Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-22T20:44:05.790Z Has data issue: false hasContentIssue false

Interactions between parasites of the cockle Austrovenus stutchburyi: hitch-hikers, resident-cleaners, and habitat-facilitators

Published online by Cambridge University Press:  16 October 2006

T. L. F. LEUNG
Affiliation:
Department of Zoology, University of Otago, P. O. Box 56, Dunedin 9054, New Zealand
R. POULIN
Affiliation:
Department of Zoology, University of Otago, P. O. Box 56, Dunedin 9054, New Zealand

Abstract

The patterns of association between parasites within a particular host are determined by a number of factors. One of these factors is whether or not infection by one parasite influences the probability of acquiring other parasite species. This study investigates the pattern of association between various parasites of the New Zealand cockle Austrovenus stutchburyi. Hundreds of cockles were collected from one locality within Otago Harbour, New Zealand and examined for trematode metacercariae and other symbionts. Two interspecific associations emerged from the study. First, the presence of the myicolid copepod Pseudomyicola spinosus was positively associated with higher infection intensity by echinostomes. The side-effect of the copepod's activities within the cockle is suggested as the proximate mechanism that facilitates infection by echinostome cercariae, leading to a greater rate of accumulation of metacercariae in cockles harbouring the copepod. Second, a positive association was also found between infection intensity of the metacercariae of foot-encysting echinostomes and that of gymnophallid metacercariae. This supports earlier findings and suggests that the gymnophallid is a hitch-hiker parasite because, in addition to the pattern of positive association, it (a) shares the same transmission route as the echinostomes, and (b) unlike the echinostomes, it is not capable of increasing the host's susceptibility to avian predation. Thus, both active hitch-hiking and incidental facilitation lead to non-random infection patterns in this parasite community.

Type
Research Article
Copyright
2006 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

