The ecological role of chemical stimuli for the zooplankton: Predator-avoidance behavior in Daphia

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1 LIMNOLOGY AND OCEANOGRAPHY I November 1988 Volume 33 I Number 6 Part 2 Limnol. Oceanogr., 33(6, part 2), 1988, 1988, by the American Society of Limnology and Oceanography, Inc. The ecological role of chemical stimuli for the zooplankton: Predator-avoidance behavior in Daphia Stanley Dodson Department of Zoology, University of Wisconsin, Madison Abstract Eight different clones (seven species) of Daphnia had behavioral responses to fish and invertebrate predators. The behavioral response was measured in the laboratory as a change in the average population depth, relative to controls, when exposed to a predator. Behavior for each clone was tested with three common predators: Chaobcvws,, and. Each Daphnia clone responded to at least onc predator. Some clones responded to all three predators. The responses are both predator and prey-specific. The stimulus produced by the predator is a water-soluble chemical that persists for up to 7 h in the laboratory. The number of predator species to which a clone responds shows a positive correlation with average body size of the Daphnia. Number of responses pcr clone is independent of lake size, although there was a tendency (not statistically significant) for the number of responses to decrease with lake size. Behavioral responses may be components of diel vertical migration and horizontal distribution patterns seen in nature. Zooplankton show a great deal of phenotypic plasticity. Although water chemistry, temperature, and zoogeography may determine the general morphology of a species (Hutchinson 1957), several studies of clones have shown that the presence of predators and competitors also affects zooplankton development and growth (Havel 1987; Kerfoot 1987; Stemberger and Gilbert 1987; Stenson 1987; Dodson 1988). In these systems, the induction of antipredator morphologies in cladocerans or rotifers is via a chemical stimulusreleased into water by potential predators. Induced morpho- Acknowledgments Jeffry Baylis, Virginia Dodson, Chris Luccke, and three anonymous reviewers helped revise this manuscript. They and Anne Hershey, Jan Leonard, and John Magnuson provided useful insights into the problem of predator-induced behavior of zooplankton. Thanks to all of you! 1431 logical changes result in prey either too large to be as easily handled or swallowed or too small to be as easily seen by visual predators, compared to the noninduced form. Behavioral defenses, whether induced by chemicals or some other signal, are less well known for zooplankton. Daphnia carinata, besides being hard to handle when it has an induced crest, is also able to swim faster to better evade its predator (Grant and Bayly 1981). Alternatively, Bosmina that hasjust escaped a copepod s grasp ceases all movement, sinks passively, and thereby becomes undetectable (Kerfoot 1978). The daily vertical migration of some zooplankton species is thought to be adaptive predator avoidance, at least in part (Johnsen and Jakobsen 1987; Lampert 1987). In a study of a similar system, Sih (1986) found that Czde.xpipiens (mosquito) larvae moved less and shifted

2 1432 Dodson their microhabitat use when exposed to water in which conspecifics had been preyed on by (backswimmers). The probable advantage of induced behavioral responses is that they can be predator specific, have a short response time, and act only when the predator is present. In Live] y s ( 1986) terms, a cue produced by a predator is highly predictive of a harsh habitat patch. The probable disadvantage of induced behavioral responses, as in induction of resistant morphs (Havel and Dodson 1987), is lowered reproduction, either directly because of the energy requirements of behavior, or indirectly, if predator-avoidance behavior causes zooplankton to move to an area of lower food. This paper reports on behavioral responses that are induced.in Daphnia by the presence of predators. Daphnia was chosen because it is a common member of the freshwater zooplankton, sometimes shows daily vertical migration, comes in a range of body sizes from lakes of all sizes, and has a large effect on the community ecology of freshwater habitats. The main purpose of these behavioral observations was to test for the existence of predator-avoidance behavior in Daphnia. I also tested the hypothesis that the cue is a -chemical and measured the response persistence of the chemical with two ckmes. Methods Observations on the vertical position of Daphnia were made in 20-cm-deep 4-liter jars. The jars were marked off into five equal 4-cm-deep strata. I