Effects of landscape anthropization on mosquito community composition and abundance

Martina Ferraguti, Josué Martínez-de la Puente, David Roiz, Santiago Ruiz, Ramón Soriguer, Jordi Figuerola, Martina Ferraguti, Josué Martínez-de la Puente, David Roiz, Santiago Ruiz, Ramón Soriguer, Jordi Figuerola

Abstract

Anthropogenic landscape transformation has an important effect on vector-borne pathogen transmission. However, the effects of urbanization on mosquito communities are still only poorly known. Here, we evaluate how land-use characteristics are related to the abundance and community composition of mosquitoes in an area with endemic circulation of numerous mosquito-borne pathogens. We collected 340 829 female mosquitoes belonging to 13 species at 45 localities spatially grouped in 15 trios formed by 1 urban, 1 rural and 1 natural area. Mosquito abundance and species richness were greater in natural and rural areas than in urban areas. Environmental factors including land use, vegetation and hydrological characteristics were related to mosquito abundance and community composition. Given the differing competences of each species in pathogen transmission, these results provide valuable information on the transmission potential of mosquito-borne pathogens that will be of great use in public and animal health management by allowing, for instance, the identification of the priority areas for pathogen surveillance and vector control.

Figures

Figure 1. Distribution of the 45 mosquito…
Figure 1. Distribution of the 45 mosquito sampling sites including 15 natural (green), 15 rural (red) and 15 urban (blue) areas.
This map was created using ArcGIS v10.2.1 (ESRI, Redland).
Figure 2
Figure 2
Partial dependence plot for mosquito log-transformed captures and: (a) the percentage of land area covered by wetlands (log ratio transformed); (b) the percentage of land area covered by urban areas (log ratio transformed); (c) human population density (log-transformed). Partial dependence plot for species richness (number of different species) and: (d) the percentage of land area covered by urban areas (log ratio transformed); (e) human population density (log-transformed); (f) the distance to the nearest marshland (m). Partial dependence plot for Cx. theileri captures and: (g) the percentage of land area covered by urban areas (log ratio transformed); (h) the percentage of land area covered by wetlands (log ratio transformed); (i) the summer NDVI index. Partial dependence is the dependence of the probability of presence of one predictor variable after averaging out the effects of the other predictor variables in the model.

