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The influence of habitat fragmentation on helminth communities in rodent populations from a Brazilian Mountain Atlantic Forest

Published online by Cambridge University Press:  24 July 2015

T.S. Cardoso ,
R.O. Simões ,
J.L.F. Luque ,
A. Maldonado Jr  and
R. Gentile
T.S. Cardoso
Affiliation:
Laboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, Instituto Oswaldo Cruz, Av. Brasil 4365 Manguinhos, 21040-360, Rio de Janeiro, RJ, Brasil Curso de Pós-Graduação em Biodiversidade e Saúde, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, Rio de Janeiro, RJ, Brasil
R.O. Simões
Affiliation:
Laboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, Instituto Oswaldo Cruz, Av. Brasil 4365 Manguinhos, 21040-360, Rio de Janeiro, RJ, Brasil
J.L.F. Luque
Affiliation:
Departamento de Parasitologia Animal, Universidade Federal Rural do Rio de Janeiro, 23851-970, Seropédica, RJ, Brasil
A. Maldonado Jr
Affiliation:
Laboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, Instituto Oswaldo Cruz, Av. Brasil 4365 Manguinhos, 21040-360, Rio de Janeiro, RJ, Brasil
R. Gentile*
Affiliation:
Laboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, Instituto Oswaldo Cruz, Av. Brasil 4365 Manguinhos, 21040-360, Rio de Janeiro, RJ, Brasil
*
*Fax: +55 21 25621572 E-mail: rgentile@ioc.fiocruz.br
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Abstract

The influence of habitat structure on helminth communities of three sigomdontinae rodent species (Akodon cursor, A. montensis and Oligoryzomys nigripes) was investigated in forest fragments within an agricultural landscape in south-eastern Brazil. This is a pionner study correlating the occurrence of helminth species of rodent hosts with microhabitat characteristics. Rodents were collected from 12 fragments and in a continuous conserved area. Up to 13 nematode, three cestode and two trematode species were identified, and habitat fragmentation was found to have more influence on the helminth composition of O. nigripes compared to the other two rodent species. Fragmentation appeared to limit the development of some helminths’ life cycles, e.g. with some species such as Trichofreitasia lenti, Protospirura numidica, Cysticercus fasciolaris and Avellaria sp., occurring mostly in areas with less anthropic impact. However, fragmentation did not seem to affect the life cycles of other dominant helminths, such as the trematode Canaania obesa, the nematodes Stilestrongylus lanfrediae,S. eta and S. aculeata, and the cestode Rodentolepis akodontis. The helminth community structure followed a nested pattern of distribution in A. montensis and O. nigripes. Stilestrongylus lanfrediae seemed to be more associated with dense understorey, C. obesa with open canopy and dense understorey, and Guerrerostrongylus zetta with organic matter on the ground. Their presence in each area may be explained by aspects of their life cycles that take place in the external environment outside the host.

