Complementarity of empirical and process-based approaches to modelling mosquito population dynamics with Aedes albopictus as an example—Application to the development of an operational mapping tool of vector populations

Autoři: Annelise Tran aff001;  Morgan Mangeas aff005;  Marie Demarchi aff006;  Emmanuel Roux aff005;  Pascal Degenne aff001;  Marion Haramboure aff001;  Gilbert Le Goff aff007;  David Damiens aff007;  Louis-Clément Gouagna aff007;  Vincent Herbreteau aff005;  Jean-Sébastien Dehecq aff008
Působiště autorů: CIRAD, UMR TETIS, Sainte-Clotilde, Reunion, France aff001;  TETIS, Univ Montpellier, AgroParisTech, CIRAD, CNRS, INRAE, Montpellier, France aff002;  CIRAD, UMR ASTRE, Sainte-Clotilde, Reunion, France aff003;  ASTRE, Univ Montpellier, CIRAD, INRAE, Montpellier, France aff004;  IRD, UMR ESPACE-DEV, Montpellier, France aff005;  Maison de la Télédétection, Montpellier, France aff006;  UMR MIVEGEC, IRD, Sainte-Clotilde, Reunion, France aff007;  Regional Health Agency, Sainte-Clotilde, Reunion, France aff008
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article


Mosquitoes are responsible for the transmission of major pathogens worldwide. Modelling their population dynamics and mapping their distribution can contribute effectively to disease surveillance and control systems. Two main approaches are classically used to understand and predict mosquito abundance in space and time, namely empirical (or statistical) and process-based models. In this work, we used both approaches to model the population dynamics in Reunion Island of the 'Tiger mosquito', Aedes albopictus, a vector of dengue and chikungunya viruses, using rainfall and temperature data. We aimed to i) evaluate and compare the two types of models, and ii) develop an operational tool that could be used by public health authorities and vector control services. Our results showed that Ae. albopictus dynamics in Reunion Island are driven by both rainfall and temperature with a non-linear relationship. The predictions of the two approaches were consistent with the observed abundances of Ae. albopictus aquatic stages. An operational tool with a user-friendly interface was developed, allowing the creation of maps of Ae. albopictus densities over the whole territory using meteorological data collected from a network of weather stations. It is now routinely used by the services in charge of vector control in Reunion Island.

Klíčová slova:

Death rates – Infectious disease control – Larvae – Oviposition – Population dynamics – Pupae – Rain – Weather stations


1. WHO. A global brief on vector-borne diseases. 2014.

2. Rodriguez-Barraquer I, Cordeiro MT, Braga C, de Souza WV, Marques ET, Cummings DA. From re-emergence to hyperendemicity: the natural history of the dengue epidemic in Brazil. PLoS neglected tropical diseases. 2011 Jan 4; 5(1):e935. doi: 10.1371/journal.pntd.0000935 21245922

3. Schuffenecker I, Iteman I, Michault A, Murri S, Frangeul L, Vaney MC, et al. Genome microevolution of chikungunya viruses causing the Indian Ocean outbreak. PLoS medicine. 2006 Jul; 3(7):e263. doi: 10.1371/journal.pmed.0030263 16700631

4. Weaver SC, Costa F, Garcia-Blanco MA, Ko AI, Ribeiro GS, Saade G, et al. Zika virus: History, emergence, biology, and prospects for control. Antiviral Res. 2016 Jun; 130:69–80. doi: 10.1016/j.antiviral.2016.03.010 26996139

5. Adde A, Roux E, Mangeas M, Dessay N, Nacher M, Dusfour I, et al. Dynamical Mapping of Anopheles darlingi Densities in a Residual Malaria Transmission Area of French Guiana by Using Remote Sensing and Meteorological Data. PLoS One. 2016; 11(10):e0164685. doi: 10.1371/journal.pone.0164685 27749938

6. Baldacchino F, Marcantonio M, Manica M, Marini G, Zorer R, Delucchi L, et al. Mapping of Aedes albopictus Abundance at a Local Scale in Italy. Remote Sensing. 2017; 9:749.

