Predatory feeding behavior of a marine copepod, Luhidocera trispinosd

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1 Limnol. Oceanogr., 23(6), 1978, , by the American Society of Limnology and Oceanography, Inc. Predatory feeding behavior of a marine copepod, Luhidocera trispinosd M. R. Landry2 Institute of Marine Rcsourccs, University of California, San Diego, La Jolla Abstract The behavior of Labidocera feeding on early devclopmcntal stages of five common species of planktonic calanoid copepods was investigated to determine its species-specific impact on a mixed copepod community. Feeding rates on individual prey were not affected by prey density or the availability of alternate prey; threshold feeding behavior was not observed. Capture rates of naupliar prey of all species increase as a function of their size even though larger nauplii appear better able to avoid capture. In general, the ability of Labidocera to capture individuals of a prey species decreases abruptly after the prey develop to the copcpodid stages. As a consequence of the limited susceptibility of copepodid stages to capture by Labidocera and higher feeding rates on larger nauplii, the predatory impact of Lnbidocera is greatest on the largest of the prey species. Recent studies in freshwater ecosystems have suggested that size-selective feeding by invertebrate predators may play a significant role in structuring communities of zooplankton (Dodson 1974; Kerfoot 1975; Zaret 1975; Stenson 1976). Invertebrate predators are generally limited by the maximum size of prey they can successfully capture or handle and therefore exert a selective impact on smaller or more easily manipulated prey with larger prey enjoying a refuge in size (Anderson 1970; Brand1 and Fernando 1974,197!3a,b; Kerfoot 1977). The impact of these predators on the size composition of zooplankton is opposite to the impact of visually feeding vertebrate predators which typically select for the larger or more conspicuous prey (HrbGck et al. 1961; Brooks and Dodson 1965; Brooks 1968; Zaret and Kerfoot 1975). Thus, different size structures of zooplanktonic communities are to be expected depending on whether vertebrate or invertebrate predators dominate in a given system. The widely observed phenomenon that large zooplankters dominate freshwater systems with invertebrate predators and without fish while small zooplankters Research supported by National Science Foundation grant OCE Present address: Department of Oceanography WB-10, University of Washington, Scattlc dominate systems with fish supports the distinction which has been made between the effects of these two types of predators. Because of its intuitive appeal the concept that zooplanktonic community structure vari es according to the balance of vertebrate and invertebrate predators has been adopted into theoretical, multispeties models of marine ecosystems (Steele and Frost 1977). The advantage of formulating invertebrate predation as a selective pressure against smaller zooplankters is that it stabilizes the simulated coexistence of large and small copepods by counteracting factors which select against the larger species, e.g. the competitive superiority of smaller species (Frost 1974) and size-selective predation by fish. However, it has yet to be demonstrated from laboratory or field studies in the marine environment that invertebrate predators exert a consistent selective pressure against small species, as they appear to do in freshwater systems. The few population studies of marine copepods indicate that mortality rates are very high during the naupliar stages (Heinle 1966; Parsons et al. 1969). Mullin and Brooks (1970) have estimated mortality rates of 1848% * d-l for the nauplii of Calanus off La Jolla, California; in comparison, mortality during the early copepodid stages was essentially zero

2 1104 Landry while adult mortality ranged as high as 11%. d-l. If we assume that the smaller developmental stages of a copepod are more likely to be consumed by small invertebrate predators than by fish, then the numerical impact of invertebrate predators on populations of marine copepods seems significant. There is some justification, therefore, in speculating that consistent differences in the feeding rates of invertebrate predators on prey species of different sizes could have important consequences on the composition of planktonic marine communities. Lahidocera trispinosa is a common copepod in the nearshore (within 3-6 km) plankton off southern California. Although early stages are almost entirely herbivorous-feeding on monads, dinoflagellates, and ciliates-later copepodids and adults arc predators (Barnett 1974). I here describe the feeding behavior of Lnbidocera on the early developmental stages of five species of Calanoid copepods common in the plankton. The purpose