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Oviposition strategies of temporary pool mosquitoes in relation to weather, tidal regime and land use in a temperate wetland

Published online by Cambridge University Press:  31 May 2012

M.V. Cardo*
Affiliation:
Unidad de Ecología de Reservorios y Vectores de Parásitos, Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria, Pabellón 2, 4° piso (C1428EHA), Buenos Aires, Argentina
D. Vezzani
Affiliation:
Unidad de Ecología de Reservorios y Vectores de Parásitos, Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria, Pabellón 2, 4° piso (C1428EHA), Buenos Aires, Argentina
A.E. Carbajo
Affiliation:
Unidad de Ecología de Reservorios y Vectores de Parásitos, Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria, Pabellón 2, 4° piso (C1428EHA), Buenos Aires, Argentina
*
*Author for correspondence Fax:+54 11 4576-3354 E-mail: [email protected]

Abstract

Wetlands have traditionally been associated with harbouring mosquitoes, a well-known nuisance and vectors of diseases. Within mosquito life cycle, oviposition is a determinant event by shaping their individual fitness and vectorial capacity. The study was conducted in one of the main temperate wetlands in South America. We used Generalized Linear Models to study the relation between temperature, precipitation, tidal regime, land use, microenvironment, and the occurrence of floodwater (Ochlerotatus and Psorophora spp.) and raft-laying (Culex and Uranotaenia spp.) mosquitoes using temporary pools as larval habitats. Pool occurrence was negatively associated with temperature, and positively related to precipitation and high tides. As regards the land use, it was lowest in domestic areas and plantations, intermediate in secondary forests, and highest in marshes. Each oviposition strategy was best modelled as a function of different environmental factors. The occurrence of floodwater mosquitoes was positively associated with high cumulative precipitation and low tide records. Raft-laying mosquitoes were related to low temperature records, while the effect of flooding varied with the land use. In view of these results, physical (water inputs and movement), chemical, and biological (egg and larval flushing, and predatory interactions) considerations are given to provide insight in the oviposition patterns of mosquitoes occurring in this complex wetland. We finally propose the generation of a tidal flow as a control measure against floodwater mosquitoes, which are the most anthropophilic in the study area.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2012

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References

Akaike, H. (1974) A new look at the statistical model identification. IEEE Transactions on Automatic Control 19, 716723.CrossRefGoogle Scholar
Baigún, C.R.M., Puig, A., Minotti, P.G., Kandus, P., Quintana, R., Vicari, R., Bo, R., Oldani, N.O. & Nestler, J.A. (2008) Resource use in the Parana River Delta (Argentina): moving away from an ecohydrological approach? Ecohydrology and Hydrobiology 2–4, 245262.Google Scholar
Beketov, M.A., Yurchenko, Y.A., Belevich, O.E. & Liess, M. (2010) What environmental factors are important determinants of structure, species richness, and abundance of mosquito assemblages? Journal of Medical Entomology 47, 129139.Google Scholar
Bentley, M.D. & Day, F.J. (1989) Chemical ecology and behavioural aspects of mosquito oviposition. Annual Review of Entomology 34, 401421.CrossRefGoogle ScholarPubMed
Berti, J., Gutiérrez, A. & Zimmerman, R. (2004) Relaciones entre tipos de hábitat, algunas variables químicas y la presencia de larvas de Anopheles aquasalis Curry y Anopheles pseudopunctipennis Theobald en un área costera del estado Sucre, Venezuela. Entomotropica 19, 7984.Google Scholar
Bian, L. & Li, I. (2006) Combining global and local estimates for spatial distribution of mosquito larval habitats. GIScience and Remote Sensing 43, 95108.Google Scholar
Blaustein, L. & Chase, J.M. (2007) The role of species sharing the same trophic level as mosquitoes on mosquito populations. Annual Review of Entomology 52, 489507.Google Scholar
Blaustein, L., Blaustein, J. & Chase, J. (2005) Chemical detection of predator Notonecta irrorata by ovipositing Culex mosquitoes. Journal of Vector Ecology 30, 299301.Google Scholar
, R.F. & Quintana, R.D. (1999) Actividades humanas y biodiversidad en humedales: el caso del Bajo Delta del Río Paraná. pp. 291315in Matteucci, S.D., Solbrig, O.T., Morello, J. & Halffter, G. (Eds) Biodiversidad y Uso de la Tierra. Conceptos y Ejemplos de Latinoamérica. Buenos Aires, Argentina, EUDEBA.Google Scholar
Campos, R.E., Fernández, L.A. & Sy, V.E. (2004) Study of the insects associated with the floodwater mosquito Ochlerotatus albifasciatus (Diptera: Culicidae) and their possible predators in Buenos Aires Province, Argentina. Hydrobiologia 524, 91102.Google Scholar
Cantoni, E. & Hastie, T. (2002) Degrees of freedom tests for smoothing splines. Biometrika 89, 251263.Google Scholar
Cardo, M.V., Vezzani, D. & Carbajo, A.E. (2011a) Community structure of ground-water breeding mosquitoes driven by land use in a temperate wetland of Argentina. Acta Tropica 119, 7683.Google Scholar
Cardo, M.V., Vezzani, D. & Carbajo, A.E. (2011b). Environmental predictors of the occurrence of ground water mosquito immatures in the Paraná Lower Delta, Argentina. Journal of Medical Entomology 48, 991998.Google Scholar
Chaves, L.F. & Kitron, U.D. (2011) Weather variability impacts on oviposition dynamics of the southern house mosquito at intermediate time scales. Bulletin of Entomological Research 101(6), 19.Google Scholar
Clements, A.N. (1992) The Biology of Mosquitoes, vol. 1: Development, Nutrition and Reproduction. UK, CABI Publishing.CrossRefGoogle Scholar
Clements, A.N. (1999) The Biology of Mosquitoes. Vol. 2-Sensory, reception and behaviour. London, UK, CABI Publishing.Google Scholar
Cressie, N.A.C. (1993) Statistics for Spatial Data. New York, USA, Wiley.CrossRefGoogle Scholar
Dale, P.E.R. & Knight, J.M. (2008) Wetlands and mosquitoes: a review. Wetlands Ecology and Management 16, 255276.Google Scholar
Darsie, R.F. Jr (1985) Mosquitoes of Argentina. Part I, keys for identification of adult females and fourth stage larvae in English and Spanish (Diptera, Culicidae). Mosquito Systematics 17, 153253.Google Scholar
Davis, C.E., Hyde, J.E., Bangdiwala, S.I. & Nelson, J.J. (1986) An example of dependencies among variables in a conditional logistic regression. pp. 140147in Moolgavkar, S.H. & Prentice, R.L. (Eds) Modern Statistical Methods in Chronic Disease Epidemiology. New York, USA, Wiley.Google Scholar
de Little, S.C., Bowman, D.M.J.S., Whelan, P.I., Brook, B.W. & Bradshaw, C.J.A. (2009) Quantifying the drivers of larval density patterns in two tropical mosquito species to maximize control efficiency. Environmental Entomology 38, 10131021.Google Scholar
Fielding, A.H. & Bell, J.F. (1997) A review of the methods for the assessment of prediction errors in conservation presence/absence models. Environmental Conservation 24, 3849.Google Scholar
Fontanarrosa, M.S., Marinone, M.C., Fischer, S., Orellano, P.W. & Schweigmann, N. (2000) Effects of flooding and temperature on Aedes albifasciatus development time and larval density in two rain pools at Buenos Aires University City. Memórias do Instituto Oswaldo Cruz 95, 787793.Google Scholar
Forattini, O. (2002) Culicidologia Medica, vol. 2. São Paulo, Brazil, Editora da Universidade de São Paulo.Google Scholar
Gleiser, R.M. & Gorla, D.E. (1997) Abundancia de Aedes (Ochlerotatus) albifasciatus (Diptera: Culicidae) en el sur de la laguna Mar Chiquita. Ecología Austral 7, 2027.Google Scholar
Gu, W., Regens, J.L., Beier, J.C. & Novak, R.J. (2006) Source reduction of mosquito larval habitats has unexpected consequences on malaria transmission. Proceedings of the National Academy of Science USA 103, 1756017563.CrossRefGoogle ScholarPubMed
Guisan, A. & Zimmermann, N.E. (2000) Predictive habitat distribution models in ecology. Ecological Modelling 135, 147186.Google Scholar
Guisan, A., Edwards, T.C. & Hastie, T. (2002) Generalized linear and generalized additive models in studies of species distributions: setting the scene. Ecological Modelling 157, 89100.Google Scholar
Hurlbert, S.H. (1969) A coefficient of interspecific association. Ecology 50, 19.Google Scholar
Juliano, S.A. (2009) Species interactions among larval mosquitoes: context dependence across habitat gradients. Annual Review of Entomology 54, 3756.Google Scholar
Kandus, P. & Malvárez, A.I. (2004) Vegetation patterns and change analysis in the lower Delta Island of the Paraná River (Argentina). Wetlands 24, 620632.Google Scholar
Kandus, P., Karszenbaum, H. & Frulla, L. (1999) Land cover classification system of the Lower Delta of the Parana River (Argentina): its relationship with Landsat Thematic Mapper spectral classes. Journal of Coastal Research 15, 909926.Google Scholar
Kandus, P., Quintana, R.D. & , R.F. (2006) Patrones de Paisaje y Biodiversidad del Bajo Delta del Río Paraná. Mapa de Ambientes. Buenos Aires, Argentina, Pablo Casamajor.Google Scholar
Klowden, M.J. (1990) The endogenous regulation of mosquito reproductive behavior. Experientia 46, 60670.CrossRefGoogle ScholarPubMed
Klowden, M.J. & Briegel, H. (1994) Mosquito gonotrophic cycle and multiple feeding potential: contrasts between Anopheles and Aedes (Diptera: Culicidae). Journal of Medical Entomology 31, 618622.Google Scholar
Koenraadt, C.J.M. & Harrington, L.C. (2008) Flushing effect of rain on container-inhabiting mosquitoes Aedes aegypti and Culex pipiens (Diptera: Culicidae). Journal of Medical Entomology 45, 2835.Google Scholar
Kokkinn, M.J., Duval, D.J. & Williams, C.R. (2009) Modelling the ecology of the coastal mosquitoes Aedes vigilax and Aedes camptorhynchus at Port Pirie, South Australia. Medical and Veterinary Entomology 23, 8591.Google Scholar
Landis, J.R. & Koch, G.C. (1977) The measurement of observer agreement for categorical data. Biometrics 33, 159174.Google Scholar
Laurito, M., Almirón, W.R. & Rossi, G.C. (2011) Description of the immature stages and redescription of the adults of Culex (Culex) lahillei Bachmann & Casal (Diptera: Culicidae). Zootaxa 2915, 2938.Google Scholar
Leisnham, P.T., Slaney, D.P., Lester, P.J. & Weinstein, P. (2005) Increased larval mosquito densities from modified landuses in the Kapiti Region, New Zealand: vegetation, water quality, and predators as associated environmental factors. EcoHealth 2, 110.Google Scholar
Linthicum, K.J., Anyamba, A., Tucker, C.J., Kelley, P.W., Meyers, M.F. & Peters, C.J. (1999) Climate and satellite indicators to forecast Rift Valley fever epidemics in Kenya. Science 285, 397400.CrossRefGoogle ScholarPubMed
Loetti, V., Burroni, N. & Vezzani, D. (2007) Seasonal and daily activity patterns of human-biting mosquitoes in a wetland system in Argentina. Journal of Vector Ecology 32, 358365.Google Scholar
Maciá, A., García, J.J. & Campos, R.E. (1995) Bionomía de Aedes albifasciatus y Ae. crinifer (Diptera: Culicidae) y sus enemigos naturales en Punta Lara, Buenos Aires. Neotrópica 41, 4350.Google Scholar
McCullagh, P. & Nelder, J.A. (1989) Generalized Linear Models. London, UK, Chapman and Hall.Google Scholar
Mercer, D.R., Sheeley, S.L. & Brown, E.J. (2005) Mosquito (Diptera: Culicidae) development within microhabitats of an Iowa wetland. Journal of Medical Entomology 42, 685693.CrossRefGoogle ScholarPubMed
Nicholls, A.O. (1989) How to make biological surveys go further with generalised linear models. Biological Conservation 50, 5175.Google Scholar
NOAA Satellite and Information Service (2011) NNDC climate data online. Available online at http://www7.ncdc.noaa.gov/CDO/cdoselect.cmd?datasetabbv=GSOD&countryabbv=ge (accessed 1 February 2011).Google Scholar
Paterson, S. & Lello, J. (2003) Mixed models: getting the best use of parasitological data. Trends in Parasitology 19, 6574.Google Scholar
Petersen, J.L. & Linley, J.R. (1995) Description of the egg of Aedeomyia squamipennis (Diptera: Culicidae). Journal of Medical Entomology 32, 888894.CrossRefGoogle ScholarPubMed
R Development Core Team (2009) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available online at http://www.R-project.org (accessed 6 April 2011).Google Scholar
Rossi, G.C., Mariluis, J.C., Schnack, J.A. & Spinelli, G.R. (2002) Dipteros Vectores (Culicidae y Calliphoridae) de la Provincia de Buenos Aires. Buenos Aires, Argentina, Universidad de La Plata.Google Scholar
Rubbo, M.J., Lanterman, J.L., Falco, R.C. & Daniels, T.J. (2011) The influence of amphibians on mosquitoes in seasonal pools: can wetlands protection help to minimize disease risk? Wetlands 31, 799804.Google Scholar
Schäfer, M.L. (2004) Mosquitoes as a part of wetland biodiversity. Comprehensive summaries of Uppsala dissertations from the Faculty of Science and Technology 1042. Acta Universitatis Upsaliensis.Google Scholar
Senise, L.V. & Sallum, M.A.M. (2008) Redescription of Culex (Culex) dolosus (Lynch Arribálzaga) (Diptera:Culicidae), based on specimens from Pico do Itapeva, Serra da Mantiqueira, São Paulo, Brazil. Zootaxa 1683, 5162.Google Scholar
Service, M.W. (1995) Mosquitoes (Culicidae). pp. 120240in Lane, R.P. & Crosskey, R.W. (Eds) Medical Insects and Arachnids. London, UK, Chapman & Hall.Google Scholar
Servicio de Hidrografía Naval (2009) Tablas de marea: Puertos de la República Argentina y algunos puertos del Uruguay. .Google Scholar
Servicio de Hidrografía Naval (2010) Tablas de marea: Puertos de la República Argentina y algunos puertos del Uruguay. .Google Scholar
Shaman, J., Stieglitz, M., Stark, C., Le Blancq, S. & Cane, M. (2002) Using a dynamic hydrology model to predict mosquito abundances in flood and swamp water. Emerging Infectious Diseases 8, 813.Google Scholar
Silver, J.B. (2008) Mosquito Ecology: Field Sampling Methods. 3rd edn.New York, USA, Springer.Google Scholar
Society of Wetland Scientists (2009) Current practices in wetland management for mosquito control. Wetland Concerns Committee. Available online at http://faculty.ucr.edu/∼walton/Berg%20et%20al%202009%20SWS.pdf (accessed 1 March 2011).Google Scholar
Titus, K. & Mosher, J.A. (1984) Chance-corrected classification for use in discriminant analysis: ecological applications. American Midland Naturalist 111, 17.Google Scholar
Washburn, J.O. & Anderson, J.R. (1993) Habitat overflow, a source of larval mortality for Aedes sierrensis (Diptera: Culicidae). Journal of Medical Entomology 30, 802804.Google Scholar
Williams, D.D. (1997) Temporary ponds and their invertebrate communities. Aquatic Conservation 7, 105117.Google Scholar
Willot, E. (2004) Restoring nature, without mosquitoes? Restoration Ecology 12, 147153.Google Scholar
WHO (2002) World Health Report 2002: Reducing risks, promoting healthy life. Geneva, Switzerland, World Health Organization.Google Scholar
Zar, J.H. (1999) Biostatistical Analysis. Upper Saddle River, NJ, USA, Prentice Hall.Google Scholar
Zuharah, W.F. & Lester, P.J. (2010) Can adults of the New Zealand mosquito Culex pervigilans (Bergorth) detect the presence of a key predator in larval habitats? Journal of Vector Ecology 35, 100105.Google Scholar
Zuur, A.F., Ieno, E. N., Walker, N.J., Saveliev, A.A. & Smith, G.M. (2009) Mixed Effects Models and Extensions in Ecology with R. New York, USA, Springer.Google Scholar