HELMINTH COMMUNITY STRUCTURE OF TWO SIGMODONTINE RODENTS IN SERRA DOS ÓRGÃOS NATIONAL PARK, STATE OF RIO DE JANEIRO, BRAZIL

Thiago Cardoso, Carla Elizabeth Macabu, Raquel de Oliveira Simoes, Arnaldo Maldonado-Junior, Jose Luis Luque, Rosana Gentile

Abstract


The fauna and community structure of the helminths of two sympatric sigmodontine rodent hosts, Akodon montensis (Thomas, 1913) and Oligoryzomys nigripes (Olfers, 1818) (Rodentia, Cricetidae) were studied in two areas of an Atlantic Forest reserve, the Serra dos Órgãos National Park in Petrópolis and Teresópolis municipalities, state of Rio de Janeiro, Brazil. During the study, 127 rodents were collected, among which 63 were parasitized (approximately 50%). The helminths recovered from A. montensis were the nematodes Protospirura numidica criceticola, Stilestrongylus aculeata, Stilestrongylus eta, Stilestrongylus lanfrediae and Trichofreitasia lenti; the trematode Canaania obesa and the cestode Rodentolepis akodontis. Oligoryzomys nigripes was infected by Avellaria sp., Guerrerostrongylus zetta, T. lenti and S. lanfrediae. Complete host specificity was observed in all helminth species only in Petrópolis; although T. lenti and S. lanfrediae were shared between host species in Teresópolis. Stilestrongylus aculeata, S. eta and S. lanfrediae had the greatest abundance, i.e. considering all hosts, and intensity, i.e. considering only infected hosts, in the study. Stilestrongylus lanfrediae and G. zetta were the most prevalent species. Guerrerostrongylus zetta and S. lanfrediae had higher abundance and prevalence in adult hosts. The latter species also had higher abundance and prevalence in male hosts. Stilestrongylus aculeata and S. eta had higher prevalence in young female hosts, and T. lenti, higher abundance in males and higher prevalence in adult females of A. montensis. Only the helminth community of O. nigripes in Teresópolis followed a nested pattern of species distribution. All the other helminth communities in A. montensis and O. nigripes had random patterns of species distribution. The results suggest the existence of intrinsic characteristics between hosts and parasites as well as different patterns of associations in those interactions with the environment. 


Keywords


Akodon montensis; Atlantic Forest; host-parasite interaction; Oligoryzomys nigripes; parasitism; protected areas

Full Text:

PDF

References


Almeida-Neto, M., Guimarães, P., Guimarães Jr., P. R., Loyola, R. D., & Ulrich, W. 2008. A consistent metric for nestedness analysis in ecological systems: reconciling concept and measurement. Oikos, 117(8), 1227–1239. DOI: 10.1111/j.0030-1299.2008.16644.x

Ayoade, J. O. 1986. Introdução à climatologia para os trópicos. 1a ed. São Paulo, SP: Editora Difel: p. 332.

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(1), 31–44. DOI: 10.1017/S0022149X99000049

Bonvicino, C. R., Oliveira, J. A., & D’Andrea, P. S. 2008. Guia dos roedores do Brasil, com chaves para gêneros baseadas em caracteres externos. Rio de Janeiro: Centro Pan-Americano de Febre Aftosa - OPAS/OMS: p. 120.

Bray, R. A., Gibson, D. I., & Jones, A. (Eds.). 2008. Keys to the Trematoda, volume 3. London: CAB International and Natural History Museum: p. 848.

Bush, A. O., Lafferty, K. D., Lotz, J. M., & Shostak, A. W. 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. The Journal of Parasitology, 83(4), 575–583. DOI: 10.2307/3284227

Callinan, A. P. L., & Westcott, J. M. 1986. Vertical distribution of trichostrongylid larvae on herbage and in soil. International Journal for Parasitology, 16(3), 241–244. DOI: 10.1016/0020-7519(86)90050-0

Cardoso, T. S., Simões, R. O., Luque, J. L. F., Maldonado, A., & Gentile, R. 2016. The influence of habitat fragmentation on helminth communities in rodent populations from a Brazilian Mountain Atlantic Forest. Journal of Helminthology, 90(4), 460–468. DOI: 10.1017/S0022149X15000589

