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Reproductive effort and seasonality associated with male-biased parasitism in Gracilinanus agilis (Didelphimorphia: Didelphidae) infected by Eimeria spp. (Apicomplexa: Eimeriidae) in the Brazilian cerrado

Published online by Cambridge University Press:  16 April 2015

A. L. S. STRONA ,
M. LEVENHAGEM  and
N. O. LEINER
A. L. S. STRONA
Affiliation:
Instituto de Biologia, Universidade Federal de Uberlândia, Uberlândia, Brazil
M. LEVENHAGEM
Affiliation:
Instituto de Ciências Biomédicas, Universidade Federal de Uberlândia, Uberlândia, Brazil
N. O. LEINER*
Affiliation:
Instituto de Biologia, Universidade Federal de Uberlândia, Uberlândia, Brazil
*
* Corresponding author. Instituto de Biologia, Universidade Federal de Uberlândia, Uberlândia, Brazil. E-mail: [email protected]
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Summary

The aggregation of parasites among hosts is associated with differential host exposure and susceptibility to parasites, which varies according to host gender, body size, reproductive status and environmental factors. We evaluated the role of these factors on infestation by Eimeria spp. (Eimeriidae) in the agile gracile mouse opossum (Gracilinanus agilis), a semelparous didelphid inhabiting neotropical savannahs. Eimeria spp. abundance and prevalence among G. agilis were associated with the breeding status of individuals and to a lesser extent to climatic season, with both sexes presenting higher Eimeria spp. burdens during late breeding/wet season. On the other hand, male-biased parasitism was restricted to dry/mating season. We suggest that male spatial organization and diet may account for increased parasite burdens within this sex, although future studies should evaluate the role of physiological differences associated with androgen hormones. Finally, a rapid increase in Eimeria spp. loads among females during the late breeding/wet season seems associated with seasonal changes in susceptibility, due to breeding costs related to semelparity, and exposure to infective propagules, while male-die off seems to explain maintenance of higher Eimeria spp. burdens within this sex in the same period.

Keywords

sex-biased parasitismreproductionsemelparityEimeriidaeDidelphidae
Type
Research Article
Information
Parasitology , Volume 142 , Issue 8 , July 2015 , pp. 1086 - 1094
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Copyright
Copyright © Cambridge University Press 2015 

