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Remnant fragments within an agricultural matrix enhance conditions for a rodent host and its fleas

Published online by Cambridge University Press:  29 October 2012

LUTHER VAN DER MESCHT ,
PETER C. LE ROUX  and
SONJA MATTHEE
LUTHER VAN DER MESCHT
Affiliation:
Department of Conservation Ecology and Entomology, Stellenbosch University, Private Bag X1, Matieland, 7602, South Africa
PETER C. LE ROUX
Affiliation:
Department of Geosciences and Geography, University of Helsinki, FI-00014 Helsinki, Finland
SONJA MATTHEE*
Affiliation:
Department of Conservation Ecology and Entomology, Stellenbosch University, Private Bag X1, Matieland, 7602, South Africa
*
*Corresponding author: Department of Conservation Ecology and Entomology, Stellenbosch University, Private Bag X1, Matieland, 7602, South Africa. Tel: +27 21 808 4777. Fax: +27 21 808 4802. E-mail: smatthee@sun.ac.za
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Summary

Habitat fragmentation can adversely impact biodiversity, although where remnant fragments of natural vegetation provide favourable conditions the negative effects of fragmentation may be mitigated. Host-parasite systems in fragmented areas have only recently been examined, with parasites generally showing higher prevalence and richness in fragments, mediated by changes in host density. However, the effect of fragmentation on parasite body size and fecundity remains poorly investigated. Thus, here we compared the body size and condition of a generalist rodent host, Rhabdomys pumilio and the body size of 2 common flea species between pristine natural areas and remnant fragments within agriculture areas. Host body length, weight and body condition values were significantly larger in fragments than in pristine natural vegetation. Listropsylla agrippinae fleas showed the same pattern, being significantly larger in fragments, while Chiastopsylla rossi fleas did not differ in size between fragments and natural areas. The differential response of the 2 flea species may reflect the strength of association between the host and parasite, with the former spending a greater proportion of its lifespan on the host. Therefore, in this study agriculture fragments provide better conditions for both an opportunistic rodent and a closely associated flea species.

Keywords

body sizefleahabitat fragmentationrodents
Type
Research Article
Information
Parasitology , Volume 140 , Issue 3 , March 2013 , pp. 368 - 377
Copyright
Copyright © Cambridge University Press 2012

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References

REFERENCES

Adler, G. H. and Levins, R. (1994). The island syndrome in rodent populations. Quarterly Review of Biology 69, 473–490.CrossRefGoogle ScholarPubMed
Allan, B. F., Keesing, F. and Ostfeld, S. (2003). Effect of forest fragmentation on Lyme disease risk. Conservation Biology 17, 267–272.CrossRefGoogle Scholar
Anderson, R. M. and May, R. M. (1978). Regulation and stability of host-parasite population interactions. 1. Regulatory processes. Journal of Animal Ecology 47, 219–247.CrossRefGoogle Scholar
Arneberg, P. (2002). Host population density and body mass as determinants of species richness in parasite communities: comparative analyses of directly transmitted nematodes of mammals. Ecography 25, 88–94.CrossRefGoogle Scholar
Arneberg, P., Skorping, A., and Read, A. F. (1998). Parasite abundance, body size, life histories, and the energetic equivalence rule. American Naturalist 151, 497–513.CrossRefGoogle ScholarPubMed
Bivand, R. (2011). Spdep: Spatial Dependence: Weighting Schemes, Statistics and Models. R Package Version 0.5–31. Available at http://CRAN.R-project.org/package=spdep.Google Scholar
