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Parasite-specific variation and the extent of male-biased parasitism; an example with a South African rodent and ectoparasitic arthropods

Published online by Cambridge University Press:  16 October 2009

SONJA MATTHEE ,
MELODIE A. McGEOCH  and
BORIS R. KRASNOV
SONJA MATTHEE*
Affiliation:
Department of Conservation Ecology and Entomology, Centre for Invasion Biology, Private Bag X1, Stellenbosch University, 7602, South Africa
MELODIE A. McGEOCH
Affiliation:
Department of Conservation Ecology and Entomology, Centre for Invasion Biology, Private Bag X1, Stellenbosch University, 7602, South Africa
BORIS R. KRASNOV
Affiliation:
Mitrani Department of Desert Ecology, Swiss Institute for Dryland Environmental Research, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sede-Boqer Campus, 84990Midreshet Ben-Gurion, Israel
*
*Corresponding author: Department of Conservation Ecology and Entomology, Private Bag X1, Stellenbosch University 7602, South Africa. Tel: +27 21 808 4777. Fax: +27 21 808 3304. E-mail: [email protected]
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Summary

We asked whether the occurrence and the extent of host gender-biased parasitism vary among higher parasite taxa, among individual species within these taxa and within parasite species among localities. To answer this question, we studied prevalence, abundance, species richness and the level of aggregation of ectoparasites (ticks, mites, lice and fleas) collected from male and female striped mice (Rhabdomys pumilio) in 9 localities of the Western Cape Province of South Africa. We used meta-analyses to compare parasitological variables between male and female hosts across localities for individual parasite species and higher taxa as well as across parasite species within a higher taxon. Whenever gender-biased parasitism was found, it indicated higher infestation of male than female hosts (except 1 low abundant mite species). We found that the occurrence and extent of gender-biased infestation varied mainly within a parasite species among localities and among parasite species within a higher taxon but not among parasite taxa. Our results suggest that the extent of a gender-biased pattern of parasite infestation of the same host may not only involve host-related mechanisms but also depends on biological features of a particular parasite species.

Keywords

gender biasRhabdomys pumilioectoparasitestickslicemitesfleas
Type
Research Article
Information
Parasitology , Volume 137 , Issue 4 , April 2010 , pp. 651 - 660
Copyright
Copyright © Cambridge University Press 2009