Babirat, C., Mouritsen, K. N. and Poulin, R. ( 2004). Equal partnership: two trematode species, not one, manipulate the burrowing behaviour of the New Zealand cockle, Austrovenus stutchburyi. Journal of Helminthology 78, 195199.Google Scholar
Brown, B. L., Creed, R. P. Jr and Dobson, W. E. ( 2002). Branchiobdellid annelids and their crayfish hosts: are they engaged in a cleaning symbiosis? Oecologia 132, 250255.Google Scholar
Byrne, C. J., Holland, C. V., Kennedy, C. R. and Poole, W. R. ( 2003). Interspecific interactions between Acanthocephala in the intestine of brown trout: are they more frequent in Ireland? Parasitology 127, 399409.Google Scholar
Cáceres-Martínez, C., Chávez-Villalba, J. and Garduño-Méndez, L. ( 2005). First record of Pseudomyicola spinosus in Argopecten ventricosus in Baja California, Mexico. Journal of Invertebrate Pathology 89, 95100.CrossRefGoogle Scholar
Cáceres-Martínez, J. and Vásquez-Yeomans, R. ( 1997). Presence and histopathological effects of the copepod Pseudomyicola spinosus in Mytilus galloprovincialis and Mytilus californianus. Journal of Invertebrate Pathology 70, 150155.CrossRefGoogle Scholar
Chilton, C. ( 1904). On the occurrence of a species of cercariae in the cockle Chione stutchburyi. Transactions and Proceedings of the New Zealand Institute 37, 322325.Google Scholar
Cremonte, F. and Ituarte, C. ( 2003). Pathologies elicited by the gymnophallid metacercariae of Bartolius in the clam Darina solenoides. Journal of the Marine Biological Association of the United Kingdom 83, 311318.CrossRefGoogle Scholar
Dinamani, P. and Gordon, D. B. ( 1974). On the habits and nature of association of the copepod Pseudomyicola spinosus with the rock oyster Crassostrea glomerate in New Zealand. Journal of Invertebrate Pathology 24, 305310.CrossRefGoogle Scholar
Esch, G. W., Bush, A. O. and Aho, J. M. ( 1990). Parasite Communities: Patterns and Processes. Chapman and Hall, New York.
Esch, G. W., Curtis, L. A. and Barger, M. A. ( 2001). A perspective on the ecology of trematode communities in snails. Parasitology 123 (Suppl.), S57S75.CrossRefGoogle Scholar
Fredensborg, B. L. and Poulin, R. ( 2005). Larval helminths in intermediate hosts: does competition early in life determine the fitness of adult parasites? International Journal for Parasitology 35, 10611070.Google Scholar
Friggens, M. M. and Brown, J. H. ( 2005). Niche partitioning in the cestode communities of two elasmobranchs. Oikos 108, 7684.CrossRefGoogle Scholar
Helluy, S. ( 1983). Relations hôtes-parasites du trématode Microphallus papillorobutus (Rankin, 1940). II Modifications du comportement des Gammarus hôtes intermédiaires et localisation des métacercaires. Annales de Parasitologie Humaine et Comparée 58, 117.Google Scholar
Hendrickson, M. A. and Curtis, L. A. ( 2002). Infrapopulation sizes of co-occurring trematodes in the snail Ilyanassa obsoleta. Journal of Parasitology 88, 884889.CrossRefGoogle Scholar
Ho, J.-S. ( 2001). Why do symbiotic copepods matter? Hydrobiologia 453/454, 17.Google Scholar
Ho, J.-S. and Zheng, G.-X. ( 1994). Ostrincola koe (Copepoda, Myicolidae) and mass mortality of cultured hard clam (Meretrix meretrix) in China. Hydrobiologia 284, 169173.CrossRefGoogle Scholar
Holmes, S. P. ( 2002). The effect of pedal mucus on barnacle cyprid settlement: a source for indirect interactions in the rocky intertidal? Journal of the Marine Biological Association of the United Kingdom 82, 117129.Google Scholar
Holmes, S. P., Walker, G. and van der Meer, J. ( 2005). Barnacles, limpets and periwinkles: the effects of direct and indirect interactions on cyprid settlement success. Journal of Sea Research 53, 181204.CrossRefGoogle Scholar
Kajihara, T. and Nakamura, K. ( 1985). Lifespan and oviposition of the parasitic copepod Pseudomyicola spinosus under rearing conditions. Marine Biology 87, 5560.CrossRefGoogle Scholar
Kuris, A. M. and Lafferty, K. D. ( 1994). Community structure: larval trematodes in snail hosts. Annual Review of Ecology and Systematics 25, 189217.CrossRefGoogle Scholar
Lafferty, K. D. ( 1999). The evolution of trophic transmission. Parasitology Today 15, 111115.CrossRefGoogle Scholar
Laland, K. N., Odling-Smee, J. and Feldman, M. W. ( 2005). On the breadth and significance of niche construction: a reply to Griffiths, Okasha and Sterelny. Biology and Philosophy 20, 3755.CrossRefGoogle Scholar
Lello, J., Boag, B., Fenton, A., Stevenson, I. R. and Hudson, P. J. ( 2004). Competition and mutualism among the gut helminths of a mammalian host. Nature, London 428, 840844.CrossRefGoogle Scholar
