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Our perceptions of phytoplankton: an historical

sketch the first Founders' Lecture

G.E. Fogg

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Br. phycol. J. 25:103-115
1 June 1990

Our Perceptions of Phytoplankton: an Historical Sketch

The First Founders' Lecture*

By G. E. FOGG

School of Ocean Sciences,

(University College of North Wales),
Marine Science Laboratories, Menai Bridge,
Anglesey, Gwynedd LL59 5EY, UK

The wide distribution, abundance and general ecological significance of phytoplankton was
first recognized by J. D. Hooker in 1847 as a result of his observations during an Antarctic
cruise. The introduction of the fine-meshed silk plankton net at about the same time led to a
great expansion of interest and a realization of the enormous variety of phytoplankton
species. The net, however, has its disadvantages and three lines of enquiry which were
neglected through over-reliance on it are considered. Following the pioneer work of Lohmann
in 1911 it was belatedly realized that the small forms which pass through the net are an
important and active fraction which forms a somewhat separate community different in its
dynamics from that of the larger plankton forms. The patchiness of phytoplankton distribu-
tion, obscured by net sampling, can now be studied by continuous recording techniques, aerial
photography and remote sensing from satellites and is found to be related in complex ways to
hydrographic features. Investigation of the metabolic activities of phytoplankton, which also
cannot properly be studied with net samples, was at first largely confined to determinations of
primary productivity. Recently, detailed biochemical studies have been carried out in situ and
the involvement of biogeochemical processes brought about by phytoplankton in global
climatic changes has been postulated.

I am deeply honoured to have been invited same indefinable assemblage of organisms,

to give the first Founders' Lecture of the
British Phycological Society. I cannot claim
the distinction of having been a founder
member; the Society came into being here in
Bangor in September 1951 as a result of
proposals made by an ad hoe committee o f
seven distinguished lady phycologists with
two male colleagues, one of whom was given
the task of being secretary as a gesture
towards equality of the sexes (Powell, 1952).
With great wisdom, our Founding Aunts, if I
may so call them, avoided any definition of
the scope of the Society, with the happy
result that taxonomists and biochemists,
geneticists and ecologists, who have it in
c o m m o n only that they are interested in the
*Delivered on 5 January 1990 at the Annual Meeting of
the Society held at the University College of North
Wales, Bangor.
forgather to their immense mutual benefit.
Phytoplankton, of course, falls well within
the Society's ambit but, as I hope to show,
our present perceptions of this form of algal
life reach to horizons that were undreamed
of even twenty years ago.
Phytoplankton is not usually obvious but
sometimes does occur in such abundance as
to attract attention and the comment of
writers such as the author of the Book of
Exodus, Giraldus Cambrensis and Shakes-
peare. If they thought about it at all our
forbears put such manifestations down as
supernatural portents without enquiring into
proximate causes. Antoni van Leeuwen-
hoeck in 1674 looked at the material forming
green clouds in the waters of a Dutch lake
with his microscope and described what we
think must have been a Spirogyra-- hardly a
typical plankton organism. Joseph Banks

