Skip to main content

Advertisement

SpringerLink
Log in

A gastropod’s induced behavioral and morphological responses to invasive Carcinus maenas in Australia indicate a lack of novelty advantage

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

Evolution has afforded many organisms the capacity to recognize predation threats and respond accordingly with behavioral and morphological defenses. Biological invasions may obviate these coevolved recognition systems resulting in biological interactions with native species that range from novelty advantages to disadvantages for the introduced species. Predator recognition initiates responses that can affect other community members through trait-mediated indirect interactions. In this study we use the Australian invasion of a marine, predatory crab (Carcinus maenas) to determine if populations of a native whelk (Haustrum vinosum) with different histories of Carcinus invasion (no previous exposure, 20 years of exposure and 100 years of exposure) recognize and respond to the introduced crab. Haustrum were subsampled from invaded and uninvaded populations then monitored for foraging behavior, shell growth and tissue growth while maintained in a common garden setting with and without waterborne cues from Carcinus. We found that both invaded and uninvaded populations of Haustrum recognize and respond to Carcinus by reducing shell growth and foraging. In feeding experiments, Carcinus showed a preference for small whelks but not thin-shelled whelks. Our results suggest that introduced populations of Carcinus in Australia do not benefit from a novelty advantage and that the induced morphological changes in Haustrum are not a defense, per se. Haustrum’s induced behavioral response to Carcinus may be more important in reducing predation than morphological defenses, and further propagate the invasive crab’s impacts.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Ahyong S (2005) Range extension of two invasive crab species in eastern Australia: Carcinus maenas (Linnaeus) and Pyromaia tuberculata (Lockington). Mar Pollut Bull 50:460–462

    Article  PubMed  CAS  Google Scholar 

  • Aschaffenburg M (2008) Different crab species influence feeding of the snail Nucella lapillus through trait-mediated indirect interactions. Marine Ecol Evol Perspect 29:348–353

    Google Scholar 

  • Bourdeau P (2011) Constitutive and inducible defensive traits in co-occurring marine snails distributed across a vertical rocky intertidal gradient. Funct Ecol 25:177–185

    Article  Google Scholar 

  • Brookes J, Rochette R (2007) Mechanism of a plastic phenotypic response: predator-induced shell thickening in the intertidal gastropod Littorina obtusata. J Evol Biol 20:1015–1027

    Article  PubMed  CAS  Google Scholar 

  • Brown K, Quinn J (1988) The effect of wave action on growth in three species of intertidal gastropods. Oecologia 75:420–425

    Article  Google Scholar 

  • Burrows M, Hughes R (1990) Variation in growth and consumption among individuals and populations of dogwhelks, Nucella lapillus: a link between foraging behaviour and fitness. J Anim Ecol 59:723–742

    Article  Google Scholar 

  • Burrows M, Hughes R (1991) Variation in foraging behavior among individuals and populations of dog whelks Nucella lapillus Natural constraints on energy intake. J Anim Ecol 60:497–514

    Article  Google Scholar 

  • Carlton J, Cohen A (2003) Episodic global dispersal in shallow water marine organisms: the case history of the European shore crabs Carcinus maenas and C. aesuaraii. J Biogeogr 30:1809–1820

    Article  Google Scholar 

  • Case T, Bolger D (1991) The role of introduced species in shaping the distribution and abundance of island reptiles. Evol Ecol 5:272–290

    Article  Google Scholar 

  • Cox G (2004) Alien species and evolution. Island Press, Washington

    Google Scholar 

  • Cox J, Lima S (2006) Naivete and an aquatic-terrestrial dichotomy in the effects of introduced predators. Trends Ecol Evol 21:674–680

    Article  PubMed  Google Scholar 

  • Edgell T (2010) 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

    Article  Google Scholar 

  • Edgell T, Neufeld C (2008) Experimental evidence for latent developmental plasticity: intertidal whelks respond to a native but not an introduced predator. Biol Lett 4:385–387

    Article  PubMed  Google Scholar 

  • Edgell T, Lynch B, Trussell G, Palmer R (2009) Experimental evidence for the rapid evolution of behavioral canalization in natural populations. Am Nat 174:434–440

    Article  PubMed  Google Scholar 

  • Etter R (1988a) Asymmetrical developmental plasticity in an intertidal snail. Evolution 42:322–334

    Article  Google Scholar 

  • Etter R (1988b) Physiological stress and color polymorphism in the intertidal snail Nucella lapillus. Evolution 42:660–680

    Article  Google Scholar 

  • Etter R (1989) Life-history variation in the intertidal snail Nucella lapillus across a wave-exposure gradient. Ecology 70:1857–1876

    Article  Google Scholar 

  • Freeman A (2007) Specificity of induced defenses in Mytilus edulis and asymmetrical predator deterrence. Mar Ecol Prog Ser 334:145–153

