Visão geral da distribuição de Ascogregarina (Apicomplexa: Lecudinidae) e seu papel no desenvolvimento biológico de Aedes aegypti e Ae. albopictus

Autores

  • Thiago Nunes Pereira Fundação Oswaldo Cruz (René Rachou-MG)
  • Josiane Somariva Prophiro Universidade do Sul de Santa Catarina
  • Guilherme Liberato da Silva Departamento de Fitossanidade - Universidade Federal de Pelotas http://orcid.org/0000-0001-6619-6622
  • Joice Guilherme de Oliveira Universidade do Sul de Santa Catarina
  • Onilda Santos da Silva Universidade Federal do Rio Grande do Sul http://orcid.org/0000-0003-4806-8285

DOI:

https://doi.org/10.5007/2175-7925.2018v31n3p1

Resumo

As ascogregarinas são protozoários, pertencentes ao filo Apicomplexa, que parasitam várias espécies de invertebrados, incluindo algumas importantes espécies de mosquitos envolvidas na transmissão de arboviroses, como dengue, febre amarela, chikungunya e zika. As espécies gregarinas mais frequentemente reportadas em mosquitos são Ascogregarina culicis, A. taiwanensis e A. barreti, as quais possuem Aedes aegypti, Ae. albopictus e Ae. triseriatus como hospedeiros naturais, respectivamente. Estudos têm demonstrado que o parasitismo de algumas espécies de Ascogregarina pode influenciar negativamente o desenvolvimento biológico desses mosquitos e tal influência depende da sua distribuição ambiental. Assim, nesta revisão, foi verificada a distribuição de espécies de Ascogregarina em vários países, bem como sua influência no desenvolvimento de mosquitos e seu possível uso como controle destes insetos.

Biografia do Autor

Thiago Nunes Pereira, Fundação Oswaldo Cruz (René Rachou-MG)

Possui graduação em Ciências Biológicas pela Universidade do Sul de Santa Catarina - UNISUL (2012) e mestrado em Microbiologia Agrícola e do Ambiente pela Universidade Federal do Rio Grande do Sul - UFRGS (2015). Atualmente é aluno de doutorado ( 2016-2020) no programa de Ciência e Saúde da Fundação Oswaldo Cruz (René Rachou-MG). Tem experiência nas áreas de Entomologia Médica e Parasitologia , atuando principalmente nos seguintes temas: Biologia e ecologia de Aedes aegypti e Aedes albopicutus, controle de origem vegetal, sintético e biológico.

Josiane Somariva Prophiro, Universidade do Sul de Santa Catarina

Possui graduação em Ciências Biológicas pela Universidade do Sul de Santa Catarina - UNISUL (2005), mestrado (2008) e doutorado (2013) em Ciências Biológicas pela Universidade Federal do Paraná - UFPR. Tem experiência nas áreas de Parasitologia, Imunologia, Zoologia de invertebrados e Entomologia Médica.

Guilherme Liberato da Silva, Departamento de Fitossanidade - Universidade Federal de Pelotas

Possui graduação em Ciências - Licenciatura e Bacharelado - em Biologia pelo Centro Universitário Univates, atualmente, mestrando no Programa de Pós-Graduação em Fitossanidade pela Universidade Federal de Pelotas. Atua na área de Acarologia.

Joice Guilherme de Oliveira, Universidade do Sul de Santa Catarina

Mestranda em Ciências da Saúde na linha de pesquisa em doenças infeccionas e parasitárias/infectologia na Universidade do Sul de Santa Catarina (UNISUL).Possui graduação em Ciências Biológicas pela UNISUL (2014). Trabalha no grupo de pesquisa em Imunoparasitologia (IMPAR) e no grupo de pesquisa em Tecnologia Farmacêutica (TecFarma) no desenvolvimento de biolarvicidas para aplicação no controle do vetor Aedes aegypti. Tem experiência nas áreas de Entomologia Médica e Parasitologia , atuando principalmente nos seguintes temas: Controle, epidemiologia, biologia e ecologia de Ae. aegypti e Ae. albopictus.

