Abstract
Mosquito-borne diseases are an increasingly important health concern, which pose great challenges for safe and sustainable control and eradication. This reality calls for management approaches that consider multiple aspects of the transmission cycle from a landscape and vector ecology perspective, to socio-economic elements that may increase exposure. This study seeks to better understand these pathways using dengue fever in the San Juan Bay Estuary (SJBE), Puerto Rico. Dengue is transmitted by Aedes aegypti, a species that thrives in cities. Here we ask which elements within the urban landscape could be managed to help prevent dengue outbreaks. We studied the potential of coastal wetlands in the SJBE to buffer vector proliferation, hypothesizing that wetland ecosystem services lead to lower dengue occurrence. We test this hypothesis using census-block level dengue data from 2010-13, including the largest epidemic in Puerto Rican history. Our analytical model includes socio-economic factors and environmental controls that may also affect dengue dynamics. Results from beta-binomial regressions and model averaging indicated that dengue occurrence was lower in neighborhoods with higher wetland cover even after controlling for population density and other socio-economic aspects. Our models suggest that heat hazard mitigation is partly responsible for the association between wetlands and dengue.
Similar content being viewed by others
References
Barbosa AM, Real R, Munoz AR, Brown JA (2013) New measures for assessing model equilibrium and prediction mismatch in species distribution models. Diversity and Distributions 19:1333–1338. https://doi.org/10.1111/ddi.12100
Barrera R, Amador M, Clark GG (2006) Ecological factors influencing Aedes aegypti (Diptera: Culicidae) productivity in artificial containers in Salinas, Puerto Rico. Journal of Medical Entomology 43(3):484–492. https://doi.org/10.1093/jmedent/43.3.484
Barrera R, Amador M, MacKay AJ (2011) Population dynamics of Aedes aegypti and dengue as influenced by weather and human behavior in San Juan, Puerto Rico. PLoS Neglected Tropical Diseases 5(12). https://doi.org/10.1371/journal.pntd.0001378
Barrera R, Bingham AM, Hassan HK, Amador M, Mackay AJ, Unnasch TR (2012) Vertebrate hosts of Aedes aegypti and Aedes mediovittatus (Diptera: Culicidae) in rural Puerto Rico. Journal of Medical Entomology 49(4):917–921. https://doi.org/10.1603/ME12046
Bartoń, K (2009) MuMIn: multi-model inference. R package, version 0.12.2. Available at: http://r-forge.r-project.org/projects/mumin/. Accessed 11/14/2017
Becker, R. A., Chambers, J. M. and Wilks, A. R. (1988) The New S Language. Wadsworth & Brooks/Cole
Bouchama A, Knochel JP (2002) Heat stroke. New England Journal of Medicine 346(25):1978–1988. https://doi.org/10.1056/NEJMra011089
Bowman LR, Runge-Ranzinger S, McCall PJ (2014) Assessing the relationship between vector indices and dengue transmission: a systematic review of the evidence. PLoS Negl Trop Dis 8(5):e2848 https://doi.org/10.1371/journal.pntd.0002848
Brandeis, T. J., Escobedo, F. J., Staudhammer, C. L., Nowak, D. J., & Zipperer, W. C. (2014). San Juan Bay Estuary watershed urban forest inventory. Available at: https://www.nrs.fs.fed.us/pubs/45759. Accessed 11/14/2017
Brody SD, Highfield WE (2013) Open space protection and flood mitigation: A national study. Land Use Policy 32:89–95. https://doi.org/10.1016/j.landusepol.2012.10.017
