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Ecological Interactions Between Bythotrephes Cederstroemi and Leptodora Kindtii and the Implications for Species Replacement in Lake Michigan

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Ecological Interactions Between Bythotrephes Cederstroemi and Leptodora Kindtii and the Implications for Species Replacement in Lake Michigan J. Great Lakes Res. 21(4):670-679 Intemat. Assoc. Great Lakes Res., 1995 NOTE Ecological Interactions Between Bythotrephes cederstroemi and Leptodora kindtii and the Implications for Species Replacement in Lake Michigan Donn K. Branstrator* Department of Biology Natural Science Building University of Michigan Ann Arbor, Michigan 48109 ABSTRACT. The zooplankton predator, Leptodora kindtii, declined in abundance at an offshore reference station in Lake Michigan in the mid-1980s following the invasion of another zooplankton predator, Bythotrephes cederstroemi. Both predators feed largely on daphnid prey and it was observed that densities of three Daphnia species declined in abundance at the reference station following the Bythotrephes invasion. Circumstantial evidence would suggest that the native predator, Leptodora, was competitively suppressed by Bythotrephes. However, results of laboratory experiments presented here show that Bythotrephes will readily attack and eat Leptodora when the predators are maintained under concentrated densities, even if alternative prey are available for the Bythotrephes. There was no evidence in these experiments that Leptodora attacked or ate Bythotrephes. These results imply that predation by Bythotrephes on Leptodora may alternatively account for the collapse of Leptodora in offshore Lake Michigan. In this note I discuss evidence in support of competition and predation as alternative hypotheses to explain the pattern of species replacement, Bythotrephes for Leptodora, observed in Lake Michigan. The existing data are not definitive and tempt further inquiry. INDEX WORDS: Bythotrephes, Leptodora, Lake Michigan, invading species. INTRODUCTION Bythotrephes cederstroemi invaded the Laurentian Great Lakes during the 1980s. Its time of arrival and dispersal pattern were particularly well documented for Lake Michigan (Lehman 1987, Evans 1988) where shortly following its invasion several contemporaneous changes occurred in the composition of the lake's native plankton community suggesting that the predator was altering the community (Lehman and Caceres 1993). Among these changes was a strikingly quick decline in the abundance of a native zooplankton predator, Leptodora kindtii. During the two years preceding the Bythotrephes invasion, Leptodora had achieved summer abundances >3,000 individuals m-2 in offshore regions of Lake Michigan (Table 1). But in regions where Bythotrephes subsequently established populations, Leptodora declined in abundance. Lehman (1991) used 128 independent zooplankton samples collected from inshore and offshore regions of Lake Michigan to demonstrate that an inverse relationship in the abundance of Bythotrephes and Leptodora occurred lake-wide from 1986 to 1990. Garton et al. (1990) reported that a similar pattern of species replacement, Bythotrephes for Leptodora, had developed in the western basin of Lake Erie following the invasion of Bythotrephes there. *Current address: The University of Chicago Department of Ecology and Evolution 1101 East 57th Street Chicago, Illinois 60637 These spatial and temporal patterns of species replacement are suggestive of strong, biotic interaction between Bythotrephes and Leptodora, however, the relative importance of alternative hypotheses remains unresolved. It seems worthwhile to investigate both compe- tition and predation as possible mechanisms that explain the pattern. The invader, Bytho- trephes, occupies a dietary niche similar to that of Leptodora in that both predators prefer small cladoceran prey (Mordukhai-Boltovskaia 1958, Edmondson and Litt 1987, Branstrator and Lehman 1991). The predators will therefore likely compete for food, especially for small daphnid instars which appear to be the selected prey of both species. Bythotrephes is also substantially larger than Leptodora, weighing up to 10 times more as adult instars (Lehman and Caceres 1993) and may therefore also prey upon Leptodora. In this report I present experimental evidence that Bythotrephes will capture and eat Leptodora in the laboratory. I also apply an encounter rate model developed by Gerritsen and Strickler (1977) to estimate rates of encounter between Leptodora and Bythotrephes in Lake Michigan. I then discuss the available evidence in support of both the predation and competition hypotheses. Finally, I address a third hypothesis that fish planktivory increased in Lake Michigan and caused the decline in Leptodora abundance. This third hypothesis is particularly relevant since Sprules et al. (1990) have argued that fish planktivory was the cause of other contemporaneous changes in the