Onilda Santos da Silva, Universidade Federal do Rio Grande do Sul

Possui graduação em Biologia pela Pontifícia Universidade Católica do Rio Grande do Sul, mestrado em Biociências (Zoologia) pela mesma Universidade, e doutorado e pós-doutorado em Ciências Naturais - Área de Parasitologia, pela Eberhard - Karls - Universität Tübingen, Alemanha. Nesta universidade atuou também como pesquisadora na área de controle de Aedes aegypti e Anopheles sp. De 2000 a 2008 atuou em pesquisa e docência na Universidade do Sul de Santa Catarina. Nesta universidade enfatizou as pesquisas no controle de Aedes aegypti e de Aedes albopictus, bem como distribuição de flebotomíneos no Sul do Brasil. A partir de 2008, iniciou atividades de docência e pesquisa na Universidade Federal do Rio Grande do Sul. Nesta Universidade desenvolve pesquisas na área de biologia e controle de Aedes aegypti e Aedes albopictus com produtos químicos e naturais e resistência a inseticidas químicos. Na linha de biologia e controle de mosquitos, avalia associações com Amebas de Vida Livre, bem como entomobacterias como Xenorhabdus nematophila, Photorhabdus luminescens, Wolbachia pipientis e microbiota bacteriana geral destas espécies de mosquitos. Também atua na área da Parasitologia Humana, com ênfase em Leishmanioses e Flebotomíneos e outras Zoonoses.

Referências

ALBICÓCCO, A. P.; VEZZANI, D. Further study on Ascogregarina culicis in temperate Argentina: prevalence and intensity in Aedes aegypti larvae and pupae. Journal of Invertebrate Pathology, Riverside, v. 101, p. 210-214, 2009.

ALIABADI, B. W.; JULIANO, S. A. Escape from gregarine parasites affects the competitive interactions of an invasive mosquito. Biological Invasions, Dordrecht, v. 4, p. 283-297, 2002.

ANDREADIS, T. G. Microsporidian parasites of mosquitoes. Journal of the American Mosquito Control Association, Washington, v. 23, p. 3-29, 2007.

ARAÚJO, H. R.; CARVALHO, D. O.; IOSHINO, R. S.; COSTA-DA-SILVA, A. L.; CAPURRO, M. L. Aedes aegypti control strategies in Brazil: Incorporation of new technologies to overcome the persistence of dengue epidemics. Insects, Basel, v. 11, p. 576-594, 2015.

BARRETT, W. L. Damage caused by Lankesteria culicis (Ross) to Aedes aegypti (L). Mosquito News, Albany, v. 28, p. 441, 1968.

BARRETT, W. L.; MILLER, F. M., KLIEWER; J. W. Distribution in Texas of Lankesteria culicis (Ross), a parasite of Aedes aegypti (L.). Mosquito News, Albany, v. 31, p. 23-27, 1971.

BEIER, J. C.; CHADEE, D. D.; CHARRAN, A.; COMISKEY, N. M.; WESSON, D. M. Country-wide prevalence of Ascogregarina culicis (Apicomplexa: Lecudinidae), a protozoan parasite of Aedes aegypti in Trinidad, West Indies. Journal of the American Mosquito Control Association, Washington, v. 11, p. 419-423, 1995.

BEIER, J. C.; CRAIG, G. B. Gregarine parasites of mosquitoes. In: LAIRD, M. (Ed.). Integrated mosquito control methodologies. Vol 2. London: Academic Press, 1985. p. 167-184.

BEIER, J. C.; HARRIS, C. Ascogregarina barretti (Sporozoa: diplocystidae) infections in natural populations of Aedes triseriatus (Diptera: Culicidae). Journal of Parasitology, Lawrence, v. 69, p. 430-431, 1983.

BENELLI, G.; JEFFRIES, C. L.; WALKER, T. Biological control of mosquito vectors: past, present, and future. Insects, Basel, v. 7, n. 4, 2016.

Biological Control of Mosquito Vectors: Past, Present, and Future. Insects 2016, 7, 52.

BELLINATO, D. F.; VIANA-MEDEIROS, P. F.; ARAÚJO, S. C.; MARTINS, A. J.; LIMA, J. B.; VALLE, D. Resistance status to the insecticides Temephos, Deltamethrin, and Diflubenzuron in Brazilian Aedes aegypti populations. BioMed Research International, Cairo, v. 2016, p. 8603263, 2016.

BHATIA, B. L. Protozoa: sporozoa. In: SEWELI, R. B. S. (Ed.). The fauna of British India. London: Taylor and Francis, 1938. p. 41-42.

BLACKMORE, M. S.; SCOLES, G. A.; CRAIG, G. B. Parasitism of Aedes aegypti and Ae. albopictus (Diptera: Culicidae) by Ascogregarina spp. (Apicomplexa: Lecudinidae) in Florida. Journal of Medical Entomology, Lanham, v. 32, p. 847-852, 1995.