recorded the number of Daphrlia visible in each stratum. The total number counted was always within 10O/oand usually within 50/0 of the initial number added to the jar. Because of the similarities in structure, algal concentration, and lighting among the controls and predator treatments, I assumed that errors due to counting were the same for the various treatments. I counted the Daphnia in a jar as quickly as possible to reduce the chance of counting rapidly swimming animals more than once: it took about 30 s to count one jar. The average depth of the Daphnia population was calculated using the number per stratum and associating al[ individuals in a stratum with its middepth. Experiments were done only during the day, with natural (north) sunlight and room lights, at about 11,000 lux. Experiments never received direct sunlight. The temperature was 21 C. Food concentration in these experiments was adjusted to mg wet wt liter 1, using ce 11counts and cell volume, as described by Dodson and Havel (1988). Food consisted of a mix of green algae (Dodson and Havel 1988). Food concentration was monitored because lower food concentrations in the range of 2-3 mg liter-1 resulted in no predator response or ambiguous responses in preliminary trials done before these eight clones were tested (Dodson and Have] 1 988). Behavioral observations were made on eight clcmes: Daphnia ambigua clone AW 1 (Lake Wingra, Dane Co., Wisconsin, 7 May 1985), Daphnia galeata mendotae clone DGA (Lake Monona, Dane Co., 9 March 1985), i!laphnia obtusa clone G5A (Utah Rock Pool No. GSA, Grand Co., Utah, 29 October 1986), Daphnia parwla clone TO 1 (Lake Tlexoma, Kingfisher Co., Oklahoma), Daphniu pzde.x clone SBL (a-gardner Pond, Univ. o:f Wisconsin Arboretum, Dane Co., 1 2June 1983), Daphnia pulicaria clone PM 1 (Big Muskie Lake, Wlas Co., Wisconsin, 26 July 1986), Daphnia retrocwva clone R 1 (Lake Waubesa, Dane Co., 15 June 198-5), D. retrocurva clone R3 (La kemendota, Dane Co., 15 September 1986). There were two kinds of experiments. In the first, predators were enclosed in mesh bags, so that test animals outside the bag were exposed to the presence of the predator, but there was no possibility of actual feeding on the test Daphnia. The purpose was to expose the Daphnia to predators to assay for behavioral changes, measured as changes in vertical distribution in a standardized environment. In the second kind of experiment, water from predator cultures was used as the predator treatment. These water-transfer experiments were designed to test two hypotheses: that the cue is a chemical dissolved in water, and that the effect clf the chemical would disappear over time. Vertical distributions in control and predator-treatment jars were observed over several hours. Enclosure experiments were done with

3 Daphnia and chemical stimuli 1433 each of the eight clones, using three controls and three predator jars. A 200-ml volume, 93-~m mesh, nylon bag was put at the top of each jar, in part of the top stratum. The predator treatment was, for each bag, either one macrochirus (bluegill sunfish -2.5 cm long), or two adult undulata (backswimmers), or four americanus (fourth instar larvae of the phantom midge). Control jars had a bag but no predator. Depending on the clone, from 80 to 200 Daphnia were placed outside the bag as test animals. These animals were counted out from a large-bulb pipette, so the number added to each jar within an experiment on a clone was similar. Numbers added per jar varied more between experiments, depending on the number available at the setup. Another 50 Daphnia were put inside the bag (including the controls) to serve as food for the predator. Predators were kept in the bags and fed once a day for the duration of the experiment. Observations on the animals outside the bag began the day after the experiment was set up. The order of control andpredator-treatment jars was arranged by someone other than the observer, so that the observer did not know which jars contained predators. The contents were stirred 2 h before and after each observation. Two observations were made, at least 2 h aparton the firstday, and another the next day. For each of the three predators in separate experiments, the average depths of Daphnia in the three control and three predator-treatment jars, for the three times of observation, were analyzed with a twoway ANOVA (Sokal and Rohlf 1981). The F-ratio, for each predator separately, had df of 1 and 12 (two predator treatments, three times, and two df for the three averages per treatment and time). Water-transfer experiments were done in the same jars with the same food concentrations and counting techniques, except that bags