Hostname: page-component-76fb5796d-25wd4 Total loading time: 0 Render date: 2024-04-26T10:26:04.171Z Has data issue: false hasContentIssue false
  • English
  • Français

An attempt to use ectoparasites as tags for habitat occupancy by small mammalian hosts in central Europe: effects of host gender, parasite taxon and season

Published online by Cambridge University Press:  15 February 2011

BORIS R. KRASNOV ,
MICHAL STANKO  and
SERGE MORAND
BORIS 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
MICHAL STANKO
Affiliation:
Institute of Zoology and Parasitological Institute, Slovak Academy of Sciences, Lofflerova 10, SK-04001 Kosice, Slovakia
SERGE MORAND
Affiliation:
Institut des Sciences de l'Evolution, CNRS-UM2, CC65, Université de Montpellier 2, 34095 Montpellier, France
*
*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 6588764. Fax: +972-8-6586369. E-mail: krasnov@bgu.ac.il
Get access Rights & Permissions [Opens in a new window]

Summary

Objective. We used data on fleas and gamasid mites parasitic on 8 species of small mammals to test whether (a) species composition of ectoparasite infracommunities may be used to predict host habitat occupancy and (b) the accuracy of this prediction differs between ectoparasite taxa, host genders and seasons. Methods. We used a Random Forests algorithm that is based on the methodology of classification trees. Results. The accuracy of prediction of habitat occupancy was relatively low and varied substantially among host species. The combined rate of the correct prediction of host habitat occupancy from data on ectoparasites was significantly higher than 50%, albeit being relatively low. The accuracy of prediction (a) did not differ between male and female hosts when it was based on species composition of fleas in summer or of mites in summer and winter, (b) was significantly higher in male hosts than in female hosts when the winter data on fleas were used and (c) was significantly higher for flea than mite assemblages. The effect of season was found in mites but not in fleas with the accuracy of prediction being significantly higher in summer than in winter assemblages. Conclusions. Ectoparasites appeared to be not especially useful as biological markers for distinguishing host populations in different habitats in temperate zones.

Keywords

gamasid mitesfleashabitat occupancyparasite tagsRandom Forests
Type
Research Article
Information
Parasitology , Volume 138 , Issue 5 , April 2011 , pp. 609 - 618
Copyright
Copyright © Cambridge University Press 2011

