Rapid emergence of most vector-borne diseases (VBDs) may be associated with range expansion of vector populations. Culex quinquefasciatus Say 1823 is a potential vector of West Nile virus, Saint Louis encephalitis virus, and lymphatic filariasis. We estimated the potential distribution of Cx. quinquefasciatus under both current and future climate conditions. The present potential distribution of Cx. quinquefasciatus showed high suitability across low-latitude parts of the world, reflecting the current distribution of the species. Suitable conditions were identified also in narrow zones of North Africa and Western Europe. Model transfers to future conditions showed a potential distribution similar to that under present-day conditions, although with higher suitability in southern Australia. Highest stability with changing climate was between 30°S and 30°N. The areas present high agreement among diverse climate models as regards distributional potential in the future, but differed in anticipating potential for distribution in North and Central Africa, southern Asia, central USA, and southeastern Europe. Highest disparity in model predictions across representative concentration pathways (RCPs) was in Saudi Arabia and Europe. The model predictions allow anticipation of changing distributional potential of the species in coming decades.
Citation: Samy AM, Elaagip AH, Kenawy MA, Ayres CFJ, Peterson AT, Soliman DE (2016) Climate Change Influences on the Global Potential Distribution of the Mosquito Culex quinquefasciatus, Vector of West Nile Virus and Lymphatic Filariasis. PLoS ONE 11(10): e0163863. https://doi.org/10.1371/journal.pone.0163863
Editor: Shannon L. LaDeau, Cary Institute of Ecosystem Studies, UNITED STATES
Received: April 5, 2016; Accepted: September 15, 2016; Published: October 3, 2016
Copyright: © 2016 Samy et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: All data are openly available via Figshare repository (https://dx.doi.org/10.6084/m9.figshare.3487046).
Funding: AMS was supported by the Graduate Fulbright Egyptian Mission Program (EFMP). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Mosquitoes are well known as vectors of many human and animal pathogens worldwide. The world has seen recent outbreaks and emergences of several tropical diseases caused by arboviruses and transmitted by mosquitoes. Species of the Culex pipiens complex transmit major etiological agents of human and animal diseases: West Nile virus (WNV), Saint Louis encephalitis virus (SLEV), Sindbis virus, Rift Valley fever virus (RVFV) and lymphatic filariasis (LF) [1, 2]. Cx. pipiens is the most widely distributed mosquito worldwide. It comprises a complex of subspecies or forms, including Cx. pipiens Linnaeus 1758, Cx. quinquefasciatus Say 1823, Cx. pipiens pallens Coquillett 1898, and Cx. australicus Dobrotworsky & Drummond 1953. These mosquitoes are closely associated with human disease in many regions [3, 4]. The Cx. pipiens complex is viewed as a questionable point in mosquito taxonomy, because species (or forms) are indistinguishable morphologically and can be separated only by molecular analysis [5, 6] or details of behavioral and physiological characteristics .
In terms of geographic distribution, Cx. quinquefasciatus differs from Cx. pipiens in that the former is most prevalent in tropical and sub-tropical areas [8, 9]. In the southern United States, Cx. quinquefasciatus is the primary vector of Saint Louis encephalitis virus and West Nile virus [10–12]. Culex quinquefasciatus is identified as the major vector of the filarial nematode, Wuchereria bancrofti (Cobbold, 1877) in Brazil , tropical Africa, and Southeast Asia , and RVFV in Africa [14, 15].
Recently, Ayres  raised the possibility of Cx. quinquefasciatus may be involved in Zika virus (ZIKV) urban transmission in Brazil, where its abundance is approximately 20-fold higher than the known ZIKV vector, Aedes aegypti. ZIKV infection has been associated with neurological complications, such as Guillain-Barré syndrome and also with a severe malformation, fetal microcephaly [17, 18]. Currently, ZIKV is spreading globally, and ZIKV outbreaks have been reported in 65 countries . Experimental studies of vector competence have confirmed that C. quinquefasciatus can disseminate and transmit ZIKV . Ongoing projects are attempting to detect ZIKV in natural Culex populations in areas where epidemics are occurring, to provide the final piece of evidence for this hypothesis.