were not used, and only D. ambigua clone AW 1 and D. pzdex SBL were tested. Six jars were set up the first day with Daphnia from a large culture. The second day, the cladocerans were counted in the jars 1-3 times over a period of + 1 h. Then, 600 ml of water was siphoned from each jar. I added 600 ml of water from a well-fed predator culture to three jars for the predator & Number o fo f4 18 Control.80 Chooborus Fig. 1. Average vertical distributions of Daphnia pzdex observed at 1100 hours on 9 January 1986 (third set of observations on the six jars). Predators were enclosed in bags; the controls had bags but no. The bars for each stratum indicate 1 SE of the mean with three replicates. Arrows indicate mean depths. treatment. Predatorswere fed the same clone as was being tested. Controls received 600 ml of day-old water from the predator culture, since preliminary observations showed that the predator response persisted for <12 h (see also results of the water- tran~fer experiments below). The predator or control water was stirred thoroughly into the jars. Observations were then made approximately hourly for * 8 h or until no response was evident for several sequential observations. These data were analyzed with a single classification model I ANOVA, comparing the paired average population depths in control and predator treatments at each time. These are orthogonal planned comparisons (Sokal and Rohlf 1981). The F-ratio used in the ANOVA had df of 1 and 16 for D. ambigua and 1 and 56 for D. pulex. Results The difference in average depth due to (Fig. 1) is representative of the subtle but consistent and statistically significant predator effects in these behavioral experiments. For each predator treatment in each experiment, I counted the Daphnia

4 1434 Dodson Table 1. Induced response: the relative vertical position of Daphrzia clones exposed to enclosed predators. Maximal depth was 20 cm. Each depth difference (cm) given below is the overall average difference between the control and predator treatment depths ofthree trials, each trial coreposed ofthree control and three predatortreatment replicates. A posjitive number indicates that the predator-treatment populations were at a greater depth than the control populations. For each of the three predators, the vertical distribution of Daphnia in the three trials was analyzed with a two-way ANOVA (Sokal and -Rohlf 1981).Signjficance levc]s arc given for the predator Ireatment effect I -ratio (all = 1,12). (Symbols: ns not significant; *** P < ). = Daphia (species and clone) Predator. Lepornis Notonecfa D. galeata mendotae DGA 2.00*** 1.81*** 1.88*** D. pulex SBL 3.03*** 7.22*** 7.66*** D. pulicaria PM *** 2.29*** 3.26*** D. ambigua AWI 0.20 ns 2.68*** 3.04*** D. retrocurva R ns 3.74*** 3.18*** D. retrocurva R ns *** 5.25*** D. obtusa G5A 0.01 ns 0.58 ns 0.50*** D. parvula TO ns. 2.27*** 0.33 ns. irt each. jar three times, with observations separated by at least 2 h. The two average depths seen in Fig. 1 (10.41 and 7.80 cm) for D. pulex SBL exposed to represent the average of one set of observations on three control and three jars replicate observations, giving a difference in depth of 2.61 cm. The average depths for the other two replicate experiments were and 3.36 cm to give the overall average of 3.03 listed in Table 1. For no entry in Table 1, did two-way ANOVA give evidence of time effects or interactions between predator treatment and time. An F~.X test for homogeneity of the variance in average ciepths failed to reject the hypothesis of homoscedasticity. Therefore,.1 felt justified 10 use average depths of each of the three replicates to calculate the overall average depth differences shown in Table 1. Fifteen of the 17 statistically significant responses listed in Table 1 are responses in which the Daphnia moved from the middle of the jars toward the top or bottom of the jars (became more highly clumped). In two of the cases (DGA with and R 1 with Lepornis), the cladocerans moved toward the middle of the jar (became more evenly distributed) in response to the predator. The data in Fig. 1 are representative of the behavioral responses seen in -these experiments. The difference in depth of 2.61 cm is statistically significant and near the median (2. 