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

Arthur, J. R. and Albert, E. (1993). Use of parasites for separating stocks of Greenland halibut (Reinhardtius hippoglossoides) in the Canadian northwest Atlantic. Canadian Journal of Fisheries and Aquatic Sciences 50, 2175–2181.CrossRefGoogle Scholar
Attuquayefio, D. K., Gorman, M. L. and Wolton, R. J. (1986). Home range sizes in the wood mouse Apodemus sylvaticus: habitat, sex and seasonal differences. Journal of Zoology (London) 210, 45–53.CrossRefGoogle Scholar
Balbuena, J. A., Aznar, F. J., Fernández, M. and Raga, J. A. (1995). Parasites as indicators of social structure and stock identity of marine mammals. Developments in Marine Biology 4, 133–139.CrossRefGoogle Scholar
Beverley-Burton, M. (1978). Population genetics of Anisakis simplex (Nematoda: Ascaridoidea) in Atlantic salmon (Salmo salar) and their use as biological indicators of host stocks. Environmental Biology of Fishes 3, 369–378.CrossRefGoogle Scholar
Brinck-Lindroth, G. (1968). Host spectra and distribution of fleas of small mammals in Swedish Lapland. Opuscula Entomologica 33, 327–358.Google Scholar
Breiman, L. (2001). Random Forests. Machine Learning 45, 5–32.CrossRefGoogle Scholar
Breiman, L., Friedman, J. H., Olshen, R. A. and Stone, C. J. (1984). Classification and Regression Trees. Wadsworth, Belmont, CA, USA.Google Scholar
Bureau, A., Dupuis, J., Falls, K., Lunetta, K. L., Hayward, B., Keith, T. P. and Van Eerdewegh, P. (2005). Identifying SNPs predictive of phenotype using random forests. Genetic Epidemiology 28, 171–182.CrossRefGoogle ScholarPubMed
Crawley, M. C. (1969). Movements and home-ranges of Clethrionomys glareolus Schreber and Apodemus sylvaticus L. in north-east England. Oikos 20, 310–319.CrossRefGoogle Scholar
Cutler, A., and Stevens, J. R. (2006). Random forests for microarrays. Methods in Enzymology 411, 422–432.CrossRefGoogle ScholarPubMed
Cutler, D. R., Edwards, T. C., Beard, K. H., Cutler, A., Hess, K. T., Gibson, J. and Lawler, J. J. (2007). Random forests for classification in ecology. Ecology 88, 2783–2792.CrossRefGoogle ScholarPubMed
Davenport, J. (1992). Animal Life at Low Temperature. Chapman & Hall, London, UK.CrossRefGoogle Scholar
Dowling, A. P. G. (2006). Mesostigmatid mites as parasites of small mammals: systematics, ecology, and the evolution of parasitic associations. In Micromammals and Macroparasites: From Evolutionary Ecology to Management (ed. Morand, S., Krasnov, B. R. and Poulin, R.), pp. 103–117. SpringerVerlag, Tokyo, Japan.CrossRefGoogle Scholar
Durieux, E. D. H., Bégout, M.-L., Pinet, P. and Sasal, P. (2010). Digenean metacercariae parasites as natural tags of habitat use by 0-group common sole Solea solea in nearshore coastal areas: a case study in the embayed system of the Pertuis Charentais (Bay of Biscay, France). Journal of Sea Research 64, 107–117.CrossRefGoogle Scholar
Elith, J. and Burgman, M. (2002). Predictions and their validation: rare plants in the Central Highlands, Victoria, Australia. In Predicting Species Occurrences. Issues of Accuracy and Scale (ed. Scott, J. M., Heglund, P. J., Morrison, M. L., Haufler, J. B., Raphael, M. G., Wall, W. A. and Samson, F. B.), pp. 303–313. Island Press, Washington, USA.Google Scholar
Fielding, A. H. and Bell, J. F. (1997). A review of methods for the assessment of prediction errors in conservation presence/absence models. Environmental Conservation 24, 38–49.CrossRefGoogle Scholar
Fleming, P. A. and Nicolson, S. W. (2004). Sex differences in space use, body condition and survivorship during the breeding season in the Namaqua rock mouse, Aethomys namaquensis. African Zoology 39, 123–132.Google Scholar
Fuller, W. A. (1967). Winter ecology of lemmings and fluctuations of their populations. Terre et la Vie 2, 97–115.Google Scholar