BLAIR, C. D.; ADELMAN, Z. N.; OLSON, K. E. Molecular strategies for interrupting arthropod-borne virus transmission by mosquitoes. Clinical Microbiology Reviews, Washington, v. 13, p. 651-661, 2000.

BORUCKI, M. K.; KEMPF, B. J.; BLAIR, C. D.; BEATY, B. J. The effect of mosquito passage on the La Crosse virus genotype. Journal of General Virology, London, v 82, p. 2919-2926, 2001.

CAIXETA, E. S.; SILVA, C. F.; SANTOS, V. S.; OLEGÁRIO DE CAMPOS JÚNIOR, E.; PEREIRA, B. B. Ecotoxicological assessment of pyriproxyfen under environmentally realistic exposure conditions of integrated vector management for Aedes aegypti control in Brazil. Journal of Toxicology and Environmental Health, Ottawa, v. 79, p.799-803, 2016.

CHEN, W. J. The life cycle of Ascogregarina taiwanensis (Apicomplexa: Lecudinidae). Parasitology Today, Cambridge, v. 15, p. 153-156, 1999.

CHEN, W. J.; FAN‐CHIANG, M. H. Directed migration of Ascogregarina taiwanensis (Apicomplexa: Lecudinidae) in its natural host Aedes albopictus (Diptera: Culicidae). Journal of Eukaryotic Microbiology, Cincinnati, v. 48, p. 537-541, 2001.

CHEN, W. J.; HUANG, C. G.; FAN-CHIANG, M. H.; LIU, Y. H.; LEE, Y. F. Apoptosis of Ascogregarina taiwanensis (Apicomplexa: Lecudinidae), which failed to migrate within its natural host. Journal of Experimental Biology, Cambridge, v. 216, p. 230-235, 2013.

CHEN, W. J.; WU, S. T.; CHOW, C. Y.; YANG, C. H. Sporogonic development of the gregarine Ascogregarina taiwanensis (Lien and Levine) (Apicomplexa: Lecudinidae) in its natural host Aedes albopictus (Skuse) (Diptera: Culicidae). Journal of Eukaryotic Microbiology, Cincinnati, v. 44, p. 326-331, 1997.

CHEN, W. J.; YANG, C. H. Developmental synchrony of Ascogregarina taiwanensis (Apicomplexa: Lecudinidae) within Aedes albopictus (Diptera: Culicidae). Journal of Medical Entomology, Lanham, v. 33, p. 212-215, 1996.

CHOUIN-CARNEIRO, T.; VEGA-RUA, A.; VAZEILLE, M.; YEBAKIMA, A.; GIROD, R.; GOINDIN, D.; DUPONT-ROUZEYROL, M.; LOURENÇO-DE-OLIVEIRA, R.; FAILLOUX, A. B. Differential susceptibilities of Aedes aegypti and Aedes albopictus from the Americas to Zika Virus. PLOS Neglected Tropical Diseases, San Francisco, v. 3, p. e0004543, 2016.

CLOPTON, R. E. Order Eugregarinorida Léger 1900. In: LEE, J. J.; LEEDALE, G. F.; BRADBURY, P. (Ed.). The illustrated guide to the Protozoa. 2 ed. Lawrence: Allen Press, 2000. p. 213-214.

COMISKEY, N.; LOWRIE, R. C.; WESSON, D. M. Role of habitat components on the bionomics of Aedes albopictus (Diptera: Culicidae) from New Orleans. Journal of Medical Entomology, Lanham, v. 36, p. 313-320, 1999.

COPELAND, R. S.; CRAIG, G. B. Interspecific competition, parasitism, and predation affect development of Aedes hendersoni and A. triseriatus (Diptera, Culicidae) in artificial treeholes. Annals of the Entomological Society of America, Washington, v. 85, p. 154-163, 1992.

CRAIG, G. B. The diaspora of the Asian tiger mosquito. In: MCKNIGHT, B. N. (Ed.). Biological pollution: the control and impact of invasive exotic species. Indianapolis: Indiana Academic of Science, 1993. p. 101-120.

DELLAPE, M. E.; MARTI, G. A.; TRANCHIDA, M. C.; GARCIA, J. J. First record of Aedes aegypti (L.) (Diptera: Culicidae) infected by the parasite Ascogregarina culicis (Ross) (Apicomplexa: Lecudinidae) in Argentina. Entomología y Vectores, Rio de Janeiro, v. 12, p. 111-115, 2005.

