Seasonality and timing of peak abundance of Aedes albopictus in Europe: Implications to public and animal health

Submitted: 9 March 2021
Accepted: 14 April 2021
Published: 14 May 2021
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Aedes albopictus is a known vector of dengue and chikungunya. Understanding the population dynamics characteristics of vector species is of pivotal importance to optimise surveillance and control activities, to estimate risk for pathogen-transmission, and thus to enhance support of public health decisions. In this paper we used a seasonal activity model to simulate the start (spring hatching) and end (autumn diapause) of the vector season. In parallel, the peak abundance of the species was assessed using both VectorNet field survey data complemented with field studies obtained from literature across the Mediterranean Basin. Our results suggest that spring hatching of eggs in the current distribution area can start at the beginning of March in southern Europe and in April in western Europe. In northern Europe, where the species is not (yet) present, spring hatching would occur from late April to late May. Aedes albopictus can remain active up to 41 weeks in southern Europe whilst the climatic conditions in northern Europe are limiting its potential activity to a maximum of 23 weeks. The peak of egg density is found during summer months from end of July until end of September. During these two months the climatic conditions for species development are optimal, which implies a higher risk for arbovirus transmission by Ae. albopictus and occurrence of epidemics.

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Allouche O, Tsoar A, Kadmon R, 2006. Assessing the accuracy of species distribution models: prevalence, kappa and the true skill statistic (TSS). J Appl Ecol 43:1223-32. DOI: https://doi.org/10.1111/j.1365-2664.2006.01214.x
Angelini R, Finarelli AC, Angelini P, Po C, Petropulacos K, Silvi G, Macini P, Fortuna C, Venturi G, Magurano F, Fiorentini C, 2007. Chikungunya in north-eastern Italy: a summing up of the outbreak. Euro Surveill 12:3313. DOI: https://doi.org/10.2807/esw.12.47.03313-en
Armbruster PA, 2016. Photoperiodic diapause and the establishment of Aedes albopictus (Diptera: Culicidae) in North America. J Med Entomol 53:1013-23. DOI: https://doi.org/10.1093/jme/tjw037
Baldacchino F, Marcantonio M, Manica M, Marini G, Zorer R, Delucchi L, Arnoldi D, Montarsi F, Capelli G, Rizzoli A, Rosà R, 2017. Mapping of Aedes albopictus abundance at a local scale in Italy. Remote Sens 9:749. DOI: https://doi.org/10.3390/rs9070749
Bonacci T, Mazzei A, Hristova VK, Ahmad MA, 2015. Monitoring of Aedes albopictus (Diptera, Cilicidae) in Calabria, Southern Italy. Int J Sci Eng Res 6:1186-9.
Brady OJ, Johansson MA, Guerra CA, Bhatt S, Golding N, Pigott DM, Delatte H, Grech MG, Leisnham PT, Maciel-de-Freitas R, Styer LM, 2013. Modelling adult Aedes aegypti and Aedes albopictus survival at different temperatures in laboratory and field settings. Parasit Vectors 6:1-2. DOI: https://doi.org/10.1186/1756-3305-6-351
Borchers HW, 2019. Pracma: practical numerical math functions. R package version 2(1).
