Oikos 116: 1895Á1903, 2007 doi: 10.1111/j.2007.0030-1299.15883.x, Copyright # Oikos 2007, ISSN 0030-1299 Subject Editor: Jonathan Shurin, Accepted 13 June 2007 Competition and intraguild egg predation among freshwater snails: re-examining the mechanism of interspecific interactions Andrew M. Turner, Rebekah R. Turner and Scott R. Ray A. M. Turner ([email protected]), R. R. Turner and S. R. Ray, Dept of Biology, Clarion Univ., Clarion, PA 16214, USA. Experimental and field studies suggest that freshwater snail species have negative effects on each other’s population growth rates. Because snails share similar diets, these interactions have been interpreted as the result of exploitative competition, but they could also result from intraguild predation. Here we present three experiments aimed at testing the hypothesis that interspecific interactions among three species of freshwater gastropod (Helisoma trivolvis, Physa acuta and Stagnicola elodes) are mediated by intraguild egg predation. Foraging trials, conducted in a laboratory, showed that some snails readily prey on eggs, but the extent of egg predation depended on both the identity of the snail predator and the identity of the egg mass. Of the three species considered, Stagnicola had the largest effect on egg mortality and Physa had no effect on egg mortality. Foraging trials also showed that the eggs of Physa were the most vulnerable to predators and that the eggs of Stagnicola were largely invulnerable. A study conducted in large outdoor mesocosms assessed the occurrence of egg mortality in an environment of more extensive spatial scale and complexity. The results largely mirrored those of the laboratory study, with Stagnicola being the most voracious predator and the eggs of Physa being most vulnerable to predation. The reproductive success of Physa and Stagnicola raised in sympatry and allopatry was assessed in a mesocosm study conducted over three months. Recruitment of both species was depressed in sympatry, but patterns of growth in the survivors suggest contrasting mechanisms of suppression: Physa suppressed Stagnicola via exploitative competition, but Stagnicola suppressed Physa via egg predation. These experiments support the hypothesis that freshwater snail assemblages are structured by strong interspecific interactions and that a rich interplay of egg predation and interspecific competition underlie interactions among the members of this guild. Studies of competitive interactions among animal because it can produce community dynamics (e.g. species are often built around experiments that manip- alternate stable states) that are qualitatively and quanti- ulate the density of hypothesized competitors, and the tatively different than those produced by pure exploi- putative competitors are selected based on similarity in tative competition (Polis et al. 1989, Polis and Holt diet and habitat use (Connell 1983, Schoener 1983). 1992). The frequency and importance of intraguild Although such tests can reveal whether negative inter- predation in nature may be underestimated because it is specific interactions exist, they do not always reveal the difficult to identify, and it can produce patterns of mechanism of interaction, as a number of studies show species replacement that are sometimes mistakenly that animals originally thought to share similar diets interpreted as the result of competition. may sometimes prey on each other (Heyer et al. 1975, Freshwater snails provide an excellent example of a Wissinger et al. 1996). An interaction in which a species guild exhibiting predictable patterns of species turnover facultatively preys on another species that otherwise uses along an important environmental gradient, in this case similar resources, and thus is also a potential compe- the pond size/hydroperiod gradient (Pip 1986, Jokinen titor, is called intraguild predation (Polis et al. 1989). A 1987, Dillon 2000). Field studies (Barbosa 1973, Adam full understanding of community structure requires a and Lewis 1992) and experimental studies (Brown 1982, knowledge of the occurrence of intraguild predation Hershey 1990) of interspecific interactions conclude that 1895 freshwater snails have negative effects on each other’s (203514 cm deep) were filled to a depth of 4 cm population growth rates. The negative interactions have (2.8 l) with aged well water. Adult snails were stocked been interpreted as the result of exploitative competition, into the containers, allowed to deposit egg masses, and but none of the above studies provide corroborating removed. Egg masses were then thinned to a constant evidence. In one important example, Brown (1982) density of five masses per container. Egg masses were found that Stagnicola elodes depressed the reproductive individually