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Broad-scale patterns of sex ratios in Patella spp.: a comparison of range edge and central range populations in the British Isles and Portugal

Published online by Cambridge University Press:  10 April 2015

C.D.G. Borges ,
C.P. Doncaster ,
M.A. Maclean  and
S.J. Hawkins
C.D.G. Borges*
Affiliation:
Centre for Biological Sciences, University of Southampton, Life Sciences Building 85, Highfield, Southampton SO17 1BJ, UK The Marine Biological Association of the United Kingdom, The Laboratory, Citadel Hill, Plymouth, Devon PL1 2PB, UK
C.P. Doncaster
Affiliation:
Centre for Biological Sciences, University of Southampton, Life Sciences Building 85, Highfield, Southampton SO17 1BJ, UK
M.A. Maclean
Affiliation:
Ocean and Earth Science, National Oceanography Centre, Waterfront Campus, European Way, University of Southampton, Southampton SO14 3ZH, UK
S.J. Hawkins
Affiliation:
Centre for Biological Sciences, University of Southampton, Life Sciences Building 85, Highfield, Southampton SO17 1BJ, UK Ocean and Earth Science, National Oceanography Centre, Waterfront Campus, European Way, University of Southampton, Southampton SO14 3ZH, UK The Marine Biological Association of the United Kingdom, The Laboratory, Citadel Hill, Plymouth, Devon PL1 2PB, UK
*
Correspondence should be addressed to: C.D.G. Borges, CIIMAR-Centro Interdisciplinar de Investigação Marinha e Ambiental, Laboratório de Biodiversidade Costeira, Rua dos Bragas, 289, 4050-123 Porto, Portugal email: [email protected]
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Abstract

Sex change, or sequential hermaphroditism, occurs in the plant and animal kingdoms and often determines a predominance of the first sex. Our aim was to explore changes in sex ratios within the range of the species studied: Patella vulgata and Patella depressa. The broad-scale survey of sex with size of limpets covered a range of latitudes from Zambujeira do Mar (southern Portugal) to the English Channel. Indirect evidence was found for the occurrence of protandry in P. vulgata populations from the south of England, with females predominating in larger size-classes; cumulative frequency distributions of males and females were different; sex ratios were biased towards males and smallest sizes of males were smaller than the smallest sizes of females. In contrast in Portugal females were found in most size-classes of P. vulgata. In P. depressa populations from the south coast of England and Portugal females were interspersed across most size-classes; size distributions of males and females and size at first maturity of males and females did not differ. P. depressa did, however, show some indications of the possibility of slight protandry occurring in Portugal. The test of sex ratio variation with latitude indicated that P. vulgata sex ratios might be involved in determining the species range limit, particularly at the equatorward limit since the likelihood of being male decreased from the south coast of England to southern Portugal. Thus at the southern range limit, sperm could be in short supply due to scarcity of males contributing to an Allee effect.

Keywords

limpetsprotandryrange distributionsex changesex ratio
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 95 , Issue 6 , September 2015 , pp. 1141 - 1153
Copyright
Copyright © Marine Biological Association of the United Kingdom 2015 

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References

REFERENCES

Allsop, D.J. (2003) The evolutionary ecology of sex change. PhD thesis, University of Edinburgh, Edinburgh, UK.Google Scholar
Bacci, G. (1955) La variabilita dei genotipi sessuali negli animali ermafroditi. Publicazioni della Stazione Zoologica di Napoli 26, 110–137.Google Scholar
Bacci, G. (1975) Sex reversal in the genus Patella (Gastropoda, Prosobranchiata). Publicazioni della Stazione Zoologica di Napoli 39, 341–344.Google Scholar
