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Sex ratio in flea infrapopulations: number of fleas, host gender and host age do not have an effect

Published online by Cambridge University Press:  19 June 2008

B. R. KRASNOV*
Affiliation:
Mitrani Department of Desert Ecology, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sede-Boqer Campus, 84990 Midreshet Ben-Gurion, Israel Ramon Science Center, P.O. Box 194, 80600 Mizpe Ramon, Israel
G. I. SHENBROT
Affiliation:
Mitrani Department of Desert Ecology, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sede-Boqer Campus, 84990 Midreshet Ben-Gurion, Israel Ramon Science Center, P.O. Box 194, 80600 Mizpe Ramon, Israel
I. S. KHOKHLOVA
Affiliation:
Wyler Department of Dryland Agriculture, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sede-Boqer Campus, 84990 Midreshet Ben-Gurion, Israel
H. HAWLENA
Affiliation:
Ramon Science Center, P.O. Box 194, 80600 Mizpe Ramon, Israel Department of Life Sciences, Ben-Gurion University of the Negev, Beer-Sheva 84105, Israel
A. A. DEGEN
Affiliation:
Wyler Department of Dryland Agriculture, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sede-Boqer Campus, 84990 Midreshet Ben-Gurion, Israel
*
*Corresponding author: Mitrani Department of Desert Ecology, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sede Boqer Campus, 84990 Midreshet Ben-Gurion, Israel. Tel: +972 8 6596841. Fax: +972 8 6596772. E-mail: krasnov@bgu.ac.il

Summary

This study set out to determine whether the sex ratio of fleas collected from host bodies is a reliable indicator of sex ratio in the entire flea population. To answer this question, previously published data on 18 flea species was used and it was tested to see whether a correlation exists between the sex ratio of fleas collected from host bodies and the sex ratio of fleas collected from host burrows. Across species, the female:male ratio of fleas on hosts correlated strongly with the female:male ratio of fleas in their burrows, with the slope of the regression overlapping 1. Controlling for flea phylogeny by independent contrasts produced similar results. It was also ascertained whether a host individual is a proportional random sampler of male and female fleas and whether the sex ratio in flea infrapopulations depends on the size of infrapopulations and on the gender and age of a host. Using field data, the sex ratio in infrapopulations of 7 flea species parasitic on 4 rodent species was analysed. Populations of 3 species (Nosopsyllus iranus, Parapulex chephrenis and Xenopsylla conformis) were significantly female-biased, whereas male bias was found in 1 species (Synosternus cleopatrae). In general, the sex ratio of fleas collected from an individual rodent did not differ significantly from the sex ratio in the entire flea population. Neither host gender, and age nor number of fleas co-occurring on a host affected (a) the sex ratio in flea infrapopulations and (b) the probability of an infrapopulation to be either female- or male-biased.

