Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-23T08:53:41.392Z Has data issue: false hasContentIssue false

Exposure of small mammals to ticks and rickettsiae in Atlantic Forest patches in the metropolitan area of Recife, North-eastern Brazil

Published online by Cambridge University Press:  04 January 2012

FILIPE DANTAS-TORRES*
Affiliation:
Dipartimento di Sanità Pubblica e Zootecnia, Università degli Studi di Bari, 70010 Valenzano, Bari, Italy
FILIPE MARTINS ALÉSSIO
Affiliation:
Laboratoire Population Environnement Développement, Université de Provence, Marseille, France
DANIEL BARRETO SIQUEIRA
Affiliation:
Departamento de Medicina Veterinária, Universidade Federal Rural de Pernambuco, 52171-900 Recife, Pernambuco, Brazil Instituto Brasileiro para Medicina da Conservação - Tríade, 52061-030 Recife, Pernambuco, Brazil
JEAN-FRANÇOIS MAUFFREY
Affiliation:
Laboratoire Population Environnement Développement, Université de Provence, Marseille, France
MARIA FERNANDA V. MARVULO
Affiliation:
Instituto Brasileiro para Medicina da Conservação - Tríade, 52061-030 Recife, Pernambuco, Brazil
THIAGO F. MARTINS
Affiliation:
Departamento de Medicina Veterinária Preventiva e Saúde Animal, Universidade de São Paulo, 05508-230 São Paulo, Brazil
JONAS MORAES-FILHO
Affiliation:
Departamento de Medicina Veterinária Preventiva e Saúde Animal, Universidade de São Paulo, 05508-230 São Paulo, Brazil
MARIA CECÍLIA G. O. CAMARGO
Affiliation:
Centro de Controle de Zoonoses, Prefeitura Municipal de São Paulo, 02031-020 São Paulo, Brazil
SANDRA REGINA NICOLETTI D'AURIA
Affiliation:
Centro de Controle de Zoonoses, Prefeitura Municipal de São Paulo, 02031-020 São Paulo, Brazil
MARCELO B. LABRUNA
Affiliation:
Departamento de Medicina Veterinária Preventiva e Saúde Animal, Universidade de São Paulo, 05508-230 São Paulo, Brazil
JEAN CARLOS RAMOS SILVA
Affiliation:
Departamento de Medicina Veterinária, Universidade Federal Rural de Pernambuco, 52171-900 Recife, Pernambuco, Brazil Instituto Brasileiro para Medicina da Conservação - Tríade, 52061-030 Recife, Pernambuco, Brazil
*
*Corresponding author: Dipartimento di Sanità Pubblica e Zootecnia, Università degli Studi di Bari, 70010 Valenzano, Bari, Italy. Tel/Fax: +39 080 4679839. E-mail: f.dantastorres@veterinaria.uniba.it

Summary

Between December 2007 and March 2009, small mammals were captured in 6 Atlantic Forest patches in Brazil. We assessed tick-host associations and whether they differ among forest strata, sites, seasons, and host age classes or between sexes. Moreover, we assessed the exposure of animals to Rickettsia spp. In total, 432 animals were captured and 808 ticks were found on 32·9% of them. Significant differences were found among host species, collection sites, and forest strata; microhabitat preference was a strong risk factor for tick infestation. The highest tick density rates were recorded in forest fragments settled in rural areas; 91·3% of the ticks were collected from animals trapped in these forest fragments. A high prevalence (68·8%) of antibodies to Rickettsia spp. was detected among animals. This study suggests that disturbed Atlantic Forest fragments provide an environment for ticks and small mammals, which are highly exposed to rickettsiae. It also indicates that forest patches settled in rural areas are usually associated with higher small mammal diversity as well as with higher tick density rates.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2012

