Effects of conspecifics and phytoplankton on predation rates of the omnivorous copepods Epischura Iacustris and Epischura nordenskioldi

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1 444 Notes microorganisms. Appl. Environ. Microbial. 47: _ AND Diel nucleic acid synthesis and particulate DNA concentrations: Conflicts with division rate estimates by DNA accumulation. Limnol. Oceanogr. 31: WRIGHT, R. T Methods for evaluating the in- teraction of substrate and grazing as factors controlling planktonic bacteria. Ergeb. Limnol. 31: Submitted: 25 March 1988 Accepted: 25 July 1988 Revised: 30 November 1988 Limnol. Oceanogr., 34(2), 1989, 44U , by the American Society of Limnology and Oceanography, Inc. Effects of conspecifics and phytoplankton on predation rates of the omnivorous copepods Epischura Iacustris and Epischura nordenskioldi Abstract-We measured the effects of conspecifics and phytoplankton on the rate at which Epischura lacustris and Epischura nordenskioldi prey upon Calanoid nauplii. Per capita predation rates of Epischura in the presence of conspecifics and phytoplankton were 73% lower than those of lone individuals in the absence of phytoplankton. Because these effects occurred at common field densities of Epischura, animal prey, and phytoplankton, it is likely that they occur in situ. Therefore, estimates of the effect of spatial and temporal patchiness on predation rates of omnivorous copepods should consider phytoplankton and conspecifics, not simply the abundance and composition of the animal prey assemblage. It is well known that zooplankton and phytoplankton distributions are spatially and temporally patchy (e.g. Dumont 1967; Malone and McQueen 1983; Tessier 1983). The significance of this patchiness cannot be assessed, however, until the consequences of patch composition for individ- Acknowledgments This research was supported by NSF grant BSR to C.L.F. and by the Dartmouth College Cramer Fund. Nelson Hairston, Jr., Hugh MacIsaac, Rich Stemberger, and two anonymous reviewers provided comments that greatly improved the manuscript. Karen Baumgartner counted the phytoplankton and assisted with preparation of the figures. We thank The Norford Lake Club and The Hanover Improvement Society for access to Norford Lake and Storr s Pond, respectively. ual animals at realistic field densities are identified. Patchiness exerts some of its most obvious effects on foraging behavior. For example, many studies have shown that zooplankton predation rates increase with prey density (e.g. Rigler 196 1; Confer 197 1; Frost 1972). In contrast, although encounters between conspecifics will also be influenced by patchiness, there are few empirical data testing the effects of conspecific predator density on foraging rates of predatory zooplankton. Studies of the effects of predator density on predator foraging have focused on parasitoids and social vertebrates. In general, increases in parasitoid density reduce per capita predation rates (mutual interference sensu Hassell 1978) while per capita predation rates of social vertebrates typically peak at some intermediate group size (Pulliam and Caraco 1986). Most studies of mutual interference examine a broad range of predator densities, which has led some investigators to question the importance of this phenomenon in the field because the reported effects are often greatest at densities that are much greater than those that commonly occur in situ. In this study we examined mutual interference at two densities of predators that routinely occur in the field. We hypothesize that per capita predation rates will be reduced by conspe-

2 Notes 445 Table 1. A comparison of the phytoplankton composition (cells ml- ) of 25-pm-filtered and unfiltered lake water. Norford Lake Starr s Pond LJn- Unfiltered Filtered filtered Filtered 15 Aug 11 Aug 3 Jun 2 Jun Bacillariophyceae Chlorophyta 1,272 1, Chrysophyceae 1, ,854 2,307 Cryptomonadineae Cyanophyta Others Total 2,825 2,492 3,213 2,569 cifics whenever conspecific interactions involve interference competition or predation. Another important consequence of plankton patchiness is that zooplankton encounter variation in the composition and abundance of phytoplankton. For omnivorous zooplankton, feeding rates are likely to respond to the presence of both phytoplankton and zooplankton prey. Even though many, if not most, predatory zooplankton are omnivores, however, only a few studies have examined the effects of phytoplankton on predatory behavior, and they have not led to a general consensus. We present data on the effects of conspecifics and phytoplankton on per capita predation rates of Epischura lacustris and Epischwa nordenskioldi - members of one of the most common genera of Calanoid copepods in the northeastern United States and eastern Canada (Carter et al. 1980). Our objectives here are to determine whether per capita predation rates decrease when conspecifics are present at realistic field densities, to measure the effect of phytoplankton presence or absence on predation rates, and to examine the interaction between the effect of conspecifics and phytoplankton, an alternative food, on predation rates by establishing a continuum from maximal to minimal predation rates based on the presence or absence of conspecifics and phytoplankton. All organisms and water were obtained from either Norford Lake (Thetford, Vermont) or Storr s Pond (Hanover, New Hampshire). We used E. lacustris in three experiments (2 June, 11 June, and 11 August 1986) and E. nordenskioldi in