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Marine Biology 42, 69-84 (1977) MARINE BIOLOGY �9 by Springer-Verlag 1977

Grazing by Adult Estuarine Calanoid Copepods of the Chesapeake Bay

S. Richman, D.R. Heinle and R. Huff

Department of Biology, Lawrence University; Appleton, Wisconsin, USA and Chesapeake Biological Laboratory, University of Maryland; Solomons, Maryland, USA

Abstract

Grazing by adult female Eurytemora affinis, Acartia tonsa and A. clausi on natural distributions of particles from the Chesapeake Bay has been investigated. During the course of a year's sampling, a wide variety of particle size-biomass distributions were observed as seasonal shifts in detritus, and over 150 algal species occurred. These distributions were grouped into 5 basic types in the analyses of feeding. All three species demonstrated similar capabilities for feeding over a broad range of particle size with selection (higher filtering rates) on larger particles and on biomass peaks. Feeding on multiple-peak distributions resulted in strong selection or "tracking" of each biomass peak with reduced filtering rates between peaks. Evi- dence is presented which suggests that the copepods first feed on large particles and then successively switch to biomass peaks of the smaller size categories. Com- parisons of the feeding behavior of Eurytemora affinis and the Acartia species showing that the Acartia species have greater capabilities for taking large particles may be associated with modifications of their mouth parts for raptorial feeding. The results suggest considerable flexibility in copepod feeding behavior which cannot be explained solely by the mechanism of a fixed sieve.

I ntroduction

Ever since the work of Parsons et al.

(1967) and Parsons and Le Brasseur (1970) when zooplankton were fed on continuous- size spectra of natural food particles, there has been considerable interest in the feeding responses of calanoid copepods under natural conditions. How do zooplankton deal with heterogeneous spectra of particles which are continu- ously changing? In order to elucidate the major processes affecting the abundance and distribution of the predominant herbivore species, detailed studies of their feeding patterns on seasonal naturally occurring particle distributions are necessary. Yet, even though there is much current interest in the feeding be-

food, compared to smaller cells (Mullin, 1963; Richman and Rogers, 1969; Paffen- h~fer, 1971; Frost, 1972). Wilson (1973) reported that Acartia tonsa fed most in- tensively on the size class of plastic beads just larger than the most abundant size category. While the experimental versatility is greatly enhanced in such simple systems, and much valuable work has been done, there is clearly a need for experiments employing more natural conditions.

In Poulet's studies (1973, 1974) it was observed that Pseudocalanus minutus shifted its grazing pressure from one size range to another depending on where the particle peak concentrations occurred. Filtering rates and thus elec-

havior and selective feeding capabilities tivity indices were higher on those of calanoid copepods, few studies of this type have been undertaken.

With the exception of Poulet 1973, 1974 (see also Poulet and Chanut, 1975), most studies have utilized laboratory cultures of both copepods and algae, and in some cases plastic beads. Several investigators have reported higher filtering rates when larger cells are the

particles included in the concentration peaks. Poulet referred to this type of grazing as "opportunistic feeding behavior", when particles are taken out of proportion to their numbers and thus filtering rates are disproportionately higher in some size categories in the food abundance distribution. In our studies we consider this behavior as

70 s. Richman et al. : Grazing by Adult Estuarine Calanoid Copepods

selective feeding behavior which may per bottle on a plankton wheel rotating maximize energy input per unit of energy at 2 rpm in the dark. At the conclusion expenditure and, at the same time, help of an experiment, the particle distribu- to maintain the diversity of the phyto- tion from both bottles was determined plankton species distribution by grazing with a Particle Data, Inc. automated the dominant species of the particle con- counting system consisting of the parti- centration peaks (Porter, 1973; Poulet, 1973; Wilson, 1973; Berman and Richman, 1974; Lehman, 1976; Nival and Nival, 1976).

While several investigators have evidence of selective feeding, the mechanism of such behavior is not understood. More work needs to be done on mouthpart morphology as in the study by Friedman and Strickler (1975) and its relation to particle retention (Nival and Nival, 1976) as well as experiments with mani- pulated size-frequency distributions before we will understand the role of ac- tive or passive feeding (Boyd, 1976) in the feeding mechanics of calanoid copepods.

