Cue specificity of predator-induced phenotype in a marine snail: is a crab just a crab?
A wide range of taxa have been shown to display inducible, phenotypically plastic responses to known predators. Most studies of inducible defenses include only known predators but not non-predatory species in experimental designs, precluding tests of specificity for these responses. We tested the specificity of predator-induced defenses in the marine snail Nucella lamellosa, when exposed to chemical cues from potential crab predators as well as more distantly related non-predatory crabs that co-occur with this snail. Surprisingly, all crabs tested, even those that are not predators, triggered the common induced response of a reduction of soft-tissue mass relative to control animals, likely reflecting a reduction in snail feeding activity. In contrast, only N. lamellosa’s major predator, Cancer productus, triggered the production of a thicker apertural lip. Increased thickening of the apertural lip may be an adaptive response specific to C. productus, which uses shell-breaking at the apertural lip (i.e., shell-peeling) as their main form of attack. Apertural lip thickening appeared to be due to reallocation of shell material (i.e., a change in shell shape) rather than an increase in shell deposition. Our findings demonstrate the importance of determining the specificity of cues triggering inducible responses in prey, and the mechanisms that underlie these plastic responses, as the responses to general versus specific cues may limit the adaptive value of an inducible defense.
We thank the director and staff of Friday Harbor Laboratories for logistical support, M. Mach for help monitoring the experiment and drawing the snail in Fig. 1, and M. Dethier for graciously surrendering lab space to accommodate the experiment. G. Trussell and 2 anonymous reviewers provided constructive criticism on earlier versions of the manuscript. This is contribution number 1254 from the Department of Ecology and Evolution at Stony Brook University. The experiments comply with the current laws of the country in which they were performed.
PEB conceived, designed, and performed the experiment, and analyzed the data. PEB and DKP wrote and edited the manuscript.
A Stephen and Ruth Wainwright Fellowship supported PEB. DKP was supported by NSF IOS 0920032 during the writing of this paper and acknowledges the Helen C. Whitley Center at the Friday Harbor Laboratories.
Compliance with ethical standards
Conflict of interest
The authors declare no conflict of interest.
All applicable international, national, and institutional guidelines for sampling, care, and experimental use of organisms for the study were followed. Research was completed under permits from the Washington Department of Fish and Wildlife (WDFW).
- DeWitt TJ, Robinson BW, Wilson DS (2000) Functional diversity among predators of a freshwater snail imposes an adaptive trade-off for shell morphology. Evol Ecol Res 2:129–148Google Scholar
- Huitema BE (1980) The analysis of covariance and alternatives. Wiley, New YorkGoogle Scholar
- Jensen GC (1995) Pacific Coast crabs and shrimps. Sea Challengers, MontereyGoogle Scholar
- Kozloff EN (1987) Marine invertebrates of the Pacific Northwest. University of Washington Press, SeattleGoogle Scholar
- Langerhans RB, DeWitt TJ (2002) Plasticity constrained: over-generalized induction cues cause maladaptive phenotypes. Evol Ecol Res 4:857–870Google Scholar
- Levins R (1968) Evolution in changing environments. Princeton University Press, PrincetonGoogle Scholar
- Padilla DK, Savedo MM (2013) A systematic review of phenotypic plasticity in marine invertebrate and plant systems. In: Advances in marine biology, vol 65. Academic Press, pp 67–94Google Scholar
- Palmer AR (1982) Growth in marine gastropods—a non-destructive technique for independently measuring shell and body-weight. Malacologia 23:63–73Google Scholar
- Quinn GP, Keough MJ (2002) Experimental design and data analysis. Cambridge University Press, New YorkGoogle Scholar
- R Development Core Team, RFFSC (2011) R: a language and environment for statistical computingGoogle Scholar
- Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research. State University of New York at Stony Brook, New YorkGoogle Scholar
- Tollrian R, Harvell CD (1999) The ecology and evolution of inducible defenses. Princeton University Press, PrincetonGoogle Scholar
- Vermeij GJ (1978) Biogeography and adaptation: patterns of marine life. Harvard University Press, CambridgeGoogle Scholar
- Vermeij GJ (1987) Evolution and escalation: an ecological history of life. Princeton University Press, PrincetonGoogle Scholar