Predator-induced alterations in Daphnia morphology

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1 Journal of Plankton Research Vol 13 no.6 pp , 1991 Predator-induced alterations in Daphnia morphology Steven S.Schwartz Department of Biology, Berry College, Mount Berry Station, Rome, GA 3149, USA Abstract. The freshwater cladocerans Daphnia pulex and Daphnia schodleri protect themselves from predation by morphological alterations induced in response to water-soluble chemicals released by their respective predators. Daphnia pulex is induced by larvae of the phantom midge, Chaoborus. Populations of D.pulex which are induced are those most likely to have intense interaction with the predator. This is true both on a broad geographic scale as well as locally Cephalic expansion in D.schodlen is induced by notonectids, in particular Buenoa sp. This predator prefers larger prey and consequently small instars of D.schodlen show no evidence of induction Both examples of predatorinduced alterations suggest that this type of response is costly to the prey and is manifested only in those individuals and populations most threatened Introduction Species cope with their environments through adaptations, genetically based morphological, physiological or behavioral modifications that increase fitness. Natural selection is often invoked when we ask why a species has acquired one set of adaptations instead of others (Williams, 1966). Alternative explanations, e.g. genetic drift or history, can ultimately be related back to natural selection. Because natural selection influences an organism's fitness, it is not unsurprising that cost:benefit ratios govern the evolution of adaptations. Costs come from two constraints. First, species must overcome constraints imposed by the physical environment. Second, species must overcome constraints based on the phylogeny of the organism. Previous adaptations have considerable influence on the evolution of new adaptations. A reduction in immediate reproductive effort is the cost of adaptations, while the benefit is accrued through long-term gains in fitness. It is these gains in fitness that are the final measure of success of an adaptation. Life in the plankton places Unique constraints on adaptations. This is because planktonic life by definition necessitates remaining in the water column. Thus being planktonic requires some combination of adaptations including low density, a shape that resists sinking (high surface to volume ratio), buoyancy devices, buoyant metabolic by-products and minimal swimming ability. If an organism is to remain planktonic this prerequisite cannot be circumvented. That is, all other adaptations are constrained by these prerequisite adaptations. Consequently, the evolution of anti-predator defense adaptations must be accomplished in the context of constraints of living in the plankton. Planktonic prey deter predation through behavioral, physiological or morphological adaptations. Behaviorally, prey may avoid predators by vertical migration (Stich and Lampert, 1981; Ohman et al., 1983) or avoiding areas with predators (Pennak, 1973; Dorgelo and Heykoop, 1985). Physiologically, they may avoid predators by masking their presence with chemicals (Schwartz and Downloaded from at Penn State University (Paterno Lib) on May 1, 216 Oxford University Press 1151

2 S.S.Schwarti Hebert, 1989) or by producing chemicals that make them distasteful (Kerfoot, 1982; Schwartz et al., 1983). Morphologically, adaptations increase handling time by making the prey item unwieldy or tough (Dodson, 1984), or by increasing the evasiveness of the prey (Barry and Bayly, 1985). The use of a particular predator deterrent is often constrained by the physical nature of the environment and the cost of the adaptation. For example, zooplanktonic species inhabiting shallow ponds cannot vertically migrate to avoid predators. Morphological adaptations are energetically expensive but particularly successful in deterring predation. Morphological adaptations have two sources of energetic costs. There is the high energetic cost of growing the feature (Kerfoot, 1977) and the additional energetic cost to stay planktonic. The high cost of morphological adaptations determines the distribution of some species. Daphnia middendorffiana, for example, has a suite of morphological features (large size of neonates, long tail spine and dorsal hump) that deter predation in arctic