Daphnia Population Dynamics in Western Lake Erie: Regulation by Food Limitation and Yellow Perch Predation

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1 J. Great Lakes 20(3): Internat. Assoc. Great Lakes Res Daphnia Population Dynamics in Western Lake Erie: Regulation by Food Limitation and Yellow Perch Predation Lin Wu 1 and David A. Culver Department of Zoology The Ohio State University Columbus, Ohio ABSTRACT. Two Daphnia species exhibited similar dynamic patterns in western Lake Erie. Populations peaked in early summer, declined to minimum abundance in mid-july, and then disappeared after August. To determine relative importance of food limitation and young-of-year (YOY) fish predation in regulating Daphnia dynamics, we examined relationships (I) between edible phytoplankton abundances and Daphnia fecundity and birth rates, and (2) between Daphnia biomass consumed by YOY yellow perch (Perca flavescens) and Daphnia death rates. The population peak was created by a burst of parthenogenetic reproduction. Suppression of birth rates (<1 individual d -1 ) by low edible phytoplankton resources (<4 g m- 3 wet wt) and increased consumption by YOY yellow perch caused a midsummer decline of Daphnia populations. Once the Daphnia populations were reduced, the predation from age-l and older planktivorous fish in western Lake Erie was likely to keep the populations at low densities in spite of increased food resources in late summer. An increased white perch (Morone americana) population and the invasion of zebra mussels (Dreissena polymorpha) in western Lake Erie may alter the cycle of Daphnia dynamics, hence influencing yellow perch population in the lake. INDEX WORDS: Zooplankton populations, yellow perch, white perch, food web, bioenergetics, Lake Erie. INTRODUCTION Daphnia populations in freshwater lakes often undergo a peak in abundance during spring or early summer and then a sharp decline in abundance during midsummer (Threlkeld 1979, Murtaugh 1985, Sommer et al. 1986). Following the midsummer decline, Daphnia remains rare through summer. Depletion of edible phytoplankton can drive the decline (DeMott 1983). If zooplankton become sufficiently abundant early in summer, they overgraze edible phytoplankton until their own reproduction decreases (Threlkeld 1985, Lampert et al. 1986, McCauley and Murdoch 1987). Daphnia often then remains rare during summer when inedible phytoplankton predominate (Sommer et al. 1986). This possibility that the decline in Daphnia is driven by a decline in available food is of particular importance currently because the invasion of Lake Erie by zebra mussels (Dreissena polymorpha) provides an additional grazer on the available algae. We have considered 1 Present address: Department of Zoology, University of New Hampshire, Durham, NH 03824, USA. the relative importance of zooplankton and Dreissena on algae dynamics elsewhere (Wu and Culver 1991). Other studies suggest that predation by planktivorous fish selectively reduces abundance of largebodied cladocerans such as Daphnia, resulting in a disappearance of large zooplankters from the systems (Brooks and Dodson 1965, Hall et al. 1976, Evans and Jude 1986, Crowder et al. 1987, Hewett and Stewart 1989). However, the impact of fish predation, especially predation by young-of-year (YOY) fish, on zooplankton dynamics is not well understood in Lake Erie. Further, both competition for limiting resources and fish predation often operate simultaneously (Tessier 1986, Threlkeld 1985) in nature; thus these two factors may interact to cause species replacement and/or zooplankton seasonal dynamics. Because we are interested in the nature of Daphnia summer dynamics and its relation to phytoplankton resources and YOY fish predation in western Lake Erie, we first documented Daphnia abundance patterns in the western basin. We then evaluated the effect of two biotic factors on Daphnia dynamics: edible phytoplankton availability and YOY yellow perch predation. 537

