Hostname: page-component-8448b6f56d-t5pn6 Total loading time: 0 Render date: 2024-04-24T04:55:51.368Z Has data issue: false hasContentIssue false
  • English
  • Français

Environment-related and host-related factors affecting the occurrence of lice on rodents in Central Europe

Published online by Cambridge University Press:  05 February 2015

MICHAL STANKO ,
JANA FRIČOVÁ ,
DANA MIKLISOVÁ ,
IRINA S. KHOKHLOVA  and
BORIS R. KRASNOV
MICHAL STANKO
Affiliation:
Institute of Parasitology, Slovak Academy of Sciences, Lofflerova 10, SK-04001 Kosice, Slovakia
JANA FRIČOVÁ
Affiliation:
Institute of Parasitology, Slovak Academy of Sciences, Lofflerova 10, SK-04001 Kosice, Slovakia
DANA MIKLISOVÁ
Affiliation:
Institute of Parasitology, Slovak Academy of Sciences, Lofflerova 10, SK-04001 Kosice, Slovakia
IRINA S. KHOKHLOVA
Affiliation:
Wyler Department of Dryland Agriculture, French Associates Institute for Agriculture, French Associates Institute for Agriculture and Biotechnology of Drylands, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sede-Boqer Campus, 84990 Midreshet Ben-Gurion, Israel
BORIS R. KRASNOV*
Affiliation:
Mitrani Department of Desert Ecology, Swiss Institute of Dryland Environmental and Energy Research, 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, Swiss Institute for Dryland Environmental and Energy Research, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sede-Boqer Campus, 84990 Midreshet Ben-Gurion, Israel. E-mail: krasnov@bgu.ac.il
Get access Rights & Permissions [Opens in a new window]

Summary

We studied the effects of environment- (habitat, season) and host-related (sex, body mass) factors on the occurrence of four species of lice (Insecta:Phthiraptera:Anoplura) on six rodent species (Rodentia:Muridae). We asked how these factors influence the occurrence of lice on an individual host and whether different rodent–louse associations demonstrate consistent trends in these effects. We found significant effects of at least one environment-related and at least one host-related factor on the louse occurrence in five of six host–louse associations. The effect of habitat was significant in two associations with the occurrence of lice being more frequent in lowland than in mountain habitats. The effect of season was significant in five associations with a higher occurrence of infestation during the warm season in four associations and the cold season in one association. Host sex affected significantly the infestation by lice in three associations with a higher frequency of infestation in males. Host body mass affected the occurrence of lice in all five associations, being negative in wood mice and positive in voles. In conclusion, lice were influenced not only by the host- but also by environment-related factors. The effects of the latter could be mediated via life history parameters of a host.

Keywords

body masshabitatlicerodentsseasonsex
Type
Research Article
Information
Parasitology , Volume 142 , Issue 7 , June 2015 , pp. 938 - 947
Check for updates
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Archer, E. K., Bennett, N. C., Ueckermann, E. A. and Lutermann, H. (2014). Ectoparasite burdens of the common mole-rat (Cryptomys hottentotus hottentotus) from the Cape provinces of South Africa. Journal of Parasitology 100, 79–84.Google Scholar
Balashov, Y. S., Bochkov, A. V., Vashchenok, V. S., Grigor'eva, L. A. and Tret'akov, K. A. (2002). Structure and seasonal dynamics of the biotic community ectoparasites of the bank vole in the Il'men’-Volkhov lowland. Parazitologiia 36, 433–446. (in Russian).Google Scholar
Barton, K. (2014). MuMIn: Multi-model inference. R package version 1.10.5. http://CRAN.R-project.org/package=MuMIn Google Scholar
Bashenina, N. V. (1962). The Ecology of the Common Vole. Moscow University Press, Moscow, USSR (in Russian).Google Scholar
Bates, D., Maechler, M., Bolker, B. and Walker, S. (2014 a). lme4: Linear mixed-effects models using Eigen and S4. R package version 1.1–7, http://CRAN.R-project.org/package=lme4 Google Scholar
Bates, D., Maechler, M., Bolker, B. and Walker, S. (2014 b). lme4: Linear mixed-effects models using Eigen and S4. ArXiv e-print; submitted to Journal of Statistical Software http://arxiv.org/abs/1406.5823 Google Scholar
Blanco, G., Tella, J. L. and Potti, J. (1997). Feather mites on group-living Red-billed Choughs: a non-parasitic interaction? Journal of Avian Biology 28, 197–206.Google Scholar
Brown, M. J. F., Loosli, R. and Schmid-Hempel, P. (2000). Condition-dependent expression of virulence in a trypanosome infecting bumblebees. Oikos 91, 421–427.Google Scholar
Bryja, J., Patzenhauerová, H., Albrecht, T., Mošanský, L., Stanko, M. and Stopka, P. (2008). Varying levels of female promiscuity in four Apodemus mice species. Behavioral Ecology and Sociobiology 63, 251–260.Google Scholar
Calvete, C., Estrada, R., Lucientes, J. and Estrada, A. (2003). Ectoparasite ticks and chewing lice of red-legged partridge, Alectoris rufa, in Spain. Medical and Veterinary Entomology 17, 33–37.CrossRefGoogle ScholarPubMed
Chełkowska, H. (1978). Variations in number and social factors in a population of field voles. Acta Theriologica 23, 213–238.Google Scholar
Colwell, D. D. (2014). Life history parameters of the cattle long-nosed sucking louse, Linognathus vituli . Medical and Veterinary Entomology 28, 432–437.Google Scholar
Dawson, R. D. and Bortolotti, G. R. (1997). Ecology of parasitism of nestling American Kestrels by Carnus hemapterus (Diptera, Carnidae). Canadian Journal of Zoology 75, 2021–2026.Google Scholar
Durden, L. A. and Eckerlin, R. P. (2001). Polyplax guatemalensis sp. n. (Phthiraptera: Anoplura), a new sucking louse from Peromyscus grandis, a montane cloud forest rodent from Guatemala. Folia Parasitologica 48, 69–72.CrossRefGoogle Scholar
Durden, L. A. and Timm, R. M. (2001). Hoplopleura janzeni n. sp. (Phthiraptera: Anoplura), a new sucking louse from a Central American swimming mouse. Journal of Parasitology 87, 1409–1413.Google Scholar
Durden, L. A., Kollars, T. M. Jr., Patton, S. and Gerhardt, R. R. (1997). Sucking lice (Anoplura) of mammals of Tennessee. Journal of Vector Ecology 22, 71–76.Google Scholar
Eccard, J. A. and Herde, A. (2013). Seasonal variation in the behaviour of a short-lived rodent. BMC Ecology 13, 43.Google Scholar
Fernandes, F. R., Cruz, L. D. and Linhares, A. X. (2012). Effects of sex and locality on the abundance of lice on the wild rodent Oligoryzomys nigripes . Parasitology Research 111, 1701–1706.Google Scholar
Fernández-Salvador, R., García-Perea, R. and Ventura, J. (2001). Reproduction and postnatal growth of the Cabrera vole, Microtus cabrerae, in captivity. Canadian Journal of Zoology 79, 2080–2085.Google Scholar
Fuller, W. A. (1967). Winter ecology of lemmings and fluctuations of their populations. Terre et la Vie 2, 97–115.Google Scholar
Gauffre, B., Petit, E., Brodier, S., Bretagnolle, V. and Cosson, J. F. (2009). Sex-biased dispersal patterns depend on the spatial scale in a social rodent. Proceedings of the Royal Society of London B 276, 3487–3494.Google Scholar
Goater, C. P. and Ward, P. I. (1992). Negative effects of Rhabdias bufonis (Nematoda) on the growth and survival of toads (Bufo bufo). Oecologia 89, 161–165.Google Scholar
Gromov, V. S. and Voznesenskaya, V. V. (2010). Parental care, aggressiveness, and testosterone secretion in male common voles (Microtus arvalis) and steppe lemmings (Lagurus lagurus). Doklady Biological Sciences 431, 86–88.Google Scholar
Haitlinger, R. (1983). Invertebrates associated with the bank vole. Arthropod communities. Acta Theriologica 28, 55–68.Google Scholar
Hudson, P. J. and Dobson, A. P. (1995). Macroparasites: observed patterns. In Ecology of Infectious Diseases in Natural Populations (eds. Grenfell, B. T. and Dobson, A. P.), pp. 144–176. Cambridge University Press, Cambridge.Google Scholar
Jore, S., Vanwambeke, S. O., Viljugrein, H., Isaksen, K., Kristoffersen, A. B., Woldehiwet, Z., Johansen, B., Brun, E., Brun-Hansen, H., Westermann, S., Larsen, I.-L., Ytrehus, B. and Hofshagen, M. (2014). Climate and environmental change drives Ixodes ricinus geographical expansion at the northern range margin. Parasites and Vectors 7, 11.Google Scholar
Khokhlova, I. S., Spinu, M., Krasnov, B. R. and Degen, A. A. (2004). Immune responses to fleas in two rodent species differing in natural prevalence of infestation and diversity of flea assemblages. Parasitology Research 94, 304–311.Google Scholar
Kiffner, C., Stanko, M., Morand, S., Khokhlova, I. S., Shenbrot, G. I., Laudisoit, A., Leirs, H., Hawlena, H. and Krasnov, B. R. (2013). Sex-biased parasitism is not universal: evidence from rodent-flea associations from three biomes. Oecologia 173, 1009–1022.Google Scholar
Kiffner, C., Stanko, M., Morand, S., Khokhlova, I. S., Shenbrot, G. I., Laudisoit, A., Leirs, H., Hawlena, H. and Krasnov, B. R. (2014). Variable effects of host characteristics on species richness of flea infracommunities in rodents from three continents. Parasitology Research 113, 2777–2788.Google Scholar
Korslund, L. and Steen, H. (2006). Small rodent winter survival: snow conditions limit access to food resources. Journal of Animal Ecology 75, 156–166.Google Scholar
Krasnov, B. R. and Matthee, S. (2010). Spatial variation in gender-biased parasitism: host-related, parasite-related and environment-related effects. Parasitology 137, 1526–1537.Google Scholar
Krasnov, B. R., Morand, S., Hawlena, H., Khokhlova, I. S. and Shenbrot, G. I. (2005 a). Sex-biased parasitism, seasonality and sexual size dimorphism in desert rodents. Oecologia 146, 209–217.Google Scholar
Krasnov, B. R., Khokhlova, I. S., Arakelyan, M. S. and Degen, A. A. (2005 b). Is a starving host tastier? Reproduction in fleas parasitizing food-limited rodents. Functional Ecology 19, 625–631.Google Scholar
Krasnov, B. R., Stanko, M. and Morand, S. (2006 a). Age-dependent flea (Siphonaptera) parasitism in rodents: a host's life history matters. Journal of Parasitology 92, 242–248.Google Scholar
Krasnov, B. R., Stanko, M. and Morand, S. (2006 b). Are ectoparasite communities structured? Species co-occurrence, temporal variation and null models. Journal of Animal Ecology 75, 1330–1339.Google Scholar
Krasnov, B. R., Stanko, M. and Morand, S. (2007). Host community structure and infestation by ixodid ticks: repeatability, dilution effect and ecological specialization. Oecologia 154, 185–194.Google Scholar
Krasnov, B. R., Stanko, M. and Morand, S. (2010). Competition, facilitation or mediation via host? Patterns of infestation of small European mammals by two taxa of haematophagous arthropods. Ecological Entomology 35, 37–44.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
