (Denman & Powell) facing
328 p. 131
Rhodochrosite in Deep-Sea Drilling „ shallow sea fronts, 146
Project cores, 170 „ remote sensing, 132, 154
„ Loch Fyne, U.K., 170 Scandium in corals, 200, 202
„ manganese carbonate, 170 Schooling of fish, effect on predation, 450
„ Panama Basin, eastern Pacific, 170 Sclerotin, 205
RNA in marine angiosperm pollen, 327 Scotland, mysids, 408, 412
„ pollen, 329 Scottish shores, currents, 25
River Amazon discharge, 62 „ fucoid zonation, 485
Rock lobster larvae on west Australian Scripps Institution of Oceanography, 59
shelf, 155 „ pier, diatom blooms, 155
Ronaldsway, weather reports, 36
SCUBA diving for observing South Africa, limpets, 474, 475

chaetognaths, 360 388 „ speciation from north to south and vice-
Sea cows, impact on algal beds, 489 versa, 577, 578, 579
Seagrass biology, 317 South African anchovy-pilchard fishery,
Seagrasses, flowering and nutrients, 323 517
„ laboratory culture, 338 „ Atlantic Bight, eddy exchanges, 154
„ type of species, 316 „ Californian Bight, boundary of, 131
Seals, haul-out areas, 489, 538 Southern hemisphere, mysids, 412
SEASAT remote sensing, 55 „ Ocean, chaetognaths, 362, 372
Seasonal thermoclines, 133, 136 „ oscillation, 157
Sea water, manganese, 171–174 Soviet Union, freshwater ferromanganese
Sea-water phototube assembly for concretions, 174
measuring bioluminescence, 75, 76 Space and time scales of variation, 126
Self-pollination (geitonogamy) prevented Spatial scales sampled by various instru-
by dichogamy, 316 ments. 92
Sellafield, Irish Sea, 13, 15 Species abundance biomass (SAB) diagram
„ bed load transport, 49 for macrobenthic invertebrates, 301
„ caesium 137 Spectral radiometers, 79–80
„ discharge, 33 Sporopollenin, component of exine, 332
„ currents, 40, 44, 46, 50 Squires Cate, near Blackpool, Irish Sea,
„ effluent from, 12, 23, 32, 33, 50 weather reports, 36, 38
Sensitivity of invertebrates to Starvation in chaetognaths, 385
environmental changes, ecological Station Papa, 133, 134
considerations, 285–304 Stigma, marine angiosperms, 334–335
Sensory hairs of chaetognaths, 354–356 „ non-papillate surface, 335
Serotonin (5-hydroxytryptamine), 268, 269 „ papillate surface, 334
Sewage effluents, effect on coral reefs, 196 „ receptive surface, 334
Sexine bacula, marine angiosperm pollen, „ papillae, Fig 9 (Pettitt) between pp. 334
326 and 335
Shallow sea fronts, 146–147 „ surface and pollen shape, 334
Sheldon spectrum, 77 „ cytochemical analysis, 334
Shelf break fronts, 142–143 „ enzyme activation, 316
„ edge canyons, 152–153 „ esterase, 334
„ waves, 149 „ protein, 334
Silurian communities, layering of fossil „ ultrastructure, 334, 335
deposits, 503 Stochastic models and production, 135
Silver in corals, 200, 202 Stoke’s Law, fluorescence, 66, 67
‘Slab models’ to simulate deepening of Stoke’s shift, 66
mixed layer, 133 Stoke’s velocity, 30
Smoky Mountains, salamanders, 560, 561 Storm surges, Irish Sea, 151
Snapper shrimps, aggression in, 451 Stratification and depth-scaled by
Society Island, chaetognaths, 372 transparency, 107
Sodium in corals, 200, 202 Strontium 90, 11
Solway Firth, currents, 32, 39 „ in copepods, 198
Somalia, Indian Ocean, biological regime, „ in corals, 200, 201, 202
156 „ input to sediments from oil platforms,
„ southwest-monsoon, 156 196
Soret absorption bands, 59 Submarine canyons, currents in, 152
SUBJECT INDEX 693
Submersibles, evidence of hydrothermal Trace metal chemistry of sea water, 172