2 538 Wu and Culver STUDY AREA The western basin of Lake Erie is the most eutrophic part of the lake (> 50 µg L -1, > 1.61 µmol L -1, total P) and serves as a nursery ground for larval and juvenile fishes (Trautman 1981). The western basin was nearly isothermal in summer (Fig. 1) and rarely becomes anoxic due to shallowness and mixing. The fish community in western Lake Erie consists primarily of white perch (Monrone americana), gizzard shad (Dorosoma cepedianum), yellow perch (Perca fluvescens), freshwater drum (Aplodinotus grunniens), walleye (Stizostedion vitreum vitreum), and various shiner species (Leach and Nepszy 1976, Hartman et al. 1992). The study was conducted during June through August in 1989 at two sites (740 m apart) in both nearshore (6 m in depth) and offshore (10 m in depth) habitats of western Lake Erie (Fig. 2). METHODS Zooplankton Sampling Zooplankton was collected weekly by duplicate vertical tows with a metered 0.5-m diameter net (112-µm mesh). Samples were preserved immedi- JUNE JULY AUGUST FIG. 1. Surface and bottom temperatures during June through August in 1989 in western Lake Erie. Temperatures are means ± SE (N = 2) measured at nearshore and offshore habitats. ately with a sucrose-formalin (40 g L -1 ) solution and analyzed in the laboratory. Two to three subsamples (5-15 ml) from each sample (diluted to 500-4,000 ml) were taken until at least 20 individuals of each abundant taxon were measured (nearest WESTERN LAKE ERIE FIG. 2. Location of sampling sites in western Lake Erie.

3 Daphnia Population Dynamics in Western Lake Erie mm) using an ocular micrometer. All zooplankton found in each subsample was counted. Cladocerans were measured from the top of the carapace to the base of the spine; copepods were measured from the top of the carapace to the base of the caudal rami. Zooplankton biomass (µg dry wt L -1 ) was calculated by multiplying the density of each species by the mean individual dry weight calculated from length-weight regressions (Culver et al. 1985). Because Daphnia carry their eggs until hatching, evidence that food limits reproduction can be obtained directly from field zooplankton samples (Hall 1964, DeMott 1983). Our preserved zooplankton samples showed little egg loss for Daphnia species. Thus, we recorded individuals carrying eggs and the number of eggs for Daphnia species in each sample. We then calculated Daphnia population instantaneous growth rates, birth rates, and death rates during June through August. Growth rates (r) were estimated from weekly Daphnia densities at two successive sampling dates (N t and the population (Paloheimo 1974) and the egg developmental time (D), and death rates (d) of Daphnia sp. were estimated as the difference between birth and population growth rates: Here t is the time between two successive sampling dates (days) and D is the egg development time for several Daphnia species (Luecke et al. 1990): where T is the mean temperature between surface and bottom at each sampling date during June through August in western Lake Erie (Table 1). Finally, we converted Daphnia death rates to mortalm) of the western basin. Phytoplankton Sampling We evaluated food availability by directly examining phytoplankton communities. Two integrated water samples were collected weekly in both nearshore and offshore habitats during June through August, using a 5-cm diameter PVC pipe (3-m length). Water samples were taken by lowering the PVC pipe vertically into the water, corking the pipe. withdrawing it, and emptying the water into a 10-L bucket. 150-mL from this sample were then taken, preserved with Lugol s solution, and concentrated by allowing it to settle for a week. Phytoplankton in at least two replicate transects across a Utermohl chamber were identified and counted under an inverted microscope for each settled phytoplankton sample (average 372 cells/sample counted). Phytoplankton taxa were grouped into edible and inedible phytoplankton (Sommer et al. 1986, Kerfoot 1987, Sterner 1989). Phytoplankton classified as edible included flagellates, small diatoms, and non-filamentous green algae; inedible were filamentous diatoms and greens, spiny greens, and bluegreen algae. Volumes of edible and inedible phytoplankton were calculated from equations based on geometric dimensions (length, width, and depth) measured for each individual species. Phytoplankton biomass was estimated based on the volume calculations (assuming specific gravity = 1). Fish Sampling Selective fish predation on large and more fecund females can reduce the number of ovigerous zooplankton and thus cause a population decline. YOY fish were sampled with two 10-min otter trawls (3.66-m diameter opening and 25-mm stretched mesh cod end) once per week during June through August both in nearshore and offshore habitats. We used the distance travelled and the cross-sectioned area of the trawl to estimate volume of water sampled, which was then used to estimate YOY fish densities. YOY fish collected by trawls were immediately chilled on ice and stored frozen. They were later identified, counted, and their stomach contents (10 yellow perch per habitat per week) were quantified. Total length and wet weights were also measured. Daphnia in each yellow perch stomach content were identified to species and 20 individuals per species were measured (nearest 0.02 mm). Daphnia lengths were converted to individual dry weights (µg) using taxon-specific length-weight regressions (Culver et al. 1985). Daphnia biomass lated as a product of the mean number of that To evaluate prey selection by YOY yellow perch, we calculated Chesson s alpha with prey items found in the sample and in the fish stomach (Ches-

