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Temporal shifts in motion behaviour and habitat use in an intertidal gastropod

Published online by Cambridge University Press:  09 August 2012

Coraline Chapperon  and
Laurent Seuront
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 Centre National de la Recherche Scientifique, Laboratoire d'Océanologie et de Géosciences, UMR LOG 8187, Université des Sciences et Technologies de Lille, Station Marine, 62930 Wimereux, France
*
Correspondence should be addressed to: C. Chapperon, School of Biological Sciences, Flinders University, GPO Box 2100, Adelaide SA 5001, Australia email: [email protected]
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Abstract

Animal movements in heterogeneous environments shape most ecological processes from individuals to ecosystems. The identification of the processes underlying animal movements thus has critical implications in a wide range of fields. Changes in the motion behaviour of free-ranging species have mainly been reported across different spatial scales but have been less investigated over time. Here the processes potentially triggering temporal changes in movement, microhabitat occupation and distribution patterns of the intertidal herbivorous gastropod Nerita atramentosa were examined on a south Australian rocky shore during 8 successive daytime low tides considered in four different months. The observed temporal shift in microhabitat occupation and aggregation behaviour was likely an adaptation to both abiotic and biotic stressors such as temperature and food distribution. In contrast, the temporal changes observed in N. atramentosa motion behaviour are consistent with optimal foraging strategies driven by the presumed variability in both microalgal density and distribution. Individuals seemed to switch from an extensive foraging strategy in February and May to an intensive strategy in August and October. Specifically, N. atramentosa seemed to adopt two different foraging strategies, a Lévy-like foraging strategy in May and a ballistic foraging strategy in February when the resources are expected to be respectively non-depleted and depleted. The Brownian foraging strategy theoretically expected under high food density conditions was however not observed. The potential role of the behavioural flexibility observed in N. atramentosa motion behaviour is discussed in relation to the persistence of this species under disrupted environmental conditions.

Keywords

motionforaging behaviourLévy flightdistributionherbivorous snailsintertidal environment
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 93 , Issue 4 , June 2013 , pp. 1025 - 1034
Copyright
Copyright © Marine Biological Association of the United Kingdom 2012 