Gomes ADC, Gotlieb LD, de Azevedo Marques C, Bicudo de Paula M, Marques GR, 1995. Duration of larval and pupal development stages of Aedes albopictus in natural and artificial containers. Rev Saude Publica 29:15-9. DOI: https://doi.org/10.1590/S0034-89101995000100004
Caminade C, Medlock JM, Ducheyne E, McIntyre KM, Leach S, Baylis M, Morse AP, 2012. Suitability of European climate for the Asian tiger mosquito Aedes albopictus: recent trends and future scenarios. J R Soc Interface 9:2708-17. DOI: https://doi.org/10.1098/rsif.2012.0138
CCCS (Copernicus Climate Change Service), 2019. ERA5-Land hourly data from 2001 to present. Available from: https://doi.org/10.24381/CDS.E2161BAC
Collantes F, Delgado JA, Alarcón-Elbal PM, Delacour S, Lucientes J, 2014. First confirmed outdoor winter reproductive activity of Asian tiger mosquito (Aedes albopictus) in Europe. An Inst Biol 36:71-6. DOI: https://doi.org/10.6018/analesbio.36.12
Collantes F, Delacour S, Alarcón-Elbal PM, Ruiz-Arrondo I, Delgado JA, Torrell-Sorio A, Bengoa M, Eritja R, Miranda MÃ, Molina R, Lucientes J, 2015. Review of ten-years presence of Aedes albopictus in Spain 2004-2014: known distribution and public health concerns. Parasit Vectors 8:1-1. DOI: https://doi.org/10.1186/s13071-015-1262-y
Cunze S, Kochmann J, Koch LK, Klimpel S, 2016. Aedes albopictus and its environmental limits in Europe. PLoS One 11:e0162116. DOI: https://doi.org/10.1371/journal.pone.0162116
Delatte H, Gimonneau G, Triboire A, Fontenille D, 2009. Influence of temperature on immature development, survival, longevity, fecundity, and gonotrophic cycles of Aedes albopictus, vector of chikungunya and dengue in the Indian Ocean. J Med Entomol 46:33-41. DOI: https://doi.org/10.1603/033.046.0105
Dieng H, Rahman GMS, Hassan AA, Salmah MRC, Satho T, Miake F, Boots M, Sazaly A, 2012. The effects of simulated rainfall on immature population dynamics of Aedes albopictus and female oviposition Int J Biometeorol 56:113-20. DOI: https://doi.org/10.1007/s00484-011-0402-0
Erguler K, Smith-Unna SE, Waldock J, Proestos Y, Christophides GK, Lelieveld J, Parham PE, 2016. Large-Scale modelling of the environmentally-driven population dynamics of temperate Aedes albopictus (Skuse). PLoS One 11:e0149282. DOI: https://doi.org/10.1371/journal.pone.0149282
Erguler K, Demirok M, Gunay F, Petrić M, Kavran M, Petrić D, Alten B, 2020. Model-based design and analysis of life table experiments for insect vectors. BioRxiv [Epub ahead of print]. DOI: https://doi.org/10.1101/2020.03.05.978684
Erickson RA, Presley SM, Allen LJS, Long KR, Cox SB, 2010. A stage-structured, Aedes albopictus population model. Ecol Model 221:1273-82. DOI: https://doi.org/10.1016/j.ecolmodel.2010.01.018
Eritja R, Escosa R, Lucientes J, Marques E, Roiz D, Ruiz S, 2005. Worldwide invasion of vector mosquitoes: present European distribution and challenges for Spain. Biol Invasions 7:87-97. DOI: https://doi.org/10.1007/s10530-004-9637-6
ECDC (European Centre for Disease Prevention and Control), 2009. Development of Aedes albopictus risk maps. Technical report: ECDC, 45 pp. Available from: https://www.ecdc.europa.eu/en/publications-data/development-aedes-albopictus-risk-maps Accessed: 26 January 2021.
ECDC (European Centre for Disease Prevention and Control), 2017. Clusters of autochthonous chikungunya cases in France. Rapid risk assessment, ECDC: 10 pp. Available from: 14-08-2017-RRA-Chikungunya-France (europa.eu) Accessed: 4 January 2021.
ECDC (European Centre for Disease Prevention and Control), 2019a. Aedes albopictus - current known distribution: August 2019. Stockholm: ECDC. Available from: https://www.ecdc.europa.eu/en/publications-data/aedes-albopictus-current-known-distribution-august-2019 Accessed: 26 January 2021.
ECDC (European Centre for Disease Prevention and Control), 2019b. Autochthonous cases of dengue in Spain and France. Rapid risk assessment, ECDC: 8 pp. Available from: https://www.ecdc.europa.eu/sites/default/files/documents/RRA-dengue-in-Spain-France_1Oct2019.pdf Accessed: 4 January 2021.
ECDC (European Centre for Disease Prevention and Control), 2019c. Zika virus disease in Var department, France. Rapid risk assessment, ECDC: 8 pp. Available from: https://www.ecdc.europa.eu/en/publications-data/rapid-risk-assessment-zika-virus-disease-var-department-france Accessed: 26 January 2021.
ECDC (European Centre for Disease Prevention and Control), 2020a. Autochthonous transmission of dengue virus in EU/EEA, 2010-2020. Surveillance and disease data, ECDC. Available from: https://www.ecdc.europa.eu/sites/default/files/documents/RRA-dengue-in-Spain-France_1Oct2019.pdf Accessed: 19 January 2021.
