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Cryptosporidium spp. and Giardia sp. in Neotropical river otters (Lontra longicaudis) and giant otters (Pteronura brasiliensis) in northern Brazil

Published online by Cambridge University Press:  16 October 2017

João Carlos Gomes Borges ,
Danielle Dos Santos Lima ,
Beatriz Mafalda Calera ,
Miriam Marmontel ,
Edson Moura Da Silva ,
André Lucas De Oliveira Moreira  and
Leucio Câmara Alves
João Carlos Gomes Borges*
Affiliation:
Programa de Pós-Graduação em Ciência Animal Tropical, Universidade Federal Rural de Pernambuco, Dom Manoel de Medeiros, s/n, Dois Irmãos, CEP: 52.171-900, Recife, Pernambuco, Brazil Fundação Mamíferos Aquáticos, Avenida 17 de Agosto, 2001, Casa Forte, CEP: 52.061-540, Recife, Pernambuco, Brazil Grupo de Pesquisa em Mamíferos Aquáticos Amazônicos, Instituto de Desenvolvimento Sustentável Mamirauá, Estrada do Bexiga, 2584, Fonte Boa, CEP: 69.553-225, Tefé, Amazonas, Brazil
Danielle Dos Santos Lima
Affiliation:
Grupo de Pesquisa em Mamíferos Aquáticos Amazônicos, Instituto de Desenvolvimento Sustentável Mamirauá, Estrada do Bexiga, 2584, Fonte Boa, CEP: 69.553-225, Tefé, Amazonas, Brazil
Beatriz Mafalda Calera
Affiliation:
Grupo de Pesquisa em Mamíferos Aquáticos Amazônicos, Instituto de Desenvolvimento Sustentável Mamirauá, Estrada do Bexiga, 2584, Fonte Boa, CEP: 69.553-225, Tefé, Amazonas, Brazil
Miriam Marmontel
Affiliation:
Grupo de Pesquisa em Mamíferos Aquáticos Amazônicos, Instituto de Desenvolvimento Sustentável Mamirauá, Estrada do Bexiga, 2584, Fonte Boa, CEP: 69.553-225, Tefé, Amazonas, Brazil
Edson Moura Da Silva
Affiliation:
Programa de Pós-Graduação em Ciência Animal Tropical, Universidade Federal Rural de Pernambuco, Dom Manoel de Medeiros, s/n, Dois Irmãos, CEP: 52.171-900, Recife, Pernambuco, Brazil
André Lucas De Oliveira Moreira
Affiliation:
Fundação Mamíferos Aquáticos, Avenida 17 de Agosto, 2001, Casa Forte, CEP: 52.061-540, Recife, Pernambuco, Brazil
Leucio Câmara Alves
Affiliation:
Programa de Pós-Graduação em Ciência Animal Tropical, Universidade Federal Rural de Pernambuco, Dom Manoel de Medeiros, s/n, Dois Irmãos, CEP: 52.171-900, Recife, Pernambuco, Brazil
*
Correspondence should be addressed to: J.C.G. Borges, Programa de Pós-Graduação em Ciência Animal Tropical, Universidade Federal Rural de Pernambuco, Dom Manoel de Medeiros, s/n, Dois Irmãos, CEP: 52.171-900, Recife, Pernambuco, Brazil email: jcgborges@hotmail.com
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Abstract

Evaluating the occurrence of diseases in aquatic mustelids is a priority in the conservation strategies for the Neotropical river otter and giant otter. Thus, the objective of this study was to determine the frequency of infection caused by Cryptosporidium spp. and Giardia sp. in both host species in northern Brazil. The collection of biological samples was carried out in the states of Amapá, Amazonas, Pará and Rondônia, totalling 337 faecal samples of these species, which were processed using Kinyoun's technique for the identification of Cryptosporidium spp. oocysts, and centrifugal flotation in zinc sulphate solution for visualization of Giardia sp. cysts. All samples were also tested by direct immunofluorescence. The frequency of infection by Cryptosporidium spp. was higher than Giardia sp., in the two otter species. In the analysed samples co-infection by both protozoa was also found in 4.47% (14/313) of Neotropical river otter and 20.83% (5/24) of giant otter samples. Oocysts and cysts of Cryptosporidium and Giardia, respectively, may remain infectious within specific environmental conditions for long periods of time. The current identification of Neotropical and giant otters as hosts of these protozoa increases the possibility of infection in this species and the transmission of those agents to other aquatic and terrestrial organisms, as well as to human populations. The findings of this study represent the first description of Cryptosporidium spp. and Giardia sp. affecting Lontra longicaudis and Pteronura brasiliensis.

