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Reference: Biol. Bull. 176:147—154. (April, 1989) The Effect of Hydra on the Outcome of Competition Between Daphnia and Simocephalus STEVEN S. SCHWARTZ AND PAUL D. N. HEBERT Department ofBiological Sciences, University of Windsor, Windsor, Ontario, Canada N9B 3P4 Abstract. The cladoceran genera Daphnia and Simo cephalus often co-occur in nature. In laboratory experi ments, populations ofthe two genera had similar growth rates when grown separately, but when cultured together Daphnia invariably excluded Simocephalus. However, the added presence of the littoral zone predator, Hydra, reversed this trend with Simocephalus remaining after Daphnia had been eliminated. This result was robust in culture vessels as small as 100 ml and as large as 85 1.It is hypothesized that Simocephalus has evolved a suite of energetically expensive traits to deter littoral zone preda tors, whereas Daphnia, which are pbanktonic, have not evolved such costly traits and hence have more energy available for reproduction and are able to exclude Simo cephalus. 1978; O'Brien and Vinyard, 1978; Cooper and Smith, 1982). When predator pressure is low, the susceptible morph is able to numerically dominate the protected morph. While the maintenance of distinct morphs is striking, predation has also been a significant selective force in the evolution of previously overlooked charac teristics which not only reduce predation rates, but which also effect interactions between prey species. Schwartz et al. (1983) demonstrated that Hydra are efficient predators ofthe cbadoceran Daphnia, but rarely capture members ofthe closely related genus, Simoceph alus, which inhabit the littoral zone along with Hydra. Simocephalus has a suite ofcharacteristics that deter pre dation by Hydra. The evolutionary origin of each trait is unknown, but may be, in part, the result of selective pressure by Hydra or other littoral zone predators. The behavior of Simocephalus is such that it spends most of the time attached to substrates and is therefore not in the water column where it might encounter the tentacles of Hydra. In addition, physiological adaptations allow Si mocephalus to swim among the tentacles ofHydra with out eliciting the discharge of nematocysts. Finally, when nematocysts are discharged, Simocephalus is unharmed, suggesting that the nematocysts fail to penetrate this cla doceran's heavy carapace. In contrast, Daphnia, which is pbanktonic, is highly vulnerable to predation by Hydra. One explanation for the vulnerability ofDaphnia is that, because Daphnia rarely encounters Hydra, it has failed to evolve mechanisms that reduce the impact ofthe pred ator. Is there a cost to Simocephalus associated with its suite of anti-predator adaptations? Competition experiments between Daphnia and Simocephalus have invariably shown that Daphnia outcompetes its relative (Frank, Introduction Over evolutionary time prey species have limited the impact of predation by behavioral, physiological, and morphological adaptations (Sih, 1987). The conse quences of these adaptations are not restricted to the predator-prey relationship, but may also be important in other facets ofthe ecology ofthe prey species. For exam pbe, morphological features of many planktonic cladoc erans not only deter predation, but also effect competi tive interactions. Predator-resistant morphs of Bosmina and Ceriodaphnia are competitively inferior to predator susceptible morphs (Nibssen et al., 1980; Zaret, l972a; b). The maintenance ofsuch morphological diversity has been termed predator balanced polymorphism (Zaret, 1969). The energetic cost ofpredator deterrence is appar ently reflected in reduced fecundity and consequently re duced competitive ability (Kerfoot, 1975, 1977; Jacobs, Received l7July 1987;accepted3Oianuary 1989. 1952; Corigliano and de Bernardi, 1978; de Bernardi 147 This content downloaded from 078.047.027.170 on October 13, 2016 12:56:56 PM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). and 148 S. S. SCHWARTZ AND P. D. N. HEBERT Manca, 1981; 1982; Crowley and Johnson, 1983). In general, these studies indicate that Simocephalus has a lower intrinsic rate of increase than Daphnia and this rate is additionally reduced by the presence of the com petitor. The results of these competition experiments have been explained by proximate differences in life his tory characteristics, without attempting to examine the ultimate factors that have selected these suites of traits. The robeofpredation has, for instance, been neglected in explanations ofthe relative position ofthe two genera in a competitive hierarchy. In this paper we show that the outcome of laboratory competition experiments between Daphnia and Simo cephalus can be altered by the presence ofa predator that consistently selects the prey species that has not been ex posed to selective pressures favoring the evolution of ap propriate defensive tactics. We suggest that the reduced competitive ability of Simocephalus as compared to Daphnia is largely the result of energetically expensive anti-predator adaptations required for life in the littoral zone. Materials