References

    1. Jones K. E. et al.. Global trends in emerging infectious diseases. Nature 451, 990–993 (2008).
    1. Gubler D. J. The 20th century re-emergence of arboviral diseases: lessons learned and prospects for the future, in Proceedings of the Eighth Sir Dorabji Tata Symposium on Arthropod Borne Viral Infections, Bangalore, India (eds Raghunath, D. & Durga Rao, C.) Sir Dorabji Tata Centre for Research in Tropical Diseases (Tata McGraw-Hill Publishing Company Limited, Bangalore, India, 2008).
    1. Tolle M. A. Mosquito-borne diseases. Curr. Probl. Pediatr. Adolesc. Health Care 39, 97–140 (2009).
    1. Higgs S. & Beaty B. J. Natural cycles of vector-borne pathogens. Biology of disease vectors, In Biology of disease vectors 2nd edn (eds Marquardt W. C. et al..) Elsevier Academic Press (New York, 2005).
    1. Manguin S. & Boëte C. Global impact of mosquito biodiversity, human vector-borne diseases and environmental change, In The importance of biological interactions in the study of biodiversity (ed. Lopez-Pujol J.) 27–50 (Intech open access Publisher, Rijeka, Croatia, 2011).
    1. Beerntsen B. T., James A. A. & Christensen B. M. Genetics of mosquito vector competence. Microbiol. Mol. Biol. Rev. 64, 115–137 (2000).
    1. Kilpatrick A. M. et al.. West Nile virus risk assessment and the bridge vector paradigm. Emerg. Infect. Dis. 11, 425–429 (2005).
    1. Roche B., Rohani P., Dobson A. P. & Guégan J.-F. The impact of community organization on vector-borne pathogens. Am. Nat. 181, 1–11 (2013).
    1. Norris D. E. Mosquito-borne diseases as a consequence of land use change. EcoHealth 1, 19–24 (2004).
    1. Johnson M. F., Gomez A. & Pinedo-Vasquez M. Land use and mosquito diversity in the Peruvian Amazon. J. Med. Entomol. 45, 1023–1030 (2008).
    1. Steiger D. M. et al.. Effects of landscape disturbance on mosquito community composition in tropical Australia. J. Vector Ecol. 37, 69–76 (2012).
    1. Becker N. D. et al.. Mosquitoes and their control 2nd edn, Springer Verlag (Berlin Heidelberg, Germany 2010).
    1. Frankie G. W. & Ehler L. E. Ecology of insects in urban environments. Annu. Rev. Entomol. 23, 367–387 (1978).
    1. McKinney M. L. Effects of urbanization on species richness: a review of plants and animals. Urban Ecosyst. 11, 161–176 (2008).
    1. McKinney M. L. Urbanization, biodiversity, and conservation. Bioscience 52, 883–890 (2002).
    1. Woolhouse M. E. J., Taylor L. E. & Haydon D. T. Population biology of multihost pathogens. Science 292, 1109–1112 (2001).
    1. Shochat E., Warren P. S., Faeth S. H., McIntyre N. E. & Hope D. From patterns to emerging processes in mechanistic urban ecology. Trends Ecol. Evol. 21, 186–191 (2006).
    1. Faeth S. H., Warren P. S., Shochat E. & Marussich W. A. Trophic dynamics in urban communities. BioScience 55, 399–407 (2005).
    1. Gilioli G. & Mariani L. Sensitivity of Anopheles gambiae population dynamics to meteo-hydrological variability: a mechanistic approach. Malaria J. 10, 294 (2011).
    1. Li Y. et al.. Urbanization increases Aedes albopictus larval habitats and accelerates mosquito development and survivorship. PLoS Negl. Trop. Dis. 8, e3301 (2014).
    1. LaDeau S. L., Allan B. F., Leisnham P. T. & Levy M. Z. The ecological foundations of transmission potential and vector-borne disease in urban landscapes. Func. Ecol. 29, 889–901 (2015).
    1. Chuang T. W., Hockett C. W., Kightlinger L. & Wimberly M. C. Landscape-level spatial patterns of West Nile virus risk in the northern Great Plains. Am. J. Trop. Med. Hyg. 86, 724–731 (2012).
    1. Versteirt V. Nationwide inventory of mosquito biodiversity (Diptera: Culicidae) in Belgium, Europe. Bull. Entomol. Res. 103, 193–203 (2013).
    1. Ibañez-Justicia A., Stroo A., Dik M., Beeuwkes J. & Scholte E. J. National mosquito (Diptera: Culicidae) survey in The Netherlands 2010–2013. J. Med. Entomol. 52, 185–198 (2015).
    1. Overgaard H. J. et al.. Effect of landscape structure on anopheline mosquito density and diversity in northern Thailand: implication on malaria transmission and control. Landscape Ecol. 18, 605–619 (2003).
    1. Byrne K. & Nichols R. A. Culex pipiens in London underground tunnels: differentiation between surface and subterranean population. Heredity 82, 7–15 (1999).
    1. Kay B. H. et al.. The importance of subterranean mosquito habitat to arbovirus vector control strategies in North Queensland, Australia. J. Med. Entomol. 37, 846–853 (2000).
    1. Muñoz J. et al.. Feeding patterns of potential West Nile virus vectors in South-West Spain. PLoS One 7, e39549 (2012).
    1. Morchón R., Carretón E., González-Miguel J. & Mellado-Hernández I. Heartworm disease (Dirofilaria immitis) and their vectors in Europe – new distribution trends. Front. Physiol. 3, 196 (2012).
    1. Figuerola J., Jiménez-Clavero M. A., Rojo G., Gómez-Tejedor C. & Soriguer R. Prevalence of West Nile Virus neutralizing antibodies in colonial aquatic birds in southern Spain. Avian Pathol. 36, 209–212 (2007).
    1. Vázquez A. et al.. West Nile and Usutu viruses in mosquitoes in Spain, 2008–2009. Am J. Trop. Med. Hyg. 85, 178–181 (2011).
    1. Ferraguti M. et al.. Avian Plasmodium in Culex and Ochlerotatus mosquitoes from Southern Spain: effects of season and host-feeding source on parasite dynamics. PLoS One 8, e66237 (2013).
