Suitability of European climate for the Asian tiger mosquito Aedes albopictus: recent trends and future scenarios

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The Asian tiger mosquito (Aedes albopictus) is an invasive species that has the potential to transmit infectious diseases such as dengue and chikungunya fever. Using high-resolution observations and regional climate model scenarios for the future, we
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  Suitability of European climate for theAsian tiger mosquito  Aedes albopictus  :recent trends and future scenarios Cyril Caminade 1, *, Jolyon M. Medlock 2 , Els Ducheyne 3 ,K. Marie McIntyre 4 , Steve Leach 2 , Matthew Baylis 4 and Andrew P. Morse 1 1 School of Environmental Sciences, University of Liverpool, Liverpool, UK  2 Emergency Response Department, Health Protection Services Division, Health Protection Agency, Porton Down, UK  3 Avia-GIS, Zoersel, Belgium  4 Liverpool University Climate and Infectious Diseases of Animals   ( LUCINDA )  Group,Institute of Infection and Global Health, University of Liverpool, Liverpool, UK  The Asian tiger mosquito ( Aedes albopictus  ) is an invasive species that has the potential totransmitinfectiousdiseasessuchasdengueandchikungunyafever.Usinghigh-resolutionobser-vations and regional climate model scenarios for the future, we investigated the suitability of Europe for  A. albopictus   using both recent climate and future climate conditions. The resultsshow that southern France, northern Italy, the northern coast of Spain, the eastern coast of the Adriatic Sea and western Turkey were climatically suitable areas for the establishmentof the mosquito during the 1960–1980s. Over the last two decades, climate conditions havebecome more suitable for the mosquito over central northwestern Europe (Benelux, westernGermany) and the Balkans, while they have become less suitable over southern Spain. Similartrends are likely in the future, with an increased risk simulated over northern Europe andslightly decreased risk over southern Europe. These distribution shifts are related to wetterand warmer conditions favouring the overwintering of   A. albopictus   in the north, and drierand warmer summers that might limit its southward expansion. Keywords:  Aedes albopictus  ; vector-borne diseases; climate change;regional climate modelling; Europe1. INTRODUCTION The Asian tiger mosquito ( Aedes albopictus  ; FamilyCulicidae) is native to tropical and subtropical areas of southeast Asia. It usually breeds in transient waterbodies in tree holes, and shows the ability to colonizehuman-made containers in urban and peri-urban areas[1]. This species lays drought-resistant eggs, which, inanurbansetting,aredepositedinanumberofcontainers,including discarded used tyres [2]. In recent decades, thisspecieshasinvadedmanycountriesglobally,owingtothetransportation of its drought-resistant eggs with ship-ments of goods (especially used tyres and plants such aslucky bamboo); the speed of such spread has been pro-portional to an increase in international trade. In 1967,its distribution area was restricted to some parts of Asia, India and a few Pacific islands. Since then, it hasspread rapidly to Europe, North and South America,theCaribbean,AfricaandtheMiddleEast (seeelectronicsupplementary material, table S1).  Aedes albopictus   isranked as one of the world’s 100 most invasive species,according to the Global Invasive Species Database(http: // www.issg.org / database / species / search.asp?st=100ss&fr=1&str=&lang=EN).Aswellasbeingabitingnuisance, A.albopictus  hasbeenlinkedtothetransmissionofarboviralandfilarialinfectiousdiseases of humans and animals. Its potential to carry awide range of human pathogens is consequently of wideconcern.  Aedes albopictus   can experimentally transmitnumerous viruses, including those that cause West Nilefever, yellow fever, St Louis encephalitis, Japanese ence-phalitis, dengue fever, Rift Valley fever and chikungunyafever,amongothers[3–6].Itisalsothevectorof  Dirofilaria immitis  , a parasitic round worm that causes heartworm indogs, and less frequently in cats, wolves, foxes and coyotes[7]. It was responsible for the chikungunya outbreak thatoccurredin2005–2006ontheFrenchIslandofLaRe´union.Mutated strains of the chikungunya virus were beingtransmitted by  A. albopictus   particularly well during thisepisode [8]. It was also the vector of chikungunya feverduring the