ponds, but make it a poor competitor with other Daphnia species (Hebert and Loaring, 198; Dodson, 1984). Predator-balanced polymorphisms also entail high costs. Two morphs of a species, one 'plain' and one exuberant, coexist because the exuberant morph has reduced fecundity but increased survivorship in the face of predation (Zaret, 1972). A strategy to hold down the cost of predator deterrence is the evolution of temporary, induced morphological alterations (Adler and Harvell, 199; Harvell, 199). Such alterations occur only in the presence of a particular predator. Inducible species have the advantage of using a 'normal' proportion of energy for reproduction in the absence of predators. In the presence of predators, many species of freshwater Protozoa, Rotifera and Cladocera have induced morphs that reduce predation rates (Havel, 1987; Jacobs, 1987). Inducible taxa typically have short generation times (2-1 days); they quickly respond to predators by producing offspring with altered morphologies. In addition, rotifers and cladocerans molt every h, giving adults the opportunity to alter their morphologies as well. Predator-induced alterations were first described in the rotifer Brachionus calyciflorus (Beauchamp, 1952a,b). Gilbert (1967) found that long spines deterred predators. He also established that these spines were induced in response to a substance produced by the predator (Gilbert and Wage, 1967; Gilbert and Thompson, 1968). The study of predator-induced morphological alteration in the Cladocera stems from work on Daphnia pulex (Krueger and Dodson, 1981) and D.cephalata (Grant and Bayly, 1981). These species show marked change in morphology in the presence of their invertebrate predators, Chaoborus and notonectids respectively. Chaoborus releases a water-soluble chemical that serves as a semiochemical signal to D.pulex (Krueger and Dodson, 1981; Parejko and Dodson, 199), Daphnia ambigua (Hebert and Grewe, 1985; Hanazato, 199) and Daphnia cucullata (Tollrian, 199). Responses to predators among the species in the nominate subgenus include reduced size (Dodson and Havel, 1988), dorsal teeth (Krueger and Dodson, 1981) and cephalic spines (Hebert and Grewe, 1985; Tollrian, 199). Immature D.pulex produce dorsal Downloaded from at Penn State University (Paterno Lib) on May 1,

3 Induced morphologies in Daphnia teeth, termed Nachenzahne, in the presence of larvae of the midge Chaoborus (Krueger and Dodson, 1981). As the animals grow and reach a size where they are no longer prey for Chaoborus the Nachenzahne are resorbed. The trade-off for protection by induction comes from increased time to maturity and smaller size at maturity (Havel and Dodson, 1987; Vuorinen et al., 1989; Walls and Ketola, 1989). Nachenzahne are also common in immature instars of Daphnia rosea (Brooks, 1957) and Daphnia longispina (Lilljeborg, 19). At present there is no evidence that Nachenzahne in these species are induced by predators, but this may well be the case. Nachenzahne were also an identifying characteristic of Daphnia minnihaha (Herrick, 1884; Richard, 1896) before the species was synonymized with D.pulex (Brooks, 1957). A distinguishing feature of this species is the retention of Nachenzahne in adults (P.D.N.Hebert, R.D.Ward and S.S.Schwartz, in preparation). By contrast, induced defenses in the subgenus Ctenodaphnia consists of a dorsal crest. Grant and Bayly (1981) showed that induction of the crest occurs in the presence of notonectids. Induced animals are at an advantage in evading predators (Grant and Bayly, 1981; Barry and Bayly, 1985) rather than having increased handling time by the predator. Induction of the crest, however, results in significantly reduced fecundity (Barry and Bayly, 1985). Additional research is required to determine if other species with cephalic expansion, e.g. longicephala and magniceps (Hebert, 1977), are also induced. In this paper, I investigate induced defenses as adaptations to predation. Because these defenses are manifested only in the presence of predators, they must have a substantial cost. Based on this assumption, it is possible to formulate a number of hypotheses regarding induction. First, populations facing a significant threat from a specific predator are most likely to be inducible. Second, within a population induction should occur in those individuals most susceptible to predation. These hypotheses reinforce the importance of understanding the