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Positive co-occurrence of flea infestation at a low biological cost in two rodent hosts in the Canary archipelago

Published online by Cambridge University Press:  21 November 2013

S. SÁNCHEZ ,
E. SERRANO ,
M. S. GÓMEZ ,
C. FELIU  and
S. MORAND
S. SÁNCHEZ*
Affiliation:
Departament de Microbiologia i Parasitologia, Facultat de Farmàcia, Universitat de Barcelona, Avda. Joan XXIII, 08028, Barcelona, Spain
E. SERRANO
Affiliation:
Servei d´Ecopatologia de Fauna Salvatge (SEFaS), Departament de Medicina i Cirurgia Animals, Universitat Autònoma de Barcelona, Barcelona, Spain Estadística i Investigació Operativa, Departament de Matemàtica, Universitat de Lleida, Lleida, Spain
M. S. GÓMEZ
Affiliation:
Departament de Microbiologia i Parasitologia, Facultat de Farmàcia, Universitat de Barcelona, Avda. Joan XXIII, 08028, Barcelona, Spain
C. FELIU
Affiliation:
Departament de Microbiologia i Parasitologia, Facultat de Farmàcia, Universitat de Barcelona, Avda. Joan XXIII, 08028, Barcelona, Spain
S. MORAND
Affiliation:
Institut des Sciences de l'Evolution, CNRS-IRD-UM2, Université Montpellier 2, Montpellier, France
*
* Corresponding author: Departament de Microbiologia i Parasitologia, Facultat de Farmàcia, Universitat de Barcelona, Avda. Joan XXIII, 08028, Barcelona, Spain. E-mail: [email protected]
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Summary

Non-random assemblages have been described as a common pattern of flea co-occurrence across mainland host species. However, to date, patterns of flea co-occurrence on islands are unknown. The present work investigates, on one hand, whether the decrease in the number of species on islands affects the pattern of flea co-occurrence, and on the other hand, how the cost of higher flea burdens affects host body mass. The study was carried out in the Canary Islands (Spain) using null models to analyse flea co-occurrence on Rattus rattus and Mus musculus. Results supported aggregation of flea species in Mus but not in Rattus, probably due to the relationship between abundance and both prevalence and intensity of infection of the main flea species parasitizing Mus. In addition, heavy individuals of both rodent species showed the highest flea burdens as well as higher species richness, probably due to the continued accumulation of fleas throughout life and/or immunological resistance mechanisms. Whatever the mechanisms involved, it is clear that co-occurrence and high parasite intensities do not imply a detrimental biological cost for the rodents of the Canary Islands.

Keywords

Canary Islandsco-occurrencefleashost-densityMus musculusnull modelsRattus rattus
Type
Research Article
Information
Parasitology , Volume 141 , Issue 4 , April 2014 , pp. 511 - 521
Copyright
Copyright © Cambridge University Press 2013 

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References

REFERENCES

Alder, G. H. and Levins, R. (1994). The island syndrome in rodent populations. Quarterly Review of Biology 69, 473–490.Google Scholar
Beaucournu, J. C. and Launay, H. (1990). Les puces de France et du basin mediterraneen occidental, Faune de France, Vol. 76. Fédération Française des Sociétes de Sciences Naturelles, Paris, France.Google Scholar
Blanco, J. C. (1998). Mamíferos de España, Vol. II. Geoplaneta, Barcelona, Spain.Google Scholar
Blondel, J. (1995). Biogéographie: Approche écologique et évolutive. Masson, Paris, France.Google Scholar
Bordes, F. and Morand, S. (2009). Parasite diversity: an overlooked metric of parasite pressures? Oikos 118, 801–806. doi: 10.1111/j.1600-0706.2008.17169.x.Google Scholar
Bordes, F., Morand, S. and Guerrero, R. (2008). Bat fly species richness in Neotropical bats: correlations with host ecology and host brain. Oecologia 158, 109–116. doi: 10.1007/s00442-008-1115-x.CrossRefGoogle ScholarPubMed
Both, C., Melo, A. S., Cechin, S. Z. and Hartz, S. M. (2011). Tadpole co-occurrence in ponds: when do guilds and time matter? Acta Oecologica 37, 140–145. doi: 10.1016/j.actao.2011.01.008.Google Scholar
Burnham, K. P. and Anderson, D. R. (2002). Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach. Springer-Verlag, New York, USA.Google Scholar
Bush, A. O., Lafferty, K. D., Lotz, J. M. and Shostack, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575–583.Google Scholar
den Hollander, N. and Allen, J. R. (1986). Cross-reactive antigens between a tick Dermacentor variabilis (Acari: Ixodidae) and a mite Prosoptes cuniculi (Acari: Psoropeptidae). Journal of Medical Entomology 23, 44–50.CrossRefGoogle Scholar
Ezenwa, V., Price, S. A., Altizer, S., Vitone, N. D. and Cook, C. (2006). Host traits and parasite species richness in even and odd-toed hoofed mammals, Artiodactyla and Perissodactyla. Oikos 115, 526–536. doi: 10.1111/j.2006.0030-1299.15186.x.Google Scholar
Feliu, C., Renaud, F., Catzeflis, F., Durand, P., Hugot, J. P. and Morand, S. (1997). A comparative analysis of parasites species richness of Iberian rodents. Parasitology 115, 453–466. doi: 10.1017/S0031182097001479.Google Scholar
Gotelli, N. J. (2000). Null model analysis of species co-occurrence patterns. Ecology 81, 2606–2621.Google Scholar
Gotelli, N. J. and McCabe, D. J. (2002). Species co-occurrence: a meta-analysis of J. M. Diamond's assembly rules model. Ecology 83, 2091–2096.CrossRefGoogle Scholar
Gotelli, N. J. and Rohde, K. (2002). Co-occurrence of ectoparasites of marine fishes: a null model analysis. Ecology Letters 5, 86–94. doi: 10.1046/j.1461-0248.2002.00288.x. Google Scholar
Entsminger, G. L. (2012). EcoSim Professional: Null Modeling Software for Ecologists. Version 1. Acquired Intelligence Inc., Kesey-Bear, & Pinyon Publishing. Montrose, CO 81403, USA. http://www.garyentsminger.com/ecosim/index.htm Google Scholar
Hawlena, H., Krasnov, B. R., Abramsky, Z., Khokhlova, I. S., Saltz, D., Kam, M., Tamir, A. and Degen, A. A. (2006 a). Flea infestation and energy requirements of rodent hosts: are there general rules? Functional Ecology 20, 1028–1036. doi: 10.1111/j.1365-2435.2006.01190.x.Google Scholar
Hawlena, H., Khokholova, I. S., Abramsky, Z. and Krasnov, B. R. (2006 b). Age, intensity of infestation by flea parasites and body mass loss in a rodent host. Parasitology 133, 187–193. doi: 10.1017/S003118200600030.Google Scholar
Hawlena, H., Krasnov, B. R., Abramsky, Z., Khoklova, I. S., Goüy de Bellocq, J. and Pinshow, B. (2008). Effects of food abundance, age, and flea infestation on the body condition and immunological variables of a rodent host, and their consequences for flea survival. Comparative Biochemistry and Physiology 150, 66–74. doi: 10.1016/j.cbpa.2008.03.004.Google Scholar
Hopkins, G. H. E. and Rothschild, M. (1962). An Illustrated Catalogue of the Rothschild Collection of Fleas (Siphonaptera) in the British Museum (Natural History), Vol III: Hystrichopsyllidae. British Museum, London, UK.Google Scholar
Johnson, J. B. and Omland, K. S. (2004). Model selection in ecology and evolution. Trends in Ecology and Evolution 19, 101–108. doi: 10.1016/j.tree.2003.10.013.Google Scholar
Jordan, K. (1958). Contribution to the Taxonomy of Stenoponia J. et R. (1911), a genus of Palearctic and Nearctic fleas. Bulletin of the British Museum (Natural History). Entomology 6, 169–202.Google Scholar
Khokhlova, I. S., Krasnov, B. R., Kam, M., Burdelova, N. I. and Degen, A. A. (2002). Energy cost of ectoparasitism: the flea Xenopsylla ramesis on the desert gerbil Gerbillus dasyurus. Journal of Zoology 258, 349–354. doi: 10.1017/S0952836902001498.Google Scholar