of this study is to generate an understanding of the factors affecting the species-specific impact of Labidocera, as a representative of the general class of small invertebrate predators, on a community of planktonic marine copepods. I acknowledge the comments of M. M. Mullin, T. Zaret, and an anonymous reviewer. K. Zakar, D. Checkley, and J. Heinbokel assisted with field collections. The photographs in Fig. 1 were taken in collaboration with J. R. Beers and G. L. Stewart. Methods Labidocera was collected by subsurface net tows (about 5 m) from the coastal waters off La Jolla, California, 1 or 2 days before being used in feeding experiments. The copepods were kept in the laboratory on a diet of brine shrimp nauplii (Artemia salina) and large dinoflagellates (Gymnodinium splendens) which sustains high levels of activity and egg production. Preliminary experiments with natural prey indicated that there was no effect of prey preconditioning on subse- quent feeding of Labidocera on prey rnixtures. Experimental prey-the immature stages of Acartia tonsa, Acartia clausi, Paracalanus parvus, L. trispinosu, and Calanus pacijicus-were mass-cultured from eggs produced by field-collected fe- males of each species. Eggs from reproducing stocks were collected daily and placed in 600- or l,ooo-ml beakers where, after hatching, the nauplii were fed algal mixtures appropriate to their size and feeding preference. The cultures were transferred to clean beakers about once a week. Development was rapid for all species and mortality generally low. When excessive mortality was observed, the remaining animals were assumed to be unhealthy and were discarded. Carbon content of the various developmental stages of copepods grown in culture was measured by placing up to 600 individuals on precombusted glassfiber filters and analyzing by standard methods (Hewlett-Packard model 185B: Sharp 1974). For rapid staging, capturing, and counting, the prey used in feeding experiments were lightly anesthetized in a solution of m-aminobenzoic acid ethyl ester, methanesulfonate salt (Cal- Biochem). The concentration of the anesthetic was adjusted for each species to minimize avoidance while allowing the animals to continue to swim slowly and maintain their vertical positions in a petri dish. Standard experiments were done in 12 4-liter glass jars, each jar initially containing Millipore-filtered seawater and a light slurry of Isochrysis galbnna or Thulassiosira jluviatilis to serve as food for the prey. Typically 50 individuals of each of four developmental stages (usually Nl, N3, N5--N6, and Cl-C2) of a single prey species were transferred from the cul- tures to each of the jars. However, during one experiment when developmental stages of Calanus were used as prey, there were enough large nauplii (N5-N6) for only five of the jars, two of which ultimately were selected as controls. All experiments with prey mixtures also con-

3 Murine copepod predation 1105 tamed 50 first stage nauplii (Nl) of A. tonsa, and an additional experiment was performed using only 50 A. tonsa Nl per jar. The standard experiments thus differed appreciably in species, size composition, and initial densities of prey. If the feeding behavior of Labidocera was sensitive to the composition of the available prey, differences in the feeding rate on the common prey in the various prey mixtures, A. tonsa Nl, would bc cxpected. Experiments were begun when four Labidoceru females were added to each of eight randomly selected jars; the four remaining jars served as controls. All of the jars were filled to the brim with seawater and topped with a piccc of Teflon film which was held in position with a screwcap lid. The jars were rotated horizontally at C for 24 h on a lightdark cycle of 16:8, Illumination during the light cycle was indirect and of about 1 lux. Experiments were ended by removing some water from each jar with a siphon protected by Nitex mesh and adding Lugols iodine fixative. Later, the contents of the jars were concentrated and the remaining organisms staged and counted under a dissecting microscope. The effect of anesthetizing prey on their subsequent survival was determined for a culture of A. tonsu (Nl-N2), the species most sensitive to the chemical. A culture of about 3,000 nauplii was divided into halves volumetrically; the animals from one half were divided into four replicate 25-ml plastic petri dishes without exposure to the anesthetic, while those from the other half were transferred to four replicate dishes containing fresh seawater after they had been completely immobilized with the anesthetic. After incubation at 18 C for 24 h, the dead nauplii in each dish were first counted and removed, and then the remaining nauplii were killed with Formalin and counted to calculate initial numbers and percentage mortality. The