DESPORTES, I. Systematics of terrestrial and freshwater gregarines In: DESPORTES, I.; SCHREVEL, J. (Ed.). Treatise on Zoology – Anatomy, taxonomy, biology, the gregarines. Vol. 2. Leiden: Koninklijke Brill NV, 2013. p. 7-195.

FANTINATTI, E.; DUQUE, J. E.; SILVA, A. M.; NAVARRO-SILVA, M. A. Abundance and aggregation egg of Aedes aegypti L. and Aedes albopictus (Skuse) (Diptera: Culicidae) in the north and northwest of the State of Paraná, Brazil. Neotropical Entomology, Piracicaba, v. 36, p. 960-965, 2007.

GANAPATI, P. N.; TATE, P. On the gregarine Lankesteria culicis (Ross), 1898, from the mosquito Aedes (Finlaya) geniculatus (Olivier). Parasitology, Cambridge, v. 39, p. 291-294, 1949.

GARCIA, G. A.; SANTOS, L. M.; VILLELA, D. A.; MACIEL-DE-FREITAS, R. Using Wolbachia releases to estimate Aedes aegypti (Diptera: Culicidae) population size and survival. PLoS One, Cambridge, v. 11, p. e0160196, 2016.

GARCIA, J. J.; FUKUDA, T.; BECNEL, J. J. Seasonality, prevalence, and pathogenicity of the gregarine Ascogregarina taiwanensis (Apicomplexa: Lecudinidae) is mosquitoes from Florida. Journal of the American Mosquito Control Association, Washington, v. 10, p. 413-418, 1994.

GENTILE, A. G.; FAY, R. W.; MCCRAY, M. The distribution, ethology and control potential of the Lankesteria culicis (Ross) – Aedes aegypti complex in southern United States. Mosquito News, Albany, v. 31, p. 12-17, 1971.

GOLSTEIN, P.; KROEMER, G. Cell death by necrosis: towards a molecular definition. Trends in Pharmacological Sciences, London, v. 32, p. 37-43, 2007.

GUBLER, D. J. Dengue, urbanization and globalization: the unholy trinity of the 21st century. Tropical Medicine and Health, Nagazaki, v. 39, p. 3-11, 2011.

GUENTHER, K. Uber eine gregarine in Ficalbia dofleini Guenther. Zoologischer Anzeiger, Berlin, v. 44, p. 264-267, 1914.

GUZMAN, M. G.; HARRIS, E. Dengue. Lancet, London, v. 385, p. 453-465, 2015.

HAUSMANN, K.; HÜLSMANN, N.; RADEK, R. Protistology. 3 ed. Stuttgart: E. Schweizerbartsche Buchhandlung (Nägele u. Obermiller), 2003. 379 p.

HAYES, G. R.; HAVERFIELD, L. E. Distribution and density of Aedes aegypti (L.) and Lankesteria culicis (Ross) in Louisiana and adjoining areas. Mosquito News, Albany, v. 31, p. 28-32, 1971.

HENRY, J. E. Natural and applied control of insects by protozoa. Annual Review of Entomology, Palo Alto, v. 26, p. 49-73, 1981.

HEUKELBACH, J.; ALENCAR, C. H.; KELVIN, A. A.; DE OLIVEIRA, W. K.; CAVALCANTI, L. P. G. Zika virus outbreak in Brazil. The Journal of Infection in Developing Countries, Viale San Pietro, v. 28, p. 116-120, 2016.

HUANG, C. G.; TSAI, K. H.; WU, W. J.; CHEN, W. J. Intestinal Expression of H+ V‐ATPase in the Mosquito Aedes albopictus is tightly associated with gregarine infection. Journal of Eukaryotic Microbiology, Cincinnati, v. 53, p. 127-135, 2006.

JONES, T. F.; CRAIG, A. S.; NASCI, R. S.; PATTERSON, L. E.; ERWIN, P. C.; GERHARDT, R. R.; USSERY, X. T.; SCHAFFNER, W. Newly recognized focus of La Crosse encephalitis in Tennessee. Clinical Infectious Diseases, Oxford, v. 28, p. 93-97, 1999.

KANDUC, D.; MITTELMAN, A.; SERPICO, R.; SINIGAGLIA, E.; SINHA, A. A.; NATALE, C.; SANTACROCE, R.; DI CORCIA, M. G.; LUCCHESE, A.; DINI, L.; PANI, P.; SANTACROCE, S.; SIMONE, S.; BUCCI, R.; FARBER, E. Cell death: apoptosis versus necrosis (review). International Journal of Oncology, London, v. 21, p. 165-170, 2002.

