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Variability in the motion behaviour of intertidal gastropods: ecological and evolutionary perspectives

Published online by Cambridge University Press:  20 April 2010

Coraline Chapperon*
Affiliation:
School of Biological Sciences, Flinders University, GPO Box 2100, Adelaide SA 5001, Australia
Laurent Seuront
Affiliation:
School of Biological Sciences, Flinders University, GPO Box 2100, Adelaide SA 5001, Australia South Australian Research and Development Institute, Aquatic Sciences, West Beach SA 5022, Australia Center for Polymer Studies, Department of Physics, Boston University, 590 Commonwealth Avenue, Boston, MA 02215, USA
*
Correspondence should be addressed to: C. Chapperon, School of Biological Sciences, Flinders University, GPO BOX 2100, Adelaide SA5001, Australia email: [email protected]

Abstract

The variability in motion behaviour properties was investigated for three species of intertidal gastropods at the inter-specific, inter-individual and individual levels in the absence of abiotic and biotic cues. Interspecific differences in movement patterns were reminiscent of the optimal searching behaviours expected for Austrocochlea porcata, Nerita atramentosa and Bembicium melanostomum in their natural environment. Specifically, N. atramentosa, A. porcata and B. melanostomum respectively displayed extensive and intensive foraging strategies consistent with their feeding ecology. The related inter-individual variability within each species highlights the potential ability of species to adapt their movement patterns to new environmental conditions and to persist over long-term changes. Finally, the strong variability observed in the speed and turning angle of individuals of the three species and the resulting behavioural plasticity may be an adaptive strategy to optimize energy expenditure and to react to an environmental fluctuation. Specifically, it is suggested that the lack of significant differences in individual behavioural variability between the three species indicates that despite clear inter-specific differences in motion behaviour, at the individual level A. porcata, N. atramentosa and B. melanostomum have similar abilities to face environmental fluctuations. This work stresses that individual variability in the motion behaviour of intertidal gastropods constitutes a fundamental evolutionary advantage when facing heterogeneous environmental conditions.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2010