    1. Burkett-Cadena N. D., McClure C. J., Estep L. K. & Eubanks M. D. Hosts or habitats: What drives the spatial distribution of mosquitoes? Ecosphere 4, art30 (2013).
    1. Hay S. I., Packer M. J. & Rogers D. J. The impact of remote sensing on the study and control of invertebrate intermediate hosts and vectors for disease. Int. J. Remote Sens. 18, 2899–2930 (1997).
    1. Johnston E. et al.. Mosquito communities with trap height and urban-rural gradient in Adelaide, South Australia: implications for disease vector surveillance. J. Vector Ecol. 39, 48–55 (2014).
    1. Cox J., Grillet M. E., Ramos O. M., Amador M. & Barrera R. Habitat segregation of dengue vectors along an urban environmental gradient. Am. J. Trop. Med. Hyg. 76, 820–826 (2007).
    1. Leisnham P. T. & Sandoval-Mohapatra S. Mosquitoes associated with ditch-plugged and control tidal salt marshes on the Delmarva Peninsula. Int. J. Environ. Res. Public Health 8, 3099–3113 (2011).
    1. Ciota A. T. et al.. Dispersal of Culex mosquitoes (Diptera: Culicidae) from a wastewater treatment facility. J. Med. Entomol. 49, 35–42 (2012).
    1. Bogojević M. S., Merdić E. & Bogdanović T. The flight distances of floodwater mosquitoes (Aedes vexans, Ochlerotatus sticticus and Ochlerotatus caspius) in Osijek, Eastern Croatia. Biologia 66, 678–683 (2011).
    1. Padmanabha H., Durham D., Correa F., Diuk-Wasser M. & Galvani A. The interactive roles of Aedes aegypti super-production and human density in Dengue transmission. PLoS Negl. Trop. Dis. 6, e1799 (2012).
    1. Roche B. et al.. The spread of Aedes albopictus in metropolitan France: contribution of environmental drivers and human activities and predictions for a near future. PLoS One 10, e012560 (2015).
    1. Collantes F. et al.. Review of ten-years presence of Aedes albopictus in Spain 2004–2014: known distribution and public health concerns. Parasite. Vector. 8, 655 (2015).
    1. Reisen W. K., Meyer R. P., Tempelis C. H. & Spoehel J. J. Mosquito abundance and bionomics in residential communities in Orange and Los Angeles counties, California. J. Med. Entomol. 27, 356–367 (1990).
    1. Roiz D., Ruiz S., Soriguer R. & Figuerola J. Landscape effects on the presence, abundance and diversity of mosquitoes in Mediterranean wetlands. PLoS One 10, e0128112 (2015).
    1. Lopes P. et al.. Modelling patterns of mosquito density based on remote sensing images. Estoril Congress Center (2005).
    1. Diuk-Wasser M. A., Brown H. E., Andreadis T. G. & Fish D. Modeling the spatial distribution of mosquito vectors for West Nile virus in Connecticut, USA. Vector-Borne & Zoonotic Diseases, 6, 283–295 (2006).
    1. Santa-Ana M., Khadem M. & Capela R. Natural infection of Culex theileri (Diptera: Culicidae) with Dirofilaria immitis (Nematoda: Filarioidea) on Madeira Island, Portugal. J. Med. Entomol. 43, 104–106 (2006).
    1. Bueno Marí R. & Jiménez Peydró R. Malaria en España: aspectos entomológicos y perspectivas de futuro. Rev. Esp. Salud Publica 82, 467–479 (2008).
    1. Toral G. M., Aragones D., Bustamante J. & Figuerola J. Using Landsat images to map habitat availability for waterbirds in rice fields. Ibis 153, 684–694 (2011).
    1. Ponçon N. et al.. Effects of local anthropogenic changes on potential malaria vector Anopheles hyrcanus and West Nile virus vector Culex modestus, Camargue, France. Emerg. Infect. Dis. 13, 1810 (2007).
    1. Vázquez A. et al.. Novel flaviviruses detected in different species of mosquitoes in Spain. Vector-Borne Zoonotic Dis. 12, 223–229 (2012).
    1. Bisanzio D. et al.. Spatio-temporal patterns of distribution of West Nile virus vectors in eastern Piedmont Region, Italy. Parasite. Vector. 4, 230 (2011).
    1. Farajollahi A., Fonseca D. M., Kramer L. D. & Kilpatrick A. M. “Bird biting” mosquitoes and human disease: a review of the role of Culex pipiens complex mosquitoes in epidemiology. Infect. Genet. Evol. 11, 1577–1585 (2011).
    1. Rizzoli A. et al.. Understanding West Nile virus ecology in Europe: Culex pipiens host feeding preference in a hotspot of virus emergence. Parasite. Vector. 8, 213 (2015).
    1. Vinogradova E. B. Culex pipiens pipiens mosquitoes: taxonomy, distribution, ecology, physiology, genetics, applied importance and control, Vol. 2 (Pensoft Publishers, 2000).
    1. Roiz D. et al.. Efficacy of mosquito traps for collecting potential West Nile mosquito vectors in a natural Mediterranean wetland. Am. J. Trop. Med. Hyg. 86, 642–648 (2012).
    1. Schaffner F. et al.. The mosquitoes of Europe, an identification and training programme. CD-Rom. Montpellier, France (IRD Editions 2001).
    1. Harbach R. E. The identity of Culex perexiguus Theobald versus ex. univittatus Theobald in southern Europe. Eur. Mosq. Bull. 4, 7 (1999).
    1. Balenghien T. et al.. Evidence of the laboratory vector competence of Culex modestus for West Nile virus. J. Am. Mosq. Control Assoc. 23, 233–236 (2007).
    1. Aitchison J. The statistical analysis of compositional data (ed. Chapman & Hall) 1–416 (London, UK, 1986).
    1. Breiman L. Random forests. Mach. Learn. 45, 5–32 (2001).
    1. Cutler D. R. et al.. Random forests for classification in ecology. Ecology 88, 2783–2792 (2007).

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