89 cm) of the absolute values of the significant differences shown in Table 1. Also, the cladocerans moved from a more even distribution to a concentration at one end of the jar, as in the majority of the responses, I present only one pair of graphs since the full data set comprises 144 graphs. Each of the eight clones responded to at least one predator (Table 1). Depending on the Daphnia clone and predator, the response was to rise or sink. Differences in the magnitude of response were not tested for significance, since I have no way of knowing if the stimulus intensity was the same in the various predator treatments. The results of the water-transfer experiments (Figs. 2 and 3) are entirely consistent with those of the enclosure experiments. The clones show statistically significant responses to the same predators and in the same directions. In addition, a second addition of or water produced the same response in D. pzdex as the first addition. The single classification AN- OVAS for pairs of control and predatortreatment averages (Figs. 2 and 3) use the within-observation variance from the entire water-transfer experiment for each particular predator. Daphnia clones generally show responses to the ~predatorswith which they co-occur. (Table 2). The correlation coefficient for lake size vs. number of responses (Table 3) is 0.54 (P > 0.05, df = 6). There is a statistically significant correlation coefficient of 0.73 (P <

5 Daphnia and chemieal stimuli 1435 I a. ocontrol predator *** 5 6 I* ***** 1P 6 a. 7 I I 0 control predator ~ T ;;~ ; - b ***** * ** 9 - ~!0 1 I , 1 I 1245 ; 6 - *******++** *** s CL7 -c II # I 1 1,,, # I Time (hours) Fig. 2. Vertical response over time of Daphnia pu- Iex clone SBL to,, and ivotonecta in 4-liter jars, 20 cm deep. The cladocerans were exposed to 600 ml of fresh or aged (control) water from predator cultures. The vertical lines at time zero and at about hour 5 (top two graphs) indicate times of addition of predator or control water. Each point represents the average depth of Daphnia in three jars. Aslerisks P <0.05 for the F-ratio of a single classification ANOVA. 0.05, df = 6) for the number of vertical responses shown by a clone and the clone s characteristic size (average body length of the primiparous instar). Discussion All eight clones, representingseven species of Daphnia, showed a statistically significant vertical response to at least one predator species. The consistency within the enclosure experiments (leading to high values of statistical significance), between the enclosure and water-transfer experiments, and between the two clones of D. retrocurva, suggeststhat these vertical responses are repeatable and represent real responses to the presence of predators. The tendency of the clones to move to the top or bottom of the jars in response to predators suggests responses are directional, rather than an increase in uniformity, which might be caused ;= b. * * * * 1115 I 1 I I 1 J 7rc. I * ** * io- IIt J -i o Time (hours) Fig. 3. As.Fig. 2, but of Daphnia ambigua clone AW1. Vertical lines at time zero indicate addition of predator or control water. by an increase in nondirectional swimming activity. Several generalizations are possible from these experiments. First, all eight clones show at least one behavioral response to a predator. Second, Daphnia responds to by rising. Third, larger species tend to sink in the presence of and, while the smaller species tend to rise (cf. Tables 1 and 3). Fourth, some Daphnia can distinguish two different predator stimuli, rising for one predator and sinking for another (Table 1), and among them, these Daphnia species have the capability of distinguishing all three predators. Fifth, the enclosure experiments show that Daphnia does not become habituated to the predator, even after 2 d. Finally, the water-transfer experiments suggest that the stimulus is probably a chemical, that the response does not depend on a chemical gradient, and that the stimulus disappears after 3-7 h. Are these vertical response patterns consistent with what is known of the biology of the predator and prey species? There is a strong tendency for a clone to show a ver-

6 1436 Dodson Table 2. A comparison of the predators to which Daphrzia clones react with a vertical response, and the predators with which they co-occur. (? The predator is scarce or occurs in the littoral zone only.). 12aphnia (species and clone) Reacts 10 Co-occurs with D. gal. mendotae DGA D. pulex SBL D, pzdicaria.pml D. ambigua AW 1 D. retrocurva R 1 D. retrocurva R3 D. obtusa G5A D. parvu[a TO 1 Nolonecla L.epon-us Notonccta????? Lcpornis? Nolonecta? tical response to a predator if that predator occurs in the lake from which the clone was isolatecl (Table 2). In only two cases did a clone fail to respond to a coexisting predator. In. these exceptions, the predators may not be an important source of mortality. Daphn~a parvzda clone TO 1 fililed to respond to. In Lake Texoma, ivotonecia probably lives in the littoral zone and not in the pelagic zone where D..parvzda is most common (Threlkeld pers. comm.). Daphnia retrocurva clone R3 failed