In this study, we used freshly cap- tured copepods and natural particle distributions to investigate the grazing of adults and young stages of Eurytemora af-

finis, Acartia tonsa and A. clausi from the middle Chesapeake Bay. This paper deals with the adults, while the grazing experiments with juvenile stages are re-

cle counter with a 120 ~m aperture tube and a 128 channel analyzer interfaced with a PDP8 computer and TTY teletype. This system provided speed and high res- olution with the simultaneous measurement of 110 to 128 size categories between 3 and 37 ~m. This range was ex- panded to 60 ~m when larger particles were present by taking a second sample at a different setting and blending the distribution, providing a usable range of approximately 3 to 40 ~un of spherical equivalent diameter. Triplicate analyses were made with each bottle. These data were subsequently analyzed with a UNIVAC 1108 computer, programmed to calculate the averages of replicated distributions, to convert mean counts per ml in each of the size categories to total volume of particles per ml of water in each size category, and to calculate the filtering rate as in Gauld (1951)

in C i -In E i F = v,

t where c i = concentration of i size category in control bottle, E i = concentra-

ported elsewhere (Allan et al.,in press), tion of i size category ~n experimental

Materials and Methods

Copepods were collected by No. 10 or 20 net tow, and water containing the natural particle distribution was obtained at the same time by pumping at the desired depth on the morning before an experiment at the mouth of the Patuxent River off Drum Point, in Chesapeake Bay, USA. The adults of the desired species and sex were sorted live under a dis- secting microscope, washed in 0.45 ~m

bottle, t = time in hours, v = number of ml/animal in the experimental bottle, and F = filtering rate in ml of water cleared of food per animal per hour. Ingestion rate was calculated as total volume in- gested per copepod per hour for each size category which is equal to the product of filtering rate and mean food concentration of the control and experimental bottles for each particle size. Plotting routines were also programmed to plot each parameter as a function of spherical equivalent diameter. The statistical significance of mean differences between

filtered bay water and placed in a beaker control and experimental distributions with approximately 400 ml of bay water for each size category was determined by with its assemblage of natural particles, means of the t test. The analysis of The water was then split into two 180 ml square bottles, pouring gradually into the two bottles so that all of the copepods ended up in one bottle with the other serving as the "control" bottle. With careful mixing and pouring, both bottles contained the same distribution. When experimental and control particle distributions were compared immediately after filling the two bottles, no differences were observed.

Grazing experiments were conducted in the dark at 50 or iO~ during winter and spring and at 20 ~ or 25~ during summer and early fall. Feeding experiments were run for 6 to 24 h using 5 to 25 copepods

feeding behavior is based on differences significant to at least the 0.05 level of probability.

Results

Feeding experiments were performed on adult females of the species Eurytemora

affinis, Acartia tonsa and A. clausi. The in situ particle distributions used in the experiments are those that occurred from November, 1974 through October, 1975 at Drum Point at the mouth of the Patuxent in Chesapeake Bay, and include distributions from surface, mid and bottom water.

S. Richman et al. : Grazing by Adult Estuarine Calanoid Copepods 71

In all cases there was an inverse relationship between number of particles per ml and particle size between 3 and 40 ~m, with the largest numbers consistently occurring in the smallest size categories. However, when total concentration is computed by the product of number per ml x particle volume, a wide variety of size-distributions were observed. These could, however, by ignoring minor variations, be grouped into 5 basic types (Fig. I). Type I, a gradually increasing volume of particles with increasing mean spherical diameter, was rarely observed. Type 2, with a distinct volume peak smaller than 10 ~m mean spherical diameter, was common, as was Type 3, a single peak of material larger than 10 ~m. Type 4 had two peaks with most of the particle volume in the smaller sized peak, while Type 5 had two peaks with most of the particle volume in the larger sized peak. Type 4 sometimes had nearly as much particle volume in the larger peak as in the smaller, and sometimes had third and fourth peaks of larger particles.