    Article  Google Scholar 

  • Freeman A, Byers J (2006) Divergent induced responses to an invasive predator in marine mussel populations. Science 313:831–833

    Article  PubMed  CAS  Google Scholar 

  • Freeman A, Hamer C (2009) The persistent effect of wave exposure on TMIIs and crab predation in Nucella lapillus. J Exp Mar Biol Ecol 372:58–63

    Article  Google Scholar 

  • Glude J (1954) The effects of temperature and predators on the abundance of the soft-shell clam, Mya arenaria, in New England. Trans Am Fish Soc 84:13–26

    Article  Google Scholar 

  • Hughes R, Elner R (1979) Tactics of a predator, Carcinus maenas, and morphological responses of the prey, Nucella lapillus. J Anim Ecol 48:65–78

    Article  Google Scholar 

  • Langkilde T (2009) Invasive fire ants alter behavior and morphology of native lizards. Ecology 90:208–217

    Article  PubMed  Google Scholar 

  • Large S, Smee D (2010) Type and nature of cues used by Nucella lapillus to evaluate predation risk. J Exp Mar Biol Ecol 396:10–17

    Article  Google Scholar 

  • Large S, Smee D, Trussell G (2011) Environmental conditions influence the frequency of prey responses to predation risk. Mar Ecol Prog Ser 422:41–49

    Article  Google Scholar 

  • Leonard G, Bertness M, Yund P (1999) Crab predation, waterborne cues, and inducible defenses in the blue mussel, Mytilus edulis. Ecology 80:1–14

    Google Scholar 

  • Marko P, Palmer A (1991) Responses of a rocky shore gastropod to the effluents of predatory and non-predatory crabs avoidance and attraction. Biol Bull 181:363–370

    Article  Google Scholar 

  • Palmer A (1982) Growth in marine gastropods: a non-destructive technique for independently measuring shell and body weight. Malacologia 23:63–73

    Google Scholar 

  • Palmer A (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

    Article  Google Scholar 

  • Parker J, Burkepile D, Hay M (2006) Opposing effects of native and exotic herbivores on plant invasions. Science 311:1459–1461

    Article  PubMed  CAS  Google Scholar 

  • Phillips B, Shine R (2004) Adapting to an invasive species: toxic cane toads induce morphological change in Australian snakes. Proc Natl Acad Sci USA 101:17150–17155

    Article  PubMed  CAS  Google Scholar 

  • Rehage J, Dunlop K, Loftus W (2009) Antipredator responses by native mosquitofish to non-native cichlids: an examination of the role of prey naivete. Ethology 115:1–11

    Article  Google Scholar 

  • Relyea R (2001) Morphological and behavioral plasticity of larval anurans in response to different predators. Ecology 82:523–540

    Article  Google Scholar 

  • Rochette R, Doyle S, Edgell T (2007) Interaction between an invasive decapod and a native gastropod: predator foraging tactics and prey architectural defenses. Mar Ecol Prog Ser 330:179–188

    Article  Google Scholar 

  • Ross D, Johnson C, Hewitt C, Ruiz G (2004) Interaction and impacts of two introduced species on a soft-sediment marine assemblage in SE Tasmania. Mar Biol 144:747–756

    Article  Google Scholar 

  • Sanford E, Worth D (2009) Genetic differences among populations of a marine snail drive geographic variation in predation. Ecology 90:3108–3118

    Article  PubMed  Google Scholar 

  • Sax D, Stachowicz J, Brown J et al (2007) Ecological and evolutionary insights from species invasions. Trends Ecol Evol 22:465–471

    Article  PubMed  Google Scholar 

  • Schmitz O, Vlastimil K, Ovadia O (2004) Trophic cascades: the primacy of trait-mediated indirect interactions. Ecol Lett 7:153–163

    Article  Google Scholar 

  • Seeley R (1986) Intense natural selection caused a rapid morphological transition in a living marine snail. Proc Natl Acad Sci 83:6897–6901

    Article  PubMed  CAS  Google Scholar 

  • Sharples C (2006) Indicative mapping of tasmanian coastal vulnerability to climate change and sea level rise: explanatory report and maps. Consultant report to Department of Primary Industries and Water, 2nd ed, Tasmania, Hobart

  • Sih A, Bolnick D, Luttbeg B et al (2010) Predator–prey naïveté, antipredator behavior, and the ecology of predator invasions. Oikos 119:610–621

    Article  Google Scholar 

  • Smee D, Weissburg M (2006) Clamming up: environmental forces diminish the perceptive ability of bivalve prey. Ecology 87:1587–1598

    Article  PubMed  Google Scholar 

  • Strauss S, Lau J, Carroll S (2006) Evolutionary responses of natives to introduced species: what do introductions tell us about natural communities? Ecol Lett 9:357–374

    Article  PubMed  Google Scholar 

  • Tanner J (2007) The influence of introduced European green crabs (Carcinus maenas) on habitat selection by juvenile native blue crabs (Portunus pelagicus). Estuaries Coasts 30:601–606

