Skip to main content
SpringerLink
Log in

Intraspecific density mediates sex-change in the territorial patellacean limpet Lottia gigantea

  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

The effects of intraspecific density and agonistic interactions on sex-change were studied in the territorial limpet Lottia gigantea. In a one-year field experiment (1982–1983) on San Nicolas Island off the southern California coast, USA, male limpets transplanted to large enclosures changed sex more frequently than those transplanted to small enclosures (9 of 13 vs 1 of 10; p=0.013), indicating that intraspecific density can profoundly influence the probability of sex change. Large limpets were more likely to change sex than small ones. Observations of gender-age distributions as well as field behavior suggested that each limpet's territorial status prior to the experiment may have been an important component of this size effect, although other interpretations including an effect of age are possible. Pooling the results with those of two previous studies confirmed that sex-change is enhanced by low density. This enhancement was observed among the largest members of a local population in the first year of each experiment, while among the smaller members the enhancement was delayed until the second or third year. Low density may be a correlate of high mortality, and therefore an adaptive cue for an earlier age of sex change. Dominant territorial status correlates with an individual's size, and therefore egg-producing capacity, relative to its neighbors, and thus may also be a good cue for the initiation of sex-change.

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

Similar content being viewed by others

Literature cited

  • Ankel, W. E. (1936). Prosobranchia. Tierwelt N. u. Ostsee 29: 1–240

    Google Scholar 

  • Bacci, G. (1947). Sex reversal in Patella and Diodora. Nature, Lond. 160: p. 94

    Google Scholar 

  • Bacci, G. (1965). International series of monographs in pure and applied biology. Vol. 26. Sex determination. Pergamon Press, Oxford

    Google Scholar 

  • Bacci, G. (1978). Genetics of sex determination in Ophryotrocha (Annelida, Polychaeta). In: Battaglia, B., Beardmore, J. (eds.) Marine organisms: genetics, ecology, and evolution. Plenum Press, New York

    Google Scholar 

  • Ballantine, W. J. (1961). The population dynamics of Patella vulgata and other limpets. Ph.D. thesis. Queen Mary College, London University

  • Blackmore, D. T. (1969). Studies of Patella vulgata L. I. Growth, reproduction and zonal distribution. J. exp. mar. Biol. Ecol. 3: 200–213

    Google Scholar 

  • Branch, G. M. (1974a). The ecology of Patella Linnaeus from the Cape peninsula, South Africa, 2. Reproductive cycles. Trans. R. Soc. S. Afr. 41: 111–160

    Google Scholar 

  • Branch, G. M. (1974b). The ecology of Patella linnaeus from the Cape peninsula, South Africa, 3. Growth rates. Trans. R. Soc. S. Afr. 41: 161–193

    Google Scholar 

  • Branch, G. M. (1975a). Intraspecific competition in Patella cochlear Born. J. Anim. Ecol. 44: 263–282

    Google Scholar 

  • Branch, G. M. (1975b). Mechanisms reducing intraspecific competition in Patella spp.: migration, differentiation, and territorial behavior. J. Anim. Ecol. 44: 575–600

    Google Scholar 

  • Branch, G. M. (1981). The biology of limpets: physical factors, energy flow and ecological interactions. Oceanogr. mar. Biol. A. Rev. 19: 235–379

    Google Scholar 

  • Breyer, A. (1980). Life history of Epitonium tinctum (Prosobranchia: Mesogastropoda). A. Rep. west. Soc. Malacologists 12: p. 9

    Google Scholar 

  • Charnov, E. L. (1982). The theory of sex allocation. Princeton University Press, Princeton, New Yersey

    Google Scholar 

  • Charnov, E. L., Bull, J. J. (1977). When is sex environmentally determined? Nature, Lond. 266: 828–830

    Google Scholar 

  • Coe, W. R. (1953). Influences of association, isolation, and nutrition on the sexuality of snails of the genus Crepidula. J. exp. Zool. 122: 5–19

    Google Scholar 

  • Daley, G. P. (1975). The effects of the reproductive cycle on seasonal growth trends in the owl limpet, Lottia gigantea. Bull. Am. malac. Un. 1975: p. 69

    Google Scholar 

  • Fisher, W. K. (1904). The anatomy of Lottia gigantea Gray. Zool. Jb. (Abt. Anat. Ont Tiere) 20: 1–66

    Google Scholar 

  • Fishelson, L. (1970). Protogynous sex reversal in the fish Anthias squamipinnis (Teleostei, Anthiidae) regulated by the presence or absence of a male fish. Nature, Lond. 227: 90–91

    Google Scholar 

  • Frank, P. W. (1965). Shell growth in a natural population of the turban snail, Tegula funebralis. Growth 29: 395–403

    Google Scholar 

  • Fretter, V. (1984). Prosobranch gastropods. In: Wilbur, K. M. (ed.) The Mollusca, 7: Reproduction. Academic Press, New York

    Google Scholar 

  • Fricke, H., Fricke, S. (1977). Monogamy and sex change by aggressive dominance in coral reef fish. Nature, Lond. 266: 830–832

    Google Scholar 

  • Funke, W. (1968). Heimfindevermögen und Ortstreue bei Patella L. (Gastropoda, Prosobranchia). Oecologia (Berl.) 2: 19–142

    Google Scholar 

  • Galbraith, R. (1965). Homing behavior in the limpets Acmaea digitalis and Lottia gigantea. Am. Midl. Nat. 74: 245–246

    Google Scholar 

  • Ghiselin, M. T. (1969). The evolution of hermaphroditism among animals. Q. Rev. Biol. 44: 189–208

    Google Scholar 

  • Gould, H. N. (1919). Studies on sex in the hermaphrodite mollusc Crepidula plana. III. Transference of the male-producing stimulus through sea-water. J. exp. Zool. 29: 113–120

    Google Scholar 

  • Gould, H. N. (1952). Studies on sex in the hermaphrodite mollusc Crepidula plana. 4. Internal and external factors influencing growth and sex development. J. exp. Zool. 119: 93–163

    Google Scholar 

  • Hawkins, S. J., Hartnoll, R. G. (1982). The influence of barnacle cover on the numbers, growth and behaviour of Patella vulgata on a vertical pier. J. mar. biol. Ass. U.K. 62: 855–867

    Google 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 

  • Leigh, E. G. Jr., Charnov E. L., Warner, R. R. (1976). Sex ratio, sex change, and natural selection. Proc. natn. Acad. Sci. U.S.A. 73: 3656–3660

    Google Scholar 

  • Lewis, J. R., Bowman, R. S. (1975). Local habitat-induced variations in the population dynamics of Patella vulgata L. J. exp. mar. Biol. Ecol. 17: 165–203

    Google Scholar 

  • Lindberg, D. R., Wright, W. G. (1985). Patterns of sex change of the protandric patellacean limpet Lottia gigantea (Mollusca: Gastropoda). Veliger 27: 261–265

    Google Scholar 

  • Montalenti, G., Bacci, G. (1951). Osservazioni e ipotesi sulla determinazione del sesso negli ermafroditi. Scientia genet. 4: 5–12

    Google Scholar 

  • Orton, J. H. (1927). A note on the physiology of sex and sex determination. J. mar. biol. Ass. U.K. 14: 1047–1055

    Google Scholar 

  • Orton, J. H. (1928). Observations on Patella vulgata. I. Sex phenomena, breeding, and shell growth. J. mar. biol. Ass. U.K. 15: 851–862

    Google Scholar 

  • Orton, J. H., Southward, A. J., Dodd, J. M. (1956). Studies on the biology of limpets. II. The breeding of Patella vulgata L. in Britain. J. mar. biol. Ass. U.K. 35: 149–176

    Google Scholar 

  • Parker, G. A. (1970). Sperm competition and its evolutionary consequences in the insects. Biol. Rev. 45: 525–567

    Google Scholar 

  • Parker, G. A. (1984). Sperm competition and the evolution of animal mating strategies. In: Smith, R. L. (ed.) Sperm competition and the evolution of animal mating systems. Academic Press, Orlando, Florida

    Google Scholar 

  • Pennington, J. T. (1984). The ecology of fertilization of echinoid eggs: the consequences of sperm dilution, adult aggregation, and synchronous spawning. Am. Zool. 24: p. 130 A

    Google Scholar 

  • Picken, G. B. (1980). The distribution, growth, and reproduction of the Antarctic limpet Nacella (patinigera) concinna (Strebel, 1908). J. exp. mar. Biol. Ecol. 42: 71–85

    Google Scholar 

  • Policansky, D. (1982). Sex change in plants and animals. A. Rev. Ecol. Syst. 13: 471–495

    Google Scholar 

  • Robertson, D. R. (1972). Social control of sex reversal in a coral reef fish. Science, N.Y. 177: 1007–1009

    Google Scholar 

  • Russell-Hunter, W. D. (1979). A life of Invertebrates. MacMillan, New York

    Google Scholar 

  • Russell-Hunter, W. D., McMahon, R. F. (1975). An anomalous sex-ratio in the sublittoral marine snail Lacuna vincta Turton, from near Woods Hols. Nautilus 89: 14–16