Vector-borne diseases are vulnerable to climate changes and may emerge in response to global warming , such that patterns of transmission of WNV and other diseases are likely to change in coming decades . This effect may result from expansions of vector ranges, which place non-endemic areas at risk if sources of infections are available . Studies of field populations of Culex mosquitoes in general have revealed that increases in temperature are likely to accelerate mosquito development , increase vector abundance, and lead to emergence of diseases . For example, in WNV epidemiology  rising temperature and changes in rainfall allowed circulation of WNV in different areas in southern USA, Europe, western Asia, and the eastern Mediterranean . In addition, transmission of WNV can be accelerated with increasing temperatures, as demonstrated by Kilpatrick et al. (2008)  for West Nile Virus in Culex pipiens.
Important knowledge gaps remain regarding effects of climate and climate change on emergence of several vector-borne diseases in the world. Here, we provide detailed global maps of current potential distributions of Cx. quinquefasciatus, the potential vector for WNV, SLEV, and LF, and examine possible changes in the potential distribution of the species under future climatic conditions, based on outputs of 11 general circulation models (GCMs) and 4 representative concentration pathways (RCPs).
Materials and Methods
Occurrence records for Culex quinquefasciatus were obtained from VectorMap (www.vectormap.org), the Global Biodiversity Information Facility (GBIF;www.gbif.org), and the PubMed database using the search term “Culex quinquefasciatus”. We included all records with geographic coordinates, and filtered data to eliminate duplicate records in the final data set. The final records of Cx. quinquefasciatus were divided into two halves: 50% for calibrating ecological niche models for the species, and 50% for evaluating predictions of those models.
Data from WorldClim (www.worldclim.org) were used to characterize current global climates, including 19 bioclimatic variables originally derived from monthly temperature and rainfall values collected from weather stations in 1950–2000 . The data are available at three spatial resolutions; we selected the coarsest (10’), in light of the global extent of our model calibration area. To characterize influences of climate change on the distribution of Cx. quinquefasciatus, we selected parallel data sets for four representative concentration pathways (RCPs; RCP 2.6, RCP 4.5, RCP 6.0, and RCP 8.5) accounting for different future emission scenarios from the Coupled Model Intercomparison Project Phase 5 (CMIP5) available in WorldClim archive. For each RCP, we included 11 GCMs for which data for all RCPs were available, for a total of 44 combinations (S1 File). Bioclimatic variables 8–9 and 18–19 were omitted from analysis, in light of known spatial artifacts in those variables. The remaining of 15 variables were submitted to a principle components analysis (PCA) to reduce the dimensionality and avoid multicollinearity between variables . The component loadings in the present-day data were used to transform future-climate data using the PCAProjection function in ENMGadgets  in R software version 3.2.0 .
Ecological niche modeling
The Grinnellian ecological niche of Cx. quinquefasciatus was estimated using the maximum entropy algorithm implemented in Maxent v3.3.3e . The Grinnellian niche is characterized as the set of environmental conditions needed by the species to maintain populations without immigrational subsidy . The models were calibrated based on the first six principal components from the PCA analysis described above, and then transferred to our 44 views of potential future conditions. We ran 100 bootstrap replicates in Maxent, and the median output was used in analyses. The median of medians across all GCMs for each RCP was as a best guess of conditions under that RCP, and final models were thresholded based on a maximum allowable omission error rate of 5% (E = 5%; ), assuming that up to 5% of occurrence data may include errors that misrepresented environmental values. Uncertainty associated with the models was estimated as the range (maximum–minimum) of suitability across models for each RCP .
The model performance was evaluated using partial receiver operating characteristic (ROC) statistics applied to the 50% subset of occurrences left out before model calibration for testing. This approach avoids possible errors raised with traditional ROC provided in Maxent outputs . Partial ROC statistics was calculated using the PartialROC function available in ENMGadgets package.