ECDC (European Centre for Disease Prevention and Control), 2020b. Aedes albopictus - current known distribution. ECDC. Available from: https://www.ecdc.europa.eu/en/publications-data/aedes-albopictus-current-known-distribution-may-2020 Accessed: 26 January 2021. DOI: https://doi.org/10.2807/1560-7917.ES.2021.26.13.2104011
ECDC & EFSA (European Centre for Disease Prevention and Control and European Food Safety Authority), 2018a. Field sampling methods for mosquitoes, sandflies, biting midges and ticks - VectorNet project 2014-2018. ECDC and EFSA: 45 pp. Available from: https://www.ecdc.europa.eu/sites/default/files/documents/Vector-sampling-field-protocol-2018.pdf Accessed: 12 February 2021.
ECDC & EFSA (European Centre for Disease Prevention and Control and European Food Safety Authority), 2018b. The importance of vector abundance and seasonality - Results from an expert consultation. ECDC and EFSA: 48 pp. Available from: https://www.ecdc.europa.eu/sites/default/files/documents/vector-abundance-and-seasonality.pdf Accessed: 12 February 2021.
Ferraguti M, Martínez-de La Puente J, Roiz D, Ruiz S, Soriguer R, Figuerola J, 2016. Effects of landscape anthropization on mosquito community composition and abundance. Sci Rep 6:1-9. DOI: https://doi.org/10.1038/srep29002
Flacio E, Engeler L, Tonolla M, Müller P, 2016. Spread and establishment of Aedes albopictus in southern Switzerland between 2003 and 2014: An analysis of oviposition data and weather conditions. Parasit Vectors 9:304. DOI: https://doi.org/10.1186/s13071-016-1577-3
Focks DA, Linda SB, Craig Jnr GB, Hawley WA, Pumpuni CB, 1994. Aedes albopictus (Diptera: Culicidae): A statistical model of the role of temperature, photoperiod, and geography in the induction of egg diapause. J Med Entomol 31:278-86. DOI: https://doi.org/10.1093/jmedent/31.2.278
Franke F, Giron S, Cochet A, Jeannin C, Leparc-Goffart I, de Valk H, Jourdain F, de Lamballerie X, L’Ambert G, Paty MC, 2019. Autochthonous chikungunya and dengue fever outbreak in Mainland France, 2010-2018. Eur J Public Health 29:ckz186-628. DOI: https://doi.org/10.1093/eurpub/ckz186.628
Gatt P, Schaffner F, Cassar LF, 2010. Aedes (Stegomyia) albopictus (Skuse) (Diptera: Culicidae) in Malta - the first winter. Eur Mosq Bull 28:225-9.
Ghasemi A, Zahediasl S, 2012. Normality tests for statistical analysis: a guide for non-statisticians. Int J Endocrinol Metab 10:486. DOI: https://doi.org/10.5812/ijem.3505
Giatropoulos A, Emmanouel N, Koliopoulos G, Michaelakis A, 2012. A study on distribution and seasonal abundance of Aedes albopictus (Diptera: Culicidae) population in Athens, Greece. J Med Entomol 49:262-9. DOI: https://doi.org/10.1603/ME11096
Giron S, Franke F, Decoppet A, Cadiou B, Travaglini T, Thirion L, Durand G, Jeannin C, L’Ambert G, Grard G, Noël H, Fournet N, Auzet-Caillaud M, Zandotti C, Aboukaïs S, Chaud P, Guedj S, Hamouda L, Naudot X, Ovize A, Lazarus C, de Valk H, Paty M-C, Leparc-Goffart I, 2019. Vector-borne transmission of Zika virus in Europe, southern France, August 2019. Euro Surveill 24:pii=1900655. DOI: https://doi.org/10.2807/1560-7917.ES.2019.24.45.1900655
Guzzetta G, Montarsi F, Baldacchino FA, Metz M, Capelli G, Rizzoli A, Pugliese A, Rosà R, Poletti P, Merler S, 2016a. Potential risk of dengue and chikungunya outbreaks in northern Italy based on a population model of Aedes albopictus (Diptera: Culicidae). PLoS Negl Trop Dis 10:e0004762. DOI: https://doi.org/10.1371/journal.pntd.0004762
Guzzetta G, Poletti P, Montarsi F, Baldacchino F, Capelli G, Rizzoli A, Rosa R, Merler S, 2016b. Assessing the potential risk of Zika virus epidemics in temperate areas with established Aedes albopictus populations. Euro Surveill 21: pii=30199. DOI: https://doi.org/10.2807/1560-7917.ES.2016.21.15.30199
Hawley WA, 1988. The biology of Aedes albopictus. J Am Mosq Control Assoc 4:1-39.