zooplankton community, particularly the decline in daphnid abundances, that followed the Bythotrephes invasion. METHODS Predation Experiments All zooplankton used in the experiments were collected with a conical net of 130-µm mesh towed obliquely through the water column. Leptodora were collected from Third Sister Lake, Ann Arbor, Michigan, and Bythotrephes were collected from offshore Lake Michigan (43°N, 86°40'W). The logistics of sampling two lakes did not permit both predator species to be collected simultaneously. Consequently, the Leptodora and Bythotrephes were starved for different amounts of time before experimentation. A reciprocal starvation schedule was employed in the 1-L jar experiments in order to control for the effects of starvation. Two experimental designs, using different sized containers, were used to test whether Bythotrephes will capture and eat Leptodora. Experiments were conducted in either polystyrene tissue culture vessels (Costar) with 10 mL Lake Michigan water, or glass jars with 1 L lake water, 50% Third Sister Lake and 50% Lake Michigan by volume. All water was pre-screened (50-µm mesh). Experimental vessels were kept in a walk-in environmental chamber at the University of Michigan and maintained at 16°C and light <2 µЕ m-2 s-1. The experimental temperature was chosen based on measured thermal tolerances of the two species (Garton et al. 1990). The low light levels were maintained in order to simulate more natural lake conditions. One experiment was conducted in the 10-mL vessels which had one control and three treatment series, with 60 replicates per series. Treatment replicates each received 1 adult Leptodora and 1 Bythotrephes. The Bythotrephes were either instar-1 or -2 (both pre-adult), or instar-3 (adult). The three instars cover the full range of body size achieved by Bythotrephes in Lake Michigan (Yurista 1992). Control replicates each received 1 Leptodora and no Bythotrephes. The animals were observed several times daily under an Olympus dissecting microscope with darkfield illumination and their conditions were noted. The Leptodora and Bythotrephes were pre-starved for 3 h and 16 h, respectively. Two experiments, designated A and B, were conducted in the 1-L jars. Each experiment had 1 control and 1 treatment series, with 20 replicates per series. The treatment jars each received 1 Leptodora, 1 Bythotrephes of instar-3, and 30 to 40 Daphnia (non-helmeted D. galeata mendotae from Third Sister Lake and juvenile D. pulicaria from Lake Michigan). The control jars each received 1 Leptodora, no Bythotrephes, and the same complement of Daphnia as that added to each treatment jar. The condition of the predators was recorded several times over 3 days by briefly holding the jar to light. Leptodora and Bythotrephes were pre-starved in experiment A for 10 h and 35 h and in experiment В for 24 h and 0 h, respectively. It was possible to distinguish between Leptodora that had been killed or eaten by Bythotrephes and those that had died with no apparent injury. Leptodora were recorded as killed by Bythotrephes if 1) Leptodora was not found in the container, 2) Leptodora was partially eaten, or 3) Bythotrephes was seen eating Leptodora. Body Size Estimates I hypothesized that predator body size would affect the experimental results. Although both species reach body lengths of 10 to 15 mm, large Bythotrephes females can weigh fully 10 times more than Leptodora of comparable length. Therefore, both lengths and dry weights of the animals were estimated. For the experiment conducted in 10-mL vessels, the mean body size of Leptodora was estimated with specimens taken from the same collection used to set up the experiment. These Leptodora were randomly selected when other specimens were being moved to the vessels for the start of the experiment. They were measured live from the center of the eye to the base of the bifurcation in the tailspine. Their dry weights in ug were estimated as where L is Leptodora length (mm) (Lehman and Caceres 1993). For experiments conducted in 1-L jars, the mean Leptodora length was estimated from Leptodora still alive in the control jars at the end of each experiment. The Leptodora were preserved individually in 4% sugar-Formalin and later measured for total length as described above. A correction factor was applied to the length measurements to account for body shrinkage caused by the preservative: where LL is live length and PL is preserved length for Leptodora preserved in 4% sugar- Formalin >55 d. Length measurements, corrected for shrinkage, were converted to µg dry weight (Eq. 1). The average weight of Bythotrephes instars can vary dramatically during the summer in Lake Michigan (Burkhardt 1994). For example, the average weight of instar-3 females ranged from approximately 100 µg to 630 µg during July to September, 1990. This variation in body weight has been shown to correlate significantly with epilimnetic water temperature
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