Baeza, J.A. and Bauer, R.T. (2004) Experimental test of socially mediated sex change in a protandric simultaneous hermaphrodite, the marine shrimp Lysmata wurdemanni (Caridea: Hippolytidae). Behavioral Ecology and Sociobiology 55, 544–550.Google Scholar
Ballantine, W.J. (1961) The population dynamics of Patella vulgata and other limpets. PhD thesis, Queen Mary College, London University, London, UK.Google Scholar
Baxter, J.M. (1983) Annual variations in soft-body dry weight, reproductive-cycle and sex-ratios in populations of Patella vulgata at adjacent sites in the Orkney islands. Marine Biology 76, 149–157.CrossRefGoogle Scholar
Blackmore, D.T. (1969) Studies of Patella vulgata growth, reproduction and zonal distribution. Journal of Experimental Marine Biology and Ecology 3, 200–213.CrossRefGoogle Scholar
Boaventura, D., Cancela da Fonseca, L. and Hawkins, S.J. (2003) Size matters: competition within populations of the limpet Patella depressa. Journal of Animal Ecology 72, 435–446.CrossRefGoogle Scholar
Boaventura, D., Fonseca, L.C. and Hawkins, S.J. (2002a) Analysis of competitive interactions between the limpets Patella depressa Pennant and Patella vulgata L. on the northern coast of Portugal. Journal of Experimental Marine Biology and Ecology 271, 171–188.CrossRefGoogle Scholar
Boaventura, D., Ré, P., Cancela da Fonseca, L. and Hawkins, S.J. (2002b) Intertidal rocky shore communities of the continental Portuguese Coast: analysis of distribution patterns. Marine Ecology 23, 69–90.CrossRefGoogle Scholar
Borges, C.D.G. (2013) The influence of environment and exploitation on sex change in limpets. PhD thesis, University of Southampton, Southampton, UK.Google Scholar
Boukal, D.S. and Berec, L. (2002) Single-species models of the Allee effect: extinction boundaries, sex ratios and mate encounters. Journal of Theoretical Biology 218, 375–394.CrossRefGoogle ScholarPubMed
Bowman, R.S. and Lewis, J.R. (1977) Annual fluctuations in the recruitment of Patella vulgata L. Journal of the Marine Biological Association of the United Kingdom 57, 793–815.CrossRefGoogle Scholar
Bowman, R.S. and Lewis, J.R. (1986) Geographical variation in the breeding cycles and recruitment of Patella spp. Hydrobiologia 142, 41–56.CrossRefGoogle Scholar
Branch, G.M. (1974) The ecology of Patella Linnaeus from the Cape peninsula, South Africa. 2. Reproductive cycles. Transactions of the Royal Society of South Africa 41, 111–160.CrossRefGoogle Scholar
Brazão, S., Boaventura, D., Morais, S., Narciso, L. and Ré, P. (2003) Reproduction of Patella depressa Pennant, 1777 on the central Portuguese coast. Boletin Instituto Espanol de Oceanografia 19, 453–460.Google Scholar
Brown, J.H. (1995) Macroecology. Chicago, IL: University of Chicago Press.Google Scholar
Buston, P.M. (2003) Size and growth modification in clownfish. Nature 424, 145–146.CrossRefGoogle ScholarPubMed
Castro, J.J.R.P.P. (2004) Predação humana no litoral rochoso alentejano: caracterização, impacte ecológico e conservação. Portugal: Tese de Doutoramento. Laboratório de Ciências do Mar, Departamento de Biologia, Universidade de Évora.Google Scholar
Charnov, E.L. (1982) The theory of sex allocation. Princeton, NJ: Princeton University Press.Google ScholarPubMed
Charnov, E.L. and Bull, J.J. (1989a) Non-Fisherian sex ratios with sex change and environmental sex determination. Nature 338, 148–150.CrossRefGoogle Scholar
Charnov, E.L. and Bull, J.J. (1989b) The primary sex ratio under environmental sex determination. Journal of Theoretical Biology 139, 431–436.CrossRefGoogle ScholarPubMed
Chen, M-H., Yang, Y-W. and Soong, K. (2004) Host effect on size structure and timing of sex change in the coral-inhabiting snail Coralliophila violacea. Marine Biology 144, 287–293.CrossRefGoogle Scholar