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References

REFERENCES

Albon, S. D., Stien, A., Irvine, R. J., Langvatn, R., Ropstad, E. and Halvorson, O. (2002). The role of parasites in the dynamics of a reindeer population. Proceedings of the Royal Society, London B 269, 1625–1632.Google Scholar
Altizer, S., Nunn, C. L., Thrall, P. H., Gittleman, J. L., Antonovics, J., Cunningham, A. A., Dobson, A. P., Ezenwa, V., Jones, K. E., Pedersen, A. B., Poss, M. and Pulliam, J. R. C. (2003). Social organization and parasite risk in mammals: integrating theory and empirical studies. Annual Review of Ecology. Evolution and Systematics 34, 517–47.Google Scholar
Altizer, S., Dobson, A., Hosseini, P., Hudson, P., Pascual, M. and Rohani, P. (2006). Seasonality and the dynamics of infectious diseases. Ecology Letters 9, 467–484.Google Scholar
Anderson, R. M. and May, R. M. (1979). Population biology of infectious diseases: part I. Nature 280, 361–367.CrossRefGoogle ScholarPubMed
Arneberg, P., Skorping, P., Grenfell, B. and Read, A. F. (1998). Host densities as determinants of abundance in parasite communities. Proceedings of the Royal Society, London B 265, 1283–1289.Google Scholar
Bolker, B. M., Brooks, M. E., Clark, C. J., Geange, S. W., Poulsen, J. R., Stevens, M. H. H. and White, J. S. (2008). Generalized linear mixed models: a practical guide for ecology and evolution. Trends in Ecology and Evolution 24, 127–135.Google Scholar
Bradley, A. J. (2003). Stress, hormones and mortality in small carnivorous marsupials. In Predators with pouches: the biology of carnivorous marsupials (ed. Jones, M., Archer, M. and Dickman, C.), pp. 254–267. CSIRO Publishing, Colingwood, Australia.Google Scholar
Burnham, K. P. and Anderson, D. R. (2002). Model Selection and Multimodel Inference:a Practical Information-theoretic Approach, 2nd Edn. Springer-Verlag, New York, USA.Google Scholar
Camargo, N. F., Ribeiro, J. F., Camargo, A. J. A. and Vieira, E. M. (2014). Diet of the gracile mouse opossum Gracilinanus agilis (Didelphimorphia: Didelphidae) in a neotropical savanna: intraspecific variation and resource selection. Acta Theriologica 59, 183–191.Google Scholar
Cardoso, E., Moreno, M. I., Bruna, E. M. and Vasconcelos, H. L. (2009). Mudanças fitofisionômicas no cerrado: 18 anos de sucessão ecológica na estação ecológica do Panga, Uberlândia-MG. Caminhos de Geografia 10, 254–268.Google Scholar
Combes, C. (2001). Parasitism: The Ecology and Evolution of Intimate Interactions, 1st Edn. The University of Chicago Press, Chicago, USA.Google Scholar
Christe, P., Arlettaz, R. and Vogel, P. (2000). Variation in intensity of a parasitic mite (Spinturnix myoti) in relation to reproductive cycle and immunocompetence of its bat host (Myotis myotis). Ecology Letters 3, 207–212.Google Scholar
Crofton, H. D. (1971). A model of host–parasite relationships. Parasitology 63, 343–364.Google Scholar
De Meeus, T. and Renaud, F. (2002). Parasites within the new phylogeny of eukaryotes. Trends in Parasitology 18, 247–251.CrossRefGoogle ScholarPubMed
Dare, O. K. and Forbes, M. R. (2009). Patterns of Infection by Lungworms, Rhabdias ranae and Haematoloechus spp., in Northern Leopard Frogs: a relationship between sex and parasitism. Journal of Parasitology 95, 275–280.Google Scholar
Duszynski, D. W. and Wilber, P. G. (1997). A guideline for the preparation of species description in the Eimeriidae. Journal of Parasitology 83, 333–336.Google Scholar
Evans, M. R., Goldsmith, A. R. and Norris, S. R. A. (2000). The effects of testosterone on antibody production and plumage coloration in male house sparrows (Passer domesticus). Behavioral Ecology and Sociobiology 47, 156–163.Google Scholar
Ezenwa, V. O., Ekernas, L. S. and Creel, S. (2012). Unravelling complex associations between testosterone and parasite infection in the wild. Functional Ecology 26, 123–133.Google Scholar