Microscopic examination of the weekly samples revealed 151 species, the major groups being diatoms (50%), dinoflagel- lates (I 9%), chlorophytes (11%) , chryso- phytes (7%), and cryptophytes (5%). The species Skeletonema costatum and Prorocen- trum minimum were major constituents of the larger size peaks (16 to 22 ~m) and Thallasiosira nana, Colycomonas ovalis, Ochro-

monas nannos, Amphidinium sp., and Chroomonas

diplococca of the smaller size categories (5 to 12 ~m). In addition, dead organic particulates were a major constituent of all the samples, often comprising 80% or more of the total particulates. The total concentration did not vary greatly with time of year, but its composition varied considerably. Detailed microscopic analyses of the particulates will be reported elsewhere (Van Valkenburg et al., 1977).

Modes of Selection

In Fig. 2, the particle distributions are given on the bottom graphs, with the closed circles representing the control

i | lo m/'- A

/ \ I/ '-"<"

Fig. i. Generalized representation of 5 types of naturally occurring particle distributions in mid-Chesapeake Bay water. Size (x axis) is from 2.0 to 30.0 ~m in spherical equivalent diameter of particle volume. Y axis is biomass. The graphs represent approximately 130 size categories. (i) Biomass progressively increasing with increasing particle size. (2) Biomass peak below IO um in particle size. (3) Biomass peak above iO um in particle size. (4) Double-peak

bottle and the open circles the distribu- distribution with peak of greater biomass below tion after feeding. The middle graphs i0 urn; biomass of secondary peak above iO um in show the filtering rate copepod-1 h-1 diameter can vary considerably. (5) Double-peak over the size range studied. This value distribution with peak of greater biomass above is equivalent to total volume of particu- I0 um in diameter lates consumed copepod-1 h-1 per unit of food available, and will be constant if feeding is non-selective or equally efficient over the range of particles available, and will increase or decrease with greater or lesser feeding efficiency

Fig. 2. Individual feeding experiments with Eurytemora affinis

(i - 6), Acartia tonsa

(7 - 9) and A. clausi

(iO - 12)

showing vari-

ations in observed feeding pattexns with different types of naturally occurring particle distributions in mid-Chesapeake Bay water.

Bottom panels: particle size-biomass distributions in controls

(filled circles)

and after feeding

(open circles) on Chesapeake Bay

water; particle size is given in spherical equivalent diameter of particle volume. Middle panels:

filtering rates as a function of

particle size calculated from differences in control

(filled circles)

and experimental

(open circles) particle size-biomass distri-

butions in bottom panels. Top panels: ingestion rates as a function of particle size

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78 S. Richman etal. : Grazing by Adult Estuarine Calanoid Copepods

1.35

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ACARTIA _'rON SA 2

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661 111~ ~612 PARTICLE DIAMETER (tim)

Fig. 3. Acartia tonsa. Particle size-biomass distributions in controls (filled circles) and after feeding (open circles) on Chesapeake Bay water with increasing numbers of copepods. Particle size is given in spherical equivalent diameter of particle volume (see text for explanation of designated

numbers i - 5)

or selectivity. The top graphs show the ingestion rate copepod-1 h-1 relative to particle size. The filtering rate curves show the major modes of selection observed during the study.

Eurytemora affinis. Individual results of some of the 21 experiments are pre-

sented in Figs. 2: i-6; 5 and 6 to show feeding on the various size-distribution types (Fig. 1). In all cases particle selection is clearly in evidence. In Fig. 2: i, 2 and 3, selection for the biomass peak and for larger particles beyond the peak is demonstrated with Type I and Type 2 distributions. While there is some indication that selection is greater

S. Richman et al. : Grazing by Adult Estuarine Calanoid Copepods 7g

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- - 6/01 11~29 30.12 - PARTICLE DIAMETER (urn)

Fig. 4. Acartia tonsa. Filtering rates as a function of particle size with increasing numbers of copepods calculated from differences in control and experimental particle size-biomass distributions shown in Fig. 3 (see text for explanation of designated numbers i - 5)

for the biomass peaks (Fig. 2: 2), these results generally support the viewpoints of Frost (1972), Boyd (1976), Lam and Frost (1976) and Nival and Nival (1976) that selection is the result of a leaky filter which is more efficient in col- lecting larger particles �9