0007-1617/90/020103 + 13 $03.00/0 © 1990 British PhycologicalSociety

¢:,
 Our perceptions of phytoplankton
accompanying James Cook on his voyage of
1768-71 to the South Seas in the Endeavour
examined what the sailors called "sea saw-
dust", Oscillatoria (Trichodesmium) spp.,
but could not decide whether it was animal
or vegetable. These were isolated observa-
tions and did not lead to any further enquir-
ies. The more subtle colours of water have
been used from the earliest times by seafarers
as a navigational aid but the first to realize
that colour has biological significance seems
to have been the whaling captain William
Scoresby. In his classic book An Account o f
the Arctic Regions published in 1820 he
described the distribution of water of
different colours, distinguishing those that
were blue and more transparent from those
which were opaque and green. The latter,
which were favoured by whales, he found to
owe their colour to the presence of innumer-
able minute organisms. Among those he
described what were clearly chains of
diatoms such as Thalassiosira and Chaeto-
ceros, although his illustrations of these are
on too small a scale and far less satisfactory
than those which he published of the larger
zooplankton. Scoresby was an outstanding
pioneer in oceanography, consorted with
many of the leading scientists of his age and
was elected to the Royal Society but
somehow this work was not followed up.
This might have been partly because the
Royal Navy regarded exploration and
research in the polar regions as its preserve
and for a long time treated Scoresby as an
interloper (Stamp, 1975).
What must be regarded as the real begin-
nings of the scientific study of phytop-
lankton (Taylor, 1980) did come from a
naval source. This was the voyage o f H.M.
ships Erebus and Terror to the Antarctic
under the command o f Captain James Clark
Ross in 1839-43. The assistant surgeon on
FIG. 1. Drawings of phytoplankton ("infusoria") made during the voyageof H.M.S. Erebus to Antarctica, 1839-43,
by Joseph Hooker, including (top left) Dictyocha sp.; (top right) Fragilariopsis sp.; centric diatoms, (bottom left)
Melosira sp.; (bottom right) Trichodesmium sp. See Davenport & Fogg, (1989) for further details. Courtesy of the
Director and Trustees of the Natural History Museum.
105
the Erebus was a young man, Joseph Dalton
Hooker, later to become Director of the
Royal Botanic Gardens, Kew, and one of the
most distinguished higher plant taxonomists
of his time. Already he was devoted to
flowering plants and had taken a crash
course in medicine only to be able to join the
expedition but, of course, he was somewhat
frustrated in his botanizing in the far south.
To fill in time usefully he assisted his captain,
who was an amateur zoologist, in collecting
planktonic invertebrates (Davenport &
Fogg, 1989). In doing this he came across
various minute organisms which he drew
without giving them names but which we can
now see as some of the earliest illustrations
of phytoplankton (Fig. 1). He further
noticed that the guts of zooplankton often
contained diatoms and that these also
became concentrated in freshly formed ice
(see Garrison, Close & Reimnitz, 1989).
Many Antarctic voyagers from Cook
onwards had noticed that pack ice was often
stained brown on its underside but had put
this down as earthy material indicating a
terrestrial origin for the ice. With Mount
Erebus in eruption as the Erebus and Terror
sailed by, the brown material was thought by
Ross to be volcanic ash. Hooker, however,
looked at it under the microscope and found
that diatoms were responsible. At that time
all microscopic life in the sea was put under
the headings of "infusoria" or "animal-
culae" and the expert on such things was the
German protozoologist C . G . Ehrenberg,
who was convinced that diatoms were
a n i m a l s - the chromatophores were ovaries.
The material collected by Hooker was sent
to Ehrenberg who described it accurately-
- - m a n y of the names he gave are still being
used t o d a y - - b u t classified the organisms as
"siliceous-shelled polygastrica" (Ross, 1847).
When he returned home and was writing up
106 G.E. Fogg
his work Hooker was in a quandary as to
whether these forms should go into his Flora
Antarctica or not, but, as he wrote:
Within these very few days, it was the
singular good fortune of my friend, Mr
Thwaites of Bristol, a most acute
observer and profound Cryptogamist,
to detect several species of Diatomaceae
conjugating, in a manner perfectly
analogous to that pursued by the
Zygnemata: a fact which leaves no
doubt of their vegetable origin."
(Hooker, 1847, p. 503).
This settled, he went on to set out for the
first time the essential nature of the phytop-
lankton: that although normally invisible
they are extremely abundant in the sea
(evidence for this being the existence of vast
sedimentary deposits which could only have
been formed by accumulation of their sili-
ceous tests at the sea bottom) and distributed
from pole to pole; that they are the main
food source of marine animals (he had been
puzzled by the abundance of animal life in
Antarctic seas without any obvious source of
food); and, like trees and grass, were prob-
ably also "purifiers of the vitiated
atmosphere".
Hooker used a tow-net to collect zoop-
lankton, as had others before him, including
Charles Darwin, but the material used was
linen, bunting or similar relatively coarse
fabric not adapted for straining off phytop-
lankton. It seems to have been the German
naturalist Johannes M/iller, who, although
not the inventor of the tow net as is some-
times supposed (Hardy, 1956), first started
using, in 1844, fine mesh silk of the sort used
in the milling industry for grading flour. By
this means the extraordinary diverse commu-
nity of minute organisms that live suspended
in water was revealed. Both freshwater and
marine biologists rushed with enthusiasm
into this new field and an expedition in the
steamer National, which cruised the North
Atlantic in 1889 under the leadership of
Victor Hensen, was supported by the
German Emperor, no less, and was specifi-
cally devoted to plankton. It was Hensen
who first used the word "plankton" and
employed plankton nets in a quantitative
manner (Schlee, 1973). It is not my intention
to review the history of the whole field of
phytoplankton research which followed, but
to concentrate on three lines of development
away from the limited view given by the net.
Admirable though the net has been in estab-
lishing the variety, distribution and periodi-
city of the larger phytoplankton, it suffers
from three serious disadvantages:
(1) The spaces between the meshes of the
finest silk are about 701xm wide (or in
modern nylon fabrics, 35 ~tm or even down
to 5 ~tm) so that organisms smaller than this
are not collected.
(2) The net essentially collects an inte-
grated sample and thus tells us nothing of
variations in phytoplankton density over the
distance or time for which it was towed.
(3) The sample, being selective, concen-
trated and possibly damaged, cannot be used
for determination of the physiological or
biochemical activity of the original
community.
Realization of these limitations has been
slow but, once it came, has extended our
perceptions of phytoplankton enormously.
The American worker, C.A. Kofoid,
pointed out in 1897 the error arising from
loss of the smaller forms and advocated
centrifugation as a better means of collec-
tion, but it was the German zoologist H.
Lohmann, who in 1911 really demonstrated
the importance of what was being missed. In
the course of a study of appendicularians
--planktonic animals which have an
elaborate and effective mechanism for
filtering extremely fine particles from sea-
water--his attention was attracted by the
minute organisms which they caught. He
concentrated water samples by centrifuga-
tion and found a variety of forms--bacteria,
yeasts and coccoid blue-green algae--too
small to be retained by the finest nets
(Fig. 2). He was not able to assess their
biomass but surmised that because their
metabolic rate was presumably high they
were probably more important in the
economy of natural waters than the larger
 Our perceptions of phytoplankton 107