outbreak that occurred in the summer of 2007in the Italian province of Ravenna, which infected over200 people [9]. Recently, in September 2010, two cases of  *Author for correspondence (cyril.caminade@liverpool.ac.uk).Electronic supplementary material is available at http: // dx.doi.org / 10.1098 / rsif.2012.0138 or via http: // rsif.royalsocietypublishing.org. J. R. Soc. Interface  doi:10.1098 / rsif.2012.0138 Published online  Received   22 February 2012 Accepted   5 April 2012  1  This journal is q 2012 The Royal Society  on October 3, 2017http://rsif.royalsocietypublishing.org/ Downloaded from  chikungunya fever and two cases of dengue fever trans-mitted by  A. albopictus   were confirmed in the VarFrench department [10]. In summer 2010, a case of dengue fever was also diagnosed in a German travellerreturning from Croatia [11]. Environmental factors mighthave exacerbated the establishment of   A. albopictus   intonew areas, as its survival range and seasonal activity havebeen shown to be influenced by a combination of climaticand environmental factors such as temperature, humidity,rainfall and photoperiods [3].Several studies have been carried out to model andmap the distribution of   A. albopictus   based on environ-mental factors [12–15]. However, they do not consider the impact of the changing climate from 1950 to thepresent on the spread of the vector. Furthermore,they do not consider the large uncertainties related tothe employed mosquito distribution model and thedifferent climate models that are used to simulatethe future distribution of the mosquito.Here, we model and map the distribution of  A. albopictus   over Europe based on climatic features,using different modelling approaches, and including theproviso that the mosquito has already been introduced.A major novelty of this study is the use of three differentdistribution models to map the climatic suitability of   A.albopictus  forboththecurrentclimateandfutureclimateprojections using a set of steps within the modelling pro-cess. First, differences and similarities across the threedifferent model outputs driven by climate observationsare discussed and validated against field-based obser-vations (mosquito absence / presence) for Europe. Wealso compare how the recent observed climate changecontext might have favoured mosquito establishmentover Europe. In a second step, these distribution modelsare driven by the simulations of the ensemble of 10regional climate models (RCMs) to evaluate how suit-ability for the mosquito might change in the nearfuture (e.g. 2030–2050). This ensemble includes themost up-to-date RCMs that are routinely run by the big-gest climate centres in Europe to study climate change(UK Met Office, Me´te´o-France, etc.). This ensemblehas been driven by the SRESA1B emission scenarioand provides the fine spatial scale information that isrequired for impact studies. Using an ensemble of RCMs (instead of a single model) takes into accountthe uncertainties in future climate projections. This fra-mework has been recently successfully applied to modelbluetongue transmission risk over Europe [16], but thishas not yet been used to map the future distribution of  A. albopictus  , as most of the former published scenariosrelyon a single climate model [15] ora single distributionmodel [14]. Finally, the uncertainties related to themethod (vector distribution model) and to the differentselected RCMs (future climate model spread)are investi-gated to make recommendations at the country level. 2. MATERIAL AND METHODS 2.1. Datasets  The observed distribution of   A. albopictus   in Europe isderived from the ECDC / VBORNET dataset which hasbeen collected since 2009 within the ECDC / VBORNETnetwork [17]. The maps are updated quarterly based onconfirmed presence and absence information from thebroad entomological community. Input of data fromexperts is possible via the VBORNET website (www.vbornet.eu). Absence and presence data of the mosquitoare available at the regional administrative level(NUTS3 or LAU1 dataset; for 52 states or microstates,members of the European Union, located in Europe orclose to it). The observations used in this study arebased on updated data from December 2011.A high-resolution (25 km 2 ) gridded climate datasethas been developed for Europe based on stationmeasurements [18] within the EC FP6 ENSEMBLESproject framework [19]. It provides information onimportant climate impact