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Resource predictability and host specificity in fleas: the effect of host body mass

Published online by Cambridge University Press:  28 March 2006

B. R. KRASNOV
Affiliation:
Ramon Science Center and Mitrani Department of Desert Ecology, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, P.O. Box 194, Mizpe Ramon 80600, Israel
S. MORAND
Affiliation:
Center for Biology and Management of Populations, Campus International de Baillarguet, CS 30016 34988 Montferrier-sur-Lez cedex, France
D. MOUILLOT
Affiliation:
UMR CNRS-UMII 5119 Ecosystemes Lagunaires, University of Montpellier II, CC093, FR-34095 Montpellier Cedex 5, France
G. I. SHENBROT
Affiliation:
Ramon Science Center and Mitrani Department of Desert Ecology, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, P.O. Box 194, Mizpe Ramon 80600, Israel
I. S. KHOKHLOVA
Affiliation:
Desert Animals Adaptations and Husbandry, Wyler Department of Dryland Agriculture, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Beer Sheva 84105, Israel
R. POULIN
Affiliation:
Department of Zoology, University of Otago, P.O. Box 56, Dunedin, New Zealand

Abstract

Ecological specialization is hypothesized to result from the exploitation of predictable resource bases. For parasitic organisms, one prediction is that parasites of large-bodied host species, which tend to be long-lived, should specialize on these hosts, whereas parasites of small host species, which represent more ephemeral and less predictable resources, should become generalists. We tested this prediction by quantifying the association between the level of host specificity of fleas and the mean body mass of their mammalian hosts, using published data from 2 large, distinct geographical regions (South Africa and northern North America). In general, we found supporting evidence that flea host specificity, measured either as the number of host species exploited or their taxonomic distinctness, became more pronounced with increasing host body mass. There were, however, some discrepancies among the results depending on the different measures of host specificity, the geographical region studied, or whether we used the raw values or phylogenetically independent contrasts. These are discussed with respect to other forces acting on the evolution of host specificity in parasites, as well as in the context of the regions' contrasting evolutionary histories. Overall, though, our findings indicate that the exploitation of large-bodied, and therefore long-lived, host species has promoted specialization in fleas, most likely because these hosts represent predictable resources.

