Comparison of the response of Daphnia galeata and Daphnia obtusa to fish-produced chemical substance
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1 1544 Notes REDFIELD, A. C The biological control of chemical factors in the environment. Am. Sci. 46: RIEMANN, B., AND M. S~NDERGAARD [EDS.] Carbon dynamics in eutrophic, temperate lakes. Elsevier. RIGLER, F. H A tracer study of the phosphorus cycle in lake water. Ecology 37: VADSTEM, O., B. 0. HARKJERR, A. JENSEN, Y. OLSEN, AND H. REINERTSEN Cycling of organic carbon in the photic zone of a eutrophic lake with special reference to the heterotrophic bacteria. Limnol. Oceanogr. 34: VADSTEIN, O., A. JENSEN, Y. OLSEN, AND H. REINERTSEN Growth and phosphorus status of limnetic phytoplankton and bacteria. Limnol. Oceanogr. 33: AND Y. OLSEN Chemical composition and phosphate uptake kinetics of limnetic bacterial communities cultured in chemostats under phosphorus limitation. Limnol. Oceanogr. 34: WETZEL, R. G Limnology, 2nd ed. Saunders. Submitted: 6 February 1992 Accepted: 31 March 1993 Revised: 5 June 1993 Limnol. Oceanogr., 38(7), 1993, , by the American Society of Limnology and Oceanography, Inc. Comparison of the response of Daphnia galeata and Daphnia obtusa to fish-produced chemical substance Abstract-Individuals of two clones of two Daphnia species were reared from neonata to primipara stage in a medium preconditioned with fish (Rutilus rutilus or Percafluviatilis). Daphnia galeata, the species usually exposed in its natural habitats to fish predators, exhibited reduced juvenile length increments, earlier maturation, and relatively larger clutches of smaller eggs. Such reactions were not found in Daphnia obtusa, a species typical of fishfree localities. Reaction to the fish factor did not include structural changes of the filtration apparatus. The relationship between fish planktivores and Daphnia species, as one of their most preferred prey, is believed to be evolutionarily quite old (Kerfoot and Lynch 1987). One can therefore assume some mechanism evolved which allows the prey to respond in the way that parries this evolutionary thrust (O Brien 1987). It is important for the prey to get a danger signal so it can employ an adequate defensive reaction. Several workers have provided evidence concerning the ability of some Daphnia species to react to chemicals released by invertebrate predators. These responses include development of various kinds of defensive structures (Have1 1985; Vuorinen et al. 1989; Hanazato 1990), modification of lifehistory traits (Ketol and Vuorinen 1989; Dodson and Have1 1988) and changes in behavior Acknowledgments I thank J. HrbaCek for improving earlier drafts of the paper and S. Threlkeld and two anonymous reviewers for comments that considerably improved the manuscript. (Dodson 1988). Fewer data are available concerning the response of Daphnia spp. to the chemicals produced by fish planktivores (Dodson 1988, 1989; MachaCek 199 1). There are two features most characteristic of the predation of planktivorous fish: the largest prey items are selected mainly on the basis of visual detection, and the whole prey item is readily ingested with minimum chance to escape once it is detected. Thus the most effective defensive reaction can be expected to be preventing detection. One mechanism is to become smaller, and it has been found that small body size is a most conspicuous attribute of Daphnia spp. or populations coexisting in habitats with dense fish stocks. HrbaCek and Hrbrickova-Esslova (1960) found that diminution of body length at the primipara stage in these populations is the result of reduced length increments in juvenile and adolescent instars. Dodson (1988, 1989) recently found that some Daphnia spp. had smaller neonates and adults as well as larger clutches when reared in a tank with a fish planktivore enclosed in a mesh bag. MachaCek (199 1) presented first results of studies on the effects of chemicals released by roach on the postembryonic growth and first reproduction of a particular clone of Daphnia galeata. These results suggest that a fish factor induced D. galeata to modify its intrinsic energy allocation pattern so that somatic growth is reduced and reproduction is enhanced. We studied this phenomenon in a clone of D. galeata, the species usually exposed in its nat-