Collin, R. (2006) Sex ratio, life history invariants, and patterns of sex change in a family of protandrous gastropods. Evolution 60, 735–745.Google Scholar
Collin, R., Mclellan, M., Gruber, K. and Bailey-Jourdain, C. (2005) Effects of conspecific associations on size at sex change in three species of calyptraeid gastropods. Marine Ecology Progress Series 293, 89–97.CrossRefGoogle Scholar
Crisp, D.J. and Southward, A.J. (1958) The distribution of intertidal organisms along the coasts of the English Channel. Journal of the Marine Biological Association of the United Kingdom 37, 157–208.CrossRefGoogle Scholar
Das, S.M. and Seshappa, G. (1948) A contribution to the biology of Patella: on population distribution and sex-proportions in Patella vulgata Linnaeus at Cullercoats, England. Proceedings of the Zoological Society of London 117, 653–662.CrossRefGoogle Scholar
Dawson, M.N., Grosberg, R.K., Stuart, Y.E. and Sanford, E. (2010) Population genetic analysis of a recent range expansion: mechanisms regulating the poleward range limit in the volcano barnacle Tetraclita rubescens. Molecular Ecology 19, 1585–1605.CrossRefGoogle ScholarPubMed
Dodd, J.M. (1956) Studies on the biology of limpets. III. Hermaphroditism in the three British species of Patella. Journal of the Marine Biological Association of the United Kingdom 35, 327–340.CrossRefGoogle Scholar
Espinosa, F., Rivera-Ingraham, G. and García-Gómez, J.C. (2009) Gonochorism or protandrous hermaphroditism? Evidence of sex change in the endangered limpet Patella ferruginea. Marine Biodiversity Records 2, e153.CrossRefGoogle Scholar
Fenberg, P.B. and Rivadeneira, M.M. (2011) Range limits and geographic patterns of abundance of the rocky intertidal owl limpet, Lottia gigantea. Journal of Biogeography 38, 2286–2298.CrossRefGoogle Scholar
Fenberg, P.B. and Roy, K. (2012) Anthropogenic harvesting pressure and changes in life history: insights from a rocky intertidal limpet. American Naturalist 180, 200–210.CrossRefGoogle ScholarPubMed
Fischer-Piette, E. (1935) Systématique et biogéographie. Les Patelles d'Europe et d’Áfrique du Nord. Journal de Conchyliologie 79, 5–66.Google Scholar
Fischer-Piette, E. and Gaillard, J. M. (1959) Les Patelles, au long des cotes atlantiques ibériques et nord-marocaines. Journal de Conchyliologie 99, 135–200.Google Scholar
Firth, L.B., Thompson, R.C., White, F.J., Schofield, M., Skov, M.W., Hoggart, S.P.G., Jackson, J., Knights, A.M. and Hawkins, S.J. (2013) The importance of water-retaining features for biodiversity on artificial intertidal coastal defence structures. Diversity and Distributions 19, 1275–1283.CrossRefGoogle Scholar
Frank, S.A. and Swingland, I.R. (1988) Sex ratio under conditional sex expression. Journal of Theoretical Biology 135, 415–418.CrossRefGoogle ScholarPubMed
Frenkiel, L. (1975) Contribuition à ĺétude des cycles de reproduction des Patellidae en Algérie. Publicazioni della Stazione Zoologica di Napoli 39, 153–189.Google Scholar
Gaines, S.D., Gaylord, B., Gerber, L.R., Hastings, A. and Kinlan, B.P. (2007) Connecting places: the ecological consequences of dispersal in the sea. Oceanography 20, 90–99.CrossRefGoogle Scholar
Gaines, S.D., Lester, S.E., Eckert, G., Kinlan, B.P., Sagarin, R. and Gaylord, B. (2009) Dispersal and geographic ranges in the sea. In Roy, K. and Witman, J.D. (eds) Marine macroecology. Chicago, IL: University of Chicago Press, pp. 227–249.CrossRefGoogle Scholar
Gaston, K.J. (2003) The structure and dynamics of geographic ranges. Oxford: Oxford University Press.CrossRefGoogle Scholar
Gaston, K.J. (2009) Geographic range limits: achieving synthesis. Proceedings of the Royal Society B – Biological Sciences 276, 1395–1406.CrossRefGoogle ScholarPubMed
Gilman, S. (2005) A test of Brown's principle in the intertidal limpet Collisella scabra (Gould, 1846). Journal of Biogeography 32, 1583–1589.CrossRefGoogle Scholar