Type
Research Article
Copyright
2006 Cambridge University Press

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References

REFERENCES

Barker, S. C., Cribb, T. H., Bray, R. A. and Adlard, R. D. ( 1994). Host-parasite associations on a coral reef: pomacentrid fishes and digenean trematodes. International Journal for Parasitology 24, 643647.CrossRefGoogle Scholar
Bates, J. K. ( 1962). Field studies on the behaviour of bird fleas. I. Behaviour of the adults of three species of bird fleas in the field. Parasitology 52, 113132.CrossRefGoogle Scholar
Brown, J. H. ( 1995). Macroecology. University of Chicago Press, Chicago.
Desdevises, Y., Morand, S. and Legendre, P. ( 2002). Evolution and determinants of host specificity in the genus Lamellodiscus (Monogenea). Biological Journal of the Linnean Society 77, 431443.CrossRefGoogle Scholar
Felsenstein, J. ( 1985). Phylogenies and the comparative method. American Naturalist 125, 115.CrossRefGoogle Scholar
Flynn, J., Finarelli, J. A., Zehr, S., Hsu, J. & Nedball, M. A. ( 2005). Molecular phylogeny of the Carnivora (Mammalia): assessing the impact of increased sampling on resolving enigmatic relationships. Systematic Biology 54, 317337.CrossRefGoogle Scholar
Fox, L. R. and Morrow, P. A. ( 1981). Specialization: species property or local phenomenon? Science 211, 887893.Google Scholar
Fry, J. D. ( 1996). The evolution of host specialization: are trade-offs overrated? American Naturalist 148, S84S107.Google Scholar
Futuyma, D. J. and Moreno, G. ( 1988). The evolution of ecological specialization. Annual Review of Ecology and Systematics 19, 207233.CrossRefGoogle Scholar
Garland, T. Jr., Harvey, P. H. and Ives, A. R. ( 1992). Procedures for the analysis of comparative data using phylogenetically independent contrasts. American Naturalist 41, 1832.Google Scholar
Garland, T. Jr., Dickerman, A. W. C., Janis, M. and Jones, J. A. ( 1993). Phylogenetic analysis of covariance by computer simulation. Systematic Biology 42, 265292.CrossRefGoogle Scholar
Harvey, P. H. and Pagel, M. D. ( 1991). The Comparative Method in Evolutionary Biology. Oxford University Press, Oxford.
Holland, G. P. ( 1985). The fleas of Canada, Alaska and Greenland (Siphonaptera). Memoirs of the Entomological Society of Canada 130, 1631.CrossRefGoogle Scholar
Hsu, M.-H., Hsu, T.-C. and Wu, W.-J. ( 2002). Distribution of cat fleas (Siphonaptera: Pulicidae) on the cat. Journal of Medical Entomology 39, 685688.CrossRefGoogle Scholar
Jurgens, K. D. and Prothero, J. ( 1987). Scaling of maximal lifespan in bats. Comparative Biochemistry and Physiology A 88, 361367.CrossRefGoogle Scholar
Krasnov, B. R. and Khokhlova, I. S. ( 2001). The effect of behavioural interactions on the exchange of flea (Siphonaptera) between two rodent species. Journal of Vector Ecology 26, 181190.Google Scholar
Krasnov, B. R., Shenbrot, G. I., Medvedev, S. G., Vatschenok, V. S. and Khokhlova, I. S. ( 1997). Host-habitat relation as an important determinant of spatial distribution of flea assemblages (Siphonaptera) on rodents in the Negev Desert. Parasitology 114, 159173.CrossRefGoogle Scholar
Krasnov, B. R., Khokhlova, I. S., Fielden, L. J. and Burdelova, N. V. ( 2001). The effect of temperature and humidity on the survival of pre-imaginal stages of two flea species (Siphonaptera: Pulicidae). Journal of Medical Entomology 38, 629637.CrossRefGoogle Scholar
Krasnov, B. R., Mouillot, D., Shenbrot, G. I., Khokhlova, I. S. and Poulin, R. ( 2004 a). Geographical variation in host specificity of fleas (Siphonaptera): the influence of phylogeny and local environmental conditions. Ecography 27, 787797.Google Scholar
Krasnov, B. R., Shenbrot, G. I., Khokhlova, I. S. and Degen, A. A. ( 2004 b). Flea species richness and parameters of host body, host geography and host “milieu” Journal of Animal Ecology 73, 11211128.Google Scholar
Krasnov, B. R., Poulin, R., Shenbrot, G. I., Mouillot, D. and Khokhlova, I. S. ( 2004 c). Ectoparasitic “jacks-of-all-trades”: relationship between abundance and host specificity in fleas (Siphonaptera) parasitic on small mammals. American Naturalist 164, 506516.Google Scholar
Krasnov, B. R., Poulin, R., Shenbrot, G. I., Mouillot, D. and Khokhlova, I. S. ( 2005). Host specificity and geographic range in haematophagous ectoparasites. Oikos 108, 449456.CrossRefGoogle Scholar
Kuris, A. M., Blaustein, A. R. and Alio, J. J. ( 1980). Hosts as islands. American Naturalist 116, 570586.CrossRefGoogle Scholar
Kuznetzov, A. A., Matrosov, A. N., Chyong, L. T. V. and Dat, D. T. ( 1999). Movements of the synantropous rats and their fleas in the settlements of the southern Vietnam. Problemy Osobo Opasnyh Infektzyi [Problems of Especially Dangerous Diseases] 79, 5965 (in Russian).Google Scholar
