Two-step dialogue between the cladoceran Bosmina and invertebrate predators: Induction and natural selection

Aquatic prey species respond to predators with fast (developmental) and slow (selective) feedbacks. Natural selection is assumed to fashion details of induction and to modify baseline morphology, but only rarely do we catch the slower (multi-generation) process in action. Laboratory experiments with Bosmina detected predatormediated induction and estimated spine heritability (h2 5 0.2–0.5). Third Sister Lake, Michigan, U.S.A., Bosmina exhibited induction to resident (Mesocyclops) and to two nonresident, neighborhood predators (Epischura and Leptodora). However, the magnitude of induction in Third Sister Lake Bosmina to nonresident predators (Epischura, Leptodora) was muted, when compared with induction and final spine lengths in Epischura–Leptodora lakes. Inadvertent escape of Leptodora into Third Sister Lake in 1987 created a long-term (multiyear), whole-lake experiment, where resident Bosmina populations fell under intense size selection. During the interval, Leptodora suppressed a late-season smaller, short-featured species (B. freyii), favored seasonal expansion of an overwintering long-featured species (B. liederi), and selected for longer features in the latter species. Before local extinction, defensive spines of B. liederi achieved lengths comparable to populations that co-occur with Epischura and Leptodora. Given the isolated and ephemeral nature of lakes, akin to islands, to what degree are species and community responses fashioned at the local (resident lake) or regional (lake district) level? Regional dispersal is receiving attention (De Meester et al. 2002; Havel and Shurin 2004), yet how does the duration of species contact modify predator–prey interactions, species persistence, and genetic adjustments (Ricklefs and Schluter 1993; Tilman and Kareiva 1997)? Zooplankton communities are probably best approached from a regional metapopulation perspective (Kerfoot et al. 2004; Leibold and Norberg 2004), because long-term survival of species is tied both to dispersal and to local interactions (Shurin and Allen 2001). However, unraveling ecological and evolutionary responses at local and regional scales requires extended studies, although insight may be aided by fortuitous circumstances. One of the challenges is that predator–prey interactions are complicated by two levels of response (developmental, selective). Early on, species in the cladoceran genera Daphnia and Bosmina were found capable of rapid developmental reaction to the presence of predators (Daphnia: Grant and Bayly 1981; Havel 1985; Bosmina: Kerfoot 1987). Since then, the nature of inducible defenses has been investigated from laboratory, field, and theoretical perspectives (Dodson 1989a; Tollrian and Harvell 1999; Gabriel et al. 2005). Yet there are many unanswered questions about the nature of the dialogue played out in ecological and evolutionary time between predators and prey (Tollrian and Harvell 1999; Relyea 2002). From the standpoint of the prey species: (1) how often and quickly does the predator–prey inductive response evolve; (2) how is it maintained (physical–chemical, developmental, and genetic feedbacks); and (3) how many predators are involved? To answer these questions, we require more information about the process of natural selection in lakes, particulars of developmental and genetic responses, and details on neighborhood and historical ecological interactions. In the mid–1980s, a series of zooplankton translocation experiments investigated predator–prey relationships at northeastern and Midwestern U.S. localities (i.e., moving predators and prey around in different lakes to explore food-web and ecological interactions [Kerfoot 1987; McNaught 1993a,b]). Near the end of the planned manipulations in Third Sister Lake, Michigan, U.S.A., during the summer of 1987, Leptodora inadvertently escaped from enclosures (McNaught et al. 2004). This highly efficient, size-selective predator rapidly increased in abundance, creating a long-term whole-lake experiment. Plankton samples from 1987 to 1992 documented that Leptodora became abundant and differentially depleted small-bodied cladoceran species (McNaught 1993a; McNaught et al. 2004). For 6 yr after 1992, as Leptodora reached the height of its abundance, Bosmina became locally extinct. When Leptodora crashed in the late 1990s, Bosmina reappeared in 1999 and became abundant again by 2004–2007. A sequence of translocation experiments, laboratory and field observations between 1987 and 2007 allow insight into developmental and selective responses by Bosmina.