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References

REFERENCES

Bazterrica, M.C., Silliman, B.R., Hidalgo, F.J., Crain, C.M. and Bertness, M.D. (2007) Limpet grazing on a physically stressful Patagonian rocky shore. Journal of Experimental Marine Biology and Ecology 353, 2234.CrossRefGoogle Scholar
Bell, W.J. (1991) Searching behaviour. The behavioural ecology of finding resources. Animal Behaviour Series. New York: Chapman and Hall.Google Scholar
Bennett, A.F. and Huey, R.B. (1990) Studying the evolution of physiological performance. In Futuyma, D.J. and Antonovics, J. (eds) Oxford surveys in evolutionary biology. Oxford: Oxford University Press, pp. 251284.Google Scholar
Bergman, C.M., Schaefer, J.A. and Luttich, S.N. (2000) Caribou movement as a correlated random walk. Oecologia 123, 364374.CrossRefGoogle ScholarPubMed
Bolnick, D.I. (2001) Intraspecific competition favours niche width expansion in Drosophila melanogaster. Nature 410, 463466.CrossRefGoogle ScholarPubMed
Byers, J.E. (2000) Effects of body size and resource availability on dispersal in a native and a non-native estuarine snail. Journal of Experimental Marine Biology and Ecology 248, 133150.CrossRefGoogle Scholar
Byers, J.E. (2001) Correlated random walk equations of animal dispersal resolved by simulation. Ecology 82, 16801690.Google Scholar
Chapperon, C. and Seuront, L. (2009) Cue synergy in Littorina littorea navigation following wave dislodgement. Journal of the Marine Biological Association of the United Kingdom 89, 12251228.CrossRefGoogle Scholar
Chapman, M.G. (2000a) Poor design of behavioural experiments gets poor results: examples from intertidal habitats. Journal of Experimental Marine Biology and Ecology 250, 7795.CrossRefGoogle ScholarPubMed
Chapman, M.G. (2000b) A comparative study of differences among species and patches of habitat on movements of three species of intertidal gastropods. Journal of Experimental Marine Biology and Ecology 244, 181201.CrossRefGoogle Scholar
Craig, T.P., Itami, J.K., Shantz, C., Abrahamson, W.G., Horner, J.D. and Craig, J.V. (2000) The influence of host plant variation and intraspecific competition on oviposition preference and offspring performance in the host races of Eurosta solidaginis. Ecological Entomology 25, 718.CrossRefGoogle Scholar
Davidson, I.C., Crook, C. and Barnes, D.K.A. (2004) Quantifying spatial patterns of intertidal biodiversity: is movement important? Marine Ecology 25, 1534.Google Scholar
Denny, M. (1980a) Locomotion: the cost of gastropod crawling. Science 208, 12881290.Google Scholar
Denny, M. (1980b) The role of gastropod pedal mucus in locomotion. Nature 285, 160161.CrossRefGoogle Scholar
Dix, T.L. and Hamilton, P.V. (1993) Chemically mediated escape behavior in the marsh periwinkle Littoraria irrorata Say. Journal of Experimental Marine Biology and Ecology 166, 135149.CrossRefGoogle Scholar
Edgar, G.J. (1997) Australian marine life: the plants and animals of temperate waters. Melbourne: Reed Books.Google Scholar
Edwards, M. and Davies, M.S. (2002) Functional and ecological aspects of the mucus trails of the intertidal prosobranch gastropod Littorina littorea. Marine Ecology Progress Series 239, 129137.CrossRefGoogle Scholar
Erlandsson, J. and Kostylev, V. (1995) Trail following, speed and fractal dimension of movement in a marine prosobranch, Littorina littorea, during a mating and a non-mating season. Marine Biology 122, 8794.Google Scholar
Fausch, K.D. (1998) Interspecific competition and juvenile Atlantic salmon (Salmo salar): on testing effects and evaluating the evidence across scales. Canadian Journal of Fisheries and Aquatic Sciences 55, 218231.CrossRefGoogle Scholar
Fernandes, T.F., Huxham, M. and Piper, S.R. (1999) Predator caging experiments: a test of the importance of scale. Journal of Experimental Marine Biology and Ecology 241, 137154.CrossRefGoogle Scholar
Haynes, K.J. and Cronin, J.T. (2006) Interpatch movement and edge effect: the role of behavioural responses to the landscape matrix. Oikos 113, 4354.CrossRefGoogle Scholar
Helmuth, B. and Denny, M.W. (2003) Predicting wave exposure in the rocky intertidal zone: do bigger waves always lead to larger forces? Limnology and Oceanography 48, 13381345.CrossRefGoogle Scholar
Hugues, R.N. (1980) Optimal foraging theory in the marine context. Oceanography and Marine Biology: an Annual Review 18, 423481.Google Scholar
Jerde, C.L. and Visscher, D.R. (2005) GPS measurement error influences on movement model parameterization. Ecological Applications 15, 806810.Google Scholar
Keppel, E. and Scrosati, R. (2004) Chemically mediated avoidance of Hemigrapsus nudus (Crustacea) by Littorina scutulata (Gastropoda): effects of species coexistence and variable cues. Animal Behaviour 68, 915920.Google Scholar
Kerr, B., Riley, M.A., Feldman, M.W. and Bohannan, B.J.M. (2002) Local dispersal promotes biodiversity in a real-life game of rock–paper–scissors. Nature 418, 171174.CrossRefGoogle Scholar
Klaassen, R.H.G., Nolet, B.A., Van Gils, J.A. and Bauer, S. (2006) Optimal movement between patches under incomplete information about the spatial distribution of food items. Theoretical Population Biology 70, 452463.Google Scholar