and Methods The effect of Hydra oligactis predation on the out come ofcompetition between Daphnia pulex and Simo cephalus vetulus, two commonly co-occurring cladocer ans, was evaluated in three sets of laboratory experi ments. Both cladoceran species and the Hydra were cbonal populations (Daphnia pulex clone Wi-i) main tamed in the laboratory and originally collected in the Windsor, Ontario, area. Experiments were initiated in synthetic pond water (Hebert and Crease, 1980), but this was gradually replaced during the experiments with con ditioned tap water containing algal food. All experiments were conducted at 15°C and 12:12 LD. During the exper iments the cladocerans were fed at two-day intervals with a mixed algal culture, primarily Scenedesmus sp., main tamed in the laboratory. No attempt was made to quan tify the feeding regime as all experiments were conducted concurrently; i.e., all vessels in an experiment received the same amount and quality offood. As control popula tions showed a rapid numerical increase (Figs. 1, 4), it was assumed that the feeding regime was adequate. The first two experiments were similar in design, differing primarily in the size of the vessel used. In one set ofexperiments, 120 ml plastic cups were filled to 100 ml. Each treatment was replicated in triplicate. Oviger ous females were used to initiate each replicate cup. Con trol cups received six individuals from one of the two cladoceran species. Competition cups were initiated with three individuals from each species. Additional competi tion cups were also set up with six D. pulex and three S. vetulus to determine if Daphnia would more quickly outcompete Simocephalus under these conditions. The impact of a selective predator, Hydra, was determined in another set of competition cups (initiated with three females from each species) as well as control cups (with six individuals of each species), with each cup receiving one adult Hydra, without buds. All individuals were counted in each cup once a week for five weeks. The impact ofcontainer size was examined in a second set of experiments conducted in 200-mb finger bowls. The experimental design was similar to the first except that the treatments with six Daphnia and three Simo cephalus and the individual species with Hydra were eliminated. All treatments were run in triplicate. Again, all individuals in each finger bowl were enumerated weekly during the seven week duration of the experi ment. Data were analyzed using an analysis of variance which took into account the experimental design of three factors (experiment, species, and weeks) with repeated measures on only one of the factors (weeks) (Winer, 1962). The large differences between initial and final population size from each of the preceding experiments necessitated the use of bog (x + 1) transformed data for statistical analysis. The experiment initiated with twice as many Daphnia as Simocephalus was not included in this analysis. A final competition experiment was conducted in 1001aquaria filled with 85 1of synthetic pond water. There were two control and two treatment aquaria. All aquaria were initiated with 20 individuals each of D. pulex and S. vetulus. In addition, the experimental aquaria also re ceived a single Hydra. The aquaria were checked at two day intervals and maintained at 85 1with the same algal mixture used in the other experiments. This experiment was allowed to run for six weeks at which time the con tents ofthe aquaria were filtered through a plankton net and preserved in ethanol. Due to the large number of individuals present in the aquaria at this time, the mdi viduals from three subsamples were sorted to species, counted, and then dried at 80°Cfor 24 h and weighed. The remainder of each sample was then dried and weighed in the same manner and the total number of individuals belonging to each species estimated on the basis ofits abundance in the original subsamples. Results The results of the small cup and finger bowl experi ments were similar, differing primarily in their final pop ulation size. The finger bowls supported about 50% more individuals of both cbadoceran species (compare Figs. 1 and 4). The rapid numerical increase in all vessels mdi This content downloaded from 078.047.027.170 on October 13, 2016 12:56:56 PM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). 149 IMPACT OF PREDATION ON COMPETITION 160 140 C') -J 0 > 0 z 120 I00 80 60 40 WEEKS 3 WEEKS Figure 1. The mean population sizeofDaphnia pu/ex(circles)and Simocephaius vetulus (squares) when grown separately in 100 ml cups during a 5-week period. Bars represent ±2S.E. Figure 2. The mean population size of Daphnia pulex (darkened circles) and Simocephalus vetulus (darkened squares) when grown to gether in 100 ml cups during a 5-week period. Open squares represent cates the adequacy of the feeding regime. Visual inspec the mean total cladoceran population in the cups. Bars represent ±2 S.E. tion ofthe untransformed data (Figs. 1, 2, 4, 5) suggested that the growth of all test populations could be divided into two distinct phases. A period of rapid, linear, popu lation growth was followed by a period during which the populations leveled off, apparently having reached their “¿carrying capacity.