Assimilation of micro- and mesozooplankton by zebra mussels: A demonstration of the food web link between zooplankton and benthic suspension feeders

We tested the hypothesis that rotifer species in the microand mesozooplankton are a potential food source for zebra mussels. We labeled phytoplankton with 14C, fed them to two species of rotifers (140–210 mm length) that were previously found abundantly in the Hudson River and had declined following a zebra mussel invasion, and estimated the assimilation of carbon. Assimilation efficiencies were found to be ;37.4–54.0%. Combined with our feeding experiments, the data on rotifer densities before and after the invasion allowed us to calculate the energy budgets for zebra mussels. Before zebra mussels dominated the Hudson River in 1992, the absorption of energy from rotifers was about two to three times higher than that necessary to maintain its routine metabolic rate and contributed about 0.349–0.662 J h21 to mussel growth and reproduction, conferring a positive scope for growth. Since the zebra mussels became abundant in the Hudson River, assimilation of rotifers is still sufficient to explain ;16.4–23.1% of the mussels’ routine metabolic rate. Therefore, rotifers play a conceivably large role in the energy budget of zebra mussels, whether at high rotifer concentrations (before the invasion) or at low rotifer concentrations (after the invasion). This is the first quantitative evidence for a trophic link between benthic bivalve mollusks and larger microand mesozooplankton that might extend to marine systems where bivalves can derive nutrition from microzooplankton, including planktonic invertebrate larvae. Combined with other recent results, this study documents a benthos–zooplankton trophic loop, demonstrating potentially strong top-down control by dense bivalves on aquatic systems. Filter-feeding bivalve populations exert keystone effects on the plankton of the coastal oceans (Prins et al. 1998) by filtering large volumes of water, severely depleting the phytoplankton, and by selectively feeding and thus altering the species composition of the phytoplankton. Overexploitation by humans in some waterbodies and invasions of exotic bivalves into others have resulted in major reorganizations of aquatic ecosystems. No change has been stronger than those caused by the invasion of the zebra mussel, Dreissena polymorpha, into lakes and rivers of North America, which has resulted in strong alterations in the composition of the plankton, resulting in strong ecological impacts (Nalepa and Schloesser 1993). The zebra mussel, D. polymorpha, was first likely introduced into Lake St. Clair and the North American Great Lakes near Detroit, Michigan, in 1986; it then spread into major basins, including the Mississippi, St Lawrence, and Hudson drainages. The expansion of zebra mussel distribution has induced significant abiotic and biotic changes mediated either directly or indirectly (MacIsaac 1996). The invasion of the tidal freshwater Hudson River in 1991 by the exotic zebra mussel has caused large changes in several components of the Hudson’s food web. Zebra mussels have strongly depleted Hudson River phytoplankton standing stocks (Caraco et al. 1997) and have altered the species composition of the phytoplankton. Selective feeding by zebra mussels might have been instrumental in the shift in phytoplankton dominance from blue-green algae to diatoms (Baker et al. 1998; Bastviken et al. 1998). Zebra mussels can also clear microzooplankton such as rotifers from suspension, and rotifer loricae have been found in zebra mussel guts (MacIsaac et al. 1991). The zebra mussel’s invasion of the Hudson ecosystem has decreased the microzooplankton, particularly rotifers (Pace et al. 1998), as they have in other lakes and rivers (Jack and Thorp 2000; Thorp and Casper 2002). Planktonic rotifers form an important constituent in the diets of many aquatic predators, such as other rotifers (Asplanchna), insect larvae (Chaoborus), cyclopoid and calanoid copepods (Diacyclops, Epischura), malacostracans (Mysis), and particulate-feeding and filter-feeding fish (Stemberger and Gilbert 1987). Zebra mussel invasions have been implicated in other rotifer declines (MacIsaac et al. 1991), and they appear to be the agent of decline of microzooplankton and mesozooplankton, such as rotifers, in the Hudson River ecosystem. However, we know of no quantitative evidence of carbon assimilation that would provide a trophic link between zooplankton and zebra mussel nutrition, or any other bivalves, even though other larger zooplankton have also been found in the guts of marine bivalves (Shumway et al. 1987). Over the last 6 yr, it has been shown that bivalves are not solely herbivores, but omnivores. Bacteria, nanozooplankton, and microzooplankton, such as heterotrophic flagellates (;4 mm) and ciliates (;20 mm), can be ingested and assimilated (Kreeger and Newell 1996, 2001; Le Gall et al. 1997), and they have been shown to be quantitatively important in the diet of many suspension feeders, such as the ribbed mussel, Geukensia demissa (Kreeger and Newell 2001). In this experiment, we discovered a strong nutritional dependence of zebra mussels on larger microand mesozooplankton with lengths from 140 to 210 mm, forming an extensive benthic–zooplankton (BZ) trophic link that could alter our understanding of aquatic, estuarine, and coastal food webs. Experimental design—We directly tested the possibility of a BZ loop between larger zooplankton and bivalves by feed-