4 540 Wu and Culver son 1978, 1983). treating individual fish as replicates within each collecting date. The formula for this index is where r i is the proportion of prey i in fish stomachs, p i is the proportion of prey i in the zooplankton samples (i.e., in the lake), and n is the number of prey types included in the calculations. Alpha ranges from 0 (no prey i present in stomachs) to 1 (only prey i present in stomachs). Preference for various zooplankton taxa was determined by comparing the alpha value for a given taxon with the alpha value expected when the prey were eaten in proportion to their availability (i.e., the reciprocal of the number of prey types in the environment). Alpha values exceeding the reciprocal indicate positive selection for a prey taxon. Bioenergetic Analyses We calculated consumption rates of Daphnia species by YOY yellow perch using a bioenergetic model (Hewett and Johnson 1992). Parameters used in the bioenergetic equations (Hewett and Johnson 1992) have been adjusted to fit the high metabolic rate of young yellow perch based on those developed by Post (1990). To run the model, we also needed information on fish growth. diet. prey and predator caloric densities, and the water temperature (Table 1). Growth was estimated from mean individual wet weight (g) of YOY yellow perch collected in the

5 Daphnia Population Dynamics in Western Lake Erie 541 trawls. The mean wet weight was calculated for each weekly sampling period. Proportions of prey species in the diet were calculated based on the percent by dry weight of prey in the stomach contents. The caloric densities of the YOY yellow perch, their zooplankton, and other invertebrate prey are approxirespectively (Hewett and Johnson 1992). Temperatures were the means between surface and bottom in western Lake Erie. The consumption rates (g Daph- YOY yellow perch to determine the daily biomass of perch population in western Lake Erie, using the mean depth of 8 m. RESULTS Daphnia Dynamics Crustacean zooplankton in the western Lake Erie fluctuated from June to August (Fig. 3) in nearshore and offshore habitats (repeated-measures ANOVA. time effect, all P < 0.05); abundances did not differ between nearshore and offshore habitats (habitat effect, P > 0.05). Therefore, data from nearshore and offshore habitats were pooled in all subsequent analyses. The overall dynamic pattern was similar for two Daphnia species (Fig. 3). Populations peaked in June or early July, and then rapidly declined (i.e., midsummer decline) to very low densities by the end of July. The timing of the midsummer decline, however, differed between species. D. retrocurva was dominant early but was replaced by D. g. mendotae in late June. Daphnia Dynamics in Relation to Edible Phytoplankton Declining Daphnia abundance could be caused by decreased Daphnia fecundity that is mainly affected by food conditions (i.e., edible algae). Our results show that the period of the lowest edible phytoplankton biomass, between June and early July (Fig. 4,