FIG. 2. Drawing from Lohmann (1911) showing phytoplankton in relation to the meshes (holes about 70 lam
diameter at their widest) of a bolting-silk plankton net.

forms. A plant physiologist of that time
would surely have agreed with him; the high
surface/volume ratio of small organisms
enables rapid uptake of nutrients and
together with their very slow sinking rate
confers competitive advantage, and it had
been generally observed that smaller organ-
isms multiply faster than bigger ones. Never-
theless, Lohmann's observations were not
followed up and most limnologists and bio-
logical oceanographers continued to think of
phytoplankton purely in terms of what could
be collected in a net. If organisms were not
easily seen and identifiable under the light
microscope there was a strong temptation to
ignore them.
However, by the 1950s a few people began
to take notice of the smaller forms. Again
the impetus was zoological. Mary Parke
--President of the Society 1959-60---became
involved in the rearing of oyster larvae and
realized that nothing was known about the
flagellate forms of 1"5 to 7 ~tm in size which
proved most suitable for their diet (Bruce,
Knight & Parke, 1940). She found that the
best way to study them was by growth in
unialgal culture and began a series of investi-
gations, some in collaboration with Irene
108 G.E. Fogg

Manton, of organisms such as Chrysochro-
mulina (Parke, Manton & Clarke, 1955) and
others, which have become classics. A little
later Wilhelm Rodhe (1955) in Sweden
pointed out the importance of what he called
la-algae for the maintenance of zooplankton
during the winter in sub-arctic lakes while
John Lund--President of the Society 1957-
5 8 - f o u n d similar algae in the English Lakes
and reported on their periodicity (Lund,
1961). Such studies drew attention to the
nanoplankton size group (2-20 I~m) but the
still smaller forms remained uninvestigated
until, in the late 1970s, the fluorescence
microscope was used by Johnson & Sieburth
(1979) and Waterbury et al. (1979) to
demonstrate the widespread occurrence, in
substantial concentrations in the surface
waters of the sea, of picoplanktonic algae in
the size range 0-2-2 lam. There is even a level
below this. Bergh et al. (1989) have found up
to 2-5 x 108 bacteriophage particles per ml in
a variety of waters, both fresh and salt. We
have scarcely any idea of the biological
implications of this; with such concentra-
tions the chances of infection seem high for
the larger forms and a considerable amount
of dissolved organic material is presumably
liberated into the water by lysis of cells.
At this size level we enter a new world,
conditions of life being very different from
those in the planktonic environment as we
are accustomed to think of it. In this world
flow is viscous rather than turbulent so that
molecular diffusion is the dominant process
transporting material to and from the cells.
Because diffusion gradients become effec-
tively steepened about a curved surface (the
steady state flux being inversely proportional
to the square of the radius) this transport is
extremely rapid so that, for example, the flux
of phosphate to cells 1 Ixm in diameter from
a low bulk phase concentration is several
hundred times faster than is needed to
sustain the maximum rate of growth (Raven,
1986). We can visualize each cell as the
centre of an activity domain and if, with
Azam & Ammerman (1984), we arbitrarily
put the boundary of this where the concen-
tration of a released metabolite falls to 10%
of what it is at the cell surface, then the
domain of a 2/am cell has a radius of 10 ~tm
and that of a 20 Ixm cell a radius of 100 lain.
Thus if cells are uniformly distributed their
domains do not overlap (Table I). Motile
bacteria can move up to a cell or particle
which is releasing dissolved organic matter,
and phagotrophic flagellates can swim from
one morsel of food to another in a few
minutes. The presence of micro- and meso-
plankton seems almost irrelevant for this
ultraplankton (a convenient term embracing
both the pico- and nano-plankton) commu-
nity, the components of which are better
placed for, and more efficient in, uptake of
dissolved nutrients. It is striking that the

TABLE I. Some approximate distances and speeds in the planktonic community.