The data in Fig. 2: 4, 5, 6 display multiple-peak distributions as of Types

4 and 5 (Fig. I). The mode of selection in these cases was for both or several peaks, with reduced or negative filtering rates between peaks. Selection for large particles is in evidence as well, although there is considerable scatter in this region due to the small number of large particles. Decreased filtering rates on intermediate-sized par-


1.60 f EURYTEMORA AFFINIS 5 adult 9

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I I 4.77 11.99

PARTICLE DIAMETER (um) 23.92

Fig. 5. Eurytemora affinis. Particle size-biomass distributions in controls (filled circles) and after feeding (open circles) on Chesapeake Bay water with increasing numbers of copepods. Particle size is given in spherical equivalent diameter of particle volume

ticles would not be predicted if the si show a definite preference for large copepods filter larger particles more particles and feed on them at a maximum efficiently than smaller ones. Thus, rate even when they occur at concentra- these results cannot be explained with a tions lower than smaller sizes, as is leaky sieve type of mechanism as proposed shown with the Type 2 distribution (Fig. by Boyd (1976). 2: 7, io, 11) and the Type 3 distribution

(Fig. 2: 8). Furthermore, when the particle distribution is skewed to the

Acartia spp. Results of some of the 36 large particle region (Figs. 2: 8, 9, 12; experiments with A. tonsa and 24 experi- and 3), preference for large size is ments with A. clausi selected to show further emphasized by the virtual ab- feeding on four of the distribution types sence of feeding on the smaller particle are presented in Figs. 2: 7-12; 3 and 4. Like Eurytemora affinis, the two Acartia species were capable of feeding over the entire size range. The filtering rates not only increased at or near the concentration peaks as compared to smaller size categories, but also maximum filtering rates consistently occurred at the large end of the size spectrum (>20 ~m). While there is evidence of tracking modal particle concentrations (Figs. 2: 9, 12;

sizes. Further evidence for behavioral se-

lection is shown by pairs of individual experiments run simultaneously, using different numbers of Acartia tonsa grazing for 7 to 8 h on a particle spectrum with a major biomass peak at 10 ~un and several peaks containing less biomass of larger particles (Fig. 3). Filtering rates (Fig. 4) were much higher in the bottle containing 5 adult A. tonsa, some-

3 and 4, both A. tonsa and A. clau- thing we commonly observed in these ex-

S. Rich/nan et al. : Grazing by Adult Estuarine Calanoid Copepods 81

1.50

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0.30

E U R Y T E M O R A AFF!NIS . . . . . "" "

5 a d u l t ? -" . .

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15 adult

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� 9 1 4 9 1 7 6 1 4 9 1 4 9 1 4 9 1 4 9 1 4 9 1 4 9 1 4 9 1 4 9 1 4 9 1 4 9

% + - - ++ + � 9 1 4 9 1 4 9 1 4 9 1 4 9 1 7 6 1 4 9 1 4 9 1 4 9 1 4 9 I I . ,

20 adult

0

�9 " �9149149149149149149149149 �9149 �9149 �9149 " ~ �9 �9149149 ,.

, �9149149149149149149149149149149149149149149 �9 ~ ~ �9

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4.77 11.?'9 23.92 PARTICLE DIAMETER (u.m)