Cardoso, T. S., Braga, C. A. C., Macabu, C. E., Simões, R. O., Costa-Neto, S. F., Maldonado-Júnior, A., Gentile, R., & Luque, J. L. 2018. Helminth metacommunity structure of wild rodents in a preserved area of the Atlantic Forest, Southeast Brazil. Revista Brasileira de Parasitologia Veterinária, 27(4), 495–504. DOI: 10.1590/S1984-296120180066

Castro, R. G. B. M., Costa-Neto, S. F., Maldonado Júnior, A., & Gentile, R. 2017. Ecological aspects of nematode parasites of Didelphis aurita (Didelphimorphia, Didelphidae) in urban-sylvatic habitats in Rio de Janeiro, Brazil. Oecologia Australis, 21(1), 54–61. DOI: 10.4257/oeco.2017.2101.06

Combes, C. 2001. Parasitism: the ecology and evolution of intimate interactions. 1st ed. Chicago, IL: University of Chicago Press: p. 552.

Dalmagro, A. D., & Vieira, E. M. 2005. Patterns of habitat utilization of small rodents in an area of Araucaria forest in Southern Brazil. Austral Ecology, 30(4), 353–362. DOI: 10.1111/j.1442-9993.2005.01447.x

Digiani, M. C., & Durette-Desset, M. C. 2003. Two new species of Nippostrongylinae (Nematoda, Heligmosomoidea, Heligmonellidae) from a sigmodontine rodent in Argentina. Acta Parasitologica, 48(1), 12–18.

Dormann, C. F., Gruber, B., & Fründ, J. 2008. Introducing the bipartite Package: analysing ecological networks. R news, 8/2, 8–11.

Durette-Desset, M. C., & Digiani, M. C. 2010. Taxonomic revision of the type specimens of Ethiopian Nippostrongylinae (Nematoda) deposited at the Natural History Museum of London. Zootaxa, 2494, 1–28. DOI: 10.5281/zenodo.195700

Freitas, J. F. T., & Lent, H. 1934. Novo nematodeo da sub-familia Heligmosominae Travassos, 1914, parasito de Agouti paca (L.): Avellaria avellari n. g., n. sp. Memórias do Instituto Oswaldo Cruz, 28(4), 577–583. DOI: 10.1590/S0074-02761934000400003

Gomes, D. C., Lanfredi, R. M., Pinto, R. M., & Souza, W. 1992. Description of Trichuris travassosi n. sp. (Nematoda: Trichurinae) from a Brazilian rodent, by light and scanning electron microscopy. Memórias do Instituto Oswaldo Cruz, 87(suppl. 1), 1–10. DOI: 10.1590/S0074-02761992000500004

Gomes, D. C., Cruz, R. P., Vicente, J. J., & 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(4), 699–707. DOI: 10.1590/S0101-81752003000400024

Grundmann, A. W., Warnock, R. G., & Wasson, D. L. 1976. Some mechanisms of natural regulation of parasitic helminth populations. American Midland Naturalist, 95(2), 347–360. DOI: 10.2307/2424399

Han, B. A., Kramer, A. M., & Drake, J. M. 2016. Global patterns of zoonotic disease in mammals. Trends in Parasitology, 32(7), 565–577. DOI: 10.1016/j.pt.2016.04.007

Jiménez-Ruiz, F. A., & Gardner, S. L. 2003. The nematode fauna of long-nosed mice Oxymycterus spp. from the Bolivian Yungas. Journal of Parasitology, 89(2), 299–308. DOI: 10.1645/0022-3395(2003)089[0299:TNFOLM]2.0.CO;2

Khalil, L. F., Jones, A., & Bray, R. A. 1994. Keys to the cestode parasites of vertebrates. Wallingford: CAB International: p. 768.

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. Revista Brasileira de Biologia, 72(3), 563–567. DOI: 10.1590/S1519-69842012000300019

Maldonado Jr., A., Gentile, R., Fernandes-Moraes, C. C., D’Andrea, P. S., Lanfredi, R. M., & Rey, L. 2006. Helminth communities of Nectomys squamipes naturally infected by the exotic trematode Schistosoma mansoni in southeastern Brazil. Journal of Helminthology, 80(4), 369–375. DOI: 10.1017/JOH2006366

Maldonado Jr., A., Pinheiro, J., Simões, R. O., & Lanfredi, R. M. 2010. Canaania obesa (Platyhelminthes: Dicrocoeliidae): redescription and new hosts records. Zoologia, 27(5), 789–794. DOI: 10.1590/S1984-46702010000500015