Mainly after Fogg, (1986) but with additional data from aBergh et al., (1989) and
bAzam & Ammerman, 0984)

,am

Distance between virus particles) 20

Picoplankton diameter 0-2-2-0
Distance between heterotrophs (106 cells ml 1) I00
Distance between phototrophs (104 cells ml -l) 465
Distance swum in 1 s by heterotrophs 20-40
Radius of activity domain of 2 `am cellb 10
Nanoplankton diameter 2.0-20
Distance between predators (10~ cells ml -t) 1000
Distance swum in 1 s by predators 150
Radius of activity domain of 20 `am cellb 100
Microplankton diameter 20-200
Distance between phototrophs (103 cells ml -~) 1000
Mesoplankton diameter 200-20,000
Distance between herbivores 100,000
 Our perceptions of phytoplankton
ultraplanktonic community seems to be
present in most kinds of water and that the
numbers per unit volume of bacteria, of
phytopicoplankton and of nanoplanktonic
predators are always about the same (Fogg,
1986). This suggests that it is a basic commu-
nity with a composition presumably deter-
mined by rates of exchange of materials and
swimming speeds of predators. It seems to be
self-contained with little of its biomass
getting through to higher trophic levels.
Lohmann was right, it does seem that it is
the ultraplankton which is most active
and largely responsible for mineral cycling in
open waters. The system is a highly dynamic
one with a short response time to changing
conditions. Sieburth (1984) speculated about
the dramatic changes taking place in what he
called the "microlitersphere" over the diel
cycle and Wheeler et al. (1989) have demon-
strated that such changes do actually take
place as far as the nitrogen cycle is
concerned. Activities of phototrophs and
heterotrophs are so intimately interwoven
that it is probably highly misleading to try to
consider them apart. Micro- and meso-
planktonic communities seem only to be
superimposed on this basic system when
nutrient supply is above a certain level
(Fogg, 1986). A fundamental difference
between the two levels of planktonic exis-
tence seems to be indicated by their different
life forms. Whereas picoplankton cells tend
to be simple and often spherical, micro-
plankton cells are usually elaborate in form
or elongate in shape, and with protuberances
and spines. This elaboration serves to
increase form resistance and hence to reduce
sinking rate and, as Reynolds (1984) has
pointed out, to promote entrainment in
turbulent flows.
Looking in the other direction, to the large
scale, the striking feature is the uneven distri-
bution of phytoplankton. It has always been
obvious that water blooms tend to collect in
patches and slicks. The first studies of patchy
distribution on the larger, 100 km, scale were
made by Alister Hardy with his continuous
plankton recorder. He devised this primarily
for the study of zooplankton in Antarctic
109
waters and it was first successfully used in
the Drake Passage, one of the most tempes-
tuous sea areas that there is. The gauze on
which the samples were collected was rela-
tively coarse but sufficed to catch the larger
dinoflagellates and to show that there can be
considerable variation in numbers of these
organisms along a linear transect (Hardy,
1956). However, this scarcely prepares one
for the picture which can be seen from an
aircraft (Fig. 3) and aerial photography, first
used seriously for this purpose, I believe, by
Wrigley & Home (1974) reveals the full
complexity of distribution patterns. False
colour enhancement images obtained by
satellite, as with the Nimbus-7 Coastal Zone
Colour Scanner, are even more spectacular
and informative, although one always has to
remember that only the surface concentra-
tions of chlorophyll are being picked up.
The distribution often seems chaotic and,
indeed, to some extent it is; the confused and
erratic nature of fluid turbulence is one of
the least understood aspects of classical
physics and virtually impossible to describe
in mathematical form (Mullin, 1989). Never-
theless, phytoplankton distribution is often
clearly related to definitive hydrographic
features. The occurrence of high concentra-
tions in regions of upwelling of nutrient-rich
water was suggested by Nathansohn (1906)
and studied in pioneering work by Strickland
(1972). A particularly clear in situ demonst-
ration of the association of phytoplankton
distribution with a specific hydrographic
structure was that of Pingree et al. (1975)
when they showed that a "red tide" of Gyro-
dinium aureolum Hulburt off Ushant was
related to a front. The cause of this pheno-
menon is still arguable, probably a combina-
tion of different processes, both physical and
biological, is involved (Fogg et al., 1985) but
water movement, through its control of
access to light and nutrients, appears more
and more to be the major factor affecting the
growth of phytoplankton. We have been
slow to realise that water bodies may be
structured. Sometimes surface slicks may
indicate that the water below has structured
movement but the idea that in a stirred water
 .m

