Cyclomorphosis of Daphnia pulex spined morph9
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1 Limnol. Oceanogr., 30(4), 1985, , by the American Society of Limnology and Oceanography, Inc. Cyclomorphosis of Daphnia pulex spined morph9 John E. Have1 Department of Zoology, University of Wisconsin, Madison Abstract Chaoborus-induced spined phenotypes of Daphnia pulex were present at frequencies >80% in two Wisconsin ponds during summer 1983 but were rare earlier in the year, even though predaceous instars of Chaoborus americanus were common. Laboratory induction experiments with one clone revealed that the proportion of Daphnia juveniles which bore the Chaobonrs-induced spines (% SM) was a positive function of both temperature and Chaoborus density, and C. americanus from different times of year could induce high percentages of spined morphs. For both ponds, clonal descendants of Daphnia isolated during the spring were less sensitive to a standard Chaoborus treatment than descendants of summer Daphnia The results suggest that the changing frequency of spined morphs in the field was due in part to a shift of Daphnia populations, one unresponsive and another responsive to the Chaoborus factor. Phenotypic plasticity to environmental factors may also influence the distribution of morphs in the field. One species of the Daphnia pulex Leydig complex (Brooks 1957; Dodson 1981), Daphnia minnehaha Herrick, is now known to be an inducible form of D. pulex (Krueger and Dodson 198 1). Neonates bearing a toothed dorsal crest not present in their parents are released by gravid parthenogenetic Daphnia in association with Chaoborus americanus. This crest is conspicuous only in the first three instars of D. pulex and first appears shortly after release from the mother. Animals with this crest are here called the spined morph or SM, and those lacking the crest are called the typical morph or TM (Fig. 1). SM is less susceptible to predation by Chaoborus than is TM (Have1 and Dodson 1984), but may have a lower intrinsic rate of increase (Have1 and Dodson in prep.). Daphnia pulex populations in ponds containing Chaoborus (C. americanus) are usually dominated by SM, while only TM is found in locations without Chaoborus (Krueger and Dodson unpubl.), although SM is sometimes absent when Chaoborus is present (Cooper 1979). Seasonal polymorphism in a planktonic species, or cyclomorphosis, has been well studied in Daphnia (Hutchinson 1967). Kerfoot (1980) suggested that there are three proximate causes of cyclomorphosis: phenotypic plasticity, clonal succession, and l Supported by NSF grant DEB 8 l to S. I. Dodson. succession of sibling species. Phenotypic plasticity occurs where single genotypes can produce different phenotypes under different environmental conditions. Phenotypes of Daphnia are plastic. Helmet size in some species, such as Daphnia galeata and Daph- nia retrocurva, can be modified independently by temperature and turbulence (Jacobs 196 1; Have1 and Dodson 1985), and crest size in others, such as the Daphnia carinata complex and D. pulex, can be modified solely by the presence or absence of specific insect predators (Grant and Bayly 1981; Krueger and Dodson 1981). Cyclomorphosis via clonal succession (and sibling species succession) occurs when the relative frequencies of specific genotypes change during a yearly cycle, and these changes are expressed in observable changes in morphology (phenotype). Cyclomorphosis of the cladoceran Bosmina Zongiros- tris is probably due to a succession of clones (Kerfoot 1977, 1980). Long- and short-featured morphs isolated from Lake Washington at different times of year maintained their morphological differences when grown under identical laboratory conditions and differed in electrophoretic phenotypes (Kerfoot 1977; Brock 1980). Seasonal clonal shifts may also influence cyclomorphic patterns in Daphnia. Numerous clones of obligately asexual D. pulex can coexist in ponds (Hebert and Crease 1980) and clones within other Daphnia species differ in responsive- 853
2 854 Have1 lmm Fig. 1. First five instars of Daphnia pulex spined and typical morph s. Spined morphs (top) are characterized by the presence of a dorsal crest during the first three instars. This crest is a developmental response to Chaoborus, ness to temperature and turbulence (Jacobs 196 1; Have1 and Dodson 1985). Using electrophoretic and life history information, Lynch (1983) found that several clonal groups of D. pulex coexisted for a long period in a small pond and that their relative frequencies changed over time, suggesting that the genetic structure of the population was changing during the course of his study. He later reported (Lynch 1984) that one of these groups is another species. I here present observations on the relative abundance of the spined and typical morphs of D. pulex in two Wisconsin ponds over several years and describe experiments testing variation in the Chaoborus induction process th: rough modification of temperature, Chaoborus density and source, and Daphnia clone. The following questions were investigated experimentally. What is the relationship between temperature and Daphnia spine inducibility? Do those Chaoborus co11 ected from ponds during periods of high Sh!: frequency cause induction more readily thzn Chaoborus isolated during periods of lc w SM frequency? Do clones established r rom populations dominated by SM resportd more readily to induction than
