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The development of Angiostrongylus vasorum (Baillet, 1866) in the freshwater snail Pomacea canaliculata (Lamarck, 1822)

Published online by Cambridge University Press:  29 December 2014

L.R. Mozzer*
Affiliation:
Laboratório de Helmintologia Veterinária, Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brasil
A.L. Coaglio
Affiliation:
Laboratório de Helmintologia Veterinária, Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brasil
R.M. Dracz
Affiliation:
Laboratório de Helmintologia Veterinária, Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brasil
V.M.A Ribeiro
Affiliation:
Laboratório de Helmintologia Veterinária, Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brasil
W.S. Lima*
Affiliation:
Laboratório de Helmintologia Veterinária, Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brasil
*
*Fax: +55 (31) 3499-2970 E-mails: wlima@icb.ufmg.br and lanuze@yahoo.com.br
*Fax: +55 (31) 3499-2970 E-mails: wlima@icb.ufmg.br and lanuze@yahoo.com.br

Abstract

Angiostrongylus vasorum is a parasitic nematode that infects the heart and pulmonary artery and its branches of domestic and wild canids. The parasite can use several species of terrestrial and aquatic molluscs as intermediate hosts, although susceptibility varies. Pomacea canaliculata is a mollusc found in lakes, swamps and rivers in South America. In this study, we evaluated the susceptibility, parasite growth, oviposition and larval development of 282 P. canaliculata infected with 500 A. vasorum first-instar larvae (L1). From day 5 post-infection (pi) to day 30 pi, seven specimens per day were sacrificed to recover the larval instars. We compared 50 egg masses from infected and uninfected molluscs to determine the number of eggs per clutch, the hatching rate and the growth of the molluscs. The percentage of recovered larvae ranged from 39.17% to 67.5%. First-stage larvae (L1) were found until day 19 pi, second-stage larvae (L2) were found from days 11 to 25 pi, and third-stage larvae (L3) were recovered only after day 19 pi. Infected snails exhibited the most eggs during spawning, although the rate of hatching and shell size were lower in the infected snails compared with controls. This is the first report of an experimental infection of P. canaliculata with A. vasorum, and the results confirm the non-specificity of the nematode in relation to the intermediate host and indicate the importance of epidemiological surveys of this parasite and mollusc.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2014 