KRAEMER, M. U.; SINKA, M. E.; DUDA, K. A.; MYLNE, A.; SHEARER, F. M.; BRADY, O. J.; MESSINA, J. P.; BARKER, C. M.; MOORE, C. G.; CARVALHO, R. G.; COELHO, G. E.; VAN BORTEL, W.; HENDRICKX, G.; SCHAFFNER, F.; WINT, G. R.; ELYAZAR, I. R.; TENG, H. J.; HAY, S. I. The global compendium of Aedes aegypti and Ae. albopictus occurrence. Nature, London, v. 2, p. 150035, 2015.

KRAMAR, J. Hromadinka Lankesteria culicis Ross, parasitkomara Aedes (Finlaya) Geniculatus Oliv. Vestn. Ceskoslovenske Zool Spolecnosti, Praga, v. 16, p. 43-49, 1952.

LANTOVA, L.; VOLF, P. Mosquito and sand fly gregarines of the genus Ascogregarina and Psychodiella (Apicomplexa: Eugregarinorida, Aseptatorina) – Overview of their taxonomy, life cycle, host specificity and pathogenicity. Infection, Genetics and Evolution, Amsterdam, v. 28, p. 616-627, 2014.

LEANDER, B. S. Marine gregarines: evolutionary prelude to the apicomplexan radiation? Trends in Parasitology, Amsterdam, v. 24, p. 60-67, 2008.

LELES, R. N.; D’ALESSANDRO, W. B.; LUZ C. Effects of Metarhizium anisopliae conidia mixed with soil against the eggs of Aedes aegypti. Parasitology Research, Heidelberg, v. 110, p. 1579-1582, 2012.

LIEN, S.; LEVINE, N. D. Three new species of Ascocystis (Apicomplexa, Lecudinidae) from mosquitoes. Journal of Protozoology, Los Angeles, v. 27, p. 147-151, 1980.

LIMA-CAMARA, T. N. Emerging arboviruses and public health challenges in Brazil. Revista de Saúde Pública, São Paulo, v. 27, p. S0034-89102016000100602, 2016.

LOUNIBOS, L. P.; BARGIELOWSKI, I.; CARRASQUILLA, M. C.; NISHIMURA, N. Coexistence of Aedes aegypti and Aedes albopictus (Diptera: Culicidae) in Peninsular Florida two decades after competitive displacements. Journal of Medical Entomology, Honolulu, v. 53, p. 1385-1390, 2016.

LU, P.; BIAN, G.; PAN, X.; XI, Z. Wolbachia induces density-dependent inhibition to dengue virus in mosquito cells. PLOS Neglected Tropical Diseases, San Francisco, v. 6, p. e1754, 2012.

MARCHOUX, E.; SALIMBENI, A.; SIMOND, P. L. La fievre jaune. Rapport de lamission francaise. Annales de l’Institut Pasteur, Paris, v. 17, p. 665-673, 1903.

MCCRAY, E. M.; FAY, R. W.; SCHOOF, H. F. The bionomics of Lankesteria culicis and Aedes aegypti. Journal of Invertebrate Pathology, Riverside, v. 16, p. 42-53, 1970.

MONTERO, A. Chikungunya fever – A new global threat. Medicina Clínica, Madrid, v. 145, p. 118-123, 2015.

MORALES, M. E.; OCAMPO, C. B.; CADENA, H.; COPELAND, C. S.; TERMINI, M.; WESSON, D. M. Differential identification of Ascogregarina species (Apicomplexa: Lecudinidae) in Aedes aegypti and Aedes albopictus (Diptera: Culicidae) by polymerase chain reaction. Journal of Parasitology, Lawrence, v. 91, p. 1352-1356, 2005.

MORRISON, D. A. Evolution of the Apicomplexa: where are we now? Trends in Parasitology, Amsterdam, v. 25, p. 375-382, 2009.

MOURY, D. T.; SINGH, D. K.; YADAV, P.; GOKHALE, M. D.; BARDE, P. V.; NARAYAN, N. B.; THAKARE, J. P.; MISHRA, A. C.; SHOUCHE, Y. S. Role of gregarine parasite Ascogregarina culicis (Apicomplexa: Lecudinidae) in the maintenance of Chikungunya virus in vector mosquito. Journal of Eukaryotic Microbiology, Cincinnati, v. 50, p. 379-382, 2003.