variables, including rainfall,temperature, minimum and maximum temperaturefor the period of 1950–2009 at daily and monthly tem-poral resolution. This observed climate dataset (EOBShereafter) was used to estimate the recent climateenvelope of   A. albopictus   in Europe.Regional scenarios for climate change impact assess-ments require finer spatial resolution than thoseprovided by general circulation models (GCMs) thathave a coarse resolution (about 300 km 2 ). The ENSEM-BLES European project provides improved RCMs, forboth recent past (1961–2000) and future climate scen-arios (1950–2050). Models covering the Europeandomain with a regular 0.25 8  step consistent with theobservation grid were retained. Two ensembles of simu-lations have been carried out, the control experiment(SimCTL) and the Scenario experiment (SimA1B). Inthe SimCTL experiment (1961–2000), all RCMs areforced at their boundaries by the ERA40 reanalysis[20]. Observed external forcing (greenhouses gases,solar, volcanic, aerosols) is applied to all RCMs. In theSimA1B experiment (1961–2050), the RCMs are forcedat their boundaries by a GCM with a coarser resolution(about 300 km 2 ) forced by the SRESA1B emission scen-ario (median scenario in terms of CO 2  emissions [21]).Different GCMs were used to drive the RCMs accordingto this plan: http: // ensemblesrt3.dmi.dk / .The 10 selected RCMs (and the related operationalcentre which ran the experiments) are: C4IRCA3 (MetE´ireann, Ireland), CNRM-RM4.5 (CNRM, Me´te´o-France), DMI-HIRAM5 (DMI, Denmark), ETHZ-CLM(ETHZ, Switzerland), ICTP-RegCM3 (ICTP, Italy),KNMI-RACMO2 (KNMI, The Netherlands), METO-HC-HadRM3.0 (Met Office, UK), MPI-M-REMO(MPI, Germany), OURANOSMRCC4.2.1 (OURANOS,Canada), SMHIRCA (SMHI, Sweden).Only the SimA1B future scenario ensemble wasconsidered in this study. Simulated precipitation andtemperature outputs for each RCM have been meanbias corrected with respect to the EOBS dataset overthe 1990–2009 reference period (see the electronicsupplementary material for further details). 2.2. Models  2.2.1. Overwintering  Different climatic thresholds were first considered todefine the ability of the mosquito to survive Europeanwinters based on Medlock  et al  . [12]. Totally, suitable 2  Asian tiger mosquito climate suitability   C. Caminade  et al  . J. R. Soc. Interface   on October 3, 2017http://rsif.royalsocietypublishing.org/ Downloaded from  overwintering conditions were defined for mean annualrainfall (AR) above 700 mm andmeanJanuary tempera-tures ( T  Jan ) above 2 8 C. Overwintering conditions for alow (defined as 600 mm , AR , 700 mm and 1 8 C , T  Jan , 2 8 C), medium (defined as 500 mm , AR , 600 mm and 0 8 C , T  Jan , 1 8 C) and highly unsuitablescenario (defined as AR , 500 mm and  T  Jan , 0 8 C)havebeeninvestigatedandare discussed intheelectronicsupplementary material. We retained the later scenarioas a standard to mask the areasthat would be unsuitablefor the mosquito for two of the following mappingmethods (this is consistent with results shown in[3,15,22–24]). For a more detailed discussion about the overwintering of   A. albopictus  , see the electronicsupplementary material.Three models were used for mapping the distributionof   A. albopictus  : 2.2.2. Model 1. Establishment criteria based on mean annual temperature and overwintering after the Geographic Information System (GIS)-based model developed by Kobayashi   et al. [ 25  ]The aforementioned overwintering criterion (suitabilityfor  T  Jan . 0 8 C and AR . 500 mm) was combined withmean annual temperatures to define basic climate suit-ability zones for the mosquitoes. Totally suitableconditions were defined for mean annual temperatureabove 12 8 C. A high, moderate and low risk was thendefined for mean annual temperature ranging from11 8 C to 12 8 C, 10 8 C to 11 8 C and 9 8 C to 10 8 C, respect-ively. The selection of these thresholds was based onthe analysis of Kobayashi  et al  . [25], which showed that  A. albopictus   was relatively well established inJapan for mean annual temperatures above 11 8 C,while establishment was more stable for annual temp-eratures above 12 8 C. Areas in North America whereannual temperatures were above 11 8 C also strongly cor-responded to the observed pattern of the distribution of  A. albopictus   in the USA. Further, this is also consistentwith the European climatic envelope for  A. albopictus  as shown in Fisher  et al  . [15] and ECDC [14]. 