Brody SD, Peacock WG, Gunn J (2012) Ecological indicators of flood risk along the Gulf of Mexico. Ecological Indicators 18:493–500. https://doi.org/10.1016/j.ecolind.2012.01.004
Burke R, Barrera R, Lewis M, Kluchinsky T, Claborn D (2010) Septic tanks as larval habitats for the mosquitoes Aedes aegypti and Culex quinquefasciatus in Playa-Playita, Puerto Rico. Medical and Veterinary Entomology 24(2):117–123. https://doi.org/10.1111/j.1365-2915.2010.00864.x
Burnham KP, Anderson DR (2002) Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach, 2nd edn. Springer, Berlin
Carrington LB, Armijos MV, Lambrechts L, Barker CM, Scott TW (2013) Effects of fluctuating daily temperatures at critical thermal extremes on Aedes aegypti life-history traits. PLoS One 8(3). https://doi.org/10.1371/journal.pone.0058824
Carver, S., Slaney, D. P., Leisnham, P. T., & Weinstein, P. (2015). Healthy wetlands, healthy people: “mosquito-borne” disease. In Wetlands and Human Health (pp. 95-121). Springer Netherlands
Centro de Recaudación de Ingresos Municipales (CRIM). (2006). Hydrography Revision, 2001-04 from CRIM Basemap, scale 1:5000. Available at: http://gis.otg.pr.gov. Accessed 06/22/2017
Chang FS, Tseng YT, Hsu PS, Chen CD, Lian IB, Chao DY (2015) Re-assess vector indices threshold as an early warning tool for predicting dengue epidemic in a dengue non-endemic country. PLoS Negl Trop Dis 9(9):e0004043 https://doi.org/10.1371/journal.pntd.0004043
Cheong YL, Leitão PJ, Lakes T (2014) Assessment of land use factors associated with dengue cases in Malaysia using boosted regression trees. Spat Spatiotemporal Epidemiol 10:75–84 https://doi.org/10.1016/j.sste.2014.05.002
Couret J, Dotson E, Benedict MQ (2014) Temperature, larval diet, and density effects on development rate and survival of Aedes aegypti (Diptera: Culicidae). PLoS One 9(2):e87468
Cox J, Grillet ME, Ramos OM, Amador M, Barrera R (2007) Habitat segregation of dengue vectors along an urban environmental gradient. The American Journal of Tropical Medicine and Hygiene 76(5):820–826. https://doi.org/10.4269/ajtmh.2007.76.820
Federal Emergency Management Agency (FEMA). (2009). Digital flood insurance rate map database, Commonwealth of Puerto Rico. Available at: http://gis.otg.pr.gov/download_gis_files.htm. Accessed 06/22/2017
Gould, W. A., Alarcón, C., Fevold, B., Jiménez, M. E., Martinuzzi, S., Potts, G., ... & Ventosa, E. (2008). The Puerto Rico Gap Analysis Project volume 1: land cover, vertebrate species distributions, and land stewardship. Gen. Tech. Rep. IITF-GTR-39. Río Piedras, PR: U.S. Department of Agriculture, Forest Service, International Institute of Tropical Forestry. 165 p
Grueber CE, Nakagawa S, Laws RJ, Jamieson IG (2011) Multimodel inference in ecology and evolution: challenges and solutions. Journal of Evolutionary Biology 24(4):699–711. https://doi.org/10.1111/j.1420-9101.2010.02210.x
Harrington LC, Scott TW, Lerdthusnee K, Coleman RC, Costero A, Clark GG et al (2005) Dispersal of the dengue vector Aedes aegypti within and between rural communities. The American Journal of Tropical Medicine and Hygiene 72(2):209–220. https://doi.org/10.4269/ajtmh.2005.72.209
Hashizume M, Dewan AM, Sunahara T, Rahman MZ, Yamamoto T (2012) Hydroclimatological variability and dengue transmission in Dhaka, Bangladesh: a time-series study. BMC Infectious Diseases 12(1):98. https://doi.org/10.1186/1471-2334-12-9
Helmersson, J. (2012) Mathematical Modeling of Dengue-Temperature Effect on Vectorial Capacity. Universitet UMEA.. Master of Science Thesis. Available at: http://www.phmed.umu.se/digitalAssets/104/104555_jing-helmersson.pdf: Umeå University; 2012. 11/14/2017