We assembled 1402 occurrence records for Cx. quinquefasciatus. The full data set is available at https://dx.doi.org/10.6084/m9.figshare.3487046. Overall, the distribution was concentrated on southern continents, although the species was well represented in North America and southern Asia (Fig 1).
The potential distribution of Cx. quinquefasciatus under present-day conditions showed high suitability across southern North America, much of South America, sub-Saharan Africa, south Asia, and most of Australia and New Zealand (Fig 2). Parts of West Africa, Western Europe, and East Asia were modeled as suitable environmentally, although few occurrence points came from these areas. Model predictions performed better than random expectations, based on the partial ROC test (P < 0.001).
Blue shaded areas were modeled as suitable; white areas were modeled as unsuitable.
Transferring the Cx. quinquefasciatus model to future conditions showed an overall distributional pattern similar to that under present-day conditions; however, the species showed higher suitability in southern Australia under future conditions (Fig 3). The future potential distribution was thus estimated as including the southern United States, Central and South America, central and southern Africa, South Asia, and Australia.
Red areas are modeled suitable conditions; white areas are unsuitable conditions.
The potential distributional area of Cx. quinquefasciatus increased from present-day conditions to RCP 6.0, and then decreased in RCP 8.5. Area increased by 4.9% from present-day conditions to RCP 6.0 then decreased by 1.3% from RCP 6.0 to RCP 8.5 (details for each GCM are presented in supporting information 2). Detailed maps of Cx. quinquefasciatus model stability in coming decades (Fig 4) illustrate differences among RCPs. Highest stability of the models among present-day and future conditions appeared in the belt between 30°S and 30°N, which includes much of South America, central and southern Africa, South and East Asia, Australia, and New Zealand. The same pattern of suitability was also observed in a narrow zone in Western Europe and the southern United States. Areas presenting full agreement among all future climate models in anticipating distributional potential in the future include only Kangaroo Island (Australia), Somalia, and Colombia. Areas showing low agreement (= high uncertainty) among climate models as regards distributional potential in the future included North and Central Africa, Afghanistan, Pakistan, the central United States, and southeastern Europe. Interactive maps for present-day and future distribution of Cx. quinquefasciatus are presented in the supplementary materials (S3–S7 Files).
Dark blue represents model stability under both current and future conditions, dark red represents agreement among all climate models in anticipating potential distributional areas in the future, and light red indicates low agreement between diverse climate models as regards distributional potential in the future.
The study provided uncertainty estimates associated with different circulation models in each RCP (Fig 5). Highest variation in model predictions across all RCPs was observed in East Asia, the Arabian Peninsula, central North America, western South America, and Europe.
This study assembled a global data set summarizing occurrences of Cx. quinquefasciatus, and provided detailed maps of its potential geographic distribution under current and future climatic conditions. The latter objective is important to anticipating any possible future distributional changes of Cx. quinquefasciatus. These maps (1) give a detailed picture of the current distribution of Cx. quinquefasciatus, which is a potential vector for several arboviruses and lymphatic filariasis; (2) anticipate possible changes in the range of the species under future conditions; (3) identify areas of risk where diseases transmitted by this vector can be established with availability of infection sources through human dynamics; and (4) identify countries with priorities for Cx. quinquefasciatus surveillance programs where data are unavailable (e.g., Western Europe). The predicted distribution of the species was focused in southern regions of the world, both under present-day and future conditions.
However, closely related species of Culex mosquitoes are distributed differently , and hybrid zones of Cx. pipiens and Cx. quinquefasciatus have been reported to occur in Madagascar, North America, and Argentina [5, 37, 38]. Hybrid zone areas in the eastern United States  were identified as showing high suitability for occurrence of Cx. quinquefasciatus in our study.
No previous reports have placed the species in Europe or North Africa; the closest area where the species occurred was in Turkey . Our models revealed environmental suitability for the species’ occurrence in parts of Europe and North Africa. Hence, either the species is present there but not documented owing to difficulties in morphological identification of the members of species complex (i.e. the species in the complex are nearly morphologically identical; ), or it is absent but vulnerable to possible introduction from Turkey or elsewhere. The behavior and physiology of Cx. pipiens complex in Europe and USA are different , and gene flow between species in the complex has been reported .
