Abstract
The susceptibility of two fish and four mosquito species to the Caiman yacare haemoparasite Hepatozoon caimani was experimentally investigated. Mosquitoes belonging to four species (Aedes fluviatilis, Aedes albopictus, Aedes aegypti and Culex quinquefasciatus) were blood-fed on two naturally infected C. yacare from the Central-West Region of Brazil that exhibited distinct levels of parasitaemia: caimans A (11.05 %) and B (1.25 %). None of the engorged A. fluviatilis, A. albopictus or A. aegypti mosquitoes fed on caiman A survived for the duration of the sporogonic cycle; the great majority of the engorged mosquitoes died within 48 h of the blood meal. All A. aegypti fed on caiman B were negative, whereas 91.3 % of dissected C. quinquefasciatus fed on the same caiman contained oocysts. Characid fish—Metynnis sp. and Astyanax sp.—were individually fed with C. quinquefasciatus females previously engorged (21–23 days) on caiman B. No parasite was found in the Astyanax fish. By contrast, 100 % of the Metynnis fish depicted numerous cysts harbouring cystozoites identical to those of H. caimani, even more than 8 months after the ingestion of the infected mosquitoes. The cysts were located near the veins of the liver and, in some cases, close to the tunica intima of these vessels. No inflammatory reaction was observed. Gametocytes were observed in the blood smears of juvenile caimans that had ingested infected fish 9–12 weeks earlier. The potential role of fish as paratenic vertebrate hosts of H. caimani in nature is discussed.
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References
Abelha MCF, Agostinho AA, Goulart E (2001) Plasticidade trófica em peixes de água doce. Acta Sci Biol Sci 23:425–434
AVMA – American Veterinary Medicine Association (2007). AVMA Guidelines on Euthanasia (Formerly Report on the AVMA panel on Euthanasia), Schaumburg, USA, 36 p. Available from http://www.avma.org/resources/euthanasia.pdf
Belkin JN, Heinemman SJ (1976) Collection Records of the Project “Mosquitoes of Middle America” 6. Southern Lesser Antilles: Barbados (BAR), Dominica (DOM), Grenada (GR, GRR), St. Lucia (LU), St. Vincent (VT). Mosq Syst 8:237–297
Borteiro C, Gutiérrez F, Tedros M, Kolenc F (2009) Food habits of the broad-snouted Caiman (Caiman latirostris: Crocodyla, Alligatoridae) in northwestern Uruguay. Studies Neotrop Fauna Environ 44:31–36
Consoli RGB, Lourenço-de-Oliveira R (1994) Principais mosquitos de importância sanitária no Brasil. Editora Fiocruz, Rio de Janeiro, Brazil
Dias ACMI, Branco CWC, Lopes VG (2005) Estudo da dieta natural de espécies de peixes no Reservatório de Riberão das Lajes, RJ. Acta Scient Biol Sci 27:355–364
Esteves KE (1996) Feeding ecology of three Astyanax species (Characidae, Tetragonopterinae) from a floodplain lake of Mogi-Guagu River, Parana River Basin, Brazil. Env Biol Fish 46:83–101
Forattini OP, Sallum MAM (1989) Taxonomic study redescription of Culex (Melanoconion) theobaldi (Lutz, 1904) (Diptera: Culicidae). Mem Inst Oswaldo Cruz 84 (Suppl. IV): 201–208
Gerking SD (1994) Feeding ecology of fish. Academic Press, London
Lainson R, Paperna I, Naiff RD (2003) Development of Hepatozoon caimani (Carini, 1909) Pessôa, De Biasi & De Souza, 1972 in the caiman Caiman c. crocodilus, the frog Rana catesbeiana and the mosquito Culex fatigans. Mem Inst Oswaldo Cruz 98:103–113
Landau I, Chabaud AG, Michel JC, Brygoo ER (1970) Mise en évidence d'un double mode de transmission chez un Hepatozoon de reptiles malgaches. C R Acad Sc Paris Sér D 270:2308–2310