Keywords

parasitesprotozoadiseaseszoonosisdiagnosticscoccidianaquatic mammalsMustelidaeAmazon biomeconservation
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 98 , Special Issue 8: Special Section: European Marine Biology Symposium Papers 2018 , December 2018 , pp. 2153 - 2157
Copyright
Copyright © Marine Biological Association of the United Kingdom 2017 

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References

REFERENCES

Appelbee, A.J., Thompson, R.C.A., Measures, L.M. and Olson, M.E. (2010) Giardia and Cryptosporidium in harp and hooded seals from the Gulf of St. Lawrence, Canada. Veterinary Parasitology 173, 19–23.Google Scholar
Ayres, J.M. (1993) As matas de várzea de Mamirauá. Belém: Sociedade Civil Mamirauá.Google Scholar
Ayres, J.M., Fonseca, G.A.B., Rylands, A.B., Queiroz, H.L., Pinto, L.P., Masterson, D. and Cavalcanti, R.B. (2005) Os corredores ecológicos das florestas tropicais do brasil. Belém: Sociedade Civil Mamirauá.Google Scholar
Bica, V.C., Dillenburg, A.F. and Tasca, T. (2011) Diagnóstico laboratorial da giardiose humana: comparação entre as técnicas de sedimentação espontânea em água e de centrífugo-flutuação em solução de sulfato de zinco. Revista Hospital de Clínicas Porto Alegre 31, 39–45.Google Scholar
Borges, J.C.G., Alves, L.C., Faustino, M.A.G. and Marmontel, M. (2011) Occurrence of Cryptosporidium spp. in Antillean manatees (Trichechus manatus) and Amazonian manatees (Trichechus inunguis) from Brazil. Journal of Zoo and Wildlife Medicine 42, 593–596.Google Scholar
Borges, J.C.G., Alves, L.C., Lima, D.S., Luna, F.O., Aguilar, C.V.C., Vergara-Parente, J.E., Faustino, M.A.G., Lima, A.M.A. and Marmontel, M. (2007) Ocurrencia de Cryptosporidium spp. em manatí Amazônico (Trichechus inunguis, NATTERER, 1883). Biotemas 20, 63–66.Google Scholar
Brasil (1996) Ministério da Saúde. Infecções oportunistas por parasitas em AIDS: técnicas de diagnóstico. Brasília, DF: Ministério da Saúde.Google Scholar
Cabral, M.M.M., Zuanon, J., Mattos, G.E. and Rosas, F.C.W. (2010) Feeding habits of giant otters Pteronura brasiliensis (Carnivora: Mustelidae) in the Balbina hydroelectric reservoir, central Brazilian Amazon. Zoologia 27, 47–53.Google Scholar
Cacciò, S.M., Thopson, R.C.A., McLauchlin, J. and Smith, H.V. (2005) Unravelling Cryptosporidium and Giardia epidemiology. Trends in Parasitology 21, 426–431.Google Scholar
Carey, C.M., Lee, H. and Trevors, J.T. (2004) Biology, persistence and detection of Cryptosporidium parvum and Cryptosporidium hominis oocyst. Water Research 38, 818–862.Google Scholar
Carter, S.K. and Rosas, F.C.W. (1997) Biology and conservation of the giant otter Pteronura brasiliensis. Mammal Review 27, 1–26.Google Scholar
Coletti, L.D., Michel, T., Sanfelice, D. and Jardim, M.M.A. (2013) Uso do espaço por Lontra longicaudis (Mustelidae, Carnivora) em ambiente alterado no rio Caí, Rio Grande do Sul, Brasil. Lheringia, Série Zoologia 13, 240–245.Google Scholar
Crawley, M.J. (2013) The R book. 2nd edition. Chichester: Wiley.Google Scholar
Deng, M., Peterson, R.P. and Cliver, D.O. (2000) First findings of Cryptosporidium and Giardia in California sea lions (Zalophus californianus). Journal of Parasitology 86, 490–494.Google Scholar
Duplaix, N. (1980) Observations on the ecology and behaviour of the giant otter Pteronura brasiliensis in Suriname. Revue Écologique 34, 495–620.Google Scholar
Fayer, R., Dubey, J.P. and Lindsay, D.S. (2004) Zoonotic protozoa: from land to sea. Trends in Parasitology 20, 531–536.Google Scholar
Gaydos, J.K., Miller, W.A., Gilardi, K.V.K., Melli, A., Schwantje, H., Fritz, H. and Conrad, P.A. (2007) Cryptosporidium and Giardia in marine-foraging river otters (Lontra canadensis) from the Puget sound Georgia Basin ecosystem. Journal of Parasitology 93, 198–202.Google Scholar
Hughes-Hanks, J.M., Rickard, L.G., Panuska, C., Saucier, J.R., O'Hara, T.M., Dehn, L. and Rolland, R.M. (2005) Prevalence of Cryptosporidium spp. and Giardia spp. in five marine species. Journal of Parasitology 91, 1255–1228.Google Scholar
Junk, W.J., Bayley, P.B. and Sparks, R.E. (1989) The flood pulse concept in river-floodplain systems. Canadian Journal of Fisheries and Aquatic Science 106, 110–127.Google Scholar
Junk, W.J. and Mello, J.A.S.N. (1990) Impactos ecológicos das represas hidrelétricas na bacia amazônica brasileira. Estudos Avançados 4, 126–143.Google Scholar
