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Microgeographical variation in shell strength in the flat periwinkles Littorina obtusata and Littorina mariae

  • C. R. Fletcher
Conference paper
Part of the Developments in Hydrobiology book series (DIHY, volume 111)

Abstract

The strength of molluscan shells has been shown to vary in adaptive ways in a number of species and one of the main factors thought to be involved is shell-crushing by predators. A recent study found that the sibling species of flat periwinkle Littorina obtusata and Littorina mariae showed significant differences in the rates at which shell strength increased with shell length in specimens which had been collected from the same location, where the species were sympatric. This paper describes differences between the shells of the two species from a number of localities around Milford Haven in Dyfed, Wales, and local geographical variation in the shells.

Littorina mariae, which is normally found at lower tidal levels than L. obtusata, matures at a smaller shell length. Both species reinforce the shell as they grow since shell strength, determined as the maximum force applied by a hydraulic tensile testing machine before the shell cracked, is strongly positively allometric; it increases at a rate close to the cube of shell length whilst isometric growth would result in strength increasing in proportion to the square of shell length. Because L. mariae matures earlier and reinforces the shell at a smaller size, the mature shell of L. mariae is substantially stronger on average than that of a similar sized but immature L. obtusata. At maturity the shell strengths of the two species are not very different despite the substantial difference in mean shell length.

Strength varies significantly from shore to shore, and with the level of the shore from which the animals were collected. Strength increases down the shore in both species. Shell strength decreases with exposure to wave action in L. mariae but increases with exposure in L. obtusata; there is also substantial shore-to-shore variation which is not explained by exposure.

Path analysis was used to explore the relationship between shell strength and other measured shell parameters (mass, length, height, thickness). The best predictor of shell strength in both species is a parameter which is heavily positively loaded on LN (shell mass) and strongly offset by negative loadings on LN (shell length) and LN (shell height). This is logical because for a given shell length a heavier shell will be thicker and stronger, whilst for a given shell mass a bigger shell will be thinner and therefore weaker. Such differential variation of shell mass and shell length explains most of the geographical variation observed in shell strength; shells are stronger in snails collected from one place than from another because, for the same shell length they are heavier or, to put it the other way, because at the same shell mass, they are smaller.

Key words

sibling species morphometrics shell strength local variation predator resistance Littorina 