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References

Barçante, T.A. (2006) Aspectos do desenvolvimento de Angiostrongylus vasorum (Baillet, 1866) Kamensky, 1905 em Biomphalaria glabrata (Say, 1818). PhD thesis, Federal University of Minas Gerais, Belo Horizonte. Available at websitehttp://hdl.handle.net/1843/SAGF-6XLM7Z (accessed accessed 10 December 2014).Google Scholar
Barçante, J.M., Barçante, T.A., Dias, S.R., Vieira, L.Q., Lima, W.S. & Negrão-Corrêa, D. (2003) A method to obtain axenic Angiostrongylus vasorum first stage larvae from dog feces. Parasitology Research 89, 8993.Google ScholarPubMed
Bessa, E.C., Lopes, C.W.G. & Pinheiro, N.L. (1996) Sítios de desenvolvimento de Angiostrongylus vasorum (Baillet, 1866) Kamensky (Nematoda: Protostrongylidae) em Subulina octona (Bruguere, 1789) (Mollusca: Subulinidae) em condições de laboratório. Boletim do Instituto de Ciências Biológicas 47, 1319.Google Scholar
Bessa, E.C.A., Lima, W.S., Daemon, E., Cury, M.C. & Araujo, J.L.B. (2000) Desenvolvimento biológico de Angiostrongylus vasorum (Baillet) Kamensky (Nematoda: Angiostrongylida) em Subulina octona Bruguere (Mollusca: Subulinidae) em condições de laboratório. Revista Brasileira de Zoologia 17, 2941.CrossRefGoogle Scholar
Bolt, G., Monrad, J., Koch, J. & Jesen, A.L. (1993) The common frog (Rana temporaria) as a potential paratenic and intermediate host for Angiostrongylus vasorum. Parasitology Research 79, 428430.CrossRefGoogle ScholarPubMed
Brumpt, E. (1941) Observations biologiques diverses concernant Planorbis (Australorbis) glabratus hôte intermédiare de Schistosoma mansoni. Annales de Parasitologie 18, 945.Google Scholar
Gerichter, C.B. (1948) Observations on the life history of lung nematodes using snails as intermediate hosts. American Journal of Veterinary Research 9, 109112.Google Scholar
Chen, R., Tong, Q., Zhang, Y., Lou, D., Kong, Q., Lv, S., Zhuo, M., Wen, L. & Lu, S. (2011) Loop-mediated isothermal amplification: rapid detection of Angiostrongylus cantonensis infection in Pomacea canaliculata. Parasitology Vectors 4, 204.CrossRefGoogle ScholarPubMed
Etges, F.J. & Gresso, W. (1965) Effect of Schistosoma mansoni infection upon fecundity in Australorbis glabratus. Journal of Parasitology 51, 757760.CrossRefGoogle ScholarPubMed
França, R.S., Suriani, A.L. & Rocha, O. (2007) Composição das espécies de moluscos bentônicos nos reservatórios do baixo rio Tietê (São Paulo, Brasil) com uma avaliação do impacto causado pelas espécies exóticas invasoras. Revista Brasileira de Zoologia 24, 4151.CrossRefGoogle Scholar
Guilhon, J. & Afghahi, A. (1969) Larval development of Angiostrongylus vasorum (Baillet 1866) in organisms of various species of terrestrial molluscs. Série D: Sciences naturelles 268, 434436.Google Scholar
Guilhon, J. & Cens, B. (1969) Migrations et évolution d'Angiostrongylus vasorum (Baillet, 1866) dans l'organisme du chien. Série D: Sciences naturelles 269, 23772380.Google Scholar
Helm, J.R., Morgan, E.R., Jackson, M.W., Wotton, P. & Bell, R. (2010) Canine angiostrongylosis: an emerging disease in Europe. Journal of Veterinary Emergency and Critical Care 20, 98109.CrossRefGoogle ScholarPubMed
Iwanaga, S. & Lee, B.L. (2005) Recent advances in the innate immunity of invertebrate animals. Journal of Biochemistry and Molecular Biology 38, 128150.Google ScholarPubMed
Koch, J. & Willesen, J.L. (2009) Canine pulmonary angiostrongylosis: an update. The Veterinary Journal 179, 348359.CrossRefGoogle ScholarPubMed
Lima, W.S., Araujo Costa, H.M., Guimaraes, M.P. & Leite, A.C. (1985) Angiostrongylus vasorum (Baillet, 1866) nematoda: protostrongylidae, in dogs of Minas Gerais, Brazil. Memorias do Instituto Oswaldo Cruz 80, 233235.CrossRefGoogle Scholar
Lum-Kong, A. & Kenny, J.S. (1989) The reproductive biology of the ampullariid snail Pomacea urceus (Müller). Journal of Molluscan Studies 55, 5365.CrossRefGoogle Scholar
Lv, S., Zhou, X.N., Zhang, Y.I., Liu, H.X., Zhu, D., Yin, W.G., Steinmann, P., Wang, X.H. & Jia, T.W. (2006) The effect of temperature on the development of Angiostrongylus cantonensis (Chen 1935) in Pomacea canaliculata (Lamarck 1822). Parasitology Research 99, 583587.CrossRefGoogle ScholarPubMed