Laidre, K.L., Heide-Jørgensen, M.P., Logsdon, M.L., Hobbs, R.C., Dietz, R. and VanBlaricom, G.R. (2004) Fractal analysis of narwhal space use patterns. Zoology 107, 311.Google Scholar
Lauga, E. and Hosoi, A.E. (2006) Tuning gastropod locomotion: modeling the influence of mucus rheology on the cost of crawling. Physics of Fluids 18, 112.CrossRefGoogle Scholar
Lima, S.L. (2002) Putting predators back into behavioral predator-prey interactions. Trends in Ecology and Evolution 17, 7075.CrossRefGoogle Scholar
Morales, J.M. and Ellner, S.P. (2002) Scaling up animal movements in heterogeneous landscapes: the importance of behaviour. Ecology 83, 22402247.CrossRefGoogle Scholar
Nams, V.O. (2005) Using animal movement paths to measure response to spatial scale. Oecologia 143, 179188.CrossRefGoogle ScholarPubMed
Pardo, L.M. and Johnson, L.E. (2004) Activity and shelter use of an intertidal snail: effects of sex, reproductive condition and tidal cycle. Journal of Experimental Marine Biology and Ecology 301, 175191.CrossRefGoogle Scholar
Pardo, L.M. and Johnson, L.E. (2006) Influence of water motion and reproductive attributes on movement and shelter use in the marine snail Littorina saxatilis. Marine Ecology Progress Series 315, 177186.Google Scholar
Petraitis, P.S. (1982) Occurrence of random and directional movements in the periwinkle, Littorina littorea. Journal of Experimental Marine Biology and Ecology 59, 207217.Google Scholar
Pyke, G.H. (1984) Optimal foraging theory: a critical review. Annual Review of Ecology and Systematics 15, 523575.Google Scholar
Przeslawski, R. and Davis, A.R. (2007) Does spawning behavior minimize exposure to environmental stressors for encapsulated gastropod embryos on rocky shores? Marine Biology 152, 9911002.CrossRefGoogle Scholar
Quinn, G.P. and Ryan, N.R. (1989) Competitive interactions between two species of intertidal herbivorous gastropods from Victoria, Australia. Journal of Experimental Marine Biology and Ecology 125, 112.Google Scholar
Rajasekharan, M. and Crowe, T.P. (2007) Intrinsic differences in dispersal between populations of gastropods separated by a few metres: evidence from reciprocal experimental transplantation. Journal of Experimental Marine Biology and Ecology 341, 264273.Google Scholar
Ríos-Jara, E., Cedillo, C.C.H., Carrillo, E.J. and Padilla, I.E. (2004) Variations in density, shell-size and growth with shore height and wave exposure of the rocky intertidal snail, Calyptraea spirata (Forbes, 1852), in the tropical Mexican Pacific. Journal of Shellfish Research 23, 545552.Google Scholar
Rossetti, Y. and Cabanac, M. (2006) Light versus temperature: an intersensitivity conflict in a gastropod (Lymnaea auricularia). Journal of Thermal Biology 31, 514520.CrossRefGoogle Scholar
Seuront, L. and Leterme, C. (2006) Microscale patchiness in microphytobenthos distributions: evidence for a critical state. In Kromkamp, J.C., de Brouwer, J., Blanchard, G.F., Forster, R.M. and Créach, V. (eds) Functioning of microphytobenthos in estuaries. The Academy of Arts and Sciences, Amsterdam/The University of Chicago Press, Chicago, pp. 165183.Google Scholar
Seuront, L., Duponchel, A.C. and Chapperon, C. (2007) Heavy-tailed distributions in the intermittent motion behaviour of the intertidal gastropod Littorina littorea (Linnaeus). Physica A 385, 573582.Google Scholar
Seuront, L. and Spilmont, N. (2002) Self-organized criticality in intertidal microphytobenthos patch patterns. Physica A 313, 513539.Google Scholar
Seuront, L., Hwang, J.-S., Tseng, L.-C., Schmitt, F.G., Souissi, S. and Wong, C.-K. (2004) Individual variability in the swimming behavior of the sub-tropical copepod Oncaea venusta (Copepoda: Poecilostomatoida). Marine Ecology Progress Series 283, 199217.Google Scholar
Stafford, R. and Davies, M.S. (2005) Spatial patchiness of epilithic biofilm caused by refuge-inhabiting high shore gastropods. Hydrobiologia 545, 279287.Google Scholar
Tews, J., Brose, U., Grimm, V., Tielbörger, K., Wichmann, M.C., Schwager, M. and Jeltsch, F. (2004) Animal species diversity driven by habitat heterogeneity/diversity: the importance of keystone structures. Journal of Biogeography 31, 7992.CrossRefGoogle Scholar
Tilman, D. (1994) Competition and biodiversity in spatially structured habitats. Ecology 75, 216.Google Scholar
Turner, A.M., Turner, S.E. and Lappi, H.M. (2006) Learning, memory and predator avoidance by freshwater snails: effects of experience on predator recognition and defensive strategy. Animal Behaviour 72, 14431450.CrossRefGoogle Scholar
Underwood, A.J. (1977) Movements of intertidal gastropods. Journal of Experimental Marine Biology and Ecology 26, 191201.Google Scholar
Underwood, A.J. (1978) An experimental evaluation of competition between three species of intertidal prosobranch gastropods. Oecologia 33, 185202.Google Scholar
Underwood, A.J. and Chapman, M.G. (2000) Variation in abundances of intertidal populations: consequences of extremities of environment. Hydrobiologia 426, 2536.CrossRefGoogle Scholar
Vásquez, A., Ebensperger, L.A. and Bozinovic, F. (2002) The influence of habitat on travel speed, intermittent locomotion, and vigilance in a diurnal rodent. Behavioural Ecology 13, 182187.CrossRefGoogle Scholar
Zar, J.H. (1996) Biostatistical analysis. Upper Saddle River, NJ: Prentice Hall.Google Scholar