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References

  1. Ash, V. B., 1989. Resistance to shell breaking in two intertidal snails. J. linn. Soc., Zool. 96: 167–184.CrossRefGoogle Scholar
  2. Ballantine, W. J., 1961. A biologically defined exposure scale for the comparative description of rocky shores. Field Studies 1: 1–19.Google Scholar
  3. Bertness, M. D. & C. Cunningham, 1981. Crab shell-crushing predation and gastropod architectural defense. J. exp. mar. Biol. Ecol. 50: 213–230.CrossRefGoogle Scholar
  4. Blundon, J. A. & G. J. Vermeij, 1983. Effect of shell repair on shell strength in the gastropod Littorina irrorata. Mar. Biol. 76: 41–45.CrossRefGoogle Scholar
  5. Boulding, E. G. & T. K. Hay, 1993. Quantitative genetics of shell form of an intertidal snail: constraints on short-term response to selection. Evolution 47: 576–592.CrossRefGoogle Scholar
  6. Brandwood, A., 1985. The effects of environment upon shell construction and strength in the rough periwinkle Littorina rudis Maton (Mollusca: Gastropoda). J. Zool., Lond. 206: 551–566.CrossRefGoogle Scholar
  7. Calder, W. A., 1984. Size, function, and life history. Harvard University Press, Massachusetts.Google Scholar
  8. Clarke, M. R. B., 1980. The reduced major axis of a bivariate sample. Biometrika 67: 441–6.CrossRefGoogle Scholar
  9. Cook, L. M. & G. Kenyon, 1993. Shell strength of colour morphs of the mangrove snail Littoraria pallescens. J. moll. Stud. 59: 29–34.CrossRefGoogle Scholar
  10. Cooke, A. H., 1985. Molluscs. In: Cambridge Natural History, Vol. III, Molluscs and Brachiopods. Macmillan, London.Google Scholar
  11. Crothers, J. H., 1985. Dog-whelks: an introduction to the biology of Nucella lapillus (L.). Field Studies 6: 291–360.Google Scholar
  12. Crothers, J. H., 1992. Shell size and shape variation in Littorina littorea (L.) from west Somerset. In: J. Grahame, P. J. Mill & D. G. Reid (eds), Proceedings of the 3rd International Symposium on Littorinid Biology. The Malacological Society of London, London: 91–97.Google Scholar
  13. Currey, J. D., 1979. The effect of drying on the strength of mollusc shells. J. Zool., Lond. 188: 301–308.CrossRefGoogle Scholar
  14. Currey, J. D. & R. N. Hughes, 1982. Strength of the dogwhelk Nucella lapillus and the winkle Littorina littorea from different habitats. J. anim. Ecol. 51: 47–56.CrossRefGoogle Scholar
  15. Dytham, C., J. Grahame & P. J. Mill, 1990. Distribution, abundance and shell morphology of Littorina saxatilis (Olivi) and Littorina arcana Hannaford Ellis at Robin Hood’s Bay, North Yorkshire. Hydrobiologia 193(Dev. Hydrobiol. 56): 233–240.CrossRefGoogle Scholar
  16. Goodwin, B. J., 1978. The growth and breeding cycle of Littorina obtusata (Gastropoda: Prosobranchiata) from Cardigan Bay. J. moll. Stud. 44: 231–242.Google Scholar
  17. Goodwin, B. J. & J. D. Fish, 1977. Inter-and intraspecific variation m Littorina obtusata and L. mariae (Gastropoda: Prosobranchia). J. moll. Stud. 43: 241–254.Google Scholar
  18. Grahame, J. & P. J. Mill, 1989. Shell shape variation in Littorina saxatilis and L. arcana: a case of character displacement? J. mar. biol. Ass. U.K. 69: 837–855.CrossRefGoogle Scholar
  19. Grahame, J. & P. J. Mill, 1992. Local and regional variation in the shape of rough periwinkles in southern Britain. In: J. Grahame, P. J. Mill & D. G. Reid (eds), Proceedings of the 3rd International Symposium on Littorinid Biology. The Malacological Society of London, London: 99–106.Google Scholar
  20. Grahame, J., P. J. Mill & A. C. Brown, 1990. Adaptive and nonadaptive variation in two species of rough periwinkle (Littorina) on British shores. Hydrobiologia 193(Dev. Hydrobiol. 56): 223–231.CrossRefGoogle Scholar
  21. Hughes, R. N. & R. W. Einer, 1979. Tactics of a predator Carcinus meanas and morphological responses of the prey, Nucella lapillus. J. anim. Ecol. 48: 65–78.CrossRefGoogle Scholar
  22. Hull, S. L., P. J. Mill & J. Grahame, 1995. Aminotransferases in Littorina: is there a functional story? [Abstract]. Cahiers de Biologie Marine 35: 248–249. Hydrobiologia.Google Scholar
  23. Janson, K., 1987. Allozyme and shell variation in two marine snails (Littorina, Prosobranchia) with different dispersal abilities. Biol. J. linn. Soc. 30: 245–256.CrossRefGoogle Scholar