effects of jar size and prey density on the feeding rates of Labidocera were tested in the range of prey-liter-l (A. tonsa Nl) in l- and 4-liter jars with one female Labidoceru per jar. Four experimental replicates were prepared for each condition; other aspects of the experiment followed standard procedures. The effects of light and dark and diurnal cycles on the feeding rates and prey selectivity of Labidocera were detcrmined in mixtures of 50 individuals each ofa. tonsa Nl, Culanus Nl, and Calanus N5-N6 in l-liter jars. Of 20 identically prepared jars four were selected as controls; the remaining jars each received two female Labidocera and were divided randomly into light and dark (aluminum foil wrapped) experimental conditions. Identical experiments following this design were run under fluorescent light at 18 C from and from lloo within a 24-h period. The results of feeding experiments are expressed as daily clearance rates by the equation F = MnJ - Wh>l V, NT where n, and n, are the numbers of prey recovered in control and experimental jars, V is the jar volume in liters, N is the number of Lnbidoceru per jar,? is the duration of the experiment in days, and F is the clcarancc rate (liters *copepod-l u d-l). Use of this equation requires that recovery of prey in control jars be virtually 100% of those added initially. Clearance rates as defined above reflect not only the feeding biology of Labidocera, e.g. search speed and perception and handling of prey of different types, but also the ability of prey to avoid capture. Qualitative differences in the avoidancc capabilities of various prey were evaluated by exposing a mixture of different prey to potential capture by a siphon tube which grossly simulates a feeding current. The experimental container was a l-liter glass jar with a nontoxic plastic lid through which two holes had been drilled. Water was siphoned out of the jar through a glass pipette (l-mm opening) fit snugly through one of the holes and extending to the middle of the jar; water was simultaneously al-

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5 Marine copepod predation 1107 ;) I t I 0! 0 1 I INITIAL PREY DENSITY (NUMBERaLITER-l) Fig. 2. Effects of initial prey density and containcr volume on clearance rates of Acartia tonsu N2 by Lnbidocera. Closed and open circles rcpresent experiments in l- and 4-liter jars. Vertical lines indicate range of four replicates. dark, indicating that perception of prey occurs without visual cues. Although significant diurnal differences (P = 0.01: Wilcoxon T-test) in the feeding rates on all prey were noted, these differences are averaged over the 24-h experiments. Clearance rates of Labidocera were not affected by the size of the experimental container at the densities of prey tested (Fig. 2). Of particular significance is the complete lack of threshold feeding behavior at extremely low values of available carbon (6 A. tonsa N l-n2 = 0.3 pg C *liter-l). Among filter-feeding, herbivorous zooplankton, reduced filtering effort at low food concentrations minimizes energy losses and may thus be regarded as an energy-optimizing aspect of their feeding behavior (Frost 1975; Lam and Frost 1976; Lehman 1976). Labidocera apparently does not alter its searching effort for prey in response to decreasing prey availability. As a consequence of its sustained high level of activity and its lack of significant lipid reserves, Labidoceru has an extremely low tolerance of starvation conditions, suffering irrevers- 01 I Nl N2 N3 N4 N5 N6 Cl c2 c3 DEVELOPMENTAL STAGE Fig. 3. Clearance rates of Labidoceru on various developmental stages ofacartia tonsa (0) andacurtiu clausi (0). Vertical lines represent 95% confidence limits for mean of eight replicates. Points without confidence limits rcprcscnt mean (eight replicates) clearance rates on A. tonsu Nl in standard experiments with various mixtures of alternate Prey. ible damage after only 2 days without food. For purposes of interpreting experiments, the losses of prey, other than to predation, are trivial. No effect of anesthetizing prey animals on subsequent mortality was observed; mortality for anesthetized nauplii was 2.0% (range %), for nonanesthctized controls 2.7% ( %). Although these are re- sults of only one experiment on one prey type, there are indications from the experiments themselves that mortality was always low for all prey organisms: The first indication is the relativelv low incidence of partially decomposed prey re- covered in control jars, not more than one or two per jar. The second indication is the high incidence of molting during experiments. The first stage nauplii of all prey species and the Nl and N2 stages of Culanus and Paraculanus, for example, were typically never recovered as these stages after an experiment, since they have durations ~24 h.