Fayer, R. (1980). Epidemiology of protozoan infections: Coccidia. Veterinary Parasitology 6, 75–103.CrossRefGoogle Scholar
Ferrari, N., Cattadori, I. M., Nespereira, J., Rizzola, A. and Hudson, P. J. (2004). The role of host sex in parasite dynamics: field experiments on the yellownecked mouse Apodemus flavicollis . Ecology Letters 7, 88–94.Google Scholar
Fisher, D. O. and Blomberg, S. P. (2011). Costs of reproduction and terminal investment by females in a semelparous marsupial. PLoS One 6, e15226.Google Scholar
Folstad, I. and Karter, A. J. (1992). Parasites, bright males and the immunocompetence handicap. American Naturalist 139, 603–622.Google Scholar
Fuller, C. A. (1996). Population dynamics of two species of Eimeria (Apicomplexa: Eimeriidae) in deer mice (Peromyscus maniculatus): biotic and abiotic factors. Journal of Parasitology 82, 220–225.Google Scholar
Fuxjager, M. J., Foufopoulos, J., Diaz-Uriarte, R. and Marler, C. A. (2011). Functionally opposing effects of testosterone on two different types of parasite: implications for the immunocompetence handicap hypothesis. Functional Ecology 25, 132–138.Google Scholar
Gordon, H. M. and Whitlock, H. V. (1939). A new technique for counting nematode eggs in sheep faeces. Journal of Commonwealth Science Industry Organizations 12, 50–52.Google Scholar
Harrison, A., Scantlebury, M. and Montgomery, W. I. (2010). Body mass and sex- biased parasitism in wood mice Apodemus sylvaticus . Oikos 119, 1090–1104.Google Scholar
Hillegass, M. A., Waterman, J. M. and Roth, J. D. (2010). Parasite removal increases reproductive success in a social African ground squirrel. Behavioral Ecology 21, 696–700.CrossRefGoogle Scholar
Hudson, P. J., Dobson, A. P. and Lafferty, K. D. (2006). Is a healthy ecosystem one that is rich in parasites? Trends in Ecology and Evolution 21, 381–385.Google Scholar
Klein, S. L. (2004). Hormonal and immunological mechanisms mediating sex differences in parasite infections. Parasite Immunology 26, 247–264.Google Scholar
Krasnov, B. R., Morand, S., Hawlena, H., Khokhlova, I. S. and Shenbrot, G. (2005). Sex-biased parasitism, seasonality and sexual size dimorphism in desert rodents. Oecologia 146, 209–217.Google Scholar
Krasnov, B. R., Bordes, F., Khokhlova, I. S. and Morand, S. (2012). Gender-biased parasitism in small mammals: patterns, mechanisms, consequences. Mammalia 76, 1–13.Google Scholar
Leiner, N. O., Setz, E. Z. F. and Silva, W. R. (2008). Semelparity and factors affecting the reproductive activity of the Brazilian slender opossum (Marmosops paulensis) in southeastern Brazil. Journal of Mammalogy 89, 153–158.Google Scholar
Lessa, L. G. and Costa, F. N. (2010). Diet and seed dispersal by five marsupials (Didelphimorphia, Didelphidade) in a Brazilian cerrado reserve. Mammalian Biology 75, 10–16.Google Scholar
Lloyd-Smith, J. O., Schreiber, S. J., Kopp, P. E. and Getz, W. M. (2005). Superspreading and the effect of individual variation on disease emergence. Nature 438, 355–359.Google Scholar
Lopes, G. P. (2014). Estratégia reprodutiva e organização espacial de uma população de Gracilinanus agilis (Didelphimorphia:Didelphidae) na Estação Ecológica do Panga, Uberlândia, MG. Master's dissertation. Universidade Federal de Uberlândia, Uberlândia, Brazil.Google Scholar
Lopes, G. P. and Leiner, N. O. (2015). Semelparity in a population of Gracilinanus agilis (Didelphimorphia: Didelphidae) inhabiting the Brazilian cerrado. Mammalian Biology 80, 1–16.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, 1263–8.Google Scholar
Macedo, J. S., Loretto, D., Vieira, M. V. and Cerqueira, R. (2006). Classes dentárias e de desenvolvimento em marsupiais: um método de análise para animais vivos em campo. Mastozoologia Neotropical 13, 133–136.Google Scholar
Martins, E. G., Bonato, V., Pinheiro, H. P. and Reis, S. F. (2006). Diet of the gracile mouse opossum (Gracilinanus microtarsus) (Didelphimorphia: Didelphidae) in a Brazilian Cerrado: patterns of food consumption and intra-population variation. Journal of Zoology 269, 21–28.Google Scholar