6 542 Wu and Culver line), corresponded to the lowest Daphnia birth rates b (Fig. 4, symbols). Birth rates were actually increasing in late July, even though the Daphnia populations remained at very low density. Daphnia populations continued to decline and remained low (Fig. 3) in spite of the fact the edible phytoplankton (food resources) improved in August. YOY Fish Abundance The YOY fish assemblage in the study area of western Lake Erie was dominated by two species, white perch and yellow perch (YOY density in Table 1). Less abundant species included freshwater drum and walleye. Disappearance of Daphnia (Fig. 3) occurred after peaks of YOY fish density, suggesting that predation by YOY fish could influence zooplankton abundances. YOY Yellow Perch Diet We chose to analyze yellow perch s diet because, as planktivores in their first year of life, yellow perch in other lakes have been shown to depress Daphnia density in the littoral zone (Whiteside 1988) as well as in the limnetic zone (Mills et al. 1987). YOY yellow perch in the western basin of Lake Erie consumed a diversity of zooplankton taxa. Larval yellow perch (< 20 TL mm) first selected copepods (Table 2). After 6 July (yellow perch TL > 30 mm TL), selection for copepods decreased while increasing dramatically for D. g. mendotae (Table 2) as yellow perch grew. Other cladocerans were avoided by all sizes of YOY yellow perch examined, except that D. retrocurva was selected on 11 July. YOY Yellow Perch Predation-Bioenergetics We used parameters in Table 1 to estimate consumption of Daphnia by YOY yellow perch in our bioenergetic simulations. To evaluate how YOY yellow perch predation influenced Daphnia dynamics, we compared consumption of Daphnia by yellow perch with Daphnia death rates. The consumption and death rate of Daphnia were both expressed as mortality of Daphnia biomass (g) per meter square per day (see Methods sections for unit conventions). The consumption of D. g. mendotae by YOY yellow perch, as estimated with the bioenergetic model, was low in early June, but rapidly increased to a seasonal maximum by mid-july (Fig. 5). The TABLE 2. The mean number of zooplankton in the stomach contents of young-of-year yellow perch collected with otter trawls during June through August in western Lake Erie, Chesson s alpha shown in parentheses. The value for neutral selection is Date

7 Daphnia Population Dynamics in Western Lake Erie 543 YOY yellow perch in western Lake Erie fed exclusively on copepods in early June, increasing their consumption of D. g. mendotae as D. g. mendotae abundance increased in the lake before the midsummer decline. Thus predation from YOY yellow perch plays little role in influencing the increase of D. g. mendotae abundance in spring in Lake Erie. Though we have no phytoplankton and zooplankton data before June, it is well known that a spring phytoplankton bloom is driven by external factors: increased nutrients from spring runoff and turnover coupled with rising temperature and light levels (Wetzel 1983, Scavia et al. 1988, Reynolds 1989). The spring increase of phytoplankton is often dominated by relatively small edible species such as flagellates and diatoms (Tilman et al. 1982, Kilham and Kilham 1984, and Sommer et al. 1986). Cladoceran densities are low in spring and then increase through parthenogenetic reproduction due to availability of edible phytoplankton (Sommer et al. 1986). Mechanisms underlying the midsummer decline have generated a great deal of controversy in the literature. When Daphnia populations reach maximum abundance, they can overgraze phytoplankton to cause a decline of their own birth rates via limiting levels of their food supply (i.e., edible phytoplankton) (Lampert et al. 1986, McCauley and Murdoch 1987). Results in this study show that overgrazing was likely in the western basin of Lake Erie in late June. Low edible phytoplankton (< 4 occurrence of maximum consumption by YOY yellow perch coincided with the start of D. g. mendotae midsummer decline. During the decline, YOY yellow perch consumption accounted for 50% of the observed D. g. mendotae mortality. In late July and August, however, D. g. mendotae consumed by YOY yellow perch in western Lake Erie decreased dramatically to almost zero. Bioenergetic results indicated that YOY yellow perch examined in this study contributed little to the mortality of D. retrocurva in western Lake Erie (Fig. 5). DISCUSSION tiated the midsummer decline, but can not be used to explain the continuing low Daphnia populations in August because food conditions improved. Once the decline occurred, food resources rebounded quickly. Thus the few Daphnia had high fecundity. The extent to which zebra mussels consume additional algae in the western basin may change the timing of the algal decline, and hence the reproductive decline of Daphnia. Mortality from fish predation, via selective removal of the more visible and egg-bearing individuals (O Brien 1979, Gliwicz et al. 1981), can lead to a population decline. Larval yellow perch started feeding on copepod species and then increased selection on large D. g. mendotae. Bioenergetic results further suggest that YOY yellow perch alone accounted for the total D. g. mendotae mortality observed during the start of midsummer decline between 4 and 11 July. Yet during the midsummer decline of D. g. mendotae, predation from YOY yellow perch accounted for only 50% of the estimated mortality. YOY yellow perch in western Lake Erie switch from feeding on zooplankton to