to respond to. In Lake Mendota, has been absent or rare since about Daphnia pulex clone SBL was the only clone to respond to a predator that does not occur in its native pond, although other fish, mud minnows (Umbra lirni) and brook sticklebacks (Eucalia inconstant), do occur. Five clones failed to respond to noncoexisting predators. The correspondence between response and coexisting predator suggests an evolutionary history to the vertical response: a clone responds only to those predators that have been a source of mortality in nature, and not just to predators in general. The direction of the vellical response is consistent with predictions based on the mode of feeding and size selectivity of the predator (Dodson 1974; Zaret 1980). Rising in the presence of makes sense in view of the tendency of to spend daylight hours deep in the lake, even in the sediments, and then to ascend at night. Thus, during the day, Daphnia can find a region o:f fewer by ascending. A refuge from the visual predators Lepowis and can be found in deeper water. This evasion will be especially effective for the larger Daplznia species, whose large body size protects them from size+elective predation by invertebrate predators, such as and Leptodora, that hide in the deeper vvaters. Smaller Daphnia species are protected somewhat from. visual predators by their small sizes. By rising, they can avoid tactile predators without significant danger from visual predators. Gil-bet-t (1980) and Lively (1986) predicted that induced morphological defenses would be in response to specific predators. The Daphnia in this study showed preyspecific and predator-specific behaviors (Table l). There is evidence that there are Table 3. A comparison of lake size and the number.of behavioral responses shown by Daphnia. Daphnia size is given as the average body length of primiparous females grown in the absence of predators. Daphia Behavioral responses I.,ake Species and clone Size (mm) Lake area (m ) (No,) Giirdner pulex SBL I X103 3 Muskie pulicaria PM C)X1(Y 3 Monona galeala mendotae DGA X107 3 Rock obfusa G5A x101 1 Mendota retrocurva R X107 2 Waubesa retrocurva R x10C 2 Wingra ambigua AW I 1.03 I.3X106 2 Tcxorna parvula TO x 10s 1.

7 Daphnia and chemical stimuli 1437 potentially three separate cues, one for each predator in this survey. That is, several of the clones rose for and sank for and. Daphnia ambig-ua and D. obtusa, however, moved in opposite directions for vs.. Taken together, these observations suggest that Daphnia can distinguish among the three different predators. If only the pelagic zone is considered, then a large lake will in general have more predators of all kinds, compared to a small lake (Browne 1981). Since largerlakes have more predators, is there a tendency for Daphnia from larger lakes to respond to more predators thandaphnia from small lakes? In this present survey of Daphnia, the number of vertical responses shows the opposite tendency: aninverse relation with lake size (Table 3), but without statistical significance. Thus, simple lake size may not be important in determining the behavioral repertoire of Daphnia. Specifically, in the present survey, it was not true that the larger lakes were more likely to have all three predators. A better test of the lake-size hypothesis would be an assay of an array of Daphnia, all the same size, from lakes of the same productivity but with different numbers of predators. In any case, it appears that Daphnia shows induced behavior in lakes of a wide range of sizes. Larger clones tend to show responses to all three predators, while the smallest clones respond to only one or two of the predators (Table 3). The literature suggests two possible explanations for this relationship. First, large cladocerans are susceptible to the full range of predators: as adults to fish and large invertebrates, and asjuveniles to small invertebrates and small fish; small Daphnia species are eaten by fewer predators, being relatively safe from adult fish (Zaret 1980; O Brien 1987). However, since the smallest species in this study show responses to and not to, I conclude that predator preferences are not the driving force. Second, large cladocerans have greater energy reserves, a lower relative metabolic rate, and survive short-term or intermittent starvation better than smaller cladocerans (Gerritsen 1984); they are therefore more likely to be able to spend energy on a larger variety of behavioral responses. The size of Daphnia occurring in a lake depends largely on the kinds of predators present (Zaret 1980) and has little or nothing to do with the size of the lake. In this current study, it is not possible to separatethe effects