the other experiment (25 May 1986). The results were qualitatively identical for both species. Calanoid nauplii (almost entirely Diaptomus minutus) that co-occur with Epischura were used as prey. It was not feasible to use nauplii of a single instar in all experiments, but in a preliminary experiment Epischura predation rates on stage I-III nauplii and stage IV-VI nauplii were not significantly different (NI-NIII mean = 6.6 prey d-l, SE = 2.1, NIV-NV1 mean = 9.3 prey d-l, SE = 2.4; t-test, P = 0.44, n = 6). Furthermore, all experiments were fully blocked and randomized. All treatments were run in lake water filtered through Whatman GF/A filters to remove phytoplankton (referred to as phytoplankton-free water) or filtered through 25-pm Nitex mesh to retain phytoplankton but remove zooplankton (referred to as natural lake water). The phytoplankton composition of 25-pm-filtered lake water was almost identical to the phytoplankton composition of the unfiltered lake water (Table 1). Epischura were preconditioned individually in the natural lake water in 3%ml shell vials in the dark for 36 h. During preconditioning, 50 Calanoid nauplii (100 liter-l) were placed into each experimental beaker. Although Calanoid nauplii are usually present at lower densities in situ, the combined density for all of the zooplankton prey of Epischura frequently surpasses this density. Experiments were run in 500 ml of natural or phytoplankton-free lake water in 600- ml beakers for 24 h at 15 C in the dark; 24-h experiments eliminate the complica- tion of diel periodicity in feeding rates and do not require extrapolation to calculate daily predation rates, and 15 C is the approximate midrange of temperatures encountered by the animals in situ over the season during which the experiments were performed. Darkness eliminates the possibility of prey aggregation toward lights. One treatment was presence or absence of conspecifics. Replicates contained either one or three adult Epischura (two or six Epischura liter- ). These densities closely bracket the mean density and the mean ex-

3 446 Notes h I n G n 2 n v Mean Prey Density h 1 ; 160 Q,.+ n Q E, I. Mean Prey Density Fig. 1. The functional response of Epischura lacustris with Calanoid nauplii as prey. Symbols show mean predation rates (A) or mean clearance rates (B) k 1 SE. The SE values for mean prey density (ind. per 500 ml) fall within the symbols for each mean. The best statistical fit to the raw data of Fig. 1 A is: predation rate = (mean prey density) (mean prey density)2, P < , R2 = 0.57 (Kleinbaum and Kupper 1978). There is no significant effect of mean prey density on clearance rate. perienced density (sensu Lloyd 1967) of adult E. lacustris in Norford Lake (3.0 and 5.3 liter-l respectively) (Folt and Schulze in press). Because we report experiments with only two treatment levels, and because the lower density treatment contained only one Epischura individual per replicate, we restrict our conclusions to the effect of conspecific presence vs. absence, rather than the effect of conspecific density. The second treatment was presence or absence of phytoplankton. Beakers contained either natural lake water or phytoplanktonfree lake water. The same two Epischura densities were included on three dates; the fourth experiment also included treatments with 12 and 24 Epischura liter-. Experiments with two Epischura densities had six replicates per combination of predator density and phytoplankton condition for a total of 24 experimental beakers. The experiment with four Epischura densities had four replicates per combination of predator density and phytoplankton condition for a total 32 experimental beakers. Each experiment included eight control beakers (four with and four without phytoplankton) that lacked predators, but contained 50 Calanoid nauplii. The controls were used to measure nonpredatory loss of prey, which was very low (mean = 1.8%). The functional response of E. Zacustris was measured under the same experimental conditions with lone individuals in phytoplankton-free lake water. Initial prey densities ranged from 5 to 60 prey per 500 ml, with a minimum of 10 replicates at each prey density. Daily per capita predation rates (number of prey predator-l d-l) were calculated as 40 SO 60 Cc where c is the average number of prey remaining in the controls after 1 d, e the number of prey remaining in the replicate after 1 d, and p the number of predators (Epischura) in the replicate. All data were also analyzed as clearance rates (volume of water cleared of prey predator- d-*, Rigler 197 1) and the conclusions were the same in every instance. We report the results as predation rates because predation rates were measured directly and because clearance rate calculations assume that predator-prey encounters occur randomly and that the functional response is linear, which is not true in this case (Fig. 1; Rigler 197 1). Prey viability was measured by pouring the contents of additional control beakers into tissue culture flasks and inspecting them under a dissecting microscope. Only 2 prey out of 360 were found dead. Therefore, prey mortality from causes other than predation was assumed to be insignificant. The main experiments were analyzed by ANOVA and differences between central tendencies were compared with t-tests and Mann-Whitney U-tests. Both tests led to the same conclusions in all cases. The functional response data were analyzed by regressing predation rate and clearance rate (in separate analyses) on mean prey density.