feeding ecology of the predator in trying to understand the defenses of the prey. Method Daphnia are excellent experimental organisms because it is possible to work with clones of parthenogenetically reproducing organisms. This eliminates genotype as a source of error when analyzing data. Experiments with D.pulex The first hypothesis that there is a relationship between the inductive ability of D.pulex and the long-term presence of Chaoborus was tested by comparing induction in a number of Daphnia clones between habitats. The production of Nachenzahne is typical of D.pulex populations in southern Ontario. A single experiment determined three points regarding induction among populations. This experiment surveyed the degree of clonal variation in induction of Nachenzahne in clones from the area of Windsor, Ontario. The same experiment also tested the degree of geographic variation between clones along 1153 Downloaded from at Penn State University (Paterno Lib) on May 1, 216

4 S.S.Schwartz a latitudinal gradient. Finally, this experiment established the degree of sensitivity to induction of a species closely related to D.pulex and a species inductive to other predators. This test of the relationship between prey and predator included 2 clones of D.pulex in the presence of larvae of Chaoborus americanus. Table I lists the place of origin of each clone. The clones from the Windsor, Ontario area are electrophoretically distinct (Hebert and Crease, 198; Hebert etal., 1989) as are all other clones. The specificity of induction within the genus Daphnia was tested by including two additional species: D.obtusa, a relative within the D.pulex group of species (Schwartz et al., 1985; Innes et a/., 1986), and D.cephalata which is induced by notonectids in nature (Grant and Bayly, 1981) and the laboratory (Barry and Bayly, 1985; S.S.Schwartz, personal observation). Ten gravid female D.pulex were placed in a 12 ml plastic cup with a mesh bottom. This cup was suspended in a 5 ml beaker containing 25 Chaoborus larvae and a number of D.pulex as prey. Earlier trials showed that starved Chaoborus did not elicit the induction of Nachenzahne. The experiments were conducted in synthetic pond water (Hebert and Crease, 198), in constant room light, at 25 C. Neonates were removed daily. After 4 days, 5 neonates from each cup were scored at a magnification of x 1 for the degree of induction of Table I. The degree to which 21 clones of Daphnia are induced to form Nachenzahne in the presence of Chaoborus larvae Species D.pulex D.cephalata D.obtusa Origin Windsor, Ontario Santee, CA Churchill, Manitoba Inuvik, NWT Old Crow, NWT Tuktoyaktuk, NWT New South Wales Lincoln, NE Clone Induction score* Downloaded from at Penn State University (Paterno Lib) on May 1, 216 * = no induction; 1 = single small tooth; 2 = well-developed single tooth, 3 = highly developed with multiple teeth. 'x' indicates the maximum degree of induction observed in 5 neonates. 1154

5 Induced morphologies In Daphnia Nachenzahne. Scores ranged from for no induction to 3 for the presence of a large, highly developed Nachenzahne bearing multiple teeth. The extent of variation of induction was examined within and between two local clones (Windsor 1 and 12). One hundred eggs of each clone were stripped from gravid females. These eggs were placed in a 12 ml mesh bottom cup suspended in a beaker with 825 ml synthetic pond water. To this beaker 25 Chaoborus larvae were added along with sufficient Daphnia to serve as food. Hatched individuals were counted and examined for development of Nachenzahne for 3 days. The experiment was conducted in duplicate. beakers contained Daphnia eggs but no Chaoborus larvae. Experiments with Daphnia schodleri The second hypothesis that induction should occur in those individuals most susceptible to predation was explored using D.schodlen and its notonectid predator, Buenoa sp. This Daphnia species is unique in the nominate subgenus as the only species which grows a cephalic crest in response to notonectids. In this regard it is similar to the Ctenodaphnia. It occurs in seasonal ponds in Texas and Oklahoma. In addition, feeding trials determined the feeding preference of the notonectid predator, Buenoa sp. and demonstrated the relationship between predator-feeding ecology and crest induction. All experiments were conducted in synthetic pond water using a single clone of D.schodleri collected in the area of Houston, T. The