Khokhlova, I. S., Spinu, M., Krasnov, B. R. and Degen, A. A. (2004 a). Immune response to fleas in a wild desert rodent: effect of parasite species, parasite burden, sex of host and host parasitological experience. Journal of Experimental Biology 207, 2725–2733. doi: 10.1242/jeb.01090.Google Scholar
Khokhlova, I. S., Spinu, M., Krasnov, B. R. and Degen, A. A. (2004 b). Immune responses to fleas in two rodent species differing in natural prevalence on infestation and diversity of flea assemblages. Parasitology Research 94, 304–311. doi: 10.1007/s00436-004-1215-4.CrossRefGoogle ScholarPubMed
Krasnov, B. R. (2008). Functional and Evolutionary Ecology of Fleas: a Model for Ecological Parasitology. Cambridge University Press, Cambridge.Google Scholar
Krasnov, B. R., Shenbrot, G. I., Khokhlova, I. S. and Degen, A. A. (2004). Flea species richness and parameters of host body, host geography and host ‘milieu’. Journal of Animal Ecology 73, 1121–1128. doi: 10.1111/j.0021-8790.2004.00883.x. Google Scholar
Krasnov, B. R., Mouillot, D., Khokhlova, I. S., Shenbrot, G. I. and Poulin, R. (2005). Covariance in species diversity and facilitation among non-interactive parasite taxa: all against the host. Parasitology 130, 557–568. doi: 10.1017/S0031182005007912 Google Scholar
Krasnov, B. R., Stanko, M. and Morand, S. (2006). Are ectoparasite communities structured? Species co-occurrence, temporal variation and null models. Journal of Animal Ecology 75, 1330–1339.CrossRefGoogle ScholarPubMed
Krasnov, B. R., Matthee, S., Lareschi, M., Korallo-Vinarskaya, N. P. and Vinarski, M. V. (2010). Co-occurrence of ectoparasites on rodent hosts; null model analyses of data from three continents. Oikos 119, 120–128. doi: 10.1111/j.1600-0706.2009.17902.x.Google Scholar
Krasnov, B. R., Shenbrot, G. I. and Khokhlova, S. (2011). Aggregative structure is the rule in communities of fleas: null model analysis. Ecography 34, 751–761. doi: 10.1111/j.1600-0587.2010.06597.x.Google Scholar
Kuris, A. M., Blaustein, A. R. and Alio, J. J. (1980). Hosts as islands. American Naturalist 116, 570–586.Google Scholar
MacArthur, R. H. and Wilson, E. O. (1967). The Theory of Island Biogeography. Princeton University Press. Princeton, NJ.Google Scholar
Mans, B. J., Louw, A. I. and Neitz, A. W. H. (2002). Evolution of hematophagy in ticks: common origins for blood coagulation and platelet aggregation inhibitors from soft ticks of the genus Ornithodoros . Molecular Biology and Evolution 19, 1695–1705.CrossRefGoogle ScholarPubMed
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 scapularis Say. Journal of Parasitology 67, 813–822.Google Scholar
Morand, S. (2000). Wormy world: comparative tests of theoretical hypotheses on parasite species richness. In Evolutionary Biology of Host–Parasite Relationships: Theory Meets Reality (ed. Poulin, R., Morand, S. and Skorping, A.), pp. 63–79. Elsevier, Amsterdam, the Netherlands.Google Scholar
Nogales, M., Rodríguez-Luengo, J. L. and Marrero, P. (2006). Ecological effects and distribution of invasive non-native mammals on the Canary Islands. Mammal Review 36, 49–65. doi: 10.1111/j.1365-2907.2006.00077.x.Google Scholar
Nunn, C. L., Altizer, S., Jones, K. E. and Sechrest, W. (2003). Comparative tests of parasites species richness in primates. American Naturalist 162, 597–614.Google Scholar
Rando, J. C. (2009). Control de roedores, equipamientos de uso público y centros del Cabildo de Tenerife localizados en Espacios Naturales Forestales. Área de Medio Ambiente y Paisaje, Cabildo de Tenerife.Google Scholar
R Development Core Team 3.0.1. (2013). A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org.Google Scholar
Stevenson, M., Nunes, T., Sanchez, J., Thornton, R., Reiczigel, J., Robison-Cox, J. and Sebastiani, P. (2013). epiR: An R package for the analysis of epidemiological data. R package version 0.9–48. http://CRAN.R-project.org/package=epiR.Google Scholar
Stanko, M., Miklisova, D., de Bellocq, J. G. and Morand, S. (2002). Mammal density and patterns of ectoparasite species richness and abundance. Oecologia 131, 289–295. doi: 10.1007/s00442-002-0889-5.Google Scholar
Stone, L. and Roberts, A. (1990). The checkerboard score and species distributions. Oecologia 85, 74–79.Google Scholar
Tobin, M. E. and Sugihara, R. T. (1992). Abundance and habitat relationships of rats in Hawaiian sugarcane fields. Journal of Wildlife Management 56, 816–822.Google Scholar
Viney, M. E., Riley, E. M. and Buchanan, K. L. (2005). Optimal immune responses: immunocompetence revisited. Trends in Ecology and Evolution 20, 665–669. doi: 10.1016/j.tree.2005.10.003.Google Scholar
Zuur, A. F., Ieno, E. N. and Smith, G. M. (2007). Analysing Ecological Data. Springer, New York, USA.Google Scholar
Zuur, A. F., Ieno, E. N., Walker, N. J., Saveliev, A. A. and Smith, G. M. (2009). Mixed Effects Models and Extension in Ecology with R. Springer, New York, USA.Google Scholar