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Filter-feeding in the polychaete Nereis diversicolor: A review

Article  in  Aquatic Ecology · September 1994

DOI: 10.1007/BF02334216

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NETHERLANDSJOURNALOFAQUATICECOLOGY28(3-4) 453-458 (1994)

FILTER-FEEDING IN THE POLYCHAETENEREISDIVERSICOLOR:

A REVIEW

HANS ULRIK RIISG~,RD

KEYWORDS:filter-feeding; energy cost; growth.

ABSTRACT

An overview of recent findings concerning filter-feeding in Nereis diversicolor is given. It has been
discovered that the facultative filter-feeder N. diversicolor may meet its metabolic requirements on a pure
diet of phytoplankton, just as a typical obligate filter-feeder. Consequently, this worm is likely to be a
hitherto undervalued key organism in the control of phytoplankton production in many shallow brackish
water areas.

INTRODUCTION has been described as a carnivore, a scavenger, a

During the last few years intense studies
have been carried out at the Institute of Biology
at Odense University in an attempt to answer a num-
ber of questions regarding the occasional filter-
feeding behaviour of the common ragworm Nereis
diversicolor (RLtSGARO,1991; BT~SGABOet aL, 1992;
VEDELAND RIISGABO, 1993; VEDELet aL, 1994). Filter-
feeding in N. diversicolor was until recently either
questioned, or regarded as a rather unimportant
peculiarity. To clarify the extent of adaptation of this
worm to filter-feeding and its possible ecological
importance, both physiological studies in the labora-
tory and population grazing assessments in the field
have been undertaken.
FILTER-FEEDINGBEHAVIOUR
The polychaete N. diversicolor is a common
benthic species of shallow areas in north-western
Europe, where it often penetrates far into estuaries
(THEEDE et aL, 1973; WOLFF, 1973; CHAMBERSand
MILNE, 1975). The ragworm is almost entirely
restricted to the littoral zone where it lives in a
U-shaped burrow in the sediment. N. diversicolor
suspension-feeder and a surface-deposit feeder,
feeding partly by ingesting detritus and micro-
phytobenthos around the openings of the burrow
(WELLS and DALES,1951; GOEBKE,1966, 1971; EVANS,
1971; SMITH, 1977; OLAFSSONand PERSSON,1986;
BONNet aL, 1988).
The occurrence of a filter-feeding mechanism
in N. diversicolor was first described by HARLEY
(1950), and later confirmed by GOERKE (1966).
Observations by RIISGARD (1991) of feeding be-
haviour in N. diversicolor were done in glass
tubes immersed in seawater (Fig. 1A-C). Within
5-20 Tin after adding a suspension of algal cells,
the worm moved to one end of the glass tube
where it fixed mucous threads to the glass wall
forming the circular opening of a net bag. The net
was completed as the worm slowly retreated down
the tube moving it's anterior end from side to side
in semi-circles. During construction of the funnel-
shaped net-bag, and for a period (5-15 Tin) after
the bag was completed, the ragworm pumped water
through the net vigorously undulating its body.
Particles suspended in the inhalant water were retai-
ned by the net and after the period of pumping the
worm moved forward to swallow the net bag and its
entrapped food particles.

453
454 HANS ULRIK RilSGARD

THE NEREIS-PUMP:ENERGYCOST
r" . . . . . "I

A In N. diversicolorthe pumping action is a result

Ner eis L.__T--a g l a s s tube
Fig. 1. Nereis diversicolo~ (A) Photograph of filter-feeding worm
lodged in a 12 cm long glass tube. (B) Magnification of anterior end
of same worm shown in (A) with mucous net bag retaining suspen-
ded particles. (C) Photograph taken 3 rain after photograph (A)
while the worm is swallowing the net bag. From: RIISGARD (1991).
of the undulating movements of the body in the
confining tube. Observations indicate that N. diversi-
color has three different phased posteriorly directed
propagating waves, one of which creates an effec-
tive stroke responsible for the pumping action.
During the effective wave the worm's body makes
firm contact with the tube wall on the dorsal and
ventral sides, suggesting good seals. On the lateral
sides, the parapodia make contact to the wall of the
tube, forming less perfect seals that may leak with
increasing backward pressure, resembling a positive
displacement pump. Back-pressure characteristics
were measured in the experimental set-up shown in
Fig. 2. Hence, the Nereis-pump was modelled as a
leaking positive displacement unit (RIISGARD et aL,
1992). The pumping rate was expressed as Q =
QP - QL, where Qp = volume flow of a leak-free
pump and QL = volume flow of leakage. Qp = ApLf,
where Ap, L and f denote piston area, stroke
length and stroke frequency of the pumping action,

