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Numerical and functional responses of intestinal helminths in three rajid skates: evidence for competition between parasites?

Published online by Cambridge University Press:  16 August 2012

HASEEB S. RANDHAWA*
Affiliation:
Ecology Degree Programme, Department of Botany, University of Otago, P.O. Box 56, Dunedin, New Zealand9054
*
*Corresponding author: Tel: +64 3 471 6146. E-mail: [email protected]

Summary

Host-parasite interactions generally involve communities of parasites. Within these communities, species will co-exist and/or interact with one another in a manner either benefiting the species involved or to the detriment of one or more of the species. At the level of helminth infracommunities, evidence for intra- and inter-specific competition includes numerical responses, i.e. those regulating helminth intensity of infection, and functional responses, i.e. where the presence of competitors modifies the realised niche of infrapopulations. The objectives of this study are to assess the numerical and functional responses of helminths in infracommunities from 3 rajid skates using general linear models. Despite a lack of numerical responses, functional responses to intra- and inter-specific interactions were observed. A positive correlation between the number of individuals in an infrapopulation and its niche breadth (functional response) was observed for the tapeworms Pseudanthobothrium spp. and Echeneibothrium spp., in all their respective hosts, and for the nematode Pseudanisakis sp. in the little skate. Evidence for inter-specific competition includes niche shifts in Pseudanthobothrium purtoni (ex little skate) and Pseudanisakis sp. (ex thorny skate) in the presence of Pseudanisakis sp. and the tapeworm Grillotia sp., respectively. These results are consistent with other studies in providing evidence for competition between helminths of skates.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2012