The global distribution of Cx. quinquefasciatus presents a risk for introduction and transmission of WNV in novel areas , such as Brazil, Peru, Australia, and New Zealand. Possible expansion of the range of Cx. quinquefasciatus may place still more countries at risk of exposure: for example, higher summer temperatures have been identified as a key factor associated with WNV expansion in British Columbia in Canada . WNV outbreaks in Europe have been nonrecurring and localized; however, they have been enzootic and widespread in USA . This pattern of disease spread may be a reflection to the distributional pattern of key vector populations or may reflect the recency of its establishment in North America.
Early studies suggested that warmer conditions are drivers of mosquito abundance [43–45]; however, other studies suggested a delay in the start of the breeding season of Cx. quinquefasciatus in sites presenting a dry and hot spring and summer, but extensions in the season with fall rains and higher temperatures . Our prediction suggested suitability of occurrence of Cx. quinquefasciatus in regions with lower temperatures than in tropical and subtropical regions. Generally, Cx. quinquefasciatus is likely to experience decreased survival as a result of elevated temperatures . A previous study showed a tripling in rates of development, fecundity, and feeding with higher temperature . Although climate change likely will affect the biology of Cx. quinquefasciatus directly, distributional changes in response to elevated temperatures will likely be manifested. Climate change can thus trigger changes in the distributional patterns of Cx. quinquefasciatus, but these changes will be strongly dependent on the location and timing of climate changes . Other environmental effects are on survival, reproductive rate, and vectorial capacity to transmit pathogens; for example, higher temperatures increase pathogen proliferation, and therefore vector competence [27, 48, 49].
Understanding vector distributions is important to understanding dynamics of pathogen transmission. In our analyses, suitable areas were identified for Cx. quinquefasciatus in central and southern Africa, Madagascar, and North Africa (i.e., northern Egypt, Libya, Tunisia, and Morocco). North African countries should be considered as priority in surveillance of this species. Establishment of integrated surveillance programs to improve mosquito data was one of the objectives for the MediLabSecure project launched for the Balkan region .
The integrated maps of current and future distributions of Cx. quinquefasciatus can guide better applications of vector surveillance and disease control programs across the world. The distributional maps of Cx. quinquefasciatus can be also useful to the Global Lymphatic Filariasis Elimination Programme (GLFEP), which considers control of Cx. quinquefasciatus as an important element in control efforts in most endemic countries . These maps are also key elements in recent events in which arboviruses have emerged worldwide. This study can guide control programs and surveillance priorities, which are primarily dependent on identification of suitable areas where the vector occurs or may occur. Finally, it is important to highlight that if Cx. quinquefasciatus is proven to be functioning as a ZIKV vector, the disease control strategies will change dramatically, since most affected countries have no control program targeting this species. In this case, these maps will form a baseline by which to anticipate areas at ZIKV risk and will help in response to the disease outbreak.
S1 File. A summary of general circulation models used for estimating the potential distribution of Culex quinquefasciatus based on future climatic conditions.
S2 File. Expansion or contraction of Culex quinquefasciatus ranges based on presence-absence matrix from the estimated ecological niche for each climate model in four representative concentration pathways.
S3 File. Interactive map for the current potential distribution of Cx. quinquefasciatus.
S4 File. Interactive map for the predicted distribution of Cx. quinquefasciatus in representative concentration pathway 2.6.
S5 File. Interactive map for the predicted distribution of Cx. quinquefasciatus in representative concentration pathway 4.5.
S6 File. Interactive map for the predicted distribution of Cx. quinquefasciatus in representative concentration pathway 6.0.
S7 File. Interactive map for the predicted distribution of Cx. quinquefasciatus in representative concentration pathway 8.5.
We thank the staff of the Department of Entomology and Research and Training Center of Ain Shams University for their personal support during the study. Thanks also to the University of Kansas Ecological Niche Modeling Group for their continuous help during the work. Authors would like to thank Omama Ali, who provided enormously useful guidance during this work.
- Conceptualization: AMS.
- Data curation: AMS ATP.
- Formal analysis: AMS.
- Investigation: AMS.
- Methodology: AMS.
- Project administration: AMS.
- Resources: AMS ATP CFJA.
- Software: AMS.
- Supervision: AMS.
- Validation: AMS.
- Visualization: AMS.
- Writing – original draft: AMS DES MAK.
- Writing – review & editing: AMS AHE MAK CFJA ATP DES.
- 1. Turell MJ. Members of the Culex pipiens complex as vectors of viruses. J Am Mosq Control Assoc. 2012; 28 (4 Suppl): 123–6. pmid:23401952
- 2. Manimegalai K, Sukanya S. Biology of the filarial vector, Culex quinquefasciatus (Diptera:Culicidae). Int J Curr Microbiol App Sci 3 (4): 718–24.
- 3. Farajollahi A, Fonseca DM, Kramer LD, Marm Kilpatrick A. "Bird biting" mosquitoes and human disease: a review of the role of Culex pipiens complex mosquitoes in epidemiology. Infect Genet Evol 11: 1577–1585. pmid:21875691
- 4. Day JF, Stark LM. Frequency of Saint Louis encephalitis virus in humans from Florida, USA: 1990–1999. J Med Entomol 37: 626–633. pmid:10916306
- 5. Cornel AJ, McAbee RD, Rasgon J, Stanich MA, Scott TW, Coetzee M. Differences in extent of genetic introgression between sympatric Culex pipiens and Culex quinquefasciatus (Diptera: Culicidae) in California and South Africa. J Med Entomol 2003; 40 (1): 36–51. pmid:12597651
- 6. Smith JL, Fonseca DM. Rapid assays for identification of members of the Culex (Culex) pipiens complex, their hybrids, and other sibling species (Diptera: Culicidae). Am J Trop Med Hyg 2004; 70 (4): 339–45. pmid:15100444
- 7. Kading RC. Studies on the origin of Culex pipiens pipiens form molestus in New York City. J Am Mosq Control Assoc. 2012; 28 (4 Suppl): 100–5. pmid:23401949
- 8. Andreadis TG. The contribution of Culex pipiens complex mosquitoes to transmission and persistence of West Nile virus in North America. J Am Mosq Control Assoc 2012; 28 (4 Suppl): 137–51. pmid:23401954
- 9. Kramer LD, Styer LM, Ebel GD. A global perspective on the epidemiology of West Nile virus. Annu Rev of Entomol. 2008; 53: 61–81.
- 10. Rutledge CR, Day JF, Lord CC, Stark LM, Tabachnick WJ. West Nile virus infection rates in Culex nigripalpus (Diptera: Culicidae) do not reflect transmission rates in Florida. J Med Entomol 2003;40 (3): 253–8. pmid:12943101
- 11. Hribar LJ, Vlach JJ, Demay DJ, Stark LM, Stoner RL, Godsey MS, et al. Mosquitoes infected with West Nile virus in the Florida Keys, Monroe County, Florida, USA. J Med Entomol 40 (3): 361–3. pmid:12943117
- 12. Vitek CJ, Richards SL, Mores CN, Day JF, Lord CC. Arbovirus transmission by Culex nigripalpus in Florida, 2005. J Med Entomol 2008; 45 (3): 483–93. pmid:18533444
- 13. Fontes G, Leite AB, Vasconcelos de Lima AR, Freitas H, Ehrenberg JP, da Rocha EMM. Lymphatic filariasis in Brazil: epidemiological situation and outlook for elimination. Parasit Vectors. 2012; 5: 272. pmid:23181663
- 14. Khan AM, Dutta P, Sarmah CK, Baruah NK, Das S, Pathak AK, et al. Prevalence of lymphatic filariasis in a tea garden worker population of Dibrugarh (Assam), India after six rounds of mass drug administration. J Vector Borne Dis. 2015; 52 (4): 314–20. pmid:26714512
- 15. Sang R, Kioko E, Lutomiah J, Warigia M, Ochieng C, O'Guinn M, et al. Rift Valley fever virus epidemic in Kenya, 2006/2007: the entomologic investigations. Am J Trop Med Hyg 2010; 83 (2): 28–37. pmid:20682903
- 16. Ayres CF. Identification of Zika virus vectors and implications for control. Lancet Infect Dis. 2016; 16 (3): 278–9. pmid:26852727
- 17. Oliveira Melo AS, Malinger G, Ximenes R, Szejnfeld PO, Alves Sampaio S, Bispo de Filippis AM. Zika virus intrauterine infection causes fetal brain abnormality and microcephaly: tip of the iceberg? Ultrasound Obstet Gynecol. 2016; 47(1):6–7. pmid:26731034
- 18. de Oliveira CS, da Costa Vasconcelos PF. Microcephaly and Zika virus. J Pediatr. 2016; 92 (2): 103–5.
