Abstract
Unless sensory control is coupled with developmental flexibility, organisms are unable to produce adaptive phenotypes in response to environmental risk cues. However, empirical examples of adaptive phenotypic plasticity focus largely on development and rarely on sensory control. Here, I ask whether past exposure to predation cues affects an intertidal whelk’s (Nucella lamellosa) sensitivity to the scent of a known predatory crab (Cancer productus). I pre-conditioned whelks for 30 days with the smell of crabs eating other whelks and then, after a period of rest (14 days in fresh seawater free of predator effluent), re-introduced them to different concentrations of waterborne crab scent. Relative to controls, pre-conditioned whelks expressed crab-defences at significantly lower concentrations of crab effluent, suggesting the pre-conditioning reduced their risk–response threshold. Results remind us that the full scope of factors controlling adaptive phenotypic plasticity in natural populations remains underappreciated.
This is a preview of subscription content, log in via an institution to check access.
References
Agrawal AA (2001) Phenotypic plasticity in the interaction and evolution of species. Science 294:321–326
Appleton RD, Palmer AR (1988) Water-borne stimuli released by predatory crabs and damaged prey induce more predator-resistant shells in a marine gastropod. Proc Nat Acad Sci USA 85:4387–4391
Davis M, Falls WA, Campeau S, Kim M (1993) Fear-potentiated startle: a neural and pharmacological analysis. Behav Brain Res 58:175–198
Edgell TC, Neufeld CJ (2008) Experimental evidence for latent developmental plasticity: intertidal whelks respond to a native but not an introduced predator. Biol Lett 4:385–387
Edgell TC, Lynch BR, Trussell GC, Palmer AR (2009) Experimental evidence for the rapid evolution of behavioral canalization in natural populations. Am Nat 174(3):434–440
Freeman AS, Byers JE (2006) Divergent induced responses to an invasive predator in marine mussel populations. Science 313:831–833
Globisch J, Hamm AO, Esteves F, Ohman A (1999) Fear appears fast: temporal course of startle reflex potentiation in animal fearful subjects. Psychophysiology 36:66–75
Grillon C, Ameli R, Woods SW, Merikangas K, Davis M (1991) Fear-potentiated startle in humans: Effects of anticipatory anxiety on the acoustic blink reflex. Psychophysiology 28:588–595
Hendrix LJ, Carter MW, Scott DT (1982) Covariance analyses with heterogeneity of slopes in fixed models. Biometrics 38:641–650
Lang PJ, Davis M, Ohman A (2000) Fear and anxiety: animal models and human cognitive psychophysiology. J Aff Disorders 61:137–159
Li W, Howard JD, Gottfried TB (2008) Aversive learning enhances perceptual and cortical discrimination of indiscriminable odor cues. Science 319:1842–1845
Lukowiak K, Martens K, Rosenegger D, Browning K, de Caigny P, Orr M (2008) The perception of stress alters adaptive behaviours in Lymnaea stagnalis. J Exp Biol 211:1747–1756
McGuinness KA (2002) Of rowing boats, ocean liners and tests of the ANOVA homogeneity of variance assumption. Aus Ecol 27:681–688
Orr MV, Hittel K, Lukowiak K (2008) Comparing memory-forming capabilities between laboratory-reared and wild Lymnaea: learning in the wild, a heritable component of snail memory. J Exp Biol 211:2807–2816
Orr MV, Hittel K, Lukowiak K (2009) Different strokes for different folks’: geographically isolated strains of Lymnaea stagnalis only respond to sympatric predators and have different memory forming capabilities. J Exp Biol 212:2237–2247
Palmer AR (1982) Growth in marine gastropods: a non-destructive technique for independently measuring shell and body weight. Malacologia 23:63–73
Palmer AR (1990) Effect of crab effluent and scent of damaged conspecifics on feeding, growth, and shell morphology of the Atlantic dogwhelk Nucella lapillus (L.). Hydrobiologia 193:155–182
Price TD, Qvarnstrom A, Irwin DE (2003) The role of phenotypic plasticity in driving genetic evolution. Proc Roy Soc Lond B 270:1433–1440
Scheiner SM (1993) Genetics and evolution of phenotypic plasticity. Ann Rev Ecol Syst 24:35–68
Schmitz OJ (2008) Effects of predator hunting mode on grassland ecosystem function. Science 319:952–954
Sultan SE (2007) Development in context: the timely emergence of eco-devo. Trends Ecol Evol 22:575–582
Trussell GC, Smith LD (2000) Induced defenses in response to an invading crab predator: an explanation of historical and geographic phenotypic change. Proc Nat Acad Sci USA 97:2123–2127
Trussell GC, Ewanchuk PJ, Matassa CM (2006a) Habitat effects on the relative importance of trait- and density-mediated indirect interactions. Ecol Lett 11:1245–1252
Trussell GC, Ewanchuk PJ, Mattassa CM (2006b) The fear of being eaten reduces energy transfer in a simple food chain. Ecology 87:2979–2984
West-Eberhard MJ (2005) Developmental plasticity and the origin of species differences. Proc Nat Acad Sci USA 102:6543–6549
Acknowledgments
Thanks to A. Richard Palmer for helpful discussion and funding and to the helpful staff at the Bamfield Marine Sciences Centre for logistical support (esp. Bruce Cameron). This article was improved by critique from two anonymous reviewers, thanks. Specimen collections and experiments were funded by a Natural Sciences and Engineering Research Council (Canada) Discovery Grant A7245 to A. R. Palmer; writing was funded by LGL Ltd. environmental research associates.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by F. Bulleri.
Rights and permissions
About this article
Cite this article
Edgell, T.C. Past predation risk induces an intertidal whelk (Nucella lamellosa) to respond to more dilute concentrations of its predator’s scent. Mar Biol 157, 215–219 (2010). https://doi.org/10.1007/s00227-009-1303-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-009-1303-1