6 1108 Landry 2,o r, 0 0 Nl N2 N3 N4 N5 N6 Cl C2 C3 DEVELOPMENTAL STAGE Fig. 4. Clearance rates of Labidoceru on various developmental stages of Parucalunus. Vertical lines represent 95% confidence limits of eight replicates. The overall percentage recovery of prey in control jars relative to the initial number I intended to use was 98.8% (SD = 2.27; n = 46). This indicates low mean counting and handling errors as well as low rates of predator-prey interactions between prey organisms; the form of the clearance rate equation is thus justified. Standard feeding experiments and prey avoidance-the clearance rates of Labidocera on various developmental stages of A. tonsa and A. clausi are presented in Fig. 3. Clearance rates for the two species clearly follow a similar pattern of increase through the naupliar stages and decrease in the early copepodid stages; corresponding early stages of the two Acartia species are of similar sizes (Table 1). Although confidence limits for clearance rates on individual stages overlap considerably, the trends in prey selectivity, as determined by rank correlation of clearance rates in individual experimental jars, are highly significant (P = 0.01: Friedmans W-test). In individual jars, Labidocera consumed a small or a large proportion of the total available prey but always followed a similar order of prey selection. Table 1. Length, width, and carbon content of common prey used in feeding experiments. For copepodid stages, length refers to cephalothorax only. Stage Length b.4 Width h) Carbon (ILd Lubidocera N N N Cl A. tonsa N N N N Cl A. cluusi N N N N c Puruculunus N N N Cl c Calanus N N N Cl Clearance rates on A. tonsa Nl were not significantly different in any of the experiments with different prey mixtures or without alternate prey (Fig. 3). This leads me to conclude that, within the various conditions of available prey in this study, Labidocera does not modify its feeding behavior on any one prey in response to the presence or absence or composition of alternate prey. Therefore, observed differences in clearance rates for various prey types probably reflect inherent differences in how Labidocera perceives and captures the different prey and are not due to artifacts of the experimental mixtures. The rates of clearance of Parucalanus (Fig. 4) and Culanus (Fig. 5) developmental stages by Labidoceru follow the pattern observed for Acurtia species. Larger naupliar stages are captured and consumed at higher rates than smaller stages; clearance rates decrease for the early copepodid stages. The pattern for

7 Marine copepod predution e I 01 Nl N2 N3 N4 N5 N6 Cl C2 C3 DEVELOPMENTAL STAGE Fig. 6. As Fig. 4, but on Labicloceru. 1 I 1 1 I 1 I 1, Nl N2 N3 N4 N5 N6 Cl C2 C3 DEVELOPMENTAL STAGE Fig. 5. As Fig. 4, but on Calanus. Labidocera feeding on its own early stages was dissimilar, however, as clearance rates continued to increase into the copepodid stages (Fig. 6). Mean clearance rates on developmental stages of the large copepod Calanus are 2-4 times greater than for corresponding stages of smaller species-acartia and Paracalunus. A composite of the preceding data normalized to the mean clearance rates on A.. tonsa Nl-N2 in individual experiments is presented in Fig. 7. The trend for higher clearance rates on larger nauplii is significant at P = 0.01 (Corner test); deviations from a more pervasive size-selective tendency occur only for copepodid prey. Experiments with mixtures of prey ranging from ParucaZanus Nl to Calanus N5-N6 have further demonstrated that relative clearance rates on naupliar prey are statistically identical for males, females, and C5 Labidocera, the stages which have the predominant effect on copepod communities in nature (Barnett 1974). Absolute clearance rates of nauplii by C5 Labidocera were 70% of the clearance rates of adult copepods. Large nauplii represent an extremely important source of food for Labidocera even when they constitute a relatively small numerical fraction of the prey in nature. As an extreme example, in order for Labidocera to consume an equal amount of carbon from Acartia N2 or Calanus N6 as prey the numerical density of Acurtia nauplii must be greater by a factor of 200. While feeding rates of Labidocera