Fig. 6. Eurytemora affinis. Filtering rates as a function of particle size with increasing numbers of copepods calculated from differences in control and experimental particle size-biomass distributions shown in Fig. 5

periments, and filtering rates more the copepods feed on the particle distr,- variable over the particle size range�9 but,on more and more to the small end of In that experiment, there were 4 distinct the size spectrum as increased feeding peaks in filtering rate (Nos. 2-5 in the pressure occurs with the addition of top panel of Fig. 4), and some feeding on particles smaller than 6 ~m. With increasing numbers of adult A. tonsa, feeding on particles smaller than about 8 ~un increased�9 The position of the 5 peaks in the filtering rate curves are

greater numbers of copepods (Fig. 3). These observations are supported further by noting that the largest filtering rates occurred on the largest particles when fewest animals were present and that filtering rates shifted to the left

shown on the particle distributions (Fig. (to smaller sizes) with increasing 3). Note that Filtering Peaks 2, 3, 4, feeding pressure�9 and sometimes 5 coincide with biomass peaks in the general particle distributions, and that Filtering Peak I is well to the left of the major biomass peak at 10 Lum. These experiments suggest that Ao tonsa can selectively feed on particles within a complex distribution, starting with the large-size categories and gradually switching to biomass peaks in smaller size categories and finally to general feeding as the original distributions are modified�9 It is clear that

Figs. 5 and 6 show the results of similar experiments with Eurytemora affinis

and indicate the same type of progres- sion from high selection for large particles to more general feeding on smaller sizes as the particle distribution is modified. As with Acartia tonsa, selection for large particles occurs first, then the copepod switches to the biomass peaks of smaller size categories as the original distributions are modified with increased feeding pressure�9

82 S. Richman et al. : Grazing by Adult Estuarine Calanoid Copepods

Discussion

There have been a number of hypotheses in the literature concerning the mechanism of feeding by calanoid copepods. Presently, filter-feeding models have been proposed by Boyd (1976), Lam and Frost (1976), Lehman (1976), and Nival and Nival (1976), which suggest that copepods are indiscriminate filterers with filter structures that have a variable retention efficiency for different particle sizes and with larger particles more efficiently retained than smaller ones. While there have been a number of investigations of feeding in the laboratory on algal or plastic bead combina-

The "tracking" response was particularly evident in the case of Eurytemora affinis, both in copepodids (Allan et al., in press) and adults. It is most appar- ent in the feeding experiments with multiple-peak distributions (Figs 2: 4, 5, 6; 5 and 6). Selection for several peaks with reduced or negative filtering rates between peaks argues for considerable flexibility in the copepod's behavior.

Experiments with Acartia adults (either A. tonsa or A. clausi) and experiments reported elsewhere with copepodid stages (Allan et al., in press) lead to similar conclusions for these species. Selection for large particles, however, shows up

tions in which larger particles are pre- to a greater extent than does feeding on ferred (Mullin, 1963; Richman and Rogers, biomass peaks although both modes of i969; Paffenh~fer, 1971; Frost, 1972; selection were observed. Large-particle Wilson, 1973), there have been few selection is particularly evident with studies with natural particle distribu- our Type 2 distribution where the bio- tions. In such studies, higher filtra- mass peak is in the small size range tion rates were at or near the biomass (>10 v/n, Fig. 2: 7, 1o, 11), while the peak as well as on larger particles tracking of biomass peaks is displayed (Parsons et al., 1967, 1969; Poulet, 1973, in the case of Type 3 distributions 1974). (biomass peaks >10 Lun, Fig. 2: 8, 12) and

In this study and in experiments with juvenile stages reported elsewhere (Allan et al., in press), we define selective feeding operationally from the filtering rate versus particle biomass curve. Non- selective feeding would be shown by a filtering rate curve which is constant over the size range which can be utilized. Selective feeding, on the other hand, would be shown by a filtering rate curve which is higher in some size categories compared to others. Poulet's (1974) use of the term "opportunistic"

with the multiple-peak distributions (Figs. 2: 9; 3 and 4). These results are consistent with Poulet's (1974) observations with Pseudocalanus minutus of a combination of feeding on biomass peaks and also larger particles.

Selection for the large-sized particles as well as biomass peaks should result in high ingestion rates at the concentration peak size and beyond, espe- cially with the Type 2 distribution (Fig. I). This result was more significant with the Acartia species in contrast to

is consistent with our use of "selective". Eurytemora affinis. The ingestion rates of However, Poulet's (1974) use of the term "unselective" to mean rigid feeding in one size range only does not correspond to our usage.

