Hostname: page-component-76fb5796d-vvkck Total loading time: 0 Render date: 2024-04-27T21:45:46.112Z Has data issue: false hasContentIssue false
  • English
  • Français

Parasitization of a hydrothermal vent limpet (Lepetodrilidae, Vetigastropoda) by a highly modified copepod (Chitonophilidae, Cyclopoida)

Published online by Cambridge University Press:  29 July 2008

V. TUNNICLIFFE ,
J. M. ROSE ,
A. E. BATES  and
N. E. KELLY
V. TUNNICLIFFE*
Affiliation:
Department of Biology, University of Victoria, PO Box 3020, Victoria, BCCanadaV8W 3N5 School of Earth and Ocean Sciences, University of Victoria, PO Box 3020, Victoria, BCCanadaV8W 3N5
J. M. ROSE
Affiliation:
Department of Biology, University of Victoria, PO Box 3020, Victoria, BCCanadaV8W 3N5
A. E. BATES
Affiliation:
Department of Biology, University of Victoria, PO Box 3020, Victoria, BCCanadaV8W 3N5
N. E. KELLY
Affiliation:
Department of Oceanography, Dalhousie University, 1355 Oxford Street, Halifax, NSCanadaB3H 4J1
*
*Corresponding author: Department of Biology, University of Victoria, PO Box 3020, Victoria, BCCanadaV8W 3N5. Tel: 1 250 721 7135. Fax: 1 250 721 7120. E-mail: verenat@uvic.ca
Get access Rights & Permissions [Opens in a new window]

Summary

The limpet Lepetodrilus fucensis McLean is very abundant at hydrothermal vents on the Juan de Fuca and Explorer Ridges in the northeast Pacific Ocean. This limpet is parasitized by an undescribed chitonophilid copepod throughout the limpet's range. The parasite copepodite enters the mantle cavity and attaches to the afferent branchial vein. The initial invasive stage is a vermiform endosome within the vein that develops an extensive rootlet system causing an enlargement of the afferent branchial vein. Subsequently, an ectosomal female body grows outside the vein to sizes up to 2 mm in width. Once a dwarf male attaches, egg clusters form and nauplii are released. In over 3000 limpets examined from 30 populations, prevalence averaged about 5% with localized infections in female limpets over 25%. After the establishment of limpet populations at new vents, copepod prevalence increased over the succeeding months to 3 years. Host effects were marked and included castration of both sexes and deterioration in gill condition which affected both food acquisition and the gill symbiont. There was a significantly greater parasite prevalence in larger females which likely modifies the reproductive and competitive success of local host populations.