Hijmans RJ, 2019. meteor: Meteorological Data Manipulation R package version 0 (3).
Hylton AR, 1969. Studies on longevity of adult Eretmapodites chrysogaster, Aedes togoi and Aedes (Stegomyia) albopictus females (Diptera: Culicidae). J Med Entomol 6:147–149. DOI: https://doi.org/10.1093/jmedent/6.2.147
Kendon M, McCarthy M, Jevrejeva S, Matthews A, Legg T, 2020. State of the UK climate 2018. Int J Climatol 39:1-55. DOI: https://doi.org/10.1002/joc.6213
Khan SU, Ogden NH, Fazil AA, Gachon PH, Dueymes GU, Greer AL, Ng V, 2020. Current and Projected Distributions of Aedes aegypti and Ae. albopictus in Canada and the US. Environ Health Perspect 128:057007. DOI: https://doi.org/10.1289/EHP5899
Knudsen AB, Romi R, Majori G, 1996. Occurrence and spread in Italy of Aedes albopictus, with implications for its introduction into other parts of Europe. J Am Mosq Control Assoc 12:177-83.
Kobayashi M, Nihei N, Kurihara T, 2002. Analysis of northern distribution of Aedes albopictus (Diptera: Culicidae) in Japan by geographical information system. J Med Entomol 39:4-11. DOI: https://doi.org/10.1603/0022-2585-39.1.4
Komagata O, Higa Y, Muto A, Hirabayashi K, Yoshida M, Sato T, Nihei N, Sawabe K, Kobayashi M, 2017. Predicting the start of the Aedes albopictus (Diptera: Culicidae) female adult biting season using the spring temperature in Japan. J Med Entomol 54:1519-24. DOI: https://doi.org/10.1093/jme/tjx159
Kuhlisch C, Kampen H, Walther D, 2018. The Asian tiger mosquito Aedes albopictus (Diptera: Culicidae) in Central Germany: Surveillance in its northernmost distribution area. Acta Trop 188:78-85. DOI: https://doi.org/10.1016/j.actatropica.2018.08.019
Kumar G, Pande V, Pasi S, Ojha VP, Dhiman RC, 2018. Air versus water temperature of aquatic habitats in Delhi: implications for transmission dynamics of Aedes aegypti. Geospat Health 13:707. DOI: https://doi.org/10.4081/gh.2018.707
Lacour G, Chanaud L, L’Ambert G, Hance T, 2015. Seasonal synchronization of diapause phases in Aedes albopictus (Diptera: Culicidae). PLoS One 10:e0145311. DOI: https://doi.org/10.1371/journal.pone.0145311
Lacour G, 2016. Eco-physiological mechanisms and adaptive value of egg diapause in the invasive mosquito Aedes albopictus (Diptera, Culicidae). Thesis. University of Louvain-La-Neuve, 229 pp. Available from: https://dial.uclouvain.be/pr/boreal/object/boreal:175328. Accessed: 12 February 2021.
