New Baseline Environmental Assessment of Mosquito Ecology in Northern Haiti during Increased Urbanization

ABSTRACT: The catastrophic 2010 earthquake in Port-au-Prince, Haiti, led to the large-scale displacement of over 2.3 million people, resulting in rapid and unplanned urbanization in northern Haiti. This study evaluated the impact of this unplanned urbanization on mosquito ecology and vector-borne diseases by assessing land use and change patterns. Land-use classification and change detection were carried out on remotely sensed images of the area for 2010 and 2013. Change detection identified areas that went from agricultural, forest, or bare-land pre-earthquake to newly developed and urbanized areas post-earthquake. Areas to be sampled for mosquito larvae were subsequently identified. Mosquito collections comprised five genera and ten species, with the most abundant species being Culex quinquefasciatus 35% (304/876), Aedes albopictus 27% (238/876), and Aedes aegypti 20% (174/876). All three species were more prevalent in urbanized and newly urbanized areas. Anopheles albimanus, the predominate malaria vector, accounted for less than 1% (8/876) of the collection. A set of spectral indices derived from the recently launched Landsat 8 satellite was used as covariates in a species distribution model. The indices were used to produce probability surfaces maps depicting the likelihood of presence of the three most abundant species within 30 m pixels. Our findings suggest that the rapid urbanization following the 2010 earthquake has increased the amount of area with suitable habitats for urban mosquitoes, likely influencing mosquito ecology and posing a major risk of introducing and establishing emerging vector-borne diseases.

[1]  D. Addiss The 6th Meeting of the Global Alliance to Eliminate Lymphatic Filariasis: A half-time review of lymphatic filariasis elimination and its integration with the control of other neglected tropical diseases , 2010, Parasites & Vectors.

[2]  Caroline W. Kabaria,et al.  Human population, urban settlement patterns and their impact on Plasmodium falciparum malaria endemicity , 2008, Malaria Journal.

[3]  E. Harris,et al.  Characterization of Aedes aegypti (Diptera: Culcidae) Production Sites in Urban Nicaragua , 2007, Journal of medical entomology.

[4]  N. Gratz,et al.  Critical review of the vector status of Aedes albopictus , 2004, Medical and veterinary entomology.

[5]  Miroslav Dudík,et al.  Modeling of species distributions with Maxent: new extensions and a comprehensive evaluation , 2008 .

[6]  Charles B. Halpern,et al.  Combining local- and large-scale models to predict the distributions of invasive plant species. , 2010, Ecological applications : a publication of the Ecological Society of America.

[7]  R. Barrera,et al.  Use of the pupal survey technique for measuring Aedes aegypti (Diptera: Culicidae) productivity in Puerto Rico. , 2006, The American journal of tropical medicine and hygiene.

[8]  P. Kittayapong,et al.  Mosquito Vector Diversity across Habitats in Central Thailand Endemic for Dengue and Other Arthropod-Borne Diseases , 2013, PLoS neglected tropical diseases.

[9]  Hanqiu Xu,et al.  Analysis of Impervious Surface and its Impact on Urban Heat Environment using the Normalized Difference Impervious Surface Index (NDISI) , 2010 .

[10]  Hanqiu Xu Modification of normalised difference water index (NDWI) to enhance open water features in remotely sensed imagery , 2006 .

[11]  A. Tatem,et al.  The effects of urbanization on global Plasmodium vivax malaria transmission , 2012, Malaria Journal.

[12]  Boris Schröder,et al.  The importance of correcting for sampling bias in MaxEnt species distribution models , 2013 .

[13]  J. Sexton,et al.  The biting and resting behavior of Anopheles albimanus in northern Haiti. , 1986, Journal of the American Mosquito Control Association.

[14]  A. Assefa,et al.  Therapeutic efficacy of Artemether/Lumefantrine (Coartem®) against Plasmodium falciparum in Kersa, South West Ethiopia , 2010, Parasites & Vectors.

