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Parasitism underground: determinants of helminth infections in two species of subterranean rodents (Octodontidae)

Published online by Cambridge University Press:  26 May 2010

M. A. ROSSIN ,
A. I. MALIZIA ,
J. T. TIMI  and
R. POULIN
M. A. ROSSIN
Affiliation:
Laboratorio de Parasitología, Departamento de Biología, Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata, Funes 3350, (7600) Mar del Plata, Argentina
A. I. MALIZIA
Affiliation:
Laboratorio de Ecofisiología, Departamento de Biología, Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata, Funes 3350, (7600) Mar del Plata, Argentina
J. T. TIMI
Affiliation:
Laboratorio de Parasitología, Departamento de Biología, Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata, Funes 3350, (7600) Mar del Plata, Argentina
R. POULIN*
Affiliation:
Department of Zoology, University of Otago, PO Box 56, Dunedin, New Zealand
*
*Corresponding author: Department of Zoology, University of Otago, PO Box 56, Dunedin, New Zealand. Tel: +64 3 479 7983. Fax: +64 3 479 7584. E-mail: robert.poulin@stonebow.otago.ac.nz
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Summary

Patterns of infection among hosts in a population are often driven by intrinsic host features such as age or sex, as well as by positive or negative interactions between parasite species. We investigated helminth parasitism in 2 South American rodent species, Ctenomys australis and C. talarum (Octodontidae), to determine whether the unusual solitary and subterranean nature of these hosts would impact their patterns of infection. We applied generalized linear models to infection data on a total of 7 helminth species (1 in C. australis and 6 in C. talarum). Host age and season of capture influenced infection levels in some of the helminth species, but none were influenced by host body condition. In C. talarum, 4 pairs of helminth species showed significant associations, either asymmetrical or symmetrical, and with 3 of the 4 being positive; strong inter-specific facilitation appears likely in 1 case. Also, we found that female hosts, especially non-pregnant ones, harboured heavier infections of 2 nematode species than male hosts. This is in sharp contrast to the general male-bias reported for most studies of nematodes in wild mammals, and we develop explanations for these results based on the unusual ecology of these subterranean rodents.

Keywords

CtenomysArgentinafossorial rodentssex-biased infectionspecies interactionshost reproductive status
Type
Research Article
Information
Parasitology , Volume 137 , Issue 10 , September 2010 , pp. 1569 - 1575
Copyright
Copyright © Cambridge University Press 2010