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References

REFERENCES

Anderson, R. M. and Gordon, D. M. (1982). Processes influencing the distribution of parasite numbers within host populations with special emphasis on parasite-induced host mortality. Parasitology 85, 373–398.CrossRefGoogle Scholar
Bandilla, M., Hakalahti, T., Hudson, P. J. and Valtonen, E. T. (2005). Aggregation of Argulus coregoni (Crustacea: Branchiura) on rainbow trout (Oncorhynchus mykiss): a consequence of host susceptibility or exposure? Parasitology 130, 169–176.CrossRefGoogle ScholarPubMed
Christe, P., Glaizot, O., Evanno, G., Bruyndonckx, N., Devevey, G., Yannic, G., Patthey, P., Maeder, A., Vogel, P. and Arlettaz, R. (2007). Host sex and ectoparasites choice: preference for, and higher survival on female hosts. Journal of Animal Ecology 76, 703–710.CrossRefGoogle ScholarPubMed
Cox, R. M. and Henry, J-A. (2007). Increased mite parasitism as a cost of testosterone in male striped plateau lizards Sceloporus virgatus. Functional Ecology 21, 327–334.CrossRefGoogle Scholar
De Graaf, G. (1981). The Rodents of Southern Africa. Butterworths, Durban, South Africa.Google Scholar
Field, L. H. (1969). The biology of Notophryxus lateralis (Isopoda: Epicaridia), parasitic on the euphausiid Nematoscelis difficilis. Journal of Parasitology 55, 1271–1277.CrossRefGoogle Scholar
Folstad, I. and Karter, A. J. (1992). Parasites, bright males, and the immunocompetence handicap. American Naturalist 139, 603–622.CrossRefGoogle Scholar
Gorrell, J. C. and Schulte-Hostedde, A. I. (2008). Patterns of parasitism and body size in red squirrels (Tamiasciurus hudsonicus). Canadian Journal of Zoology 86, 99–107.CrossRefGoogle Scholar
Hillegass, M. A., Waterman, J. M. and Roth, J. D. (2008). The influence of sex and sociality on parasite loads in an African ground squirrel. Behavioral Ecology 19, 1006–1011.CrossRefGoogle Scholar
Hilton, C. D. and Best, T. L. (2000). Gastrointestinal helminth parasites of bats in Alabama. In Fourth Colloquium on Conservation of Mammals in the Southeastern United States (ed. Chapman, B. R. and Laerm, J.), Occasional Papers of the North Carolina Museum of Natural Sciences and the North Carolina Biological Survey No. 12, Raleigh, NC, USA.Google Scholar
Hughes, V. L. and Randolph, S. E. (2001). Testosterone depresses innate and acquired resistance to ticks in natural rodent hosts: a force for aggregated distributions of parasites. Journal of Parasitology 87, 49–54.CrossRefGoogle ScholarPubMed
Krasnov, B. R. (2008). Functional and Evolutionary Ecology of Fleas: A Model for Ecological Parasitology. Cambridge University Press, Cambridge.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Kuris, A. M., Poinar, G. O. and Hess, R. T. (1980). Post-larval mortality of the endoparasitic isopod castrator Portunion conformis (Epicaridea: Entoniscidae) in the shore crab Hemigrapsus oregonensis, with a description of the host response. Parasitology 80, 211–232.CrossRefGoogle Scholar
Lareschi, M. (2006). The relationship of sex and ectoparasite infestation in the water rat Scapteromys aquaticus (Rodentia: Cricetidae) in La Plata, Argentina. Revista de biología tropical 54, 673–679.CrossRefGoogle ScholarPubMed
Lott, D. F. (1991). Intraspecific Variation in the Social Systems of Wild Vertebrates. Cambridge University Press, Cambridge.Google Scholar
Matthee, S., Horak, I. G., Beaucournu, J-C., Durden, L. A., Ueckermann, E. A. and McGeoch, M. A. (2007). Epifaunistic arthropod parasites of the four-striped mouse, Rhabdomys pumilio, in the Western Cape Province, South Africa. Journal of Parasitology 93, 47–59.CrossRefGoogle ScholarPubMed
McCurdy, D. G. (1998). Sex-biased parasitism of avian hosts: relations to blood parasite taxon and mating system. Oikos 82, 303–312.CrossRefGoogle Scholar
McTier, T. L., George, J. E. and Bennet, S. N. (1981). Resistance and cross-resistance of guinea pigs to Dermacentor andersoni Stiles, D. variabilis (Say), Amblyomma americanum (Linnaeus) and Ixodes capularis Say. Journal of Parasitology 67, 813–822.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
Mooring, M. S. and Hart, B. L. (1995). Differential grooming rate and tick load of territorial-male and female impala, Aepyceros melampus. Behavioural Ecology 6, 94–101.CrossRefGoogle Scholar
Morales-Montor, J., Chavarria, A., De León, M. A., Del Castillo, L. I., Escobedo, E. G., Sánchez, E. N., Vargas, J. A., Hernández-Flores, M., Romo-González, T. and Larralde, C. (2004). Host gender in parasitic infections of mammals: an evaluation of the female host supremacy paradigm. Journal of Parasitology 90, 531–546.CrossRefGoogle ScholarPubMed