first experiment determined the degree to which notonectids induce crest formation in D.schodlen. Ten gravid females were placed in a 12 ml mesh bottom cup suspended in a 5 ml beaker. The beaker contained 1 notonectids along with sufficient Daphnia to serve as food for the predators. The notonectids were fed daily. A control beaker contained all but the notonectids. Daphnia in the cups were examined after 4 weeks. Length was measured from the top of the head to the base of the tail spine. Head width was measured as the width immediately below the eye. Data from this experiment were analyzed by an analysis of covariance (ANCOVA) on untransformed values. The second set of experiments determined the feeding preference of the predator. Can notonectids feed on any size D.schodleri and is there a preference? All experiments were conducted at 2 C in constant light. Prior to use in the feeding trials all notonectids were fed ad libitum on Daphnia for 24 h and then starved for 24 h. The initial experiment consisted of one notonectid held with 15 D.schodlen from one of five size classes. Size classes ranged from a mean of mm with a range of individual size from.74 to 2.5 mm. The experiments were conducted in a 5 ml beaker and lasted 3 h. Based on the results of the first feeding trials, a second experiment consisted of 1 large (mean size 1.9 mm) and 1 small (mean size.8 mm) D.schodleri along with a single notonectid in a 5 ml beaker for 1 h. There were 15 replicates. Data from this experiment were analyzed by a paired Mest on untransformed values. A final experiment consisted of five large (mean size 1.6 mm) along with 15 small (mean size 1155 Downloaded from at Penn State University (Paterno Lib) on May 1, 216

6 S.S.Schwartz.7 mm) in a 5 ml beaker along with a single notonectid for 1 h. There were 23 replicates. Data from this experiment were analyzed with an analysis of variance (ANOVA) on values transformed by arcsine Vx. Results Among the three species, induction was specific to D.pulex (Table I). Neonates of D.cephalata and D.obtusa failed to produce Nachenzahne. Not all clones of D.pulex were equally inducible. Many clones from the Windsor area produced class two or three Nachenzahne. Clones from the most northerly site, Tuktoyaktuk, produced small or no teeth. Clones from the other subarctic sites Churchill, Inuvik and Old Crow had limited induction by the predator. An interesting result was that clones from the same immediate vicinity had variable induction. Of the Windsor clones, seven produced well-developed Nachenzahne. However, individuals of clone 1 from two different sites produced no more than a single, small tooth. Table II includes the results of the experiment testing the extent of the variation of induction between clones 1 and 12. Clone 12 produced more, larger toothed individuals than did clone 1. Development of more elaborate Nachenzahne took ~2 days but few (4%) clone 1 neonates scored as high as a 2, while >6% of clone 12 neonates developed elaborate Nachenzahne. None of the control animals developed Nachenzahne. The results of the D.schodleri experiments show that cephalic expansion in this daphniid is induced by the presence of the predacious notonectid Buenoa sp. Head width increased faster in D.schodlen grown in the presence of notonectids (Figure 1) compared with control animals (ANCOVA testing for differences of homogeneity of slopes F = 38.96, P <.1). The difference between treatment and control groups was clear in those animals larger than ~1.5 mm. Animals smaller than this were indistinguishable. Table n. Mean number of neonates from 1 eggs induced to produce Nachenzahne in the presence of Chaoborus larvae Day done Treatment Eggs hatched Induction score Downloaded from at Penn State University (Paterno Lib) on May 1, 216 Neonates were examined daily for 3 days after hatch. Induction classes same as in Table I 1156