[15]  J. Keating,et al.  Characterization of aquatic mosquito habitat, natural enemies, and immature mosquitoes in the Artibonite Valley, Haiti , 2008, Journal of vector ecology : journal of the Society for Vector Ecology.

[16]  L. F. Chaves,et al.  Combined Sewage Overflow Enhances Oviposition of Culex quinquefasciatus (Diptera: Culicidae) in Urban Areas , 2009, Journal of medical entomology.

[17]  J. R. Landis,et al.  The measurement of observer agreement for categorical data. , 1977, Biometrics.

[18]  S. P. Kachur,et al.  Malaria survey in post-earthquake Haiti--2010. , 2012, The American journal of tropical medicine and hygiene.

[19]  R. Garry,et al.  Dengue in the Dominican Republic: Epidemiology for 2004 , 2005, Microscopy research and technique.

[20]  R. Real,et al.  AUC: a misleading measure of the performance of predictive distribution models , 2008 .

[21]  K. Kain,et al.  Lack of Evidence for Chloroquine-Resistant Plasmodium falciparum Malaria, Leogane, Haiti , 2012, Emerging infectious diseases.

[22]  María del Carmen Arias Fernández,et al.  The first report of Aedes (Stegomyia) albopictus in Haiti. , 2012, Memorias do Instituto Oswaldo Cruz.

[23]  F. Sangermano,et al.  Evaluation of species distribution model algorithms for fine‐scale container‐breeding mosquito risk prediction , 2011, Medical and veterinary entomology.

[24]  Eric F. Lambin,et al.  Impact of Land-use Change on Dengue and Malaria in Northern Thailand , 2007, EcoHealth.

[25]  Richard Miller,et al.  Predictive modeling and mapping sage grouse (Centrocercus urophasianus) nesting habitat using Maximum Entropy and a long-term dataset from Southern Oregon , 2008, Ecol. Informatics.

[26]  B. Wilcox,et al.  The ecological dimensions of vector-borne disease research and control. , 2009, Cadernos de saude publica.

[27]  Hanqiu Xu,et al.  A new index for delineating built‐up land features in satellite imagery , 2008 .

[28]  Hanqiu Xu Extraction of Urban Built-up Land Features from Landsat Imagery Using a Thematicoriented Index Combination Technique , 2007 .

[29]  Hanqiu Xu,et al.  The impact of impervious surface development on land surface temperature in a subtropical city: Xiamen, China , 2013 .

[30]  Trevor Hastie,et al.  A statistical explanation of MaxEnt for ecologists , 2011 .

[31]  L. P. Lounibos,et al.  Ecological Links Between Water Storage Behaviors and Aedes aegypti Production: Implications for Dengue Vector Control in Variable Climates , 2010, EcoHealth.

[32]  J. Kazura,et al.  Perspectives on Haiti Two Years after the Earthquake , 2012, The American journal of tropical medicine and hygiene.

[33]  J. Le bras,et al.  Chloroquine-Resistant Malaria in Travelers Returning from Haiti after 2010 Earthquake , 2012, Emerging infectious diseases.

[34]  R. Barrera,et al.  Septic tanks as larval habitats for the mosquitoes Aedes aegypti and Culex quinquefasciatus in Playa‐Playita, Puerto Rico , 2010, Medical and veterinary entomology.

[35]  Richard H. Cuenca,et al.  Application of Landsat to Evaluate Effects of Irrigation Forbearance , 2013, Remote. Sens..

[36]  R. Halvorsen A strict maximum likelihood explanation of MaxEnt, and some implications for distribution modelling , 2013 .

[37]  A. Githeko,et al.  A geographic sampling strategy for studying relationships between human activity and malaria vectors in urban Africa. , 2003, The American journal of tropical medicine and hygiene.