on nauplii of Calanoid copepods are dependent on prey size, they are not obviously affected by the species composition of similarly sized prey. The possible exception to this is a slight tendency for clearance rates to be lower for nauplii of Labidoceru than for other prey of the same length. It is difficult, of course, to demonstrate conclusively that the observed size-selective feeding of Labidocera on nauplii is really due to feeding specificity of the copepod rather than to an inherent reduccd ability of larger nauplii to avoid predators. Sluggishness of advanced naupliar stages could also occur as a consequence of culturing procedures if vitality decreases with the length of exposure to

8 Landry I I I I I I 1 J,2,4,6 18 PREY LENGTH (mm> Fig. 7. Relative clearance rates of Lubidoceru as a function of prey size. Data normalized to mean clearance rate on Acurtiu tonsa Nl. Prey species- A. tonsa (0), Acartia clausi (x), PurucuZunus (O), Calanus (+), and Lubidoceru (A); C-copepodid stages. Vertical lines represent 95% confidence limits of eight replicates; broken line represents range of three replicates. laboratory conditions. The results of avoidance experiments gave no indications of these problems, however. Ability to avoid a siphon current increases with the increasing size of naupliar and copepodid stages with no apparent differences between species (Fig. 8). The ability of individual prey to avoid capture by the siphon current increases with decreasing strength of the current, and the effects are proportionately greater for larger prey. Discussion The following observations can be made regarding the feeding behavior of Labidocera at low densities of naturally occurring prey. First, Labidocera cap- tures prey at rates which simply reflect its ability to detect given prey and the ability of the prey to avoid capture. There is apparently no behavioral adaptation to prey density or prey preference; behavioral changes should have appeared as changes in feeding rates on Acartia nauplii, the standard prey in all experiments. Second, Lubidoceru feeds selectively on larger nauplii despite the fact that these nauplii are more capable of avoiding capture than smaller prey. Since detection of prey by the copepod and prey avoidance of capture are the variables that determine the relative rates with which Labidocera feeds on different prey, this means that the copepod detects larger nauplii at a greater range than smaller prey. OBrien et al. (1976) have

9 Marine copepod predution 1111 COPEPOD LENGTH hrd Fig. 8. Efficiency of capture of various prey by a siphon current. Prey-Acartia tonsu (0), ParacuZanus (O), Lubidoceru (A), and Culunus (+); C-copepodid stages. Lower points and line represent replicate experiment with 50% reduction in mean velocity of siphon current. discussed this phenomenon as it applies to size selection by planktivorous fish on the basis of apparent size of prey. Rather than visually detecting prey, Labidocera probably uses the long setae located at the base of each of its first antennae (see Fig. 1) to sense disturbances generated by the prey. These disturbances may be caused by the beating of the swimming appendages of the prey or by the preys presence in the swimming current of Labidocera and, therefore, its disruption of normal streamlines. In addition to prey size measured as length, the signal generated by a prey may also be dependent on its body shape. Thus, relative to the ovoid nauplii of the other prey species, the long, slender shape of Labidocera nauplii might be advantageous if it rcduces their turbulent wake when they are in a predators swimming current. This could be one reason why Labidocera nauplii arc captured by predatory adults at lower rates than comparably sized nauplii of other species. Third, clearance rates generally fall off sharply for copepodid stages relative to the largest nauplii of a given prey species. This is probably due to morphological changes during the molt from N6 to Cl stages, as copepodids have swimming legs and long antennae which afford them more rapid and effective escape responses than nauplii. While Labidocera feeds on nauplii at rates more dependent on prey size than on species, species identity and development stage seem to be important variables in characterizing the feeding of Labidocera on copepodids. In expcriments similar to those detailed here I have not observed a single instance where Labidocera was able to capture adult Acartia or Paracalanus, even though these copepods are similar in size to early copepodids of Calanus which are