marked with inscriptions on the outside of output of Physa gyrina. Brown concluded that the the opaque container. A single adult snail was stocked reproductive suppression was due to resource competi- into each container and allowed to forage. After four days tion between Stagnicola and Physa, and this study is now the predator was removed and the remaining egg masses a textbook example of how exploitative competition were tallied. Finely ground fish food was added to each structures community composition (Townsend et al. container to provide an alternate food source for the 2003, Begon et al. 2006). Our field observations suggest, snails. Temperature was maintained at 228C, and light- however, that Stagnicola is a predator of Physa eggs ing was set at 14:10 h day: night. Eggs of three species (Turner unpubl.), leading us to question whether (S. elodes, P. acuta and H. trivolvis) were used as prey, interspecific interactions involving Stagnicola are driven and the same three species were employed as predators, by exploitative competition or egg predation. with all nine possible predator/prey combinations tested. This paper presents the results of three experiments The experiment consisted of n9 replicate trials per testing the hypothesis that interspecific interactions predator/prey combination, for a total of 81 predation among freshwater gastropods are mediated in part by trials. Every set of nine trials was accompanied by a no- intraguild egg predation. We first examine whether predator control trial in order to assure that there was no three species of pulmonate snails, common in the ponds apparent egg mortality in the absence of predators. of eastern North America, are capable of preying on Effects of predator identity and egg identity on egg each other’s eggs in a laboratory setting. We then mortality were analyzed with 33 ANOVA. expand the spatial scale, and test whether egg predation occurs in mesocosms that better mimic natural ponds. Finally, we conduct a mesocosm experiment examining Egg mortality study the population level consequences of egg predation and interspecific competition. We assessed the importance of egg predation at broader spatial scales by monitoring egg mortality in large mesocosms (1.5 m Ø, 0.5 m deep, 900 l), meant to Methods mimic small ponds, placed outdoors at the Pymatuning Laboratory of Ecology in northwestern Pennsylvania, Study system USA. Three target species (P. acuta, H. trivolvis and S. elodes) were stocked by themselves and in pairwise Our study focuses on species interactions among three combinations with the two other species. Thus, each species of large-bodied pulmonate snails: Physa acuta, species was subject to three treatments, an allopatry Stagnicola elodes and Helisoma trivolvis. These three treatment and two sympatry treatments. In the third species are widespread and commonly co-occur in the week of June, we filled 36 mesocosms with well water, ponds and marshes of northeastern and midwestern inoculated them with zooplankton and phytoplankton, North America (Pip 1986, Jokinen 1987). Physa acuta and added 5 g dry red maple, Acer rubrum, to each tank. and H. trivolvis are especially widespread and abundant Growth of periphyton and decaying leaves provided food in the ponds of northwest Pennsylvania (Mower and for snails and some physical complexity, though the lack Turner 2004). Stagnicola elodes has a more narrow of macrophytes resulted in an environmental with less habitat distribution, being restricted to shallow ponds complexity than is typical of natural ponds. After four with some forest cover, but within such ponds they are weeks, reproductive snails were stocked at the rate of 15 also quite abundant (Brown 1982, Mower and Turner individuals per tank (allopatry treatments) or 30 snails 2004). All three species have traditionally been consid- per tank (sympatry treatments, 15 individuals of each ered detritivores and herbivores as their diet consists species). This density (8.5 and 17 snails m2)is largely of detritus, periphyton, and senescent macro- considerably lower than snail densities typically observed phytes (Bovbjerg 1965, Clampitt 1970, Calow 1975, in ponds (Brown 1982, Dillon 2000). We observed egg reviewed by Dillon 2000). deposition and survivorship for one week following stocking of adults. Egg mortality was assessed by locating Laboratory foraging trials individual egg masses on the tank sides and monitoring their survivorship over a period of 72 h. The effect of The ability of snails to prey upon snail eggs was assessed sympatric neighbors on egg mortality was assessed with in laboratory trials. Polypropylene ‘‘shoebox’’ containers one-way ANOVA, with a separate test run for each target 1896 species, followed by Tukey’s post-hoc test. We