Gilman, S.E. (2006) The northern geographic range limit of the intertidal limpet Collisella scabra: a test of performance, recruitment, and temperature hypotheses. Ecography 29, 709–720.CrossRefGoogle Scholar
Guallart, J., Calvo, M., Acevedo, I. and Templado, J. (2013) Two-way sex change in the endangered limpet Patella ferruginea (Mollusca, Gastropoda). Invertebrate Reproduction and Development 57, 247–253.CrossRefGoogle Scholar
Guerra, M.T. and Gaudêncio, M.J. (1986) Aspects of the ecology of Patella spp. on the Portuguese coast. Hydrobiologia 142, 57–69.CrossRefGoogle Scholar
Herbert, R.J.H. and Hawkins, S.J. (2006) Effect of rock type on the recruitment and early mortality of the barnacle Chthamalus montagui. Journal of Experimental Marine Biology and Ecology 334, 96–108.CrossRefGoogle Scholar
Herbert, R.J.H., Hawkins, S.J., Sheader, M. and Southward, A.J. (2003) Range extension and reproduction of the barnacle Balanus perforatus in the eastern English Channel. Journal of the Marine Biological Association of the United Kingdom 83, 73–82.CrossRefGoogle Scholar
Herbert, R.J.H., Southward, A.J., Clarke, R.T., Sheader, M. and Hawkins, S.J. (2009) Persistent border: an analysis of the geographic boundary of an intertidal species. Marine Ecology-Progress Series 379, 135–150.CrossRefGoogle Scholar
Hoagland, K.E. (1978) Protandry and the evolution of environmentally mediated sex change: a study of the Mollusca. Malacologia 17, 365–391.Google Scholar
Hodgson, A.N., Le Quesne, W.J.F., Hawkins, S.J. and Bishop, J.D.D. (2007). Factors affecting fertilization success in two species of patellid limpet (Mollusca: Gastropoda) and development of fertilization kinetics models. Marine Biology 150, 415–426.CrossRefGoogle Scholar
Hyder, K., Aberg, P., Johnson, M.P. and Hawkins, S.J. (2001) Models of open populations with space-limited recruitment: extension of theory and application to the barnacle Chthamalus montagui. Journal of Animal Ecology 70, 853–863.CrossRefGoogle Scholar
Keith, S.A., Herbert, R.J.H., Norton, P.A., Hawkins, S.J. and Newton, A.C. (2011) Individualistic species limitations of climate-induced range expansions generated by meso-scale dispersal barriers. Diversity and Distributions 17, 275–286.CrossRefGoogle Scholar
Kendall, M.A., Burrows, M.T., Southward, A.J. and Hawkins, S.J. (2004) Predicting the effects of marine climate change on the invertebrate prey of the birds of rocky shores. IBIS 146, 40–47.CrossRefGoogle Scholar
Kent, A., Hawkins, S.J. and Doncaster, C.P. (2003) Population consequences of mutual attraction between settling and adult barnacles. Journal of Animal Ecology 72, 941–952.CrossRefGoogle Scholar
Kuwamura, T. and Nakashima, Y. (1998) New aspects of sex change among reef fishes: recent studies in Japan. Environmental Biology of Fishes 52, 125–135.CrossRefGoogle Scholar
Lasky, J.R., Jetz, W. and Keitt, T.H. (2011) Conservation biogeography of the US-Mexico border: a transcontinental risk assessment of barriers to animal dispersal. Diversity and Distributions 17, 673–687.CrossRefGoogle Scholar
Le Quesne, W.J.F. and Hawkins, S.J. (2006) Direct observations of protandrous sex change in the patellid limpet Patella vulgata. Journal of the Marine Biological Association of the United Kingdom 86, 161–162.CrossRefGoogle Scholar
Lee, A.M., Saether, B.E. and Engen, S. (2011) Demographic stochasticity, Allee effects, and extinction: the influence of mating system and sex ratio. American Naturalist 177, 301–313.CrossRefGoogle ScholarPubMed
Lewis, J.R. (1964) The ecology of rocky shores. London: English Universities Press.Google Scholar
Lewis, J.R. (1986) Latitudinal trends in reproduction, recruitment and population characteristics of some rocky littoral molluscs and cirripedes. Hydrobiologia 142, 1–13.CrossRefGoogle Scholar