FOOD-TRAPPING NET AND RETENTIONEFFICIENCY

cole [--]
- loser
The structure of the food-trapping net of
N. diversicolor was studied by RIISG,~RD et aL _ i
(1992). Electron-micrographs (EM) of the filter- - T
Anet structure showed that the net is composed
of an irregular mesh made up of long, relatively thick
filaments (up to 300 nm) inter-connected with a
variety of shorter and thinner filaments with
diameters ranging from 5 to about 25 nm. The
average mesh size, measured directly on the
EM-pictures, was found to be between 0.5 and
1.0 ~m, but due to shrinkage during preparation
for EM these values represent only approxi
mately 75% of the actual dimension of the intact
net.
RIISG/~RD(1991) measured simultaneously the
clearance of different sized particles and showed
that particles >7.5 ~m were cleared at a rate,
identical to the pumping rate (measured directly),
Le., the particles are retained with 100% efficiency
by the net. Subsequent measurements performed by
RIISG.~RDet aL (1992) showed that even particles
down to 2-3 ~m can be efficiently (near 100%)
cleared from the water. Thus, it may be concluded Fig. 2. (A) Equipment used for direct measurement of pumping rate
that the retention efficiency of N. diversicotor is as in Nereis diversicolor, The water level is monitored with a laser
beam striking a mirror (m) fixed on a tethered floating ping-pong
efficient as that found in a number of obligate sus- ball. Pumping rate of the worm is equal to the volume of water col-
pension feeding bivalves (MOHLENBERG and R,SGARD, lected in the beaker (b) by maintaining the laser deflection point is
1978; B,SGARD, 1988) and ascidians (Jergensen et maintained at a constant position on the scale using pump (p). (B)
aL, 1984). Filter-feeding worm in glass tube. From RIISGARD (1991).
 Filter-feeding in Nereis diversicolor 455

Table 1. Normal operating pressure of pump (~Hop), power pressure could then be estimated as 2~l-lop = AHfo +
output (Pop), total metabolic rate of 'standard' animal (Rtot) AHex = 1.487 + 0.0057 = 1.493 mm H20. Finally, the
and 'pump work' (Pop/Rtot) in different marine filter-feeding power output, Pp, of the pump was calculated as the
macroinvertebrates.From RIISG/~ROand LARSEN(1994).
product of pressure increase, AHop, and the volume
flow rate, Q, being 2.10 pW. Assuming a metabolic
z~Hop Pop Rtot Pop/Rtot rate Rtot = 12.6 pl 02 h-1 (which is equivalent to 70
(mm H20) (p.W) (p.W) (%) p.W), the 'pump work' was found to be Pop/Rtot =
Sponges (2.10/70)100 = 3% of the total metabolic energy
Haliclona urceolus 0.673 0.677 80 0.85 expenditure (BllSGARD et aL, 1992). This value is
almost identical to the 'pump work' in the obligate
Bivalves
Mytilus edulis 1.0 10 900 1.1 filter-feeding polychaete Chaetopterus variopedatus
which has a mucous trapping-net and a muscular
Polychaetes piston pump comparable to that of N. diversicolor
Chaetopterus (RIISGARD, 1989). When comparing the performance
variopedatus 1.43 4.3 107 4.0
Nereis diversicolor 1.49 2,10 70 3.0
of the facultative filter-feeding polychaete, N. diver-
Sabella penicillus 0.0224 0.451 112 0.403 sicolor with that of some obligate filter-feeders
(Table 1) it can be noted that N. diversicolorcan very
Ascidians well compete with other species in terms of the
Styela clava 0.3 2.3 891 0.26
energy cost of filter-feeding.