MUNSTERMANN, L. E.; LEVINE, N. D. Ascogregarina geniculati sp. n. (Protozoa, Apicomplexa) from the mosquito Aedes geniculatus. Journal of Parasitology, Lawrence, v. 69, p. 769-772, 1983.

MUNSTERMANN, L. E.; WESSON, D. M. First record of Ascogregarina taiwanensis (Apicomplexa: Lecudinidae) in north American Aedes albopictus. Journal of the American Mosquito Control Association, Washington, v. 6, p. 235-243, 1990.

OTTA, D. A.; ROTT, M. B.; CARLESSO, A. M.; SILVA, O. S. Prevalence of Acanthamoeba spp. (Sarcomastigophora: Acanthamoebidae) in wild populations of Aedes aegypti (Diptera: Culicidae). Parasitology Research, Heidelberg, v. 111, p. 2017-2022, 2012.

PASSOS, R. A.; TADEI, W. P. Parasitism of Ascogregarina taiwanensis and Ascogregarina culicis (Apicomplexa: Lecudinidae) in larvae of Aedes albopictus and Aedes aegypti (Diptera: Culicidae) from Manaus, Amazon region, Brazil. Journal of Invertebrate Pathology, Riverside, v. 97, p. 230-236, 2008.

PILLAI, J. S.; NEILL, H. J. C.; SONE, P. F. Lankesteria culicis a gregarine parasite of Aedes polynesiensis in Western Samoa. Mosquito News, Albany, v. 36, p. 150-154, 1976.

PORTER, C. H.; DEFOLIART, G. R. Gonotrophic age, insemination, and Ascogregarina infection in a southern Wisconsin population of Aedes triseriatus. Journal of the American Mosquito Control Association, Washington, v. 1, p. 238-240, 1985.

PROPHIRO, J. S. Metodos alternativos para o controle fitoquimico e biologico de Aedes spp. Meigen, 1818 (Diptera: Culicidae). Tese (Doutorado em Ciências Biológicas - Entomologia) - Universidade Federal do Paraná, Curitiba. 2013.

PROPHIRO, J. S.; NUNES, T.; OLIVEIRA, J. G.; DANDOLINI, G. W.; SILVA, M. A. N.; SILVA, O. S. First registration and molecular characterization of Ascogregarina taiwanensis in Aedes albopictus and Aedes aegypti in Santa Catarina, south Brazil. Revista da Sociedade Brasileira de Medicina Tropical, Uberaba, 2017 (In press).

PROPHIRO, J. S.; SILVA, O. S.; LUNA, J. E. D.; PICCOLI, C. F.; KANIS, L. A.; SILVA, M. A. N. Aedes aegypti and Aedes albopictus (Diptera: Culicidae): coexistence and susceptibility to temephos, in municipalities with occurrence of dengue and differentiated characteristics of urbanization. Revista da Sociedade Brasileira de Medicina Tropical, Uberaba, v. 44, p. 300-305, 2011.

REEVES, W. K. Oviposition by Aedes aegypti (Diptera: Culicidae) in relation to conspecific larvae infected with internal symbiotes. Journal of Vector Ecology, Moscow, v. 29, p. 159-163, 2004.

REEVES, W. K.; MCCULLOUGH, S. D. Laboratory susceptibility of Wyeomyia smithii (Diptera: Culicidae) to Ascogregarina taiwanensis (Apicomplexa: Lecudinidae). Journal of Eukaryotic Microbiology, Cincinnati, v. 49, p. 391-392, 2002.

REINERT, J. F. New classification for the composite genus Aedes (Diptera: Culicidae: Aedini), elevation of subgenus Ochlerotatus to generic rank, reclassification of the other subgenera, and notes on certain subgenera and species. Journal of the American Mosquito Control Association, Washington, v. 16, p. 175-188, 2000.

REYES-VILLANUEVA, F.; BECNEL, J. J.; BUTLER, J. F. Morphological traits for distinguishing extracellular gamonts of Ascogregarina culicis and Ascogregarina taiwanensis in Aedes aegypti and Aedes albopictus. Journal of Invertebrate Pathology, Riverside, v. 77, p. 227-229, 2001.

REYES-VILLANUEVA, F.; BECNEL, J. J.; BUTLER, J. F. Susceptibility of Aedes aegypti and Aedes albopictus larvae to Ascogregarina culicis and Ascogregarina taiwanensis (Apicomplexa: Lecudinidae) from Florida. Journal of Invertebrate Pathology, Riverside, v. 84, p. 47-53, 2003.