Lewis, J.R. and Bowman, R.S. (1975) Local habitat-induced variations in the population dynamics of Patella vulgata L. Journal of Experimental Marine Biology and Ecology 17, 165–203.CrossRefGoogle Scholar
Lindberg, D.R. and Wright, W.G. (1985) Patterns of sex change of the protandric patellacean limpet Lottia gigantea (Mollusca: Gastropoda). Veliger 27, 261–265.Google Scholar
Lutenesky, M.M.F. (1994) Density-dependent protogynous sex change in territorial-haremic fishes: models and evidence. Behavioral Ecology 5, 375–383.CrossRefGoogle Scholar
Mieszkowska, N., Hawkins, S.J., Burrows, M.T. and Kendall, M.A. (2007) Long-term changes in the geographic distribution and population structures of Osilinus lineatus (Gastropoda: Trochidae) in Britain and Ireland. Journal of the Marine Biological Association of the United Kingdom 87, 537–545.CrossRefGoogle Scholar
Mieszkowska, N., Kendall, M.A., Hawkins, S.J., Leaper, R., Williamson, P., Hardman-Mountford, N.J. and Southward, A.J. (2006) Changes in the range of some common rocky shore species in Britain – a response to climate change? Hydrobiologia 555, 241–251.CrossRefGoogle Scholar
Montalenti, G. (1958) Perspectives of research on sex problems in marine organisms. In Buzzati-Travesso, A.A. (ed) Perspectives in marine biology. Berkeley, CA: University of California Press, pp. 589–602.CrossRefGoogle Scholar
Moore, P.J., Thompson, R.C. and Hawkins, S.J. (2011) Phenological changes in intertidal conspecific gastropods in response to climate warming. Global Change Biology 17, 709–719.CrossRefGoogle Scholar
Moschella, P.S., Abbiati, M., Åberg, P., Airoldi, L., Anderson, J.M., Bacchiocchi, F., Bulleri, F., Dinesen, G.E., Frost, M., Gacia, E., Granhag, L., Jonsson, P.R., Satta, M.P., Sundelöf, A., Thompson, R.C. and Hawkins, S.J. (2005) Low-crested coastal defence structures as artificial habitats for marine life: using ecological criteria in design. Coastal Engineering 52, 1053–1071.CrossRefGoogle Scholar
Munday, P.L. (2002) Bi-directional sex change: testing the growth-rate advantage model. Behavioral Ecology and Sociobiology 52, 247–254.CrossRefGoogle Scholar
Munday, P.L., Buston, P.M. and Warner, R.R. (2006) Diversity and flexibility of sex-change strategies in animals. Trends in Ecology and Evolution 21, 89–95.CrossRefGoogle ScholarPubMed
Orton, J.H. (1919) Sex phenomena in the common limpet (Patella vulgata). Nature 104, 373–374.CrossRefGoogle Scholar
Orton, J.H. (1928) Observations on Patella vulgata. I. Sex phenomena, breeding and shell growth. Journal of the Marine Biological Association of the United Kingdom 15, 851–862.CrossRefGoogle Scholar
Orton, J.H. (1946) The biology of Patella in Great Britain. Nature 158, 173–174.CrossRefGoogle Scholar
Orton, J.H. and Southward, A.J. (1961) Studies on the biology of limpets. IV. The breeding of Patella depressa Pennant on the North Cornish Coast. Journal of the Marine Biological Association of the United Kingdom 41, 653–662.CrossRefGoogle Scholar
Orton, J.H., Southward, A.J. and Dodd, J.M. (1956) Studies on the biology of limpets. II. The breeding of Patella vulgata L. in Britain. Journal of the Marine Biological Association of the United Kingdom 35, 149–176.CrossRefGoogle Scholar
Peña-Othaiz, J. (1996) Estudio de los ciclos reproductores de cuatro especies de lapas y dos de traquidos (Gastropoda, Prosobranchia) del piso intermareal de la costa vasca. Tesis doctoral. Universidad Autónoma de Madrid, Madrid.Google Scholar
Poloczanska, E.S., Hawkins, S.J., Southward, A.J. and Burrows, M.T. (2008) Modeling the response of populations of competing species to climate change. Ecology 89, 3138–3149.CrossRefGoogle ScholarPubMed
Ribeiro, P.A., Xavier, R., Santos, A.M., and Hawkins, S.J. (2009) Reproductive cycles of four species of Patella (Mollusca: Gastropoda) on the northern and central Portuguese coast. Journal of the Marine Biological Association of the United Kingdom 89, 1215–1221.CrossRefGoogle Scholar