[38]  Eli Schwartz,et al.  Malaria among patients and aid workers consulting a primary healthcare centre in Leogane, Haiti, November 2010 to February 2011 - a prospective observational study. , 2011, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[39]  I. Wayan Nuarsa,et al.  Enhanced Built-Up and Bareness Index (EBBI) for Mapping Built-Up and Bare Land in an Urban Area , 2012, Remote. Sens..

[40]  M. McMorrow,et al.  The increase of imported malaria acquired in Haiti among US travelers in 2010. , 2012, The American journal of tropical medicine and hygiene.

[41]  R. Novak,et al.  Integrated vector management for malaria control , 2008, Malaria Journal.

[42]  Omri Allouche,et al.  Assessing the accuracy of species distribution models: prevalence, kappa and the true skill statistic (TSS) , 2006 .

[43]  S. Lindsay,et al.  Promoting Health and Advancing Development through Improved Housing in Low-Income Settings , 2013, Journal of Urban Health.

[44]  日本リモート・センシング協会 Remote sensing note , 1993 .

[45]  Jean Gaudart,et al.  The Dry Season in Haiti: a Window of Opportunity to Eliminate Cholera , 2013, PLoS currents.

[46]  P. Atkinson,et al.  Opinion — tropical infectious diseases: Urbanization, malaria transmission and disease burden in Africa , 2005, Nature Reviews Microbiology.

[47]  Julia A. Barsi,et al.  The next Landsat satellite: The Landsat Data Continuity Mission , 2012 .

[48]  Ehrenkranz Nj,et al.  Endemic Dengue Virus Infection in Hispaniola. I. Haiti , 1976 .

[49]  Wei Wu,et al.  Maximum entropy niche-based modeling (Maxent) of potential geographical distributions of fruit flies Dacus bivittatus, D. ciliatus and D. vertebrates (Diptera: Tephritidae). , 2009 .

[50]  P. Villa Mapping urban growth using Soil and Vegetation Index and Landsat data: The Milan (Italy) city area case study , 2012 .

[51]  R. M. Gleiser,et al.  Mosquito Fauna Inhabiting Water Bodies in the Urban Environment of Córdoba City, Argentina, Following a St. Louis Encephalitis Outbreak , 2010, Journal of vector ecology : journal of the Society for Vector Ecology.

[52]  P. McCall,et al.  Insecticide‐treated bednets to control dengue vectors: preliminary evidence from a controlled trial in Haiti , 2008, Tropical medicine & international health : TM & IH.

[53]  Zhenfeng Shao,et al.  MNDISI: a multi-source composition index for impervious surface area estimation at the individual city scale , 2013 .

[54]  M. Malecela,et al.  Urban lymphatic filariasis in the metropolis of Dar es Salaam, Tanzania , 2013, Parasites & Vectors.

[55]  D. Norris,et al.  Mosquito-borne Diseases as a Consequence of Land Use Change , 2004, EcoHealth.

[56]  J. Muñoz-Jordán,et al.  A cluster of dengue cases in American missionaries returning from Haiti, 2010. , 2012, The American journal of tropical medicine and hygiene.

[57]  Robert P. Anderson,et al.  Maximum entropy modeling of species geographic distributions , 2006 .

[58]  C. Raccurt Le point sur le paludisme en Haïti , 2004 .

[59]  John C. Beier,et al.  A geographical sampling method for surveys of mosquito larvae in an urban area using high-resolution satellite imagery , 2008, Journal of vector ecology : journal of the Society for Vector Ecology.

[60]  P. Hernandez,et al.  The effect of sample size and species characteristics on performance of different species distribution modeling methods , 2006 .

[61]  D. Addiss,et al.  Geographic distribution of lymphatic filariasis in Haiti. , 2004, The American journal of tropical medicine and hygiene.

[62]  David L. Smith,et al.  Urbanization and the global malaria recession , 2013, Malaria Journal.

[63]  C. Paupy,et al.  Aedes albopictus, an arbovirus vector: from the darkness to the light. , 2009, Microbes and infection.