7. Dickens BL, Sun H, Jit M, Cook AR, Carrasco LR. Determining environmental and anthropogenic factors which explain the global distribution of Aedes aegypti and Ae. albopictus. BMJ Glob Health. 2018; 3(4):e000801. doi: 10.1136/bmjgh-2018-000801 30233829

8. Ducheyne E, Tran Minh NN, Haddad N, Bryssinckx W, Buliva E, Simard F, et al. Current and future distribution of Aedes aegypti and Aedes albopictus (Diptera: Culicidae) in WHO Eastern Mediterranean Region. Int J Health Geogr. 2018 Feb 14; 17(1):4. doi: 10.1186/s12942-018-0125-0 29444675

9. Erguler K, Smith-Unna SE, Waldock J, Proestos Y, Christophides GK, Lelieveld J, et al. Large-Scale Modelling of the Environmentally-Driven Population Dynamics of Temperate Aedes albopictus (Skuse). PLoS One. 2016; 11(2):e0149282. doi: 10.1371/journal.pone.0149282 26871447

10. Ezanno P, Aubry-Kientz M, Arnoux S, Cailly P, L'Ambert G, Toty C, et al. A generic weather-driven model to predict mosquito population dynamics applied to species of Anopheles, Culex and Aedes genera of southern France. Prev Vet Med. 2015 Jun 1; 120(1):39–50. doi: 10.1016/j.prevetmed.2014.12.018 25623972

11. Johnson TL, Haque U, Monaghan AJ, Eisen L, Hahn MB, Hayden MH, et al. Modeling the Environmental Suitability for Aedes (Stegomyia) aegypti and Aedes (Stegomyia) albopictus (Diptera: Culicidae) in the Contiguous United States. Journal of medical entomology. 2017 Nov 7; 54(6):1605–14. doi: 10.1093/jme/tjx163 29029153

12. Jung JM, Lee JW, Kim CJ, Jung S, Lee WH. CLIMEX-based analysis of potential geographical distribution of Aedes albopictus and Aedes aegypti in South Korea. Journal of Biosystems Engineering. 2017; 42(3):217–26.

13. Lord CC. Modeling and biological control of mosquitoes. Journal of the American Mosquito Control Association. 2007; 23(2 Suppl):252–64. doi: 10.2987/8756-971x(2007)23[252:mabcom];2 17853610

14. Machault V, Gadiaga L, Vignolles C, Jarjaval F, Bouzid S, Sokhna C, et al. Highly focused anopheline breeding sites and malaria transmission in Dakar. Malar J. 2009 Jun 24; 8:138. doi: 10.1186/1475-2875-8-138 19552809

15. Magori K, Legros M, Puente ME, Focks DA, Scott TW, Lloyd AL, et al. Skeeter Buster: a stochastic, spatially explicit modeling tool for studying Aedes aegypti population replacement and population suppression strategies. PLoS neglected tropical diseases. 2009 Sep 1; 3(9):e508. doi: 10.1371/journal.pntd.0000508 19721700

16. Roiz D, Neteler M, Castellani C, Arnoldi D, Rizzoli A. Climatic factors driving invasion of the tiger mosquito (Aedes albopictus) into new areas of Trentino, northern Italy. PLoS One. 2011 Apr 15; 6(4):e14800. doi: 10.1371/journal.pone.0014800 21525991

17. Tran A, L'Ambert G, Lacour G, Benoit R, Demarchi M, Cros M, et al. A rainfall- and temperature-driven abundance model for Aedes albopictus populations. Int J Environ Res Public Health. 2013 May; 10(5):1698–719. doi: 10.3390/ijerph10051698 23624579

18. Moiroux N, Djenontin A, Bio-Bangana AS, Chandre F, Corbel V, Guis H. Spatio-temporal analysis of abundances of three malaria vector species in southern Benin using zero-truncated models. Parasites & vectors. 2014 Mar 12; 7:103.

19. Cailly P, Tran A, Balenghien T, L'Ambert G, Toty C, Ezanno P. A climate-driven abundance model to assess mosquito control strategies. Ecological Modelling. 2012 Feb 24; 227:7–17.

20. Dumont Y, Chiroleu F. Vector control for the chikungunya disease. Math Biosci Eng. 2010 Apr; 7(2):313–45. doi: 10.3934/mbe.2010.7.313 20462292

21. Kles V, Michault A, Rodhain F, Mevel F, Chastel C. A serological survey regarding Flaviviridae infections on the island of Reunion (1971–1989). Bull Soc Pathol Exot. 1994; 87(2):71–6. 8061530

22. D'Ortenzio E, Balleydier E, Baville M, Filleul L, Renault P. [Dengue fever in the Reunion Island and in South Western islands of the Indian Ocean]. Med Mal Infect. 2011 Sep; 41(9):475–9. doi: 10.1016/j.medmal.2010.11.021 21295427

23. CIRE. Surveillance de la dengue à la Réunion. Point épidémiologique au 19 février 20192019. Available from:

24. Boyer S, Foray C, Dehecq JS. Spatial and temporal heterogeneities of Aedes albopictus density in La Reunion Island: rise and weakness of entomological indices. PLoS One. 2014; 9(3):e91170. doi: 10.1371/journal.pone.0091170 24637507

25. Dumont Y, Tchuenche JM. Mathematical studies on the sterile insect technique for the chikungunya disease and Aedes albopictus. J Math Biol. 2012 Nov; 65(5):809–54. doi: 10.1007/s00285-011-0477-6 22038083

26. Dufourd C, Dumont Y. Modeling and Simulations of Mosquito Dispersal. The Case of Aedes albopictus. Biomath. 2012; 1:1209262.