Ibarra AMS, Ryan SJ, Beltrán E, Mejía R, Silva M, Muñoz Á (2013) Dengue vector dynamics (Aedes aegypti) influenced by climate and social factors in Ecuador: implications for targeted control. PLoS One 8(11). https://doi.org/10.1371/journal.pone.0078263
Kling LJ, Juliano SA, Yee DA (2007) Larval mosquito communities in discarded vehicle tires in a forested and unforested site: detritus type, amount, and water nutrient differences. Journal of Vector Ecology 32(2):207–217. https://doi.org/10.3376/1081-1710
LaDeau SL, Leisnham PT, Biehler D, Bodner D (2013) Higher mosquito production in low-income neighborhoods of Baltimore and Washington, DC: understanding ecological drivers and mosquito-borne disease risk in temperate cities. International Journal of Environmental Research and Public Health 10(4):1505–1526. https://doi.org/10.3390/ijerph10041505
Lesnoff M. and Lancelot R (2012) Analysis of Overdispersed Data (aod, ver 1.3). Available at: https://cran.r-project.org/web/packages/aod/index.html. Accessed 01/20/2017
Lugo AE, Snedaker SC (1974) The ecology of mangroves. Annual Review of Ecology and Systematics 5(1):39–64. https://doi.org/10.1146/annurev.es.05.110174.000351
Lugo, A. E., Ramos, O., & Rodriguez, C. (2011). The Río Piedras watershed and its surrounding environment. U.S. Department of Agriculture Forest Service, International Institute of Tropical Forestry. 48 p. Available at: https://www.researchgate.net/profile/Ariel_Lugo/publication/267236241_ThE_RiO_PiEdRAs_WATERshEd_and_Its_Surrounding_Environment_ACknOWLEdGMEnTs/links/548863900cf289302e30a35e.pdf. Accessed 11/14/2017
Mackay AJ, Amador M, Diaz A, Smith J, Barrera R (2009) Dynamics of Aedes aegypti and Culex quinquefasciatus in septic tanks. Journal of the American Mosquito Control Association 25(4):409–416. https://doi.org/10.2987/09-5888.1
Méndez-Lázaro P, Muller-Karger FE, Otis D, McCarthy MJ, Peña-Orellana M (2014) Assessing climate variability effects on dengue incidence in San Juan, Puerto Rico. International Journal of Environmental Research and Public Health 11(9):9409–9428. https://doi.org/10.3390/ijerph110909409
Méndez-Lázaro, P., Muller-Karger, F. E., Otis, D., McCarthy, M. J., & Rodríguez, E. (2017). A heat vulnerability index to improve urban public health management in San Juan, Puerto Rico. International journal of biometeorology, 1-14. https://doi.org/10.1007/s00484-017-1319-z
Morin CW, Comrie AC, Ernst K (2013) Climate and dengue transmission: evidence and implications. Environmental Health Perspectives 121(11-12):1264. https://doi.org/10.1289/ehp.1306556
Morin CW, Monaghan AJ, Hayden MH, Barrera R, Ernst K (2015) Meteorologically driven simulations of dengue epidemics in San Juan, PR. PLoS Neglected Tropical Diseases 9(8). https://doi.org/10.1371/journal.pntd.0004002
Mulligan K, Dixon J, Sinn CLJ, Elliott SJ (2015) Is dengue a disease of poverty? A systematic review. Pathogens and Global Health 109(1):10. https://doi.org/10.1179/2047773214Y.0000000168
Murugan K, Priyanka V, Dinesh D, Madhiyazhagan P, Panneerselvam C, Subramaniam J et al (2015) Predation by Asian bullfrog tadpoles, Hoplobatrachus tigerinus, against the dengue vector, Aedes aegypti, in an aquatic environment treated with mosquitocidal nanoparticles. Parasitol Res 114(10):3601–3610 https://doi.org/10.1007/s00436-015-4582-0