Furlanello, C., Neteler, M., Merler, S., Menegon, S., Fontanari, S., Donini, A., Rizzoli, A. and Chemini, C. (2003). GIS and the Random Forests predictor: integration in R for tick-borne disease risk assessment. In Proceedings of the 3rd International Workshop on Distributed Statistical Computing (DSC 2003), March 20–22, Vienna, Austria (ed. Hornik, K., Leisch, F. and Zeileis, A), pp. 1–11. Vienna University of Technology, Vienna, Austria.Google Scholar
Girardello, M., Griggio, M., Whittingham, M. J. and Rushton, S. P. (2010). Models of climate associations and distributions of amphibians in Italy. Ecological Research 25, 103–111.CrossRefGoogle Scholar
Gromov, V. S., Krasnov, B. R. and Shenbrot, G. I. (2000). Space use in Wagner's gerbil Gerbillus dasyurus (Wagner, 1842) in the Negev Highlands, Israel. Acta Theriologica 45, 175–182.CrossRefGoogle Scholar
Haapakoski, M. and Ylönen, H. (2010). Effects of fragmented breeding habitat and resource distribution on behavior and survival of the bank vole (Myodes glareolus). Population Ecology 52, 427–435.CrossRefGoogle Scholar
He, Y. F., Wang, J. W., Lek-Ang, S. and Lek, S. (2010). Predicting assemblages and species richness of endemic fish in the upper Yangtze River. Science of the Total Environment 408, 4211–4220.CrossRefGoogle ScholarPubMed
Holmstad, P. R., Holstad, O., Karbol, G., Revhaug, J. O., Schei, E., Vandvik, V. and Skorping, A. (2004). Parasite tags in ecological studies of terrestrial hosts: a study on ptarmigan (Lagopus spp.) dispersal. Ornis Fennica 81, 128–136.Google Scholar
Horváth, G. and Trócsányi, B. (1998). Home range size of Apodemus agrarius and small mammal population dynamics in the rodent assemblage of a Querco robori-carpinetum forest habitat. Tiscia 31, 63–69.Google Scholar
Jung, C. and Croft, B. A. (2001). Aerial dispersal of phytoseiid mites (Acari: Phytoseiidae): estimating falling speed and dispersal distance of adult females. Oikos 94, 182–190.CrossRefGoogle Scholar
Kennedy, C. R. and Bush, A. O. (1994). The relationship between pattern and scale in parasite communities: a stranger in a strange land. Parasitology 109, 187–196.CrossRefGoogle Scholar
Korn, H. (1986). Changes in home range size during growth and maturation of the wood mouse (Apodemus sylvaticus) and the bank vole (Clethrionomys glareolus). Oecologia 68, 623–628.CrossRefGoogle ScholarPubMed
Krasnov, B. R. (2008). Functional and Evolutionary Ecology of Fleas: A Model for Ecological Parasitology. Cambridge University Press, Cambridge, UK.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
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, 159–173.CrossRefGoogle ScholarPubMed
Krasnov, B. R., Shenbrot, G. I., Medvedev, S. G., Khokhlova, I. S. and Vatschenok, V. S. (1998). Habitat-dependence of a parasite-host relationship: flea assemblages in two gerbil species of the Negev Desert. Journal of Medical Entomology 35, 303–313.CrossRefGoogle ScholarPubMed
Krasnov, B. R., Khokhlova, I. S., Fielden, L. J. and Burdelova, N. V. (2001 a). The effect of air temperature and humidity on the survival of pre-imaginal stages of two flea species (Siphonaptera: Pulicidae). Journal of Medical Entomology 38, 629–637.CrossRefGoogle ScholarPubMed
Krasnov, B. R., Khokhlova, I. S., Fielden, L. J. and Burdelova, N. V. (2001 b). Development rates of two Xenopsylla flea species in relation to air temperature and humidity. Medical and Veterinary Entomology 15, 249–258.CrossRefGoogle ScholarPubMed
Krasnov, B. R., Khokhlova, I. S., Fielden, L. J. and Burdelova, N. V. (2002 a). Time to survival under starvation in two flea species (Siphonaptera: Pulicidae) at different air temperatures and relative humidities. Journal of Vector Ecology 27, 70–81.Google ScholarPubMed