2 Notes 1545 Table 1. Results of rearing Daphnia galeata from neonata to primipara in control and experimental (preconditioned with roach) media. Numbers are average values for individuals from 10 series of experiments (1 SE in parentheses). Instar IV or V is that in which individuals reached maturity. Both groups in experimental media are compared to the group of animals in control media maturing in instar V; significantly different values are marked with asterisks (ttest, **-P ). Relative frequency of ind. (%) Primiparae body length (w-0 Relative body length of primiparae as percent length of neonates Age at first ovulation (h) Clutch size (eggs per female) Avg egg vol. (lo-? mm ) N (No. of ind.) ** 37** 1,4 1 O(30) 1,720(20) 1,330**(10) 1,470**(20) ** 206** 90(5) 107(3) 86**(2) 102 (2) 5.5(0.5) 9.8(0.3) 7.1**(0.4) 9.5 (0.4) 2.30(0.08) 2.78(0.10) 1.84**(0.06) 2.17**(0.07) ural habitats to fish predation, in comparison described above. The density of the algal suswith a clone of Daphnia obtusa which is not. pension dropped in the period between me- We also studied the influence of the fish factor dium exchange to -50% of its initial value on the length of the filtering setae in D. galeata. due to sedimentation. The temperature of the As shown by Kotinek et al. (1986) this pa- cultivation media was in the range of C rameter is one that determines the size of the and fluctuations during a particular experifiltration area of the thoracic limbs; it was found ment did not exceed +0.5 C. The rearing vesto immediately reflect changes in the amount sels were kept under continuous illumination of food available. Hence we would expect that of PEinst mp2 s- l. As no allometric fish-induced changes of growth and reproduc- growth of the carapace, head, and tail spine tion- the characteristics simultaneously con- was recorded, only the body length from the trolled by food concentration - are connected top of the head to the base of the tail spine is by modifications of the filtering structures. given. The core of the experimental design was to cultivate daphniids individually from neonata to primipara stage with fresh medium every 24 h. The medium consisted of aged tapwater either inhabited for the preceding 24 h with fish (three roach of -7-cm fork length in a 15 liter aquarium) or without them (control). Af- ter a 24-h exposure, the media were filtered through a GF/C glass-fiber filter and a unialgal culture of Scenedesmus dimorphus was added so that the resulting concentration of algal food corresponded to pg liter- l Chl a. Neonates at the age of several hours after release from the brood pouch of the mother were placed individually into the rearing vessels with a medium volume of ml so that individuals from the same clutch were evenly distributed between control and experiment. Every 24 h, the animals were measured and transferred into new medium prepared as The experiments were usually stopped several hours after the first clutch of eggs was laid into the brood pouch of the female (ovulation). At this time, the eggs stopped swelling and their size remained constant for a certain period. The time of ovulation, if not directly registered, was derived from the developmental stage of the eggs. The animals were preserved in 4% Formalin solution and the clutch size and egg size determined. The average mortality of animals in the trials did not exceed 10% and was not significantly different in control and experimental groups. More than a half of this figure is, however, formed by animals trapped in the surface film when molting (usually to the 2nd and 3rd instar). Their carapace was deformed and although they did not die, their further development was not normal and they were discarded.