of sizespecific predation and size-specific metabolic advantages on the number of responses shown by clones of different body size. In the water-transfer experiments (Figs. 2 and 3), two clones responded to water from predator cultures as if the actual predators were present (Table 1). The cue is therefore probably chemical. These results are consistent with studies reviewed by Havel (1987) which report evidence that chemical stimuli induce morphological responses. Predator water was mixed throughout the jars of the water-transferexperiments. Thus, the chemical cue acted even when agradient was absent. Response to a nondirectional chemical stimulus seems adaptive, in that directional gradientsarc unlikely to be found in the turbulent upper waters of lakes and ponds. Daphnia expressed a consistent predatorresponse over 2 d in the enclosure experiments. In none of the enclosure trials was there significant temporal variation. I assume that the constant presence of the predators in the enclosures meant the stimulus was constantly produced. Daphnia did not habituate to predators. In a lake, lack of habituation would have the advantage that zooplankton could avoid portions of the lake as long as the predator was present. A significant difference between control and predator treatments usually appeared within 5-30 min (Figs. 2 and 3). Behavior resulting from a single dose of stimulus, however, persisted for 4 6 h. This hysteresis suggests that Daphnia in nature could respond within a few minutes to the appearance of a predator, but could only reoccupy water several hours after an inducing predator left. On the other hand, persistence may be a laboratory artifact, due to unnaturally high concentrations of the chemical stimulus. Once the chemical is characterized, it will be possible to assay for its concentration and measure its kinetics in nature. In

8 1438 Dodson any case, Daphnia in the water-transfer experiments did -tend to return to the same level as the controls, suggesting that, just as in the systems of morphological induction, the behavioral response has some cost that is avoided when predators are absent. Much more work needs to be done on Dap/znia physiology to demonstrate that there actually is a cost to induced vertical migration. There would seem to be strong selection against predators that advertise their presence. Perhaps once some of the chemical stimuli are characterized, we will understand why predators can t avoid inducing defenses in their prey. What evidence is there that these induced vertical responses happen in nature? Nonrandom distribution patterns and diel vertical. and horizontal migrations of zooplankton are usually interpreted as evolved antipredator defenses. These behaviors are assumed to be cued by predictable environmental factors, especially light level. For example, a survey of eight Tatra lakes showed that Cyclops abyssorum migrates only in lakes with predatory fish and most strongly when the copepod has lived with the fish for centuries (Gliwicz 1986). The occurrence of the strongest migration patterns with the longest coexistence is used as evidence of a long-term process of natural selection. Similarly, studies of horizontal migration have tended to use the model of an evolved behavior cued by physical factors (Johnsen and Jakobsen 1987). An evolved response to predation, cued by physical factors, does not rule out behavioral responses to chemical cues produced by the predators themselves. Eviclencc is accumulating that predator-avoidance behavior affects vertical migration and horizontal distribution patterns. A recent field cxperimen.t with enclosures 10 m deep in a Michigan lake provided evidence that D. galeata (mendotae) and D. pulicaria tended to sink in the presence of (Leibold unpubl. data). Luecke (1 986) found that adding trout to Lake Lenore (Washington) enhanced vertical migration of C haoborus. He concluded that trout predation was responsible for the change in migratory patterns, but pointed out the rapid response (over -=6 yr) might indicate intense selection against nonmigrating forms. Ifthe also had an inducible predator avoidance behavior, then strong selection is not required to explain the rapid. change. Dorazio et al. (1987) found that Daphnia in Lake Michigan showed an increase in die] vertical migration between 1983 and 1985, when predation intensity was probably increasing. Again, this is a relatively fast response, requiring strong selection or a combination of selection and induced behavioral response. These examples are suggestive, but it is important that experiments be designed with the.specific goal of testing for predator-induced avoidance behavior in nature. Lampert ( 1987) and Johnsen and Jakobsen ( 198 7) argued that zoo plankton will migrate t.oi~voidfish predation only if the zooplankton are well enough fed. Stitch and Lampert (1981) demonstrated a definite metabolic cost to vertica lmigration. Induction experiments of Dodson (1988) and Dodson and Havel (1988) showed that the morphological responses of smaller body size in D. pulex and elongated helmets and tailspirws in D. galeata mendotae and D. retrocurva are most pronounced at higher food levels. Thus, I would add to Gilbert s (1980) hypothesis the generalization that zooplankton. will show predator defenses, whether morphological or behavioral, only when thley are not food limited. Finally, it seems appropriate to ask whether induced responses have community-wide effects. The studies reviewed by Havel (1987) make a strong case for the ecological importance to the prey species of inducecl responses. Effects of induction on community structure and species diversity are as yet unknown. Diel vertical migration of herbivorous zooplankton provides a pathway bywhich predators of zooplankton can indirectly modify phytoplankton production (Lampert 1987) and can cause a net downward flux of phosphorus in stratified lakes (Dini et al. 1987). Thus, evidence is emerging that induction might have effects beyond. individual prey species. References BROWNE,,R. A Lakes as islands: Biogeographic distribution, turnover rates, and species compo-

9 ~a~lmia and chemical stimuli 1439 sition in the lakes of central New York. J. Biogeogr. 8: DINI, M. L., ANDOTHERS Daphnia size structure, vertical migration, and phosphorus redistribution. Hydrobiologia 150: DODSON,S. I Adaptive change in plankton morphology in response to size-selective predation: A new hypothesis of cyclomorphosis. Limnol. Oceanogr. 19: Cyclomorphosis in Daphnia galeata mendotae Birge and D. retrocurva Forbes as a predator-induced response. Freshwater Biol. 19: , ANDJ. E. HAVEL Indirect prey effects: Some morphological and life history responses of Daphnia pulex exposed to undulata. Limnol. Oceanogr. 33: DORAZIO,R. M., J. A. BOWERS,ANDJ. T. LEHMAN Food web manipulation influences grazer control of ph ytoplankton growth rates in Lake Michigan. J. Plankton Res. 9: GERRITSEN,J Size efficiency reconsidered: A general foraging model for free-swimming aquatic animals. Am. Nat. 123: GILBERT,J. J Further observations on developmental polymorphism and its evolution in the rotifer Brachionus calycijlorus. Freshwater Bi01. 10: GLIWICZ,M. J Predation and the evolution of vertical migration in zooplankton. Nature 320: GRANT,J. W. G., ANDI. A. E. BAYLY Predator induction of crests in morphs of the Daphnia carinata King complex. Limnol. Oceanogr. 26: HAVEL,J. E Predator-induced defenses: A review, p In W. C. Kerfoot and A. Sih [eds.], Predation: Direct and indirect impacts on aquatic communities. Ncw England. ANDS. I. DODSON Reproductive costs of -induced polymorphism in Daphnia pulex. Hydrobiologia 150: HUTCHINSON,G. E A treatise on limnology. V. 2. Wiley. JOHNSENG. H., ANDP. J. JAKOBSEN The effect of food limitation on vertical migration in Daphnia longispina. Limnol. Oceanogr. 32: KFRFOOT,W. C Combat between predatory copepods and their prey: Cyclops, Epischura, and Bosmina. Limnol. Oceanogr. 23: Translocation experiments: Bosmina re;ponses to cyclopoid predation. Ecology 68: LAMPERT,W Vertical migration of freshwater zooplankton: Indirect effects of vertebrate predators on algal communities, p In W. C. Kerfoot and A. Sih [eds.], Predation: Direct and indirect impacts on aquatic communities. New England. LIVELY,C. M Canalization versus developmental conversion in a spatially variable environment. Am. Nat. 128: LUECKE,C A change in the pattern of vertical migration of j7avicans after the introduction of trout. J. Plankton Res. 8: O BRIEN,W. J Planktivory by freshwater fish, p In W. C. Kerfoot and A. Sih [eds.], Predation: Direct and indirect impacts on aquatic communities. New England. SIH, A Antipredator responses and the perception ofdangcr by mosquito larvae. Ecology 67: SOKAL,R. R., ANDF. J. ROHLF Biometry, 2nd ed. Freeman. STEMBERGER, R. S., ANDJ. J. GILBERT Defenses of planktonic roti fers against predators, p In W. C. Kerfoot and A. Sih [eds.], Predation: Direct and indirect impacts on aquatic communities. New England. STENSON,J. A. E Variation in capsule size of Holopedium gibberum (Zaddach): A response to invertebrate predation. Ecology 68: STITCH,H. B., ANDW. LAMPERT Predator evasion as an explanation of diurnal vertical migration by zooplankton. Nature 293: ZARET,T. M Predation and freshwater communities. Yale. Submitted: 17 November 1987 Accepted: 8 February 1988 Revised: 15 August 1988