Local environmental factors drive distributions of ecologically-contrasting mosquito species (Diptera: Culicidae).


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
20 08 2024
Historique:
received: 19 02 2024
accepted: 14 06 2024
medline: 21 8 2024
pubmed: 21 8 2024
entrez: 20 8 2024
Statut: epublish

Résumé

Mosquitoes are important vectors of disease pathogens and multiple species are undergoing geographical shifts due to global changes. As such, there is a growing need for accurate distribution predictions. Ecological niche modelling (ENM) is an effective tool to assess mosquito distribution patterns and link these to underlying environmental preferences. Typically, macroclimatic variables are used as primary predictors of mosquito distributions. However, they likely undervalue local conditions and intraspecific variation in environmental preferences. This is problematic, as mosquito control takes place at the local scale. Utilising high-resolution (10 × 10 m) Maxent ENMs on the island of Bonaire as model system, we explore the influence of local environmental variables on mosquito distributions. Our results show a distinct set of environmental variables shape distribution patterns across ecologically-distinct species, with urban variables strongly associated with introduced species like Aedes aegypti and Culex quinquefasciatus, while native species show habitat preferences for either mangroves, forests, or ephemeral water habitats. These findings underscore the importance of distinct local environmental factors in shaping distributions of different mosquitoes, even on a small island. As such, these findings warrant further studies aimed at predicting high-resolution mosquito distributions, opening avenues for preventative management of vector-borne disease risks amidst ongoing global change and ecosystem degradation.

Identifiants

pubmed: 39164289
doi: 10.1038/s41598-024-64948-y
pii: 10.1038/s41598-024-64948-y
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

19315

Subventions

Organisme : Ministry of Health, Welfare and Sport, The Netherlands
ID : MOBOCON
Organisme : Ministry of Health, Welfare and Sport, The Netherlands
ID : MOBOCON
Organisme : Ministry of Health, Welfare and Sport, The Netherlands
ID : MOBOCON
Organisme : Ministry of Health, Welfare and Sport, The Netherlands
ID : MOBOCON
Organisme : Ministry of Health, Welfare and Sport, The Netherlands
ID : MOBOCON
Organisme : Ministry of Health, Welfare and Sport, The Netherlands
ID : MOBOCON
Organisme : Ministry of Health, Welfare and Sport, The Netherlands
ID : MOBOCON

Informations de copyright

© 2024. The Author(s).

