Epilimnetic rotifer community responses to Bythotrephes longimanus invasion in Canadian Shield lakes

We studied whether the effects of Bythotrephes longimanus, a new predatory cladoceran zooplankton species to North America, can extend beyond the macrozooplankton to the rotifer community, which is known to be an important controller of the microbial loop. During summer 2003, 14 Canadian Shield lakes were sampled biweekly to evaluate the effect of Bythotrephes on epilimnetic rotifers. Rotifer densities, particularly those of Conochilus unicornis, significantly increased, with elevated Bythotrephes densities. Conochilus became the dominant rotifer species in the pelagic community of lakes with high B. longimanus populations. Bythotrephes densities were a better estimator of rotifer densities than physical and chemical lake properties. Bythotrephes has indirect effects beyond its preferred prey species, cladocerans. The potential for increased rotifer densities to act as a secondary source of food for Bythotrephes was also investigated. In a 24-h feeding experiment, Bythotrephes did not prey on various common rotifer species, suggesting that Bythotrephes ignores rotifer species as a prey even when they form the sole food source. Rotifer increases are likely either due to competitive release when crustacean zooplankton decline or predatory release when native invertebrate predator populations decline. Nonindigenous species have been considered a major cause of extinction for native flora and fauna, reducing native biodiversity in invaded ecosystems (Wilcove et al. 1998). Lakes are perhaps the most susceptible ecosystem to invasions, due to the opening of trade shipping routes and increased between-lake boating activities, both of which act as dispersal vectors for nonindigenous species (Ricciardi and MacIsaac 2000). Bythotrephes longimanus, a predatory cladoceran, is one of the most recent invaders of concern in North America, likely arriving from the Baltic Sea area via ballast water into the Great Lakes in 1982 (Johannsson et al. 1991). Bythotrephes has since spread to an estimated 70 Canadian inland lakes, with hundreds of lakes in central Canada potentially colonizable (MacIsaac et al. 2000; Yan et al. 2002). Bythotrephes is known to largely affect macrozooplankton 1 Corresponding author: ([email protected]). Acknowledgments Thanks to A. Strecker and G. Puncher who helped with sampling during the summer of 2003 and to Emily Parrott for counting and calculating the Bythotrephes densities at York University. J. Rip helped collect organisms from Peninsula Lake for the feeding experiment. N. Yan, D. Lynn, S. Arnott, O. Johannsson, W. Taylor, and M. Arts provided useful discussion throughout this project. The Ontario Ministry of the Environment Science Centre provided some sampling equipment and field station space. Funding in the form of an academic subvention grant from the Department of Fisheries and Oceans Canada to BEB and from NSERC Discovery grants to BEB and KSM is gratefully acknowledged. communities. Bythotrephes preys predominantly on medium-sized daphnids (Yan and Pawson 1997; Schulz and Yurista 1998), needing 14–20 Cladocera per day to meet its energetic requirements (Burkhardt and Lehman 1994). Because of these large feeding requirements, significant decreases of Daphnia pulicaria and D. retrocurva populations in Lake Michigan were observed following invasion (Schulz and Yurista 1998). Similarly, Harp Lake, a Canadian Shield lake, was invaded by Bythotrephes in 1993 and has since shown a 17% decline in zooplankton species richness, with the loss of several cladoceran species (Yan et al. 2002; Boudreau and Yan 2003). Boudreau and Yan (2003) have suggested that Bythotrephes with a density as low as 2 individuals m23 can significantly depress cladoceran populations in Canadian Shield lakes. Relatively few studies have examined Bythotrephes effects beyond cladocerans, their direct prey. There is potential, however, for Bythotrephes, through the reduction of cladocerans (Yan and Pawson 1997; Boudreau and Yan 2003), to cause major changes throughout the food web because cladocerans are known to have strong structural and functional effects in lake food webs (Brooks and Dodson 1965; Ives et al. 1999). Major food-web effects frequently involve cross-linkage cascades, whereby the suppression of one species by predation influences the abundance, biomass, or productivity of competing species within the same prey guild. By depressing cladoceran populations, predation by Bythotrephes could favor other pelagic herbivores. The focus here will be on the response of the epilimnetic rotifer community 1005 Rotifer communities in shield lakes to Bythotrephes invasions. Rotifers are minute (,250 mm) herbivores, feeding on small (1–20 mm) phytoplankton, bacteria, and protists (Nogrady et al. 1993; Yoshida et al. 2003), and are key contributors to nutrient cycling in pelagic food webs (Makarewicz and Likens 1979; Nogrady et al. 1993). Rotifers may be responsible for up to 70% of small phytoplankton (,10 mm) grazing in the epilimnion (Armengol et al. 2001). In additioon, rotifers are an important food resource for planktivorous invertebrates (Williamson 1983) and larval fish (Guma’a 1978). Brooks and Dodson (1965) were first to propose that a decrease in Daphnia populations could result in an increase in rotifer abundances through their ‘‘size efficiency hypothesis.’’ This hypothesis and their work since (e.g., Romare et al. 1999; Sondergaard et al. 1997) suggest that the more efficiently filtering cladoceran species suppress rotifer populations through exploitative competition, unless predators are present, since planktivores generally select as prey larger zooplankton like Daphnia species. Further evidence suggests that rotifers also benefit from a reduction in interference competition with planktivory. Interference competition occurs when rotifers are killed, injured, or forced to drop their eggs as a result of direct physical interaction with cladocerans, including being swept into the feeding chamber of Daphnia (Gilbert 1985). Evidence supporting a release of rotifers from competition, owing to reduced Daphnia densities has come from studies on lake acidification (Yan and Geiling 1985; Svensson and Stenson 2002) and from experiments (Gilbert 1985, 1989). A recent experiment evaluating the prey-choice selection of Bythotrephes indicates a preference for slow-moving prey, of a size class between 0.5 mm and 1.4 mm in length (Vanderploeg et al. 1993). It has been suggested that rotifers could act as a small alternative food source for Bythotrephes when food becomes scarce (Wahlstrom and Westman 1999). Thus far, the only rotifer reported to be preyed upon by Bythotrephes is Asplanchna, a large (0.6 mm) predatory rotifer (Vanderploeg et al. 1993). The characteristics of preferred prey for Bythotrephes suggests that another rotifer species, Conochilus unicornis, commonly found in Shield lakes, could be a potential prey species. Conochilus is unique among rotifers because it forms colonies. The colonies range from between 2 and 100 individuals, vary from 0.4 mm to 2 mm in length (Dieguez and Balseiro 1998), with dimensions that match the prey size of Bythotrephes. In addition, Conochilus colonies are slow moving and lack predatory escape movements. The purpose of this study is to evaluate the cascading effects of Bythotrephes on rotifer populations by comparing epilimnetic rotifer communities in invaded and noninvaded lakes in the Canadian Shield. Increasing presence of Bythotrephes is predicted to result in an increase in rotifer densities across the 14 lakes included in this study. Rotifer community composition will be evaluated to determine whether there are any shifts in dominance owing to the invasion. The degree to which Bythotrephes density relative to physical and chemical lake properties are correlated with rotifer densities within lakes will be determined. Finally, the feasibility of rotifers as an alternate food source for Bythotrephes when preferred food sources are excluded will be evaluated using a laboratory feeding experiment.