Lysne, D. A., Skorping, A. and Hemmingsen, W. ( 1998). Transmission of Cryptocotyle lingua cercariae in natural environments: a field experiment. Journal of Fish Biology 53, 879885.Google Scholar
Montaudouin, X. de., Kisielewski, I., Bachelet, G. and Desclaux, C. ( 2000). A census of macroparasites in the intertidal bivalve community, Arcachon Bay, France. Oceanologica Acta 23, 453468.CrossRefGoogle Scholar
Mouritsen, K. N. ( 2002). The parasite-induced surfacing behaviour in the cockle Austrovenus stutchburyi: a test of an alternative hypothesis and identification of potential mechanisms. Parasitology 124, 521528.CrossRefGoogle Scholar
Mouritsen, K. N. ( 2004). Intertidal facilitation and indirect effects: cause and consequences of crawling in the New Zealand cockle. Marine Ecology Progress Series 271, 207220.CrossRefGoogle Scholar
Mouritsen, K. N. and Poulin, R. ( 2003 a). Parasite-induced trophic facilitation exploited by non-host predator: a manipulator's nightmare. International Journal for Parasitology 33, 10431050.Google Scholar
Mouritsen, K. N. and Poulin, R. ( 2003 b). The mud flat anemone-cockle association: mutualism in the intertidal zone? Oecologia 135, 131137.Google Scholar
Mouritsen, K. N. and Poulin, R. ( 2005 a). Parasites boosts biodiversity and changes animal community structure by trait-mediated indirect effects. Oikos 108, 344350.Google Scholar
Mouritsen, K. N. and Poulin, R. ( 2005 b). Parasitism can influence the intertidal zonation of non-host organisms. Marine Biology 148, 111.Google Scholar
Odling-Smee, F. J., Laland, K. N. and Feldman, M. W. ( 2003). Niche Construction: the Neglected Process in Evolution. Princeton University Press, New Jersey.
Olivas-Valdez, J. A. and Cáceres-Martínez, J. ( 2002). Infestation of the blue mussel Mytilus galloprovincialis by the copepod Pseudomyicola spinosus and its relation to size, density, and condition index of the host. Journal of Invertebrate Pathology 79, 6571.CrossRefGoogle Scholar
Perissinotto, R. and Pakhomov, E. A. ( 1997). Feeding association of the copepod Rhincalanus gigas with the tunicate salp Salpa thompsoni in the southern ocean. Marine Biology 127, 479483.CrossRefGoogle Scholar
Poulin, R. and Fitzgerald, G. J. ( 1989). Risk of parasitism and microhabitat selection in juvenile sticklebacks. Canadian Journal of Zoology 67, 1418.CrossRefGoogle Scholar
Poulin, R. and Grutter, A. S. ( 1996). Cleaning symbioses: proximate and adaptive explanations. BioScience 46, 512517.CrossRefGoogle Scholar
Poulin, R. and Valtonen, E. T. ( 2001). Interspecific associations among larval helminths in fish. International Journal for Parasitology 31, 15891596.CrossRefGoogle Scholar
Poulin, R., Hecker, K. and Thomas, F. ( 1998). Host manipulated by one parasite incur additional costs from infection by another parasite. Journal of Parasitology 84, 10501052.CrossRefGoogle Scholar
Poulin, R., Steeper, M. J. and Miller, A. A. ( 2000). Non-random patterns of host use by the different parasite species exploiting a cockle population. Parasitology 121, 289295.CrossRefGoogle Scholar
Rodgers, J. K., Sandland, G. J., Joyce, S. R. and Minchella, D. J. ( 2005). Multi-species interactions among a commensal (Chaetogaster limnaei limnaei), a parasite (Schistosoma mansoni), and an aquatic snail host (Biomphalaria glabrata). Journal of Parasitology 91, 709712.CrossRefGoogle Scholar
Thomas, F., Mete, K., Helluy, S., Santalla, F., Verneau, O., de Meeüs, T., Cézilly, F. and Renaud, F. ( 1997). Hitch-hiker parasites or how to benefit from the strategy of another parasite. Evolution 51, 13161318.CrossRefGoogle Scholar
Thomas, F. and Poulin, R. ( 1998). Manipulation of a mollusc by a trophically transmitted parasite: convergent evolution or phylogenetic inheritance? Parasitology 116, 431436.Google Scholar
Thomas, F., Renaud, F., de Meeüs, T. and Poulin, R. ( 1998). Manipulation of host behaviour by parasites: ecosystem engineering in the intertidal zone? Proceedings of the Royal Society of London, B 265, 10911096.Google Scholar
Thomas, F., Renaud, F. and Poulin, R. ( 1998). Exploitation of manipulators: ‘hitch-hiking’ as a parasite transmission strategy. Animal Behaviour 56, 199206.CrossRefGoogle Scholar
Wang, C. L., Renaud, F. and Thomas, F. ( 2002). Negative influence of Gammarinema gammari (Nematoda) on the fecundity of Microphallus papillorobustus (Trematoda): field and experimental evidence. Journal of Parasitology 88, 425427.CrossRefGoogle Scholar
Wegeberg, A. M., Montaudouin, X. de. and Jensen, K. T. ( 1999). Effect of intermediate host size (Cerastoderma edule) on infectivity of cercariae of three Himasthla species (Echinostomatoidae, Trematoda). Journal of Experimental Marine Biology and Ecology 238, 259269.CrossRefGoogle Scholar