Références

Wilkerson, R. C., Linton, Y.-M. & Strickman, D. Mosquitoes of the World (John Hopkins University Press, 2020).
Kraemer, M. U. G. et al. Past and future spread of the arbovirus vectors Aedes aegypti and Aedes albopictus. Nat. Microbiol. 4, 854–863 (2019).
pubmed: 30833735 pmcid: 6522366 doi: 10.1038/s41564-019-0376-y
Caminade, C. et al. Global risk model for vector-borne transmission of Zika virus reveals the role of El Niño 2015. Proc. Natl. Acad. Sci. U. S. A. 114, 119–124 (2017).
pubmed: 27994145 doi: 10.1073/pnas.1614303114
Kraemer, M. U. G. et al. The global distribution of the arbovirus vectors Aedes aegypti and Ae. albopictus. Elife 4, 1–18 (2015).
doi: 10.7554/eLife.08347
Medley, K. A. Niche shifts during the global invasion of the Asian tiger mosquito, Aedes albopictus Skuse (Culicidae), revealed by reciprocal distribution models. Glob. Ecol. Biogeogr. 19, 122–133 (2010).
doi: 10.1111/j.1466-8238.2009.00497.x
Lounibos, L. P. Invasions by insects vectors of human disease. Annu. Rev. Entomol. 47, 233–266 (2002).
pubmed: 11729075 doi: 10.1146/annurev.ento.47.091201.145206
Ding, F., Fu, J., Jiang, D., Hao, M. & Lin, G. Mapping the spatial distribution of Aedes aegypti and Aedes albopictus. Acta Trop. 178, 155–162 (2018).
pubmed: 29191515 doi: 10.1016/j.actatropica.2017.11.020
Brady, O. J. et al. Global temperature constraints on Aedes aegypti and Ae. albopictus persistence and competence for dengue virus transmission. Parasit. Vectors https://doi.org/10.1186/1756-3305-7-338 (2014).
doi: 10.1186/1756-3305-7-338 pubmed: 25052008 pmcid: 4148136
Campbell, L. P. et al. Climate change influences on global distributions of dengue and chikungunya virus vectors. Philos. Trans. R. Soc. B Biol. Sci. 370, 1–9 (2015).
doi: 10.1098/rstb.2014.0135
Lafferty, K. D. The ecology of climate change and infectious diseases. Ecology 90, 888–900 (2009).
pubmed: 19449681 doi: 10.1890/08-0079.1
Reinhold, J. M., Lazzari, C. R. & Lahondère, C. Effects of the environmental temperature on Aedes aegypti and Aedes albopictus mosquitoes: A review. Insects https://doi.org/10.3390/insects9040158 (2018).
doi: 10.3390/insects9040158 pubmed: 30404142 pmcid: 6316560
Stresman, G. H. Beyond temperature and precipitation: Ecological risk factors that modify malaria transmission. Acta Trop. 116, 167–172 (2010).
pubmed: 20727338 doi: 10.1016/j.actatropica.2010.08.005
Schrama, M. et al. Human practices promote presence and abundance of disease-transmitting mosquito species. Sci. Rep. 10, 1–6 (2020).
doi: 10.1038/s41598-020-69858-3
Zhang, Y., Bi, P. & Hiller, J. E. Climate change and the transmission of vector-borne diseases: A review. Asia. Pac. J. Public Health 20, 64–76 (2008).
pubmed: 19124300 doi: 10.1177/1010539507308385
Reiskind, M. H., Griffin, R. H., Janairo, M. S. & Hopperstad, K. A. Mosquitoes of field and forest: the scale of habitat segregation in a diverse mosquito assemblage. Med. Vet. Entomol. 31, 44–54 (2017).
pubmed: 27759165 doi: 10.1111/mve.12193
O’Brien, V. A. & Reiskind, M. H. Host-seeking mosquito distribution in habitat mosaics of southern great plains cross-timbers. J. Med. Entomol. 50, 1231–1239 (2013).
pubmed: 24843927 doi: 10.1603/ME13007
Chandrasegaran, K., Lahondère, C., Escobar, L. E. & Vinauger, C. Linking mosquito ecology, traits, behavior, and disease transmission. Trends Parasitol. 36, 393–403 (2020).
pubmed: 32191853 doi: 10.1016/j.pt.2020.02.001
Barker, J. R. & MacIsaac, H. J. Species distribution models applied to mosquitoes: Use, quality assessment, and recommendations for best practice. Ecol. Model. 472, 110073 (2022).
doi: 10.1016/j.ecolmodel.2022.110073
Cianci, D., Hartemink, N. & Ibáñez-Justicia, A. Modelling the potential spatial distribution of mosquito species using three different techniques. Int. J. Health Geogr. 14, 1–10 (2015).
doi: 10.1186/s12942-015-0001-0
Khatchikian, C., Sangermano, F., Kendell, D. & Livdahl, T. Evaluation of species distribution model algorithms for fine-scale container-breeding mosquito risk prediction. Med. Vet. Entomol. 25, 268–275 (2011).
pubmed: 21198711 doi: 10.1111/j.1365-2915.2010.00935.x
Raes, N. & Ter Steege, H. A null-model for significance testing of presence-only species distribution models. Ecography (Cop.) 30, 727–736 (2007).
doi: 10.1111/j.2007.0906-7590.05041.x
Estallo, E. L. et al. Modelling the distribution of the vector Aedes aegypti in a central Argentine city. Med. Vet. Entomol. 32, 451–461 (2018).
pubmed: 30027565 doi: 10.1111/mve.12323
Johnson, T. L. et al. Modeling the environmental suitability for Aedes (Stegomyia) aegypti and Aedes (Stegomyia) albopictus (Diptera: Culicidae) in the Contiguous United States. J. Med. Entomol. 54, 1605–1614 (2017).
pubmed: 29029153 doi: 10.1093/jme/tjx163
Hopperstad, K. A., Sallam, M. F. & Reiskind, M. H. Estimations of fine-scale species distributions of Aedes aegypti and Aedes albopictus (Diptera: Culicidae) in Eastern Florida. J. Med. Entomol. 58, 699–707 (2021).
