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Spatial clustering and longitudinal variation of Anopheles darlingi (Diptera: Culicidae) larvae in a river of the Amazon: the importance of the forest fringe and of obstructions to flow in frontier malaria

Published online by Cambridge University Press:  01 July 2011

F.S.M. Barros ,
M.E. Arruda ,
H.C. Gurgel  and
N.A. Honório
F.S.M. Barros*
Affiliation:
Departamento de Zoologia, Universidade Federal de Pernambuco, Recife-PE, Brazil
M.E. Arruda
Affiliation:
Laboratório de Imunoepidemiologia, Centro de Pesquisas Aggeu Magalhães, Fundação Oswaldo Cruz, Recife, PE, Brazil
H.C. Gurgel
Affiliation:
Secretaria de Diversidade e Floresta, Ministério do Meio Ambiente, Brasília-DF, Brazil
N.A. Honório
Affiliation:
Laboratório de Transmissores de Hematozoários, Departamento de Entomologia, Instituto Oswaldo Cruz-Fiocruz, Rio de Janeiro, RJ, Brazil
*
*Author for correspondence Fax: +55 81 21268353 E-mail: fsaito1@yahoo.com.br
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Abstract

Deforestation has been linked to a rise in malaria prevalence. In this paper, we studied longitudinally 20 spots, including forested and deforested portions of a temporary river in a malarigenous frontier zone. Larval habitat parameters influencing distribution of Anopheles darlingi (Diptera: Culicidae) larvae were studied. We observed that larvae were clustered in forested-deforested transitions. For the first time in the literature, it was verified that parameters determining larval distribution varied from deforested to forested areas. The proximity to human dwellings was also a significant factor determining distribution, but larvae was most importantly associated with a previously undescribed parameter, the presence of small obstructions to river flow, such as tree trunks within the river channel, which caused pooling of water during the dry season (‘microdams’). In deforested areas, the most important factor determining distribution of larvae was shade (reduced luminance). Larvae were absent in the entire studied area during the wet season and present in most sites during the dry season. During the wet-dry transition, larvae were found sooner in areas with microdams, than in other areas, suggesting that flow obstruction prolongs the breeding season of An. darlingi. Adult mosquito densities and malaria incidence were higher during the dry season. Our data correlate well with the published literature, including the distribution of malaria cases near the forest fringes, and has permitted the creation of a model of An. darlingi breeding, where preference for sites with reduced luminance, human presence and microdams would interact to determine larval distribution.

Keywords

Anopheles darlingbreedingmalarialarvaedeforestationAmazonfrontier zones
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 101 , Issue 6 , December 2011 , pp. 643 - 658
Copyright
Copyright © Cambridge University Press 2011

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References

Achee, N.L., Grieco, J.P., Andre, R.G., Roberts, D.R. & Rejmankova, E. (2006) Experimental evaluation of overhanging bamboo in Anopheles darlingi larval habitat selection in Belize, Central America. Journal of Vector Ecology 31, 145–151.CrossRefGoogle ScholarPubMed
Alemayehu, T., Ye-ebiyo, Y., Ghebreyesus, T.A., Witten, K.H., Bosman, A. & Tekle-haimanot, A. (1998) Malaria, schistosomiasis, and intestinal parasites in relation to microdams in Tigray, Northern Ethiopia. Parassitologia 40, 259–267.Google ScholarPubMed
Barros, F.S.M. & Honório, N.A. (2007) Man biting rate seasonal variation of malaria vectors in Roraima, Brazil. Memórias do Instituto Oswaldo Cruz 102, 299–302.CrossRefGoogle Scholar
Barros, F.S.M., Vasconcelos, S.D., Arruda, M.E., Confalonieri, U., Luitgards-Moura, J.F. & Honório, N.A. (2006) Tetrahymenidae infection in mosquito populations in a malaria-endemic region of the Amazon. Journal of Invertebrate Pathology 91, 199–201.CrossRefGoogle Scholar