3 1546 Notes D. galeata / I 1 I I body length (mm) Fig. 1. Relation between body length and clutch size in Daphnia obtusa and Daphnia galeata primiparae. Bartlett s best-fit lines stand for both control (0) and experimental (0) animals. Different-sized symbols illustrate cumulation of l-4 identical points. Confidence limits (95%) are drawn for D. galeata. The equations and coefficients of determination corresponding to regression lines are Y = 18.4X , r2 = 0.53, and Y = 19.9X , r2 = 0.51 for D. galeata; Y = 11.4X - 9.6, r2 = 0.66, and Y = 22.7X , r2 = 0.61 for D. obtusa. Two Daphnia species were tested in these experiments. D. galeata commonly lives in reservoirs with rather dense fish populations. The clone used in experiments was isolated from the Rimov Reservoir (southern Bohemia). D. obtusa, on the other hand, is typical of small temporary pools without fish. The clone used was isolated from a sma.jl pool in a field near Zliv (- 10 km north of Ceske Budejovice). Roach (Rutilus rutilus) served as the fish planktivore in all experiments except one in which european perch (Perca j7uviatizi.s) of similar size and density was used. Both fish and Daphnia were kept under laboratory conditions for several months before the experiments started. The fish were fed both living Daphnia and artificial food, but several weeks before the experiment, as well as during it, they were fed only Daphnia. The conditions of Daphnia cultivation (medium, food, tem- perature, illumination) were the same as in the experiments. The length of the filtering setae was investigated under the influence of both different food concentration and fish factor in D. galeata. The above-mentioned experimental design was modified so that the daphniids were reared at two levels of food concentration corresponding to 150 and 10 pg liter- Chl a. Neonates of the same clutch were randomly allocated to the four treatments, i.e. control and fish-treated water in both high and low food variants. The length of the filtering setae of primiparae in the middle of the comb of the third pair of thoracic limbs was measured with an eyepiece micrometer after dissection of Formalin-preserved animals. Results presented in Table 1 show a demonstrable tendency of D. galeata to earlier maturation in experimental animals. About
4 Notes 1547 I I I I I I I I body length (m 4 Fig. 2. Relation between body length and clutch volume in Daphnia galeata primiparae. Clutch volume was calculated as the product of average egg volume and clutch size. Symbols and statistics as in Fig. 1. The equations and coefficients of determination corresponding to regression lines are Y = 5.7X - 7.4, r2 = 0.62, and Y = 5.3X - 5.8, r2 = two-thirds of the experimental animals matured in instar IV, whereas nearly all control animals matured in instar V. Moreover the experimental animals exhibited a larger reproductive output compared to the similar-sized control ones. This difference can be seen when expressed in terms of both clutch size (Fig. 1) and volume (Fig. 2). Larger reproductive investment seemed to be connected to lower investment in somatic growth, as relative body length increments were smaller in experimental animals than in controls (Table 1). Relative units of somatic growth were used so that the body length increments of animals with different sizes of neonates could be compared. The average body length of the neonates (in pm k SD) was for D. galeata and for D. obtusa. The energy saved by lower increments is allotted to acceleration of development of the gonads or to production of relatively larger amounts of germinal matter. In addition, this germinal matter is divided into smaller eggs, as shown in Table 1. The alternative pattern of energy allocation between growth and reproduction is illustrated Table 2. Relative body-length increments (in % body length of preceding instar) in juvenile instars of Daphnia galeata reared in the control and experimental (preconditioned with roach) media. Confidence interval (95%) illustrates variability within the series of 10 experiments. Instar Control IV Experimental I-II & k2.9 II-III 27.2kO III-IV 21.5k IV-V 17.7* kl.l Mean per instar
5 1548 Notes Table 3. As Table 1, but of Daphnia obtusa from four series of experiments. The differences between control and experimental groups of animals were not significant in any parameter investigated. Parameter Relative frequency of ind. (O/o) Primiparae body length (m-d Relative body length of primiparae as percent length of neonates Age at first ovulation (h) Clutch size (eggs per female) Avg egg vol. (lo- mm ) N (No. of ind.) IV Control V IV Experimental ,000(20) 1,080(50) 980(40) 1,030(20) (O) 99(3) 90(2) 9fW) 4.8(0.3) 6.3(0.8) 4.7(0.8) 5.7(0.7) 1.43(0.0 1) 1.67(0.03) 1.46(0.04) 1.60(0.06) V in Table 2, where relative body-length increments that apparently represent only somatic growth are given. Remarkable growth reduction first occurs (i.e. in instar II, when the development of gonads probably begins; Mc- Cauley et al. 1990) in the group with the shortest postembryonic development. The smallest mean increment per instar corresponds with the relatively highest reproductive effort in the group of experimental animals maturing in instar V. However, for the more precise information on the pattern of energy allocation we lack data on ingestion and metabolic rates. A similar reaction of D. galeata to the fish factor described above was found in experiments in which perch was used to precondition the experimental medium. Completely different results were obtained in experiments with D. obtusa. As is apparent body length (mm) Fig. 3. Relation between body length and length of filtering setae of the 3rd thoracic limb in Daphnia galeata primiparae. Low concentrations of food (10 pg liter Chl a): fish-treated media-o; controls-& High concentrations of food (150 Kg liter Chl a): fish-treated media-o; controls-a. Bartlett s best-fit lines stand for each variant and correspond to the following regression equations and coefficients of determination: high food- Y = 136.1X , Y = 0.86, and Y = 133.6X , r2 = 0.85 for control and fish-treated media; low food- Y = X , r = 0.57, and Y = 154.2X , r2 = 0.64 for control and fish-treated media.