27. Dufourd C, Dumont Y. Impact of environmental factors on mosquito dispersal in the prospect of sterile insect technique control. Computers and Mathematics with Applications. 2013; 66(9):1695–715.

28. Dumont Y, Thuillez J. Human behaviors: A threat to mosquito control? Mathematical Biosciences. 2016; 281:9–23. doi: 10.1016/j.mbs.2016.08.011 27590772

29. Chang CC, Lin CJ. LIBSVM: A Library for Support Vector Machines 2001. Available from:

30. Honorio NA, Silva Wda C, Leite PJ, Goncalves JM, Lounibos LP, Lourenco-de-Oliveira R. Dispersal of Aedes aegypti and Aedes albopictus (Diptera: Culicidae) in an urban endemic dengue area in the State of Rio de Janeiro, Brazil. Memorias do Instituto Oswaldo Cruz. 2003 Mar; 98(2):191–8. doi: 10.1590/s0074-02762003000200005 12764433

31. Lacroix R, Delatte H, Hue T, Reiter P. Dispersal and survival of male and female Aedes albopictus (Diptera: Culicidae) on Reunion Island. Journal of medical entomology. 2009 Sep; 46(5):1117–24. doi: 10.1603/033.046.0519 19769043

32. Liew C, Curtis CF. Horizontal and vertical dispersal of dengue vector mosquitoes, Aedes aegypti and Aedes albopictus, in Singapore. Medical and veterinary entomology. 2004 Dec; 18(4):351–60. doi: 10.1111/j.0269-283X.2004.00517.x 15642001

33. Marini F, Caputo B, Pombi M, Tarsitani G, della Torre A. Study of Aedes albopictus dispersal in Rome, Italy, using sticky traps in mark-release-recapture experiments. Medical and veterinary entomology. 2010 Dec; 24(4):361–8. doi: 10.1111/j.1365-2915.2010.00898.x 20666995

34. Niebylski ML, Craig GB Jr. Dispersal and survival of Aedes albopictus at a scrap tire yard in Missouri. Journal of the American Mosquito Control Association. 1994 Sep; 10(3):339–43. 7807074

35. Rosen L, Rozeboom LE, Reeves WC, Saugrain J, Gubler DJ. A field trial of competitive displacement of Aedes polynesiensis by Aedes albopictus on a Pacific atoll. The American journal of tropical medicine and hygiene. 1976 Nov; 25(6):906–13. doi: 10.4269/ajtmh.1976.25.906 1008133

36. Vapnik V. The nature of statistical learning theory. New York (NY): Springer-Verlag; 1995.

37. Team RC. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2017. Available from:

38. Lacour G, Vernichon F, Cadilhac N, Boyer S, Lagneau C, Hance T. When mothers anticipate: effects of the prediapause stage on embryo development time and of maternal photoperiod on eggs of a temperate and a tropical strains of Aedes albopictus (Diptera: Culicidae). J Insect Physiol. 2014 Dec; 71:87–96. doi: 10.1016/j.jinsphys.2014.10.008 25450563

39. Delatte H, Gimonneau G, Triboire A, Fontenille D. Influence of temperature on immature development, survival, longevity, fecundity, and gonotrophic cycles of Aedes albopictus, vector of chikungunya and dengue in the Indian Ocean. Journal of medical entomology. 2009 Jan; 46(1):33–41. doi: 10.1603/033.046.0105 19198515

40. Delatte H, Dehecq JS, Thiria J, Domerg C, Paupy C, Fontenille D. Geographic distribution and developmental sites of Aedes albopictus (Diptera: Culicidae) during a chikungunya epidemic event. Vector Borne Zoonotic Dis. 2008 Spring; 8(1):25–34. doi: 10.1089/vbz.2007.0649 18171104

41. Dieng H, Rahman GM, Abu Hassan A, Che Salmah MR, Satho T, Miake F, et al. The effects of simulated rainfall on immature population dynamics of Aedes albopictus and female oviposition. Int J Biometeorol. 2012 Jan; 56(1):113–20. doi: 10.1007/s00484-011-0402-0 21267602

42. Hammami P, Tran A, Kemp A, Tshikae P, Kgori P, Chevalier V, et al. Rift Valley fever vector diversity and impact of meteorological and environmental factors on Culex pipiens dynamics in the Okavango Delta, Botswana. Parasites & vectors. 2016 Aug 8; 9(1):434.