In this study, a total of 81 experiments have been conducted with adults of Eurytemora affinis, Acartia tonsa, and A. clausi that yielded results which could be interpreted with confidence. There is no doubt that selection for large particles is important. This may occur by means of a variably efficient fixed sieve (Boyd, 1976), by raptorial feeding (Conover, 1956, 1960, 1966; Richman and Rogers, 1969) or by a combination of mechanisms. It is also clear that particles in concentration peaks are grazed more heavily than other portions of the size spectrum. This result is not ex-

E. affinis feeding on the Type 2 distribution (Fig. 2: 2, 3, 4) drop sharply beyond the biomass peak, whereas with A. tonsa (Fig. 2: 7) and A. clausi (Fig. 2: I0, 11), ingestion rates beyond the biomass peaks are approximately half as large as the maximum rates.

Earlier microscopic observations of the mouth parts and feeding behavior of Acartia tonsa show that this species is an omnivore which can eat either plant or animal food efficiently. Conover (1956, 1960) has observed this species grasping Artemia sp. nauplii and single cells of Thallassiosira decipiens of 70 to 85 ~/n diameter. Anraku and Omori (1963), Gauld (1966), and Parsons and Takahashi (1973) all point out differences in the mouth parts of Acartia species compared

plained solely by the mechanics of a to more typical herbivorous filter- fixed sieve (Boyd, 1976) nor by the model feeders, in having a reduced maxilliped proposed by Lehman (1976) where maximum and using their second maxillae as a selection is for particles slightly "scoop" to filter small particles and larger than those most numerous in the grasp larger ones. This type of behavior mixture, may explain the ability of both A. tonsa

S. Richman et al. : Grazing by Adult Estuarine Calanoid Copepods 83

and A. clausi to preferentially consume large particles even when they are less abundant numerically and in terms of total concentration. Eurytemora affinis, on the other hand, appears to be more typical, having a larger maxilliped and not using the second maxillae in a scoop- like arrangement.

Although more work needs to be done on the kinetics of the process, the feeding response of adult copepods on a variety of estuarine particle distributions appears to take the form of a gradation of grazing pressures, starting with larger particles and switching to biomass peaks. The results suggest considerable flexibility in copepod feeding behavior which cannot be explained solely by the mechanism of a fixed sieve. Such behavior could account for the seasonal predominance of microalgae which has been described in the Chesapeake Bay

(McCarthy et al., 1974; Van Valkenburg and Flemer, 1974)

Acknowledgements. We are grateful to Dr. R. Ulanowicz, Mr. J. Leo and Mr. C. Langdon for their help in the development of computer pro- gramming for this study. Thanks are also due to the C.B.L. personnel at Solomons for the hospi- tality extended to the senior author while he was on a sabbatical leave. This investigation was supported by ERDA Contract No. AT-(401-I)- 4848 and by a Lawrence University Sabbatical.

Literature Cited

Allan, J.D., S. Richman, D.R. Heinle and R. Huff: Grazing in juvenile stages of some estuarine calanoid copepods. Mar. Biol. (In press)

Anraku, M. and M. Omori: Preliminary survey of the relationship between the feeding habit and the structure of the mouth-parts of marine copepods. Limnol. Oceanogr. 8, 116-126 (1963)

Berman, M. and S. Richman: The feeding behavior of Daphnia pulex from Lake Winnebago, Wiscon- sin. Limnol. Oceanogr. 19, 105-109 (1974)

Boyd, C.M.: Selection of particle sizes by filter-feeding copepods: a plea for reason. Limnol. Oceanogr. 21, 175-179 (1976)

Conover, R.J.: Oceanography of Long Island Sound, 1952-54. VI. Biology of Acartia clausi and A. tonsa. Bull. Bingham oceanogr. Coll. 15, 156- 233 (1956)

- The feeding behavior and respiration of some marine planktonic Crustacea. Biol. Bull. mar. biol. Lab., Woods Hole 119, 399-415 (1960)

- Feeding on large particles by Calanus hyper-

poda: Crustacea). Proc. natn. Acad. Sci. U.S.A. 72, 4185-4188 (1975)