pubmed: 33128447 doi: 10.1093/jme/tjaa216
Li, Q. et al. Ecological niche modeling identifies fine-scale areas at high risk of dengue fever in the Pearl River delta, China. Int. J. Environ. Res. Public Health 14, 1–13 (2017).
doi: 10.3390/ijerph14010001
Lippi, C. A. et al. Trends in mosquito species distribution modeling: Insights for vector surveillance and disease control. Parasites Vectors 16, 1–17 (2023).
doi: 10.1186/s13071-023-05912-z
Belkin, J. N., Heinemann, S. J. & Page, W. A. The Culicidae of Jamaica (Mosquito Studies. XXI). Contrib. Am. Entomol. Inst. 6, 1–458 (1970).
Van der Beek, J. G. et al. Taxonomy, ecology and distribution of the mosquitoes (Diptera: Culicidae) of the Dutch Leeward Islands, with a key to the adults and fourth instar larvae. Contrib. Zool. 89, 373–392 (2020).
doi: 10.1163/18759866-bja10005
Van der Kuyp, E. Mosquitoes of the Netherlands Antilles and their hygienic importance. Stud. Fauna Curaçao Other Caribb. Islands 5, 37–114 (1954).
Bonne, C. & Bonne-Wepster, J. Mosquitoes of Surinam. A Study of Neotropical Mosquitoes (Het Instituut, 1925).
Cova-García, P., Sutil, E. & Rausseo, J. A. Mosquitos de Venezuela Vol. II (Ministerio de Sanidad y Asistencia Social, 1966).
Cova-García, P., Sutil, E. & Rausseo, J. A. Mosquitos de Venezuela Vol. I (Ministerio de Sanidad y Asistencia Social, 1966).
Verdonschot, P. F. M. & Besse-Lototskaya, A. A. Flight distance of mosquitoes (Culicidae): A metadata analysis to support the management of barrier zones around rewetted and newly constructed wetlands. Limnologica 45, 69–79 (2014).
doi: 10.1016/j.limno.2013.11.002
Elmore, C. M. Jr. & Schoof, H. F. Dispersal of Aedes taeniorhynchus Weidemann near Savannah. Georgia. Mosquito News 23, 1–7 (1963).
Powell, J. R. & Tabachnick, W. J. History of domestication and spread of Aedes aegypti—A review. Mem. Inst. Oswaldo Cruz 108, 11–17 (2013).
pubmed: 24473798 pmcid: 4109175 doi: 10.1590/0074-0276130395
Belkin, J. N. The Mosquitoes of the South Pacific (Diptera, Culicidae) Vol. 1 and 2 (University of California Press, 1962).
Arnell, J. H. Mosquito studies (Diptera, Culicidae). A revision of the genus Haemagogus. Contrib. Am. Entomol. Inst. 10, 1–174 (1973).
Chase, F. A. & Holthuis, L. B. Land and fresh water decapod Crustacea from The Leeward Group and Northern South America. Stud. Fauna Curaçao Other Caribb. Islands 3, 21–28 (1948).
Lanzaro, G. C., Collier, T. C. & Lee, Y. Defining genetic, taxonomic, and geographic boundaries among species of the Psorophora confinnis (Diptera: Culicidae) complex in North and South America. J. Med. Entomol. 52, 907–917 (2015).
pubmed: 26336224 doi: 10.1093/jme/tjv084
Freitas, J. a De, Nijhof, B. S. J., Rojer, a C. & Debrot, a O. Landscape Ecological Vegetation Map of Bonaire. http://www.dcbd.nl/sites/www.dcbd.nl/files/documents/Freitasetal2005LandscapeecologicalvegetationmapBonaire.pdf (2005).
KNMI. KNMI: hour data Caribbean area. https://www.knmi.nl/nederland-nu/klimatologie/uurgegevens_Caribisch_gebied (2023).
Mücher, C. A. & Verweij, P. J. F. M. Land Cover Classification Bonaire. (2020).
Brisco, K. K., Cornel, A. J., Lee, Y., Mouatcho, J. & Braack, L. Comparing efficacy of a sweep net and a dip method for collection of mosquito larvae in large bodies of water in South Africa. F1000Research 5, 1–9 (2016).
doi: 10.12688/f1000research.8351.1
Van der Beek, J. G. et al. First record of a phlebotomine sand fly (Diptera: Psychodidae) on the Dutch Caribbean island of Curaçao. Deinsea 22, 23–30 (2024).
Lane, J. Neotropical Culicidae Vol. 1 (University of São Paulo, 1953).
Lane, J. Neotropical Culicidae Vol. 2 (University of São Paulo, 1953).
Pratt, H. D. Key to the Culicidae of Puerto Rico. (1969).
Darsie, R. F., Taylor, D. S., Prusak, Z. A. & Verna, T. N. Checklist of the mosquitoes of the Bahamas with three additions to its fauna and keys to the adult females and fourth instars. J. Am. Mosq. Control Assoc. 26, 127–134 (2010).
pubmed: 20649121 doi: 10.2987/09-5982.1
Burkett-Cadena, N. D. Mosquitoes of the Southeastern United States (The University of Alabama Press, 2013).
Dowle, M. & Srinivasan, A. data.table: Extension of `data.frame`. R package version 1.14.8.
Wickham, H., François, R., Henry, L., Müller, K. & Vaughan, D. dplyr: A Grammar of Data Manipulation. R package version 1.1.2.
Pierce, D. ncdf4: Interface to Unidata netCDF (Version 4 or Earlier) Format Data Files. R package version 1.22.
Hijmans, R. J. raster: Geographic Data Analysis and Modeling. R package version 3.6-26.
Bivand, R., Keitt, T. & Rowlingson, B. rgdal: Bindings for the ‘Geospatial’ Data Abstraction Library. R package version 1.6-7.
Bivand, R. & Rundel, C. rgeos: Interface to Geometry Engine—Open Source ('GEOS’). R package version 0.6-4.
Pebesma, E. Simple features for R: Standardized support for spatial vector data. R J. 10, 439–446 (2018).
doi: 10.32614/RJ-2018-009