Meyer-Lucht, Y., Otten, C., Püttker, T., Pardini, R., Metzger, J. P. and Sommer, S. (2010). Variety matters: adaptive genetic diversity and parasite load in two mouse opossums from the Brazilian Atlantic Forest. Conservation Genetics 11, 2001–2013.Google Scholar
Moore, S. L. and Wilson, K. (2002). Parasites as a viability cost of sexual selection in natural populations of mammals. Science 297, 2015–2017.Google Scholar
Morand, S., Bellocq, G., Stanko, M. and Miklisova, D. (2004). Is sex-biased ectoparasitism related to sexual size dimorphism in small mammals of central Europe? Parasitology 129, 505–510.Google Scholar
Naylor, R., Richardson, S. J. and McAllan, B. M. (2008). Boom and bust: a review of the physiology of the marsupial genus Antechinus . Journal of Comparative Physiology B 178, 545–562.CrossRefGoogle ScholarPubMed
Owen-Ashley, N. T., Hasselquist, D. and Wingfield, J. C. (2004). Androgens and the immunocompetence handicap hypothesis: unraveling direct and indirect pathways of immunosuppression in song sparrows. American Naturalist 164, 490–505.Google Scholar
Poulin, R. (1993). The disparity between observed and uniform distributions: a new look at parasite aggregation. International Journal of Parasitology 23, 937–944.Google Scholar
Poulin, R. (1999). The functional importance of parasites in animal communities: many roles at many levels? International of Journal Parasitology 29, 903–914.Google Scholar
R Development Core Team (2008). R: A language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org Google Scholar
Roberts, M. L., Buchanan, K. L. and Evans, M. R. (2004). Testing the immunocompetence handicap hypothesis: a review of the evidence. Animal Behavior 68, 227–239.Google Scholar
Roberts, M. L., Buchanan, K. L., Hasselquist, D. and Evans, M. R. (2007). Effects of testosterone and corticosterone on immunocompetence in the zebra finch. Hormones and Behavior 51, 126–134.Google Scholar
Ryser, J. (1992). The mating system and male mating success of the Virginia Opossum (Didelphis virginiana) in Florida. Journal of Zoology London 228, 127–139.Google Scholar
Sanchez, A., Devevey, G. and Bize, P. (2011). Female-biased infection and transmission of the gastrointestinal nematode Trichuris arvicolae infecting the common vole Microtus arvalis . International Journal of Parasitology 41, 1397–1402.Google Scholar
Sheldon, B. C. and Verhulst, S. (1996). Ecological immunology: costly parasite defenses and trade-offs in evolutionary ecology. Trends in Ecology and Evolution 11, 317–321.Google Scholar
Shine, R. (1989). Ecological causes for the evolution of sexual dimorphism: a review of the evidence. Quarterly Review of Biology 64, 419–461.Google Scholar
Speakman, J. R. (2008). The physiological costs of reproduction in small mammals. Philosophical Transactions of the Royal Society B 363, 375–398.Google Scholar
Thomas, F., Guégan, J. and Renaud, F. (2009). Ecology and Evolution of Parasitism, 1st Edn. Oxford University Press, Oxford, USA.Google Scholar
Viljoen, H., Bennet, N. C., Ueckermann, E. A. and Lutermann, H. (2011). The role of host traits, season and group size on parasite burdens in a cooperative mammal. PLoS ONE 6, e27003.Google Scholar
Voss, R. S. and Jansa, S. A. (2009). Phylogenetic relationships and classification of Didelphid Marsupials, an extant radiation of new World Metatherian Mammals. Bulletin of the American Museum of Natural History 322, 1–177.Google Scholar
Wilson, K., Bjornstad, O. N., Dobson, A. P., Merler, S., Poglayen, G., Randolph, S. E., Read, A. F. and Skorping, A. (2001). Heterogeneities in macroparasite infections: patterns and processes. In The Ecology of Wildlife Diseases (ed. Hudson, P. J., Rizzoli, A., Grenfell, B. T., Heesterbeek, H. and Dobson, A. P.), pp. 6–44. Oxford University Press, Oxford, USA.Google Scholar