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References

REFERENCES

Adamson, M. L. and Noble, S. J. (1993). Interspecific and intraspecific competition among pinworms in the hindgut of Periplaneta americana. Journal of Parasitology 79, 5056. doi: 10.2307/3283276.CrossRefGoogle Scholar
Alarcos, A. J., Ivanov, V. A. and Sardella, N. H. (2006). Distribution patterns and interactions of cestodes in the spiral intestine of the narrownos smooth-hound shark, Mustelus schmitti Springer, 1939 (Chondrichthyes, Carcharhiniformes), Acta Parasitologica 51, 100106. doi: 10.2478/s11686-006-0015-7.CrossRefGoogle Scholar
Anderson, D. R. (2008). Model Based Inference in the Life Sciences: A Primer on Evidence. Springer, New York, NY, USA.CrossRefGoogle Scholar
Andreassen, J., Bennet-Jenkins, E. M. and Bryant, C. (1999). Immunology and biochemistry of Hymenolepis diminuta. Advances in Parasitology 42, 223275. doi:10.1016/S0065-308X(08)60150-5.CrossRefGoogle ScholarPubMed
Borucinska, J. and Caira, J. N. (1993). A comparison of mode of attachment and histopathogenicity of four tapeworm species representing two orders infecting the spiral intestine of the nurse shark, Ginglymostoma cirratum. Journal of Parasitology 79, 238246. doi: 10.2307/3283514.CrossRefGoogle ScholarPubMed
Burnham, K. P. and Anderson, D. R. (2002). Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach. Springer, New York, NY, USA.Google Scholar
Bush, A. O. and Holmes, J. C. (1986). Intestinal helminths of lesser scaup ducks: An interactive community. Canadian Journal of Zoology 64, 142152. doi: 10.1139/z86-023.CrossRefGoogle Scholar
Bush, A. O. and Lotz, J. M. (2000). The ecology of “crowding”. Journal of Parasitology 86, 212213. doi: 10.1645/0022-3395(2000)086[0212:TEOC]2.0.CO;2Google ScholarPubMed
Carvajal, J. G. and Dailey, M. D. (1975). Three new species of Echeneibothrium (Cestoda: Tetraphyllidea) from the skate, Raja chilensis Guichenot, 1848, with comments on mode of attachment and host specificity. Journal of Parasitology 61, 8994. doi: 10.2307/3279115.CrossRefGoogle ScholarPubMed
Cislo, P. R. and Caira, J. N. (1993). The parasite assemblage in the spiral valve of the shark Mustelus canis. Journal of Parasitology 79, 886899. doi: 10.2307/3283727.CrossRefGoogle Scholar
Curran, S. and Caira, J. N. (1995). Attachment site specificity and the tapeworm assemblage in the spiral intestine of the blue shark (Prionace glauca). Journal of Parasitology 81, 149157. doi: 10.2307/3283913.CrossRefGoogle ScholarPubMed
Dobson, A. P. (1985). The population dynamics of competition between parasites. Parasitology 91, 317347. doi: 10.1017/S0031182000057401.CrossRefGoogle ScholarPubMed
Ehman, K. D. (2001). Nematode parasites of the eastern chipmunk from Armstrong County, Pennsylvania. Journal of the Pennsylvania Academy of Sciences 75, 6265.Google Scholar
Euzet, L. (1959). Recherches sur les cestodes Tétraphyllides de Sélaciens des côtes de France. D.Sc. thesis, Faculté des Sciences, Université de Montpellier, France.Google Scholar
Friggens, M. M. and Brown, J. H. (2005). Niche partitioning in the cestode communities of two elasmobranchs. Oikos 108, 7684. doi: 10.1111/j.0030-1299.2005.13275.x.CrossRefGoogle Scholar
Graham, A. L. (2008). Ecological rules governing helminth-microparasite coinfection. Proceedings of the National Academy of Sciences, USA 105, 566570. doi: 10.1073/pnas.0707221105.CrossRefGoogle ScholarPubMed
Hamann, M. I., Kehr, A. I. and Gonzalez, C. E. (2009). Niche specificity of two glyphtelmins (Trematoda) congeners infecting Leptodactylus chaquensis (Anura: Leptodactylidae) from Argentina. Journal of Parasitology 95, 817822. doi: 10.1645/GE-1860.1.CrossRefGoogle ScholarPubMed
Hassanine, R. M. E.-S. and Al-Jahdali, M. O. (2007). Ecological comments on the intestinal helminths of the rabbitfish Siganus rivulatus (Teleostei, Siganidae) from the northern Red Sea. Acta Parasitologica 52, 278285. doi: 10.2478/s11686-007-0030-3.CrossRefGoogle Scholar