Barros, F.S.M., Aguiar, D.B., Rosa-Freitas, M.G., Luitgards-Moura, J.F., Gurgel, H.C., Honório, N.A., Arruda, M.E., Tsouris, P. & Vasconcelos, S.D. (2007a) Distribution summaries of malaria vectors in the Northern Brazilian Amazon. Journal of Vector Ecology 32, 161–167.CrossRefGoogle ScholarPubMed
Barros, F.S.M., Arruda, M.E., Vasconcelos, S.D., Luitgards-Moura, J.F., Confalonieri, U., Rosa-Freitas, M.G., Tsouris, P., Lima-Camara, T. & Honório, N.A. (2007b) Parity and age composition for Anopheles darlingi Root (Diptera: Culicidae) and Anopheles albitarsis Lynch-Arribálzaga (Diptera: Culicidae) of the northern Amazon Basin, Brazil. Journal of Vector Ecology 32, 1–15.CrossRefGoogle Scholar
Barros, F.S.M., Arruda, M.E. & Honório, N.A. (2010) Mosquito Anthropophily: Implications on Malaria Transmission in the Northern Brazilian Amazon. Neotropical Entomology 39, 1039–1043.CrossRefGoogle ScholarPubMed
Barros, F.S.M., Honório, N.A. & Arruda, M.E. (2011) Temporal and spatial distribution of malaria within an agricultural settlement of the Brazilian Amazon. Journal of Vector Ecology 36, 159–169.CrossRefGoogle ScholarPubMed
Brochero, H.L., Rey, G., Buitrago, L.S. & Olano, V. (2005) Biting activity and breeding sites of Anopheles species in the municipality Villavicencio, Meta, Colombia. Journal of the American Mosquito Control Association 21, 182–186.CrossRefGoogle ScholarPubMed
Camargo, L.M., dal Colletto, G.M., Ferreira, M.U., Gurgel, S., Escobar, A.L., Marques, A., Krieger, H., Camargo, E.P. & Silva, L.H.P. (1996) Hypoendemic malaria in Rondonia (Brazil, western Amazon region): seasonal variation and risk groups in an urban locality. American Journal of Tropical Medicine and Hygiene 55, 32–38.CrossRefGoogle Scholar
Cattell, R.B. (1966) Higher order factor structure and reticular vs. hierarchical formulae for their interpretation. pp. 223–266 in Banks, C. & Broadhurst, P.L. (Eds) Studies in Psychology. London, UK, University of London Press.Google Scholar
Charlwood, J.D. (1980) Observations on the bionomics of Anopheles darlingi Root (Diptera: Culicidae) from Amazonas, Brazil. Bulletin of Entomological Research 70, 685–692.CrossRefGoogle Scholar
Charlwood, J.D. (1996) Biological variation in Anopheles darlingi Root. Memórias do Instituto Oswaldo Cruz 91, 391–398.CrossRefGoogle ScholarPubMed
Chaves, S.S. & Rodrigues, L.C. (2000) An initial examination of the epidemiology of malaria in the state of Roraima, in the Brazilian Amazon basin. Revista do Instituto de Medicina Tropical de São Paulo 42, 269–275.CrossRefGoogle ScholarPubMed
Consoli, R.A.G.B. & Lourenço-de-Oliveira, R. (1994) Principais Mosquitos de Importância Sanitária no Brasil. Rio de Janeiro, Brazil, Fiocruz.CrossRefGoogle Scholar
Cruz, R.M.B., Gil, L.H.S., Silva, A.A., Araújo, S.A. & Katsuragawa, T.H. (2009) Mosquito abundance and behavior in the influence area of the hydroelectric complex on the Madeira River, western Amazon, Brazil. Transactions of the Royal Society of Tropical Medicine and Hygiene 103, 1174–1176.CrossRefGoogle ScholarPubMed
de Castro, M.C., Monte-Mor, R.L., Sawyer, D.O. & Singer, B.H. (2006) Malaria risk on the Amazon frontier. Proceedings of the National Academy of Sciences USA 103, 2452–2457.CrossRefGoogle ScholarPubMed
Deane, L.M., Causey, O.R. & Deane, M.P. (1948) Notas sobre a distribuição e a biologia dos anofelinos das regiões nordestina e amazônica do Brasil. Revista do Serviço Especial de Saúde Pública 1, 827–966.Google Scholar
Detinova, T.S. (1962) Age-grouping methods in Diptera of medical importance. WHO, Monographic series no. 47.Google Scholar
Dias, R.C. (2003) Uma contribuição ao estudo da malária no estado de Roraima e sua associação com a precipitação pluviométrica no período de 1985 a 1996. PhD thesis. Escola Nacional de Saúde Pública, Fundação Oswaldo Cruz, Rio de Janeiro, Brazil.Google Scholar