3 Cyclomorphosis of D. pulex 855 those established from populations dominated by TM? In others words, are there genetic differences between and changes within populations that influence their susceptibility to induction? I thank D. Krueger for supplying the samples and S. Dodson, A. Hershey, K. Spitze, and two outside reviewers for criticisms of the manuscript. Methods Field samples- Samples were collected during 1982, 1983, and 1984 from two permanent ponds in southern Wisconsin: Arboretum Pond Alpha (Neess 1949) in Madison, and Dead Dog Pond in Columbia County (RlOE, T13N, S27 NWG). The maximum depth of both ponds varied from about 2 m in the spring to 1 m in midsummer. Although vertebrate predators were never observed in either pond, insect predators were abundant. Chaoborus americanus larvae were abundant year round and hemipterans of the Belostomatidae and Notonecta spp., damselfly larvae, and beetle larvae were common during summer. Both ponds had large beds of submerged macrophytes, along with associated herbivores: chironomids, ostracods, Simocephalus, snails, tadpoles, and amphipods. Cyclopoid copepods, frogs, Chydoridae, and water mites were also present in Dead Dog Pond. Alpha Pond is dystrophic, receives water by rainfall and seepage, has a midsummer area of 200 m*, is located in dense deciduous woods, and has an anoxic marl and black ooze bottom. Dead Dog Pond is eutrophic, receives water by rainfall, has an area of about 5,000 m*, a black ooze bottom, and is surrounded by a thin margin of woods with a cornfield and pasture beyond. Zooplankton was collected during midmorning by oblique 3-m tows with a 180- pm mesh plankton net and preserved in 70% ethanol. Twenty haphazardly chosen 2nd or 3rd instar D. pulex (body length, BL = 0.78-l -32 mm) from each sample were examined at 50 x and classed as spined or typical morphs. Spined animals include only those with a distinct dorsal crest, characterized by two or more points projecting from a hump on the neck (Fig. 1). For each date, Chaoborus density was estimated by counting a subsample of one plankton sample and assuming that the entire volume of a cylinder 3 m long and 0.13 m in radius passed through the net. Since the usual procedure in the field was to take one sample, variance estimates could be made for field Chaoborus densities on only one date. Some Chaoborus populations migrate into the sediments (Roth 1968; Bass and Sweet 1984); my samples were taken only from the plankton and may therefore underestimate the true density of Chaoborus in the ponds. Chaoborus in the sample was identified as C. americanus (Saether 1972) and assigned to instar according to head length (Swift and Fedorenko 1975). Water temperature was measured near shore during midmorning on each sampling date with a glass thermometer. Samples from Dead Dog Pond for were supplied by D. Krueger. Laboratory induction experiments- Clones were started from Daphnia isolated on a known date and location. In the standard induction procedure each clone was divided into replicate experimental and control jars by placing 5-10 adults into 1 liter of 80-pm filtered pond water. Experimental jars usually received two well fed, recently collected, 4th instar Chaoborus larvae; controls received no Chaoborus. The cultures were preserved after 2 weeks at 20 C (unless indicated otherwise), during which time the Chaoborus ate Daphnia in the jar. Direct association between Chaoborus and Daphnia was necessary for maximum induction of spined morphs; screened enclosures and chemical extracts (as used by Krueger and Dodson 198 1; Schwartz and Hebert unpubl.) were less successful. Since some midges pupated and emerged during the 2-week period, their density was readjusted every few days in most experiments. To ensure that Daphnia juveniles spent their entire developmental histories under the experimental conditions, I discarded the first two broods of neonates. Twenty 2nd or 3rd instar Daphnia from later broods in each jar were classed as SM or TM. The separate experiments were conducted as follows. In experiment 1, I tested clone DDP (Dead Dog Pond) August 1982 at 20 C with Chaoborus concentrations ranging from 0.5 to 4 liter-l. Except for the 0.5 per liter