Bivand, R., Pebesma, E. & Gomez-Rubio, V. Applied Spatial Data Analysis with R 2nd edn. (Springer, 2013).
doi: 10.1007/978-1-4614-7618-4
Oksanen, J. et al. vegan: Community Ecology Package. R package version 2.6-4.
Dray, S., Dufour, A. & Chessel, D. The ade4 package - II: Two-table and K-table methods. R News 7, 47–52 (2007).
Hijmans, R. J., Phillips, S., Leathwick, J. & Elith, J. dismo: Species Distribution Modeling. R package version 1.3-14.
Broennimann, O., Di Cola, V. & Guisan, A. ecospat: Spatial Ecology Miscellaneous Methodsitle. R package version 3.5.1.
Kass, J. M. et al. ENMeval 2.0: Redesigned for customizable and reproducible modeling of species’ niches and distributions. Methods Ecol. Evol. 12, 1602–1608 (2021).
doi: 10.1111/2041-210X.13628
Warren, D. & Dinnage, R. ENMTools: Analysis of Niche Evolution using Niche and Distribution Models.
Evans, J. S. & Murphy, M. A. spatialEco. R package version 2.0-1.
Van Oosterhout, L. et al. An integrated assessment of climate change impacts and implications on Bonaire. Econ. Disasters Clim. Chang. 7, 147–178 (2023).
doi: 10.1007/s41885-023-00127-z
Phillips, S. J., Anderson, R. P. & Schapire, R. E. Maximum entropy modeling of species geographic distributions. Ecol. Model 190, 231–259 (2006).
doi: 10.1016/j.ecolmodel.2005.03.026
Wisz, M. S. et al. Effects of sample size on the performance of species distribution models. Divers. Distrib. 14, 763–773 (2008).
doi: 10.1111/j.1472-4642.2008.00482.x
Valavi, R. et al. Modelling climate change effects on Zagros forests in Iran using individual and ensemble forecasting approaches. Theor. Appl. Climatol. 137, 1015–1025 (2019).
doi: 10.1007/s00704-018-2625-z
Morales, N. S., Fernández, I. C. & Baca-González, V. MaxEnt’s parameter configuration and small samples: Are we paying attention to recommendations? A systematic review. PeerJ 2017, 1–16 (2017).
Low, B. W., Zeng, Y., Tan, H. H. & Yeo, D. C. J. Predictor complexity and feature selection affect Maxent model transferability: Evidence from global freshwater invasive species. Divers. Distrib. 27, 497–511 (2021).
doi: 10.1111/ddi.13211
Velasco, J. A. & González-Salazar, C. Akaike information criterion should not be a “test” of geographical prediction accuracy in ecological niche modelling. Ecol. Inform. 51, 25–32 (2019).
doi: 10.1016/j.ecoinf.2019.02.005
Bohl, C. L., Kass, J. M. & Anderson, R. P. A new null model approach to quantify performance and significance for ecological niche models of species distributions. J. Biogeogr. 46, 1101–1111 (2019).
doi: 10.1111/jbi.13573
Feng, X., Park, D. S., Liang, Y., Pandey, R. & Papeş, M. Collinearity in ecological niche modeling: Confusions and challenges. Ecol. Evol. 9, 10365–10376 (2019).
pubmed: 31624555 pmcid: 6787792 doi: 10.1002/ece3.5555
Rödder, D., Schmidtlein, S., Veith, M. & Lötters, S. Alien invasive slider turtle in unpredicted habitat: A matter of niche shift or of predictors studied?. PLoS One https://doi.org/10.1371/journal.pone.0007843 (2009).
doi: 10.1371/journal.pone.0007843 pubmed: 19956684 pmcid: 2776975
Zeng, Y., Low, B. W. & Yeo, D. C. J. Novel methods to select environmental variables in MaxEnt: A case study using invasive crayfish. Ecol. Modell. 341, 5–13 (2016).
doi: 10.1016/j.ecolmodel.2016.09.019
Petitpierre, B., Broennimann, O., Kueffer, C., Daehler, C. & Guisan, A. Selecting predictors to maximize the transferability of species distribution models: Lessons from cross-continental plant invasions. Glob. Ecol. Biogeogr. 26, 275–287 (2017).
doi: 10.1111/geb.12530
Jueterbock, A. ‘MaxentVariableSelection’ vignette. https://cran.r-project.org/web/packages/MaxentVariableSelection/vignettes/MaxentVariableSelection.pdf (2016).
Shabani, F., Kumar, L. & Ahmadi, M. Assessing accuracy methods of species distribution models: AUC, Specificity, Sensitivity and the True Skill Statistic. Glob. J. Hum. Soc. Sci. 18, 6–18 (2018).
Konowalik, K. & Nosol, A. Evaluation metrics and validation of presence-only species distribution models based on distributional maps with varying coverage. Sci. Rep. 11, 1–15 (2021).
doi: 10.1038/s41598-020-80062-1
Fielding, A. H. & Bell, J. F. A review of methods for the assessment of prediction errors in conservation presence/absence models. Environ. Conserv. 24, 38–49 (1997).
doi: 10.1017/S0376892997000088
Yackulic, C. B. et al. Presence-only modelling using MAXENT: When can we trust the inferences?. Methods Ecol. Evol. 4, 236–243 (2013).
doi: 10.1111/2041-210x.12004
Merow, C., Smith, M. J. & Silander, J. A. A practical guide to MaxEnt for modeling species’ distributions: What it does, and why inputs and settings matter. Ecography (Cop.) 36, 1058–1069 (2013).
doi: 10.1111/j.1600-0587.2013.07872.x
Hirzel, A. H., Le Lay, G., Helfer, V., Randin, C. & Guisan, A. Evaluating the ability of habitat suitability models to predict species presences. Ecol. Modell. 199, 142–152 (2006).
doi: 10.1016/j.ecolmodel.2006.05.017