Divari, N.B. & Plotnikova, L.I. (1966) Computed brightness of the twilight sky. Soviet Astronomy 9, 840–851.Google Scholar
Furley, P.A. (1994) The Forest Frontier. London, UK, Routledge.CrossRefGoogle Scholar
Gil, L.H.S., Alves, F.P., Zieler, H., Salcedo, J.M.V., Durlacher, R.R., Cunha, R.P.A., Tada, M.S., Camargo, L.M.A., Camargo, E.P. & Pereira da Silva, L.H. (2003) Seasonal malaria transmission and variation of anopheline density in two distinct endemic areas in Brazilian Amazon. Journal of Medical Entomology 40, 636–641.CrossRefGoogle Scholar
Gomes, A.C., Paula, M.B., Natal, D. & Gotlieb, S.L.D. (2010) Ecologia de Anopheles (Nyssorhynchus) darlingi Root em área de implantação de empreendimento hidrelétrico, na divisa dos Estados do Mato Grosso do Sul e São Paulo. Revista da Sociedade Brasileira de Medicina Tropical 43, 272–276.CrossRefGoogle Scholar
Gorham, J.R., Stojanovic, C.J. & Scott, H.G. (1973) Illustrated Key to the Anopheline Mosquitoes of Western South America. Mosquito Systematics 5, 97–156.Google Scholar
Guarda, J.A., Sayag, C.R. & Witzig, R. (1999) Malaria reemergence in the Peruvian Amazon region. Emerging Infectious Diseases 5, 209–215.CrossRefGoogle Scholar
Hatcher, L.H. & Stepanski, E.J. (1994) A Step-by-Step Approach to Using the SAS System for Univariate and Multivariate Statistics. Cary, NC, USA, SAS Institute Inc.Google Scholar
Holm, S. (1979) A simple sequentially rejective multiple test procedure. Scandinavian Journal of Statistics 6, 65–70.Google Scholar
Hudson, J. (1984). Anopheles darlingi Root (Diptera, Culicidae) in the Suriname rainforest. Bulletin of Entomological Research 74, 129–142.CrossRefGoogle Scholar
Iles, T.C. (1993) Multiple regression. pp. 127–172 in Fry, J.C. (Ed.) Biological Data Analysis. Oxford, UK, Oxford University Press.CrossRefGoogle Scholar
Klein, T.A. & Lima, J.B.P. (1990) Seasonal distribution and biting patterns of Anopheles mosquitoes in Costa Marques, Rondonia, Brazil. Journal of the American Mosquito Control Association 6, 700–707.Google Scholar
Komp, W.H.W. (1942) The anopheline mosquitoes of the Caribbean region. Washington. Bulletin of the National Institute of Health 179, 1–195.Google Scholar
Kulldorff, M. (1997) Bernoulli, Discrete, Poisson and Continuous Models: A Spatial Scan Statistic. Communications in Statistics: Theory and Methods 26, 1481–1496.CrossRefGoogle Scholar
Kulldorff, M. & Nagarwalla, N. (1995) Spatial disease clusters: detection and inference. Statistics in Medicine 14, 799–819.CrossRefGoogle ScholarPubMed
León, W., Valle, J., Naupay, R., Tineo, E., Rosas, A. & Palomino, M. (2003) Comportamiento estacional del Anopheles (Nyssorhynchus) darlingi Root 1926 en localidades de Loreto y Madre de Díos, Perú 1999–2000. Revista Peruana de Medicina Experimental e Salud Pública 20, 22–27.Google Scholar
Magris, M., Rubio-Palis, Y., Menares, C. & Villegas, L. (2007) Vector bionomics and malaria transmission in the Upper Orinoco River, Southern Venezuela. Memórias do Instituto Oswaldo Cruz 102, 303–312.CrossRefGoogle ScholarPubMed
Manguin, S., Roberts, D.R., Andre, R.G., Rejmankova, E. & Hakre, S. (1996) Characterization of Anopheles darlingi (Diptera: Culicidae) larval habitats in Belize, Central America. Journal of Medical Entomology 33, 205–211.CrossRefGoogle ScholarPubMed
Menach, A.L., McKenzie, F.E., Flahault, A. & Smith, D.L. (2005) The unexpected importance of mosquito oviposition behaviour for malaria: non-productive larval habitats can be sources for malaria transmission. Malaria Journal 4, 23.CrossRefGoogle ScholarPubMed
Moreno, J., Rubio-Palis, Y. & Acevedo, P. (2000) Identificación de criaderos de anofelinos en un área endémica del estado Bolívar, Venezuela. Boletín de Malariolgía e Salud Ambiental 40, 21–30.Google Scholar