Krištofík, J. and Lysy, J. (1982). Seasonal dynamics of sucking lice (Anoplura) in small mammals (Insectivora, Rodentia) in the natural foci of infections in south-west Slovakia. Biologia (Bratislava) 47, 605–617.Google Scholar
Leeson, H. S. (1941). The effect of temperature upon the hatching of the eggs of Pediculus humanus corporis De Geer (Anoplura). Parasitology 33, 243–249.Google Scholar
Lehane, M. (2005). The Biology of Blood-Sucking in Insects, 2nd edn. Cambridge University Press, Cambridge.Google Scholar
Leonardi, M. S. and Palma, R. L. (2013). Review of the systematics, biology and ecology of lice from pinnipeds and river otters (Insecta: Phthiraptera: Anoplura: Echinophthiriidae). Zootaxa 3630, 445–466.Google Scholar
Lin, L. K., Nishino, T. and Shiraishi, S. (1993). Postnatal growth and development of the Formosan wood mouse Apodemus semiotus . Journal of the Mammalogical Society of Japan 18, 1–18.Google Scholar
Linardi, P. M. and Krasnov, B. R. (2013). Patterns of diversity and abundance of fleas (Insecta: Siphonaptera) and mites (Acari: Mesostigmata) in the Neotropics: host-related, parasite-related and environment-related factors. Medical and Veterinary Entomology 27, 49–58.Google Scholar
Łopucki, R. (2007). Social relationships in a bank vole Clethrionomys glareolus (Schreber 1780) population: video monitoring under field conditions. Polish Journal of Ecology 55, 543–558.Google Scholar
Marshall, A. D. (1981). The Ecology of Ectoparasitic Insects. Academic Press, London.Google Scholar
Matthee, S., McGeoch, M. A. and Krasnov, B. R. (2010). Parasite-specific variation and the extent of male-biased parasitism; an example with a South African rodent and ectoparasitic arthropods. Parasitology 137, 651–660.Google Scholar
Mazur, E. and Jakal, J. (1982). Atlas Slovenskej Socialistickej Republiky. Slovenska Academia Vied, Bratislava (in Slovak).Google Scholar
Miller, R. A. (1996). The aging immune system: primer and prospectus. Science 273, 70–74.Google Scholar
Mize, E. L., Tsao, J. I. and Maurer, B. A. (2011). Habitat correlates with the spatial distribution of ectoparasites on Peromyscus leucopus in southern Michigan. Journal of Vector Ecology 36, 308–320.Google Scholar
Moyer, B. R., Drown, D. D. and Clayton, D. H. (2002). Low humidity reduces ectoparasite pressure: implications for host life history evolution. Oikos 97, 223–228.Google Scholar
Musser, G. G., Durden, L. A., Holden, M. E. and Light, J. E. (2010). Systematic review of endemic Sulawesi squirrels (Rodentia, Sciuridae), with descriptions of new species of associated sucking lice (Insecta, Anoplura), and phylogenetic and zoogeographic assessments of sciurid lice. Bulletin of the American Museum of Natural History 339, 1–260.Google Scholar
Nakagawa, S. and Schielzeth, H. (2013). A general and simple method for obtaining R 2 from generalized linear mixed-effects models. Methods in Ecology and Evolution 4, 133–142.Google Scholar
Nakatsu, A. (1975). Some observations on the Japanese field vole, Microtus montebelli (Milne-Edwards) in captivity. I. Postnatal growth and development. Bulletin of the Government Forest Experiment Station 276, 23–29.Google Scholar
Oguge, N. O., Durden, L. A., Keirans, J. E., Balami, H. D. and Schwan, T. G. (2009). Ectoparasites (sucking lice, fleas and ticks) of small mammals in southeastern Kenya. Medical and Veterinary Entomology 23, 387–392.Google Scholar
Oppliger, A., Christe, P. and Richner, H. (1996). Clutch size and malaria resistance. Nature 381, 565.Google Scholar
Pacala, S. W. and Dobson, A. P. (1988). The relation between the number of parasites/host and host age: population dynamic causes and maximum likelihood estimation. Parasitology 96, 197–210.Google Scholar