Type
Original Articles
Copyright
Copyright © 2008 Cambridge University Press

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References

REFERENCES

Bodrova, T. V. and Zhovty, I. F. (1961). Fleas of the Daurian ground squirrel in the area of Zun-Torei Lake (S.-E. Trans-Baikalia). Transactions of the Irkutsk State Scientific Anti-Plague Institute of Siberia and Far East 1, 8285 (in Russian).Google Scholar
Bursten, S. N., Kimsey, R. B. and Owings, D. H. (1997). Ranging of male Oropsylla montana fleas via male California ground squirrel (Spermophilus beecheyi) juveniles. Journal of Parasitology 83, 804809.CrossRefGoogle ScholarPubMed
Clark, A. B. (1981) Sex ratio and local resource competition in a prosimian primate. Science 201, 163165.Google Scholar
Clayton, D. H., Gregory, R. D. and Price, R. D. (1992). Comparative ecology of Neotropical bird lice (Insecta: Phthiraptera). Journal of Animal Ecology 61, 781795.CrossRefGoogle Scholar
Combes, C. (2001). Parasitism. The Ecology and Evolution of Intimate Interactions. University of Chicago Press, Chicago, USA.Google Scholar
Cooke, B. D. (1999). Notes on the life history of the rabbit flea Caenopsylla laptevi ibera Beaucornu & Marquez, 1987 (Siphonaptera: Ceratophyllidae) in eastern Spain. Parasite 6, 347354.Google Scholar
Dean, S. R. and Meola, R. W. (2002). Factors influencing sperm transfer and insemination in cat fleas (Siphonaptera: Pulicidae) fed on an artificial membrane system. Journal of Medical Entomology 39, 475479.CrossRefGoogle Scholar
Edney, E. B. (1945). Laboratory studies on the bionomics of the rat fleas, Xenopsylla brasiliensis Baker and X. cheopis Roths. I. Certain effects of light, temperature and humidity on the rate of development and on adult longevity. Bulletin of Entomological Research 35, 399416.Google Scholar
Felsenstein, J. (1985). Phylogenies and the comparative method. American Naturalist, 125, 115.Google Scholar
Fielden, L. J., Krasnov, B. R., Khokhlova, I. S. and Arakelyan, M. S. (2004). Respiratory gas exchange in the desert flea Xenopsylla ramesis (Siphonaptera: Pulicidae): Response to temperature and blood-feeding. Comparative Biochemistry and Physiology A 137, 557565.Google Scholar
Fisher, R. A. (1930). The Genetical Theory of Natural Selection. Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
Garland, T., 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., Dickerman, A. W. C., Janis, M. and Jones, J. A. (1993). Phylogenetic analysis of covariance by computer simulation. Systematic Biology 42, 265292.CrossRefGoogle Scholar
Hawlena, H., Abramsky, Z. and Krasnov, B. R. (2005). Age-biased parasitism and density-dependent distribution of fleas (Siphonaptera) on a desert rodent. Oecologia 146, 200208.CrossRefGoogle ScholarPubMed
Hawlena, H., Abramsky, Z. and Krasnov, B. R. (2007). Ultimate mechanisms of age-biased flea parasitism. Oecologia 154, 601609.CrossRefGoogle ScholarPubMed
Hsu, M. H. and Wu, W. J. (2001). Off-host observations of mating and postmating behaviors in the cat flea (Siphonaptera: Pulicidae). Journal of Medical Entomology 38, 352360.CrossRefGoogle ScholarPubMed
Iqbal, Q. J. and Humphries, D. A. (1970). Temperature as a critical factor in the mating behavior of the rat flea, Nosopsyllus fasciatus (Bosc.). Parasitology 61, 375380.CrossRefGoogle Scholar
Iqbal, Q. J. and Humphries, D. A. (1976). Remating of the rat flea, Nosopsyllus fasciatus (Bosc.). Pakistan Journal of Zoology 8, 3941.Google Scholar
Khokhlova, I. S., Krasnov, B. R., Shenbrot, G. I. and Degen, A. A. (2001). Body mass and environment: a study in Negev rodents. Israel Journal of Zoology 47, 114.CrossRefGoogle Scholar