Oliveira-Ferreira, J.R., Lourenço-de-Oliveira, R., Teva, A., Deane, L.M. & Ribeiro, C.T. (1990) Natural malaria infections in anophelines in Rondonia State, Brazilian Amazon. American Journal of Tropical Medicine and Hygiene 43, 6–10.CrossRefGoogle ScholarPubMed
Olson, S.H., Gangnon, R., Silveira, G.A. & Patz, J.A. (2010) Deforestation and Malaria in Mâncio Lima County, Brazil. Emerging Infectious Diseases 16, 1108–1115.CrossRefGoogle ScholarPubMed
Paaijmans, K.P., Wandago, M.O., Githeko, A.K. & Takken, W. (2007) Unexpected high losses of Anopheles gambiae larvae due to rainfall. PLoS ONE 2(11), e1146.CrossRefGoogle ScholarPubMed
Roberts, D.R., Manguin, S., Harbach, R.E., Woodruff, R., Rejmankova, E., Polanco, J. & Wullschleger, B. (1996) Predictions of malaria vector distributions in Belize based on multispectral satellite data. American Journal of Tropical Medicine and Hygiene 54, 302–308.CrossRefGoogle ScholarPubMed
Roberts, D.R., Manguin, S., Rejmankova, E., Andre, R., Harbach, R.E., Vanzie, E., Kakre, S. & Polanco, J. (2002) Spatial distribution of adult Anopheles darlingi and An. albimanus in relation to riparian habitats in Belize, Central America. Journal of Vector Ecology 27, 21–30.Google Scholar
Rosa-Freitas, M.G., Tsouris, P., Peterson, A.T., Honório, N.A., Barros, F.S.M., Aguiar, D.B., Gurgel, H.C., Arruda, M.E., Vasconcelos, S.D. & Luitgards-Moura, J.F. (2007) An ecoregional classification for the State of Roraima, Brazil. The importance of landscape in malaria biology. Memórias do Instituto Oswaldo Cruz 102, 349–356.CrossRefGoogle ScholarPubMed
Rozendaal, J.A. (1990) Observations on the distribution of anophelines in Suriname with particular reference to the malaria vector Anopheles darlingi. Memórias do Instituto Oswaldo Cruz 85, 221–234.CrossRefGoogle Scholar
Rozendaal, J.A. (1992) Relations between Anopheles darlingi breeding habits, rainfall, river level and malaria transmission rates in the rain forest of Suriname. Medical Veterinary Entomology 6, 16–22.CrossRefGoogle Scholar
Russell, P.F. & Rao, T.R. (1942) On the swarming, mating and ovipositing behaviour of An. culifacies. American Journal of Tropical Medicine and Hygiene 22, 417.CrossRefGoogle Scholar
Russell, P.F., West, L.S., Manwell, R.D. & MacDonald, G. (1963) Practical Malariology. London, UK, Oxford University Press.Google Scholar
Sawyer, D.R. (1988) Frontier Malaria in the Amazon Region of Brazil: Types of Malaria Situations and Some Implications for Control. Brasília, Pan American Health Organization/WHO/Special Programme for Research Training in Tropical Diseases.Google Scholar
Service, M.W. (1991) Agricultural development and arthropod-borne diseases: a review. Revista de Saúde Pública 25, 165–178.CrossRefGoogle ScholarPubMed
Silva, A.P.B., Tadei, W.P. & Santos, J.M.M. (2010) Genetic variability in populations of Anopheles darlingi(Diptera: Culicidae) and relationship to biting activity behavior as analyzed by RAPD. Acta Amazônica 40, 585–590.CrossRefGoogle Scholar
Silva, N.S., Silva-Nunes, M., Malafronte, R.S., Menezes, M.J., D'Arcadia, R.R., Komatsu, N.T., Scopel, K.K., Braga, E.M., Cavasini, C.E., Cordeiro, J.A. & Ferreira, U.M. (2010) Epidemiology and control of frontier malaria in Brazil: lessons from community-based studies in rural Amazonia. Transactions of the Royal Society of Tropical Medicine and Hygiene 104, 343–350.CrossRefGoogle ScholarPubMed
Silva-Nunes, M., Codeço, C.T., Malafronte, R.S., Silva, N.S., Juncansen, C., Muniz, P.T. & Ferreira, M.U. (2008) Malaria on the Amazonian frontier: transmission dynamics, risk factors, spatial distribution, and prospects for control. American Journal of Tropical Medicine and Hygiene 79, 624–635.CrossRefGoogle ScholarPubMed
Singer, B.H. & de Castro, M.C. (2001) Agricultural colonization and malaria on the Amazon frontier. Annals of the New York Academy of Sciences 954, 184–222.CrossRefGoogle ScholarPubMed