Bolger, D. T., Alberts, A. C., Sauvajot, R. M., Potenza, P., McCalvin, C., Tran, D., Mazzoni, S. and Soulé, M. E. (1997). Response of rodents to habitat fragmentation in coastal southern California. Ecological Applications 7, 552–563.CrossRefGoogle Scholar
Chapin, F. S., Zavaleta, E. S., Eviner, V. T., Naylor, R. L., Vitousek, P. M., Reynolds, H. L., Hooper, D. U., Lavorel, S., Sala, O. E., Hobbie, S. E., Mack, M. C. and Diaz, S. (2000). Consequences of changing biodiversity. Nature, London 405, 234–242.CrossRefGoogle ScholarPubMed
Chapman, C. A., Wasserman, M. D., Gillespie, T. R., Speirs, M. L., Lawes, M. J., Saj, T. L. and Ziegler, T. E. (2006). Do food availability, parasitism, and stress have synergistic effects on red colobus populations living in forest fragments? American Journal of Physiological Anthropology 131, 525–534.CrossRefGoogle ScholarPubMed
Cottontail, V. M., Wellinghausen, N. and Kalko, E. K. V. (2009). Habitat fragmentation and haemoparasites in the common fruit bat, Artibeus jamaicensis (Phyllostomidae) in a tropical lowland forest in Panamá. Parasitology 136, 1133–1145.CrossRefGoogle Scholar
Cowling, R. M. and Hilton-Taylor, C. (1994). Patterns of plant diversity and endemism in southern Africa: a overview. In Botanical Diversity in Southern Africa (ed. Huntley, B. J.), pp. 31–52. National Botanical Institute, Pretoria, South Africa.Google Scholar
de la Penã, N. M., Butet, A., Delettre, Y., Paillat, G., Morant, P., Le Du, L. and Burel, F. (2003). Response of small mammal community to changes in western French agricultural landscapes. Landscape Ecology 18, 265–278.CrossRefGoogle Scholar
De Meillon, B., Davis, D. and Hardy, F. (1961). Plaque in Southern Africa, Vol.1. The Siphonaptera (excluding Ischnopsyllidae). Government Printer, Pretoria. South Africa.Google Scholar
Díaz, M. and Alonso, C. L. (2003). Wood mouse Apodemus sylvaticus winter food supply: density, condition, breeding and parasites. Ecology 84, 2680–2691.CrossRefGoogle Scholar
Fietz, J. and Weis-Dootz, T. (2012). Stranded on an island: consequences of forest fragmentation for body size variations in an arboreal mammal, the edible dormouse (Glis glis). Population Ecology 54, 313–320. doi 10.1007/s10144-012-0310-0.CrossRefGoogle Scholar
Friggens, M. M. and Beier, P. (2010). Anthropogenic disturbance and the risk of flea-borne disease transmission. Oecologia 164, 809–820.CrossRefGoogle ScholarPubMed
Froeschke, G. and Sommer, S. (2005). MHC Class II DRB variability and parasite load in the Striped Mouse (Rhabdomys pumilio) in the southern Kalahari. Molecular Biology and Evolution 22, 1254–1259.CrossRefGoogle ScholarPubMed
Froeschke, G., Sommer, S. and Matthee, S. (2010). Effects of precipitation on parasite burden along a natural climatic gradient in southern Africa – implications for possible shifts in infestation patterns due to global changes. Oikos 119, 1029–1039.CrossRefGoogle Scholar
Goldblatt, P. and Manning, J. (2000). Cape Plants: a Conspectus of the Cape Flora of South Africa. Strelitzia 9. National Botanical Institute and Missouri Botanical Garden, Cape Town, South Africa.Google Scholar
Goüy de Bellocq, J., Morand, S. and Feliu, C. (2002). Patterns of parasite species richness of western palearctic micro-mammals: island effects. Ecography 25, 173–183.CrossRefGoogle Scholar
Harvey, P. H. and Keymer, A. E. (1991). Comparing life histories using phylogenies. Transactions of the Royal Society of London, B 332, 31–39.Google Scholar
Haukisalmi, V., Heino, M. and Kaitila, V. (1998). Body size variation in tapeworms (Cestoda): adaptation to intestinal gradients? Oikos 83, 152–160.CrossRefGoogle Scholar
Haukisalmi, V. and Henttonen, H. (1994). Distribution patterns and microhabitat segregation in gastrointestinal helminths of Sorex shrews. Oecologia 97, 236–242.CrossRefGoogle ScholarPubMed