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References

REFERENCES

Behnke, J. M., Eira, C., Rogan, M., Gilbert, F. S., Torres, J., Miquel, J. and Lewis, J. W. (2009). Helminth species richness in wild wood mice, Apodemus sylvaticus, is enhanced by the presence of the intestinal nematode Heligmosomoides polygyrus. Parasitology 136, 793–804.Google Scholar
Behnke, J. M., Gilbert, F. S., Abu-Madi, M. A. and Lewis, J. W. (2005). Do the helminth parasites of wood mice interact? Journal of Animal Ecology 74, 982–993.Google Scholar
Behnke, J. M., Lewis, J. W., Zain, S. N. M. and Gilbert, F. S. (1999). Helminth infections in Apodemus sylvaticus in southern England: interactive effects of host age, sex and year on the prevalence and abundance of infections. Journal of Helminthology 73, 31–44.CrossRefGoogle ScholarPubMed
Busch, C., Malizia, A. I., Scaglia, O. A. and Reig, O. A. (1989). Spatial distribution and attributes of a population of Ctenomys talarum (Rodentia: Octodontidae). Journal of Mammalogy 70, 204–208.CrossRefGoogle Scholar
Comparatore, V. M., Agnusdei, M. and Busch, C. (1992). Habitat relations in sympatric populations of Ctenomys australis and Ctenomys talarum (Rodentia, Octodontidae) in a natural grassland. Zeitschrift für Säugetierkunde 57, 47–55.Google Scholar
Crawley, M. J. (2007). The R Book. John Wiley & Sons, Chichester, UK.Google Scholar
del Valle, J. C., Lohfelt, M. I., Comparatore, V. M., Cid, M. S. and Busch, C. (2001). Feeding selectivity and food preference of Ctenomys talarum (tuco-tuco). Mammalian Biology 66, 165–173.Google Scholar
Dick, C. W., Gannon, M. R., Little, W. E. and Patrick, M. J. (2003). Ectoparasite associations of bats from central Pennsylvania. Journal of Medical Entomology 40, 813–819.Google Scholar
Eira, C., Torres, J., Vingada, J. and Miquel, J. (2006). Ecological aspects influencing the helminth community of the wood mouse Apodemus sylvaticus in Dunas de Mira, Portugal. Acta Parasitologica 51, 300–308.CrossRefGoogle Scholar
Fanjul, M. S., Zenuto, R. R. and Busch, C. (2003). Use of olfaction for sexual recognition in the subterranean rodent Ctenomys talarum. Acta Theriologica 48, 35–46.Google Scholar
Ferrari, N., Cattadori, I. M., Nespereira, J., Rizzoli, A. and Hudson, P. J. (2004). The role of host sex in parasite dynamics: field experiments on the yellow-necked mouse Apodemus flavicollis. Ecology Letters 7, 88–94.Google Scholar
Gardner, S. L. (1991). Helminth parasites of Thomomys bulbivorus (Richardson) (Rodentia: Geomyidae), with the description of a new species of Hymenolepis (Cestoda). Canadian Journal of Zoology 63, 1463–1469.CrossRefGoogle Scholar
Haukisalmi, V. and Henttonen, H. (1993). Coexistence in helminths of the bank vole, Clethrionomys glareolus. I. Patterns of co-occurrence. Journal of Animal Ecology 62, 221–229.Google Scholar
Haukisalmi, V. and Henttonen, H. (1998). Analysing interspecific associations in parasites: alternative methods and effects of sampling heterogeneity. Oecologia 116, 565–574.CrossRefGoogle ScholarPubMed
Holland, C. (1984). Interactions between Moniliformis (Acanthocephala) and Nippostrongylus (Nematoda) in the small intestine of laboratory rats. Parasitology 88, 303–315.Google Scholar
Krasnov, B. R., Morand, S., Hawlena, H., Khokhlova, I. S. and Shenbrot, G. I. (2005). Sex-biased parasitism, seasonality and sexual size dimorphism in desert rodents. Oecologia 146, 209–217.Google 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, 840–844.Google Scholar
Luong, L. T., Grear, D. A. and Hudson, P. J. (2009). Male hosts are responsible for the transmission of a trophically transmitted parasite, Pterygodermatites peromysci, to the intermediate host in the absence of sex-biased infection. International Journal for Parasitology 39, 1263–1268.Google Scholar
Malizia, A. I. (1998). Population dynamics of the fossorial rodent Ctenomys talarum (Rodentia: Octodontidae). Journal of Zoology 244, 545–551.CrossRefGoogle Scholar
Malizia, A. I. and Busch, C. (1991). Reproductive parameters and growth in the fossorial rodent Ctenomys talarum (Rodentia, Octodontidae). Mammalia 55, 293–305.Google Scholar