Type
Research Papers
Information
Journal of Helminthology , Volume 90 , Issue 4 , July 2016 , pp. 460 - 468
Copyright
Copyright © Cambridge University Press 2015 

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References

Almeida-Neto, M., Guimarães, P., Guimarães, P.R. Jr, Loyola, R.D. & Ulrich, W. (2008) A consistent metric for nestedness analysis in ecological systems: reconciling concept and measurement. Oikos 117, 1227–1239.Google Scholar
Antunes, P.C., Campos, M.A.A., Oliveira-Santos, L.G.R. & Graipel, M.E. (2010) Population dynamics of Akodon montensis (Rodentia, Cricetidae) in the Atlantic Forest of Southern Brazil. Mammalian Biology 75, 186–190.Google Scholar
Ayoade, J.O. (1986) Introdução à climatologia para os trópicos. 1st edn. 332 pp. São Paulo, Editora Difel.Google Scholar
Behnke, J.M., Lewis, J.W., Mohd Zain, S.N. & Gilbert, F.S. (1999) Helminth infections in Apodemus sylvaticus in southern England: interactive effects of host-age, sex and year on prevalence and abundance of infections. Journal of Helmintholology 73, 31–44.Google Scholar
Bomfim, T.C.B. do. (2001) Algumas observações sobre infecção natural em Rattus norvegicus por Cysticercus fasciolaris (Eucestoda: Taeniidae). Revista Brasileira de Parasitologia Veterinária 10, 79–82.Google Scholar
Bonecker, S.T., Portugal, L.G., Costa-Neto, S.F. & Gentile, R. (2009) A long term study of small mammals populations in a Brazilian agricultural landscape. Mammalian Biology 74, 467–477.Google Scholar
Bordes, F., Morand, S., Pilosof, S., Claude, J., Krasnov, B.R., Cosson, J.F., Chaval, Y., Ribas, A., Chaisiri, K., Blasdell, K., Herbreteau, V., Dupuy, S. & Tran, A. (2015) Habitat fragmentation alters the properties of a host–parasite network: rodents and their helminths in South-East Asia. Journal of Animal Ecology doi:10.1111/1365-2656.12368.Google Scholar
Brouat, C. & Duplantier, J.M. (2007) Host habitat patchiness and the distance decay of similarity among gastro-intestinal nematode communities in two species of Mastomys (south-eastern Senegal). Oecologia 152, 715–720.CrossRefGoogle Scholar
Brouat, C., Kane, M., Diouf, M., Bâ, K., Sall-Dramé, R. & Duplantier, J.M. (2007) Host ecology and variation in helminth communitiy structure in Mastomys rodents from Senegal. Parasitology 134, 437–450.Google Scholar
Bush, A.O., Lafferty, K.D., Lotz, J.M. & Shostak, A.W. (1997) Parasitology meets ecology in its own terms: Margolis et al. revisited. Journal of Parasitology 86, 575–583.Google Scholar
Cerqueira, R. & Freitas, S.R. (1999) A new study method of microhabitat structure of small mammals. Revista Brasileira de Biologia 59, 219–223.Google Scholar
Crook, J.R. & Grundmann, A.W. (1964) The life history of Protospirura numidica Seurat, 1914 (Nematoda: Spiruroidea). Proceedings of the Helminthological Society of Washington 31, 225–229.Google Scholar
Dallas, T. & Presley, S.J. (2014) Relative importance of host environment, transmission potential and host phylogeny to the structure of parasite metacommunities. Oikos 123, 866–874.CrossRefGoogle Scholar
Epstein, P.R., Dobson, A. & Vandermeer, J. (1997) Biodiversity and infectious emerging diseases: Integrating health and ecosystem monitoring. pp. 60–86 in Rosenthal, F.G.J. (Ed.) Biodiversity and human health. Washington DC, Island Press.Google Scholar
Freitas, S.R., Cerqueira, R. & Vieira, M.V. (2002) A device and standard variables to describe microhabitat structure of small mammals based on plant cover. Brazilian Journal of Biology 62, 795–800.CrossRefGoogle ScholarPubMed
Fried, B. & Graczyk, T.K. (1997) Advances in trematode biology. 1st edn. 480 pp. New York, CRC Press.Google Scholar
Froeschke, G. & Matthee, S. (2014) Landscape characteristics influence helminth infestations in a peri-domestic rodent – implications for possible zoonotic disease. Parasites & Vectors 7, 1–13.Google Scholar