Auteurs

Roel M Wouters (RM)

NL Biodiversity and Society Research Group, Naturalis Biodiversity Center, 2333 CR, Leiden, The Netherlands. WoutersRoel1@gmail.com.
Institute of Environmental Sciences, Leiden University, 2333 CC, Leiden, The Netherlands. WoutersRoel1@gmail.com.
Department of Ecology, Faculty of Science, Charles University, 12844, Prague, Czechia. WoutersRoel1@gmail.com.

Wouter Beukema (W)

NL Biodiversity and Society Research Group, Naturalis Biodiversity Center, 2333 CR, Leiden, The Netherlands.
RAVON, Reptile, Amphibian and Fish Conservation Netherlands, 6501 BK, Nijmegen, The Netherlands.

Maarten Schrama (M)

Institute of Environmental Sciences, Leiden University, 2333 CC, Leiden, The Netherlands.

Koos Biesmeijer (K)

NL Biodiversity and Society Research Group, Naturalis Biodiversity Center, 2333 CR, Leiden, The Netherlands.
Institute of Environmental Sciences, Leiden University, 2333 CC, Leiden, The Netherlands.

Marieta A H Braks (MAH)

Institute of Environmental Sciences, Leiden University, 2333 CC, Leiden, The Netherlands.
Centre for Zoonoses and Environmental Microbiology, Centre for Infectious Disease Control, National Institute for Public Health and the Environment, 3721 MA, Bilthoven, The Netherlands.

Pepijn Helleman (P)

Institute of Environmental Sciences, Leiden University, 2333 CC, Leiden, The Netherlands.

Francis Schaffner (F)

Francis Schaffner Consultancy, 4125, Riehen, Switzerland.

Joey van Slobbe (J)

Bonaire Public Health Department, Public Body Bonaire, 4PXG+GH4, Kralendijk, Dutch Caribbean, The Netherlands.

Arjan Stroo (A)

Centre for Monitoring of Vectors (CMV), Netherlands Food and Consumer Product Safety Authority (NVWA), 6706 EA, Wageningen, The Netherlands.

Jordy G van der Beek (JG)

NL Biodiversity and Society Research Group, Naturalis Biodiversity Center, 2333 CR, Leiden, The Netherlands.
Institute of Environmental Sciences, Leiden University, 2333 CC, Leiden, The Netherlands.
Pandemic and Disaster Preparedness Center, Delft, Rotterdam, The Netherlands.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH