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Tree hole mosquito species composition and relative abundances differ between urban and adjacent forest habitats in northwestern Argentina

Published online by Cambridge University Press:  03 August 2017

C. Mangudo ,
J.P. Aparicio ,
G.C. Rossi  and
R.M. Gleiser
C. Mangudo
Affiliation:
Instituto de Investigaciones en Energía No Convencional (INENCO, UNSa-CONICET), Universidad Nacional de Salta, Salta, Argentina Instituto de Investigaciones en Enfermedades Tropicales, Sede Regional Orán, Universidad Nacional de Salta, Salta, Argentina
J.P. Aparicio
Affiliation:
Instituto de Investigaciones en Energía No Convencional (INENCO, UNSa-CONICET), Universidad Nacional de Salta, Salta, Argentina Instituto de Investigaciones en Enfermedades Tropicales, Sede Regional Orán, Universidad Nacional de Salta, Salta, Argentina Mathematical, Computational and Modeling Sciences Center, Arizona State University, Tempe, United States
G.C. Rossi
Affiliation:
CEPAVE-Centro de Estudios Parasitológicos y de Vectores, CCT La Plata, CONICET-UNLP, La Plata, Argentina
R.M. Gleiser*
Affiliation:
Facultad de Ciencias Agropecuarias, Centro de Relevamiento y Evaluación de Recursos Agrícolas y Naturales-IMBIV (CONICET-UNC), Córdoba, Argentina Facultad de Ciencias Exactas, Físicas y Naturales, Cátedra de Ecología, Universidad Nacional de Córdoba, Córdoba, Argentina
*
*Author for correspondence: Phone: +54 (0351) 4334105/16/17 Fax: +54 (0351) 4334118 E-mail: raquel.gleiser@unc.edu.ar
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Abstract

Water-holding tree holes are main larval habitats for many pathogen vectors, especially mosquitoes (Diptera: Culicidae). Along 3 years, the diversity and composition of mosquito species in tree holes of two neighbouring but completely different environments, a city and its adjacent forest, were compared using generalized linear mixed models, PERMANOVA, SIMPER and species association indexes. The city area (Northwest Argentina) is highly relevant epidemiologically due to the presence of Aedes aegypti L. (main dengue vector) and occurrence of dengue outbreaks; the Yungas rainforests are highly biologically diverse. In total seven mosquito species were recorded, in descending order of abundance: Ae. aegypti, Haemagogus spegazzinii Brèthes, Sabethes purpureus (Theobald), Toxorhynchites guadeloupensis Dyar and Knab, Aedes terrens Walker, Haemagogus leucocelaenus Dyar & Shannon and Sabethes petrocchiae (Shannon and Del Ponte). The seven mosquito species were recorded in both city sites and forested areas; however, their mosquito communities significantly diverged because of marked differences in the frequency and relative abundance of some species: Tx. guadeloupensis and Ae. aegypti were significantly more abundant in forest and urban areas, respectively. Positive significant associations were detected between Ae. aegypti, Hg. spegazzinii and Hg. leucocelaenus. The combined presence of Ae. aegypti, Haemagogus and Sabethes in the area also highlight a potential risk of yellow fever epidemics. Overall results show an impoverished tree hole mosquito fauna in urban environments, reflecting negative effects of urbanization on mosquito diversity.

Keywords

Culicidaeecologyinterspecific associationphytotelmatavectorYungas rainforest
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 108 , Issue 2 , April 2018 , pp. 203 - 212
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Copyright © Cambridge University Press 2017 

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References

Alencar, J., Gleiser, R.M., Morone, F., Mello, C.F., Silva, J.S., Serra-Freire, N.M. & Guimarães, A.É. (2014) A comparative study of the effect of multiple immersions on Aedini (Diptera: Culicidae) mosquito eggs with emphasis on sylvan vectors of yellow fever virus. Memorias do Instituto Oswaldo Cruz 109, 114–117.Google Scholar
Alencar, J., Mello, C.F., Gil-Santana, H.R., Guimarães, A.É., Almeida, S.A.S. & Gleiser, R.M. (2016) Vertical oviposition activity of mosquitoes in the Atlantic Forest of Brazil with emphasis on the sylvan vector of yellow fever virus, Haemagogus leucocelaenus (Diptera: Culicidae). Journal of Vector Ecology 41, 18–26.Google Scholar
Alberti, M. & Marzluff, J. (2004) Ecological resilience in urban ecosystems: linking urban patterns to human and ecological functions. Urban Ecosystems 7, 241–265.Google Scholar
Alto, B.W., Lounibos, L.P., Mores, C.N. & Reiskind, M.H. (2008) Larval competition alters susceptibility of adult Aedes mosquitoes to dengue infection. Proceedings of the Royal Society B: Biological Sciences 275, 463–471.Google Scholar
Anosike, J.C., Nwoke, B.E., Okere, A.N., Oku, E.E., Asor, J.E., Emmy-Egbe, I.O. & Adimike, D.A. (2007) Epidemiology of tree hole breeding mosquitoes in the tropical rainforest of Imo State, south-east Nigeria. Annals of Agricultural and Environmental Medicine 14, 31–38.Google Scholar
Bevins, S.N. (2008) Invasive mosquitoes, larval competition, and indirect effects on the vector competence of native mosquito species (Diptera: Culicidae). Biological Invasions 10, 1109–1117.Google Scholar
Bonaldo, M.C., Gómez, M.M., Santos, A.A.C., Abreu, F.V.S., Ferreira-de-Brito, A., Miranda, R.M., Castro, M.G. & Lourenço-de-Oliveira, R. (2017) Genome analysis of yellow fever virus of the ongoing outbreak in Brazil reveals polymorphisms. Memorias do Instituto Oswaldo Cruz 112, 447–451.Google Scholar
Bradshaw, W.E. & Holzapfel, C.M. (1983) Predator-mediated, non-equilibrium coexistance of tree hole mosquitoes in southeastern North America. Oceologia 57, 239–256.Google Scholar
Brown, A.D., Grau, H.R., Malizia, L. & Grau, A. (2001) Los bosques nublados de la Argentina. pp. 623–659 in Kappelle, M. & Brown, A.D. (Ed.) Bosques Nublados de Latinoamérica, Costa Rica, Editorial INBio.Google Scholar
Burkot, T.R., Handzel, T., Schmaedick, M.A., Tufa, J., Roberts, J.M. & Graves, P.M. (2007) Productivity of natural and artificial containers for Aedes polynesiensis and Aedes aegypti in four American Samoan villages. Medical and Veterinary Entomology 21, 22–29.Google Scholar
Cardoso, J., Almeida, M.A.B., Santos, E., Fonseca, D.F., Sallum, M.A.M.I., Noll, C.A., Monteiro, H.A.O., Cruz, A.C.R., Carvalho, V.L., Pinto, E.V., Castro, F.C., Nunes Neto, J.P., Segura, M.N.O. & Vasconcelos, P.F.C. (2010) Yellow fever virus in Haemagogus leucocelaenus and Aedes serratus mosquitoes, Southern Brazil, 2008. Emerging Infectious Diseases 12, 1918–1924.CrossRefGoogle Scholar
Cardoso, J.C., Corseuil, E. & Barata, J.M.S. (2005) Culicinae (Diptera: Culicidae) ocorrentes no Estado do Rio Grande do Sul, Brasil. Revista Brasilera de Entomologia 49, 275–287.Google Scholar
Chao, A. & Jost, L. (2012) Coverage-based rarefaction and extrapolation: standardizing samples by completeness rather than size. Ecology 93, 2533–2547.Google Scholar
Chao, A. & Shen, T.J. (2010) Program SPADE (Species Prediction and Diversity Estimation). Available online at http://chao.stat.nthu.edu.tw.Google Scholar
Chaves, L.F., Hamer, G.L., Walker, E.D., Brown, W.M., Ruiz, M.O. & Kitron, U.D. (2011) Climatic variability and landscape heterogeneity impact urban mosquito diversity and vector abundance and infection. Ecosphere 2(6), art70, 1–21. doi: 10.1890/ES11-00088.1.CrossRefGoogle Scholar
Cole, L.M. (1949) The measurement of interspecific association. Ecology 30, 411–424.Google Scholar
Colwell, R.K. (2013) EstimateS: Statistical estimation of species richness and shared species from samples. Version 9. User's Guide. Available online at http://purl.oclc.org/estimates.Google Scholar
Colwell, R.K., Chao, A., Gotelli, N.J., Lin, S.Y., Mao, C.X., Chazdon, R.L. & Longino, J.T. (2012) Models and estimators linking individual-based and sample-based rarefaction, extrapolation, and comparison of assemblages. Journal of Plant Ecology 5, 3–21.CrossRefGoogle Scholar
Corbet, P.S. (1964) Observations on mosquitoes ovipositing in small containers in Zika Forest, Uganda. Journal of Animal Ecology 33, 141–164.Google Scholar
Correa, F.F., Gleiser, R.M., Leite, P.J., Fagundes, E., Gil-Santana, H.R., Mello, C.F., Gredilha, R. & Alencar, J. (2014) Mosquito (Diptera: Culicidae) communities in Nova Iguaçu Natural Park Rio de Janeiro, Brazil. Journal of the American Mosquito Control Association 30, 83–90.Google Scholar
Darsie, R.F. (1985) Mosquitoes of Argentina. Part I. Keys for identification of adult females and fourth stage larvae (Diptera: Culicidae). Mosquito Systematics Journal 17, 153–253.Google Scholar
Degallier, N., Travassos Da Rosa, A.P.A., Vasconcelos, P.F.C., Travassos Da Rosa, E.S., Rodrigues, S.G., Sa Filho, G.C. & Travassos Da Rosa, J.F.S. (1992) New entomological and virological data on the vectors of sylvatic yellow fever in Brazil. Journal of the Brazilian Association for the Advancement of Science 44, 136–142.Google Scholar
D'Oria, J.M., Martí, D.A. & Rossi, G.C. (2010) Culicidae, province of Misiones, northeastern Argentina. Check List 6, 176–179.Google Scholar
Di Rienzo, J.A., Casanoves, F., Balzarini, M.G., Gonzalez, L., Tablada, M. & Robledo, C.W. (2014) InfoStat versión 2014. Grupo InfoStat, FCA, Universidad Nacional de Córdoba, Argentina. Available online at http://www.infostat.com.ar.Google Scholar
Forattini, O.P. (1996) Culicidologia Médica. Principios Gerais, Morfologia, Glossario Taxonómico, vol. 1. São Paulo, Ed Univ. São Paulo.Google Scholar
Forattini, O.P. (2002) Culicidologia Médica. São Paulo, Ed Univ. de São Paulo, pp. 860.Google Scholar
Forattini, O.P. & Gomes, A.C. (1988) Biting activity of Aedes scapularis and Haemagogus mosquitoes in southern Brazil (Diptera: Culicidae). Revista de Saúde Pública 22, 84–93.Google Scholar
Gotelli, N.J. & Chao, A. (2013) Measuring and estimating species richness, species diversity, and biotic similarity from sampling data. pp. 195–211 in Levin, S.A. (Ed.) Encyclopedia of Biodiversity. 2nd edn, vol. 5. Waltham, MA, Academic Press.Google Scholar
Gubler, D.J. (2004) The changing epidemiology of yellow fever and dengue, 1900 to 2003: full circle? Comparative Immunology, Microbiology & Infectious Diseases 27, 319–330.CrossRefGoogle ScholarPubMed
Guimarães, A.E., Macedo Lopes, C., Pinto de Mello, R. & Alencar, J. (2003) Ecología de mosquitos (Diptera: Culicidae) em áreas do Parque Nacional do Iguaçu, Brasil. Distribuicão por hábitat. Caderno de Saúde Publica 19, 1107–1116.CrossRefGoogle ScholarPubMed
Hammer, Ø., Harper, D.A.T. & Ryan, P.D. (2001) PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica [Internet]. 49 pp. Available online at http://palaeo-electronica.org/2001_1/past/issue1_01.htm.Google Scholar
Hervé, J.P., Dégallier, N., Travassos da Rosa, A.P.A., Pinheiro, F.P. & Sá, G.C. (1986) Aspectos ecológicos. pp. 409–437 in Instituto Evandro Chagas (Ed.) Evandro Chagas: 50 anos de contribuição às ciências biológicas e à medicina tropical. Belém, Fundação Serviço Especial de Saúde Pública. cap. 1.Google Scholar
Hribar, L.J. & Whiteside, M.E. (2010) Seasonal habitat use by immature Aedes aegypti (LINNAEUS) (Diptera: Culicidae) in the Florida Keys, USA. Studia Dipterologica 17, 237–251.Google Scholar
Hurlbert, S.H. (1969) A coefficient of interspecific association. Ecology 50, 1–9.CrossRefGoogle Scholar
INDEC, Instituto Nacional de Estadística y Censos (2010) Resultados correspondientes al censo nacional de población, hogares y viviendas. Buenos Aires, Argentina. Available online at http://www.indec.gob.ar (accessed 2015).Google Scholar
INTA (2004) Instituto Nacional de Tecnología Agropecuaria. in Arroyo, E.R. (Ed.) Diagnostico Productivo del Departamento de Orán. Orán, INTA Orán. Available online at http://inta.gob.ar/documentos/diagnostico-productivo-del-departamento-de-oran (accessed 2016).Google Scholar
Jost, L. (2006) Entropy and diversity. Oikos 113, 363–375.CrossRefGoogle Scholar
Juliano, S.A. (2009) Species interactions among larval mosquitoes: context dependence across habitat gradients. Annual Review of Entomology 54, 37–56.Google Scholar
Karabatsos, N. (1985) International Catalogue of Arboviruses Including Certain Other Viruses of Vertebrates. 3rd edn. San Antonio, American Society of Tropical Medicine and Hygiene, p. 1147.Google Scholar
Kitching, R.L. (2000) The Container Flora. The Water-Holding Plants. Food Webs and Container Hábitats. The Natural History and Ecology of Phytotelmata. UK, Cambridge University Press, pp. 25–32.Google Scholar
Lounibos, L.P. (1979) Temporal and spatial distribution, growth and predatory behaviour of Toxorhynchites brevipalpis (Diptera: Culicidae) from the Kenya coast. Journal of Animal Ecology 48, 213–236.CrossRefGoogle Scholar
Lounibos, L.P. (1981) Habitat segregation among African treehole mosquitoes. Ecological Entomology 6, 129–154.Google Scholar
Lounibos, L.P., Frank, J.H., Machado-Allison, C.E., Ocanto, P. & Navarro, J.C. (1987) Survival, development and predatory effects of mosquito larvae in Venezuelan phytotelmata. Journal of Tropical Ecology 3, 221–242.CrossRefGoogle Scholar
Lounibos, L.P., Nishimura, N. & Escher, R.L. (1993) Fitness of a treehole mosquito–influences of food type and predation. Oikos 66, 114–118.Google Scholar
Lounibos, L.P., O'Meara, G.F., Escher, R.L., Nishimura, N., Cutwa, M., Nelson, T., Campos, R.E. & Juliano, S.A. (2001) Testing predictions of displacement of native Aedes by the invasive Asian Tiger Mosquito Aedes albopictus in Florida, USA. Biological Invasions 3, 151–166.Google Scholar
Lounibos, P. & Campos, R.E. (2002) Investigaciones recientes sobre Toxorhynchites rutilus (Diptera: Culicidae) con referencia al control biológico de mosquitos habitantes en recipientes. Entomotropica 17, 145–156.Google Scholar
Malizia, L., Pacheco, S., Blundo, C. & Brown, A.D. (2012). Caracterización altitudinal, uso y conservación de las Yungas subtropicales de Argentina. Ecosistemas 21, 53–73.Google Scholar
Mangudo, C., Aparicio, J.P. & Gleiser, R.M. (2011) Tree holes as larval habitats for Aedes aegypti in public areas in Aguaray, Salta province, Argentina. Journal of Vector Ecology 36, 227–230.Google Scholar
Mangudo, C., Aparicio, J.P. & Gleiser, R.M. (2014) Notes on the occurrence and habitats of Sabethes purpureus (Diptera: Culicidae) in Salta Province, Argentina. Journal of the American Mosquito Control Association 30, 57–60.Google Scholar
Mangudo, C., Aparicio, J.P. & Gleiser, R.M. (2015) Tree holes as larval habitats for Aedes aegypti in urban, suburban and forest habitats in a dengue affected area. Bulletin of Entomological Research 105, 679–684.Google Scholar
Marquetti, M.C., Suárez, S., Bisset, J. & Leyva, M. (2005) Reporte de hábitats utilizados por Aedes aegypti en Ciudad de La Habana, Cuba. Revista cubana de medicina tropical 57, 159–161.Google Scholar
Merritt, R.W., Dadd, R.H. & Walker, E.D. (1992) Feeding behavior, natural food, and nutritional relationships of larval mosquitoes. Annual Review of Entomology 37, 349–376.Google Scholar