World Health Organization (WHO). Zika virus, Microcephaly, and Guillain Barré Syndrome. Available at http://apps.who.int/iris/bitstream/10665/246180/1/zikasitrep7Jul16-eng.pdf?ua=1. 2016.
- 20. Franca RF, Neves MH, Ayres CF, Melo-Neto OP, Filho SP. First International Workshop on Zika Virus Held by Oswaldo Cruz Foundation FIOCRUZ in Northeast Brazil March 2016—A Meeting Report. PLoS Negl Trop Dis. 2016;10 (6): e0004760. pmid:27258065
- 21. Mills JN, Gage KL, Khan AS. Potential influence of climate change on vector-borne and zoonotic diseases: a review and proposed research plan. Environ Health Perspect 2010; 118 (11): 1507–14. pmid:20576580
- 22. Sutherst RW. Global change and human vulnerability to vector-borne diseases. Clin Microbiol Rev. 2004; 17 (1): 136–73. pmid:14726459
- 23. Kilpatrick AM, Randolph SE. Drivers, dynamics, and control of emerging vector-borne zoonotic diseases. Lancet 2012; 380 (9857): 1946–55. pmid:23200503
- 24. Rueda LM, Patel KJ, Axtell RC, Stinner RE. Temperature-dependent development and survival rates of Culex quinquefasciatus and Aedes aegypti (Diptera: Culicidae). J Med Entomol 1990; 27 (5): 892–8. pmid:2231624
- 25. Paz S, Semenza JC. Environmental drivers of West Nile fever epidemiology in Europe and Western Asia—a review. Int J Environ Res Public Health. 2013;10 (8): 3543–62. pmid:23939389
- 26. Paz S. Climate change impacts on West Nile virus transmission in a global context. Philos Trans R Soc Lond B Biol Sci 2015; 370 (1665). pmid:25688020
- 27. Kilpatrick AM, Meola MA, Moudy RM, Kramer LD. Temperature, viral genetics, and the transmission of West Nile virus by Culex pipiens mosquitoes. PLoS Pathog 2008; 4 (6): e1000092. pmid:18584026
- 28. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A. Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 2005; 25 (15): 1965–78.
Peterson A, Soberón J, Pearson R, Anderson R, Martínez-Meyer E, et al. Ecological Niches and Geographic Distributions Princeton: Princeton University. 2011.
Barve N, Barve V. ENMGadgets: Tools for pre- and post-processing in ENM Workflows. Available at https://github.com/vijaybarve/ENMGadgets. 2013.
R Development Core Team. A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austia. Available at http://www.R-project.org. 2015.
- 32. Phillips SJ, Anderson RP, Schapire RE. Maximum entropy modeling of species geographic distributions. Ecol Model 2006;190 (3–4): 231–59.
- 33. Peterson AT, Papeş M, Soberón J. Rethinking receiver operating characteristic analysis applications in ecological niche modeling. Ecol Model 2008; 213(1):63–72.