    Google Scholar 

  • Russell-Hunter, W. D., McMahon, R. F. (1976). Evidence for functional protandry in a fresh-water basommatophoran limpet, Laevapex fuscus. Trans. Am. microsc. Soc. 95: 174–182

    Google Scholar 

  • Sastry, A. N. (1979). Petecypoda (excluding Ostreidae). In: Giese, A. C., Pearse, J. S. (eds.) Reproduction of marine invertebrates, Vol. 5. Academic Press, New York

    Google Scholar 

  • Shanks, A. L., Wright, W. G. (1986). Adding teeth to wave action: the destructive effects of waveborne rocks on intertidal organisms. Oecologia 69: 420–428

    Google Scholar 

  • Smith, R. L. (ed.) (1984) Sperm competition and the evolution of animal mating systems. Academic Press, Orlando, Florida

    Google Scholar 

  • Sokal, R. R., Rohlf, F. J. (1981). Biometry. The principles and practice of statistics in biological research. 2nd ed. W. H. Freeman & Co., San Francisco

    Google Scholar 

  • Steele, M. E. (1984). Growth and behavior of the owl limpet Lottia gigantea: a field and laboratory study using time lapse cinematography. Master's thesis, University of California, Santa Cruz

    Google Scholar 

  • Stimson, J. S. (1968). The population ecology of the limpets Lottia gigantea (Gray) and several species of Acmaea (Eschsholtz) coexisting on an intertidal shore. PhD dissertation, University of California Santa Barbara

    Google Scholar 

  • Stimson, J. S. (1970). Territorial behavior of the owl limpet Lottia gigantea. Ecology 51: 113–118

    Google Scholar 

  • Stimson, J. S. (1973). The role of the territory in the ecology of the owl limpet Lottia gigantea (Gray). Ecology 54: 1020–1030

    Google Scholar 

  • Sutherland, J. P. (1970). Dynamics of high and low populations of the limpet, Acmaea scabra (Gould). Ecol. Monogr. 40: 169–188

    Google Scholar 

  • Thompson, G. B. (1980). Distribution and population dynamics of the limpet Patella vulgata L. in Bantry Bay. J. exp. mar. Biol. Ecol. 45: 173–217

    Google Scholar 

  • Tranter, D. J. (1958). Reproduction in Australian pearl oysters (Lamellibranchia) III. Pictada albina (Lamarck) breeding season and sexuality. Aust. J. mar. Freshwat. Res. 9: 191–216

    Google Scholar 

  • Von Medem, F. G. (1945). Untersuchungen über die Ei- und Spermawirkstoffe bei marinen Mollusken. Zool. Jb. (Abt. Anat. Ont. Tiere) 61: 1–44

    Google Scholar 

  • Warner, R. R. (1975). The adaptive significance of sequential hermaphroditism in animals. Am. Nat. 109: 61–82

    Google Scholar 

  • Webber, H. H. (1977). Gastropoda: Prosobranchia. In: Giese, A. C., Pearse, J. S. (eds.) Reproduction of marine Invertebrates, Vol. 4. Academic Press, New York

    Google Scholar 

  • Wright, W. G. (1982). Ritualized behavior in a territorial limpet. J. exp. mar. Biol. Ecol. 60: 245–251

    Google Scholar 

  • Wright, W. G. (1985). The behavioral ecology of the limpet Lottia gigantea: interaction between territoriality, demography, and protandric hermaphroditism. Ph.D. dissertation, University of California, San Diego

    Google Scholar 

  • Wright, W. G., Lindberg, D. R. (1979). A non-fatal method of sex determination for patellacean gastropods. J. mar. biol. Ass. U.K. 59: p. 803

    Google Scholar 

  • Wright, W. G., Lindberg, D. R. (1982). Direct observation of sex change in the patellacean limpet Lottia gigantea. J. mar. biol. Ass. U.K. 62: 737–738

    Google Scholar 

Download references

Author information

Author notes

  1. W. G. Wright

    Present address: Department of Psychology, Yale University, Yale Station, P.O. Box 1 A, 06520, New Haven, Connecticut, USA

Authors and Affiliations

  1. Scripps Institution of Oceanography, University of California at San Diego, 92093, La Jolla, California, USA

    W. G. Wright

Authors
  1. W. G. Wright
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Communicated by P. C. Schroeder, Pullman

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wright, W.G. Intraspecific density mediates sex-change in the territorial patellacean limpet Lottia gigantea . Mar. Biol. 100, 353–364 (1989). https://doi.org/10.1007/BF00391151

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00391151

Keywords

Search

Navigation