Rivadeneira, M.M., Hernaez, P., Baeza, J.A., Boltana, S., Cifuentes, M., Correa, C., Cuevas, A., Valle, E., Hinojosa, I., Ulrich, N., Valdivia, N., Vásquez, N., Zander, A. and Thiel, M. (2010) Testing the abundant-centre hypothesis using intertidal porcelain crabs along the Chilean coast: linking abundance and life-history variation. Journal of Biogeography 37, 486–498.CrossRefGoogle Scholar
Rivera-Ingraham, G.A., Espinosa, F. and García-Gómez, J.C. (2011) Environmentally mediated sex change in the endangered limpet Patella ferruginea (Gastropoda: Patellidae). Journal of Molluscan Studies 77, 226–231.CrossRefGoogle Scholar
Ross, R.M. (1990) The evolution of sex-change mechanisms in fishes. Environmental Biology of Fishes 29, 81–93.CrossRefGoogle Scholar
Sagarin, R.D., Gaines, S.D. and Gaylord, B. (2006) Moving beyond assumptions to understand abundance distributions across the ranges of species. Trends in Ecology and Evolution 21, 524–530.CrossRefGoogle ScholarPubMed
Sanford, E. (2002) Water temperature, predation, and the neglected role of physiological rate effects in rocky intertidal communities. Integrative and Comparative Biology 42, 881–891.CrossRefGoogle ScholarPubMed
Sexton, J.P., Mcintyre, P.J., Angert, A.L. and Rice, K.J. (2009) Evolution and ecology of species range limits. Annual Review of Ecology, Evolution and Systematics 40, 415–436.CrossRefGoogle Scholar
Shapiro, D.Y. (1984) Sex reversal and sociodemographic processes in coral reef fishes. In Potts, G.W. and Wooton, R.J. (eds) Fish reproduction: strategies and tactics. London: Academic Press, pp. 103–118.Google Scholar
Sokal, R.R. and Rohlf, F.J. (1998) Biometry: the principles and practice of statistics in biological research. New York, NY: Freeman W.H. and Company.Google Scholar
Southward, A.J. and Crisp, D.J. (1954) The distribution of certain intertidal animals around the Irish coast. Proceedings of the Royal Irish Academy 57, 1–29.Google Scholar
Southward, A.J., Hawkins, S.J. and Burrows, M.T. (1995) Seventy years’ observations of changes in distribution and abundance of zooplankton and intertidal organisms in the western English Channel in relation to rising sea temperature. Journal of Thermal Biology 20, 127–155.CrossRefGoogle Scholar
Walker, S.P.W., Thibaut, L. and Mccormick, M.I. (2010) Density-dependent sex ratio adjustment and the Allee effect: a model and a test using a sex-changing fish. American Naturalist 176, 312–321.CrossRefGoogle Scholar
Warner, R.R. (1984) Mating behavior and hermaphroditism in coral reef fishes. American Scientist 72, 128–136.Google Scholar
Warner, R.R., Fisch, D.L. and Standish, J.D. (1996) Social control of sex in the shelf limpet, Crepidula norrisiarum: size-specific responses to local group composition. Journal of Experimental Marine Biology and Ecology 204, 155–167.CrossRefGoogle Scholar
Warner, R.R. and Swearer, S.E. (1991) Social control of sex change in the bluehead wrasse Thalassoma bifasciatum (Pisces: Labridae). Biological Bulletin 181, 199–204.CrossRefGoogle ScholarPubMed
Wright, W.G. (1989) Intraspecific density mediates sex-change in territorial patellacean Lottia gigantea. Marine Biology 100, 353–364.CrossRefGoogle Scholar
Wright, W.G. and Lindberg, D.R. (1979) A non-fatal method of sex determination for patellacean gastropods. Journal of the Marine Biological Association of the United Kingdom 59, 803.CrossRefGoogle Scholar
Wright, W.G. and Lindberg, D.R. (1982) Direct observations of sex change in the patelacean Lottia gigantea. Journal of the Marine Biological Association of the United Kingdom 62, 737–738.CrossRefGoogle Scholar
Zacherl, D., Gaines, S.D. and Lonhart, S.I. (2003) The limits to biogeographical distributions: insights from the northward range extension of the marine snail, Kelletia kelletii (Forbes, 1852). Journal of Biogeography 30, 913–924.CrossRefGoogle Scholar