  24. Janson, K. & R. D. Ward, 1984. Microgeographic variation in allozyme and shell characters in Littorina saxatilis Olivi (Prosobranchia: Littorinidae). Biol. J. linn. Soc. 22: 289–307.CrossRefGoogle Scholar
  25. Johannesson, B., 1986. Shell morphology of Littorina saxatilis Olivi: the relative importance of physical factors and predation. J. exp. mar. Biol. Ecol. 102: 183–195.CrossRefGoogle Scholar
  26. Kemp, P. & M. D. Bertness, 1984. Snail shape and growth rates: evidence for plastic shell allometry in Littorina littorea. Proc. Natn. Acad. Sci. USA 81: 811–813.CrossRefGoogle Scholar
  27. Kitching, J. A. & J. F. Ebling, 1967. Ecological studies at Lough Ine. Adv. ecol. Res. 4: 197–311.CrossRefGoogle Scholar
  28. Knight, A. J. & R. D. Ward, 1986. Purine nucleoside phosphorylase polymorphism in the genus Littorina (Prosobranchia: Mollusca). Biochem. Gen. 24: 405–413.CrossRefGoogle Scholar
  29. Lowell, R. B., 1985. Selection for increased safety factors of biological structures as environmental unpredictability increases. Science 228: 1009–1011.PubMedCrossRefGoogle Scholar
  30. Lowell, R. B., 1986. Crab prediction on limpets: predator behavior and defensive features of the shell morphology of the prey. Biol. Bull. 171: 577–596.CrossRefGoogle Scholar
  31. Lowell, R. B., 1987. Safety factors of tropical versus temperate limpet shells: multiple selection pressures on a single structure. Evolution 41: 638–650.CrossRefGoogle Scholar
  32. Lowell, R. B., C. R. Fletcher, J. Grahame & P. J. Mill, 1994. Ontogeny of shell morphology and shell strength of the marine snails Littorina obtusata and Littorina mariae: different defence strategies in a pair of sympatric, sibling species. J. Zool., Lond. 234: 149–164.CrossRefGoogle Scholar
  33. McMahon, R. F., 1992. Microgeographic variation in the shell morphometrics of Nodilittorina unifasciata from southwestern Australia in relation to wave exposure of shore. In: J. Grahame, P. J. Mill & D. G. Reid (eds), Proceedings of the 3rd International Symposium on Littorinid Biology. The Malacological Society of London, London: 107–117.Google Scholar
  34. Mill, P. J. & J. Grahame, 1992. Clinal changes in esterase variability in Littorina saxatilis (Olivi) and L. arcana Hannaford Ellis in southern Britain. In: J. Grahame, P. J. Mill & D. G. Reid (eds), Proceedings of the 3rd International Symposium on Littorinid Biology. The Malacological Society of London, London: 31–37.Google Scholar
  35. Naylor, R. & M. Begon, 1982. Variation within and between populations of Littorina nigrolineata Gray on Holy Island, Anglesey. J. Conch. 31: 17–30.Google Scholar
  36. Nielsen, C., 1980. On the occurrence of the prosobranchs Littorina neritoides L. mariae and L. obtusata in Denmark. J. moll. Stud. 46: 312–316.Google Scholar
  37. Norton, T. A., S. J. Hawkins, N. L. Manley, G. A. Williams & D. C. Watson, 1990. Scraping a living: a review of littorinid grazing. Hydrobiologia 193(Dev. Hydrobiol. 56): 117–138.CrossRefGoogle Scholar
  38. Palmer, A. R., 1979. Fish predation and evolution of gastropod shell sculpture: experimental and geographic evidence. Evolution 33: 697–713.CrossRefGoogle Scholar
  39. Palmer, A. R., 1981. Do carbonate skeletons limit the rate of body growth? Nature, Lond. 292: 150–152.CrossRefGoogle Scholar
  40. Palmer, A. R., 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(Dev. Hydrobiol. 56): 155–182.CrossRefGoogle Scholar
  41. Peters, R. H., 1983. The ecological implications of body size. Cambridge University Press, Cambridge, England.CrossRefGoogle Scholar
  42. Reid, D. G., 1989. The comparative morphology, phylogeny and evolution of the gastropod family Littorinidae. Phil. Trans. Soc., Lond. B 324: 1–110.CrossRefGoogle Scholar
  43. Reid, D. G., 1990a. Note on the discrimination of females of Littorina mariae Sacchi & Rastrelli and L. obtusata (Linnaeus). J. moll. Stud. 56: 113–114.CrossRefGoogle Scholar
  44. Reid, D. G., 1990b. A cladistic phylogeny of the genus Littorina (Gastropoda): implications for evolution of reproductive strategies and for classification. Hydrobiologia 193(Dev. Hydrobiol. 56): 1–19.CrossRefGoogle Scholar
  45. Reimchen, T. E., 1979. Substratum heterogeneity, crypsis, and colour polymorphism in an intertidal snail (Littorina mariae). Can. J. Zool. 57: 1070–1085.CrossRefGoogle Scholar