    Google Scholar 

  • Thresher R, Proctor C, Ruiz G et al (2003) Invasion dynamics of the European shore crab, Carcinus maenas, in Australia. Mar Biol 142:867–876

    Google Scholar 

  • Trussell G (2000a) Predator-induced plasticity and morphological trade-offs in latitudinally separated populations of Littorina obtusata. Evol Ecol Res 2:803–822

    Google Scholar 

  • Trussell G (2000b) Phenotypic clines, plasticity, and morphological trade-offs in an intertidal snail. Evolution 54:151–166

    PubMed  CAS  Google Scholar 

  • Trussell G (2002) Evidence of countergradient variation in the growth of an intertidal snail in response to water velocity. Mar Ecol Prog Ser 243:123–131

    Article  Google Scholar 

  • Trussell G, Nicklin M (2002) Cue sensitivity, inducible defense, and trade-offs in a marine snail. Ecology 83:1635–1647

    Article  Google Scholar 

  • Trussell G, Smith L (2000) Induced defenses in response to an invading crab predator: an explanation of historical and geographic phenotypic change. Proc Natl Acad Sci USA 97:2123–2127

    Article  PubMed  CAS  Google Scholar 

  • Trussell G, Ewanchuk P, Bertness M (2003) Trait-mediated effects in rocky intertidal food chains: predator risk cues alter prey feeding rates. Ecology 84:629–640

    Article  Google Scholar 

  • Trussell G, Ewanchuk P, Bertness M, Silliman B (2004) Trophic cascades in rocky shore tide pools: distinguishing lethal and nonlethal effects. Oecologia 139:427–432

    Article  PubMed  Google Scholar 

  • Trussell G, Ewanchuk P, Matassa C (2006a) The fear of being eaten reduces energy transfer in a simple food chain. Ecology 87:2979–2984

    Article  PubMed  Google Scholar 

  • Trussell G, Ewanchuk P, Matassa C (2006b) Habitat effects on the relative importance of trait- and density-mediated indirect interactions. Ecol Lett 9:1245–1252

    Article  PubMed  Google Scholar 

  • Vadas R Sr, Burrows M, Hughes R (1994) Foraging strategies of dogwhelks, Nucella lapillus (L.): interacting effects of age, diet and chemical cues to the threat of predation. Oecologia 100:439–450

    Article  Google Scholar 

  • Van Buskirk J (2000) The costs of an inducible defense in anuran larvae. Ecology 81:2813–2821

    Article  Google Scholar 

  • Van Buskirk J (2002) Phenotypic lability and the evolution of predator-induced plasticity in tadpoles. Evolution 56:361–370

    PubMed  Google Scholar 

  • Vermeij G (1982) Phenotypic evolution in a poorly dispersing snail after arrival of a predator. Nature 299:349–350

    Article  Google Scholar 

  • Walton W, MacKinnon C, Rodriguez L et al (2002) Effect of an invasive crab upon a marine fishery: Green crab, Carcinus maenas, predation upon a venerid clam, Katelysia scalarina, in Tasmania (Australia). J Exp Mar Biol Ecol 272:171–189

    Article  Google Scholar 

  • Whitlow W (2010) Changes in survivorship, behavior, and morphology in native soft-shell clams induced by invasive green crab predators. Mar Ecol 31:418–430

    Google Scholar 

Download references

Acknowledgments

Support was provided by an ARCIF grant to J.W., A.F., C.H. and M.C. In-kind support and facilities were provided by AMC/UTas, Launceston. Fellowship support was provided by UNH SURF to K.S. Valuable assistance was provided by I. Jermyn, L. Gregory, S. Partridge, J. Strugarek, and A. Tyson.

Author information

Authors and Affiliations

  1. Biology Department, Adelphi University, Garden City, NY, 11530, USA

    Aaren S. Freeman

  2. Australian Maritime College, University of Tasmania, Launceston, TAS, 7248, Australia

    Aaren S. Freeman, Jeffrey T. Wright, Chad L. Hewitt & Marnie L. Campbell

  3. Central Queensland University, Gladstone, QLD, 4680, Australia

    Chad L. Hewitt & Marnie L. Campbell

  4. Massachusetts College of Pharmacy and Health Sciences, Manchester, NH, 03104, USA

    Kaylene Szeto

Authors
  1. Aaren S. Freeman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jeffrey T. Wright
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chad L. Hewitt
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marnie L. Campbell
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kaylene Szeto
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Aaren S. Freeman.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 18 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Freeman, A.S., Wright, J.T., Hewitt, C.L. et al. A gastropod’s induced behavioral and morphological responses to invasive Carcinus maenas in Australia indicate a lack of novelty advantage. Biol Invasions 15, 1795–1805 (2013). https://doi.org/10.1007/s10530-013-0409-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-013-0409-z

Keywords

Search

Navigation