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

Abel, I. S., Marzagão, G., Yoshinari, N. H. and Schumaker, T. T. (2000). Borrelia-like spirochetes recovered from ticks and small mammals collected in the Atlantic Forest Reserve, Cotia county, State of São Paulo, Brazil. Memórias do Instituto Oswaldo Cruz 95, 621624.CrossRefGoogle ScholarPubMed
Aragão, H. B. and Fonseca, F. (1961). Notas de ixodologia. VIII. Lista e chave para os representantes da fauna ixodológica brasileira. Memórias do Instituto Oswaldo Cruz 59, 115129.CrossRefGoogle Scholar
Ayres, M., Ayres, M. Jr. and Ayres, D. L. (2007). BioEstat 5.0: Aplicações Estatísticas nas áreas das Ciências Biológicas e Médicas. MCT, IDSM, CNPq, Belém.Google Scholar
Barros-Battesti, D. M., Arzua, M., Linardi, P. M., Botelho, J. R. and Sbalqueiro, I. J. (1998). Interrelationship between ectoparasites and wild rodents from Tijucas do Sul, state of Paraná, Brazil. Memórias do Instituto Oswaldo Cruz 93, 719725.CrossRefGoogle Scholar
Barros-Battesti, D. M., Yoshinari, N. H., Bonoldi, V. L. and Castro Gomes, A. (2000). Parasitism by Ixodes didelphidis and I. loricatus (Acari: Ixodidae) on small wild mammals from an Atlantic Forest in the State of Sao Paulo, Brazil. Journal of Medical Entomology 37, 820827.CrossRefGoogle ScholarPubMed
Barros-Battesti, D. M., Onofrio, V. C., Labruna, M. B., Martins, J. R. and Guglielmone, A. A. (2005). Redescription of Amblyomma fuscum Neumann, 1907 (Acari: Ixodidae), a rare South America tick confirmed in Brazil. Systematic Parasitology 61, 8592.CrossRefGoogle ScholarPubMed
Bittencourt, E. B. and Rocha, C. F. (2003). Host-ectoparasite specificity in a small mammal community in an area of Atlantic Rain Forest (Ilha Grande, State of Rio de Janeiro), Southeastern Brazil. Memórias do Instituto Oswaldo Cruz 98, 793798.CrossRefGoogle Scholar
Bonvicino, C. R., Oliveira, J. A. and D'Andrea, P. S. (2008). Guia dos Roedores do Brasil comCchaves para Gêneros Baseadas em Caracteres Externos. Centro Pan-Americano de Febre Aftosa, Rio de Janeiro, Brasil.Google Scholar
Bown, K. J., Lambin, X., Telford, G. R., Ogden, N. H., Telfer, S., Woldehiwet, Z. and Birtles, R. J. (2008). Relative importance of Ixodes ricinus and Ixodes trianguliceps as vectors for Anaplasma phagocytophilum and Babesia microti in field vole (Microtus agrestis) populations. Applied and Environmental Microbiology 74, 71187125.CrossRefGoogle ScholarPubMed
Bradley, C. and Altizer, S. (2006). Urbanization and the ecology of wildlife diseases. Trends in Ecology and Evolution 22, 95102.CrossRefGoogle ScholarPubMed
Bush, A. O., Lafferty, K. D., Lotz, J. M. and Shostak, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. The Journal of Parasitology 83, 575583.CrossRefGoogle Scholar
Dantas-Torres, F. (2008). Towards the standardization of the abbreviations of genus names of ticks (Acari: Parasitiformes: Ixodida). Veterinary Parasitology 154, 9497.CrossRefGoogle ScholarPubMed
Dantas-Torres, F., Ferreira, D. R., Melo, L. M., Lima, P. A., Siqueira, D. B., Rameh-de-Albuquerque, L. C., de Melo, A. V. and Ramos, J. A. (2010). Ticks on captive and free-living wild animals in northeastern Brazil. Experimental and Applied Acarology 50, 181189.CrossRefGoogle ScholarPubMed
Dantas-Torres, F., Oliveira-Filho, E. F., Soares, F. A., Souza, B. O., Valença, R. B. and , F. B. (2008). Ticks infesting amphibians and reptiles in Pernambuco, Northeastern Brazil. Revista Brasileira de Parasitologia Veterinária 17, 218221.CrossRefGoogle ScholarPubMed
Dantas-Torres, F., Onofrio, V. C. and Barros-Battesti, D. M. (2009). The ticks (Acari: Ixodida: Argasidae, Ixodidae) of Brazil. Systematic and Applied Acarology 14, 3046.CrossRefGoogle Scholar
Emmons, L. H. and Feer, F. (1997). Neotropical Rainforest Mammals: a Field Guide. University of Chicago Press, Chicago, IL, USA.Google Scholar
Freitas, L. H., Faccini, J. L. and Labruna, M. B. (2009). Experimental infection of the rabbit tick, Haemaphysalis leporispalustris, with the bacterium Rickettsia rickettsii, and comparative biology of infected and uninfected tick lineages. Experimental and Applied Acarology 47, 321345.CrossRefGoogle ScholarPubMed
Galindo-Leal, C. and Câmara, I. G. (2003). The Atlantic Forest of South America: Biodiversity Status, Threats, and Outlook. Island Press, Washington, DC, USA.Google Scholar
Guglielmone, A. A., Beati, L., Barros-Battesti, D. M., Labruna, M. B., Nava, S., Venzal, J. M., Mangold, A. J., Szabó, M. P., Martins, J. R., González-Acuña, D. and Estrada-Peña, A. (2006). Ticks (Ixodidae) on humans in South America. Experimental and Applied Acarology 40, 83100.CrossRefGoogle ScholarPubMed