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References

REFERENCES

Agudo, R., Rico, C., Hiraldo, F. and Donázar, J.A. (2011) Evidence of connectivity between continental and differentiated insular populations in a highly mobile species. Diversity and Distributions 17, 1–12.CrossRefGoogle Scholar
Barahona, M. and Navarrete, S.A. (2010) Movement patterns of the seastar Heliaster helianthus in central Chile: relationship with environmental conditions and prey availability. Marine Biology 157, 647–661.CrossRefGoogle Scholar
Bartumeus, F. (2009) Behavioral intermittence, Lévy patterns, and randomness in animal movement. Oikos 118, 488–494.CrossRefGoogle Scholar
Bartumeus, F., Peters, F., Pueyo, S., Marrasé, C. and Catalan, J. (2003) Helical Lévy walks: adjusting searching statistics to resource availability in microzooplankton. Proceedings of the National Academy of Sciences of the United States of America 22, 12771–12775.CrossRefGoogle Scholar
Bates, T.W. and Hicks, D.W. (2005) Locomotory behavior and habitat selection in littoral gastropods on Caribbean limestone shores. Journal of Shellfish Research 24, 75–84.Google Scholar
Berger, E.A. and Weaver, J.E. (2004) The influence of crevice size on the protection of epilithic algae from grazers. Freshwater Biology 49, 1014–1025.CrossRefGoogle Scholar
Bowler, D.E. and Benton, T.G. (2005) Causes and consequences of animal dispersal strategies: relating individual behaviour to spatial dynamics. Biological Reviews 80, 205–225.CrossRefGoogle ScholarPubMed
Buchanan, M. (2008) Ecological modelling: the mathematical mirror to animal nature. Nature 453, 714–716.CrossRefGoogle ScholarPubMed
Chapman, M.G. (2000a) Poor design of behavioural experiments gets poor results: examples from intertidal habitats. Journal of Experimental Marine Biology and Ecology 250, 77–95.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, 181–201.CrossRefGoogle 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, 1133–1136.CrossRefGoogle Scholar
Chapperon, C. and Seuront, L. (2011a) Variability in the motion behaviour of intertidal gastropods: ecological and evolutionary perspectives. Journal of the Marine Biological Association of the United Kingdom 91, 237–244.CrossRefGoogle Scholar
Chapperon, C. and Seuront, L. (2011b) Behavioral thermoregulation in a tropical gastropod: links to climate change scenarios. Global Change Biology 17, 1740–1749.CrossRefGoogle Scholar
Chapperon, C. and Seuront, L. (2011c) Space–time variability in environmental thermal properties and snail thermoregulatory behaviour. Functional Ecology 25, 1040–1050.CrossRefGoogle Scholar
Coffin, M.R.S., Drolet, D., Hamilton, D.J. and Barbeau, M.A. (2008) Effect of immersion at low tide on distribution and movement of the mud snail Ilyanassa obsolete (Say), in the upper Bay of Fundy, eastern Canada. Journal of Experimental Marine Biology and Ecology 364, 110–115.CrossRefGoogle Scholar
Coleman, R.A. (2008) Overestimations of food abundance: predator responses to prey aggregation. Ecology 89, 1777–1783.CrossRefGoogle ScholarPubMed
Cooke, S.J., Hinch, S.G., Wikelski, M., Andrews, R.D., Kuchel, L.J., Wolcott, T.G. and Butler, P.J. (2004) Biotelemetry: a mechanistic approach to ecology. Trends in Ecology and Evolution 19, 334–343.CrossRefGoogle ScholarPubMed
Croll, R.P. (1983) Gastropod chemoreception. Biological Reviews 58, 293–319.CrossRefGoogle Scholar
Dubois, Y., Blouin-Demers, G., Shipley, B. and Thomas, D. (2009) Thermoregulation and habitat selection in wood turtles Glyptemys insculpta: chasing the sun slowly. Journal of Animal Ecology 78, 1023–1032.CrossRefGoogle ScholarPubMed
Edwards, A.M., Phillips, R.A., Watkins, N.W., Freeman, M.P., Murphy, E.J., Afanasyev, V., Buldyrev, S.V., da Luz, M.G.E., Raposo, E.P., Stanley, H.E. and Viswanathan, G.M. (2007) Revisiting Lévy flight search patterns of wandering albatrosses, bumblebees and deer. Nature 449, 1044–1049.CrossRefGoogle ScholarPubMed
Feder, M.E., Garland, T., Marden, J.H. and Zera, A.J. (2010) Locomotion in response to shifting climate zones: not so fast. Annual Review of Physiology 72, 167–190.CrossRefGoogle Scholar
Franklin, J. (2010) Moving beyond static species distribution models in support of conservation biogeography. Diversity and Distributions 16, 321–330.CrossRefGoogle Scholar
Garrity, S.D. and Levings, S.L. (1981) A predator–prey interaction between two physically and biologically constrained tropical rocky shore gastropods: direct, indirect and community effects. Ecological Monographs 51, 267–286.CrossRefGoogle Scholar