Singer, B. & de Castro, M.C. (2006) Enhancement and suppression of malaria in the Amazon. American Journal of Tropical Medicine and Hygiene 74, 1–2.CrossRefGoogle ScholarPubMed
Souza-Santos, R. (2002) Distribuição sazonal de vetores da malária em Machadinho d'Oeste, Rondônia, Região Amazônica, Brasil. Cadernos de Saúde Pública 18, 1813–1818.CrossRefGoogle Scholar
Tadei, W.P. & Thatcher, B.D. (2000) Malaria vectors in the Brazilian Amazon: Anopheles of the subgenus Nyssorhynchus. Revista do Instituto de Medicina Tropical de São Paulo 42, 87–94.CrossRefGoogle ScholarPubMed
Tadei, W.P., Mascarenhas, B.M. & Podestá, M.G. (1983) Biologia de anofelinos amazônicos VIII. Conhecimentos sobre a distribuição de espécies de Anopheles na região de Tucuruí-Marabá (Pará). Acta Amazônica 13, 103–140.CrossRefGoogle Scholar
Tadei, W.P., Santos, J.M.M., Costa, W.L.S. & Scardana, V.M. (1988) Biologia dos anofelinos amazônicos. XII. Ocorrência de espécies de Anopheles, dinâmica da transmissão e controle da malária na zona urbana de Ariquemes, Rondônia. Revista do Instituto de Medicina Tropical de São Paulo 30, 221–251.CrossRefGoogle Scholar
Tadei, W.P., Santos, J.M.M., Scarpassa, V.M. & Rodrigues, I.B. (1993) Incidência, distribuição e aspectos ecológicos de espécies de Anopheles (Diptera: Culicidae), em regiões naturais e sob impacto ambiental da Amazônia brasileira. pp. 167–196 in Ferreira, E.J.G., Santos, G.M., Leão, E.L.M. & Oliveira, L.A. (Eds) Bases Científicas para Estratégias de Preservação e Desenvolvimento da Amazônia, vol. 2. Manaus, Amazonas, Brazil, Instituto Nacional de Pesquisas da Amazônia.Google Scholar
Tadei, W.P., Thatcher, B.D., Santos, J.M.M., Scarpassa, V.M., Rodrigues, I.B. & Rafael, M.S. (1998) Ecologic observations on anopheline vectors of malaria in the Brazilian Amazon. American Journal of Tropical Medicine and Hygiene 59, 325–335.CrossRefGoogle ScholarPubMed
Tineo, E., Medina, A., Fallaque, C., Chávez, L., Quispe, S., Mercado, M., Zevallos, J., León, W. & Palomino, M. (2003) Distribución geográfica y comportamiento estacional de la picadura Del Anopheles (Nyssorhynchus) darlingi Root 1926 en localidades de la frontera Perú-Bolivia, Madre de Díos, Perú. Revista Peruana de Medicina Experimental e Salud Pública 20, 78–83.Google Scholar
Vasconcelos, C.H., Novo, E.M. & Donalisio, M.R. (2006) Use of remote sensing to study the influence of environmental changes on malaria distribution in the Brazilian Amazon. Cadernos de Saúde Pública 22, 517–526.CrossRefGoogle Scholar
Vittor, A.Y., Gilman, R., Tielsch, J., Glass, G., Shields, T. & Patz, J.A. (2002) Deforestation and the presence of Anopheles darlingi larvae in the Peruvian Amazon. PhD thesis, John Hopkins Bloomberg School of Public Health, Baltimore, MD, USA.Google Scholar
Vittor, R., Gilman, J., Tielsch, J., Glass, G., Shields, T., Lozano, W.S., Cancino, V.P. & Patz, J.A. (2006) The effect of deforestation on the human-biting rate of Anopheles darlingi, the primary vector of falciparum malaria in the Peruvian Amazon. American Journal of Tropical Medicine and Hygiene 74, 3–11.CrossRefGoogle ScholarPubMed
Vittor, A.Y., Pan, W., Gilman, R.H., Tielsch, J., Glass, G., Shields, T., Sánchez-Lozano, W., Pinedo, V.V., Salas-Cobos, E., Flores, S. & Patz, J.A. (2009) Linking Deforestation to Malaria in the Amazon: Characterization of the Breeding Habitat of the Principal Malaria Vector, Anopheles darling. American Journal of Tropical Medicine and Hygiene 81, 5–12.Google Scholar
Yasuoka, J. & Levins, R. (2007) Impact of deforestation and agricultural development on anopheline ecology and malaria epidemiology. American Journal of Tropical Medicine and Hygiene 76, 450–460.CrossRefGoogle ScholarPubMed
Zeilhofer, P., Santos, E.S., Ribeiro, A.L.M., Miyazaki, R.D. & Santos, M.A. (2007) Habitat suitability mapping of Anopheles darlingi in the surroundings of the Manso hydropower plant reservoir, Mato Grosso, Central Brazil. Internacional Journal of Health Geographics 7, 6–7.Google Scholar