- 34. Samy AM, Peterson AT. Climate Change Influences on the Global Potential Distribution of Bluetongue Virus. PloS ONE. 2016;11 (3): e0150489. pmid:26959424
- 35. Lobo JM, Jiménez-Valverde A, Real R. AUC: a misleading measure of the performance of predictive distribution models. Global Ecol Biogeogr 2008; 17 (2): 145–51.
- 36. Conley AK, Fuller DO, Haddad N, Hassan AN, Gad AM, Beier JC. Modeling the distribution of the West Nile and Rift Valley Fever vector Culex pipiens in arid and semi-arid regions of the Middle East and North Africa. Parasites & vectors. 2014; 7: 289. pmid:24962735
- 37. Humeres SG, Almiron WR, Sabattini MS, Gardenal CN. Estimation of genetic divergence and gene flow between Culex pipiens and Culex quinquefasciatus (Diptera: Culicidae) in Argentina. Mem Inst Oswaldo Cruz 1998; 93 (1): 57–62. pmid:9698844
- 38. Urbanelli S, Silvestrini F, Sabatinelli G, Raveloarifera F, Petrarca V, Bullini L. Characterization of the Culex pipiens complex (Diptera: Culicidae) in Madagascar. J Med Entomol 1995; 32 (6): 778–86. pmid:8551499
- 39. Huang S, Molaei G, Andreadis TG. Reexamination of Culex pipiens hybridization zone in the Eastern United States by ribosomal DNA-based single nucleotide polymorphism markers. Am J Trop Med Hyg. 2011; 85 (3): 434–41. pmid:21896800
- 40. Gunay F, Alten B, Simsek F, Aldemir A, Linton Y-M. Barcoding Turkish Culex mosquitoes to facilitate arbovirus vector incrimination studies reveals hidden diversity and new potential vectors. Acta tropica. 2015; 143: 112–20. pmid:25446171
- 41. Fonseca DM, Keyghobadi N, Malcolm CA, Mehmet C, Schaffner F, Mogi M, et al. Emerging vectors in the Culex pipiens complex. Science 2004; 303 (5663): 1535–8. pmid:15001783
- 42. Roth D, Henry B, Mak S, Fraser M, Taylor M, Li M, et al. West Nile virus range expansion into British Columbia. Emerg Infect Dis. 2010; 16(8): 1251–8. pmid:20678319
- 43. Khasnis AA, Nettleman MD. Global warming and infectious disease. Arch Med Res. 2005; 36(6): 689–96. pmid:16216650
- 44. Weaver SC, Reisen WK. Present and future arboviral threats. Antiviral Res 2010; 85(2): 328–45. pmid:19857523
- 45. McMichael AJ, Lindgren E. Climate change: present and future risks to health, and necessary responses. J Intern Med 2011; 270 (5): 401–13. pmid:21682780
- 46. Morin CW, Comrie AC. Regional and seasonal response of a West Nile virus vector to climate change. Proc Natl Acad Sci USA 2013;110 (39): 15620–5. pmid:24019459
- 47. Ciota AT, Matacchiero AC, Kilpatrick AM, Kramer LD. The effect of temperature on life history traits of Culex mosquitoes. J Med Entomol 2014; 51 (1): 55–62. pmid:24605453
- 48. Dohm DJ, O'Guinn ML, Turell MJ. Effect of environmental temperature on the ability of Culex pipiens (Diptera: Culicidae) to transmit West Nile virus. J Med Entomol 2002; 39 (1): 221–5. pmid:11931261
- 49. Reisen WK, Fang Y, Martinez VM. Effects of temperature on the transmission of west nile virus by Culex tarsalis (Diptera: Culicidae). J Med Entomol 2006;43 (2): 309–17. pmid:16619616
MediLabSecure project. Medical and Veterinary Entomology Working group-4. Available at www.medilabsecure.com/ (Accessed 03/30/2016).
- 51. Sunish IP, Rajendran R, Mani TR, Munirathinam A, Dash AP, Tyagi BK. Vector control complements mass drug administration against bancroftian filariasis in Tirukoilur, India. Bull World Health Organ. 2007;85(2):138–45. pmid:17308735