Holland, C. (1984). Interaction between Moniliformis (Acanthocephala) and Nippostrongylus (Nematoda) in the small intestine of laboratory rats. Parasitology 88, 303315. doi: 10.1017/S003118200005455X.CrossRefGoogle ScholarPubMed
Holmes, J. C. (1973). Site selection by parasitic helminths: Interspecific interactions, site segregation, and their importance to the development of helminth communities. Canadian Journal of Zoology 51, 333347. doi: 10.1139/z73-047.CrossRefGoogle Scholar
Irvine, R. J., Stien, A., Dallas, J. F., Halvorsen, O., Langvatn, R. and Albon, S. D. (2001). Contrasting regulation of fecundity in two abomasal nematodes of Svalbard reindeer (Rangifer tarandus platyrhynchus). Parasitology 122, 673681. doi: 10.1017/S0031182001007818.CrossRefGoogle ScholarPubMed
Keeling, C. P. and Burt, M. D. B. (1996). Echeneibothrium canadensis n. sp. (Tetraphyllidea: Phyllobothriidae) in the spiral intestine of the thorny skate (Raja radiata) from the Canadian Atlantic Ocean. Canadian Journal of Zoology 74, 15901593. doi: 10.1139/z96-173.CrossRefGoogle Scholar
Keymer, A. E. (1982). Density-dependent mechanisms in the regulation of intestinal helminth populations. Parasitology 84, 573587. doi: 10.1017/S0031182000052847.CrossRefGoogle ScholarPubMed
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. doi: 10.1038/nature02490.CrossRefGoogle ScholarPubMed
May, R. M. (1992). How many species inhabit the Earth? Scientific American 267, 4248.CrossRefGoogle Scholar
McVicar, A. H. (1979). The distribution of cestodes within the spiral intestine of Raja naevus Müller & Henle. International Journal for Parasitology 9, 165176. doi: 10.1016/0020-7519(79)90024-9.CrossRefGoogle Scholar
Moqbel, R. and Wakelin, D. (1979). Trichinella spiralis and Strongyloides ratti: immune interaction in adult rats. Experimental Parasitology 45, 6572. doi: 10.1016/0014-4894(79)90008-0.CrossRefGoogle Scholar
Parker, T. J. (1879). On the intestinal spiral valve in the genus Raia. Transactions of the Zoological Society of London 11: 4961.CrossRefGoogle Scholar
Pie, M. R., Engers, K. B. and Boeger, W. A. (2006). Density-dependent topographical specialization in Gyrodactylus anisopharynx (Monogenoidea, Gyrodactylidae): boosting transmission or evading competition? Journal of Parasitology 92, 459463. doi: 10.1645/GE-641.1.CrossRefGoogle ScholarPubMed
Poulin, R. (2001). Interactions between species and the structure of helminth communities. Parasitology 122 (Suppl.) S3S11. doi: 10.1017/S0031182000016991.CrossRefGoogle ScholarPubMed
Poulin, R. (2007). Evolutionary Ecology of Parasites. Princeton University Press, Princeton, NJ, USA.CrossRefGoogle Scholar
Poulin, R., Nichol, K. and Latham, A. D. M. (2003). Host sharing and host manipulation by larval helminths in shore crabs: cooperation of conflict? International Journal for Parasitology 33, 425433.CrossRefGoogle ScholarPubMed
Randhawa, H. S. (2000). A biological study of intestinal helminths infecting elasmobranchs from the West Isles of the Bay of Fundy, New Brunswick. M.Sc. thesis, Institute of Parasitology, McGill University, Canada.Google Scholar
Randhawa, H. S. and Burt, M. D. B. (2008). Determinants of host specificity and comments on attachment site specificity of tetraphyllidean cestodes infecting rajid skates from the northwest Atlantic. Journal of Parasitology 94, 436461. doi: 10.1645/GE-1180.1CrossRefGoogle ScholarPubMed
Randhawa, H. S. and Poulin, R. (2009). Determinants and consequences of interspecific body size variation in tetraphyllidean tapeworms. Oecologia 161, 759769. doi: 10.1007/s00442-009-1410-1.CrossRefGoogle ScholarPubMed
Randhawa, H. S., Saunders, G. W. and Burt, M. D. B. (2007). Establishment of the onset of host specificity in four phyllobothriid tapeworm species (Cestoda: Tetraphyllidea) using a molecular approach. Parasitology 134, 12911300. doi: 10.1017/S0031182007002521.CrossRefGoogle ScholarPubMed