7 Induced morphologies in Daphnia The feeding trials showed the close relationship between predator-feeding ecology and prey-defensive adaptations. The feeding experiments showed first that notonectids can successfully feed on D.schodleri of all sizes (Table III). However, there was a clear preference for larger prey as the survivorship declined quickly with increasing size. The results of the second feeding experiment with equal numbers of the two size classes revealed a significant difference in survivorship between large and small animals (Student's Mest for matched groups = 8.273, d.f. = 22, P <.1). The mean percent survivorship for large animals was only 2. ± 16.2 compared with 71.3 ± 22.6 for the small animals. The preference for larger prey was further emphasized by the final feeding experiment. Even though small prey were three times more abundant than large prey the percent survivorship of small animals (63.8%, untransformed) was significantly greater than that of large animals (32.%, untransformed) (ANCOVA on arcsine Vx transformed data, F = 19.71, P <.1). a -d 1.5 -i 1. :.5 - co Length (mm) 3. Fig. 1. Head width as a function of body length for D.schodlen Squares represent individuals grown in the absence of the notonectid predator Buenoa sp (slope = solid line); stars represent individuals grown in the presence of the predator (slope = dashed line) Table m. Mean percent survivorship per hour of 15 uninduced D.schodlen from each of five size classes in the presence of one notonectid for 3 h Downloaded from at Penn State University (Paterno Lib) on May 1, 216 Mean length (mm) Mean percent survivorship

8 S.S.Schwartz Discussion Although the experiments reported here are from two different sets of predatorprey pairs, there is a common theme to the results. The prey species in each group have defenses finely tuned to their particular predator and the feeding ecology of that predator. There are three interesting results from the Chaoborus-D.pulex set of experiments. First, among the tested species, induction is specific to D.pulex. Neonates of neither D.cephalata nor D.obtusa were induced to produce Nachenzahne. This indicates that induction of D.cephalata is specific to notonectids and is not a general response to all predators. Barry and Bayly (1985) similarly found that only notonectids, and no other potential predator, induced cephalic crests in D.cephalata. Chaoborus are known from Australia, the source for the animals used in this experiment. However, they must not represent the same degree of threat as do notonectids. That D.obtusa does not induce is indicative of it also living in habitats where Chaoborus is a limited threat. Further research will determine the degree to which species are inducible in the pulex group of species. Another interesting result was that Nachenzahne induction was most commonly observed in clones from sites likely to have high Chaoborus densities. Thus, many clones from the Windsor area produced large and multiple-toothed Nachenzahne. Clones from the most northerly site, Tuktoyaktuk, where Chaoborus is absent, produced no or small teeth. Clones from other subarctic sites (Churchill, Inuvik and Old Crow), all from ponds with limited densities of Chaoborus, had variable induction. All but Inuvik clone 23 had some degree of induction. The third result was that clones from the same immediate vicinity did not induce to the same degree. At Windsor, seven clones produced category 3 Nachenzahne, but individuals of clone 1 from two different sites had only category 1 induction. Other clones from the area developed as many as four teeth in the shape of a rosette. In comparison to the other clones, clone 1 inhabits a particularly small habitat, ~2 by 1 m. This pond dries annually and does not have Chaoborus in appreciable numbers. The other habitats are significantly larger, rarely dry, and support large populations of Chaoborus. Again, the conclusion is that clones which live in the absence of Chaoborus are unable to express the defensive adaptation, while clones facing the predator can protect themselves. The difference in induction in hatched eggs between clones 1 and 12 further emphasized this point. Initially clone 12 has more neonates not induced than clone 1 but this situation quickly changed. Clone 1 neonates and young individuals failed, with but rare exception, to be induced beyond a minimal degree. By contrast, most clone 12 neonates achieved some degree of induction by day three. Again, the explanation may lie in the lack of Chaoborus in the source pond of clone 1. The distribution of clones in the Windsor area may thus be partially determined by the distribution of the predator. This is a situation analogous to that of Daphnia species in the arctic (Hebert and Loaring, 198). Downloaded from at Penn State University (Paterno Lib) on May 1,