QtQ

FIG. 3. Vertical aerial photograph of a Trichodesmium bloom east of the Whitsunday Group of islands, Great Barrier Reef. Courtesy of L. Zell, Great
Barrier Reef Marine Park Authority, Queensland, Australia.
 Our perceptions of phytoplankton
body islands of unmixed water may be
formed and persist for long periods
(Wiggins, 1988) has not been sufficiently
explored by phytoplanktonologists. Even
small scale vortices in rivers may retain their
identities for days (Fig. 4) and the rings
which peel off from the Gulf Stream are
known to persist in the open ocean for
several years (Richardson, 1983). These life
times may thus be long relative to the
generation times of phytoplankton so that
we can imagine communities being main-
tained in particular structures in a turbulent
water body. I believe that this may often be
the explanation for patchy distributions.
Thus the variation in phytoplankton distri-
bution, as measured by chlorophyll fluores-
cence in the sea area to the east of the South
Sandwich Islands, a particularly well-mixed
body of water, does not seem explicable in
terms of light, nutrients, temperature or
water-column stability but is strongly corre-
lated with depth (Hayes, Whitaker & Fogg,
1984). The ocean thereabouts is up to 5 km
in depth but features of bottom topography
might nevertheless produce matching
standing eddies at the surface, holding
phytoplankton populations, in the Circum-
polar Current flowing over them. These are
but pointers to what seems to be an impor-
tant and scarcely touched field of enquiry.
The third extension of our perception of
phytoplankton takes in its biogeochemical
aspect. Hooker (1847) recognized its role as
the main food source for marine life and the
magnitude of the deposits accumulated as
the result of the secretion of silica by
diatoms. Hensen in 1887 obtained rough
estimates of cell concentrations but little
progress was made in characterizing and
quantifying the metabolic activities of
phytoplankton for yet another forty years.
A.H. Church, a botanist of wide interests
who is now chiefly remembered for his
beautiful illustrations of flower pollination
mechanisms, returned to the problem in 1919
with a paper on what he called the
"plankton-rate". This was not actually a rate
but a concentration, and apart from drawing
attention to lack of knowledge of something
111
that was of fundamental importance in
aquatic biology did not really make much
contribution. The problem of the magnitude
of production was first approached by
Lohmann and others by studying changes in
numbers, an obviously unreliable method.
Moore, Prideaux & Herdman (1915) at Port
Erin made estimates of phytoplankton
production from seasonal changes in alkali-
nity, which were related to carbon dioxide
uptake. W. R. G. Atkins (1926) did similar
measurements and found that production
estimated from the results agreed with that
based on phosphate uptake. Such estimates
were derived from measurements made in
the unconfined water column. Containment
of samples in bottles was the next step and
brought problems which are still unresolved
(Fogg & Calvario-Martinez, 1989). The
method of oxygen determinations in light
and dark bottles was introduced by Gaarder
& Gran (1927) as a means of estimating
primary productivity. The respective esti-
mates, 1400 metric tons wet weight ( ~ 140
metric tons carbon) per km 2 per annum for
the English Channel by Atkins, and 2.4
metric tons glucose ( ,-~ 1 metric ton carbon)
per km 2 per day foi the Oslo Fjord in spring
and autumn by Gaarder & Gran, are within
the same range as recent estimates. Steemann
Nielsen's (1952) radiocarbon technique for
determining marine primary productivity
was far more sensitive than either of these
other methods and was quickly applied to
freshwaters by Rodhe and his colleagues
(1958). This technique was, seemingly,
extremely accurate and reproducable but the
more that people have thought about what is
actually being measured the less certain they
have become (Gieskes & Kraay, 1984). This
is no place to review the various attempts
that have been made to estimate the total
primary productivity of the oceans, which is
very largely contributed by phytoplankton,
but the consensus seems to be that it is of the
order of 3 x 101° metric tons of carbon per
year, that is, about the same as for the land
(Platt & Subba Rao, 1975). To think of this
production merely in terms of carbon in
particulate form is to miss all the intricate
 O