Krasnov, B. R., Burdelov, S. A., Khokhlova, I. S. and Burdelova, N. V. (2003 a). Sexual size dimorphism, morphological traits and jump performance in seven species of desert fleas (Siphonaptera). Journal of Zoology 261, 181189.Google Scholar
Krasnov, B. R., Hastriter, M., Medvedev, S. G., Shenbrot, G. I., Khokhlova, I. S. and Vatschenok, V. S. (1999). Additional records of fleas (Siphonaptera) on wild rodents in the southern part of Israel. Israel Journal of Zoology 45, 333340.Google Scholar
Krasnov, B. R., Khokhlova, I. S., Burdelov, S. A. and Fielden, L. J. (2004). Metabolic rate and jumping performance in seven species of desert fleas. Journal of Insect Physiology 50, 149156.CrossRefGoogle ScholarPubMed
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 ScholarPubMed
Krasnov, B. R., Morand, S., Khokhlova, I. S., Shenbrot, G. I. and Hawlena, H. (2005). Abundance and distribution of fleas on desert rodents: linking Taylor's power law to ecological specialization and epidemiology. Parasitology 131, 825837.CrossRefGoogle ScholarPubMed
Krasnov, B. R., Sarfati, M., Arakelyan, M. S., Khokhlova, I. S., Burdelova, N. V. and Degen, A. A. (2003 b). Host-specificity and foraging efficiency in blood-sucking parasite: Feeding patterns of a flea Parapulex chephrenis on two species of desert rodents. Parasitology Research 90, 393399.CrossRefGoogle ScholarPubMed
Krasnov, B. R., Shenbrot, G. I., Khokhlova, I. S., Degen, A. A. and Rogovin, K. V. (1996). On the biology of Sundevall's jird (Meriones crassus Sundevall) in Negev Highlands, Israel. Mammalia 60, 375391.CrossRefGoogle Scholar
Krasnov, B. R., Shenbrot, G. I., Medvedev, S. G., Vatschenok, V. S. and Khokhlova, I. S. (1997). Host-habitat relations as an important determinant of spatial distribution of flea assemblages (Siphonaptera) on rodents in the Negev Desert. Parasitology 114, 159173.CrossRefGoogle ScholarPubMed
Kunitskaya, N. T., Gauzshtein, D. M., Kunitsky, V. N., Rodionov, I. A. and Filimonov, V. I. (1965). Feeding activity of fleas parasitic on the great gerbil in experiments. In Proceedings of the IV Scientific Conference on Natural Focality and Prophylaxis of Plague (ed. Aikimbaev, M. A.), pp. 135137. Kainar, Alma-Ata, USSR (in Russian).Google Scholar
Leeson, H. S. (1936). Further experiments upon the longevity of Xenopsylla cheopis Roths. (Siphonaptera). Parasitology 28, 403409.CrossRefGoogle Scholar
Linsdale, J. M. and Davis, B. S. (1956). Taxonomic appraisal and occurrence of fleas at the Hastings Reservation in Central California. University of California Publications in Zoology 54, 293370.Google Scholar
Ma, L.-M. (1993). The sex ratios of some fleas in north China. Acta Entomologica Sinica 36, 6366 (in Chinese).Google Scholar
Maddison, W. P. and Maddison, D. R. (2007). Mesquite: a Modular System for Evolutionary Analysis. Version 2.01. http://mesquiteproject.org.Google Scholar
Margolis, L., Esch, G. W., Holmes, J. C., Kuris, A. M. and Schad, G. A. (1982). The use of ecological terms in parasitology (report of an ad hoc committee of the American Society of Parasitologists). Journal of Parasitology 68, 131133.Google Scholar
Marshall, A. G. (1981 a). Sex ratio in ectoparasitic insects. Ecological Entomology 6, 155174.CrossRefGoogle Scholar
Marshall, A. G (1981 b). The Ecology of Ectoparasitic Insects. Academic Press, London.Google Scholar
Mears, S., Clark, F., Greenwood, M. and Larsen, K. S. (2002). Host location, survival and fecundity of the Oriental rat flea Xenopsylla cheopis (Siphonaptera: Pulicidae) in relation to black rat Rattus rattus (Rodentia: Muridae) host sex and age. Bulletin of Entomological Research 92, 375384.Google Scholar
Midford, P. E., Garland, T. and Maddison, W. (2007). PDAP:PDTREE Package for Mesquite, version 1.1. http://mesquiteproject.org/pdap_mesquite/index.htmlGoogle Scholar