4 856 Have1 Table 1. Fielc 1 densities of 3rd and 4th larval instars of Chaoborus, proportions of Daphnia pulex that were spined morphs, and water temperatures for Alpha Pond. Standard t Deviation for Chaoborus density on 29 June 1984 (in p rrentheses) is based on five replicate samples. All sari ples were collected during midmorning with a plank;on net. 8 Jun Ju182 5 Apr May Jun Ju Aug Apr 84 7 Jun Jun 84 Temp ( 0 21? Chaoborus liter- %SM (0.39) 95 loo AP urll M AMJJASON MONTH Fig. 2. Succession of Daphnia pulex morphs in field samples. Depicted are % SM from ponds near Madison, Wisconsin. Chaoborus larvae were present on all dates. The sample from was supplied by D. Krueger. treatment, all concentrations were tested in 1 liter of medium with 5-12 replicate jars for each concentration. Three replicates of the 0.5 per liter treatment were set up, each in 2 liters of medium. With the exception of Chaoborus concentration, the standard induction procedure was followed. In experiment 2, I tested clone DDP August 1982 at several temperatures. Five-eleven replicate jars were incubated at 5, lo, 15, 20, and 25 C with the standard induction procedure. In this experiment emerging midges were not replaced, so densities were typically between 1 and 2 liter-. Experiment 3 tested clone DDP August 1982 with groups of Chaoborus obtained about every month from Alpha Pond. Each month, the freshly gathered midges were fed Daphnia juveniles for 2 days, then introduced to duplicate 4-liter Daphr2ia cultures at a density of 2-3 liter-. Aft zr 2 weeks at 2O C, 2nd instar Daphnia larrae were preserved and examined. Experiment 4 used clones established on each of t: le sampling dates in the standard induction procedure. For each date on which I isolated live Daphnia, one-five replicate cultur,:s, each started with a single field-collected individual, were tested with Chaoborus ;tfter the cultures were established in the laboratory. Although I refer to these cultures as clones, they are not necessarily distinct clones. Some may be identical genotypes because of the clonal structure of some Daphnia populations (Hebert and Crease,980). The statisic of interest for all field samples and experiments is the proportion of juveniles belring a distinct dorsal crest (percentage spired: % SM). All references to population I*esponsiveness or spine inducibility refer, to this population estimate. Statistical inferences are based on Mann- Whitney U-tests and simple linear regression (Snedecor and Cochran 1980). Results Field sam,oles-the % SM of D. pulex in the field followed a distinct seasonal succession during and 1983, with a frequency of zero from March through May and
5 Cyclomorphosis of D. pulex 857 loo- A B 80- f 60- z a cn $ Chuoborus DENSITY I# liter- ) TEMPERATURE ( C) Fig. 3. % SM as a function of Chaoborus density and temperature. The standard induction procedure was used with clone DDP August 1982, varying either density or temperature. The density experiment was run at 20 C; the temperature experiment with l-2 Chaoborus liter-. Error bars show + 1 SE for three-five different jars set up under each condition % during the summer months (Fig. 2). Since the first samples containing Daphnia consisted only of 1st and 2nd instars, this population presumably hatched from ephippia during the spring in both ponds. All juvenile instars of this exephippial generation were TM. During June through September 1982, SM always comprised at least 85% of the D. pulex populations in Alpha Pond (Fig. 2). For all years studied, the D. pulex populations declined abruptly before the end of September. A small population reappeared in Dead Dog Pond during late fall 1983; juveniles in the samples were 100% SM on 27 October and 0% SM on 27 November. Chaoborus in samples collected from March through September 1983 revealed no change in species composition: C. americanus always comprised at least 98% of the Chaoborus in the community. Estimated densities of 3rd and 4th instar Chaoborus during 3 years of sampling ranged from 0.3 to 6.5 liter-l, with a C.V. of 39% on one date (Table 1). During 1983, the temperature of Alpha Pond reached 18 C by the middle of May and exceeded that on all later sampling dates during the summer (Table 1). The temperature in Dead Dog Pond was 8 C on 27 October and 0.5 on 27 November; during 198 1, it averaged 14 C during April and early May, and from late May to August (D. Krueger pers. comm.). Laboratory induction experiments- Chaoborus density influenced the proportion of spined offspring. Spined morphs were recovered from experimental jars only when densities of Chaoborus were 11 per liter, and % SM was higher at higher densities of Chaoborus (Fig. 3A). Spined morphs never developed when Chaoborus was absent. Temperature also influenced the proportion of spined offspring. In experiment 2, low percentages of SM were recovered from experimental jars at 10 and 15 C and high percentages at 20 and 25 C (Fig. 3B). The % SM increased with temperature (? = 64%, 34 df, P < 0.005). Chaoborus isolated during periods of high % SM in Alpha Pond does not appear to be any more effective at inducing Daphnia in