Gibson, R.N. (2003) Go with the flow: tidal migration in marine animals. Hydrobiologia 503, 153–161.CrossRefGoogle Scholar
Gray, D.R. and Williams, G.A. (2010) Knowing when to stop: rhythms of locomotor activity in the high-shore limpet, Cellana grata Gould. Journal of Experimental Marine Biology and Ecology 391, 125–130.CrossRefGoogle Scholar
Henry, P.Y. and Jarne, P. (2007) Marking hard-shelled gastropods: tag loss, impact on life-history traits, and perspectives in biology. Invertebrate Biology 126, 138–153.CrossRefGoogle Scholar
Humphries, N.E., Queiroz, N., Dyer, J.R.M., Pade, N.G., Musyl, M.K., Schaefer, K.M., Fuller, D.W., Brunnschweiler, J.M., Doyle, T.K., Houghton, J.D.R., Hays, G.C., Jones, C.S., Noble, L.R., Wearmouth, V.J., Southall, E.J. and Sims, D.W. (2010) Environmental context explains Lévy and Brownian movement patterns of marine predators. Nature 465, 1066–1069.CrossRefGoogle Scholar
Jackson, A.C., Underwood, A.J., Murphy, R.J. and Skilleter, G.A. (2010) Latitudinal and environmental patterns in abundance and composition of epilithic microphytobenthos. Marine Ecology Progress Series 417, 27–38.CrossRefGoogle Scholar
Jerde, C.L. and Visscher, D.R. (2005) GPS measurement error influences on movement model parameterization. Ecological Applications 15, 806–810.CrossRefGoogle Scholar
Jones, K.M.M. and Boulding, E.G. (1999) State-dependent habitat selection by an intertidal snail: the costs of selecting a physically stressful microhabitat. Journal of Experimental Marine Biology and Ecology 242, 149–177.CrossRefGoogle Scholar
Little, C. (1989) Factors governing patterns of foraging activity in littoral marine herbivorous molluscs. Journal of Molluscan Studies 55, 273–284.CrossRefGoogle Scholar
Mårell, A., Ball, J.P. and Hofgaard, A. (2002) Foraging and movement paths of female reindeer: insights from fractal analysis, correlated random walks, and Lévy flights. Canadian Journal of Zoology 80, 854–865.CrossRefGoogle Scholar
Matthews, S.N. and Rodewald, P.G. (2010) Movement behaviour of a forest songbird in an urbanized landscape: the relative importance of patch-level effects and body condition during migratory stopover. Landscape Ecology 25, 955–965.CrossRefGoogle Scholar
Miller, L.P., O'Donnell, M.J. and Mach, K.J. (2007) Dislodged but not dead: survivorship of a high intertidal snail following wave dislodgement. Journal of the Marine Biological Association of the United Kingdom 87, 735–739.CrossRefGoogle Scholar
Morales, J.M., Moorcroft, P.R., Matthiopoulos, J., Frair, J.L., Kie, J.G., Powell, R.A., Merrill, E.H. and Haydon, D.T. (2010) Building the bridge between animal movement and population dynamics. Philosophical Transactions of the Royal Society, B: Biological Sciences 365, 2289–2301.CrossRefGoogle Scholar
Murphy, R.J., Underwood, A.J., Tolhurst, T.J. and Chapman, M.G. (2008) Field-based remote-sensing for experimental intertidal ecology: hyperspatial and hyperspectral data for New South Wales (Australia). Remote Sensing of Environment 112, 3353–3365.CrossRefGoogle Scholar
Nathan, R., Getz, W.M., Revilla, E., Holyoak, M., Kadmon, R., Saltz, D. and Smouse, P.E. (2008) A movement ecology paradigm for unifying organismal movement research. Proceedings of the National Academy of Sciences of the United States of America 105, 19052–19059.CrossRefGoogle ScholarPubMed
Orrock, J.L., Dill, L.M., Sih, A., Grabowski, J.H., Peaor, S.D., Peckarsky, B.L., Preisser, E.L., Vonesh, J.R. and Werner, E.E. (2010) Predator effects in predator-free space: the remote effects of predators on prey. Open Ecology Journal 3, 22–30.CrossRefGoogle Scholar
Owen-Smith, N., Fryxell, J.M. and Merrill, E.H. (2010) Foraging theory upscaled: the behavioural ecology of herbivore movement. Philosophical Transactions of the Royal Society, B: Biological Sciences 365, 2267–2278.CrossRefGoogle ScholarPubMed
Patterson, T.A., Thomas, L., Wilcox, C., Ovaskainene, O. and Matthiopoulos, J. (2008) State–space models of individual animal movement. Trends in Ecology and Evolution 23, 87–94.CrossRefGoogle ScholarPubMed
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, 177–186.CrossRefGoogle Scholar
Przeslawski, R. (2008) Temporal patterns of gastropod egg mass deposition on south-eastern Australian shores. Marine Freshwater Research 59, 457–466.CrossRefGoogle Scholar