Haukisalmi, V., Henttonen, H. and Batzli, G. O. (1995). Helminth parasitism in the voles Microtus oeconomus and M. miurus on the North Slope of Alaska: host specificity and the effects of host sex, age and breeding status. Annales Zoologici Fennici 32, 193–201.Google Scholar
Hawlena, H., Abramsky, Z. and Krasnov, B. R. (2005). Age-biased parasitism and density-depedent distribution of fleas (Siphonaptera) on a desert rodent. Oecologia 146, 200–208.CrossRefGoogle ScholarPubMed
Hawlena, H., Khokhlova, I. S., Abramsky, Z. and Krasnov, B. R. (2006). Age, intensity of infestation by flea parasites and body mass loss in a rodent host. Parasitology 133, 187–193.CrossRefGoogle Scholar
Hughes, V. L. and Randolph, S. E. (2001). Testosterone depresses innate and acquired resistance to ticks in natural rodent hosts: a force for aggregated distribution of parasites. Journal of Parasitology 87, 49–54.CrossRefGoogle ScholarPubMed
Hulbert, S. H. (1984). Pseudoreplication and the design of ecological field experiments. Ecological Monographs 54, 187–211.CrossRefGoogle Scholar
Johnson, P. T. J. and Thieltges, D. W. (2010). Diversity, decoys and the dilution effect: how ecological communities affect disease risk. Journal of Experimental Biology 213, 961–970.CrossRefGoogle ScholarPubMed
Khokhlova, I. S., Serobyan, V., Degen, A. A. and Krasnov, B. R. (2010). Host gender and offspring quality in a flea parasitic on a rodent. Journal of Experimental Biology 213, 3299–3304.CrossRefGoogle Scholar
Khokhlova, I. S., Serobyan, V., Krasnov, B. R. and Degen, A. A. (2009). Is the feeding and reproductive performance of the flea, Xenopsylla ramesis, affected by the gender of its rodent host, Meriones crassus? Journal of Experimental Biology 212, 1429–1435.CrossRefGoogle ScholarPubMed
Kirk, W. D. J. (1991). The size relationship between insects and their hosts. Ecological Entomology 16, 351–359.CrossRefGoogle Scholar
Klein, S. L. (2000). The effects of hormone on sex differences in infection: from genes to behaviour. Neuroscience and Biobehavioral Review 24, 627–638.CrossRefGoogle Scholar
Krasnov, B. R. (2008). Functional and Evolutionary Ecology of Fleas. Cambridge University Press, New York, USA.CrossRefGoogle Scholar
Krasnov, B. R., Khokhlova, I. S., Arakelyan, M. S. and Degen, A. A. (2005). Is a starving host tastier? Reproduction in fleas parasitizing food-limited rodents. Functional Ecology 19, 625–631.CrossRefGoogle Scholar
Krasnov, B. R., Khoklova, I. S., Fielden, L. J. and Burdelova, N. V. (2001 a). 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., Khoklova, 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. and Matthee, S. (2010). Spatial variation in gender-biased parasitism: host-related, parasite-related and environment-related effects. Parasitology 137, 1527–1536.CrossRefGoogle ScholarPubMed
Krasnov, B. R., Sarfati, M., Arakelyan, M. S., Khokhlova, I. S., Burdelova, N. V., Degen, A. A. (2003). Host specificity and foraging efficiency in blood-sucking parasite: feeding patterns of the flea Parapulex chephrenis on two species of rodents. Parasitological Research 90, 393–399.CrossRefGoogle ScholarPubMed
Krasnov, B., Shenbrot, G., Khoklova, I., Medvedev, S. and Vatschenok, V. (1998). Habitat dependence of a parasite-host relationship: flea (Siphonaptera) assemblages in two gerbil species of the Negev desert. Journal of Medical Entomology 35, 303–313.CrossRefGoogle ScholarPubMed
Krasnov, B. R., Shenbrot, G. I., Medvedev, S. G., Vatschenok, V. S. and Khoklova, 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, 159–173.CrossRefGoogle ScholarPubMed
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
Laakkonen, J., Fisher, R. N. and Case, T. J. (2001). Effect of land cover, habitat fragmentation and ant colonies on the distribution and abundance of shrews in southern California. Ecology 70, 776–788.Google Scholar