Miño, M. H. 2008. Infection pattern of the spirurid nematode Protospirura numidica criceticola in the cricetid rodent Akodon azarae on poultry farms of central Argentina. Journal of Helminthology, 82(2), 153–158. DOI: 10.1017/S0022149X08912396

Navone, G. T., Notarnicola, J., Nava, S., Robles, M. R., Galliari, C., & Lareschi, M. 2009. Ensamble de artrópodos y helmintos parásitos en roedores sigmodontinos de los humedales del Río de la Plata, Argentina. Mastozoología Neotropical, 16(1), 121–134.

Oksanen, J., Blanchet, F. G., Kindt, R., Legendre, P., Minchin, P. R., O’Hara, R. B., Simpson, G. L., Solymos, P., Stevens, M. H. H., Szoecs, E., & Wagner, H. 2017. vegan: community ecology package. R package version 2.4-2. (Retrieved on February 10, 2017, from http://CRAN.R-project.org/package=vegan).

Owen, R. D., Goodin, D. G., Koch, D. E., Chu, Y.-K., & Jonsson, C. B. 2010. Spatiotemporal variation in Akodon montensis (Cricetidae: Sigmodontinae) and hantaviral seroprevalence in a subtropical forest ecosystem. Journal of Mammalogy, 91(2), 467–481. DOI: 10.1644/09-MAMM-A-152.1

Paglia, A. P., Fonseca, G. A. B., Rylands, A. B., Herrmann, G., Aguiar, L. M. S., Chiarello, A. G., Leite, Y. L. R., Costa, L. P., Siciliano, S., Kierulff, M. C. M., Mendes, S. L., Tavares, V. C., Mittermeier, R. A., & Patton, J. L. 2012. Annotated checklist of Brazilian Mammals. Occasional Paper No. 6. 2nd ed. Arlington, VA: Conservation International: p. 76.

Panisse, G., Robles, M. D. R., Digiani, M. C., Notarnicola, J., Galliari, C., & Navone, G. T. 2017. Description of the helminth communities of sympatric rodents (Muroidea: Cricetidae) from the Atlantic Forest in northeastern Argentina. Zootaxa, 4337(2), 243–262. DOI: 10.11646/zootaxa.4337.2.4

Patterson, B. D., & Atmar, W. 1986. Nested subsets and the structure of insular mammalian faunas and archipelagos. Biological Journal of the Linnean Society, 28(1-2), 65–82. DOI: 10.1111/j.1095-8312.1986.tb01749.x

Patton, J. L., Pardiñas, U. F. J., & D’Elía, G. 2015. Mammals of South America, Volume 2: rodents. Chicago: The University of Chicago Press: p. 1384.

Pinto, R. M., Knoff, M., Gomes, D. C., & Noronha, D. 2011. Nematodes from mammals in Brazil: an updating. Neotroprical Helminthology, 5(2), 139–183.

Poulin, R. 2007. Evolutionary ecology of parasites. 2nd ed. Princeton, NJ: Princeton University Press: p. 360.

Poulin, R. 2014. Parasite biodiversity revisited: frontiers and constraints. International Journal for Parasitology, 44(9), 581–589. DOI: 10.1016/j.ijpara.2014.02.003

Püttker, T., Meyer-Lucht, Y., & Sommer, S. 2006. Movement distances of five rodent and two marsupial species in forest fragments of the coastal Atlantic rainforest, Brazil. Ecotropica, 12(2), 131–139.

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 the coastal Atlantic Forest, Brazil. Ecological Research, 23(1), 207–215. DOI: 10.1007/s11284-007-0366-z

Quentin, J.-C. 1971. Morphologie comparée des structures céphaliques et génitales des Oxyures du genre Syphacia. Annales de Parasitologie Humaine et Comparee, 46(1), 15–60. DOI: 10.1051/parasite/1971461015

R Core Team. 2017. R: a language and environment for statistical computing. R Foundation for statistical computing, Vienna, Austria. (Retrieved on February 10, 2017, from https://www.R-project.org/).

