Marine Biology

, Volume 159, Issue 9, pp 2015–2023 | Cite as

The selective advantage of host feminization: a case study of the green crab Carcinus maenas and the parasitic barnacle Sacculina carcini

  • Tommy Kristensen
  • Anders Isberg Nielsen
  • Anders Isak Jørgensen
  • Kim N. Mouritsen
  • Henrik Glenner
  • Jens T. Christensen
  • Jørgen Lützen
  • Jens T. Høeg
Original Paper

Abstract

Male crabs infected by parasitic barnacles (Rhizocephala) are known to be morphologically feminized. Here, we investigate morphological chances in green crabs, Carcinus maenas, induced by the parasitic barnacle Sacculina carcini. Infected males acquire a broader, longer and segmented abdomen, fringed with marginal setae. Copulatory appendages and pereopods are reduced in length, and the chelae become smaller. The feminization show great individual variation. Males with scars from lost externae, the parasites reproductive organ situated under the abdomen, are less modified than males carrying an externa, and the feminization is more pronounced in smaller than in larger males. No super-feminization is evident in female crabs that remain morphologically unaffected by infection. The protective value of a parasitically induced enlargement of the male abdomen may constitute an adaptation that increases parasite longevity. The additional effects on male morphology are viewed as pleiotropic side effects of the main adaptive value of enlarging the abdomen.

Notes

Acknowledgments

We are very grateful to the Carlsberg Foundation for covering all expenses connected with the study (grant no. 2008-01-0491). We also wish to thank the staff of the Danish Shellfish Center, Nykøbing Mors, Denmark, for collecting some of the material and providing laboratory facilities, and Dr. David R. Nash, Section for Social Evolution, Department of Biology, University of Copenhagen, Denmark, for advice and assistance.