6 858 Have J F M A M J J A S O N DATE OF Chaoborus ISOLATION Fig. 4. % SM as a function of Chaoborus isolation date, using one clone and the standard induction procedure. Chaoborus density was maintained at 2-3 liter-i. The median plus range for each sample date is indicated. the laboratory than midges isolated during periods of low % SM. Chaoborus captured in January through April 1983 induced clone DDP August 1982 at frequencies no lower than Chaoborus captured in June through August 1983 (Fig. 4). Daphnia clones isolated from Alpha Pond during March through early June 1983 did not produce spines in standard laboratory induction trials, while those isolated in August and September did produce spines (Fig. 5A). There is a positive relationship between % SM for laboratory experiments and % SM in field samples taken on the date of clonal isolation (Fig. 5B); i.e. clones isolated during periods of low % SM in the field were not responsive to Chaoborus induction in the lab, but clones isolated during periods of high % SM in the field were highly responsive in the laboratory. The clones isolated from Dead Dog Pond in May and June 1983 were much more responsive in the induction experiments than those isolated from Alpha Pond during the same period (Mann-Whitney U-test P < 0.01). The first clones isolated from Dead Dog Pond (May 1983) were highly responsive in the laboratory, even though field samples from the same date had no SM. Clones isolated on 27 October 1983 were still highly responsive. Discussion The seasonal succession of D. pulex morphs reported here for two Wisconsin ponds is another example of cyclomorphosis or seasonal polymorphism in a planktonic species (Hutchinson 1967). Cooper (1979) observed that SM replaced TM during the summer in yet another pond (BVSP) in southern Wisconsin. Samples from other populations of D. pulex coexisting with Chaoborus should help clarify whether this cyclomorphic pattern is widespread and also whether spined morphs coexist with species other than C. americanus. My experimental results confirm those of Krueger and Dodson (198 1). Third and fourth instar C. americanus larvae induce the typical ntorph of D. pulex to produce spined morph offspring, and these will produce typical morphs if Chaoborus is absent. Similar cone: usions have been reported for other predai or-induction groups in zooplankton conrmunities: AspZanchna-Brachionus (Gilbe , Anisops-D. carinata complex (Grmt and Bayly 198 l), and Tropocyclops-Keratella (Stemberger and Gilbert 1984); presence or absence of the predator was the principal factor determining morphology of the prey. In each of these studies, the inducing factor is probably a water-soluble substance. Chaoborw density proved an important determinant of the % SM in my laboratory experiments; with < 2 Chaoborus liter-, only small proportions of juvenile Daphnia were spined. Because of the experimental design, two lactors could cause an increase in % SM with increased Chaoborus density; increased concentration of the Chaoborus substance ar:d selective predation on TM. Although C..zmericanus larvae eat TM twice as efficiently< as SM (Have1 and Dodson 1984), selec tive predation probably accounted for only a small amount of the vari- ation in the present study. After removal of the first 1 or 2 broods of D. pulex, the next brood of ju\teniles (typically n > 100) was exposed to Chaoborus for at most 3 days. Because preciaceous Chaoborus can eat be-
7 Cyclomorphosis of D. pulex 859 I A AP loo- 80- B AP 60- DDP 1983 loo t DDP 00 MAMJJASON ISOLATION DATE % SPINED IN FIELD Fig. 5. Evidence of clonal succession. A. % SM from standard laboratory induction experiments using different clones. Each point represents a separate clone, the founder of which was isolated on the date indicated. Error bars show +_ 1 SE for experiments using five clones isolated on the same date. B. Time series analysis. The points represent % SM for different clones in laboratory experiments (ordinate) plotted against similar proportions in field samples taken on the dates the clones were isolated (abscissa). tween 3 (Pastorok 1980) and 15 (Spitze 1985) juvenile Daphnia per day, the mortality from predation probably affected the population structure in the jars. However, predation from one additional Chaoborus, even if 100% selective on TM, can only account for a shift of 10% to 20% SM, while the data (Fig. 3A) show a shift of 10% to 65%. Chaoborus density was also an important parameter in the results of Krueger and Dodson (1981) over a range of Chaoborus liter-. The highest % SM in their study was 79%-lower than the proportion reported here (average 89% SM at 4 Chaoborus liter- ). This may have been because in the study of Krueger and Dodson the Chaoborus and experimental Daphnia were separated by a screen mesh, whereas I kept the two species in direct association. Selective predation on TM could increase the proportion of SM, as might better distribution of the inducing substance. These assays of sensitivity to the Chaoborus factor suggest that the inducing substance affects embryonic D. pulex only when it is present above a certain concentration. Such a density threshold may be potentially important, since Chaoborus is frequently found at densities < 1 liter-, especially in larger bodies of water (Fedorenko 1975). I do not know whether those Daphnia hatched from ephippia are sensitive to Chaoborus induction during embryonic development. The exephippial generations in my ponds during 1983 and in BVSP in 1978 (Cooper 1979) were unspined. This may have been due to other factors (such as too