emanations, 184 Trans-Atlantic Geotraverse (TAG) hydro-
Succession, mechanisms of, 542 thermal field, 184
Succinate pathway of anaerobic Transient thermoclines, 133
catabolism, 283 Transmissometer, 73, 91, 94
Sunfish, 527 „ schematic, 70
Suruga Bay, Japan, chaetognaths, 362, Transmissometry, 70–72
382, 388 Tropical environments, sources of heavy
Swedish lakes, isopod, 396 metal pollution, 195–196
„ myspids, 410 Trypsin, 278
Synoptic meteorological ‘event’ scales, Turbidity in nearshore zones, 132
132, 133 Turbulence at sea surface, 133
„ meteorology time scale, 149, 150 Turbulent mixing and phytoplankton, 135
Syringodium filiforme, enzyme systems, Turner III Design, fluorometer, 72, 73, 74,
322 77
„ flowering in culture, 322 Tyrrhenian Sea, manganese on volcanic
„ isoetifolium, flowering 323, 324 sea-mounts, 183
„ mysids, 408
Tellurium in corals, 200
Temperature and flowering of Zostera Ultrastructure of marine angiosperm
marina, 317, 318 pollen, 326
„ pollen release in Zostera marina, 319 „ pollen, 328, 329, 330, 332, 333
„ Irish Sea, 13–17 „ stigma surface, 334, 335
Temporal and spatial scales, planktonic U.V. absorption microscope, 67
eco-systems, 128–132 United Kingdom estuaries, manganese, 178
Terbium in corals, 204 United States, shelf break fronts, 142
Terns, on Christmas Island, 515 „ estuaries, manganese, 178
Territoriality in fish, 520, 521, 522 „ west coast, manganese, 179
Texas, Syringodium filiforme, 322 Upper ocean processes and planktonic eco-
„ Zostera marina cultures, 321 systems, 132 138
Thailand, Conus sp., 461 Upwelling, coastal, British Columbia, 131
„ corals, 203 „ effect on biota, 125
„ mining and dredging operations, 195, 196 „ Washington, 131
Thalassia hemprichii cultures, 324 „ ecosystems, 149–151; 136
„ flowering rhythm in Kenya, 324, 325 Upwelling fronts, 143–145; 142
Thermal discharges as a source of metals in „ regions and fish production, 118
ionic form, 196 „ systems, conference on, 149
Thermocline fronts, 142 „ three ‘event’ time scales, 150
Thursday Island, Queensland, Cymodocea „ wind-driven, 149
serrulata 323 „ zone, zooplankton, 150
Tidal Currents, Irish Sea, 25–27 Uranium in corals, 200, 202, 203, 204, 205
Tides, Irish Sea, 23–27
Time-space domains for oceanic Valley weather station wind stress, 36, 37,
phenomena, 56 38, 39, 40, 42, 43, 44, 45
Tin in corals, 201 Vancouver Island, nutrient-rich water, 156
Titanium in corals, 200 Vertical mixing and primary production,
Total dissolvable manganese (TDM), 172 100–109
Vineyard Sound, Mass., chaetognaths, 372, „ microzones, 116

376, 382, 389 Zooxan thellae of corals and calcium
Virgin Islands, Syringodium filiforme, 322 deposition, 198
Virginia continental shelf, chaetognaths, „ influence on arsenic uptake, 198, 199
362, 376, 381, 382, 387 „ influence on strontium in skeleton, 198
„ influence on uranium in skeleton, 198
Water colour as a source of information, Zostera marina, annual, a natural ecopheno
57–66 type, 318, 319
West Africa, frontal circulations and zoo- „ and perennial forms 318
plankton, 144 „ dichogamous devel opment, 320
„ variability of production cycle, 151 „ ecophenotype, pollination of 335
West Australian continental shelf, „ anther depiscence, 319, 320
impinging eddies, 154 „ diclinous species and proto gyny, 319
„ larvae of rock lobster, 155 „ flowering and temperature 317, 318, 321
Western Europe continental shelf, „ homogamy, 319
ecosystems, 157 „ pollination, 335–366
Whales, decline of, and increase of
penguins and crabeater seals, 518
White-fronted sandplover, southern Africa,
515, 516
Wind-driven upwelling of Oregon and
Washington, U.S.A., 156
Winds, effect on primary production, 136
Windscale effluent, 44
Woodhead sea-bed drifters for measuring
currents, 32
Xylose in pollen, 328
Yellow substances, light absorption by, 61–

62
„ Gelbstoff, 58, 60, 61, 62, 70, 71, 81,
Yttrium in corals, 200
Zinc effect on phosphoglucose isomerase

genotypes, 282
,, in chiton, 205
„ copepods, 198
„ corals, 200, 201, 202, 203
„ sea water, 172
,, input to sediments from oil platforms,
196
Zinc sulphide in Atlantis II Deep
sediments, 195, 196
Zooplankton, definition of, 99
„ excretion creating microenvironments,
159