respectively. The engineering principles of pump FILTRATION RATES

analysis and modelling of N. diversicolor and other
filter-feeding macroinvertebrates have recently been
reviewed by RIISG/~ROand LARSEN(1994). Therefore,
only the energy cost of pumping shall be mentioned
here.
The pump characteristic is the relationship
between the pressure increase delivered by the
pump, ~Hp, and the volume flow rate, Q. This
relationship is not directly accessible for analysis
in filter-feeding animals, but may be approached
indirectly through studies of the relationship
between pressure resistance exerted by the system
(canals, filters etc.), AHsys, and Q. The latter rela-
tionship is called the system characteristic. When
plotted on the same graph, the intersection of the
two types of characteristics defines the operating
point of the pump. Thus, in steady state the pump
pressure equals the system resistance, &Hp =
&Hsys. In filter-feeding N. diversicolor the system
resistance is the sum of total frictional resistance,
AHfo, and loss of kinetic energie loss, 2~Hex,due to
the propulsion of water out of the worm-tube. The
frictional resistance was resolved into several com-
ponents by RIISGABD et aL (1992). These compo-
nents include the pressure drop over the mucous
net, &H n, and the frictional pressure drop due to
flow i) in the part of the tube unoccupied by the
worm, AH r, ii) through the annular space between
worm and tube, •H e, and iii) parallel to the net,
both inside and outside the bag, 2~Ha. The different
cocnponents were calculated producing the total
frictional pressure decrease. The normal operating
The filtration rate of N. diversicolor individuals
was measured directly for the first time by RIISG/~RD
(1991) using the method depicted in Fig. 2, in addi-
tion to indirect measurements using the 'clearance'
and 'suction' methods, where the filtration rate is
measured as volume of water cleared of suspended
particles in unit time. To obtain enough food to meet
the minimal energy requirements the performance
of filter-feeders inhabiting inshore waters must
generally exceed 10 I of water per ml of oxygen
consumed (JORGENSEN, 1975). By relating the pum-
ping rates to respiration RIISG/~RD(1991) found that
N. diversicolor pumps approximately 40 I of water
per ml oxygen consumed. This pumping rate shows
that the ragworm fulfils the conditions for subsistan-
ce exclusively as a suspension feeder. Furthermore,
RIISG,~BD(1991) measured filtration rate as a func-
tion of N. diversicolor dry weight. Using this rela-
tionship and knowing the density and size distribu-
tion at the collecting site in Odense Fjord the popula-
tion pumping rate was estimated to be about 10 m3
d-1, Le. a volume corresponding to 10 times the
whole water column daily (BIISG,~RD, 1991 ).
EFFECTSOF TEMPERATURE
Acute temperature effects on pumping activity
were measured in the laboratory by RIISGARD et
al. (1992) using clearance, direct determination of
pumping rate and stroke frequency, and the infrared
456 HANSULRIKRIISGARD

Table 2. Nereisdiversicolor. Sizedistribution,populationdensity GROWTH

and biomass,and estimatedpopulationpumpingrateof ragworms
at OdenseFjord,Denmark,from Marchto June1992.FromVEDEL Field studies performed by VEDELand RIISG/~RD
et aL (1994).
(1993) in Danish waters (Odense Fjord and Fyns
Hoved) showed that N. diversicolor (kept in U-
Size Individual Density
clearance shaped glass tubes elevated 15 cm above the bot-
at 17"C (ind. m-2) tom) is able to grow on phytoplankton as the sole
wet wt
food source. The growth was expressed as the
(mg) (pls -1) March April May June instantaneous specific growth rate p calculated as
In(Wt/Wo)t-1, where Wt = body weight at time t
<50 7 1713 1771 1748 1706
50-100 17 373 408 448 406 and W o = body weight at time zero. The highest
100-150 37 163 138 224 265 increase in body weight, corresponding to p = 0.039
150-200 57 245 221 238 153 d-1 or 3.9% d-1, was measured in worms from the
200-250 77 93 163 182 125 eutrophic Odense Fjord. When fed in the laboratory
250-300 97 70 128 70 154 on a diet of monocultured suspended algal cells
300-350 117 82 35 70 112 the ragworms (kept in glass tubes) obtained
350-400 137 82 70 42 28
400-450 157 47 58 28 28 growth rates !1 = 0.031 d-1, comparable to those
450-500 177 70 58 28 14 found in the field. Higher specific growth rates have,
500-550 197 12 12 28 however, been obtained in worms offered meat.
550-600 217 35 35 14 Thus, when fed on a diet consisting of abundant
600-650 237 12 12 shrimp-meat the specific growth rate of N. diversi-
650-700 257 23 colorand N. virens (which is apparently not able to
700-750 277 12
filter-feed) was recently found to be 0.051 - 0.059
d-t and 0.047 - 0.052 d-t, respectively (Annemette
Population
density (ind. m-2) 3032 3109 3 1 2 0 2991 M. Nielsen, pers. comm.).
Biomass (gm -2) 343 326 294 268
Filtration at 5.20C 7 . 5 " C 13.2~ 19.2"C FILTER-FEEDING ACTIVITY IN THE FIELD
capacity (m3m-2d-1) 3,6 4.2 5.6 7.0
To investigate to what extent filter feeding of
N. diversicolor in the field varies over the season,
phototransducer technique. A doubling of tem- VEDELetal. (1994) used the infrared phototransducer
perature (from 13"C) led to a doubling of the system to obtain continuous, long-term measure-
stroke frequency and a halving of the net cycle ments of the characteristic undulating body move-
length. At low temperatures a tendency to pause ments of the filter-feeding activity of N. diversicolor
for extended periods between pumping was ob-
served, tn the temperature interval from appro-
ximately 5 to 15"C there was a linear increase in Table 3. Nereis diversicolor. Duration of monitoring with the
clearance, and a doubling of the temperature was phototransducersystem,and filtrationactivityat differenttimesof
year and at different phytoplanktonconcentration(chlorophylla
followed by a doubling in clearance. Direct mea- measured in surface water samples) at two Danish locations,
surements of the pumping rate showed that high OdenseFjordand FynsHove&Datafrom VEDELetaL (1994).
stroke frequency was correlated with high pumping
rate. Localibj& date Observation Chlorophylla Filtrationactivity
Estimates of the N. diversicolor population fil- time(h) (pg I-~) (% of time)
tration capacities in Odense Fjord in different OdenseFjord
months showed that increased pumping activity 1992-April-22 42 2.4 _+ 0.9 5.6
accompanying rising water temperature led to a 1992-May-13 96 2.0 _+ 0.7 12.5
doubling of the population filtration potential from 1992-May-27 72 11.5 +_ 6.4 51.0
1992-July-09 48 15.0 _+ 6.0 54.0
March to June (Table 2). In May the population
filtration rate was potentially 5.6 m3 m-2 d-t, re- FynsHoved
presenting a volume 11-56 times greater than the 1992-June-15 118 1.9 _+ 0.9 52.5
overlying water column at the sampling locality in 1991-August-19 32 2.7 _+ 0.8 100.0
1991-September-01 72 1.8 + 1.2 18.0
Odense Fjord where the water depth was about 1991-September-12 45 1.8 _+ 0.5 46.7
50 cm at high tide and 10 cm at low tide.
 Filter-feeding in Nereis diversicolor 457