Morand, S. and Krasnov, B. R. (2008). Why apply ecological laws to epidemiology? Trends in Parasitology 24, 304–309.CrossRefGoogle ScholarPubMed
Morand, S., De Bellocq, J. G., Stanko, M. and Miklisová, D. (2004). Is sex-biased ectoparasitism related to sexual size dimorphism in small mammals of Central Europe? Parasitology 129, 505–510.CrossRefGoogle ScholarPubMed
Nikitina, N. A. and Nikolaeva, G. (1981). Ability of rodents to clean themselves of specific and non-specific fleas. Zoologicheskyi Zhurnal 60, 165–167 (in Russian).Google Scholar
Patterson, B. D., Dick, C. W. and Dittmar, K. (2008). Sex biases in parasitism of neotropical bats by bat flies (Diptera: Streblidae). Journal of Tropical Ecology 24, 387–396.CrossRefGoogle Scholar
Perez-Orella, C. and Schulte-Hostedde, A. I. (2005). Effects of sex and body size on ectoparasite loads in the northern flying squirrel (Glaucomys sabrinus). Canadian Journal of Zoology 83, 1381–1385.CrossRefGoogle Scholar
Perkins, S. E., Cattadori, I. M., Tagliapietra, V., Rizzoli, A. P. and Hudson, P. J. (2003). Empirical evidence for key hosts in persistence of a tick-borne disease. International Journal for Parasitology 33, 909–917.CrossRefGoogle ScholarPubMed
Perry, J. N. (1988). Some models for spatial variability of animal species. Oikos 51, 124–130.CrossRefGoogle Scholar
Perry, J. N. and Taylor, L. R. (1986). Stability of real interacting populations in space and time: Implications, alternatives and negative binomial k c. Journal of Animal Ecology 55, 1053–1068.CrossRefGoogle Scholar
Poulin, R. (1996). Sexual inequalities in helminth infections: a cost of being a male? The American Naturalist 14, 287–295.CrossRefGoogle Scholar
Poulin, R. (2007). Evolutionary Ecology of Parasites: From Individuals to Communities, 2nd Edn.Princeton University Press, Princeton, NJ, USA.CrossRefGoogle Scholar
Presley, S. J. and Willig, M. R. (2008). Intraspecific patterns of ectoparasite abundances on Paraguayan bats: effects of host sex and body size. Journal of Tropical Ecology 24, 75–83.CrossRefGoogle Scholar
Reimchen, T. E. and Nosil, P. (2001). Ecological causes of sex-biased parasitism in threespine stickleback. Biological Journal of the Linnean Society 73, 51–63.Google Scholar
Rechav, Y. (1992). Naturally acquired resistance to ticks – a global veiew. Insect Science and its Application 13, 495–504.Google Scholar
Rechav, Y., Heller-Haupt, A. and Varma, M. G. R. (1989). Resistance and cross-resistance in guinea-pigs and rabbits to immature stages of ixodid ticks. Medical and Veterinary Entomology 3, 333–336.CrossRefGoogle ScholarPubMed
Roberts, M. L., Buchanan, K. L. and Evans, M. R. (2004). Testing the immunocompetence handicap hypothesis: a review of the evidence. Animal Behaviour 68, 227–239.CrossRefGoogle Scholar
Schalk, G. and Forbes, M. R. (1997). Male bias in parasitism of mammals: effects of study type, host age, and parasite taxon. Oikos 78, 67–74.CrossRefGoogle Scholar
Seeman, O. D. and Nahrung, H. F. (2004). Female biased parasitism and the importance of host generation overlap in a sexually transmitted parasite of beetles. Journal of Parasitology 90, 114–118.CrossRefGoogle Scholar
Shaw, D. J. and Dobson, A. P. (1995). Patterns of macroparasite abundance and aggregation in wildlife populations: A quantitative review. Parasitology 111, S111–S127.CrossRefGoogle ScholarPubMed
Sheridan, L. A. D., 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
Sonenshine, D. E. (2005). The biology of tick vectors of human disease. In Tick-borne Diseases of Humans (ed. Goodman, J. L., Dennis, D. T. and Sonenshine, D. E.), pp. 12–36. ASM Press, Washington, USA.Google Scholar
Sonenshine, D. E. (1993). Biology of Ticks. Vol. 2. Part IV. Ecology, Behaviour, and Host-Parasite Interactions. Oxford University Press, New York, USA.Google Scholar
Studdert, V. P. and Arundel, J. H. (1988). Dermatitis of the pinnae of cats in Australia associated with the European rabbit flea (Spilopsyllus cuniculi). Veterinary Record 123, 624–625.Google ScholarPubMed
Taylor, L. R. (1961). Aggregation, variance and the mean. Nature, London 189, 732–735.CrossRefGoogle Scholar
Taylor, L. R. and Taylor, R. A. J. (1977). Aggregation, migration and population dynamics. Nature, London 265, 415–421.CrossRefGoogle Scholar
Taylor, L. R. and Woiwod, I. P. (1980). Temporal stability as a density-dependent species characteristic. Journal of Animal Ecology 49, 209–224.CrossRefGoogle Scholar
Veldtman, R. and McGeoch, M. A. (2004). Spatially explicit host parasitoid relationships: density dependence revisited. Proceedings of the Royal Society London, B 271, 2439–2444.CrossRefGoogle Scholar