(Oceanography and Marine Biology 22) Harold Barnes (Ed.), Margaret Barnes (Ed.) - Oceanography and Marine Biology, Vol. 22-Aberdeen University Press (1984)

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(Oceanography and Marine Biology 22) Harold Barnes (Ed.), Margaret Barnes (Ed.) - Oceanography and Marine Biology, Vol. 22-Aberdeen University Press (1984)

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OCEANOGRAPHY AND

HAROLD BARNES, Founder Editor

MARGARET BARNES, Editor

ABERDEEN UNIVERSITY PRESS

ISBN 0-203-40062-3 Master e-book ISBN

ISBN 0-203-70886-5 (Adobe eReader Format)

Currents in the Eastern Irish Sea 2

Ecophysiology of Marsupial Development and Reproduction in 417

AUTHOR INDEX 628

Manuscripts continue to be submitted to this series of Annual Reviews. The

Oceanogr. Mar. Biol. Ann. Rev., 1984, 22, 11–53

SALINITY, TEMPERATURE AND DENSITY

RECORDING CURRENT METERS

Speed (m/s), Range : 0·025 to 2·5, threshold 0·02

themselves studied, their relative importance determined or changes in their

At these frequencies the dominant mechanism for dissipation is, however,

Two-dimensional models, with or without advection and with quadratic bottom

vertical—here two-dimensional models can give misleading results. An

then the mean of U3 over a tidal cycle, ξ 3, is given by

LOW FREQUENCY CURRENTS

Horizontal density gradients

where the overbar denotes a time average (Longuet-Higgins, 1969).

There are two length scales—the M2 wavelength ( if

Barrow-in-Furness measurements were made over one tidal cycle by deploying

the measurements of Williamson (1952, 1956a), Sharaf el Din (1970, 1972)

Site (Vector mean speed)2 (m/s) Variance (m/s)2×10−5 % Variance explained by

included—their (observed—wind fitted) variance was reduced to 0·0011 m2/s2—

Site Position Water Meter Record Response to 1 Pa stress

Fig. 13.—Predicted response by Proctor’s (1981) three-dimensional numerical model of

LOW FREQUENCY CURRENTS

MOVEMENT OF RADIOACTIVE WASTE

The important gap in our knowledge is the movement of radionuclides in the

Kautsky, H., 1981. Dt. hydrogr. Z., 34, 125–148.

Simpson, J.H., 1971. Deep-Sea Res., 18, 309–319.

Oceanogr. Mar. Biol. Ann. Rev., 1984, 22, 55–98

THE TIME-SPACE DILEMMA

Fig. 1.—Time-space domains for oceanic phenomena as described by Esaias (1980). A,

important unifying characteristic of important modern instrument advances is

WHY ARE OPTICAL INSTRUMENTS IDEAL TO TEST

Fig. 2.—Absorption of light. A, by water absorption. B, by different algal pigments in the

WATER COLOUR AS A SOURCE OF INFORMATION

maximum theoretical yield of primary production (Steele & Menzel, 1962;

LIGHT ABSORPTION BY INORGANIC PARTICLES

Fig. 3.—Contribution of phytoplankton (scattering plus absorption) and water (scattering

LIGHT ABSORPTION BY DISSOLVED YELLOW

Fig. 5.—Contribution to light attenuation (per metre) of yellow substances to water

Yellow substances ‘compete’ with phytoplankton for short wavelength light

Fig. 6.—Logarithmic scattering diagram showing angular variability from an individual

LIGHT SCATTERING BY WATER

LIGHT SCATTERING BY PARTICLES

Fig. 7—Percentage of light transmitted at various depths for particles of 2 μ m and 5 μ m

Fig. 11.—Schematic representation of importance of size, refractive index and slope to

LIGHT EMITTED BY BIOLOGICAL PROCESSES

FLUORESCENCE EMISSION BY THE PHYTOPLANKTON

found immense differences in fluorescence according to growth state. The

TABLE I Table of early significant advances in the application of fluorescent techniques

Year Event Individual

We know from microscopic counts of microorganisms in the sea that the

A strong emission peak at 570–580 nm is present in every measurement. The

WHOLE POPULATION INSTRUMENTS

most part, investigators requiring a measure of total scattering use an instrument

Fig. 14.—Schematic of transmissometer or beam attenuation meter: courtesy of Sea Tech,

Fig. 15.—Data from Spinrad et al. (1978) demonstrating additional information on