Landau I, Michel JC, Chabaud AG (1972) Cycle biologique d'Hepatozoon domerguei; discussion sur les caractères fondamentaux d'un cycle de Coccidie. Z Parasitenk 38:250–270
Lennert K (1978) Malignant lymphomas other than Hodgkin's disease. Springer, Berlin
Mackerras MJ (1962) The life history of a Hepatozoon (Sporozoa: Adeleidea) of varanid lizards in Australia. Austr J Zool 10:35–44
Paperna I, Lainson R (2003) Ultrastructural studies on the sporogony of Hepatozoon spp. in Culex quinquefasciatus Say, 1823 fed on infected Caiman crocodilus and Boa constrictor from northern Brazil. Parasitology 127:147–154
Paperna I, Lainson R (2004) Hepatozoon cf. terzii (Sambon and Seligman, 1907) infection in the snake Boa constrictor constrictor from north Brazil: transmission to the mosquito Culex quinquefasciatus and the lizard Tropidurus torquatus. Parasite 11:175–181
Pauvolid-Corrêa A, Morales MA, Levis S, Figueiredo LTM, Couto-Lima D, Campos Z, Nogueira MF, Silva EE, Nogueira RMR, Schatzmayr HG (2011) Neutralising antibodies against West Nile virus in horses from Brazilian Pantanal. Mem Inst Oswaldo Cruz 106:467–474
Pessoa SB, de Biasi P, Souza DM (1972) Esporulação do Hepatozoon caimani (Carini 1909), parasita do jacaré-de-papo-amarelo: Caiman latirostris Daud, no Culex dolosus (L. Arribalzaga). Mem Inst Oswaldo Cruz 70:379–383
Resende EK, Pereira RAC, Almeida VLL (1998) Peixes herbívoros da planície inundável do rio Miranda, Pantanal, Mato Grosso do Sul. EMBRAPA-CPAP, Corumbá, Brazil
Santos AS, Stoll MN, Pinheiro MS, Campos Z, Magnusson WE, Mourão G (1996) Diets of Caiman crocodilus yacare from different habitats in Brazilian Pantanal. Herpetol J 6:111–117
Sloboda M, Kamler M, Bulantová J, Votýpka J, Modrý D (2008) Rodents as intermediate hosts of Hepatozoon ayorgbor (Apicomplexa: Adeleina: Hepatozoidae) from the African ball python, Python regius? Folia Parasitol 55:13–16
Smith TG, Desser SS, Martin DS (1994) The development of Hepatozoon sipedon sp. nov. (Apicomplexa: Adeleina: Hepatozoidae) in its natural host, the Northern water snake (Nerodia sipedon sipedon), in the culicine vectors Culex pipiens and C. territans, and in an intermediate host, the Northern leopard frog (Rana pipiens). Parasitol Res 80:559–568
Viana LA, Paiva F, Coutinho ME, Lourenço-de-Oliveira R (2010a) Hepatozoon caimani (Apicomplexa: Hepatozoidae) in wild caiman, Caiman yacare, from the Pantanal region, Brazil. J Parasitol 96:83–88
Viana LA, Soares P, Paiva F, Lourenço-de-Oliveira R (2010b) Caiman-biting mosquitoes and the natural vectors of Hepatozoon caimani in Brazil. J Med Entomol 47:670–676
Viana LA, Soares P, Paiva F, Silva JE, Coutinho ME (2012) Anurans as paratenic hosts in the transmission of Hepatozoon caimani to caimans Caiman yacare and Caiman latirostris. Parasitol Res 110:883–886
Wozniak EJ, Telford SR Jr (1991) The fate of Hepatozoon species naturally infecting Florida black racers and water snakes in potential mosquito and soft tick vectors, and histological evidence of pathogenicity in unnatural host species. Intern J Parasitol 21:511–516
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Pereira, G.R., Soares, P., Gomes, M.Q. et al. Are fish paratenic natural hosts of the caiman haemoparasite Hepatozoon caimani?. Parasitol Res 113, 39–45 (2014). https://doi.org/10.1007/s00436-013-3623-9
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DOI: https://doi.org/10.1007/s00436-013-3623-9