―The initial phase lasted three weeks in the cups and four weeks in the finger bowls. The analysis ofvariance (Tables I, II) indicated that in both sets ofexperiments there was a significant difference between the population size in the control and experi mental vessels. This may be due to the fact that the tra jectory of total population growth was slower in the ex Table! ANOVAfor the 100-micup set of experiments perimental vessels (compare Figs. 1, 2 and 3, 4). How ever, the combined carrying capacity in all of the competition vessels was greater than the population in the control vessels, which may indicate that the two spe cies utilized slightly different food resources. There was a significant difference in population size between the species only in the bowls (Table II). Thus, in the bowls at least, there were significantly fewer Simo cephalus than Daphnia in the experimental vessels than Table!! ANOVAfor bowlexperimentsSourcedfSSMSFBetween 200-mifinger Sourcedf55MSFBetween cups91.49A l**B(species)10.160.164.36AB10.050.051.47Error60.220.04Within .061 .0628.9 (experiment)11 bowls102.93A (experiments)I2.242.2460.980*B (species)10.260.266.97*AB10.180.184.88Error70.260.04Within bowls7720.79C(weeks)619.613.27400.94*0AC60.040.010.86BC60.940.1619.140*ABC60.000 cups5014.15C(weeks)511.942.3935.16**AC50.020.000.06BC50.060.010.20ABC50. 100.020.28Error302.040.07 This content downloaded from 078.047.027.170 on October 13, 2016 12:56:56 PM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). 150 S. S. SCHWARTZ AND P. D. N. HEBERT 180 160 140 0) -J 120 :@ a I00 > a z 80 60 40 20 I 4 23 WEEKS 5 three weeks. Simocephalus achieved almost 40% of the densities observed in the control population in the cups until the fifth week when Hydra, which had been unable to reproduce due to the bow densities of suitable prey, died. Simocephalus then rapidly increased to 76% of the size of the control populations. Similarly, in the finger bowls, Simocephalus reached 82% of densities in the control by the end ofthe seventh week (Fig. 4). Similar results were observed in the aquarium study indicating that the outcome was robust over a range of container size (Fig. 6). In the aquaria lacking predators, Daphnia outnumbered Simocephalus individuals al though the two aquaria differed in degree of dominance, the ratio being 1.4: 1 in one aquarium and 7. 1:1 in the other. By contrast, all Daphnia individuals were ebimi nated in the aquaria with Hydra. Because only one Hy dra was used to initiate the experiment, Daphnia popuba tions expanded before the Hydra reproduced sufficiently to make a significant impact on their density. However, the large Daphnia population then served as food for the rapidly increasing predator population. Bytheendofsix weeks, all Daphnia individuals had been eliminated leav Figure 3. The mean population size ofDaphnia pulex(circles) and Simocephalusvetulus(squares)from an initial population containing twice as many individuals of Daphnia as Simocephalus. The animals were grown in lOO-mlcups for a 5-week period. Barsrepresent±2S.E. 200 180 in the control vessels. In both sets of experiments there 160 was a significant difference associated with time, i.e., not surprisingly the populations were significantly larger at the end ofthe observations than at the beginning. The only interaction term found to be significant was the species by vessel interaction in the bowl experiments, i.e., the species were changing in a different manner U) -J through time. Most likely the Daphnia a population grew faster in the experimental bowls than the Simocephalus population through a suppression of the batter by either exploitative or interference competition. Competitive replacement did not occur in any of the competition vessels, including the cups initiated with six Daphnia and three Simocephalus (Fig. 3). After only two weeks, Daphnia made up more than 90% ofthese popu lations. By the end of five weeks, Simocephalus popula tions had decreased to less than 5% ofthe Daphnia popu lation. Dc Bernardi and Manca (1982) similarly found that competitive replacement is a slow process with Si mocephalus populations persisting at low densities over a long period. Those vessels which were initiated with Hydra in addi tion to the cladocerans all showed the same pattern: Daphnia individuals were eliminated in 97% ofthe yes sels within the first week and, in all cases, by the end of @I20 I00 @80 60 40 20 I Figure 4. 234567 WEEKS The mean population size ofDaphnia pu!ex(circles) and Simocephalusvetulus(squares)whengrown separatelyin 200-mi finger bowls during a 7-week period. The mean population size ofS. vetulus in the presence of Hydra is indicated by triangles. Bars represent ±2 SE. This content downloaded from 078.047.027.170 on October 13, 2016 12:56:56 PM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). 