Hydrobiologia 495: 59–72, 2003. © 2003 Kluwer Academic Publishers. Printed in the Netherlands.
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Zebra mussels (Dreissena polymorpha) limit food for larval fish (Pimephales promelas) in turbulent systems: a bioenergetics analysis∗ L. A. Bartsch1 , W. B. Richardson1 & M. B. Sandheinrich2 1 U.S.
Geological Survey, Upper Midwest Environmental Sciences Center, 2630 Fanta Reed Road, La Crosse, WI 54603, U.S.A. Tel: 01-608-781-6286. Fax: 01-608-783-6066. E-mail:
[email protected] 2 River Studies Center, Department of Biology, University of Wisconsin- La Crosse, La Crosse, WI 54601, U.S.A. Received 25 March 2002; in revised form 4 December 2002; accepted 19 January 2003
Key words: Dreissena, Pimephales, larval fish, turbulence, bioenergetics
Abstract We conducted a factorial experiment, in outdoor mesocosms, on the effects of zebra mussels and water column mixing (i.e., turbulence) on the diet, growth, and survival of larval fathead minnows (Pimephales promelas). Significant (P < 0.05) larval mortality occurred by the end of the experiment with the highest mortality (90%) occurring in the presence of both turbulence and zebra mussels, whereas mortality was 37% in treatment with turbulence and 17% and 18% in the zebra mussels treatment, and the control, respectively. The size of individual fish was significantly different among treatments at the end of the experiment and was inversely related to survival. Levels of trophic resources (i.e., phyto and zooplankton) varied among treatments and were treatment specific. Turbulent mixing facilitated removal of phytoplankton by zebra mussels by making the entire water column of the tanks available to these benthic filter feeders. Early in the experiment (Day = 0 to 14) the physical process of turbulent mixing likely caused a reduction in standing stocks of zooplankton. The interactive effect of turbulence and mussels reduced copepod and rotifer stocks, through physical processes and through filtration by zebra mussels, relative to the turbulence treatment. The reductions in the number of total zooplankton in the turbulent mixing mesocosms and the further reduction of rotifer and copepod in the turbulence and mussels treatment coincided with a period of increased reliance of larval fathead minnows on these prey. Estimates of consumption from bioenergetics modeling and measured prey standing stocks indicated caloric resources of suitable prey in turbulence treatments during the early weeks of the experiment were insufficient to prevent starvation. Early mortality in the turbulence and mussels treatment likely released surviving fish from intense intraspecific competition and resulted in higher individual growth rates. A combination of high abundance of zebra mussels in an environment with a well-mixed water column can have significant effects on larval fish survival and growth.
Introduction The zebra mussel, Dreissena polymorpha, has significantly changed energy pathways in European lakes (Karatayev et al., 1997), the Laurentian Great Lakes (Dermott & Kerec, 1997) and North American rivers (Effler et al., 1996; Strayer et al., 1997; Caraco et al., 1997). These changes include reduced standing stocks of phytoplankton (MacIsaac et al., 1992; Effler ∗ The U.S. Government right to retain a non-exclusive, royaltyfree licence in and to any copyright is acknowledged.
et al., 1996; Strayer et al., 1997), declines in smallbodied zooplankton (e.g., rotifers and some cladocera, MacIsaac et al., 1995), and increased species richness (Stewart et al., 1998) and standing stocks of benthic invertebrates (Karatayev et al., 1997; Strayer et al., 1997). The removal of phytoplankton from the water column, and the subsequent shift of energy from the plankton into the benthos, has occurred in both lentic (MacIsaac et al., 1992) and lotic systems (Strayer et al., 1997). Increases in biomass of benthic invertebrates are probably due to (1) shunting of pelagic
60 energy from the water column to the benthos through feeding activity and particle deposition by zebra mussels and (2) increased physical structure that mussel shells provide as refuge from predators. The ability of zebra mussels to redirect energy from the water column to the benthos is likely a function of their density and the rate of seston resupply to the mussel beds (MacIsaac, 1996; Richardson & Bartsch, 1997). Although the mechanisms of seston supply are different in lotic and lentic systems, both ultimately depend on the degree of exchange and mixing of water over the mussel beds (Smit et al., 1992; Yu & Culver, 1999). Changes in energy pathways in North American waters caused by zebra mussels have not resulted in detectable changes in upper trophic levels (i.e., standing stocks or survival of fishes). Although we would expect an eventual increase in the proportion of benthivorous fishes within the community [as observed in lakes of Europe and the former Soviet Union (Karatayev et al., 1997)], and, potentially, a reduction in the biomass of planktivorous fishes as a result of redirected energy to the benthos. In shallow, confined areas densely populated by zebra mussels (e.g., small lakes, poorly mixed littoral zones, or permanent eddies in large rivers), the production of planktonbased food webs (obligatory zooplanktivorous fishes and invertebrates) should decline. The reliance of most temperate fishes on microzooplankton during larval development potentially places these populations at risk of mortality due to a "trophic resource bottleneck" (MacIsaac, 1996); no studies have specifically tested the hypothesis that zebra mussels can limit food for larval fishes. Our objectives were to experimentally test the hypotheses that (1) zebra mussels can limit trophic resources for larval fish; (2) turbulent mixing would increase efficiency of particle removal by zebra mussels and enhance resource limitation; and (3) resource limitation would reduce growth and survival of larval fish.
Materials and methods Experimental design We designed a factorial experiment to test if zebra mussels can exert a trophic bottleneck on larval fish, particularly in the presence of a well-mixed water column. Turbulent mixing over mussel beds is a common determinant of the extent of phytoplankton and particle removal from the water column (sensu Wild-
ish & Kristmanson, 1997; Ackerman, 2001). The factorial design permitted the testing of all possible combinations of the two factors. We, therefore, expected a significant reduction in lower trophic resources (phytoplankton and zooplankton) in well-mixed tanks containing zebra mussels. We also expected reductions of lower trophic resources to result in poor overall survival of larval fish reliant on these missing resources. To test this hypothesis we placed 350 newly hatched larval (