6 Notes 1549 from Table 3, as well as from Fig. 1, there are no significant differences in any variable investigated. The influence of food concentration and the fish factor on the length of filtering setae in D. galeata is illustrated in Fig. 3, where length of the filtering setae is plotted against body length. It is apparent that primiparae cultured in low concentrations of food have significantly longer filtering setae compared to those cultured in high concentrations of food. This reaction is consistent with results of KoEinek et al. (1986) who found that the length of filtering setae is inversely related to the concentration of seston. On the other hand, the regression lines in Fig. 3 for individuals in fish-treated and control media showed no significant difference at either food concentration when tested for identity of their slopes as well as intercepts (ANCOVA, P I 0.05). This similarity indicates that the relation between body length and length of filtering setae is unaffected by the fish factor, suggesting that the fish factor does not induce structural changes of filtering apparatus. This lack of effect suggests that the efficiency of food collection is unaffected and the response is solely a modification of the intrinsic energy allocation pattern. This result is also supported by the finding that the response is independent of the amount as well as the quality of available food (Machacek 1991). It is well known that abundant fish populations lead to changes of the size structure of the zooplankton community (HrbaEek 1962). The induced response of the daphniids is probably an additional mechanism-besides sizeselective predation -contributing to this phenomenon. The population influenced by the fish factor is better able to resist fish predation mainly because the mature adults are smaller. In addition it seems to be reproductively more efficient. The situation in natural reservoirs is much more complex, as the parameters in question are simultaneously influenced by oth- er environmental factors. The results of Dodson (1989) suggest that the responses of various Daphnia spp. to three types of predators are quite specific and that they usually correspond to the predator-prey co-occurrence pattern. The same applies to our results. The response was obtained in species usually co-occurring in their natural habitats with fish planktivores. Moreover, a similar response was found in Daphnia p&curia from a fish pond as well as in another clone of D. galeata (MachaEek unpubl.). On the other hand, the fact that D. obtusa did not respond to the fish planktivore corresponds well to its bionomics. These results suggest that the ability to respond adaptively to a fish predator is either not evolved as a species character in D. obtusa or is typical only for populations that come in contact with fish. Nevertheless, the neonates and primiparae of our clone of D. obtusa are markedly smaller than those of D. galeata. It can thus be hypothesized, in accordance with Dodson (1989), that some species are small enough to escape detection by the fish predator and so there is no need to become still smaller. Consistent results in experiments with two different fish species (three if results of Dodson 1989 with Lepomis macrochirus are taken into account) suggest that the effective factor is either some unspecific product of fish metabo- lism or that species-specific factors have similar effects on the daphniids. These are only some of the numerous aspects of this phenomenon that deserve attention in future investigations. Hydrobiological Institute Academy of Sciences of the Czech Republik Na sadkach 7, CS Ceske Budejovice Czech Republic References DODSON, S. I Cyclomorphosis in Daphnia galeata mendotae Birge and D. retrocurva Forbes as a predator-induced response. Freshwater Biol. 19: 109-l The ecological role of chemical stimuli for the zooplankton: Predator-induced morphology in Daphnia. Oecologia 78: 36 l , AND J. E. HAVEL Indirect prey effects: Some morphological and life history responses of Daphnia pulex exposed to Notonecta undulata. Limnol. Oceanogr. 33: 1276-l 287. HANAZATO, T Induction of helmet development by a Chaoborus factor in Daphnia ambigua during juvenile stages. J. Plankton Res. 12: HAVEL, J. E Cyclomorphosis of Daphnia pulex spined morphs. Limnol. Oceanogr. 30: HRBEEK, J Species composition and the amount of zooplankton in relation to the fish stock. Rozpr. Cesk. Akad. Ved Rada Mat. Prir. Ved 72: l-l 17.