FIG. 4. Toroid accumulation of foam on river, Corral Glen, Co. Fermanagh, N. Ireland, outside diameter about 60 cm. Photo G. E. Fogg.
 Our perceptions of phytoplankton
detail of the cycling of organic matter in the
sea. A simple modification of the original
Steemann Nielsen technique enabled deter-
mination of the proportion of photosyn-
thetic product which is liberated in
extracellular form (Fogg, 1958) and it now
seems generally accepted that such release by
healthy cells feeds into the ultraplanktonic
level and provides a substantial energy
source for the heterotrophic microbial popu-
lations of lakes and seas (Jones & Cannon,
1986). A pioneer in conducting more detailed
biochemical work at sea on the products of
photosynthesis in phytoplankton and the
manner in which the balance between them
changes with environmental conditions and
the physiological state of the algae was the
late Ian Morris, a plant biochemist turned
oceanographer. He and his colleagues found
some surprisingly large shifts towards pro-
tein at low irradiances and towards fat in
cold polar waters which must have repercus-
sions all up the food chain (Morris, 1981).
The biochemical activities of phytop-
lankton, however, have effects extending out
of the sea into its deposits below and the
atmosphere above and these effects have
become of particular interest because of the
current concern about the global environ-
ment. It is obvious from the vast deposits of
chalk, which is largely composed of the
coccoliths of the Coccolithophoridaceae,
that massive transfer of carbon from atmo-
sphere to sea bottom has occurred in the
past. This process is undoubtedly offsetting
to some extent the present anthropogenic
increase of carbon dioxide in the atmosphere
and one would like to know whether it is
likely to provide negative feedback enough
to slow down the rate of this accumulation.
Emiliania huxleyi (Lohm.) Hay & Mohler,
the most abundant and most studied cocco-
lithophorid, should be favoured both by the
slight increase in the bicarbonate/carbon
dioxide ratio in sea-water brought about by
the rise in carbon dioxide concentration
(Pentecost, 1985) and by the rise in sea-
surface temperature (Braarud, 1962)
resulting from the "greenhouse" effect.
Increased growth of Emiliania would result
113
in increased coccolith formation and locking
up of carbon in marine deposits*. In the
present state of our knowledge it cannot be
said to what extent and how quickly this
feedback might operate. Another possible
feedback system affecting global heating may
operate via dimethylsulphide. Production of
this substance, although it may to some
extent be species specific, is now recognized
as an activity of marine phytoplankton
which results in a flux of sulphur from the
oceans to the atmosphere and thence to the
land (Savoie, Prosperor & Saltzman, 1989)
which is commensurate with the flux of anth-
ropogenic sulphur, one of the contributing
factors in "acid rain" (Turner et al., 1988).
Apart from this major role in the biogeoche-
mical cycling of sulphur, sulphate produced
by oxidation of dimethylsulphide provides
cloud condensation nuclei and it is argued
plausibly by Charlson et al. (1987) that this
provides a mechanism for biological regula-
tion of climate. Increased phytoplankton
growth might in this way lead to increase in
cloud albedo and thus might counteract the
warming effect due to increased carbon
dioxide concentration. This has been
regarded as a test case for the Gaia hypothe-
sis (Lovelock, 1989) but the evidence still
seems equivocal.
Our better perceptions of what phytop-
lankton is and does have thus taken us into
one of the most interesting developing fields
in marine microbiology, into oceanography
and the still unresolved problems of fluid
mechanics, and into the current anxieties
about the global environment. The British
Phycological Society, among its many other
interests, has a crucial role to play in conti-
nuing to provide a common focus for these
diverse perceptions.
ACKNOWLEDGEMENTS
I am grate]~ul to Dr H. Canter-Lund and Dr
E. G. Mitchelson for the loan of slides to illus-
*Proctor & Fuhrman (1990) have recentlyreported
that viral infection may account for 30% of
cyanobacterial and 60% of heterotrophic mortalityin
the sea and thus provide a significant pathway for
cyclingof carbon and nitrogen.
114 G . E . Fogg