Malizia, A. I., Vassallo, A. I. and Busch, C. (1991). Population and habitat characteristics of two sympatric species of Ctenomys (Rodentia: Octodontidae). Acta Theriologica 36, 87–94.CrossRefGoogle Scholar
Malizia, A. I., Zenuto, R. R. and Busch, C. (1995). Demographic and reproductive attributes of dispersers in two populations of the subterranean rodent Ctenomys talarum (tuco-tuco). Canadian Journal of Zoology 73, 732–738.Google Scholar
Poulin, R. (1996). Sexual inequalities in helminth infections: a cost of being a male? American Naturalist 147, 287–295.CrossRefGoogle Scholar
Poulin, R. (2001). Interactions between species and the structure of helminth communities. Parasitology 122, S3–S11.Google Scholar
Poulin, R. (2005). Detection of interspecific competition in parasite communities. Journal of Parasitology 91, 1232–1235.CrossRefGoogle ScholarPubMed
Poulin, R. (2007). Evolutionary Ecology of Parasites, 2nd Edn.Princeton University Press, Princeton, NJ, USA.Google Scholar
R Development Core Team (2009). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria (URL, http://www.R-project.org).Google Scholar
Rossin, M. A. and Malizia, A. I. (2002). Relationship between helminth parasites and demographic attributes of a population of the subterranean rodent Ctenomys talarum (Rodentia: Octodontidae). Journal of Parasitology 88, 1268–1270.Google Scholar
Rossin, M. A. and Malizia, A. I. (2005). Redescription of Trichuris pampeana (Nematoda: Trichuridae) from the South American subterranean rodent Ctenomys talarum Thomas, 1898 (Rodentia: Octodontidae). Journal of Parasitology 91, 127–130.CrossRefGoogle ScholarPubMed
Rossin, M. A., Poulin, R., Timi, J. T. and Malizia, A. I. (2005 a). Causes of inter-individual variation in reproductive strategies of the parasitic nematode Graphidioides subterraneus. Parasitology Research 96, 335–339.Google Scholar
Rossin, M. A., Timi, J. T. and Malizia, A. I. (2004). Redescription and new host record of Paraspidodera uncinata (Rudolphi, 1819) (Nematoda: Aspidoderidae) from the South American rodent Ctenomys talarum (Rodentia: Octodontidae). Acta Parasitologica 49, 325–331.Google Scholar
Rossin, M. A., Timi, J. T. and Malizia, A. I. (2005 b). Graphidioides subterraneus n. sp. (Nematoda: Trichostrongylidae) from the South American subterranean rodent Ctenomys talarum Thomas, 1898 (Rodentia: Octodontidae). Parasite 12, 145–149.Google Scholar
Rossin, M. A., Timi, J. T. and Malizia, A. I. (2006 a). New Pudicinae (Trichostrongylina, Heligmosomoidea), Pudica ctenomidis n. sp. parasite of Ctenomys talarum (Rodentia: Octodontidae) from Argentina. Parasitology International 55, 83–87.CrossRefGoogle Scholar
Rossin, M. A., Timi, J. T. and Malizia, A. I. (2006 b). A new Trichostrongylus parasitizing the subterranean rodent Ctenomys talarum (Rodentia: Octodontidae) from Mar de Cobo, Argentina. Acta Parasitologica 51, 286–289.Google Scholar
Rossin, M. A., Varela, G. and Timi, J. T. (2009). Strongyloides myopotami in ctenomyid rodents: Transition from semi-aquatic to subterranean life cycle. Acta Parasitologica 54, 257–262.Google Scholar
Schalk, G. and Forbes, M. R. L. (1997). Male biases in parasitism of mammals: effects of study type, host age, and parasite taxon. Oikos 78, 67–74.Google Scholar
Scharff, A., Burda, H., Tenora, F., Kawalika, M. and Barus, V. (1997). Parasites in social subterranean Zambian mole-rats (Cryptomys spp., Bathyergidae, Rodentia). Journal of Zoology 241, 571–577.CrossRefGoogle Scholar
Vandegrift, K. J. and Hudson, P. J. (2009). Could parasites destabilize mouse populations? The potential role of Pterygodermatites peromysci in the population dynamics of free-living mice, Peromyscus leucopus. International Journal for Parasitology 39, 1253–1262.Google Scholar
Wilkes, C. P., Thompson, F. J., Gardner, M. P., Paterson, S. and Viney, M. E. (2004). The effect of the host immune response on the parasitic nematode Strongyloides ratti. Parasitology 128, 661–669.CrossRefGoogle ScholarPubMed
Zahn, A. and Rupp, D. (2004). Ectoparasite load in European vespertilionid bats. Journal of Zoology 262, 383–391.Google Scholar
Zuk, M. and McKean, K. A. (1996). Sex differences in parasite infections: patterns and processes. International Journal for Parasitology 26, 1009–1023.Google Scholar