A f
fL co o, li

/m
transducer

sediment surface filter-net

DI133

B glass tube C m
Fig. 3. Phototransducer system for monitoring filter-feeding activity of Nereis diversicolor in field studies. (A) Platform with computer and
phototransducer system. (B) Glass tube holding a worm. (C) The phototransducer system consists of an infra-red (IR) light-emitting diode
and a phototransistor detector. The phototransistor detects variations in reflected I R light intensity, which is a function of the undulating body
activity of the filter-feeding worm. The reflected IR light generates a light-dependent current which is amplified and filtered prior to input to
a portable personal computer. (D) Real-time signals from the phototransducers are displayed on the computer screen in oscilloscope-like
windows; upper (UT) and lower (LT) threshold levels are indicated. (E) Undulatory strokes per minute are presented in histogram windows,
All histogram data are stored on disc. From VEDEL et aL (1994).

in glass tubes immersed in the natural sediment
(Fig. 3). This study was done in two areas (Odense
Fjord and Pughavn at Fyns Hoved, Northern Fyn,
Denmark). The phototransducer system consisted
of an infra-red light-emitting diode and a phototran-
sister detector. The phototransistor detected varia-
tions in reflected infra-red light intensity caused by
the undulating body activity of the filter-feeding
worm.
VEDEL et al. (1994) found that filter-feeding
was 'triggered' by the presence of phytoplankton
in the water, and that IV. diversicolor was filter-
feeding 50 to 100% of the time during the productive
May-August period (Table 3). In early spring and
autumn filter-feeding occurred for approximately 5
to 20% of the total time. The potential grazing
impact was assumed to be restricted by a thin
layer of phytoplankton drained water overlying the
sediment, especially on days when wind-induced
mixing of the water column was low. No clear corre-
lation between filtration activity and chlorophyll a
(unfortunately only measured in surface water
 458 HANS ULRIK RIISGARD

samples) can be seen in Table 3. This phenomenon
awaits an explanation. Preliminary results of on-
going studies showed that the algal concentration in
near-surface water samples may be several times
higher than in water samples collected at 0.5 m
water depth just above a sediment with a dense pop-
ulation of N. diversicolor. This result may indicate
that N. diversicolor effectively clears bottom-near
water layers of phytoplankton, and that effective
vertical mixing may be extremely important for the
realization of the great potential of N, diversicolorin
controlling phytoplankton production. In conclusion,
it is very likely that this w o r m is a hitherto under-
valued key organism in the control of phytoplankton
production in many shallow brackish water areas.
ACKNOWLEDGEMENTS
Thanks are due to Drs. Anne Katrine Lundebye,
Gary Banta and the a n o n y m o u s referees for im-
provements in the style of the manuscript,

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Addressofthe author:

Institute of Biology, OdenseUniversity, Campusvej55, DK-5230 Odense M, Denmark.

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