10 1112 Landry captured at relatively high rates. The additional swimming legs which develop as a copepod matures as well as the extra strength and experience it may acquire could be important in limiting the stagespecific susceptibility of a given species to predation by small invertebrates; apparently adult copepods are relatively immune to predators like Labidocera irrespective of their actual size. The limited vulnerability of copepodid stages to predation by Labidoceru has important consequences in assessing the effect of this predator on the size and species composition of the prey community in nature. During Barn&ts (1974) study of the nearshore distribution of Labidocera off southern California, there were about 1,000 predatory individuals (male, female, and CS) per m2 in the upper 25 m of the water column within 5 km of shore. At this density, if we assume randomly distributed predators and prey (an assumption which underestimates the impact of the predator since Barnett demonstrated a correspondence between the depth strata of maximum Labidocera and prey abundance), then Labidocera will cause average daily rates of mortality of 7.5,2.8, and 2.0% on early developmental stages (Nl-Cl) of Calanus, Paracahus, and Acartia. When cxtendcd over the developmental times I have observed for these species (Calanus-10 d; Acartiu- 10 d; Paracalanus-6 d from Nl-C2 at LYC), these rates account for population mortalities of 54% for Calunus but only 18 and 15% for the smaller Acartiu and Paracalanus. During the interval in which Acartia or Parncalanus develops from early copepodid to adult there will undoubtedly be additional mortality due to predation by Labidocera; however, the probability of copepodid stages being captured is much lower than for nauplii, so this mortality is unlikely to significantly add to the population mortality of the naupliar stages. Therefore, in contrast to what would have been predicted from studies of predatory copepods in freshwater ecosystems, Labidoceru exerts a selective impact on larger prey species. The discrepancy between the suggest- ed impact of Labidoceru on marine zooplankton and the observation that invertebrate predators generally favor the dominance of large zooplankton in freshwater systems can be reconciled if we consider the differences between the dominant prey in freshwater and marine plankton. Freshwater ecosystems are dominated by herbivorous cladocerans which, unlike copepods, do not undergo major morphological changes during their development; newly liberated young differ from adults basically only in size. Assuming that there are no consistent differences in the growth rates of similarly sized individuals of large and small species or their abilities to avoid predators, we find small predators exert a greater impact on smaller cladoceran species because these species spend a disproportionately greater fraction of their lifetime within a size range that can be exploited. This conclusion assumes that larger zooplankton enjoy a refuge in size from invertebrate predators but is not affected by the possibility that those predators might feed size selectively on larger prey within the range of prey they can handle. In contrast, the tendency for all predators to select for the largest prey they can capture is critical in the marine plankton where the dominant herbivores are copepods. The ability of small predators to capture copepods decreases sharply after the prey develop to the copepodid stages. Consequently, the prey available to the predator consist of the small nauplii of smaller species and the large nauplii of larger species, with little size overlap. My study has demon- strated that even though a small predator may be physically limited to capturing only the smaller developmental stages (i.e. nauplii) of any individual prey species, it can, through size-selective predation on this limited range of prey, exert a greater impact on the larger copepods in the planktonic community. Labidocera is apparently not alone in its tendency to feed size selectively on nauplii. For example, Tortanus discaudatus, another predatory copepod, also