9 Induced morphologies in Daphnia The results of the D.schodleri experiments are the first evidence that cephalic expansion in this species is the result of induction by notonectids. Animals similar in shape to those illustrated in plate 22, figure B of Brooks (1957) are common in ponds with high notonectid density in the area of Houston. This shape is similar to that of the species of the subgenus Ctenodaphnia which are also induced by notonectids. It is therefore likely that this is the optimal configuration for deterring predation by notonectids. The evolution of induced cephalic expansion was probably independent in the two subgenera. All age classes are inducible in the Ctenodaphnia (Barry and Bayly, 1985; S.S.Schwartz, personal observation) but only larger individuals of D.schodleri were induced. This difference in induction in D.schodleri can be understood in light of the feeding ecology of the notonectid predator, Buenoa. This predator is capable of feeding on Daphnia of all sizes as the preliminary feeding experiment indicated. However, given equal numbers of large and small prey, Buenoa prefers the larger prey items. Even when three times as many small as large prey were present Buenoa took larger individuals in greater proportion than small individuals. Australian notonectids apparently do not have the same feeding ecology and readily feed on all size-class individuals (Barry and Bayly, 1985; S.S.Schwartz, personal observation). This explains why small individuals of D.schodleri, in the presence of the predators, are indistinghishable from uninduced animals. Large individuals, the preferred prey of Buenoa, are induced to grow a significantly wider head. The results of these experiments are in accord with the hypotheses tested. Firstly, those populations of Daphnia which have faced a particular predator over evolutionary time are most likely to have evolved a defense against that predator. Secondly, only those individuals that are threatened respond to the predator. Thus large individuals of D.pulex and small individuals of D.schodleri are morphologically identical to uninduced individuals of their respective species. Both results support the idea that morphological defensive adaptations among zooplanktonic organisms are energetically expensive. These results also support the conclusion of Hanazato (199) that D.ambigua adults retain their induced cephalic spine because they are within the size range of food for Chaoborus throughout their lives. The conditions favoring the evolution of inducible defenses may require prey species living in highly competitive environments and faced with efficient seasonal predators. In such an instance, prey species are perhaps best served by a defensive strategy that is expressed only when it is needed. Understanding the evolution of particular defenses requires detailed knowledge of the feeding ecology of the predator. Differences in the shape of the morph and the size classes involved can only be understood with such knowledge. Downloaded from at Penn State University (Paterno Lib) on May 1, 216 Acknowledgements I am grateful for the encouragement, comments and criticisms of P.D.N.Hebert, S.I.Dodson and J.H.Graham. This research was supported by a grant from the University of Houston Coastal Center. Additional assistance came from a 1159

10 S.S.Schwartz Natural Sciences and Engineering Research Council (Canada) grant to P.D.N.H. References Adler.F R and Harvell.C.D. (199) Indudblc defenses, phenotypic variability and biotic environments. Trends Ecol Evol., 5, Barry,M.J. and Bayly,I A E. (1985) Further studies on predator induction of crests in Australian Daphnia and the effects of crests on predation Aust. J Mar. Freshwater Res., 36, Beauchamp.P. (1952a) Un facteur de la variability chez les rouferes du genre Brachwnus. C. R Soc. Bioi, 234, Beauchamp.P. (1952b) Variation chez les rotiferes du genre Brachwnus. C. R., 235, Brooks.J L. (1957) The systematics of North Amencan Daphnia. Mem Conn. Acad. Arts Set., 13, Dodson.S.I (1984) Predation of Heterocope sepuntrionalts on two species of Daphnia: morphological defenses and their cost. Ecology, 65, Dodson.S.I. and HavelJ.E. (1988). Indirect prey effects: some morphological and life history responses of Daphnia pulex exposed to Notonecta undulata. Umnol. Oceanogr., 33, DorgeloJ. and Heykoop (1985) Avoidance of macrophytes by Daphnia longispma. Verh Internal. Verein Limnol., 22, Gilbert.J J (1967) Asplanchna and postero-lateral spine production in Brachwnus calyaflorus Arch. Hydrobwl., 64, Gilbert^ J. and