trate the lecture, to the Director and Trustees of GARRISON, D. L., CLOSE,A. R. & REIMNITZ,E. (1989).
the Natural History Museum and to L. Zell of the Algae concentrated by frazil ice: evidence from
Great Barrier Reef Marine Park Authority for laboratory experiments and field measurements.
permission to use Figs 1 and 3 respectively, and Antarctic Science. 1: 313-316.
GmsKEs, W. W. C. & KRAAY,W. (1984). State-of-the-art
finally to D r G. T. Boalch for his helpful
in the measurement of primary production. In
comments. Flows o f Energy and Materials in Marine
Ecosystems (Fasham, M. J. R., editor), 171-190,
REFERENCES Plenum Press, New York.
HARDY, A. C. (1956). The Open Sea. Its Natural
ATKINS, W. R. G. (1926). A quantitative consideration History: The World o f Plankton. Collins,
of some factors concerned in plant growth in London.
water. Part II. Some chemical factors. J. Cons. HAYES, P. K., WHITAKER,T. M. & FOC,G, G. E. (1984).
Perm. Int. Explor. Met., 1: 197-226. The distribution and nutrient status of
AZAM, F. & AMMERMAN, J. W. (1984). Cycling of phytoplankton is the Southern Ocean between
organic matter by bacterioplankton in pelagic 20° and 70°W. Polar Biology, 3: 153-165.
marine ecosystems: microenvironmental HOOKER, J. D. (1847). The Botany o f the Antarctic
considerations. In Flow of Energy and Materials Voyage o f H.M. Discovery Ships Erebus and
in Marine Ecosystems (Fasham, M. J. R., editor), Terror in the Years 1839-1843. Reeve Bros.,
345-360, Plenum Press, New York. London, Reprint 1963, J. Cramer, Weinheim.
BERGH, O., BORSHEIM,K. Y., BRATBAK,G. & HELDAL, JOHNSON, P. W. & SmBURTH, J. McN. (1979).
M. (1989). High abundance of viruses found in Chroococcoid cyanobacteria in the sea: a
aquatic environments. Nature, Lond., 340: ubiquitous and diverse phototrophic biomass.
467-468. Limnol. Oceanogr., 24: 928-935.
BRAARUD, T. (1962). Species distribution in marine JONES, A. K. & CANNON, R. C. (1986). The release of
phytoplankton. J. oceanogr. Soc. Japan, 20th micro-algal photosynthate and associated
anniversary vol.: 628-649. bacterial uptake and heterotrophic growth. B?.
BRUCE, J. R., KNIGHT, M. & PARKE, M. (1940). The phycol. J., 21: 341-358.
rearing of oyster larvae on an algal diet. J. mar. LOHMANN,H. (1911). Ober das Nannoplankton und die
biol. Ass. U.K., 24: 337-374. Zentrifugierung kleinster Wasserproben zur
CHARt,SON, R. J., LOVELOCK,J. E., ANDREAE,M. O. & Gewinnung desselben in lebendem Zustande. Int.
WARREN, S. G. (1987). Oceanic phytoplankton, Rev. Gesamten Hydrobiol. Hydrogr., 4: 1-38.
atmospheric sulphur, cloud albedo and climate. LOVELOCK,J. E. (1989). Gaia. J. mar. biol. Ass. U.K., 69:
Nature, Lond., 326: 655-661. 746-758.
CHURCH, A. H. (1919). The plankton-phase and LUND, J. W. G. (1961). The periodicity of p:algae in
plankton-rate. J. Bot., June 1919 (supplement three English lakes. Verh. int. Ver. Limnol., 14:
III): 1-8. 147-154.
DAVENPORT,J. & FOGG, G. E. (1989). The invertebrate MOORE, B., PR1DEAUX, E. B. R. & HERDMAN, G. A.
collections of the Erebus and Terror Antarctic (1915). Studies of certain photo-synthetic
expedition; a missed opportunity. Polar Record, phenomena in sea-water. I Seasonal variations in
25: 323-327. the reaction of sea-water in relation to the
EHRENBERG,C. G. (1844). Resultate fiber das Verhalten activities of vegetable and animal plankton. II
des kleinsten Lebens in den Oceanen und den The limitations of photo-synthesis by algae in
gr6ssten bisher zug/inglichen Tiefen des sea-water. Proc. & Trans. Liverpool Biol. Soc.,
Weltmeers. Verhandl. d. KiJnigl. Preuss. Akad. d. 29: 233-264.
Wissenschaft. Berlin, 1844: 182-207. MORRIS, I. (1981). Photosynthetic products,
FOGG, G. E. (1958). Extrac.ellular products of physiological state, and phytoplankton growth.
phytoplankton and the estimation of primary Can. Bull. Fish. Aquat. Sci., 210: 83-102.
production. Rapp. P.-v. Bdun. Cons. perm. int. MULLm, T. (1989). Turbulent times for fluids. New
Explor. Mer., 144: 56-60. Scientist, no. 1690, 11 Nov. 1989, 52-55.
FOGG, G. E. (1986). Picoplankton. Proc. R. Soc. Lond. NATrIANSOI-IN,A. (1906). Uber die Bedeutung vertikaler
B228: 1-30. Wasserbewegungen ffir die Produktion des
FOGG, G. E. & CALVARIo-MARTINEZ,O. (1989). Effects Planktons im Mecre. Kdnigl. siichs. Gesells. d.
of bottle size in determinations of primary Wissensch., Leipzig, Abhandl. d. Math.-Phys.
productivity by phytoplankton. Hydrobiologia, Klasse, Bd 29, no. 5.
173: 89-94. PARKE, M., MANTON,I. & CLARKE,B. (1955). Studies on
FOGG, G. E., EGAN, B., FLOODGATE,G. D., JONES, D. marine flagellates. II. Three new species of