Myer MH, Campbell SR, Johnston JM (2017) Spatiotemporal modeling of ecological and sociological predictors of West Nile virus in Suffolk County, NY, mosquitoes. Ecosphere 8(6) https://doi.org/10.1002/ecs2.1854
Myers SS, Gaffikin L, Golden CD, Ostfeld RS, Redford KH, Ricketts TH et al (2013) Human health impacts of ecosystem alteration. Proceedings of the National Academy of Sciences 110(47):18753–18760. https://doi.org/10.1073/pnas.1218656110
Navarro DMAF, De Oliveira PES, Potting RPJ, Brito AC, Fital SJF, Sant'Ana AE (2003) The potential attractant or repellent effects of different water types on oviposition in Aedes aegypti L.(Dipt., Culicidae). Journal of Applied Entomology 127(1):46–50. https://doi.org/10.1046/j.1439-0418.2003.00690.x
Philip GM, Watson DF (1982) A precise method for determining contoured surfaces. APPEA J 22(1):205–212 https://doi.org/10.1071/AJ81016
Pires DA, Gleiser RM (2010) Mosquito fauna inhabiting water bodies in the urban environment of Córdoba city, Argentina, following a St. Louis encephalitis outbreak. Journal of Vector Ecology 35(2):401–409. https://doi.org/10.1111/j.1948-7134.2010.00099.x
Poole-Smith BK, Hemme RR, Delorey M, Felix G, Gonzalez AL, Amador M et al (2015) Comparison of vector competence of Aedes mediovittatus and Aedes aegypti for dengue virus: implications for dengue control in the Caribbean. PLoS Neglected Tropical Diseases 9(2):e0003462. https://doi.org/10.1371/journal.%20pntd.0003462
Puerto Rico Department of Health (PRDH). (2017). Informe seminal de enfermedades arbovirales (Semana 4-10 de Junio de 2017). Available at: http://www.salud.gov.pr/Estadisticas-Registros-y-Publicaciones/Informes%20Arbovirales/Reporte%20ArboV%20semana%2023-2017.pdf/ Accessed 06/29/2017
Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press
Quiroz-Martínez H, Rodríguez-Castro A (2007) Aquatic insects as predators of mosquito larvae. Journal of the American mosquito control association, 23(sp2), 110-117. https://doi.org/10.2987/8756-971X(2007)23%5B110:AIAPOM%5D2.0.CO;2
Ramasamy R, Surendran SN, Jude PJ, Dharshini S, Vinobaba M (2011) Larval development of Aedes aegypti and Aedes albopictus in peri-urban brackish water and its implications for transmission of arboviral diseases. PLoS Neglected Tropical Diseases 5(11):e1369. https://doi.org/10.1371/journal.pntd.0001369
Reiter P, Amador MA, Anderson RA, Clark GG (1995) Dispersal of Aedes aegypti in an urban area after blood feeding as demonstrated by rubidium-marked eggs. The American Journal of Tropical Medicine and Hygiene 52(2):177–179. https://doi.org/10.4269/ajtmh.1995.52.177
Ruiz-Fons, F., Acevedo, P., Sobrino, R., Vicente, J., Fierro, Y., & Fernández-de-Mera, I. G. (2013). Sex-biased differences in the effects of host individual, host population and environmental traits driving tick parasitism in red deer. Frontiers in cellular and infection microbiology, 3. doi: https://doi.org/10.3389/fcimb.2013.00023
San Juan Bay Estuary (SJBE). (2015). Area cientifica: datos de monitoreo. Available at: http://www.estuario.org/index.php/datos/ciencia?limitstart=0. Accessed 01/30/2017
Sanford MR, Chan K, Walton WE (2005) Effects of inorganic nitrogen enrichment on mosquitoes (Diptera: Culicidae) and the associated aquatic community in constructed treatment wetlands. Journal of Medical Entomology 42(5):766–776. https://doi.org/10.1093/jmedent/42.5.766
Sarfraz MS, Tripathi NK, Tipdecho T, Thongbu T, Kerdthong P, Souris M (2012) Analyzing the spatio-temporal relationship between dengue vector larval density and land-use using factor analysis and spatial ring mapping. BMC Public Health 12(1):853 https://doi.org/10.1186/1471-2458-12-853