  46. Reimchen, T. E., 1981. Microgeographical variation in Littorina mariae Sacchi & Rastelli and a taxanomic consideration. J. Conch. 30: 341–350.Google Scholar
  47. Reimchen, T. E., 1982. Shell size divergence in Littorina mariae and L. obtusata and predation by crabs. Can. J. Zoo. 60: 687–695.CrossRefGoogle Scholar
  48. Ricker, W. E., 1973. Linear regressions in fishery research. J. Fish. Res. Bd. Can. 30: 409–434.CrossRefGoogle Scholar
  49. Rolán-Alvarez, E., 1992. A method of breeding Littorina obtusata (L.) and L. mariae Sacchi & Rastelli: preliminary results. In: J. Grahame, P. J. Mill & D. G. Reid (eds), Proceedings of the 3rd International Symposium on Littorinid Biology. The Malacological Society of London, London: 163–180.Google Scholar
  50. Rolán-Alvarez, E., K. Johannesson & A. Ekendahl, 1995. Frequency-and density-dependent sexual selection in natural populations of Galician Littorina saxatilis (Olivi). Hydrobiologia 309(Dev. Hydrobiol. 111): 167–172.CrossRefGoogle Scholar
  51. Sacchi, C. F., 1969. Recherches sur L’écologie comparée de Littorina obtusata (L.) et de Littorina mariae Sacchi et Rastelli (Gastropoda, Prosobranchia) en Galice et en Bretagne. Investigatión Pesquera 33: 381–414.Google Scholar
  52. Sacchi, C. F. & M. Rastelli, 1966. Littorina mariae, nov. sp.: les différences morphologiques et écologiques entre ‘nains’ en ‘normeaux’ chez l’‘espece’ L. obtusata (L.) (Gastr. Prosobr.) et leur significance adaptive et évolutive. Atti delia Società Italiana de Scienze Naturali e del Museo Civico di Storia Naturale di Milano 105: 351–370.Google Scholar
  53. Smith, D., P. J. Mill & J. Grahames, 1995. Environmentally induced variation in uric acid concentration and xanthine dehydrogenase activity in Littorina saxaiilis (Olivi) and L. arcana Hannaford Ellis. Hydrobiologia 309(Dev. Hydrobiol. 111): 111–116.CrossRefGoogle Scholar
  54. Sokal, R. R. & F. J. Rohlf, 1981. Biometry, 2nd ed. Freeman & Co., New York.Google Scholar
  55. Sundberg, P., A. J. Knight, R. D. Ward & K. Johannesson, 1990. Estimating the phylogeny in mollusc Littorina saxatilis (Olivi) from enzyme data: methodological considerations. Hydrobiologia 193(Dev. Hydrobiol. 56): 29–40.CrossRefGoogle Scholar
  56. Tresierra-Aquilar, A., 1985. Between site variation in shell and body measures of Littorina littorea. Biol. Bull. 169: 537–538.Google Scholar
  57. Vermeij, G. J., 1978. Biogeography and Adaptation. Harvard University Press, Cambridge.Google Scholar
  58. Vermeij, G. J. & J. D. Currey, 1980. Geographical variation in the strength of thaiid snail shells. Biol. Bull. 158: 383–389.CrossRefGoogle Scholar
  59. Ward, R. D., 1990. Biochemical genetic variation in the genus Littorina (Prosobranchia: Mollusca). Hydrobiologia 193(Dev. Hydrobiol. 56): 53–69.CrossRefGoogle Scholar
  60. Warmoes, T., T. Backeljau & L. de Bruyn, 1988. The littorinid fauna of the Belgian coast (Mollusca, Gastropoda). Bull. Inst. r. Sci. nat. Belg. 58: 51–70.Google Scholar
  61. Watson, D. C. & T. A. Norton, 1987. The habitat and feeding preferences of Littorina obtusata (L.) and L. mariae Sacchi et Rastelli. J. exp. mar. Biol. Ecol. 112: 61–72.CrossRefGoogle Scholar
  62. Williams, G. A., 1990a. Littorina mariae — a factor structuring low shore communities? Hydrobiologia 193(Dev. Hydrobiol. 56): 139–146.CrossRefGoogle Scholar
  63. Williams, G. A., 1990b. The comparative ecology of the flat periwinkles, Littorina obtusata (L.) and L. mariae Sacchi et Rastelli. Field Studies 7: 469–482.Google Scholar
  64. Williams, G. A., 1992. The effect of predation on the life histories of Littorina obtusata and L. mariae. J. mar. biol. Ass. U.K. 72: 403–416.CrossRefGoogle Scholar
  65. Williams, G. A., 1995. Maintenance of zonation patterns in two species of flat periwinkle, Littorina obtusata and L. mariae. Hydrobiologia 309(Dev. Hydrobiol. 111): 143–150.CrossRefGoogle Scholar
  66. Zipser, E. & G. J. Vermeij, 1978. Crushing behaviour of tropical and temperate crabs. J. exp. mar. Biol. Ecol. 31: 155–172.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 1995

Authors and Affiliations

  • C. R. Fletcher
    • 1
  1. 1.Department of Pure and Applied BiologyUniversity of LeedsLeedsUK

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