Laurance, W. F. (2008). Theory meets reality: How habitat fragmentation research has transcended island biogeographic theory. Biological Conservation 141, 1731–1744.CrossRefGoogle Scholar
Lomolino, M. V. (1985). Body size of mammals on islands: The island rule reexamined. The American Naturalist 125, 310–316.CrossRefGoogle Scholar
Lomolino, M. V., Perault, D. R. (2007). Body size variation of mammals in a fragmented, temperate rainforest. Conservation Biology 21, 1059–1069.CrossRefGoogle Scholar
Manor, R. and Saltz, D. (2008). Conservation implications of competition between generalist and specialist rodents in Mediterranean afforested landscape. Biodiversity Conservation 17, 2513–2523.CrossRefGoogle Scholar
Martínez-Mota, R., Valdespino, C., Sanchez-Ramos, M. A. and Serio-Silva, J. C. (2007). Effects of forest fragmentation on the physiological stress response of black howler monkeys. Animal Conservation 10, 374–379.CrossRefGoogle Scholar
Matthee, S., Horak, I. G., Beaucournu, J-C., Durden, L. A., Ueckermann, E. A. and McGeoch, M. A. (2007). Epifaunistic arthropod parasites of the four-striped mouse, Rhabdomys pumilio, in the Western Cape Province, South Africa. Journal of Parasitology 93, 47–59.CrossRefGoogle ScholarPubMed
Matthee, S., McGeoch, M. A. and Krasnov, B. R. (2010 a). Parasite-specific variation and the extent of male-biased parasitism; an example with a South African rodent and ectoparasitic arthropods. Parasitology 137, 651–660.CrossRefGoogle ScholarPubMed
Matthee, S., Horak, I. G., van der Mescht, L., Ueckermann, E. A. and Radloff, F. G. T. (2010 b). Ectoparasite diversity on rodents at De Hoop Nature Reserve, Western Cape Province. African Zoology 45, 213–224.CrossRefGoogle Scholar
Mbora, D. N. M. and McPeek, M. A. (2009). Host density and human activities mediate increased parasite prevalence and richness in primates threatened by habitat loss and fragmentation. Journal of Animal Ecology 78, 210–218.CrossRefGoogle ScholarPubMed
Midgley, G. F., Hannah, L., Millar, D., Thuiller, W. and Booth, A. (2003). Developing regional and species-level assessments of climate change impacts on biodiversity in the Cape Floristic Region. Biological Conservation 112, 87–97.CrossRefGoogle Scholar
Moore, S. L. and Wilson, K. (2002). Parasites as viability cost of sexual selection in natural populations of mammals. Science 297, 2015–2018.CrossRefGoogle ScholarPubMed
Morand, S. (1996). Life-history traits in parasitic nematodes: a comparative approach for the search of invariants. Functional Ecology 10, 210–218.CrossRefGoogle Scholar
Morand, S., Bouamer, S. and Hugot, J-P. (2006). Nematodes. In Micromammals and Macroparasites: From Evolutionary Ecology to Management (ed. Morad, S., Krasnov, B. R., Poulin, R.), pp. 63–79. Springer, Tokyo, Japan.CrossRefGoogle Scholar
Morand, S. and Poulin, R. (2002). Body size-density and species diversity in parasitic nematodes: patterns and likely processes. Evolutionary Ecology Research 4, 951–961.Google Scholar
Mortelliti, A., Amori, G., Capizzi, D., Cervone, C. and Fagiani, S. (2011). Independent effects of habitat loss, habitat fragmentation and structural connectivity on the distribution of two arboreal rodents. Journal of Applied Ecology 48, 153–162.CrossRefGoogle Scholar
Mucina, L. and Rutherford, M. C. (2006). The Vegetation of South Africa, Lesotho and Swaziland. National Botanical Institute. Strelitzia 19, Pretoria, South Africa.Google Scholar
Mugabe, J. C. (2008). Small mammal communities in the transformed landscape of the Western Cape lowlands and their role in alien invasion into fynbos remnants. M.Sc. thesis. Stellenbosch University, South Africa.Google Scholar
Nieberding, C., Morand, S., Libois, R. and Michaux, J. R. (2006). Parasites and the island syndrome: the colonization of the western Mediterranean islands by Helgmosomoides polygyrus (Dujardin, 1845). Journal of Biogeography 33, 1212–1222.CrossRefGoogle Scholar