7 1550 Notes -, AND M. HRBA~ovA-ESSLOVA Fish stock as a protective agent in the occurrence of slow-developing dwarf species and strains in the genus Daphnia. Int. Rev. Gesamten Hydrobiol. 45: KERFOOT, W. C., AND M. LYNCH Branchiopod communities: Associations with planktivorous fish in space and time, p In W. C. Kerfoot and A. Sih [eds.], Predation: Direct and indirect impacts on aquatic communities. New England. KETOLA, M., AND I. VUORINEN Modification of life history parameters of Daphnia pulex Leydig and D. magna Straus by the presence of Chaoborus sp. Hydrobiologia 179: 149-l 55. KOGNEK, V., B. GEPELOVA-MACHA~KOVA, AND J. MACHAEEK Filtering structures of Cladocera and their ecological significance. 2. Relation between the concentration of the seston and the size of filtering combs in some species of the genera Daphnia and Ceriodaphnia. Vest. Cesk. Spol. Zool. 50: MCCAULEY, E.,W. W. MURDOCH, R.M. NISBET, AND W. S. C. GURNEY The physiological ecology of Daphnia: Development of a model of growth and reproduction. Ecology 71: MACHACEK, J Indirect effect of planktivorous fish on the growth and reproduction of Daphnia galeata. Hydrobiologia 225: O'BRIEN, W. J Planktivory by freshwater fish, thrust and parry in the pelagia, p Zn W. C. Kerfoot and A. Sih [eds.], Predation: Direct and indirect impacts on aquatic communities. New England. VUORINEN, I., M. KJSTOLA, AND M. WALLS Defensive spine formation in Daphnia pulex Leydig and induction by Chaoborus crystallinus DeGeer. Limnol. Oceanogr. 34: Submitted: 4 September 1992 Accepted: 22 April 1993 Revised: 1 June 1993 Lmnol. Oceanogr., 38(7), 1993, , by the American Society of Limnology and Oceanography, Inc. Efficiencies of ingestion and assimilation by an invertebrate predator using C and P dual isotope labeling Abstract- Daphnia rosea was uniformly labeled with both 14C and 33P, then offered as prey to Bvthotrephes cederstroemi Schoedler, a nonindigenous predatory cladoceran which has become established in the Laurentian Great Lakes. Both C and P from the prey were ingested with equal efficiency (58-59%, SE = 2%) by Bythotrephes and retained with equal efficiency over the next 12 h. Feeding behavior by the predator involves a fastidious process of shredding and discard of exoskeletal material and selective ingestion of soft tissue. Most of the ingested matter is consequently digested; assimilation efficiency is 85% (SE = 2%). Investigations of the effects of an introduced, nonindigenous invertebrate predator, Bythotrephes cederstroemi (Cladocera: Cercopagidae), on Great Lakes food webs (Lehman 1988, 199 1) raised important questions about the nutritional physiology of the organism. In particular, estimates of in situ prey mortality Acknowledgments D. K. Branstrator prepared the labeled Daphnia for these experiments. This study was supported by NSF grant OCE (Lehman and Caceres 1993) are sensitive to efficiencies of ingestion and assimilation. The predator discards much debris, mainly exoskeletal refuse, while feeding on its plankton prey. In terms of mass balance, the discarded fractions are analogous to losses during sloppy feeding (Dagg 1974; Lampert 1978). Observation suggests that soft prey tissues alone are consumed, which may mean that discrimination practiced during the initial handling time provides a highly assimilable diet. It is possible, therefore, that assimilation efficiencies achieved by Bythotrephes are high compared with values commonly cited for crus- tacean zooplankton in general (e.g. Conover 1966; Dagg 1976). Stoichiometries of C: P for herbivorous freshwater zooplankton have been found to vary among taxa (Andersen and Hessen 199 1). Body tissue stoichiometries of the animals may differ from those of their algal food (Hessen 1990; Sterner 1990), which means that rates of ingestion, assimilation, or metabolism must become uncoupled on an element-specific ba-
Efficiencies of ingestion and assimilation by an invertebrate predator using C and P dual isotope labeling
1550 Notes -, AND M. HRBA~ovA-ESSLOVA. 1960. Fish stock as a protective agent in the occurrence of slow-developing dwarf species strains in the genus Daphnia. Int. Rev. Gesamten Hydrobiol. 45: 355-358.
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