Keywords

ChitonophilidaeLepetodrilaceahydrothermal ventparasitizationpathogenesisparasitic copepodcastrationhost conditionhost sex bias
Type
Original Articles
Information
Parasitology , Volume 135 , Issue 11 , September 2008 , pp. 1281 - 1293
Copyright
Copyright © 2008 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Avdeev, G. V. and Sirenko, B. I. (1991). Chitonophilidae fam. n., a new family of parasitic copepods from the chitons of the North-Western Pacific. Parazitologiya 25, 370–374.Google Scholar
Avdeev, G. V. and Sirenko, B. I. (2005). New and recognized species of copepods (Chitonophilidae) – parasites of chitons of Northern Pacific. Parazitologiya 39, 516–543.Google Scholar
Bates, A. E. (2007 a). Persistence, morphology, and nutritional state of a gastropod hosted bacterial symbiosis in different levels of hydrothermal vent flux. Marine Biology 152, 557–568.Google Scholar
Bates, A. E. (2007 b). Feeding strategy, morphological specialization, and the presence of bacterial episymbionts in lepetodrilid gastropods from hydrothermal vents. Marine Ecology Progress Series 347, 87–99.CrossRefGoogle Scholar
Bates, A. E., Tunnicliffe, V. and Lee, R. W. (2005). Role of thermal conditions in habitat selection by hydrothermal vent gastropods. Marine Ecology Progress Series 305, 1–15.Google Scholar
Brown, S. P., Loot, G., Grenfell, B. T. and Guegan, J. F. (2001). Host manipulation by Ligula intestinalis: accident or adaptation? Parasitology 123, 519–529.Google Scholar
Bush, A. O., Lafferty, K. D., Lotz, J. M. and Shostak, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575–583.CrossRefGoogle Scholar
de Buron, I. and Morand, S. (2004). Deep-sea hydrothermal vent parasites: why do we not find more? Parasitology 128, 1–6.Google Scholar
Ebert, D., Carius, H., Little, T. and Decasestecker, E. (2004). The evolution of virulence when parasites cause host castration and gigantism. The American Naturalist 164, S19–S32.Google Scholar
Embley, R. W., Chadwick, J. W. W., Clague, D. and Stakes, D. (1999). 1998 Eruption of Axial Volcano: Multibeam anomalies and seafloor observations. Geophysical Research Letters 26, 3425–3428.CrossRefGoogle Scholar
Franz, J. C. and Bullock, R. C. (1990). Ischnochitonika lasalliana, new genus, new species (Copepoda), a parasite of tropical western Atlantic chitons (Polyplacophora: Ischnochitonidae). Journal of Crustacean Biology 10, 544–549.Google Scholar
Fretter, V. (1988). New archaeogastropod limpets from hydrothermal vents; Superfamily Lepetodrilacea II. In Mid-Ocean Ridges: Dynamics of Processes Associated with Creation of New Ocean Crust (ed. Cann, J. R., Elderfield, H. and Laughton, A.), Vol. 318, pp. 33–82. Philosophical Transactions of the Royal Society of London, Series B.Google Scholar
Gotto, R. V. (1962). Egg-number and ecology in commensal and parasitic copepods. Annals and Magazine of Natural History 5, 97–107.Google Scholar
Hall, S. R., Becker, C. and Caceres, C. E. (2007). Parasitic castration: a perspective from a model of dynamic energy budgets. Integrative and Comparative Biology 47, 295–309.CrossRefGoogle Scholar
Hurd, H. (2001). Host fecundity reduction: a strategy for damage limitation? Trends in Parasitology 17, 363–368.Google Scholar
Huys, R., Lopez-Gonzalez, P. J., Roldan, E. and Luque, A. A. (2002). Brooding in cocculiniform limpets (Gastropoda) and familial distinctiveness of the Nucellicolidae (Copepoda): misconceptions reviewed from a chitonophilid perspective. Biological Journal of the Linnean Society 75, 187–217.Google Scholar
Jones, J. B. and Marshall, B. A. (1986). Cocculinika myzorama, new genus, new species, a parasitic copepod from a deep-sea wood-ingesting limpet. Journal of Crustacean Biology 6, 166–169.CrossRefGoogle Scholar
Kelly, N. E. and Metaxas, A. (2007). Influence of habitat on the reproductive biology of the deep-sea hydrothermal vent limpet Lepetodrilus fucensis (Vetigastropoda: Mollusca) from the Northeast Pacific. Marine Biology 151, 649–662.Google Scholar
Lamb, E. J., Boxshall, G. A., Mill, P. J. and Grahame, J. (1996). Nucellicolidae: a new family of endoparasitic copepods (Poecilostomatoida) from the dog whelk Nucella lapillus (Gastropoda). Journal of Crustacean Biology 16, 142–148.Google Scholar
Lamb, E. J., Boxshall, G. A., Mill, P. J. and Grahame, J. (1998). Postembryonic stages of Nucellicola holmanae (Copepoda, Poecilostomatoida), an endoparasite of the dog whelk Nucella lapillus (Gastropoda). Journal of Marine Systems 15, 261–267.Google Scholar
Marcus, J. and Tunnicliffe, V. (2002). Living on the edges of diffuse vents on the Juan de Fuca Ridge. Cahiers de Biologie Marine 43, 263–266.Google Scholar
Metaxas, A. (2004). Spatial and temporal patterns in larval supply at hydrothermal vents in the northeast Pacific Ocean. Limnology and Oceanography 49, 1949–1956.Google Scholar
Micheli, F., Peterson, C. H., Mullineaux, L. S., Fisher, C. R., Mills, S. W., Sancho, G., Johnson, G. A. and Lenihan, H. S. (2002). Predation structures communities at deep-sea hydrothermal vents. Ecological Monographs 72, 365–382.Google Scholar
Moore, J. (2002). Parasites and Behavior of Animals. Oxford University Press.CrossRefGoogle Scholar
Moore, S. L. and Wilson, K. (2002). Parasites as a viability cost of sexual selection in natural populations of mammals. Science 297, 2015–2018.CrossRefGoogle ScholarPubMed
Mouritsen, K. N. and Poulin, R. (2002). Parasitism, community structure and biodiversity in intertidal ecosystems. Parasitology 124, S101–S117.Google Scholar
Poulin, R. (1995). Clutch size and egg size in free-living and parasitic copepods – a comparative-analysis. Evolution 49, 325–336.Google Scholar
Poulin, R. (1996 a). Sexual size dimorphism and transition to parasitism in copepods. Evolution 50, 2520–2523.CrossRefGoogle ScholarPubMed
Poulin, R. (1996 b). Sexual inequalities in helminth infections: a cost of being a male? The American Naturalist 147, 287–295.Google Scholar
Ramirez Llodra, E. (2002). Fecundity and life-history strategies in marine invertebrates. Advances in Marine Biology 43, 87–170.Google Scholar
Robb, T. and Forbes, M. R. (2006). Sex biases in parasitism of newly emerged damselflies. Ecoscience 13, 1–4.Google Scholar
Sarrazin, J. and Juniper, S. K. (1999). Biological characteristics of a hydrothermal edifice mosaic community. Marine Ecology Progress Series 185, 1–19.CrossRefGoogle Scholar
Sheridan, L. A., Poulin, R., Ward, D. F. and Zuk, M. (2000). Sex differences in parasitic infections among arthropod hosts: is there a male bias? Oikos 88, 327–334.CrossRefGoogle Scholar
Slansky, F. (1986). Nutritional ecology of endoparasitic insects and their hosts – an overview. Journal of Insect Physiology 32, 255–261.Google Scholar
Terlizzi, C. M., Ward, M. E. and Van Dover, C. L. (2004). Observations on parasitism in deep-sea hydrothermal vent and seep limpets. Diseases of Aquatic Organisms 62, 17–26.Google Scholar
Tsurumi, M. (2003). Diversity at hydrothermal vents. Global Ecology and Biogeography 12, 181–190.Google Scholar
Tsurumi, M. and Tunnicliffe, V. (2003). Tubeworm-associated communities at hydrothermal vents on the Juan de Fuca Ridge, northeast Pacific. Deep-sea Research I 50, 611–629.Google Scholar
Van Dover, C. L. (2002). Community structure of mussel beds at deep-sea hydrothermal vents. Marine Ecology Progress Series 230, 137–158.CrossRefGoogle Scholar
Webb, T. J. and Hurd, H. (1999). Direct manipulation of insect reproduction by agents of parasitic origin. Proceedings of the Royal Society of London, B 266, 1537–1541.CrossRefGoogle Scholar