REYES-VILLANUEVA, F.; GARZA-HERNANDEZ, J. A.; GARCIA-MUNGUIA, A. M.; HOWARD, A. F.; ORTEGA-MORALES, A. I.; ADELEKE, M. A.; RODRIGUEZ-PEREZ, M. A. Aedes albopictus in northeast Mexico: An update on adult distribution and first report of parasitism by Ascogregarina taiwanensis. Journal of Vector Borne Diseases, New Delhi, v. 50, p. 202-205, 2013.

ROSS, R. Report on preliminary investigation into malaria in Sigur Ghat, Ootacamund. Transactions of the South Indian Branch of the British Medical Association, London, v. 8, p. 143-152, 1898.

ROYCHOUDHURY, S.; ISAWA, H.; HOSHINO, K.; SASAKI, T.; SAITO, N.; SAWABE, K.; KOBAYASHI, M. Comparison of the morphology of oocysts and the phylogenetic analysis of four Ascogregarina species (Eugregarinidae: Lecudinidae) as inferred from small subunit ribosomal DNA sequences. Parasitology International, Amsterdam, v. 56, p. 113-118, 2007a.

ROYCHOUDHURY, S.; ISAWA, H.; HOSHINO, K.; SASAKI, T.; SAITO, N.; SAWABE, K.; KOBAYASHI, M. The new species of Ascogregarina from Ochlerotatus japonicus japonicas. Medical Entomology and Zoology, Tokyo, v. 58, p. A06, 2007b.

ROYCHOUDHURY, S.; KOBAYASHI, M. New findings on the developmental process of Ascogregarina taiwanensis and Ascogregarina culicis in Aedes albopictus and Aedes aegypti. Journal of the American Mosquito Control Association, Washington, v. 22, p. 29-36, 2006.

SALOKHE, S. G.; DESHPANDE, S. G.; MUKHERJEE, S. N. Evaluation of the insect growth regulator Lufenuron (Match®) for control of Aedes aegypti by simulated field trials. Parasitology Research, Heidelberg, v. 111, p. 1325-1329, 2012.

SÁNCHEZ-TRINIDAD, A.; ORDOÑEZ-SÁNCHEZ, F.; VALDES-PEREZGASGA, M. T.; SÁNCHEZ-RAMOS, F. J.; ZAVORTINK, T. J.; CORTÉS-GUZMÁN, A. J.; ORTEGA-MORALES, A. I. Geographical distribution of the Aedes triseriatus Group (Diptera: Culicidae) in Mexico. Journal of Vector Ecology, Moscow, v. 39, p. 134-137, 2014.

SANDERS, R. D.; POINAR, G. O. Fine structure and life cycle of Lankesteria clarki sp. n. (Sporozoa: Eugregarinida) parasitic in the mosquito Aedes sierrensis (Ludlow). Journal of Protozoology, Los Angeles, v. 20, p. 594-602, 1973.

SILVA, O. S.; PRADO, G. R.; DA SILVA, J. L.; SILVA, C. E.; DA COSTA, M.; HEERMANN, R. Oral toxicity of Photorhabdus luminescens and Xenorhabdus nematophila (Enterobacteriaceae) against Aedes aegypti (Diptera: Culicidae). Parasitology Research, Heidelberg, v. 112, p. 2891-2896, 2013.

SMITH, L. B.; KASAI, S.; SCOTT, J. G. Pyrethroid resistance in Aedes aegypti and Aedes albopictus: Important mosquito vectors of human diseases. Pesticide Biochemistry and Physiology, Amherst, v. 133, p. 1-12, 2016.

SPENCER, J. P.; OLSON, J. K. Evaluation of the combined effects of methoprene and the protozoan parasite Ascogregarina culicis (Eugregarinida, Diplocystidae), on Aedes mosquitoes. Mosquito News, Albany, v. 42, p. 384-390, 1982.

STAPLES, J. E.; FISCHER, M. Chikungunya virus in the Americas – What a vector borne pathogen can do. The New England Journal of Medicine, Boston, v. 371, p. 887-889, 2014.

STAPP, R. R.; GASTEN, J. Field studies on Lankesteria culicis and Aedes aegypti in Florida. Mosquito News, Albany, v. 31, p. 18-22, 1971.

SULAIMAN, I. Infectivity and pathogenicity of Ascogregarina culicis (Eugregarinida: Lecudinidae) to Aedes aegypti (Diptera: culicidae). Journal of Medical Entomology, Lanham, v. 29, p. 1-4, 1992.