Sharp TM, Hunsperger E, Santiago GA, Muñoz-Jordan JL, Santiago LM, Rivera A et al (2013) Virus-specific differences in rates of disease during the 2010 Dengue epidemic in Puerto Rico. PLoS Neglected Tropical Diseases 7(4):e2159. https://doi.org/10.1371/journal.pntd.0002159
Stanforth A, Moreno-Madriñán MJ, Ashby J (2016) Exploratory analysis of dengue fever niche variables within the Río Magdalena watershed. Remote Sens 8(9):770 https://doi.org/10.3390/rs8090770
Tiong V, Abd-Jamil J, Zan MH, Abu-Bakar RS, Ew CL, Jafar FL et al (2015) Evaluation of land cover and prevalence of dengue in Malaysia. Trop Biomed 32(4):587–597
Torres-Valcárcel Á, Harbor J, González-Avilés C, Torres-Valcárcel A (2014) Impacts of Urban Development on Precipitation in the Tropical Maritime Climate of Puerto Rico. Climate 2(2):47–77. https://doi.org/10.3390/cli2020047
U.S. Geological Survey, (1941) A. USGS 1:30000-scale Quadrangle for San Juan, PR 1941: U.S. Geological Survey: Reston, Virginia. Available at: https://prd-tnm.s3.amazonaws.com/StagedProducts/Maps/HistoricalTopo/2/14619/4985332.pdf. Accessed 01/25/2017
U.S. Geological Survey. (1944). 1:20000 scale Topographic contours for Puerto Rico quadrangles converted form USGS Digital Line Graph data. Available at: http://gis.otg.pr.gov/download_gis_files.htm. Accessed 01/25/2017
United States Census Bureau. (2015). 2011-5-year summary American Community Survey. U.S. Census Bureau’s American Community Survey Office. Available at: http://ftp2.census.gov/. Accessed 01/25/2017
Venables WN, Ripley BD (2003) Modern Applied Statistics with S, 4th edn. Springer-Verlag, New York
Watson DF, Philip GM (1985) A refinement of inverse distance weighted interpolation. Geoprocessing 2(4):315–327
World Health Organization (WHO). (2006). Communicable diseases following natural disasters: Risk assessment and priority interventions (WHO/CDS/NTD/DCE/2006.4). Available at: http://www.who.int/diseasecontrol_emergencies/guidelines/CD_Disasters_26_06.pdf Accessed 01/30/2017
Yee DA, Himel E, Reiskind MH, Vamosi SM (2014) Implications of saline concentrations for the performance and competitive interactions of the mosquitoes Aedes aegypti (Stegomyia aegypti) and Aedes albopictus (Stegomyia albopictus). Medical and Veterinary Entomology 28(1):60–69. https://doi.org/10.1111/mve.12007
Acknowledgements
We thank Roberto Barrera from the CDC Dengue Branch for providing data and advice in the development of this work. Matthew Harwell, Marc Russell and Richard Fulford provided suggestions that greatly helped improved this research. The views expressed in this paper are those of the authors and do not necessarily reflect the views or policies of the U.S. Environmental Protection Agency. Any mention of trade names, products or services does not imply an endorsement by the U.S. Government or the U.S. Environmental Protection Agency (EPA). The EPA does not endorse any commercial products, services, or enterprises.
Author information
Authors and Affiliations
Corresponding author
Electronic Supplementary Material
ESM 1
(DOC 349 kb)
Rights and permissions
About this article
Cite this article
de Jesús Crespo, R., Méndez Lázaro, P. & Yee, S.H. Linking Wetland Ecosystem Services to Vector-borne Disease: Dengue Fever in the San Juan Bay Estuary, Puerto Rico. Wetlands 39, 1281–1293 (2019). https://doi.org/10.1007/s13157-017-0990-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13157-017-0990-5