Lv, S., Zhang, Y., Liu, H.X., Hu, L., Yang, K., Steinmann, P., Chen, Z., Wang, L.Y., Utzinger, J. & Zhou, X.N. (2009) Invasive snails and an emerging infectious disease: results from the First National Survey on Angiostrongylus cantonensis in China. PLoS Neglected Tropical Diseases 3, e368.CrossRefGoogle Scholar
Minchella, D.J. (1985) Host life-history variation in response to parasitism. Parasitology 90, 205216.CrossRefGoogle Scholar
Morgan, E.R., Shaw, S.E., Brennan, S.F., De Waal, T.D., Jones, B.R. & Mulcahy, G.M. (2005) Angiostrongylus vasorum: a real heartbreaker. Trends in Parasitology 21, 4951.CrossRefGoogle ScholarPubMed
Morrison, W.E. & Hay, M.E. (2011) Feeding and growth of native, invasive and noninvasive alien apple snails (Ampullariidae) in the United States: invasives eat more and grow more. Biological Invasions 13, 945955.CrossRefGoogle Scholar
Mozzer, L.R., Montresor, L.C., Vidigal, T.H. & Lima, W.S. (2011) Angiostrongylus vasorum: experimental infection and larval development in Omalonyx matheroni. Journal of Parasitology Research 2011, 14.CrossRefGoogle ScholarPubMed
Pereira, C.A., Martins-Souza, R.L., Coelho, P.M., Lima, W.S. & Negrão-Corrêa, D. (2006) Effect of Angiostrongylus vasorum infection on Biomphalaria tenagophila susceptibility to Schistosoma mansoni. Acta Tropica 98, 224233.CrossRefGoogle ScholarPubMed
Qiu, J.W., Chan, M.T., Kwong, K.L. & Sun, J. (2011) Consumption, survival and growth in the invasive freshwater snail Pomacea canaliculata: does food freshness matter? Journal of Molluscan Studies 77, 17.CrossRefGoogle Scholar
Rawlings, T.A., Hayes, K.A., Cowie, R.H. & Collins, T.M. (2007) The identity, distribution, and impacts of non-native apple snails in the continental United States. BMC Evolutionary Biology 7, 97.CrossRefGoogle ScholarPubMed
Rosen, L., Ash, L.R. & Wallace, G.D. (1970) Life history of the canine lungworm Angiostrongylus vasorum (Baillet, 1866). American Journal of Veterinary Research 31, 131143.Google Scholar
Sauerländer, R. & Eckert, J. (1974) The African giant snail (Achatina fulica) as experimental intermediate host of Angiostrongylus vasorum (Nematoda). Zeitschrift für Parasitenkunde 44, 5972.CrossRefGoogle ScholarPubMed
Schallig, H.D., Sassen, M.J. & Jong-Brink, M. (1992) In vitro release of the antigonadotropic hormone, schistosomin, from the central nervous system of Lymnaea stagnalis is induced with a methanolic extract of cercariae of Trichobilharzia ocellata. Parasitology 104, 309314.CrossRefGoogle ScholarPubMed
Seuffert, M.E. & Martín, P.R. (2013) Juvenile growth and survival of the apple snail Pomacea canaliculata (Caenogastropoda: Ampullariidae) reared at different constant temperatures. Springerplus 2, 312.CrossRefGoogle ScholarPubMed
Thiengo, S. (1995) Sistemática e biogeografia família pilidae connoly: gênero pomacea (Perry, 1810). pp. 53–69 in Barbosa, F.S. (Ed.) Tópicos em malacologia médica. Rio de Janeiro, FIOCRUZ Press.Google Scholar
Thiengo, S.C., Fernandez, M.A., Boaventura, M.F. & Stortti, M.A. (1998) A survey of freshwater gastropods in the Microrregião Serrana of the State of Rio de Janeiro, Brazil. Memórias do Instituto Oswaldo Cruz 93, 233234.CrossRefGoogle ScholarPubMed
Tunholi, V.M., Lustrino, D., Tunholi-Alves, V.M., de Mello-Silva, C.C., Maldonado, A. Jr, Rodrigues, Mde.L. & Pinheiro, J. (2011) Changes in the reproductive biology of Biomphalara glabrata infected with different doses of Echinostoma paraensei miracidia. Journal of Invertebrate Patholology 106, 192195.CrossRefGoogle ScholarPubMed
Tsai, H.C., Liu, Y.C., Kunin, C.M., Lee, S.S., Chen, Y.S., Lin, H.H., Tsai, T.H., Lin, W.R., Huang, C.K., Yen, M.Y. & Yen, C.M. (2001) Eosinophilic meningitis caused by Angiostrongylus cantonensis: report of 17 cases. American Journal of Medicine 111, 109114.CrossRefGoogle ScholarPubMed
Williams, J.F., Lindemann, B., Padgett, G.A. & Smith, O.L. (1985) Angiostrongylus in a greyhoud. Journal of the American Veterinary Medical Association 186, 11011103.Google Scholar