8 544 Wu and Culver feeding on benthic prey after the decline of zooplankton populations in the lake (Wu and Culver 1992). Thus, predation from juvenile yellow perch in August contributed little to the continued low abundance of D. g. mendotae in August. In western Lake Erie, yellow perch, although still common, are no longer the dominant species in fish community. White perch and gizzard shad are the most commonly encountered YOY fish (Hartman et al. 1992). White perch were the dominant species in our sampling habitats. Because white perch and yellow perch prefer similar prey in western Lake Erie (Parrish and Margraf 1991) we extrapolated the parameters and variables used in yellow perch bioenergetic simulations to white perch. When we multiplied the consumption rate calculated from the bioenergetic model for yellow perch by total abundance of YOY fishes to estimate the overall impact of YOY fish predation on Daphnia populations, we obtained a consumption much greater than 100% of the mortality observed in D. g. mendotae. This could indicate that extrapolation of yellow perch parameters for white perch in bioenergetic analyses is not reasonable. The consumption by YOY white perch has to be estimated based on white perch specific metabolic variables, growth, and diet. Luecke et al. (1990) examined the predation by age-l and older yellow perch and cisco (Coregonus artedii) in regulating Daphnia dynamics in Lake Mendota, Wisconsin. They concluded that consumption from these planktivorous fish resulted in only 2% of Daphnia mortality during the midsummer decline, but accounted for essentially 100% of the observed Daphnia mortality in late July and August. Therefore, feeding from other YOY fish and age-l and older planktivorous fish in western Lake Erie may result in the maintenance of low abundances of D. g. mendotae even though food condition for Daphnia had improved in August Although yellow perch rarely preyed on D. retrocurva, this species underwent a similar dynamic cycle. This suggested that predation from YOY yellow perch was not responsible for summer dynamics of this species. This, however, does not necessarily devalue the importance of other YOY fish predation in regulating D. retrocurva summer dynamics. Our trawl with a 25mm mesh cod end is probably biased in catching small YOY fish larvae. The decline of 1). retrocurva occurred before that of D. g. mendotae. Thus. the role of predation from small fish larvae remains to he examined. In conclusion, Daphia populations exhibited a relatively predictable dynamic pattern in the western basin of Lake Erie. A population peak was created by a burst of parthenogenetic reproduction; reproduction was then suppressed due to low edible algal abundances. Suppression of birth rates and the increased consumption by YOY fishes (e.g., yellow perch on D. g. mendotae) initiated a decline of the population, i.e., the midsummer decline. Predation by age-l and older planktivorous fish may cause the continuing decline of Daphnia density even though edible algal resources had improved in the lake during late summer. However, a shift in western Lake Erie fish community from yellow perch dominated to white perch and gizzard shad dominated (Hartmen et al. 1992) and the invasion of zebra mussels may alter the cycle of Daphnia populations, hence influencing yellow perch, an important sport fishery in Lake Erie. ACKNOWLEDGMENTS Funds for this research were provided by an Ohio Sea Grant project (No. NA84AA-D-00079) to David A. Culver and a Stone Laboratory Research Fellowship to Lin Wu, and the Department of Zoology (The Ohio State University). REFERENCES Brooks, J. L., and Dodson, S. I Predation, body size, and composition of plankton. Science 150: Chesson, J Measuring preference in selective predation. Ecology 59: The estimation and analysis of preference and its relationship to foraging models. Ecology 64: Crowder, L. B., McDonald, M. E., and Rice, J. A Understanding recruitment of Lake Michigan fishes: the importance of size-based interactions between fish and zooplankton. Can. J. Fish. Aquat. Sci. 44 (Suppl. 2): Culver, D.A., Boucherle, M. M., Bean, D. J., and Fletcher, J. W Biomass of freshwater crustacean zooplankton from length-weight regressions. Can. J. Fish. Aquat. Sci. 42: DeMott, W. R Seasonal succession in natural Daphnia assemblage. Ecol. Monogr. 53: Evans, M. S., and Jude, D. J Recent shifts in Daphnia community structure in southeastern Lake Michigan: A comparison of the inshore and offshore regions. Limnol. Oceanogr. 31: Gliwicz. Z. M., Ghilarov A., and Pijanowska, J Food and predation as major factors limiting two natural population:, of Daphnia cucullata Hydrobiol. 80: Hall, D. J An experimental approach to the

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