Lallo, M.A., Pereira, A., Araújo, R., Favorito, S.E., Bertolla, P. and Bondan, E.F. (2009) Ocorrência de Giardia, Cryptosporidium e microsporídios em animais silvestres em áreas de desmatamento no Estado de São Paulo, Brasil. Ciência Rural 39, 1465–1470.Google Scholar
Lasek-Nesselquist, E., Bogomolni, A.L., Gast, R.J., Welch, D.M., Ellis, J.C., Sogin, M.L. and Moore, M.J. (2008) Molecular characterization of Giardia intestinalis haplotypes in marine mammals: variation and zoonotic potential. Diseases of Aquatic Organisms 81, 39–51.Google Scholar
LeChevallier, M.W., Norton, W.D. and Lee, R.G. (1991) Occurrence of Giardia and Cryptosporidium spp. in surface water supplies. Applied Environmental Microbiology 57, 2610–2616.Google Scholar
Lima, D.S. (2009) Ocorrência de ariranhas Pteronura brasiliensis (Carnivora: Mustelidae) e interferências antrópicas à espécie no lago Amanã, Reserva de Desenvolvimento Sustentável Amanã, Amazonas. PhD Dissertation. Federal University of Amapá.Google Scholar
Lima, D.S., Marmontel, M. and Bernard, E. (2013) Reoccupation of historical areas by the endangered giant river otter Pteronura brasiliensis (Carnivora: Mustelidae) in Central Amazonia, Brazil. Mammalia 78, 1–8.Google Scholar
Measures, L.N. and Olson, M. (1999) Giardiasis in pinnipeds from Eastern Canada. Journal of Wildlife Diseases 35, 779–782.Google Scholar
Méndez-Hermida, F., Gómez-Couso, H., Romero-Suances, R. and Ares-Mazás, E. (2007) Cryptosporidium and Giardia in wild otters (Lutra lutra). Veterinary Parasitology 144, 153–156.Google Scholar
Monteiro, M.A. (2005) Meio século de mineração industrial na Amazônia e suas implicações para o desenvolvimento regional. Estudos Avançados 19, 187–207.Google Scholar
Morgan, U.M., Xiao, L., Hill, B.D., O'Donoghue, P., Limor, J., Lal, A. and Thompson, R.C.A. (2000) Detection of the Cryptosporidium parvum ‘human’ genotype in a dugong (Dugong dugong). Journal of Parasitology 86, 1352–1354.Google Scholar
Palmeirim, A.F., Peres, C.A. and Rosas, F.C.W. (2014) Giant otter population responses to habitat expansion and degradation induced by a mega hydroelectric dam. Biological Conservation 174, 30–38.Google Scholar
Patz, J.A., Graczyk, T.K., Geller, N. and Vittor, A.Y. (2000) Effects of environmental change on emerging parasitic diseases. International Journal for Parasitology 30, 1394–1405.Google Scholar
Quinn, G.P. and Keough, M.J. (2002) Experimental design and data analysis for biologists. New York, NY: Cambridge University Press.Google Scholar
Quintela, F.M., Porciuncula, R.A. and Colares, E.P. (2008) Dieta de Lontra longicaudis (Olfers) (Carnivora, Mustelidae) em um arroio costeiro da região sul do estado do Rio Grande do Sul, Brasil. Neotropical Biology and Conservation 3, 119–125.Google Scholar
R Core Team (2014) R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. Available at http://www.R-project.org/Google Scholar
Reboredo-Fernández, A., Ares-Mazás, E., Martínez-Cedeira, J.A., Romero-Suances, R., Cacciò, S.M. and Gómez-Couso, H. (2015) Giardia and Cryptosporidium in cetaceans on the European Atlantic coast. Parasitology Research 114, 693–698.Google Scholar
Rengifo-Herrera, C., Ortega-Mora, L.M., Gómes-Bautista, M., García-Moreno, F.T., García-Párraga, D., Castro-Urda, J. and Pedraza-Díaz, S. (2011) Detection and characterization of a Cryptosporidium isolate from a southern elephant seal (Mirounga leonina) from the Antarctic Peninsula. Applied Environmental Microbiology 77, 1524–1527.Google Scholar
Thrusfield, R.C. (2004) Epidemiologia Veterinária. São Paulo, SP: Roca.Google Scholar
Ueno, H. and Gonçalves, P.C. (1994) Manual para diagnóstico das helmintoses de ruminantes. Porto Alegre, RS: Universidade Federal do Rio Grande do Sul.Google Scholar
Wagnerová, P., Sak, B., Mcevoy, J., Rost, M., Matysiak, A.P., Jezková, J. and Kvác, M. (2015) Genetic diversity of Cryptosporidium spp. Including novel identification of the Cryptosporidium muris and Cryptosporidium tyzzeri in horses in the Czech Republic and Poland. Parasitology Research 114, 1619–1624. doi: 10.1007/s00436-015-4353-y.Google Scholar
Xiao, L., Sulaiman, I.M., Ryan, U.M., Zhou, L., Atwill, E.R., Tischler, M.L., Zhang, X., Fayer, R. and Lal, A.S. (2002) Host adaptation and host-parasite co-evolution in Cryptosporidium: implications for taxonomy and public health. International Journal for Parasitology 32, 1773–1785.Google Scholar