Pruitt, W. O. (1984). Snow and small mammals. In Winter Ecology of Small Mammals (ed. Merritt, J. F.), pp. 1–8. Carnegie Museum of Natural History, Pittsburgh.Google Scholar
R Core Team (2013). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/ Google Scholar
Reiczigel, J. (2003). Confidence intervals for the binomial parameter: some new considerations. Statistics in Medicine 22, 611–621.Google Scholar
Rózsa, L., Reiczigel, J. and Majoros, G. (2000). Quantifying parasites in samples of hosts. Journal of Parasitology 86, 228–232.Google Scholar
Scantlebury, M., Maher McWilliams, M., Marks, N. J., Dick, J. T. A., Edgar, H. and Lutermann, H. (2010). Effects of life-history traits on parasite load in grey squirrels. Journal of Zoology 282, 246–255 Google Scholar
Schrader, G., Schmolz, E., Könning, M. and Dahl, R. (2008). Survival and reproduction of a laboratory strain of body lice (Phthiraptera: Pediculidae) at different ambient temperatures. In Proceedings of the Sixth International Conference on Urban Pests (ed. Robinson, W. H. and Bajomi, D.), pp. 307–314. OOK-Press Kft., Veszprém, Hungary.Google Scholar
Simon, A., Thomas, D. W., Blondel, J., Lambrechts, M. M. and Perret, P. (2003). Within-brood distribution of ectoparasite attacks on nestling blue tits: a test of the tasty chick hypothesis using inulin as a tracer. Oikos 102, 551–558.Google Scholar
Smith, V. S., Light, J. E. and Durden, L. A. (2008). Rodent louse diversity, phylogeny, and cospeciation in the Manu Biosphere Reserve, Peru. Biological Journal of the Linnean Society 95, 598–610.Google Scholar
Sosnina, E. F., Nazarova, I. V. and Sadekova, L. K. (1981). Sucking lice of small mammals from the Volga-Kama State Reserve. Parazitologiia 15, 157–162. (in Russian).Google Scholar
Stanko, M. (1988). Fleas (Siphonaptera) of small mammals in eastern part of Volovské vrchy mountains. Acta Rerum Naturalium Musei Nationalis Slovaci 34, 29–40. (in Slovakian).Google Scholar
Stanko, M. (1994). Fleas synusy (Siphonaptera) of small mammals from the central part of the East-Slovakian lowlands. Biologia (Bratislava) 49, 239–246.Google Scholar
Stanko, M., Miklisová, D., Goüy de Bellocq, J. and Morand, S. (2002). Mammal density and patterns of ectoparasite species richness and abundance. Oecologia 131, 289–295.Google Scholar
Stanko, M., Krasnov, B. R., Miklisová, D. and Morand, S. (2007). Simple epidemiological model predicts the relationships between prevalence and abundance in ixodid ticks. Parasitology 134, 59–68.Google Scholar
Štefka, J. and Hypša, V. (2008). Host specificity and genealogy of the louse Polyplax serrata on field mice, Apodemus species: a case of parasite duplication or colonisation? International Journal for Parasitology 38, 731–741.Google Scholar
Tschirren, B., Bischoff, L. L., Saladin, V. and Richner, H. (2007). Host condition and host immunity affect parasite fitness in a bird-ectoparasite system. Functional Ecology 21, 372–378.Google Scholar
Viljoen, H., Bennett, 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
Whiteman, N. K. and Parker, P. G. (2004). Body condition and parasite load predict territory ownership in the Galapagos hawk. The Condor 106, 915–921.Google Scholar
Wilson, N. A., Telford, S. R. and Forrester, D. J. (1991). Ectoparasites of a population of urban gray squirrels in northern Florida. Journal of Medical Entomology 28, 461–464.Google Scholar
Zuk, M. and McKean, K. A. (1996). Sex differences in parasite infections: patterns and processes. International Journal for Parasitology 26, 1009–1024.Google Scholar