Thompson,G. A,Jr (1968) Alpha-tocopherol control of sexuality and polymorphism in the rotifer Asplanchna. Science, 159, Gilbert^.J. and Waage.J K. (1967) Asplanchna, Asplanchna-substznce. and posterolateral spine length variation of the rotifer Brachionus calyaflorus in a natural environment. Ecology, 48, Grant^I.W.G. and Bayly,1.A.E. (1981) Predator induction of crests in morphs of the Daphnia carinata King complex Limnol. Oceanogr., 26, Hanazato.T. (199) Induction of helmet development by a Chaoborus factor in Daphnia ambigua during juvenile stages. /. Plankton Res., 12, Harvell.C D. (199) The ecology and evolution of inducible defenses. Q. Rev Bioi, 65, HavelJ.E. (1987) Predator-induced defenses: a review. In Kerfoot.W.C. and Sih.A. (eds), Predatwn: Direct and Indirect Impacts on Aquatic Communities. University Press of New England, Hanover, pp HavelJ.E. and Dodson.S.I. (1987) Reproductive costs of Owohoruj-induced polymorphism in Daphnia pulex Hydrobiologia, 15, Hebert,P D N. (1977) A revision of the taxonomy of the genus Daphnia (Crustacea. Daphnidae) in southeastern Australia. Aust. J. Zool, 25, Hebert.P D N. and Crease,T J (198) Clonal coexistence in Daphnia pulex- another planktomc paradox. Science, 27, Hebert.P.D.N. and Grewe.P.M (1985) Chaoborus induced shifts in the morphology of Daphnia ambigua. Limnol Oceanogr, 3, Hebert.P D.N. and Loaring.J.M (198) Selective predation and the species composition of arctic ponds. Can. J. Zool., 58, Hebert.P D.N., Beaton.M.J., Schwartz.S.S and Stanton.D.J. (1989) Polyphyletic origins of asexuality in Daphnia pilex. I Breeding system variation and levels of clonal diversity. Evolution, 43, Hernck,C.L. (1884) A final report on the Crustacea of Minnesota included in the orders Cladocera and Copepoda. Geol. Nat Hist. Survey Minn. 12th annual report, pp Innes.D J., Schwartz.S.S. and Hebert.P.D.N (1986) Genotypic diversity and variation in mode of reproduction among populations in the Daphnia pulex group Heredity, 57, Jacobs^J. (1987) Cyclomorphosis in Daphnia In Peters,R H. and de Bemardi.R. (eds), Daphnia Mem. 1st. Ital. Idrobiol., 45, Kerfoot.W C. (1977) Competition in dadoceran communities: the cost of evolving defenses against copepod predation. Ecology, 58, Kerfoot.W.C (1982) A question of taste: crypsis and warning coloration in freshwater zooplankton communities. Ecology, 63, Kruger.D A. and Dodson.S.I. (1981) Embryological induction and predation ecology in Daphnia pulex Limnol. Oceanogr., 26, Downloaded from at Penn State University (Paterno Lib) on May 1, 216

11 Induced morphologies in Daphnia Lilljeborg.W. (19) Cladocera Sueciae Kongd. GcsiU Wiss, Uppsala Ohrnan.M D., Frost,B W. and Cohen.E.B (1983) Reverse diel migration an escape from invertebrate predators. Science, 22, Parejko.K. and Dodson.S (199) Progress towards characterization of a predator/prey kairomone: Daphnia pulex and Chaoborus amencanus. Hydrobiologia, 198, Pennak.R. (1973) Some evidence for aquatic macrophytes as repellants for limnetic species of Daphnia. Int. Rev. Ges. Hydrobwl., 58, Richard,J. (1896) Revision des dadoceres Deuxieme partie. Ann Sci. Nat., Bot Biol Veg, 8th Ser, 2, Schwartz.S.S. and Hebert.P.D.N. (1989) The effect of Hydra on the outcome of competition between Daphnia and Simocephalus Biol. Bull, 176, Schwartz.S.S., Hann.B.J. and Hebert.P D.N (1983) The feeding ecology of Hydra and possible implications in the structuring of pond zooplankton communities. Biol. Bull, 164, Schwartz,S.S., Innes.D.J. and Hebert.P.D.N (1985) Morphological separation of Daphnia pulex and Daphnia obtusa in North America. Limnol Oceanogr., 3, Stich.H. and Lampert.W. (1981) Predator evasion as an explanation of diumal vertical migration by zooplankton. Nature, 293, Tollrian.R. (199) Predator-induced helmet formation in Daphnia cucullata (Sars). Aivh Hydrobiol., 119, Vuorinen.I, Ketola.M. and Walls.M (1989) Defensive spine formation in Daphnia pulex Leydig and induction by Chaoborus crystalhnus De Geer. Limnol. Oceanogr., 34, Walls,M. and Ketola.M. (1989) Effects of predator-induced spines on individual fitness in Daphnia pulex Limnol. Oceanogr, 34, Williams,G.C. (1966) Adaptation and Natural Selection. Princeton University Press, Princeton, NJ. Zaret.T M. (1972) Predators, invisible prey, and the nature of polymorphism in the Cladocera Limnol Oceanogr., 17, Received on July 24, 199; accepted on March 27, 1991 Downloaded from at Penn State University (Paterno Lib) on May 1,