4 Notes 447 Mean prey density was calculated for each beaker as the arithmetic mean of the initial and final prey densities. Predation rates of lone Epischura were nearly twice as high as those of individuals in the treatments with three conspecifics per 500 ml under natural phytoplankton conditions (Fig. 2A). Differential prey depletion was not responsible for the differences in predation rates between these treatments. The mean numbers of prey present during the experiments (Fig. 2A) in the treatments with one and three Epischura were 48 and 47. Although regression equations fit to functional response data predict only a 1% difference in predation rates at these prey densities (Fig. l), predation rates in treatments with one Epischura were twice as high as those in treatments with three Epischura (Fig. 2A). The effect of conspecifics was not significant in phytoplankton-free water, but there was a trend toward reduced predation rates in the presence of conspecifics in three of four experiments (Fig. 2B). Regression analysis of the experiment with four Epischura densities (1, 3, 6, and 12 individuals per 500 ml) showed that predation rates declined significantly with predator density over the entire range of predator densities, but prey depletion in the 6- and 12-Epischura treatments may have been responsible for the further decline in predation rates measured at those densities. Therefore, we do not know whether the effect of conspecifics plateaus at densities above 3 per 500 ml, or whether predation rates continue to decline at higher densities. We can conclude that at normal field densities the effect of conspecifics is significant and that this effect is large (biologically meaningful); a 50% decrease in predation rates results from trebling the abundance of Epischura. Because the effect was large and was measured at normal field densities of phytoplankton and conspecifics, it is likely to be important in the field. There is very little published information on the effect of conspecifics on zooplankton predation rates. The data for Epischura nevadensis (Folt and Byron 1989), combined with the data provided above (Fig. 2A), suggest that the effect of conspecifics is consistent across the genus Epischura. Because,a 14 I B s 8 1 Epischura 3 Epischura -- Fig. 2. The effect of conspecifics on Epischura predation rates. The figure shows means + 1 SE. Pairs of bars represent experiments of a given date. Lines connect means that are not significantly different (P L 0.05) (within-date comparisons). A. Natural lake water (phytoplankton present, 25-lrn-filtered water). Overall significance level: P < (Mann-Whitney U-test based on data pooled from four dates). B. Phytoplankton-free lake water. Overall significance level: P > 0.1 (Mann-Whitney U-test based on data pooled from four dates). neither Jamieson (1980, Mesocyclops leuckarti) nor Cooper and Goldman (1980, Mysis relicta) found an effect of conspecifics on predation rates, however, it appears that the importance of mutual interference may vary significantly among other genera. Changes in either prey or predator behavior could be responsible for the effect of conspecifics on predation rate. Although it is possible that prey (nauplii) behavior changes as the density of Epischura increases, we hypothesize that Epischura behavior changes in the presence of conspecifics because Epischura adults are cannibalistic at natural field densities. For instance, in an experiment designed to measure survivorship and egg production rates with one male and one female E. Zacustris in each of ml jars, cannibalism occurred among seven pairs of adults, accounting for 13% of the mortality (Schulze and Folt unpubl. data). We did not identify the specific behav-

5 448 Notes 8 T! El Phytoplankton present Phytoplankton absent 0 Fig. 3. The effect of phytoplankton availability on Epischura predation rates. The figure shows means + 1 SE. Pairs of bars represent experiments of a given date. Lines connect means that are not significantly different (P , within-date comparisons). A. One Epischwa per 500 ml. Overall significance level: P < 0.05 (Mann-Whitney U-test based on data pooled from four dates). B. Three Epischura per 500 ml. C. Six Epischura per 500 ml. D. Twelve Epischura per 500 ml. All within-date differences are significant in panels B, C, and D. ior responsible for the effects in the present study, but others have identified mechanisms that could cause reductions in zooplankton feeding rates in the presence of conspecifics (see Folt 1987). For example, Epischura (or nauplii) may use predator avoidance behaviors such as reduced activity (Kerfoot 1978; Williamson 1980; Wong et al. 1986) or active escape responses (Williamson 1983; Gilbert 1985; Wong et al. 1986) that would reduce contacts with predators (Epischura). We suspect that by reducing encounters with conspecifics Epischura coincidently reduces encounters with prey as well. Furthermore, we hypothesize that conspecifics have the greatest effects on each other in cannibalistic zooplankton species, which may explain the absence of conspecific effects in other studies. Jamieson stated that cannibalism is very rare among A4. Zeuckarti. We know of no evidence of cannibalism in M. relicta. Predation rates in the presence of phytoplankton were reduced by almost 50% compared to those in the absence of phytoplankton (Fig. 3). Although several studies have examined the effects of phytoplankton on copepod predation rates, a single general relationship has not emerged. Studies of marine species suggest, however, that phytoplankton effects tend to be consistent within some genera. Predation rates of both Calanus jinmarchicus (Anraku and Omori 1963) and Calanus pacz$cus (Landry 198 1) decline as phytoplankton concentration increases. In contrast, predation rates of Centropages hamatus, Centropages typicus (Anraku and Omori 1963), and Centropages furcatus (Paffenhiifer and Knowles 1980) are unaffected by phytoplankton, as are those of Temora stylifera (Paffenhofer and Knowles 1980). Conflicting results for Acartia tonsa (Anraku and Omori 1963; Lonsdale et al. 1979) prohibit generalization about the effect of phytoplankton on the predation rate of this species. There is less information about the effect of phytoplankton on predation rates of freshwater copepods. Williamson and Butler (1986) clearly showed that Diaptomus pallidus predation rates decline as the concentration of phytoplankton increases. This result is consistent with our results on the effect of phytoplankton on E. Zacustris and E. nordenskioldi predation rates (Fig. 3). Two other studies are less instructive. Jamieson (1980) found that M. leuckarti predation rates declined in the presence of cyanobacteria (Microcystis) colonies, even though these colonies were present at a density that is several orders of magnitude greater than the phytoplankton concentration in most lakes (2.5 x 1 O6 mll l); Jamieson described the water as resembling green soup. Therefore, her results may not be representative of the response of this species to more common lacustrine situations. In a

6 Notes 449 Table 2. A comparison of the four treatment combinations from data pooled across dates (experiments). The mean predation rates (prey predator- d-l) (*SE) for each treatment are given along with the significance of the differences between each mean and the mean for the one Epischuru, phytoplankton-absent treatment. The percentage change for the same comparison is also shown. Statistical results are from Mann-Whitney U-test comparisons; asterisks indicate significance at the 0.05 (*) or the 0.01 (**) level. Phytoplankton One Epischura Three Epischura Mean? SE Percent change Mean -t SE Percent change &0.47* kO ** study that is particularly relevant to our data, Wong (198 1) concluded that phytoplankton do not affect E. lacustris predation rates. There are two problems with this conclusion. First, in one of two reported experiments, predation rates actually declined with increases in phytoplankton density, which is what we found. Second, more than 75% of the E. Zacustris died in some treatments. Wong attributed this mortality to adverse or toxic effects of the phytoplankton Ankistrodesrnus sp. We agree that this cause is probable, especially since E. lacustris can live for over a month on diets limited to other species of algae (Schulze unpubl. data). If the Ankistrodesmus sp. had toxic effects on survival, it is likely to have had adverse effects on predation rates as well, which makes this study difficult to interpret. We have presented two main findings: that E. lacustris and E. nordenskioldi predation rates decline in the presence of conspecifics under natural phytoplankton conditions, and that the presence of natural phytoplankton leads to a decline in the predation rates of the same two species when offered zooplankton as prey. There is a continuum from maximal to minimal predation rates based on the presence or absence of conspecifics and phytoplankton at natural field abundances (Table 2). Due to the combined effects of mutual interference and phytoplankton availability, maximal predation rates occurred in the treatments with one Epischura, and without phytoplankton, while minimal predation rates occurred in the treatments with three Epischura and with phytoplankton. As shown, reductions from the maximum varied from 20% (nonsignificant) to 73%. We contend that these effects