Randhawa, H. S., Saunders, G. W., Scott, M. E. and Burt, M. D. B. (2008). Redescription of Pseudanthobothrium hanseni Baer, 1956 and description of P. purtoni n. sp. (Cestoda: Tetraphyllidea) from different pairs of rajid skate hosts, with comments on the host specificity of the genus in the northwest Atlantic. Systematic Parasitology 70, 4160. doi: 10.1007/s11230-007-9122-6.CrossRefGoogle Scholar
Rauque, C. A. and Semenas, L. (2011). Parasite volume as an indicator of competition: the case of Acanthocephalus tumescens and Pseudocorynosoma sp. (Acanthocephala) in their intermediate host. Journal of Parasitology 97, 9991002.CrossRefGoogle ScholarPubMed
Read, C. P. (1951). The “crowding effect” in tapeworm infections. Journal of Parasitology 37, 174178.CrossRefGoogle Scholar
Rees, G. and Williams, H. H. (1965). The functional morphology of the scolex and the genitalia of Acanthobothrium coronatum (Rud.) (Cestoda: Tetraphyllidea). Parasitology 55, 617651.CrossRefGoogle ScholarPubMed
Richards, D. T. and Lewis, J. W. (2001). Fecundity and egg output by Toxocara canis in the red fox, Vulpes vulpes. Journal of Helminthology 75, 157164. doi: 10.1079/JOH2001066.Google ScholarPubMed
Roberts, L. S. (2000). The crowding effect revisited. Journal of Parasitology 86, 209211. doi: 10.1645/0022 3395(2000)086[0209:TCER]2.0.CO;2.Google ScholarPubMed
Sanmartin, M. L., Alvarez, M. F., Peris, D., Iglesias, R. and Leiro, J. (2000). Parasite community study of the undulate ray Raja undulata in the Ria of Muros (Galicia, northwest Spain). Aquaculture 184, 189201. doi: 10.1016/S0044-8486(99)00332-4.CrossRefGoogle Scholar
Shostak, A. W. and Scott, M. E. (1993). Detection of density-dependent growth and fecundity of helminths in natural infections. Parasitology 106, 527539. doi: 10.1017/S0031182000076836.CrossRefGoogle ScholarPubMed
Silver, B. B., Dick, T. A. and Welch, H. E. (1980). Concurrent infection of Hymenolepis diminuta and Trichinella spiralis in the rat intestine. Journal of Parasitology 66, 786791. doi: 10.2307/3280669.CrossRefGoogle ScholarPubMed
Simkova, A., Desdevises, Y., Gelnar, M. and Morand, S. (2000). Co-existence of nine gill ectoparasites (Dactylogytus: Monogenea) parasitising the roach (Rutilus rutilus L.): history and present ecology. International Journal for Parasitology 30, 10771088. doi: 10.1016/S0020-7519(00)00098-9CrossRefGoogle ScholarPubMed
Stock, T. M. and Holmes, J. C. (1988). Functional relationships and microhabitat distributions of enteric helminths of grebes (Podicioedidae): The evidence for interactive communities. Journal of Parasitology 74, 214227. doi: 10.2307/3282447.CrossRefGoogle ScholarPubMed
Szalai, A. J. and Dick, T. A. (1989). Differences in numbers and inequalities in mass and fecundity during the egg-producing period for Rhaphidascaris acus (Nematoda: Anisakidae). Parasitology 98, 489495. doi: 10.1017/S0031182000061588.CrossRefGoogle Scholar
Tanzola, R. D., Guagliardo, S. E., Brizzola, S. M., Arias, M. V. and Botte, S. E. (1998). Parasite assemblage of Sympterygia bonapartei (Pisces: Rajidae), an endemic skate of the Southwest Atlantic. Helminthologia 35, 123129.Google Scholar
Thomson, J. D. (1980). Implications of different sorts of evidence for competition. American Naturalist 116, 719726. doi: 10.1086/283662.CrossRefGoogle Scholar
Twohig, M. E., Caira, J. N. and Fyler, C. A. (2008). Two new cestode species from the dwarf whipray, Himantura walga (Batoidea: Dasyatidae), from Borneo, with comments on site and mode of attachment. Journal of Parasitology 94, 11181127. doi: 10.1645/GE-1475.1.CrossRefGoogle ScholarPubMed
Williams, H. H. (1961). Observations of Echeneibothrium maculatum (Cestoda: Tetraphyllidea). Journal of the Marine Biological Association of the United Kingdom 41, 631652. doi: 10.1017/S0025315400016209.CrossRefGoogle Scholar
Williams, H. H. (1968). Phyllobothrium piriei sp. nov. (Cestoda: Tetraphyllidea) from Raja naevus with comments on its habitat and mode of attachment. Parasitology 58, 929937. doi: 10.1017/S0031182000069699.CrossRefGoogle Scholar
Windsor, D. A. (1998). Most species on Earth are parasites. International Journal for Parasitology 28, 19391941. doi: 10.1016/S0020-7519(98)00153-2.CrossRefGoogle ScholarPubMed