Nupp, T. E. and Swihart, R. K. (1998). Effect of forest patch area on population attributes of white-footed mice (Peromyscus leucopus) in fragmented landscapes. Canadian Journal of Zoology 74, 467–472.CrossRefGoogle Scholar
Peters, R. H. (1983). The Ecological Implications of Body Size. Cambridge University Press, Cambridge, UK.CrossRefGoogle Scholar
Poulin, R. (1996). The evolution of life history strategies in parasitic animals. Advances in Parasitology 37, 107–133.CrossRefGoogle ScholarPubMed
Poulin, R. (ed.) (2007). Evolutionary Ecology of Parasites, 2nd Edn. Princeton University Press, Princeton, NJ, USA.CrossRefGoogle Scholar
Poulin, R. and Morand, S. (1997). Parasite body size distributions: interpreting patterns of skewness. International Journal of Parasitology 27, 959–964.CrossRefGoogle ScholarPubMed
Pretorius, E. C. (1993). The ecology of small mammals (Rodentia, Insectivora) in the coastal mountain fynbos of the southern Cape. M.Sc. thesis. Stellenbosch University, South Africa.Google Scholar
Püttker, T., Meyer-Lucht, Y. and Sommer, S. (2008). Effects of fragmentation on parasite burden (nematodes) of generalist and specialist small mammal species in secondary forest fragments of the coastal Atlantic Forest, Brazil. Ecological Research 23, 207–215.CrossRefGoogle Scholar
Quinnell, R. J. (1988). Host age and the growth and fecundity of Hymenolepis diminuta in the rat. Journal of Helminthology 62, 158–162.CrossRefGoogle ScholarPubMed
Rands, M. R. W., Adams, W. M., Bennun, L., Butchart, S. H. M., Clements, A., Coomes, D., Entwistle, A., Hodge, I., Kapos, V., Scharlemann, J. P. W., Sutherland, W. J. and Vira, B. (2010). Biodiveristy conservation: challenges beyond 2010. Science 329, 1298–1303.CrossRefGoogle Scholar
Rodríguez, C. and Peris, S. (2007). Habitat associations of small mammals in farmed landscapes: implications for agri-environmental schemes. Animal Biology 57, 301–314.CrossRefGoogle Scholar
Rouget, M., Richardson, D. M., Cowling, R. M., Lloyd, W. and Lombard, A. T. (2003). Current patterns of habitat transformation and future threats to biodiversity in terrestrial ecosystems of the Cape Floristic Region, South Africa. Biological Conservation 112, 63–85.CrossRefGoogle Scholar
Sala, O. E., Chapin, F. S., Armesto, J. J., Berlow, E., Bloomfield, J., Dirzo, R., Huber-Sanwald, E., Huenneke, L. F., Jackson, R. B., Kinzig, A., Leemans, R., Lodge, D. M., Mooney, H. A., Oesterheld, M., Poff, N. I., Sykes, M. T., Walker, B. H., Walker, M. and Wall, D. H. (2000). Global biodiversity scenarios for the year 2100. Science 287, 1770–1774.CrossRefGoogle ScholarPubMed
Saunders, D. A., Hobbs, R. J. and Margules, C. R. (1991). Biological consequences of ecosystem fragmentation: A review. Conservation Biology 5, 18–32.CrossRefGoogle Scholar
Schmidt, N. M. and Jensen, P. M. (2003). Changes in mammalian body length over 175 years adaptations to a fragmented landscape? Conservation Ecology 7, 6. http://www.consecol.org/vol7/iss2/art6CrossRefGoogle Scholar
Schradin, C. and Pillay, N. (2005). Intraspecific variation in the spatial and social organization of the African striped mouse. Journal of Mammalogy 86, 99–107.2.0.CO;2>CrossRefGoogle Scholar
Schulte-Hostedde, A. I., Millar, J. S. and Gibbs, H. L. (2004). Sexual selection and mating patterns in a mammal with female-biased sexual size dimorphism. Behavioural Ecology 15, 351–356.CrossRefGoogle Scholar
Segerman, J. (1995). Siphonaptera of Southern Africa. Handbook for the Identification of Fleas. Publications of The South African Institute for Medical Research No. 57. South African Institute for Medical Research, Johannesburg, South Africa.Google Scholar
Shepherd, A. J., Hummitzsch, D. E., Leman, P. A. and Hartwig, E. K. (1983). Studies on plague in the eastern cape province of South Africa. Transactions of the Royal Society of Tropical Medicine and Hygiene 77, 800–808.CrossRefGoogle Scholar