Robles, M. R. 2011. New species of Trichuris (Nematoda: Trichuridae) from Akodon montensis Thomas, 1913 of the Paranaense forest in Argentina. Journal of Parasitology, 97(2), 319–327. DOI: 10.1645/GE-2434.1

Simões, R., Gentile, R., Rademaker, V., D’Andrea, P., Herrera, H., Freitas, T., Lanfredi, R., & Maldonado Jr., A. 2010. Variation in the helminth community structure of Thrichomys pachyurus (Rodentia: Echimyidae) in two sub-regions of the Brazilian Pantanal: the effects of land use and seasonality. Journal of Helminthology, 84(3), 266–275. DOI: 10.1017/S0022149X09990629

Simões, R. O., Souza, J. G. R., Maldonado Jr., A., & Luque, J. L. 2011. Variation in the helminth community structure of three sympatric sigmodontine rodents from the coastal Atlantic Forest of Rio de Janeiro, Brazil. Journal of Helminthology, 85(2), 171–178. DOI: 10.1017/S0022149X10000398

Stein, M., Suriano, D. M., & Novaro, A. J. 1994. Parasite nematodes from Dusycion griseus (Gray, 1837), D. culpaeus (Molina, 1782) and Conepatus chinga (Molina, 1782) (Mammalia:Carnivora) in Neuquen, Argentina. Systematics and ecology. Boletin Chileno de Parasitologia, 49(3-4), 60–65.

Sutton, C. A. 1989. Contribution to the knowledge of Argentina's parasitological fauna. XVII. Spirurida (Nematoda) from Neotropical Cricetidae: Physaloptera calnuensis n. sp. and Protospirura numidica criceticola Quentin, Karimi and Rodriguez de Almeida. Bulletin du Museum National d'Histoire Naturelle, 11(1), 61–67.

Teixeira, B. R., Loureiro, N., Strecht, L., Gentile, R., Oliveira, R. C., Guterres, A., Fernandes, J., Mattos, L. H. B. V., Raboni, S. M., Rubio, G., Bonvicino, C. R., Duarte dos Santos, C. N., Lemos, E. R. S., & D’Andrea, P. S. 2014. Population ecology of hantavirus rodent hosts in southern Brazil. The American Journal of Tropical Medicine and Hygiene, 91(2), 249–257. DOI: 10.4269/ajtmh.13-0465

Thomas, F., Bonsall, M. B., & Dobson, A. P. 2005. Parasitism, biodiversity, and conservation. In: F. Thomas, F. Renaud & J.-F. Guégan (Eds.), Parasitism and ecosystems. pp. 124–139. New York: Oxford University Press.

Thul, J. E., Forrester, D. J., & Abercrombie, C. L. 1985. Ecology of parasitic helminths of wood ducks, Aix sponsa, in the Atlantic flyway. Proceedings of the Helminth Society Washington, 52(2), 297–310.

Travassos, L. 1937. Revisão da família Trichostrongylidae Leiper 1912. Memórias Do Instituto Oswaldo Cruz, 1, 1–512.

Travassos, L. 1944. Revisão da família Dicrocoeliidiae, Odhner, 1910. Rio de Janeiro: Imprensa Nacional: p. 357.

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(suppl. 1), 1–452. DOI: 10.1590/S0101-81751997000500001

Wells, K., Smales, L. R., Kalko, E. K. V., & Pfeiffer, M. 2007. Impact of rain-forest logging on helminth assemblages in small mammals (Muridae, Tupaiidae) from Borneo. Journal of Tropical Ecology, 23(01), 35–43. DOI: 10.1017/S0266467406003804

Werk, D. F., Gallas, M., Silveira, E. F., & Périco, E. 2016. New locality records for Guerrerostrongylus zetta (Travassos, 1937) Sutton; Durette-Desset, 1991 (Nematoda: Heligmonellidae) parasitizing Oligoryzomys nigripes (Olfers, 1818) (Rodentia: Sigmodontinae) from southern Brazil. Check List, 12(2), 1861. DOI: 10.15560/12.2.1861

Yamaguti, S. 1961. Systema Helminthum. The nematodes of vertebrates, Vol III. New York: Interscience Publisher: p. 1261.

Zuk, M., & McKean, K. A. 1996. Sex differences in parasite infections: patterns and processes. International Journal for Parasitology, 26(10), 1009–1023. DOI: 10.1016/S0020-7519(96)80001-4




DOI: https://doi.org/10.4257/oeco.2019.2302.09

Refbacks

  • There are currently no refbacks.