Frost, B.W.: Effects of size and concentration of food particles on the feeding behavior of the marine planktonic copepod Calanus pacifi- cus. Limnol. Oceanogr. 17, 805-815 (1972)

Gauld, D.T.: The grazing rate of planktonic copepods. J. mar. biol. Ass. U.K. 29, 695- 706 (1951)

- The swimming and feeding of planktonic copepods. In: Some contemporary studies in marine science, pp 313-334. Ed. by H. Barnes. Lon- don: Allen & Unwin 1966

Lam, R.K. and B.W. Frost: Model of copepod filtering response to changes in size and concentration of food. Limnol. Oceanogr. 21, 490-500 (1976)

Leb/nan, J.T.: The filter-feeder as an optimal forager, and the predicted shapes of feeding curves. Limnol. Oceanogr. 21, 501-516 (1976)

McCarthy, J.J., W.Rowland Taylor and M.E. Loftus: Significance of nanoplankton in the Chesa- peake Bay Estuary and problems associated with the measurement of nanoplankton productivity. Mar. Biol. 24, 7-16 (1974)

Mullin, M.M.: Some factors affecting the feeding of marine copepods of the genus Calanus. Limnol. Oceanogr. 8, 239-250 (1963)

Nival, P. and S. Nival: Particle retention ef- ficiences of an herbivorous copepod, Acartia clausi (adult and copepodite stages): effects on grazing. Limnol. Oceanogr. 21, 24-38 (1976)

Paffenh6fer, G.A.: Grazing and ingestion rates of nauplii, copepodids, and adults of the marine planktonic copepod Calanus helgolandicus. Mar. Biol. 11, 286-298 (1971)

Parsons, T.R. and R.J. LeBrasseur: The avail- ability of food to different trophic levels in the marine food chain. In: Marine food chains, pp 325-343. Ed. by J.H. Steele. Berkeley and Los Angeles: University of Cali- fornia Press 1970

-- and J.D. Fulton: Some observations on the dependence of zooplankton grazing on the

cell size and concentration of phytoplankton blooms. J. oceanogr. Soc. Japan 23, 10-17 (1967)

- - - and O.D. Kennedy: Production studies in the Strait of Georgia. II. J. exp. mar. Biol. Ecol. 3, 39-50 (1969)

- and M. Takahashi: Environmental control of phytoplankton cell size. Limnol. Oceanogr. 18, 511-515 (1973)

Porter, K.G.: Selective grazing and differential digestion of algae by zooplankton. Nature, Lond. 244, 179-180 (1973)

Poulet, S.A.: Grazing of Pseudocalanus minutus on naturally occurring particulate matter. Limnol. Oeeanogr. 18, 564-573 (1973)

boreus (Kr~yer) . In: Some contemporary studies - Seasonal grazing of Pseudocalanus minutus on in marine science, pp 187-194. Ed. by H. particles. Mar. Biol. 25, 109-123 (1974) Barnes. London: Allen & Unwin Ltd. 1966 - and J.P. Chanut: Nonselective feeding of

Friedman, M.M. and J.R. Strickler: Chemorecep- Pseudocalanus minutus. J. Fish. Res. Bd Can. tots and feeding in calanoid copepods (Arthro- 32, 706-713 (1975)


Richman, S. and H.N. Rogers: The feeding of Ca- lanus helgolandicus on synchronously growing populations of the marine diatom Ditylum brightwelli. Limnol. Oceanogr. 14, 701-709 (1969)

Van Valkenburg, S.D. and D.A. Flemer: The distribution and productivity of nannoplankton in a temperate estuarine area. Estuar. cstl mar. Sci. 2, 311-322 (1974)

-, J.K. Jones and D.R. Heinle: A comparison by size class and volume of detritus versus phy-

toplankton in Chesapeake Bay. Estuar. cstl mar. Sci. (In press). (1977)

Wilson, D.S.: Food selection among copepods. Ecology 54, 909-914 (1973)

Professor Sumner Richman Department of Biology Lawrence University Appleton, Wisconsin 54911 USA

Date of final manuscript acceptance: February 18, 1977. Communicated by M.R. Tripp, Newark

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