43. Degenne P, Lo Seen D. Ocelet: Simulating processes of landscape changes using interaction graphs. SoftwareX. 2016; 5:89–95.

44. Soumahoro MK, Boelle PY, Gauzere BA, Atsou K, Pelat C, Lambert B, et al. The chikungunya epidemic on La Reunion Island in 2005–2006: a cost-of-illness study. PLoS neglected tropical diseases. 2011 Jun; 5(6):e1197. doi: 10.1371/journal.pntd.0001197 21695162

45. WHO. Dengue fever—Reunion, France. Disease Outbreak News [Internet]. 2018. Available from:

46. Larrieu S, Dehecq JS, Balleydier E, Jaffar MC, Michault A, Vilain P, et al. Re-emergence of dengue in Reunion, France, January to April 2012. Euro surveillance: bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin. 2012 May 17; 17(20).

47. Alto BW, Juliano SA. Precipitation and temperature effects on populations of Aedes albopictus (Diptera: Culicidae): implications for range expansion. Journal of medical entomology. 2001 Sep; 38(5):646–56. doi: 10.1603/0022-2585-38.5.646 11580037

48. Roiz D, Rosa R, Arnoldi D, Rizzoli A. Effects of temperature and rainfall on the activity and dynamics of host-seeking Aedes albopictus females in northern Italy. Vector Borne Zoonotic Dis. 2010 Oct; 10(8):811–6. doi: 10.1089/vbz.2009.0098 20059318

49. Waldock J, Chandra NL, Lelieveld J, Proestos Y, Michael E, Christophides G, et al. The role of environmental variables on Aedes albopictus biology and chikungunya epidemiology. Pathog Glob Health. 2013 Jul; 107(5):224–41. doi: 10.1179/2047773213Y.0000000100 23916332

50. Lacour G, Chanaud L, L'Ambert G, Hance T. Seasonal Synchronization of Diapause Phases in Aedes albopictus (Diptera: Culicidae). PLoS One. 2015; 10(12):e0145311. doi: 10.1371/journal.pone.0145311 26683460

51. Adams HD, Williams AP, Xu C, Rauscher SA, Jiang X, McDowell NG. Empirical and process-based approaches to climate-induced forest mortality models. Front Plant Sci. 2013; 4:438. doi: 10.3389/fpls.2013.00438 24312103

52. Kearney MR, Wintle BA, Porter WP. Correlative and mechanistic models of species distribution provide congruent forecsts under climate change. Conservation letters. 2010; 3:203–13.

53. Fischer D, Thomas SM, Neteler M, Tjaden NB, Beierkuhnlein C. Climatic suitability of Aedes albopictus in Europe referring to climate change projections: comparison of mechanistic and correlative niche modelling approaches. Euro surveillance: bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin. 2014 Feb 13; 19(6).

54. Carlson CJ, Dougherty E, Boots M, Getz W, Ryan SJ. Consensus and conflict among ecological forecasts of Zika virus outbreaks in the United States. Scientific reports. 2018 Mar 21; 8(1):4921. doi: 10.1038/s41598-018-22989-0 29563545

55. Wenger SJ, Olden JD. Assessing transferability of ecological models: an underappreciated aspect of statistical validation. Methods in Ecology and Evolution. 2012; 3:260–7.

56. Gouagna LC, Dehecq JS, Fontenille D, Dumont Y, Boyer S. Seasonal variation in size estimates of Aedes albopictus population based on standard mark-release-recapture experiments in an urban area on Reunion Island. Acta Trop. 2015 Mar; 143:89–96. doi: 10.1016/j.actatropica.2014.12.011 25592432

57. Unlu I, Suman DS, Wang Y, Klingler K, Faraji A, Gaugler R. Effectiveness of autodissemination stations containing pyriproxyfen in reducing immature Aedes albopictus populations. Parasites & vectors. 2017 Mar 9; 10(1):139.

58. Machault V, Yébakima A, Etienne M, Vignolles C, Palany P, Tourre YM, et al. Mapping Entomological Dengue Risk Levels in Martinique Using High-Resolution Remote-Sensing Environmental Data. ISPRS Int J Geo-Inf. 2014; 3(4):1352–71.

59. Moiroux N, Bio-Bangana AS, Djenontin A, Chandre F, Corbel V, Guis H. Modelling the risk of being bitten by malaria vectors in a vector control area in southern Benin, west Africa. Parasites & vectors. 2013 Mar 15; 6:71.

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