Shepherd, A. J. and Leman, P. A. (1983). Plaque in South African rodents. Transactions of the Royal Society of Tropical Medicine and Hygiene 77, 208–211.CrossRefGoogle Scholar
Skinner, J. D. and Chimimba, C. T. (2005). The Mammals of the Southern African Subregion. Cambridge University Press, Cape Town, South Africa.CrossRefGoogle Scholar
Skorping, A., Read, A. F. and Keymer, A. E. (1991). Life history covariation in intestinal nematodes of mammals. Oikos 60, 365–372.CrossRefGoogle Scholar
Sorci, G., Morand, S. and Hugot, J-P. (1997). Host-parasite coevolution: comparative evidence for covariation of life history traits in primates and oxyurid parasites. Proceedings of the Royal Society of London, B 264, 285–289.CrossRefGoogle ScholarPubMed
Soulé, M. E. (1991). Conservation: Tactics for a constant crisis. Science 253, 744–750.CrossRefGoogle ScholarPubMed
Stear, M. J., Bairden, K., Duncan, J. L., Holmes, P. H., McKellar, Q. A., Park, M., Strain, S., Murray, M., Bishop, G. and Gettinby, G. (1997). How hosts control worms. Nature, London 389, 27.CrossRefGoogle ScholarPubMed
Terborgh, J., Lopez, L., Nuñez, P., Rao, M., Shahabuddin, G., Orihuela, G., Riveros, M., Ascanio, R., Adler, G. H., Lambert, T. D. and Balbas, L. (2001). Ecological meltdown in predator-free forest fragments. Science 294, 1923–1926.CrossRefGoogle ScholarPubMed
Traub, R. (1985). Coevolution of fleas and mammals. In Coevolution of Parasitic Arthropods and Mammals (ed. Kim, K. C.), pp. 295–437. John Wiley, New York, USA.Google Scholar
Valero, M. A., Panova, M., Comes, A. M., Fons, R. and Mas-Coma, S. (2002). Patterns in size and shedding of Fasciola hepatica eggs by naturally and experimentally infected murid rodents. Journal of Parasitology 88, 308–313.CrossRefGoogle ScholarPubMed
Van Valen, L. (1973). A New Evolutionary Law. Evolutionary Theory 1, 1–30.Google Scholar
Vaz, V. C., D'andrea, P. S. and Jansen, A. M. (2007). Effects of habitat fragmentation on wild mammal infection by Trypanosoma cruzi. Parasitology 134, 1785–1793.CrossRefGoogle ScholarPubMed
Viney, M. (2002). How do host immune responses affect nematode infections? Trends in Parasitology 18, 63–66.CrossRefGoogle ScholarPubMed
Walker, J. B. (1991). A review of the ixodid ticks (Acari, Ixodidae) occurring in southern Africa. Onderstepoort Journal of Veterinary Research 58, 81–105.Google ScholarPubMed
Wasserberg, G., Abramsky, Z., Kotler, B. P., Ostfeld, R. S., Yarom, I. and Warburg, A. (2003). Anthropogenic disturbances enhance occurrence of cutaneous Leishmaniasis in Israel deserts: patterns and mechanisms. Ecological Applications 13, 868–881.CrossRefGoogle Scholar
Wilcox, B. A. and Gubler, D. J. (2005). Disease Ecology and the Global Emergence of Zoonotic Pathogens. Environmental Health and Preventative Medicine 10, 263–272.CrossRefGoogle ScholarPubMed
Wolff, J. O., Schauber, E. M. and Edge, W. D. (1997). Effects of habitat loss and fragmentation on the behaviour and demography of gray-tailed voles. Conservation Biology 11, 945–956.CrossRefGoogle Scholar
Wright, P. C., Arrigo-Nelson, S. J., Hogg, K. L., Bannon, B., Moreli, T. L., Wyatt, J., Harivelo, A. L. and Ratelolahy, F. (2009). Habitat disturbance and seasonal fluctuations of lemur parasites in the rain forest of Ranomafana National Park, Madagascar. In Primate Parasite Ecology – The Dynamics and Study of Host–Parasite Relationships (ed. Huffman, M. A. and Chapman, C. A.), pp. 311–330. Cambridge University Press, Cambridge, UK.Google Scholar
Zhang, Y., Zhang, Z. and Liu, J. (2003). Burrowing rodents as ecosystem engineers: the ecology and management of plateau zokors Myospalax fontanierri in alpine meadow ecosystems on the Tibetan Plateau. Mammalogy Review 33, 284–294.CrossRefGoogle Scholar