Prioritized phenotypic responses to combined predators in a marine snail

Abstract

Although many species face numerous predators in nature, the combined impact of multiple predators on the inducible defenses of prey has rarely been studied. Prey may respond with an intermediate phenotype that balances the risk from several sources or may simply respond to the most dangerous predator. I examined the separate and combined effects of the presence of shell-breaking (crabs, Cancer productus) and shell-entry (seastars, Pisaster ochraceus) predators fed conspecific snails on the defensive shell morphology and antipredator behavior of a marine snail (Nucella lamellosa). When exposed to each feeding predator separately, snails responded with a combination of morphological defenses that reflect the attack mode of the predator and a generalized behavioral response. Snails responded to feeding crabs by increasing refuge use and producing a thick, rotund shell. Snails responded to feeding seastars with increased refuge use but produced elongate shells with high spires that allowed for greater retraction of the soft tissue. Seastar-induced phenotypes reduced susceptibility to seastars relative to crab-induced phenotypes, but crab-induced phenotypes did not significantly reduce susceptibility to crabs, indicating an asymmetrical functional trade-off. When feeding predators were combined, snails produced a morphological phenotype similar to that expressed in the presence of the predator that imposed the highest mortality at the population level, suggesting that predator-induced morphology was prioritized according to predation risk. These results suggest that prioritizing conflicting defenses according to predator danger may be a common strategy for prey responding to combined predators, particularly in conjunction with generalized behavioral responses that reduce overall risk in multiple-predator environments.

Evolutionary ecology of inducible morphological plasticity in predator–prey interaction: toward the practical links with population ecology

“…Hence, when dragonflies are present, salamanders are less active, which reduces the intensity of the salamander-tadpole interactions that are necessary to induce the tadpole defense. Such modification of predator-specific inducible defenses by presence of another predator have been documented in other predator-prey systems (Teplitsky et al 2004;Hoverman and Relyea 2007;Lakowitz et al 2008;Bourdeau 2009). …”

“…To address this issue, one must examine how antagonistic phenotypic plasticity has coevolved and is maintained in a focal predator-prey interaction. Previous theoretical models have focused on either the inducible defense or offense and have concluded that both types of plasticity can stabilize predator-prey population dynamics (Abrams 1984(Abrams , 1992(Abrams , 1995Matsuda et al 1993Matsuda et al , 1994Matsuda et al , 1996Abrams and Matsuda 1997;Bolker et al 2003;Kondoh 2003Kondoh , 2007Ramos-Jiliberto 2003;Vos et al 2004a,b;Kopp and Gabriel 2006;DeAngelis et al 2007;Mougi and 18 Nishimura 2007, 2008a, 2009. However, few studies have specifically focused on reciprocity in plasticity for both the predator and its prey and behavioral reciprocity has received more attention than morphological reciprocity (Abrams 1992;van Baalen and Sabelis 1993;Adler and Grünbaum 1999;Kokko and Ruxton 2000;Abrams 2007;Krivan 2007;Krivan et al 2008;Mougi and Nishimura 2008b; but see Mougi and Kishida 2009).…”

What can aquatic gastropods tell us about phenotypic plasticity? A review and meta-analysis

“…Plastic shell responses are not limited to shell thickening via increased calcium carbonate deposition, and both marine and freshwater gastropods are capable of plastically altering different aspects of their shell shape (for example, aspect ratio; DeWitt, 1998;Hollander et al, 2006;Bourdeau, 2009). Altering shell shape may not require additional investment in shell deposition, just re-allocation of shell material to different shell locations, which could allow for the development of adaptive shell forms without the necessity for increased shell deposition in calcium-limited habitats.…”

“…Soft-bottom taxa are mostly absent (but see Martín-Mora et al, 1995 andDelgado et al, 2002 for examples of a species found on both rocky and softbottom substrates), as are studies involving predators that use methods other than shell breakage (but see Bourdeau, 2009 for exceptions). It is possible that gastropods living in softsediment habitats or those preyed on mainly by slow-moving shellentry predators (for example, seastars) may rely chiefly on plastic avoidance and/or escape behaviour as their antipredator defense, rather than plastic morphological defenses.…”

“…These plastic responses appear ubiquitous; they have been found in multiple species (for example, Appleton and Palmer, 1988;Palmer, 1990;Trussell, 1996;DeWitt, 1998;Hoverman et al, 2005;Hollander et al, 2006;Bourdeau, 2009;Brönmark et al, 2011), in species with different dispersal capabilities (for example, Behrens Yamada, 1989;Hollander et al, 2006), from different geographic locations (for example, Trussell, 2000a, b;Trussell and Smith, 2000) and in response to several predator species (for example, Hoverman and Relyea, 2007;Bourdeau, 2009). However, populations and species often differ in their degree of shell plasticity (for example, Appleton and Palmer, 1988;Palmer, 1990;Trussell, 1996;Edgell and Neufeld, 2008;Bourdeau, 2012).…”