TROUT FRYXELL, R. T.; FREYMAN, K.; ULLOA, A.; HENDRICKS, B.; PAULSEN, D.; ODOI, A.; MONCAYO, A. Cemeteries are effective sites for monitoring la crosse virus (LACv) and these environments may play a role in LACv infection. PloS One, Cambridge, v. 10, n. 4, e0122895, 2015.

TSENG, M. Ascogregarine parasites as possible biocontrol agents of mosquitoes. Journal of the American Mosquito Control Association, Washington, v. 23, p. 30-34, 2007.

VAN RHEIN, S. L.; FLANARY, B. E.; JULIANO, S. A. Effects of habitat type and drying on Ascogregarina barretti (Eugregarinida: Lecudinidae) infection in Aedes triseritatus (Diptera: Culicidae). Journal of Medical Entomology, Lanham, v. 37, p. 950-956, 2000.

VAVRA, J. Lankesteria barretti n. sp. (Eugregarinida, Diplocystidae), a parasite of the mosquito Aedes triseriatus (Say) and a review of the genus Lankesteria Mingazzini. Journal of Protozoology, Los Angeles, v. 16, p. 546-570, 1969.

VEZZANI, D.; WISNIVESKY, C. Prevalence and seasonality of Ascogregarina culicis (Apicomplexa: Lecudinidae) in natural populations of Aedes aegypti (Diptera: Culicidae) from temperate Argentina. Journal of Invertebrate Pathology, Riverside, v. 91,p. 183-187, 2006.

VIEIRA, C. J.; SILVA, D. J.; BARRETO, E. S.; SIQUEIRA, C. E.; COLOMBO, T. E.; OZANIC, K.; SCHMIDT, D. J.; DRUMOND, B. P.; MONDINI, A.; NOGUEIRA, M. L.; BRONZONI, R. V. Detection of Mayaro virus infections during a dengue outbreak in Mato Grosso, Brazil. Acta Tropica, Amsterdam, v. 147, p. 12-16, 2015.

VIVIER, E.; DESPORTES, I. Phylum Apicomplexa. In: MARGULIS, L.; CORLISS, J. O.; MELKONIAN, M.; CHAPMAN, D. J. (Ed.). The hand book of Protoctista. Boston: Jones and Bartlett, 1990. p. 1-21.

VOTÝPKA, J.; LANTOVA, L.; GHOSH, K.; BRAIG, H.; VOLF, P. Molecular characterization of gregarines from sand flies (Diptera: Psychodidae) and description of Psychodiella ng (Apicomplexa: Gregarinida). Journal of Eukaryotic Microbiology, Cincinnati, v. 56, p. 583-588, 2009.

WALKER, E. D.; POIRIER, S. J.; VELDMAN, W. T. Effects of Ascogregarina barretti (Eugregarinida: Lecudinidae) infection on emergence success, development time, and size of Aedes triseriatus (Diptera: Culicidae) in microcosms and tires. Journal of Medical Entomology, Lanham, v. 24, p. 303-309, 1987.

WALSH, R. D.; OLSON, J. K. Observations on the susceptibility of certain mosquito species to infection by Lankesteria culicis (Ross). Mosquito News, Albany, v. 36, p. 536-545, 1976.

WEAVER, S. C.; FORRESTER, N. L. Chikungunya: Evolutionary history and recent epidemic spread. Antiviral Research, Leuven, v. 120, p. 32-33, 2015.

WENYON, C. M. Oriental sore in Bagdad, together with observations on a gregarine in Stegomyia fasciata, the haemogregarine of dogs and the flagellates of house flies. Parasitology, Cambridge, v. 4, p. 273-344, 1911.

WESTBY, K. M.; FRITZEN, C.; PAULSEN, D.; POINDEXTER, S.; MONCAYO, A. C. La Crosse Encephalitis Virus Infection in field-collected Aedes albopictus, Aedes japonicus, and Aedes triseriatus in Tennessee. Journal of the American Mosquito Control Association, Washington, v. 31, p. 233-241, 2015.

WETZEL, D. M.; HÅKANSSON, S.; HU, K.; ROOS, D.; SIBLEY, L. D. Actin filament polymerization regulates gliding motility by apicomplexan parasites. Molecular Biology of the Cell, Bethesda, v. 14, p. 396-406, 2003.

YEH, M. L.; CHEN, C. S.; LIU, K. C. Experimental infection of mosquitoes with two Ascogregarina species (Eugregarinida: Lecudinidae). Bulletin of Tung Hai University, Taichung City, v. 35, p. 87-106, 1994.

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2018-09-17

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