Gardner, S.L. & Campbell, M.L. (1992) Parasites as probes for biodiversity. Journal of Parasitology 78, 596–600.Google Scholar
Gibson, D.I., Jones, A. & Bray, R.A. (2002) Keys to the Trematoda. Vol 1. 1st edn. 521 pp. London, CABI Publishing and the Natural History Museum.Google Scholar
Godinho, V.M. (2003) Estudo sobre a ocorrência de ovos de helmintos e viabilidade de Ascaris sp. em lodos anaeróbios in natura e submetidos à higienização por caleação e por tratamento térmico. MSc dissertation, Universidade Federal de Minas Gerais, Belo Horizonte, Brasil.Google Scholar
Gomes, D.C., Cruz, R.P., Vicente, V. & Pinto, R.M. (2003) Nematode parasites of marsupials and small rodents from the Brazilian Atlantic Forest in state of Rio de Janeiro, Brazil. Revista Brasileira de Zoologia 20, 699–707.Google Scholar
Goüy de Bellocq, J., Sarà, M., Casanova, J.C., Feliu, C. & Morand, S. (2003) A comparison of the structure of helminth communities in the woodmouse, Apodemus sylvaticus, on islands of the western Mediterranean and continental Europe. Parasitology Research 90, 64–70.Google Scholar
Guimarães, P.R. & Guimarães, P. (2006) Improving the analyses of nestedness for large sets of matrices. Environmental modelling and software 21, 1512–1513.Google Scholar
Hammer, O., Harper, D.A.T. & Ryan, P.D. (2001) PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4, 9.Google Scholar
Harrison, S. (1991) Local extinction in a metapopulation context: an empirical evaluation. Biological Journal of the Linnean Society 42, 73–88.Google Scholar
Heck, K., De Marco, É.G., Hahn, A.B.B., Kluge, M., Spilki, F.R. & Van Der Sand, S.T. (2013) Temperatura de degradação de resíduos em processo de compostagem e qualidade microbiológica do composto final. Revista Brasilieira de Engenharia Agrícola e Ambiental 17, 54–59.Google Scholar
Hernandez, A. & Sukhdeo, M.V. (1995) Host grooming and transmission strategy of Heligmosomoides polygyrus . Journal of Parasitology 81, 865–869.CrossRefGoogle ScholarPubMed
Hudson, P.J., Dobson, A.P & Lafferty, K.D. (2006) Is a healthy ecosystem one that is rich in parasite species? TREE 21, 381–385.Google Scholar
Hulbert, I.A.R. & Boag, B. (2001) The potential role of habitat on intestinal helminths of mountain hares, Lepus timidus . Journal of Helminthology 75, 345–349.Google Scholar
INMET (Instituto Nacional de Meteorologia). (2005) Previsão do Tempo: Municípios. Available at http://www.inmet.gov.br/html/prev_tempo.php (accessed accessed 4 April 2005).Google Scholar
Jones, A., Bray, R.A. & Gibson, D.I. (2005) Keys to the Trematoda. Vol. 2. 1st edn. 768 pp. London, CABI Publishing and the Natural History Museum.Google Scholar
Khalil, L.F., Jones, A. & Bray, R.A. (1994) Keys to the cestode parasites of vertebrates. 1st edn. 768 pp. London, CABI Publishing and the Natural History Museum.Google Scholar
Kuhnen, V.V., Graipel, M.E. & Pinto, C.J.C. (2012) Differences in richness and composition of gastrointestinal parasites of small rodents (Cricetidae, Rodentia) in a continental and insular area of the Atlantic Forest in Santa Catarina state, Brazil. Brazilian Journal of Biology 72, 563–567.Google Scholar
Lafferty, K. & Kuris, A. (1999) How environmental stress affects the impacts of parasites. Limnology & Oceanography 44, 925–931.CrossRefGoogle Scholar
Laurance, W.F. & Bierregaard, R.O. (1997) Tropical forest remnants: Ecology, management, and conservation of fragmented communities. 1st edn. 632 pp. Chicago, University of Chicago Press.Google Scholar
Maldonado, A. Jr, Pinheiro, J., Simões, R.D.O. & Lanfredi, R.M. (2010) Canaania obesa (Platyhelminthes: Dicrocoeliidae): redescription and new hosts records. Zoologia (Curitiba, Impresso) 27, 789–794.Google Scholar