Morand, S., Pointier, J.-P., Borel, G. and Théron, A. (1993). Pairing probability of schistosomes related to their distribution among the host population. Ecology 74, 24442449.CrossRefGoogle Scholar
Peters, R. H. (1983). The Ecological Implications of Body Size. Cambridge University Press, Cambridge, UK.Google Scholar
Poulin, R. (2007). Evolutionary Ecology of Parasites. From Individuals to Communities, 2nd Edn. Princeton University Press, Princeton, USA.Google Scholar
Poulin, R., Krasnov, B. R., Shenbrot, G. I., Mouillot, D. and Khokhlova, I. S. (2006). Evolution of host specificity in fleas: is it directional and irreversible? International Journal for Parasitology 36, 185191.Google Scholar
Ribeiro, J. M. C., Vaughan, J. A. and Azad, A. F. (1990). Characterization of the salivary apyrase activity of three rodent flea species. Comparative Biochemistry and Physiology B 95, 215218.CrossRefGoogle ScholarPubMed
Rothschild, M. and Ford, R. (1972). Breeding cycle of the flea Cediopsylla simplex is controlled by breeding cycle of host. Science 178, 625626.CrossRefGoogle ScholarPubMed
Rothschild, M. and Ford, R. (1973). Factors influencing the breeding of the rabbit flea (Spilopsyllus cuniculi): A spring-time accelerator and a kairomone in nestling rabbit urine (with notes on Cediopsylla simplex, another “hormone bound” species). Journal of Zoology 170, 87137.CrossRefGoogle Scholar
Rousset, F., Thomas, F., de MeeÛs, T. and Renaud, F. (1996). Inference of parasite-induced host mortality from distribution of parasite loads. Ecology 77, 22032211.Google Scholar
Rozsa, L., Récási, J. and Reiczigel, J. (1996). Relationship of host coloniality to the population ecology of avian lice (Insecta: Phthiraptera). Journal of Animal Ecology 65, 242248.Google Scholar
Sarfati, M., Krasnov, B. R., Ghazaryan, L., Khokhlova, I. S., Fielden, L. J. and Degen, A. A. (2005). Energy costs of blood digestion in a host-specific haematophagous parasite. Journal of Experimental Biology 208, 24892496.CrossRefGoogle Scholar
Shenbrot, G. I., Krasnov, B. R. and Khokhlova, I. S. (1997). On the biology of Wagner's gerbil (Gerbillus dasyurus (Wagner, 1842)) (Rodentia: Gerbillidae) in the Negev Highlands, Israel. Mammalia 61, 467486.CrossRefGoogle Scholar
Slonov, M. N. (1965). On the biology of a flea Ceratophyllus tamias Wagn., 1927. Medical Parasitology and Parasitic Diseases 34, 485487 (in Russian).Google Scholar
Stark, H. E. (2002). Population dynamics of adult fleas (Siphonaptera) on hosts and in nests of the California vole. Journal of Medical Entomology 39, 818824.Google Scholar
Tripet, F., Jacot, A. and Richner, H. (2002). Larval competition affects the life histories and dispersal behavior of an avian ectoparasite. Ecology 83, 935945.Google Scholar
Vatschenok, V. S. (1988). Fleas – Vectors of Pathogens Causing Diseases in Humans and Animals. Nauka, Leningrad, USSR (in Russian).Google Scholar
Whiting, M. F., Whiting, A. S., Hastriter, M. W. and Dittmar, K. (2008). A molecular phylogeny of fleas (Insecta: Siphonaptera): origins and host associations. Cladistics (in the Press).Google Scholar
Wilson, K. and Hardy, I. C. W. (2002). Statistical analysis of sex ratios: an introduction. In Sex Ratios: Concepts and Research Methods (ed. Hardy, I. C. W.), pp. 4892. Cambridge University Press, Cambridge, UK.Google Scholar
Zhovty, I. F. and Peshkov, B. I. (1958). Observations on the overwintering of fleas parasitic on the gray marmots in Trans-Baikal. Proceedings of the Irkutsk State Scientific Anti-Plague Institute of Siberia and Far East 17, 2732 (in Russian).Google Scholar
Zuk, M. and McKean, K. A. (1996). Sex differences in parasite infections: patterns and proceses. International Journal for Parasitology 26, 10091024.Google Scholar