Lajeunesse MJ, 2016. Facilitating systematic reviews, data extraction, and meta-analysis with the metagear package for R. Methods Ecol Evol 7:323-30. DOI: https://doi.org/10.1111/2041-210X.12472
Lindh E, Argentini C, Remoli ME, Fortuna C, Faggioni G, Benedetti E, Amendola A, Marsili G, Lista F, Rezza G, Venturi G, 2019. The Italian 2017 outbreak Chikungunya virus belongs to an emerging Aedes albopictus-adapted virus cluster introduced from the Indian subcontinent. Open Forum Infect Dis 6:ofy321. DOI: https://doi.org/10.1093/ofid/ofy321
Liu-Helmersson J, Quam M, Wilder-Smith A, Stenlund H, Ebi K, Massad E, Rocklöv J, 2016. Climate change and Aedes vectors: 21st Century projections for dengue transmission in Europe. EBioMedicine 7:267-77. DOI: https://doi.org/10.1016/j.ebiom.2016.03.046
Maclean IM, Mosedale JR, Bennie JJ, 2018. Microclima: An r package for modelling mesoâ€and microclimate. Methods Ecol Evol 10:280-90. DOI: https://doi.org/10.1111/2041-210X.13093
Manica M, Filipponi F, D’Alessandro A, Screti A, Neteler M, Rosà R, Solimini A, Della Torre A, Caputo B, 2016. Spatial and temporal hot spots of Aedes albopictus abundance inside and outside a south European metropolitan area. PLoS Negl Trop Dis 10:e0004758. DOI: https://doi.org/10.1371/journal.pntd.0004758
Manica M, Rosa R, Della Torre A, Caputo B, 2017. From eggs to bites: do ovitrap data provide reliable estimates of Aedes albopictus biting females? PeerJ 5:e2998. DOI: https://doi.org/10.7717/peerj.2998
McKenzie BA, Wilson AE, Zohdy S, 2019. Aedes albopictus is a competent vector of Zika virus: A meta-analysis. PLoS One 14:e0216794. DOI: https://doi.org/10.1371/journal.pone.0216794
Medlock JM, Avenell D, Barrass I, Leach S, 2006. Analysis of the potential for survival and seasonal activity of Aedes albopictus (Diptera: Culicidae) in the United Kingdom. J Vector Ecol 31:292-304. DOI: https://doi.org/10.3376/1081-1710(2006)31[292:AOTPFS]2.0.CO;2
Medlock JM, Hansford KM, Versteirt V, Cull B, Kampen H, Fontenille D, Hendrickx G, Zeller H, Van Bortel W, Schaffner F, 2015. An entomological review of invasive mosquitoes in Europe. B Entomol Res 105:637. DOI: https://doi.org/10.1017/S0007485315000103
Metelmann S, Caminade C, Jones AE, Medlock JM, Baylis M, Morse AP, 2019. The UK’s suitability for Aedes albopictus in current and future climates. J R Soc Interface 16:20180761. DOI: https://doi.org/10.1098/rsif.2018.0761
Mogi M, Tuno N, 2014. Impact of climate change on the distribution of Aedes albopictus (Diptera: Culicidae) in northern Japan: retrospective analyses. J Medl Entomol 51:572-9. DOI: https://doi.org/10.1603/ME13178
Nawrocki S, Hawley W, 1987. Estimation of the northern limits of distribution of Aedes albopictus in North America. J Am Mosq Control Assoc 3:314-7.
Neteler M, Metz M, Rocchini D, Rizzoli A, Flacio E, Engeler L, Guidi V, Lüthy P, Tonolla M, 2013. Is Switzerland suitable for the invasion of Aedes albopictus?. PLoS One 8:e82090. DOI: https://doi.org/10.1371/journal.pone.0082090
Ogden NH, Milka R, Caminade C, Gachon P, 2014. Recent and projected future climatic suitability of North America for the Asian tiger mosquito Aedes albopictus. Parasit & Vectors 1:1-4. DOI: https://doi.org/10.1186/s13071-014-0532-4
Pasquali S, Mariani L, Calvitti M, Moretti R, Ponti L, Chiari M, Sperandio G, Gilioli G, 2020. Development and calibration of a model for the potential establishment and impact of Aedes albopictus in Europe. Acta Trop 202:105228. DOI: https://doi.org/10.1016/j.actatropica.2019.105228
Petrić M, Lalić B, Pajović I, Micev S, ÄurÄ‘ević V, Petrić D, 2018. Expected changes of Montenegrin climate, impact on the establishment and spread of the Asian tiger mosquito (Aedes albopictus), and validation of the model and model-based field sampling. Atmosphere 9:453. DOI: https://doi.org/10.3390/atmos9110453
Poletti P, Messeri G, Ajelli M, Vallorani R, Rizzo C, Merler S, 2011. Transmission potential of chikungunya virus and control measures: The case of Italy. PLoS One 6:e18860. DOI: https://doi.org/10.1371/journal.pone.0018860