Pyke, G.H. (1984) Optimal foraging theory: a critical review. Annual Review of Ecology and Systematics 15, 523–575.CrossRefGoogle Scholar
Rochette, R. and Dill, L.M. (2000) Mortality, behaviour and the effects of predators on the intertidal distribution of littorinid gastropods. Journal of Experimental Marine Biology and Ecology 253, 165–191.CrossRefGoogle ScholarPubMed
Schmitz, O.J., Grabowski, J.H., Peckarsky, B.L., Preisser, E.L., Trussell, G.C. and Vonesh, J.R. (2008) From individuals to ecosystem function: toward an integration of evolutionary and ecosystem ecology. Ecology 89, 2436–2445.CrossRefGoogle ScholarPubMed
Seuffert, M.E., Burela, S. and Martín, P.R. (2010) Influence of water temperature on the activity of the freshwater snail Pomacea canaliculata (Caenogastropoda: Ampullariidae) at its southernmost limit (Southern Pampas, Argentina). Journal of Thermal Biology 35, 77–84.CrossRefGoogle ScholarPubMed
Seuront, L. (2010) Fractals and multifractals in ecology and aquatic science. Boca Raton, FL: CRC Press.Google Scholar
Seuront, L. and Spilmont, N. (2002) Self-organized criticality in intertidal microphytobenthos patch patterns. Physica A 313, 512–539.CrossRefGoogle Scholar
Seuront, L. and Vincent, D. (2008) Impact of a Phaeocystis globosa spring bloom on Temora longicornis feeding and swimming behaviours. Marine Ecology Progress Series 363, 131–145.CrossRefGoogle Scholar
Seuront, L., Brewer, M. and Strickler, J.R. (2004) Quantifying zooplankton swimming behavior: the question of scale. In Seuront, L. and Strutton, P.G. (eds) Handbook of scaling methods in aquatic ecology: measurement, analysis, simulation. Boca Raton, FL: CRC Press, pp. 333–359.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. Physica A 385, 573–582.CrossRefGoogle Scholar
Shane, K. (2001) Temporal variation in the movement of the spiny lobster Jasus edwardsii. Marine Freshwater Research 52, 323–331.Google Scholar
Sims, D.W., Southall, E.J., Humphries, N.E., Hays, G.C., Bradshaw, C.J.A., Pitchford, J.W., James, A., Ahmed, M.Z., Brierley, A.S., Hindell, M.A., Morritt, D., Musyl, M.K., Righton, D., Shepard, E.L.C., Wearmouth, V.J., Wilson, R.P., Witt, M.J. and Metcalfe, J.D. (2008) Scaling laws of marine predator search behaviour. Nature 451, 1098–1102.CrossRefGoogle ScholarPubMed
Stafford, R., Davies, M.S. and Williams, G.A. (2007) Computer simulations of high shore littorinids predict small-scale spatial and temporal distribution patterns on rocky shores. Marine Ecology Progress Series 342, 151–161.CrossRefGoogle Scholar
Thompson, R.C., Norton, T.A. and Hawkins, S.J. (2004) Physical stress and biological control regulate the producer–consumer balance in intertidal biofilms. Ecology 85, 1372–1382.CrossRefGoogle Scholar
Turchin, P. (1998) Quantitative analysis of movement: measuring and modelling population redistribution in animals and plants. Sunderland, MA: Sinauer Associates.Google Scholar
Underwood, A.J. (1976) Nearest neighbour analysis of spatial dispersion of intertidal prosobranch gastropods within two substrata. Oecologia 26, 257–266.CrossRefGoogle ScholarPubMed
Underwood, A.J. (1984) Vertical and seasonal patterns in competition for microalgae between intertidal gastropods. Oecologia 64, 211–222.CrossRefGoogle ScholarPubMed
Viswanathan, G.M. (2010) Fish in Lévy-flight foraging. Nature 465, 1018–1019.CrossRefGoogle ScholarPubMed
Viswanathan, G.M., Buldyrev, S.V., Havlin, S., da Luz, M.G.E., Raposo, E.P. and Stanley, H.E. (1999) Optimizing the success of random searches. Nature 401, 911–914.CrossRefGoogle ScholarPubMed
Viswanathan, M., da Luz, M.G.E., Raposo, E.P. and Stanley, H.E. (2011) The physics of foraging: an introduction to random searches and biological encounters. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Williams, G.A. (1994) The relationship between shade and molluscan grazing in structuring communities on a moderately-exposed tropical rocky shore. Journal of Experimental Marine Biology and Ecology 178, 79–95.CrossRefGoogle Scholar
Williams, G.A. (1995) Maintenance of zonation patterns in two species of flat periwinkle, Littorina obtusata and L. mariae. Hydrobiologia 309, 143–150.CrossRefGoogle Scholar
Williams, G.A. and Little, C. (2007) Foraging behaviour. In Denny, M.W. and Gaines, S.D. (eds) The encyclopaedia of tidepools and rocky shores. Berkeley, CA: University of California Press, pp. 239–242.Google Scholar
Zar, J.H. (2010) Biostatistical analysis. 5th edition.Upper Saddle River, NJ: Prentice-Hall.Google Scholar