8 860 Navel low a density of Chaoborus) or to insensitivity of ephippia to the Chaoborus factor. Temperature also proved an important determinant of the % SM in the present study; cultures grown at 20 and 25 C produced considerably higher % SM than those grown at cooler temperatures. Grant and Bayly (198 1) also found temperature to influence predator induction in the D. carinata complex: Anisops induced larger crests in several populations at 25 C, but not in most at 10 C. The increased % SM at higher temperatures in my study has several possible explanations. First, Chaoborus feeds at higher rates at warmer temperatures (Fedorenko 197 5) and, since the midges ingest TM more efficiently than SM (Have1 and Dodson 1984), the % SM increases due to selective predation would be higher at warmer temperatures. Second, Chaoborus may release more inducing factor at warmer temperatures. Third, developing D. pulex may be more responsive to a fixed concentration of inducing factor at warmer temperatures. The present data do not allow discrimination between these mechanisms, although calculations such as that for the Chaoborus concentration experiment suggest that the first mechanism accounts for little of the observed variation. Chaoborus may release more inducing factor at warmer temperatures, since it feeds at higher rates (Fedorenko 1975), and metabolic status influences the ability of Chaoborus to induce (Krueger and Dodson 198 l), but it is not clear whether the ambient concentration would be changed since the factor may also decay more rapidly at warmer temperatures. The inducing factor is active for <2 days in filtered pond water at 20 C (pers. obs.). From an evolutionary perspective, a positive effect of temperature on the responsiveness of Daphnia to predator induction should be expected, because Daphnia probably suffers significant mortality to Chaoborus predation only at the higher temperatures (Fedorenko 197 5) and produces spines (and associated structures) at a reproductive cost (Have1 and Dodson in prep.). My results here and those of Grant and Bayly (198 1) are consistent with work on the effects of temperature on induction of helmet growth in other species of Daphnia (see Jacobs 196 1; Have1 and Dodson 1985): increasing te mperature up to 25 C increased the growth c f the helmet relative to that of the rest of the body. The results of my induction experiments suggest that SM will be found in the field only when the density of Chaoborus is near or above 1 liter- and the temperature is near or above 10 C. The field data from Alpha Pond (Table 1) for most dates are consistent ti th this hypothesis, although the high variation in densities of Chaoborus on one date suggests that these are rough estimates; Chaoborus densities are difficult to measure act Jrately, and the vertical migration and patchy distribution of the midges may result in a patchy distribution of the inducing substance. Chaoboru, 3 at all seasons could induce SM in the laboratory. This suggests that qualitative differences in resident Chaoborus populations do not account for the absence of SM in the two ponds during spring Since feeding Chaoborus induce a higher % SM than strrved Chaoborus (Krueger and Dodson 19E l), one would expect that the low densities of prey (hence the poor nutritional status of Chaoborus) could also influence the % S im in the field. Perhaps the varying nutritional status of Chaoborus affects the induction process in the field. The work reported here suggests that a succession ()f inducible and noninducible populations occurred in the ponds during Descendants of TM Daphnia in the field were unresponsive to the Chaoborus treatment in the laboratory, while descen- dants of SM Daphnia were responsive. Seasonal variation in clonal responsiveness to a predator-nduced trait has been shown with the rcltifer Brachionus calyciflorus (Halbach and Jacobs 197 1). The relative length of pc sterolateral spines in B. calyci- Jlorus was srongly correlated #with the field densities of the predaceous rotifer Asplanchna b? tight welli, which increased during the course of summer. In laboratory experiments, clones of B. calyciflorus isolated early in the year produced individuals with shorter Aspianchna-induced spines than did clones isolated later in the year.