Lewis, R. E. and Lewis, H. H. ( 1990 a). Catalogue of Invalid Genus-Group and Species-Group Names in Siphonaptera (Insecta), Theses Zoologocae, v. 11. Koeltz Scientific Books, Koenigstein.
Lewis, R. E. and Lewis, J. H. ( 1990 b). An annotated checklist of the fleas (Siphonaptera) of the Middle East. Fauna of Saudi Arabia 11, 251277.Google Scholar
Maddison, W. P. and Maddison, D. R. ( 2005). Mesquite: a Modular System for Evolutionary Analysis. Version 1.06. http://mesquiteproject.org.
Marshall, A. G. ( 1981). The Ecology of Ectoparasite Insects. Academic Press., London.
Matthee, C. A. and Robinson, T. J. ( 1999). Cytochrome b phylogeny of the family bovidae: resolution within the alcelaphini, antilopini, neotragini, and tragelaphini. Molecular Phylogenetics and Evolution 12, 3146.CrossRefGoogle Scholar
Medvedev, S. G. ( 2005). An Attempt of a System Analysis of the Evolution of the Order of Fleas (Siphonaptera), Lectures in Memoriam N. A. Kholodkovsky, No. 57. Russian Entomological Society and Zoological Institute of Russian Academy of Sciences, Saint-Petersburg (in Russian).
Medvedev, S. G., Lobanov, A. L. and Lyanguzov, I. A. ( 2005). World database of fleas (Nov 2004 version). In: Species 2000 and ITIS Catalogue of Life: 2005 Annual Checklist ( ed. Bisby, F. A., Ruggiero, M. A., Wilson, K. L., Cachuela-Palacio, M., Kimani, S. W., Roskov, Y. R., Soulier-Perkins, A. and van Hertum, J.). Species 2000, Reading (CD-ROM).
Midford, P. E., Garland, T. Jr. and Maddison, W. ( 2005). PDAP:PDTREE Package for Mesquite, version 1.07. http://mesquiteproject.org/pdap_mesquite/index.html
Morand, S. and Poulin, R. ( 1998). Density, body mass and parasite species richness of terrestrial mammals. Evolutionary Ecology 12, 717727.CrossRefGoogle Scholar
Muller, G. H., Kirk, R. W., Scott, D. W., Miller, W. H., Griffin, C. E. and Miller, W. T. ( 2001). Muller and Kirk's Small Animal Dermatology. Saunders, Philadelphia.
Norton, D. A. and Carpenter, M. A. ( 1998). Mistletoe as parasites: host specificity and speciation. Trends in Ecology and Evolution 13, 101105.CrossRefGoogle Scholar
Pagel, M. D. ( 1992). A method for the analysis of comparative data. Journal of Theoretical Biology 156, 431442.CrossRefGoogle Scholar
Peters, R. H. ( 1983). The Ecological Implications of Body Size. Cambridge University Press, Cambridge.CrossRef
Poulin, R. ( 1992). Determinants of host specificity in parasites of freshwater fishes. International Journal for Parasitology 22, 753758.CrossRefGoogle Scholar
Poulin, R. ( 1998). Large-scale patterns of host use by parasites of freshwater fishes. Ecology Letters 1, 118128.CrossRefGoogle Scholar
Poulin, R. and Mouillot, D. ( 2003). Parasite specialization from a phylogenetic perspective: a new index of host specificity. Parasitology 126, 473480.CrossRefGoogle Scholar
Reed, D. L. & Hafner, M. S. ( 1997). Host specificity of chewing lice on pocket gophers: a potential mechanism for cospeciation. Journal of Mammalogy 78, 655660.CrossRefGoogle Scholar
Sasal, P., Desdevises, Y. and Morand, S. ( 1998). Host-specialization and species diversity in fish parasites: phylogenetic conservatism? Ecography 21, 639645.Google Scholar
Sasal, P., Trouvé, S., Muller-Graf, C. and Morand, S. ( 1999). Specificity and host predictability: a comparative analysis among monogenean parasites of fish. Journal of Animal Ecology 68, 437444.CrossRefGoogle Scholar
Segerman, J. ( 1995). Siphonaptera of Southern Africa: handbook for the identification of fleas. Publications of the South African Institute for Medical Research 57, 1264.Google Scholar
Shepherd, R. C. H. and Edmonds, J. W. ( 1979). The distribution of the stickfast fleas, Echidnophaga mirmecobii Rotschild and E. perilis Jordan, on the wild rabbit, Oryctolagus cuniculus (L.). Australian Journal of Zoology 27, 261271.Google Scholar
Silva, M. and Downing, J. A. ( 1995). CRC Handbook of Mammalian Body Masses. CRC Press, Boca Raton, Florida.
Simkova, A., Desdevises, Y., Gelnar, M. and Morand, S. ( 2001). Morphometric correlates of host specificity in Dactylogyrus species (Monogenea) parasites of European Cyprinid fish. Parasitology 123, 169177.CrossRefGoogle Scholar
Vatschenok, V. S. ( 1988). Fleas – Vectors of Pathogens Causing Diseases in Humans and Animals. Nauka Publishing House, Leningrad, USSR (in Russian).
Ward, S. A. ( 1992). Assessing functional explanations of host-specificity. American Naturalist 139, 883891.CrossRefGoogle Scholar
Warwick, R. M. and Clarke, K. R. ( 2001). Practical measures of marine biodiversity based on relatedness of species. Oceanography and Marine Biology Annual Review 39, 207231.Google Scholar
Wilkinson, G. S. and South, J. M. ( 2002). Life history, ecology and longevity of bats. Aging Cell 1, 124131.CrossRefGoogle Scholar
Wilson, D. E. and Reeder, D. M. (eds.) ( 1993). Mammal Species of the World: A Taxonomic and Geographic Reference. Smithsonian Institution Press, Washington.