will occur in situ because they occurred at field densities of predators, phytoplankton, and prey. Although it was previously well known that predation rates vary with prey density, these results advance our understanding of the consequences of spatial and temporal patchiness in plankton distributions by showing that both phytoplankton and predator patchiness may also be expected to influence predation rates. Even under conditions of constant animal prey density, these other patch variables may cause 73% reductions in predation rates. Given the magnitude of these effects, they may very well have substantial consequences for the fitness of individual predators, as well as dramatic consequences for prey populations. Therefore, these variables should be considered in attempts to predict omnivore ingestion rates and impacts on prey populations in the field, as well as in the design of laboratory experiments. Department of Biological Sciences Dartmouth College Hanover, New Hampshire References Peter C. Schulze Carol L. Fob 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-l 26. CARTER, J. C. H., M. J. DADSWELL, J. C. ROFF, AND W. G. SPRULES Distribution and zoogeography of planktonic crustaceans and dipterans in glaciated eastern North America. Can. J. Zool. 58: 1355-l 387. CONFER J. L Intrazooplankton predation by

7 450 Notes Mesocyclops edax at natural prey densities. Limnol. Oceanogr. 16: COOPER,~. D., ANDC. R. GOLDMAN Opossum shrimp (Mysis relicta) predation on zooplankton. Can. J. Fish. Aquat. Sci. 37: DUMONT, H. J A five day study of patchiness in Bosmina coregoni Baird in a shallow eutrophic lake. Mem. 1st. Ital. Idrobiol. 22: FOLT, C. L An experimental analysis of costs and benefits of zooplankton aggregation, p Zn W. C. Kerfoot and A. Sih [eds.], Predation: Direct and indirect impacts on aquatic communities. New England. p, AND E. R. BYRON A comparison of the effects of prey and non-prey neighbors on foraging rates of Epischura nevadensis (Copepoda: calanoida). Freshwater Biol. In press. AND P. C. SCHULZE. In press. Spatial distribution and zooplankton behavior. Bull. Mar. Sci. FROST, B. W Effects of size and concentration of food particles on the feeding behavior of the marine planktonic copepod Calanus pacificus. Limnol. Oceanogr. 17: GILBERT, J. J Escape response of the rotifer Polyarthra: A high-speed cinematographic analysis. Oecologia 66: HASSELL, M. P Arthropod predator-prey systems. Princeton. JAMIESON, C. D The predatory feeding of copepodid stages III to adult Mesocyclops leuckarti (Claus). Am. Sot. Limnol. Oceanogr. Spec. Symp. 3: New England. KERFOOT, W. C Combat between predatory copepods and their prey: Cyclops, Epischura, and Bosmina. Limnol. Oceanogr. 23: 1089-l 102. KLEINBAUM, D.G., AND L.L. KUPPER Applied regression analysis and other multivariable methods. Duxbury. LANDRY, M. R Switching between herbivory and carnivory by the planktonic marine copepod Calanus pacificus. Mar. Biol. 65: LLOYD, M Mean crowding. J. Anim. Ecol. 36: l-30. LONSDALE, D. J., D. R. HEINLE, AND C. SIEGFRIED Carnivorous feeding behavior of the adult Calanoid copepod Acartia Biol. Ecol. 36: tonsa Dana. J. Exp. Mar. MALONE, B.J., AND D.J. MCQUEEN Horizontal patchiness in zooplankton populations in two Ontario kettle lakes. Hydrobiologia 99: 10 l-l 24. PAFFENH~FER, G.-A., ANDS.C.KNOWLES Omnivorousness in marine planktonic copepods. J. Plankton Res. 2: PULLIAM, H. R., AND T. CARACO Living in groups: Is there an optimal group size?, p Zn J. R. Krebs and N. B. Davies [eds.], Behavioural ecology: An evolutionary approach. Sinauer. RIGLER, F. H The relation between concentration of food and feeding rate of Daphnia magna Straus. Can. J. Zool. 39: Feeding rates. Zooplankton, p Zn W. T. Edmondson and G. G. Winberg [eds.], A manual for the assessment of secondary productivity in freshwaters. IBP Handbook 17. Blackwell. TESSIER, A. J Coherence and horizontal movements of patches of Holopedium gibberurn (Cladocera). Oecologia 60: 7 l-75. WILLIAMSON, C. E The predatory behavior of Mesocyclops edax: Predator preferences, prey de- fenses, and starvation-induced changes. Limnol. Oceanogr. 25: p Behavioral interactions between a cyclopoid copepod predator and its prey. J. Plankton Res. 5: 70 l , AND N. M. BUTLER Predation on ro- tifers by the suspension-feeding Calanoid copepod Diaptomus pallidus. Limnol. Oceanogr. 31: WONG, C. K Predatory feeding behavior of Epischura lacustris (Copepoda, Calanoida) and prey defense. Can. J. Fish. Aquat. Sci. 38: ,C. W. RAMCHARAN,AND W.G. SPRULES Behavioral responses of a herbivorous Calanoid copepod to the presence of other zooplankton. J. Zool. 64: Can. Submitted: 12 January 1988 Accepted: 3 November 1988 Revised: 2 December 1988