A., KAss~, J. Y., LOCHTE, K., REES, E. I. S., Chrysoehromulina. J. mar. biol. Ass. U.K., 34:
SCROPE-HOWE, S. & TURLEY, C. M. (1985). 579-609.
Biological studies in the vicinity of a shallow-sea PENTECOST, A. (1985). Photosynthetic plants as
tidal mixing front. VII. The frontal ecosystems. intermediary agents between environmental
Phil. Trans. R. Soe. Lond. B, 310: 555-571. HCO 3 and carbonate deposition. In Inorganic
GAARDER, T. & GRAN, H. H. (1927). Investigations of Carbon Uptake by Aquatic Photosynthetic
the production of plankton in the Oslo Fjord. Organisms (Lucas, W. J. & Berry, J. A., editors),
Rapp. P.-v. Rdun. Cons. perm. int. Explor. Mer., 459-480, American Society of Plant
42: 1-48. Physiologists, Rockville, Maryland.
 Our perceptions of phytoplankton
P1NGI(EE, R. D., PUGH, P. R., HOLLIGAN, P. M. &
FORSTER, G. R. (1975). Summer phytoplankton
blooms and red tides along tidal fronts in the
approaches to the English Channel. Nature,
Lond., 258: 627~77.
PLATT, T. & SUBBA RAO, n. V. (1975). Primary
production of marine microphytes. In
Photosynthesis and Productivity in Different
Environments (Cooper, J. P., editor), 249-280,
Cambridge University Press.
POWELL, H. T. (1952). Bangor Meeting, September
1951. British Phycological Bulletin, no. I: 1-2 (re-
issued June 1955).
PROCTOR, L. M., & FUrtRMAN, J. A. (1990). Viral
mortality of marine bacteria and cyanobacteria.
Nature, Lond., 343: 60-62.
RAV~N, J. A. (1986). Physiological consequences of
extremely small size for autotrophic organisms in
the sea. In Photosynthetic Picoplankton (Platt, T.
& Li, W. K. W., editors), 1-70, Can. Bull. Fish.
Aquat. Sci., 214.
REYNOLDS, C. S. (1984). The Ecology of Freshwater
Phytoplankton. Cambridge University Press.
RICHARDSON,P. L. (1983). Gulf stream rings. In Eddies
in Marine Science (Robinson, A. R., editor), 19-
45, Springer-Verlag, Berlin.
RODrtE, W. (1955). Can plankton production proceed
during winter darkness in sub-arctic lakes? Verh.
int. Ver. Limnol., 12, 117-122.
RODHE, W., VOLLENWEIDER,R. A. & NAUWERK, A.
(1958). The primary production and standing
crop of phytoplankton. In Perspectives in Marine
Biology (Buzzati-Traverso, A. A., editor), 299-
322, University of California Press, Berkeley and
Los Angeles.
Ross, J. C. (1847). A Voyage of Discovery and Research
in the Southern and Antarctic Regions During the
Years 1839-43, John Murray, vol. 1 (reprint by
David & Charles (Holdings) Ltd., Newton
Abbot, Devon, 1969).
SAVOm, D. L., PROSPERO, J. M. & SALTZMAN,E. S.
(1989). Nitrate, non-seasalt sulfate and
methanesulfonate over the Pacific Ocean. In
Chemical Oceanography, vol. 10 (Riley, J. P.,
Chester, R. & Duce, R. A., editors), 219-250,
Academic Press, London.
SCHLEE, S. (1973). A History of Oceanography. Robert
Hale & Co., London.
115
SCORKSSY,W. (1820). An Account of the Arctic Regions,
vol. I, Archibald Constable, Edinburgh (reprint
by David & Charles (Holdings) Ltd., Newton
Abbot, Devon, 1969).
SIEBURTH, J. McN. (1984). Protozoan bacterivory in
pelagic marine waters. In Heterotrophic Activity
in the Sea (Hobble, J. E. & Williams, P. J. leB,
editors), 405 444, Plenum Press, New York.
STAMP, T. & STAMP, S. (1975). William Scoresby: Arctic
Scientist, Caedmon of Whitby Press.
STEEMANNNmLSON, E. (1952). The use of radioactive
carbon (C-14) for measuring organic production
in the sea. J. Cons. Perm. Int. Explor. Mer., 18:
117-140.
STRICKLAND,J. D. H. (1972). Research on the marine
planktonic food web at the Institute of Marine
Resources: a review of the past seven years of
work. Oceanogr. Mar. Biol. Ann. Rev., 10:
349-414.
TAYLOR, F. J. R. (1980). Phytoplankton ecology before
1900: Supplementary notes to the "Depths of the
Ocean". In Oceanography." the Past (Sears, M. &
Merriman, D., editors), 509-521, Springer-
Verlag, New York.
TURNER, S. M., MALIN, G., LISS, P. S., HARBOUR,D. S.
& HOLLIGAN, P. M. (1988). The seasonal
variation of dimethyl sulfide and
dimethylsulfoniopropionate concentrations in
nearshore waters. Limnol. Oceanogr., 33:
364-375.
WATERBURY,J. B., WATSON,S. W., GUILLARD,R. R. L.
& BRAND, L. E. (1979). Widespread occurrence
of a unicellular, marine, planktonic,
cyanobacterium. Nature, Lond., 277: 293-294.
WHEELER, P. A., KIRCHMAN,D. L., LANORY, M. R. &
HARRISON, P. J. (1989). Diel periodicity in
ammonium uptake and regeneration in the
oceanic subarctic Pacific: Implications for
interactions in microbial food webs. Limnol.
Oceanogr., 34: 1025-1033.
WIGGINS, S. (1988). Fluid dynamics: Stirred but not
mixed. Nature, Lond., 333: 395-396.
WRIGLEY, R. C. & HORNE, A. J. (1974). Remote sensing
and lake eutrophication. Nature, Land., 250:
213-214.