Proestos Y, Christophides GK, Ergüler K, Tanarhte M, Waldock J, Lelieveld J, 2015. Present and future projections of habitat suitability of the Asian tiger mosquito, a vector of viral pathogens, from global climate simulation. Philos Trans R Soc 370:20130554. DOI: https://doi.org/10.1098/rstb.2013.0554
Rezza G, Nicoletti L, Angelini R, Romi R, Finarelli AC, Panning M, Cordioli P, Fortuna C, Boros S, Magurano F, Silvi G, 2007. Infection with chikungunya virus in Italy: an outbreak in a temperate region. Lancet 370:1840-6. DOI: https://doi.org/10.1016/S0140-6736(07)61779-6
Roiz D, Rosà R, Arnoldi D, Rizzoli A, 2010. Effects of temperature and rainfall on the activity and dynamics of host-seeking Aedes albopictus females in northern Italy. Vector Borne Zoonotic Dis 10:811-6. DOI: https://doi.org/10.1089/vbz.2009.0098
Roiz D, Neteler M, Castellani C, Arnoldi D, Rizzoli A, 2011. Climatic factors driving invasion of the tiger mosquito (Aedes albopictus) into new areas of Trentino, northern Italy. PLoS One 6:e14800. DOI: https://doi.org/10.1371/journal.pone.0014800
Schaffner F, Medlock JM, Van Bortel AW, 2013. Public health significance of invasive mosquitoes in Europe. Clin Microbiol Infect 19:685-92. DOI: https://doi.org/10.1111/1469-0691.12189
Scheiner SM, 1993. Genetics and evolution of phenotypic plasticity. Annu Rev Ecol Evol Syst 24:35-68. DOI: https://doi.org/10.1146/annurev.es.24.110193.000343
Sherpa S, Guéguen M, Renaud J, Blum MG, Gaude T, Laporte F, Akiner M, Alten B, Aranda C, Barreâ€Cardi H, Bellini R, 2019. Predicting the success of an invader: niche shift versus niche conservatism. Ecol Evol 9:12658-75. DOI: https://doi.org/10.1002/ece3.5734
Shocket MS, Watts M, Windram F, Rund S, Cator L, Johnson LR, Pawar S, 2019. VectorByte: Public databases of vector abundances and vector performance traits. Entom ESA 2019. Available from: https://www.vectorbyte.org/ Accessed: 07 April 2021.
Stefopoulou Α, Balatsos G, Petraki A, LaDeau SL, Papachristos D, Michaelakis Α, 2018. Reducing Aedes albopictus breeding sites through education: A study in urban area. PLoS One 13:0202451. DOI: https://doi.org/10.1371/journal.pone.0202451
Steiger DBM, Ritchie SA, Laurance SG, 2016. Mosquito communities and disease risk influenced by land use change and seasonality in the Australian tropics. Parasit Vectors 9:387. DOI: https://doi.org/10.1186/s13071-016-1675-2
Succo T, Leparc-Goffart I, Ferré JB, Roiz D, Broche B, Maquart M, Noel H, Catelinois O, Entezam F, Caire D, Jourdain F, 2016. Autochthonous dengue outbreak in Nîmes, south of France, July to September 2015. Euro Surveill 21:30240. DOI: https://doi.org/10.2807/1560-7917.ES.2016.21.21.30240
Succo T, Noël H, Nikolay B, Maquart M, Cochet A, Leparc-Goffart I, Catelinois O, Salje H, Pelat C, de Crouy-Chanel P, de Valk H, 2018. Dengue serosurvey after a 2-month long outbreak in Nîmes, France, 2015: was there more than met the eye? Euro Surveill 23:1700482. DOI: https://doi.org/10.2807/1560-7917.ES.2018.23.23.1700482
Suter TT, Flacio E, Feijoó Fariña B, Engeler L, Tonolla M, Regis LN, De Melo Santos MAV, Müller P, 2016. Surveillance and control of Aedes albopictus in the Swiss-Italian border region: Differences in egg densities between intervention and non-intervention areas. PLoS Negl Trop Dis 10:e0004315. DOI: https://doi.org/10.1371/journal.pntd.0004315
Swanson J, Lancaster M, Anderson J, Crandell M, Haramis L, Grimstad P, Kitron U, 2000. Overwintering and establishment of Aedes albopictus (Diptera: Culicidae) in an urban La Crosse virus enzootic site in Illinois. J Medical Entomol 37:454-60. DOI: https://doi.org/10.1093/jmedent/37.3.454
Takumi K, Scholte EJ, Braks M, Reusken C, Avenell D, Medlock JM, 2009. Introduction, scenarios for establishment and seasonal activity of Aedes albopictus in The Netherlands. Vector Borne Zoonotic Dis 9:191-6. DOI: https://doi.org/10.1089/vbz.2008.0038
Tippelt L, Werner D, Kampen H, 2020. Low temperature tolerance of three Aedes albopictus strains (Diptera: Culicidae) under constant and fluctuating temperature scenarios. Parasit Vectors 13:1-2. DOI: https://doi.org/10.1186/s13071-020-04386-7
Toma L, Severini F, Di Luca M, Bella A, Romi R, 2003. Seasonal patterns of oviposition and egg hatching rate of Aedes albopictus in Rome. J Am Mosq Control Assoc 19:19-22.