Krasnov, B. R., Khokhlova, I. S., Fielden, L. J. and Burdelova, N. V. (2002 b). The effect of substrate on survival and development of two species of desert fleas (Siphonaptera: Pulicidae). Parasite 9, 135–142.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Krasnov, B. R., Burdelova, N. V., Khokhlova, I. S., Shenbrot, G. I. and Degen, A. A. (2005 b). Pre-imaginal interspecific competition in two flea species parasitic on the same rodent host. Ecological Entomology 30, 146–155.CrossRefGoogle Scholar
Krasnov, B. R., Stanko, M., Miklisova, D. and Morand, S. (2006). Habitat variation in species composition of flea assemblages on small mammals in central Europe. Ecological Research 21, 460–469.CrossRefGoogle Scholar
Krasnov, B. R., Stanko, M., Khokhlova, I. S., Shenbrot, G. I., Morand, S., Korallo-Vinarskaya, N. P. and Vinarski, M. V. (2011). Nestedness and beta-diversity in ectoparasite assemblages of small mammalian hosts: effects of parasite affinity, host biology and scale. Oikos (in the Press). doi: 10.1111/j.1600-0706.2010.19072.xCrossRefGoogle Scholar
Lang, J. D. (1996). Factors affecting the seasonal abundance of ground squirrel and wood rat fleas (Siphonaptera) in San Diego County, California. Journal of Medical Entomology 33, 790–804.CrossRefGoogle ScholarPubMed
Lehane, M. (2005). The Biology of Blood-Sucking in Insects, 2nd Edn. Cambridge University Press, Cambridge, UK.CrossRefGoogle Scholar
Liaw, A. and Wiener, M. (2002). Classification and regression by randomForest. R News 2, 18–22.Google Scholar
MacKenzie, K. (2005). Parasites as biological tags. In Marine Parasitology (ed. Rhode, K.), pp. 351–355. CABI Publishing, Oxon, UK.Google Scholar
MacKenzie, K. and Abaunza, P. (1998). Parasites as biological tags for stock discrimination of marine fish: a guide to procedures and methods. Fisheries Research 38, 45–56.CrossRefGoogle Scholar
Madison, D. (1980). Space use and social structure in meadow voles, Microtus pennsylvanicus. Behavioral Ecology and Sociobiology 7, 65–71.CrossRefGoogle Scholar
Marshall, A. G. (1981). The Ecology of Ectoparasitic Insects. Academic Press, London, UK.Google Scholar
Mašán, P. and Fenda, P. (2010). A Review of the Laelapid Mites Associated with Terrestrial Mammals in Slovakia, with a Key to the European Species (Acari: Mesostigmata: Dermanyssoidea). Institute of Zoology, Slovak Academy of Sciences, Bratislava, Slovakia.Google Scholar
Mašán, P. and Halliday, B. (2010). Review of the European genera of Eviphididae (Acari: Mesostigmata) and the species occurring in Slovakia. Zootaxa 2585, 1–122.CrossRefGoogle Scholar
Matthee, S., McGeoch, M. A. and Krasnov, B. R. (2010). Gender-biased ectoparasite infections: species-specific variation and the extent of male-biased parasitism. Parasitology 137, 651–660.CrossRefGoogle Scholar
Mazur, E. and Jakal, J. (1982). Atlas Slovenskej Socialistickej Republiky. Slovenska Academia Vied, Bratislava (in Slovak).Google Scholar
Mazzone, P. J., Hammel, J., Dweik, R., Na, J., Czich, C., Laskowski, D. and Mekhail, T. (2007). Diagnosis of lung cancer by the analysis of exhaled breath with a colorimetric sensor array. Thorax 62, 565–568.CrossRefGoogle ScholarPubMed
Morand, S., Gouy de Bellocq, J., Stanko, M. and Miklisova, D. (2004). Is sex-biased ectoparasitism related to sexual size dimorphism in small mammals of Central Europe? Parasitology 129, 505–510.CrossRefGoogle ScholarPubMed
Murphy, P. W. and Sardar, M. A. (1991). Resource allocation and utilization contrasts in Hypoaspis aculeifer (Can.) and Alliphis halleri (G. & R. Can.) (Mesostigmata) with emphasis on food source. In The Acari. Reproduction, Development and Life-History Strategies (ed. By Schuster, R. and Murphy, P. W.), pp. 301–311. Chapman & Hall, London, UK.Google Scholar
Perdiguero-Alonso, D., Montero, F. E., Kostadinova, A., Raga, J. A. and Barrett, J. (2008). Random forests, a novel approach for discrimination of fish populations using parasites as biological tags. International Journal for Parasitology 38, 1425–1434.CrossRefGoogle ScholarPubMed