9 BASS, D., AND M. H. SWEET Do Chaoborus migrate in temporary pools? Hydrobiologia 108: BROCK, D. A Genetic succession in the cyclomorphosis of Bosmina Zongirostris (Cladocera). Freshwater Biol. 10: BROOKS, J. L The systematics of North American Daphnia. Yale Univ. COOPER, S. D The impact of predation on cladoceran assemblages. Ph.D. thesis, Univ. Wisconsin, Madison. 179 p. DODSON, S. I Morphological variation in Daphnia pulex Leydig (Crustacea: Cladocera) and related species from North America. Hydrobiologia 83: 101-l 14. FEDORENKO, A. Y Feeding characteristics and predation impact of Chaoborus (Diptera, Chaoboridae) larvae in a small lake. Limnol. Oceanogr.20: GILBERT, J. J Rotifer ecology and embryological induction. Science 151: GRANT, J. W., AND I. A. BAYLY Predator induction of crests in morphs of the Daphnia carinata King complex. Limnol. Oceanogr. 26: 20 l HALBACH, U., AND J. JACOBS Seasonal selection as a factor in rotifer cyclomorphosis. Naturwissenschaften 57: HAVEL, J. E., AND S. I. D~DSON Chaoborus predation on typical and spined morphs of Daphnia pulex: Behavioral observations. Limnol. Oceanogr. 29: , AND Environmental cues of Cyclomorphosis of D. pulex 861 The genetic mechanism behind the clonal cyclomorphosis in Daphnia retrocurva. Freshwasensitivity differences described here is un- ter Biol. 15: in press. HEBERT, P. D., AND T. J. CREASE Clonal coknown. One possibility is that the relative existence in Daphnia pulex (Leydig): Another frequencies of coexisting genotypes changed planktonic paradox. Science 207: during the year, one genotype sensitive and HUTCHINSON, G. E A treatise on limnology, the other insensitive to the Chaoborus fac- v. 2. Wiley. JACOBS, J Cyclomorphosis in Daphnia galeata tor. Seasonal shifts in clone frequencies have mendotae, a case of environmentally controlled been documented in other cladoceran pop- allometry. Arch. Hydrobiol. 58: ulations (Kerfoot 1977; Brock 1980; Lynch I(E RFOOT. W. C The divergence of adiacent 1983). Similar studies of Chaoborukin- populations. Ecology 56: 1298-i3 13. duced Daphnia should improve our under Perspectives on cyclomorphosis: Separation of phenotypes and genotypes. Am. Sot. standing of the distribution of these morphs Limnol. Oceanogr. Spec. Symp. 3: New in the field. England. KRUEGER, D. A., AND S. I. DODSON Embryological induction and predation ecology in Daph- References nia pulex. Limnol. Oceanogr. 26: LYNCH, M Ecological genetics of Daphnia pulex. Evolution 37: The genetic structure of a cyclical parthenogen. Evolution 38: NEESS, J. C A contribution to aquatic population dynamics. Ph.D. thesis, Univ. Wisconsin, Madison. 103 p. PASTOROK, R. A Selection of prey by Cha- oborus larvae: A review and new evidence for behavioral flexibility. Am. Sot. Limnol. Oceanogr. Spec. Symp. 3: New England. ROTH, J. C Benthic and limnetic distributions of three Chaoborus species in a southern Michigan lake (Diptera, Chaoboridae). Limnol. Oceanogr. 13: SAETHER, 0. A Chaoboridae. Binnengewasser 26: SNEDECOR,G. W., AND W.G. COCHRAN Statistical methods. Iowa State. SPITZE, K Implications of the functional response of an ambush predator: Laboratory experiments of Chaoborus americanus predation on Daphnia pulex. Ecology 66: in press. STEMBERGER, R. S., AND J. J. GILBERT Spine development in the rotifer Keratella cochlearis: Induction by cyclopoid copepods and Asplanchna. Freshwater Biol. 14: SWIFT, M. C., AND A. Y. FEDORENKO Some aspects of prey capture by Chaoborus larvae. Limnol. Oceanogr. 20: Submitted: 28 February 1984 Accepted: 8 January 1985
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