Marcogliese, D.J. (2003) Food webs and biodiversity: are parasites the missing link? Journal of Parasitology 89, S106–S113.Google Scholar
Mas-Coma, S., Valero, M.A. & Bargues, M.D. (2008) Effects of climate change on animal and zoonotic helminthiases. Revue Scientifique et Technique 27, 443–452.Google Scholar
McLaughlin, A. & Mineau, P. (1995) The impact of agricultural practices on biodiversity. Agriculture, Ecosystems & Environment 55, 201–212.Google Scholar
Navone, G.T., Notarnicola, J., Nava, S., Robles, M.R., Galliari, C. & Lareschi, M. (2009) Arthropods and helminths assemblage in sigmodontine rodents from wetlands of the Río de La Plata, Argentina. Mastozoología Neotropical 16, 121–133.Google Scholar
Pakdeenarong, N., Siribat, P., Chaisiri, K., Douangboupha, B., Ribas, A., Chaval, Y., Herbreteau, V. & Morand, S. (2014) Helminth communities in murid rodents from southern and northern localities in Lao PDR: the role of habitat and season. Journal of Helminthology 88, 302–309.Google Scholar
Patz, J.A., Graczyk, T.K., Geller, N. & Vittor, A.Y. (2000) Effects of enviromental change on emerging parasitic diseases. International Journal for Parasitology 30, 1394–1405.Google Scholar
Pinto, R.M., Knoff, M., Gomes, D.C. & Noronha, D. (2011) Nematodes from mammals in Brazil: an updating. Neotropical Helminthology 5, 139–183.Google Scholar
Poulin, R. (2007) Evolutionary ecology of parasites. 2nd edn. 332 pp. Princeton, Princeton University Press.Google Scholar
Püttker, T., Meyer-Lucht, Y. & Sommer, S. (2008) Effects of fragmentation on parasite burden (nematodes) of generalist and specialist small mammal species in secondary forest fragments of coastal Atlantic Forest, Brazil. Ecological Research 23, 207–215.Google Scholar
Reperant, L.A., Hegglin, D., Tanner, I., Fischer, C. & Deplazes, P. (2009) Rodents as shared indicators for zoonotic parasites of carnivores in urban environments. Parasitology 136, 329–337.Google Scholar
Simões, R.O., Souza, J.R., Maldonado, A. Jr & Luque, J.L. (2011) Variation in the helminth community structure of the sympatric sigmodontine rodents from the coastal Atlantic Forest of Rio de Janeiro, Brazil. Journal of Helminthology 85, 171–178.CrossRefGoogle ScholarPubMed
Simões, R.O., Maldonado, A. Jr & Luque, J.L. (2012) Helminth communities in three sympatric rodents from the Brazilian Atlantic Forest: contrasting biomass and numerical abundance. Brazilian Journal of Biology 72, 909–914.Google Scholar
Suzán, G., Esponda, F., Carrasco-Hernández, R. & Aguirre, A.A. (2012) Habitat fragmentation and infectious disease ecology. pp. 135–163 in Aguirre, A.A., Ostfeld, R.S. & Daszask, P. (Eds) New directions in conservation medicine: Applied cases of ecological health. Oxford, Oxford University Press.Google Scholar
Travassos, L. (1937) Revisão da família Trichostrongylidea Leiper 1912. Memórias do Instituto Oswaldo Cruz 1, 1–512.Google Scholar
Travassos, L. (1944) Revisão da família Dicrocoellidae Odhner, 1910. Monografias do Instituto Oswaldo Cruz. 1st edn. 500 pp. Rio de Janeiro, Editora Imprensa Nacional.Google Scholar
Umetsu, F. & Pardini, R. (2007) Small mammals in a mosaic of forest remnants and anthropogenic habitats – evaluating matrix quality in an Atlantic Forest landscape. Journal of Landscape Ecology 22, 517–530.Google Scholar
Urquhart, G.M., Armour, J., Duncan, J.L., Dunn, A.M. & Jennings, F.W (1998) Parasitologia veterinária. 2nd edn. 285 pp. Rio de Janeiro, Guanabara Koogan.Google Scholar
Vicente, J.J., Rodrigues, H.O., Gomes, D.C. & Pinto, R.M. (1997) Nematóides do Brasil. Parte V: Nematóides de mamíferos. Revista Brasileira de Zoologia 14, 1–452.Google Scholar
Yamaguti, F. (1961) Sistema Helminthum. Vol II. The nematodes of vertebrates. 1261 pp. New York, Interscience.Google Scholar