Pérez-del-Olmo, A., Montero, F. E., Fernández, M., Barrett, J., Raga, J. A. and Kostadinova, A. (2010). Discrimination of fish populations using parasites: Random Forests on a “predictable” host-parasite system. Parasitology 137, 1833–1847.CrossRefGoogle ScholarPubMed
Prasad, A. M., Iverson, L. R. and Liaw, A. (2006). Newer classification and regression tree techniques: bagging and Random Forests for ecological prediction. Ecosystems 9, 181–199.CrossRefGoogle Scholar
R Development Core Team. (2009). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org.Google Scholar
Radovsky, F. J. (1985). Evolution of mammalian mesostigmatid mites. In Coevolution of Parasitic Arthropods and Mammals (ed. Kim, K. C.), pp. 441–504. John Wiley, New York, USA.Google Scholar
Rose, R. K. and Dueser, R. D. (1980). Lifespan of Virginia meadow voles. Journal of Mammalogy 61, 760–763.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, 467–486.CrossRefGoogle Scholar
Siroky, D. (2009). Navigating Random Forests and related advances in algorithmic modeling. Statistics Surveys 3, 147–163.CrossRefGoogle Scholar
Stanko, M. (1987). Fleas (Siphonaptera) of small mammals from Javorie mountains. Acta Rerum Naturalium Musei Nationalis Slovaci 33, 95–108 (in Slovakian).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., Miklisova, D., Gouy De Bellocq, J. and Morand, S. (2002). Mammal density and patterns of ectoparasite species richness and abundance. Oecologia 131, 289–295.CrossRefGoogle ScholarPubMed
Stradiotto, A., Cagnacci, F., Delahay, R., Tioli, S., Nieder, L. and Rizzoli, A. (2009). Spatial organization of the yellow-necked mouse: effects of density and resource availability. Journal of Mammalogy 90, 704–714.CrossRefGoogle Scholar
Swets, J. A. (1988). Measuring the accuracy of diagnostic systems. Science 240, 1285–1293.CrossRefGoogle ScholarPubMed
Tagiltsev, A. A. (1957). On the relationships between parasitic and nidicolous Acari. Medical Parasitology and Parasitic Diseases [Meditsinskaya parazitologiya and parazitarnyye bolezni] 26, 440–447 (in Russian).Google Scholar
Tagiltsev, A. A. (1967). Ecology of gamasoid mites in the nests of the forest dormouse (Dryomys nitedula Pall.). Parazitologiya 1, 507–511 (in Russian).Google Scholar
Tew, T. E. and Macdonald, D. W. (1994). Dynamics of space use and male vigour amongst wood mice, Apodemus sylvaticus, in the cereal ecosystem. Behavioral Ecology and Sociobiology 34, 337–345.CrossRefGoogle Scholar
Thomassen, H. A., Cheviron, Z. A., Freedman, A. H., Harrigan, R. J., Wayne, R. K. and Smith, T. B. (2010). Spatial modelling and landscape-level approaches for visualizing intra-specific variation. Molecular Ecology 19, 3532–3548.CrossRefGoogle ScholarPubMed
Timi, J. (2007). Parasites as biological tags for stock discrimination in marine fish from South American Atlantic waters. Journal of Helminthology 81, 107–111.CrossRefGoogle ScholarPubMed
Ylönen, H. and Mappes, T. (1995). Spacing behavior and key resources: an experiment on seasonal preference of male bank voles, Clethrionomys glareolus, for food and females. Annales Zoologici Fennici 32, 445–448.Google Scholar
Ylönen, H., Altner, H.-J. and Stubbe, M. (1991). Seasonal dynamics of small mammals in an isolated woodlot and its agricultural surroundings. Annales Zoologici Fennici 28, 7–14.Google Scholar
Williams, G. J. (2009). Rattle: a data mining GUI for R. The R Journal 1, 45–55.CrossRefGoogle Scholar
Williams, H. H., MacKenzie, K. and McCarthy, A. M. (1992). Parasites as biological indicators of the population biology, migrations, diet, and phylogenetics of fish. Reviews of Fish Biology and Fisheries 2, 144–176.CrossRefGoogle Scholar
Zemskaya, A. A. (1973). Parasitic Gamasid Mites and their Medical Importance Meditsina, Moscow, USSR (in Russian).Google Scholar