References

  1. Bulgurkov K (1938) Study of Rhizocephala and Bopyridae from the Bulgarian Black Sea coast. Trudy na Chernorskata Biol Sta. v’Varna 7:69–81Google Scholar
  2. Day JH (1935) The life-history of Sacculina. Q J Microsc Sci 77:549–583Google Scholar
  3. Foxon GEH (1940) Notes on the life history of Sacculina carcini Thompson. J Mar Biol Assoc UK 24:253–264CrossRefGoogle Scholar
  4. Galil BS, Lützen J (1995) Biological observations on Heterosaccus dollfusi Boschma (Cirripedia: Rhizocephala), a parasite of Charybdis longicollis Leene (Decapoda: brachyura), a lessepsian migrant to the Mediterranean. J Crust Biol 15:659–670CrossRefGoogle Scholar
  5. George AI (1959) Heterosaccus ruginosus (Boschma), a rhizocephalan parasite of the crab Neptunus sanguinolentus (Herbst). J Zool Soc India 11:171–204Google Scholar
  6. Giard A (1886) De l’influence de certains parasitès rhizocéphales sur les caractères sexuels extérieures de leur hôte. C R Hebd Acad Sci 103:84–86Google Scholar
  7. Glenner H, Hebsgaard MB (2006) Phylogeny and evolution of life history strategies of the parasitic barnacles (Crustacea, Cirripedia, Rhizocephala). Mol Phylogenet Evol 41:528–538CrossRefGoogle Scholar
  8. Hartnoll RG (1967) The effects of sacculinid parasites on two Jamaican crabs. J Linn Soc (Zool) 46:275–295CrossRefGoogle Scholar
  9. Høeg JT (1995) The biology and life cycle of the Rhizocephala (Cirripedia). J Mar Biol Assoc UK 75:517–550CrossRefGoogle Scholar
  10. Høeg JT, Lützen J (1985) Crustacea Rhizocephala. Marine invertebrates of Scandinavia 6. Norwegian University Press, Oslo, pp 1–92Google Scholar
  11. Lützen J (1981) Field studies on regeneration in Sacculina carcini Thompson (Crustacea: rhizocephala) in the Isefjord, Denmark. J Exp Mar Biol Ecol 53:241–249CrossRefGoogle Scholar
  12. Lützen J (1984) Growth, reproduction and life span in Sacculina carcini Thompson (Cirripedia: rhizocephala) in the Isefjord, Denmark. Sarsia 69:91–106Google Scholar
  13. Matsumoto K (1952) On the sacculinization of Charybdis japonioca (A. Milne-Edwards). Biol J Okayama Univ 1:84–89Google Scholar
  14. Nair NB, Gurumani ON (1956) On the occurrence of three Sacculina parasitising the edible crab Neptunus sanguinolentus. J Bombay Nat Hist Soc 53:730–732Google Scholar
  15. Nielsen S-O (1970) The effects of the rhizocephalan parasites Peltogaster paguri Rathke and Gemmosaccus sulcatus (Lilljeborg) on five species of paguridan hosts (Crustacea: decapoda). Sarsia 42:17–32Google Scholar
  16. Okada YK, Miyashita Y (1935) Sacculinization in Eriocheir japonicus de Haan, with remarks on the occurrence of complete sex-reversal in parasitized male crabs. Mem Col Sci Kyoto Imp Univ B 10:169–208Google Scholar
  17. Øksnebjerg B (2000) The Rhizocephala (Crustacea: cirripedia) of the Mediterranean and Black Seas: taxonomy, biogeography, and ecology. Israel J Zool 46:1–102CrossRefGoogle Scholar
  18. Pérez C (1933) Action de la sacculine sur les caractères sexuels extérieures du Pachygrapsus marmoratus. C R Soc Biol Paris 113:1027–1029Google Scholar
  19. Phillips WJ, Cannon LRG (1978) Ecological observations on the commercial sand crab, Portunus pelagicus (L.), and its parasite, Sacculina granifera Boschma, 1973 (Cirripedia: rhizocephala). J Fish Dis 1978:137–149CrossRefGoogle Scholar
  20. Potts FA (1909) Observations on the changes in the common shore-crab caused by Sacculina. P Camb Philos Soc 15:96–100Google Scholar
  21. Reinhard EG (1950) An analysis of the effects of a sacculinid pasrasite on the external morphology of Callinectes sapidus Rathbun. Biol Bull Wood’s Hole 98:255–288Google Scholar
  22. Smith G (1906) Rhizocephala. Fauna Flora Golf Neapel 29:1–123Google Scholar
  23. Smith G (1910) Studies in the experimental analysis of sex. Part 3. Further observations on parasitic castration. Q J Microsc Sci 55:225–240Google Scholar
  24. Srinivasagam S (1982) An instance of large scale parasitism of Heterosaccus dollfusi Boschma on the edible crab, Portunus sanguinoletus (Herbst) in Pulicat Lake. J Inland Fish Soc India 14:88–90Google Scholar
  25. Veillet A (1945) Recherches sur le parasitisme des crabes et des Galathées par les Rhizocéphales et les épicarides. Ann I Océanogr Paris 22:193–341Google Scholar
  26. Veillet A, Graf F (1958) Dégénérescence de la glande androgène des Crustacés décapodes parasités par les Rhizocéphales. Bull Mens Soc Sci N 18:123–127Google Scholar
  27. Vernet-Cornubert G (1958) Recherches sur la sexualité du crabe Pachygrapsus marmoratus (Fabricius). Arch Zool Exp Gén 96:101–276Google Scholar
  28. Weng HT (1987) The parasite barnacle, Sacculina granifera Boschma, affecting the commercial sand crab, Portunus pelagicus (L.), in populations from two different environments in Queensland. J Fish Dis 10:221–227CrossRefGoogle Scholar
  29. Werner M (2001) Prevalence of the parasite Sacculina carcini Thompson 1836 (Crustacea, Rhizocephala) on its host crab Carcinus maenas (L.) on the west coast of Sweden. Ophelia 55:101–110CrossRefGoogle Scholar
  30. Yamaguchi T, Aratake H (1997) Morphological modifications caused by Sacculina polygenea in Hemigrapsus sanguineus (De Haan) (Brachyura: grapsidae). Crust Res 23:89–101Google Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Tommy Kristensen
    • 2
  • Anders Isberg Nielsen
    • 1
  • Anders Isak Jørgensen
    • 1
  • Kim N. Mouritsen
    • 1
  • Henrik Glenner
    • 3
  • Jens T. Christensen
    • 1
  • Jørgen Lützen
    • 2
  • Jens T. Høeg
    • 2
  1. 1.Department of Bioscience, Marine EcologyAarhus UniversityAarhus CDenmark
  2. 2.Department of Biology, Section for Marine BiologyCopenhagen UniversityCopenhagenDenmark
  3. 3.Department of Biology, Biological InstituteUniversity of BergenBergenNorway

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