Hammer, Ø., Harper, D. A. T. and Ryan, P. D. (2001). PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4, 19.Google Scholar
Horta, M. C., Pinter, A., Schumaker, T. T. and Labruna, M. B. (2006). Natural infection, transovarial transmission, and transstadial survival of Rickettsia bellii in the tick Ixodes loricatus (Acari: Ixodidae) from Brazil. Annals of the New York Academy of Science 1078, 285290.CrossRefGoogle ScholarPubMed
Horta, M. C., Labruna, M. B., Pinter, A., Linardi, P. M. and Schumaker, T. T. (2007). Rickettsia infection in five areas of the state of São Paulo, Brazil. Memórias do Instituto Oswaldo Cruz 102, 793801.CrossRefGoogle ScholarPubMed
Horta, M. C., Moraes-Filho, J., Casagrande, R. A., Saito, T. B., Rosa, S. C., Ogrzewalska, M., Matushima, E. R. and Labruna, M. B. (2009). Experimental infection of opossums Didelphis aurita by Rickettsia rickettsii and evaluation of the transmission of the infection to ticks Amblyomma cajennense. Vector-Borne and Zoonotic Diseases 9, 109118.CrossRefGoogle ScholarPubMed
Horta, M. C., Sabatini, G. S., Moraes-Filho, J., Ogrzewalska, M., Canal, R. B., Pacheco, R. C., Martins, T. F., Matushima, E. R. and Labruna, M. B. (2010). Experimental infection of the opossum Didelphis aurita by Rickettsia felis, Rickettsia bellii, and Rickettsia parkeri and evaluation of the transmission of the infection to ticks Amblyomma cajennense and Amblyomma dubitatum. Vector-Borne Zoonotic Diseases 10, 959967.CrossRefGoogle ScholarPubMed
Labruna, M. B. (2009). Ecology of Rickettsia in South America. Annals of the New York Academy of Science 1166, 156166.CrossRefGoogle ScholarPubMed
Marques, S., Col, R. D., Matos, M. O. Jr., Gonçalves, E. F. B., Pinter, A. and Labruna, M. B. (2006). Parasitismo de Amblyomma fuscum (Acari: Ixodidae) em humanos. Ciência Rural 36, 13281330.CrossRefGoogle Scholar
Martins, T. F., Dantas-Torres, F., Nieri-Bastos, F. A., Marcili, A., de Siqueira, D. B., Aléssio, F. M., Mauffrey, J.-F., DA Silva, J. C. R. and Labruna, M. B. (2009). Host records for the immature stages of Amblyomma fuscum (Acari: Ixodidae), a South American tick species. Entomological News 120, 370374.CrossRefGoogle Scholar
Martins, T. F., Onofrio, V. C., Barros-Battesti, D. M. and Labruna, M. B. (2010). Nymphs of the genus Amblyomma (Acari: Ixodidae) of Brazil: descriptions, redescriptions, and identification key. Ticks and Tick-borne Diseases 1, 7599.CrossRefGoogle ScholarPubMed
Onofrio, V. C., Barros-Battesti, D. M., Labruna, M. B. and Faccini, J. L. (2009). Diagnoses of and illustrated key to the species of Ixodes Latreille, 1795 (Acari: Ixodidae) from Brazil. Systematic Parasitology 72, 143157.CrossRefGoogle Scholar
Randolph, S. and Gern, L. (2003). Co-feeding transmission and its contribution to the perpetuation of the Lyme disease spirochete Borrelia afzelii. Emerging Infectious Diseases 9, 893894.CrossRefGoogle Scholar
Ranta, P., Blom, T. O. M., Niemela, J., Joensuu, E. and Siitonem, M. (1998). The fragmented Atlantic Rain Forest of Brazil: size, shape, and distribution of forest fragments. Biodiversity and Conservation 7, 385403.CrossRefGoogle Scholar
Redford, K. H. and Eisenberg, J. F. (1992). Mammals of the Neotropics. The Southern Cone: Chile, Argentina, Uruguay, Paraguay. University of Chicago Press, Chicago, IL, USA.Google Scholar
Reis, N. R., Peracchi, A. L., Pedro, W. A. and Lima, I. P. (2006). Mamíferos do Brasil. Universidade Estadual de Londrina, Londrina., Brazil.Google Scholar
Ribeiro, M. C., Metzger, J. P., Martensen, A. C., Ponzoni, F. J. and Hirota, M. M. (2009). The Brazilian Atlantic Forest: How much is left, and how is the remaining forest distributed? Implications for conservation. Biological Conservation 142, 11411153.CrossRefGoogle Scholar
Silveira, I., Pacheco, R. C., Szabó, M. P., Ramos, H. G. and Labruna, M. B. (2007). Rickettsia parkeri in Brazil. Emerging Infectious Diseases 13, 11111113.CrossRefGoogle ScholarPubMed
Spolidorio, M. G., Labruna, M. B., Mantovani, E., Brandao, P. E., Richtzenhain, L. J. and Yoshinari, N. H. (2010). Novel spotted fever group rickettsiosis, Brazil. Emerging Infectious Diseases 16, 521523.CrossRefGoogle ScholarPubMed
Streilen, K. E. (1982). The ecology of small mammals in the semiarid Brazilian Caatinga. III. Reproductive biology and population ecology. Annals of Carnegie Museum 51, 251269.CrossRefGoogle Scholar
Zhan, L., Cao, W. C., Chu, C. Y., Jiang, B. G., Zhang, F., Liu, W., Dumler, J. S., Wu, X. M., Zuo, S. Q., Zhang, P. H., Huang, H. N., Zhao, Q. M., Jia, N., Yang, H., Richardus, J. H. and Habbema, J. D. (2009). Tick-borne agents in rodents, China, 2004–2006. Emerging Infectious Diseases 15, 19041908.CrossRefGoogle ScholarPubMed