151 IMPACT OF PREDATION ON COMPETITION limit the impact of predation. The cost of these adapta tions is, in part, responsible for the differing competitive ability ofthe two genera. Simocephalus is a genus that occupies the littoral zone where many of the predators employ ambush tactics (Greene, 1985). Faced with such predators one success ful prey strategy is to avoid ambush by not swimming. Consequently, the sedentary behavior of Simocephalus can be viewed as a means of avoiding predation. Simo cephalus makes use of glands on the dorsal portion of the carapace which allow it to attach to substrates and continue filter feeding. This behavioral adaptation frees Simocephalus ofcertain constraints on morphology; i.e., the cost of developing a more robust exoskeleton is de rived solely from costs of producing the structure, whereas planktonic cladocerans incur additional costs associated with increased weight. 200 180 160 Cl) -J 140 :@120 a ?l00 a @80 60 40 Physiological 20 I 234567 WEEKS Figure 5. The mean population size ofDaphnia pu!ex(circles) and Simocephalusvetulus(squares)when grown togetherin 200-mi finger bowls during a 7-week period. Open squares represent the total cladoc eran population. Bars represent ±2SE. adaptations similar to that which allows Simocephalus not to elicit the firing of coelenterate ne matocysts have evolved many times in the Crustacea. Cyprid larvae of the barnacle Ba/anus crenatus do not elicit the discharge of nematocysts nor the mouth open ing response of Obelia dichotoma (Standing, 1976) al though larvae that are damaged are consumed. Numer ous copepod genera live in association with sea anemo nes (Gotto, 1979; Humes, 1982). A well-studied example Daphnia ing an average of 9625 Simocephalus and 853 Hydra. There were many more Simocephalus in the experimen tab aquaria than total cladocerans Simocephalus in the control aquaria. Discussion It has often been demonstrated that predators may de termine the outcome of competition between two prey species (Kerfoot, 1975, 1977; Jacobs, 1978; O'Brien and Vinyard, 1978; Cooper and Smith, 1982). In the present study the rapidity of the predators' effect de pended on container size and was observed within a few days or at most a few weeks. As observed in previous studies, Daphnia outcompeted Simocephalus in the ab sence of predators. This latter result is in part due to Si mocepha/us reducing its reproductive rate in the pres ence ofDaphnia, but ofgreater importance is the higher intrinsic reproductive rate of Daphnia. However, in the presence of predators the outcome of competition was determined by the evolutionary interaction between Si mocephalus and these predators. Daphnia and Simo cephalus have faced different predation regimes over ev obutionary time and have responded to these differing se bective pressures with unique suites of adaptations to v) 4 > 6000 ID w 4000 2000 0 Figure 6. A comparison of the cladoceran populations in 100-1 aquaria after 6 weeks. The two pairs of columns on the left represent the two control aquaria and the other two pair represent aquaria to which Hydra were also added. This content downloaded from 078.047.027.170 on October 13, 2016 12:56:56 PM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). S. S. SCHWARTZ AND P. D. N. HEBERT 152 is Paranthessius anemoniae, which moves freely over the tentacles ofAnemonia sulcata (Briggs, 1976). However, free-living copepod species are paralyzed and consumed. In addition, an extract ofthe anemone's tentacles caused paralysis among the free-living copepods but not in P. anemoniae. Similar results have been reported for the li chomolgid cope@, Doridicola, which lives on a num ber of species of anemones and does not elicit the firing of nematocysts (Lonning and Vader, 1984). There are also amphipods which are associated with sea anemones that are immune to its host's toxins (Vader and Lonning, 1973). The immunity to coelenterate nematocysts has also been suggested to be important in determining the out come of competition between two hermit crab genera, Pagurus and Clibanarius (Wright, 1973). The former ge nus is able to occupy shells to which hydroids are at tached, while the latter genus is stung and therefore can not inhabit these shells. Thus the adaptations of Simo cephalus are similar to those found in a number of other crustaceans. A likely explanation is that Simocephalus has evolved biochemical products that mask its presence, as the first step in the firing of nematocysts by Hydra is chemosensory (Lenhoff, 1968). Once this mask is breached, Hydra readily consumes Simocephalus (Schwartz et a!., 1983). The energetic cost ofsuch an ad aptation has not been determined, but is most likely small in comparison with the benefits. In contrast to Simocephalus, Daphnia is unable to evolve adaptations to predators that would compromise its success in the open water environment. Behaviorally, Daphnia actively avoids macrophytes (Pennak, 1973; Dorgebo and Heykoop, 1985), which are obvious indica tors of the littoral zone and the suite of predators that lurk within. By avoiding the littoral zone Daphnia ne gates the need for adaptations necessary to deter those predators. In addition to being sensitive to Hydra preda tion, Daphnia has been shown to be more easily captured than Simocephalus by damseifly naiads (Akre and John son, 1979; Johnson and Crowley, 