Ministerio de Salud, Presidencia de la Nación Argentina (2016) Boletín Integrado de Vigilancia No 328 – SE 38.Google Scholar
Mogi, M. & Yong, H.S. (1992) Aquatic arthropod communities in Nepenthes pitchers: the role of niche differentiation, aggregation, predation and competition in community organization. Oecologia 90, 172–184.Google Scholar
Monath, T.P. (1988) Yellow fever. pp. 139–231 in Monath, T.P. (Ed.) Arboviruses: Ecology and Epidemiology, vol. V. Boca Raton, CRC Press.Google Scholar
Omlin, F.X., Carlson, J.C., Ogbunugafor, C.B. & Hassanali, H. (2007) Anopheles gambiae exploits the treehole ecosystem in Western Kenya: a new urban malaria risk? American Journal of Tropical Medicine & Hygiene 77, 264–269.CrossRefGoogle Scholar
Pan American Health Organization (2017) Zika-Epidemiological Report Argentina. Washington, DC, PAHO/WHO World Health Organization.Google Scholar
Reinert, J.F. (2009) List of abbreviations for currently valid generic-level taxa in family Culicidae (Diptera). European Mosquito Bulletin 27, 68–76.Google Scholar
Reis, M., Muller, G.A. & Marcondes, C. (2010). Inventário de mosquitos (Diptera: Culicidae) da Unidade de Conservacão Ambiental Desterro, Ilha de Santa Catarina, Sul do Brasil. Biota Neotropica 10, 333–337.Google Scholar
Selvan, P.S., Jebanesan, A. & Reetha, D. (2016) Entomofaunal diversity of tree hole mosquitoes in Western and Eastern Ghats hill ranges of Tamilnadu, India. Acta Tropica 159, 69–82.Google Scholar
Shen, T-J., Chao, A. & Lin, J-F. (2002) Predicting the number of new species in further taxonomic sampling. Ecology 84, 798–804.Google Scholar
Sota, T., Mogi, M. & Hayamizu, E. (1994) Habitat stability and the larval mosquito community in treeholes and other containers on a temperate island. Researches on Population Ecology 36, 93–104.Google Scholar
Srivastava, D.S. (2005) Do local processes scale to global patterns? The role of drought and the species pool in determining treehole insect diversity. Oecologia 145, 204–214.CrossRefGoogle ScholarPubMed
Stein, M., Ludueña-Almeida, F., Willener, J.A. & Almirón, W.R. (2011) Classification of immature mosquito species according to characteristics of larval habitat in the subtropical province of Chaco, Argentina. Memórias do Instituto Oswaldo Cruz 106, 400–407.Google Scholar
Suzuki, T. & Sone, F. (1978) Breeding habits of vector mosquitoes of filariasis and dengue fever in Western Samoa. Japanese Journal of Sanitary Zoology 29, 279–286.Google Scholar
Szumik, C., Aagesen, L., Casagranda, D., Arzamendia, V., Baldo, D., Claps, L.E., Cuezzo, F., Díaz Gómez, J.M., Di Giacomo, A., Giraudo, A., Goloboff, P., Gramajo, C., Kopuchian, C., Kretzschmar, S., Lizarralde, M., Molina, A., Mollerach, M., Navarro, F., Nomdedeu, S., Panizza, A., Pereyra, V.V., Sandoval, M., Scrocchi, G. & Zuloaga, F.O. (2012) Detecting areas of endemism with a taxonomically diverse data set: plants, mammals, reptiles, amphibians, birds, and insects from Argentina. Cladistics 28, 317–329.Google Scholar
Torres, J. (2010) Dengue, casos: Actualización – Latino América. ProMED-mail. Archive 20100704.2227 (accessed 12 November 2010).Google Scholar
Tóthmérész, B., Máthé, I., Balázs, E. & Magura, T. (2011) Responses of carabid beetles to urbanization in Transylvania (Romania). Landscape and Urban Planning 101, 330–337.Google Scholar
WHO (2014) Risk Assessment on Yellow Fever Virus Circulation in Endemic Countries. Geneva, World Health Organization, 38 p. WHO/HSE/PED/CED/2014.2 (accessed 20 May 2017).Google Scholar
Yadav, R.S., Sharma, V.P. & Chand, S.K. (1997) Mosquito breeding and resting in tree holes in a forest ecosystem in Orissa. Indian Journal of Malariology 34, 8–16.Google Scholar
Yanoviak, S.P. (1999) Community structure in water-filled tree holes of Panama: effects of hole height and size. Selbyana 20, 106–115.Google Scholar
Yanoviak, S.P. (2001) The macrofauna of water filled tree holes on Barro Colorado Island, Panama. Biotropica 33, 110–120.Google Scholar