11 Marine copepod predation 1113 feeds at higher rates on the larger nauplii of Calanus (Ambler and Frost 1974). While this by no means demonstrates that invertebrate predators as a whole have opposite effects on the size structures of freshwater and marine zooplankton, it does suggest that because different types of organisms dominate in the two systems, processes and relationships which seem well demonstrated or intuitive in one of the systems do not necessarily apply in the other. References AMBLER, J. W., AND B. W. F~osr The fecding behavior of a predatory planktonic copcpod, Tortanus discaudatus. Limnol. Oceanogr. 19: ANDERSON, R. S Predator relationships and predation rates for crustacean zooplankters from some lakes in western Canada. Can. J. Zool. 48: BAFLNETT, A. M The feeding ecology of an omnivorous neritic copepod, Labidocera trispinosa Esterly. Ph.D. thesis, Univ. Calif. 215 p. BRANDL,~., AND C. 1I. FEIWANDO Feeding of the copepod Acanthocyclops vernalis 011 the cladoceran Ceriodaphnia reticulata under laboratory conditions. Can. J. Zool. 52: ,AND u. Food consumption and utilization in two freshwater cyclopoid copepods (Mesocyclops edax and Cyclops vicinus). Int. Rev. Gesamten IIydrobiol. 60: ,AND -, 1975b. Investigations on the feeding of carnivorous cyclopoids. Int. Ver. Theor. Angew. Limnol. Verh. 19: BROOKS, J. L The effects of prey size selection by lake planktivores. Syst. Zool. 17: AND S. I. DODSON Predation, body size, and composition of plankton. Science 150: DODSON, S. I Zooplankton competition and predation: An experimental test of the size-cfficiency hypothesis. Ecology 55: FROST, B. W Feeding processes at lower trophic levels in pelagic communities, p. 5% 77. Zn C. B. Miller [ed.], The biology of the oceanic Pacific. Oregon State A threshold feeding behavior in Calanus pacificus. Limnol. Oceanogr. 20: HEINLE, D. R Production of a Calanoid copepod, Acartia tonsa, in the Patuxent River Estuary. Chesapeake Sci. 7: IIRBA~EK, J.,M. DVO&~KOVA, V. KO~~NEK,ANDL. PROCI-IAZK~VA Demonstration of the effect of the fish stock on the species composition of zooplankton and the intensity of mctabolism of the whole plankton association. Int. Ver. Theor. Angew. Limnol. Verh. 14: KERFOOT, W. C The divergence of adjacent populations. Ecology 56: Implications of copepod predation. Limnol. Oceanogr. 22: LAM, R. K., AND B. W. FROST Model of copepod filtering response to changes in size and concentration of food. Limnol. Oceanogr. 2 1: LE~IMAN, J. T The filter-feeder as an optimal forager, and the predicted shapes of feeding curves. Limnol. Oceanogr. 2 1: LILLELUNI), K., AND R. LASKER Laboratory studies of predation by marine copepods on fish larvae. Fish. Bull. 69: MULLIN, M. M.,AND E. R. BROOKS Production of the planktonic copepod, Calanus helgolandicus. Bull. Scripps Inst. Oceanogr. 17: OB~UEN, W. J., N. A. SLADE, AND G. L. VINYARD Apparent size as the determinant of prey selection by bluegill sunfish (Lepomis macrochirus). Ecology 57: PARSONS, T. R., R. J. LEBRASSEUR, J. D. FULTON, AND 0. D. KENNEDY Production studies in the Strait of Georgia. 2. Secondary production under the Fraser River plume, February to May, J. Exp. Mar. Biol. Ecol. 3: SI-IARP, J. II Improved analysis for particulate organic carbon and nitrogen from seawater. Limnol. Oceanogr. 19: STEELE, J. H., AND B. W. FROST The structure of planktonic communities. Phil. Trans. R. Sot. Land. 280: STENSON, J. A Significance of predator influencc on composition of Bosmina spp. populations. Limnol. Oceanogr. 2 1: STEWART, G. L., J. R. BEERS, AND C. KNOX Application of holographic techniques to the study of marine plankton in the field and in the laboratory. Proc. Sot. Photo-opt. Instr. Eng. 41: ZARET, T. M Strategies for cxistcncc of zooplankton prey in homogeneous environments. Int. Vcr. Thcor. Angew. Limnol. Vcrh. 19: , AND W. C. KERFOOT Fish predation on Bosmina Zongirostris: Body-size selection versus visibility selection. Ecology 56: Submitted: 9 November 1977 Accepted: 5 July 1978