1980) and the rhabdo cod flatworm Mesostoma lingua (Schwartz and Hebert, 1986), most probably because it is constantly swimming while Simocephalus is sedentary. Members ofthe genus Daphnia have evolved a variety ofmorphobogical adaptations whose function can be ex plained as predator deterrence. In general, these adapta tions consist of cuticular extensions to the head, tail spine, and fornices, as opposed to cuticubar thickening which would increase weight and lead to major increases in basal metabolic rates. Morphological adaptations take two forms—those that have evolved as permanent struc tures and those that are produced in the presence of par ticular predators. Dodson (1984) documented the costs of the permanent adaptations of D. middendorffiana to predation by the copepod Heterocope septentrionalis. He suggested that these adaptations result in a lower repro ductive rate of D. middendorfJlana compared to that of its competitor, D. pulex. The cost to D. pulex is its elimi nation from those habitats containing the copepod, while D. middendorJJiana is limited to living with its predator rather than its competitor. The other class of morphological anti-predator adap tations ofDaphnia are temporary features cued by chem icals produced by particular predators, a phenomenon recently termed chemomorphosis (Hebert and Grewe, 1985). Predators known to cause these effects are larvae ofthe phantom midge Chaoborus(Krueger and Dodson, 198 1; Hebert and Grewe, 1985) and notonectids (Grant and Bayly, 198 1; Barry and Bayly, 1985). The value of these morphological alterations in reducing predation has been demonstrated (Krueger and Dodson, 1982; Ha vel and Dodson, 1985), but Dodson (1984) has shown that even small cuticular extensions such as nachen zahnen reduce the intrinisic rate of increase. Daphnia and Simocephalus have faced unique sebec tive pressures for adaptations deterring predation from the predators they most frequently encounter. An impor tant consequence of these adaptations involves the co occurence ofthese cladocerans. The two species often co occur in ponds that are large enough to support both lit torab and pelagic zones (Anderson, 1974; pers. obs.). Ponds backing either of these habitats are typically nu merically dominated by one ofthe genera. Habitats lack ing ambush predators (rock pools for example) are domi nated by Daphnia as Simocephalus are excluded (Gan ning, 197 1; Ranta, 1979), most probably by continued competitive pressure. As observed in the aquaria study, Simocephalus can produce considerable populations in the absence of competitors but has smaller populations when co-occurring with Daphnia. These reduced popu lations may be due to both exploitative competition and antagonism between the two genera. Inhibitory sub stances have been proposed to be important in zooplank ton species interactions (Frank, 1952; Seitz, 1984). At the other habitat extreme, those ponds with a high density of macrophytic growth and the associated inver tebrate predators often back Daphnia but contain barge populations of Simocephalus (pers. obs.). Species distri bution is made more complex by the fact that Daphnia becomes a browser when pbanktonic food resources are limited (Mitchell and Williams, 1982). At such times Daphnia is particularly vulnerable to littoral and benthic predators. Therefore, the distribution of the two species is regulated by a surface area:volume ratio that takes into account not only morphometric contributions to surface area but also that due to macrophytes. This content downloaded from 078.047.027.170 on October 13, 2016 12:56:56 PM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). IMPACT OF PREDATION ON COMPETITION In conclusion, we have demonstrated in laboratory ex periments that the outcome of competition between Daphnia and Simocephalus is regulated by the presence ofHydra. The broad range ofmorphobogical and behav ioral adaptations to predation place Simocephalus at a competitive disadvantage. The divergence oflife history characteristics between the species may be partially a product of competitive interactions. Daphnia, which faces a different suite of predators, may have evolved a unique assortment ofadaptations constrained by the ne cessity ofmaintaining itselfin the plankton. Acknowledgments This research was supported by a grant from the Natu rab Sciences and Engineering Research Council to P.D.N.H. Comments by anonymous reviewers im proved this manuscript as well as the comments of G. Cameron and L. Weider on early drafts. All are appreci ated. Literature Cited Akre, B. G., and D. M. Johnson. 1979. Switching and sigmoid func tional response curves by damselfly naiads with alternative prey available. J. Anim. Ecol. 48: 703—720. Anderson, R. S. 1974. Crustacean plankton communities of340 lakes and ponds in and near the National Parks of the Canadian Rocky Mountains. .1.Fish. Res. BoardCan. 31: 855—869. Barry, M. J., and I. A. E. Bayly. 1985. Further studies on predator induction of crests in Australian Daphnia and the effects of crests on predation.Aust.J. Mar. Freshw.Res.36: 519—535. 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