Tran A, L’Ambert G, Lacour G, Benoît R, Demarchi M, Cros M, Cailly P, Aubry-Kientz M, Balenghien T, Ezanno P, 2013. A rainfall- and temperature-driven abundance model for Aedes albopictus populations. Int J Environ Res Public Health 10:1698-719. DOI: https://doi.org/10.3390/ijerph10051698
Tsunoda T, Chaves LF, Nguyen GT, Nguyen YT, Takagi M, 2015. Winter Activity and Diapause of Aedes albopictus (Diptera: Culicidae) in Hanoi, Northern Vietnam. J Med Entomol 52:1203-12. DOI: https://doi.org/10.1093/jme/tjv122
Vanwambeke SO, Somboon P, Harbach RE, Isenstadt M, Lambin EF, Walton C, Butlin RK, 2007. Landscape and land cover factors influence the presence of Aedes and Anopheles larvae. J Med Entomol 44:133-44. DOI: https://doi.org/10.1603/0022-2585(2007)44[133:LALCFI]2.0.CO;2
Venturi G, Di Luca M, Fortuna C, Remoli ME, Riccardo F, Severini F, Toma L, Del Manso M, Benedetti E, Caporali MG, Amendola A, 2017. Detection of a chikungunya outbreak in Central Italy, August to September 2017. Euro Surveill 22:17-00646. DOI: https://doi.org/10.2807/1560-7917.ES.2017.22.39.17-00646
Waldock J, Chandra NL, Lelieveld J, Proestos Y, Michael E, Christophides G, Parham PE, 2013. The role of environmental variables on Aedes albopictus biology and chikungunya epidemiology. Pathog Glob Health 107:224-41. DOI: https://doi.org/10.1179/2047773213Y.0000000100
Wint W, Petric D, Bortel W, Alexander N, Schaffner F, 2020. RVF vector spatial distribution models: vector abundance. EFSA Support Publ 17:1847E. DOI: https://doi.org/10.2903/sp.efsa.2020.EN-1847
Wu F, Liu Q, Lu L, Wang J, Song X, Ren D, 2011. Distribution of Aedes albopictus (Diptera: Culicidae) in northwestern China. Vector Borne Zoonotic Dis 11:1181-6. DOI: https://doi.org/10.1089/vbz.2010.0032
Xia D, Guo X, Hu T, Li L, Teng PY, Yin QQ, Luo L, Xie T, Wei YH, Yang Q, Li SK, 2018. Photoperiodic diapause in a subtropical population of Aedes albopictus in Guangzhou, China: optimized field-laboratory-based study and statistical models for comprehensive characterization. Infect Dis Poverty 7:1-3. DOI: https://doi.org/10.1186/s40249-018-0466-8
Žitko T, Merdić E, 2014. Seasonal and spatial oviposition activity of Aedes albopictus (Diptera: Culicidae) in Adriatic Croatia. J Med Entomol 51:760-8. DOI: https://doi.org/10.1603/ME13071

How to Cite

Petrić, M., Ducheyne, E., Gossner, C. M., Marsboom, C., Nicolas, G., Venail, R., Hendrickx, G., & Schaffner, F. (2021). Seasonality and timing of peak abundance of <em>Aedes albopictus</em> in Europe: Implications to public and animal health. Geospatial Health, 16(1). https://doi.org/10.4081/gh.2021.996