2.2.3. Model 2. Multi-criteria decision analysis after ECDC   [ 14 ]AR, January and summer (June–July–August) temp-eratures were first transformed into an interval rangingbetween 0 and 255 using sigmoidal functions (figure 1).This model does not include the overwintering criterion.Instead, forannual precipitation, suitability was reducedto zero when rainfall was lower than 450 mm, and maxi-mum when precipitation was higher than 800 mm; forsummer temperatures, suitability was zero when temp-eratures were lower than 15 8 C and higher than 30 8 C,and maximum between 20 8 C and 25 8 C; for Januarytemperatures, suitability was zero when temperatureswere lower than  2 1 8 C, and maximum when tempera-tures were higher than 3 8 C. The three parameters werethen linearly combined (arithmetic average) to definethe suitability for  A. albopictus  . The suitability wasfinally arbitrarily rescaled to range between 0 and 100. 2.2.4. Model 3. GIS-based seasonal activity model after Medlock et al.  [ 12  ]This model combines the aforementioned overwinteringcriterion with weekly temperatures and photoperiods tosimulate the weeks of activity of   A. albopictus   betweenthe onset of hatching and the autumn egg diapause.Photoperiod was calculated based on the differencebetween sunrise and sunset for each grid point of theclimate dataset grid (using astronomical equationsfrom the National Oceanic and Atmospheric Adminis-tration). First, the aforementioned overwinteringcriterion was employed to mask the areas wherethe mosquito would not be able to survive. Then, thestart of spring hatching and autumn egg diapause wascomputed based on the medium scenario: the onset of hatching starts when spring temperature and photo-period are above 10.5 8 C and 11.25 h, respectively. Theautumn diapause occurs for a temperature thresholdof 9.5 8 C and a photoperiod threshold of 13.5 h. 2.2.5. Model validation  The performances of different models in reproduc-ing the observed distribution of   A. albopictus   were 280( a ) ( b ) ( c )240200160120      s     u       i       t     a        b       i        l       i       t     y 80400200 400 600 –2 –1 0 1 2 3 4 5 8 12 16 20 24 28 32 36summer temperature (ºC)January temperature (ºC)rainfall annual (mm)800 1000 Figure 1. Sigmoidal functions that are employed to relate  A. albopictus   suitability (ranging from 0 to 255) to climate predictorvariables such as ( a  ) annual precipitation, ( b ) January temperature and ( c  ) summer temperature. This is carried out for model 2.For annual precipitation, suitability is dropped to zero when rainfall is lower than 450 mm, and maximum (255) when precipi-tation is higher than 800 mm; for January temperature, the suitability is zero when temperatures are lower than  2 1 8 C, andmaximum when temperatures are higher than 3 8 C; for summer temperature, the suitability is zero when temperatures arelower than 15 8 C and higher than 30 8 C, and maximum between 20 8 C and 25 8 C. Asian tiger mosquito climate suitability   C. Caminade  et al  . 3 J. R. Soc. Interface   on October 3, 2017http://rsif.royalsocietypublishing.org/ Downloaded from  evaluated using the area under the receiver operatingcharacteristic (AUC), a threshold independent qualitycriterion [26]. The AUC is equal to the probability (ran-ging from 0 to 1) that a classifier will rank a randomlychosen positive instance (presence location) higher thana randomly chosen negative one (absence location).UsefulpredictivemodelshaveanAUCofabout0.7,excel-lent models would be above AUC  0.9 and a randommethod would have an AUC  0.5. All model outputswere linearly rescaled between 0 and 1 before being com-pared with the observed absence / presence data. Spatialcorrelations between the different distribution modelsare also investigated. 3. RESULTS 3.1. Recent trends  The recent observed distribution of   A. albopictus   basedon field measurements is shown in figure 2. The speciesis mainly abundant around the coasts of the Mediterra-nean and the Adriatic. More precisely,  A. albopictus  has been reported over the eastern coast of Spain,southeastern France, Corsica, Sardinia, Sicily, most of Italy, southern Switzerland, the coast of Slovenia, thecoast of Croatia, northwestern Bosnia and Herzegovina,most of Montenegro and Albania, northwestern Serbia,the western coast of Greece, southeastern Bulgariaand in Turkey near the Greek border. The species hasalso been sporadically observed in several used-tyrestorage centres in northern France, Belgium and TheNetherlands (here, also in greenhouses) since 1999, aswell as on parking areas in southwestern Germany nearthe French / Swiss border (2007 and 2011). In most of these locations, the mosquito has not established or hasbeen eliminated (elimination is ongoing in The Nether-lands). Thus, these findings do not appear on figure 2,where only current established populations are con-sidered. Whether the recent finding in Germanycorresponds to an established population is not yetknown (see electronic supplementary material, table S1and references). The UK, Portugal, Czech Republic,Slovakia and Moldova appear to have no  A. albopictus  .Figure 3 depicts the changes in simulated cli-mate suitability for  A. albopictus   based on differentmodels, provided it has been previously introduced.  Aedes albopictus indigenousrecently presentabsentno dataunknownoutermost regionsAzores (PT)Canary Islands (ES)Madeira (PT)Svalbard/Jan Mayen (NO)current known distribution: December 2011 Figure 2. Known distribution of   A. albopictus   based on field observations from the ECDC / VBORNET project (December 2011).Dark red denotes established: the species is observed in at least one municipality of the shown administrative unit for at least 5years counting back from the ‘distribution status date’. Red, recently present: the species was observed at least in one munici-pality during the last 5 years. Green, absent: surveys and studies on mosquitoes were conducted during the last 5 years andno specimens were reported. Medium grey, no data: no data over the last 5 years are available to local experts. Light grey,unknown: no information is available on the existence of studies on mosquito fauna over the last 5 years. 4  Asian tiger mosquito climate suitability   C. Caminade  et al  . J. R. Soc. Interface   on October 3, 2017http://rsif.royalsocietypublishing.org/ Downloaded from  Considering model 1, southwestern and southeasternFrance, Portugal, the northeastern and northwesterncoasts of Spain (including the south west, Corsica andSardinia), northern Italy and its western coasts, theeastern coasts of the Adriatic Sea and western Turkeyappear to be highly suitable for the establishment of  A. albopictus   over the 1960–1989 period (figure 3 a  ).During the last two decades (1990–2009), climate suit-ability increased over France, Italy, the southern UKand it spread over central Europe (Benelux and westernborder of Germany), western Hungary, the Balkans(Croatia, the northern part of Serbia and Montenegro,Bosnia and Herzegovina) and Sicily, while it decrea-sed over southern Spain and Sardinia (figure 3 b ).These changes are mainly related to observed warmerwinter temperatures over northwestern Europe, whilethe decrease in suitability can be attributed to drierconditions over southern Spain and Sardinia (seeelectronic supplementary material, figure S4).Similar results are highlighted over Western Europeusing model 2. The hot spots for the establishmentof the tiger mosquito in Europe can also be seen oversouthern France, Sardinia, Corsica and Italy, thecoasts of the Adriatic, Spain and Portugal for theperiod of 1960–1989 (figure 3 c  ). However, the simulatedsuitability pattern is different over the UK and is signifi-cantly less over southern Spain and Portugal withrespect to model 1. This is related to the inclusion of con-tinuous summer temperatures and AR in model 2 andthe fact that no strict overwintering criterion has beenincluded. Indeed, the climate suitability decreases overeastern England as the area is too dry and not warmenough in summer, whereas the differences in southernSpain and Portugal can be related to too dry and warmsummer conditions (see electronic supplementarymaterial, figure S4). The risk then spreads and increasesoverFrance,northernItaly,centralEurope(Beneluxandwestern Germany) and the Balkans during the last twodecades (figure 3 d  ).Finally, the simulated periods of activity of  A. albopictus   are compared between the periods1960–1989 and 1990–2009 using model 3. The areaswhere the mosquito has the longest activity (aboutfive months) are southern France, the northwesterncoast and the southwest of Spain, Portugal, northernItaly, the eastern coast of the Adriatic and westernTurkey for the period 1960–1989 (figure 3 e  ). The mos-quito is simulated to be active for four months overBenelux and western Germany, and between threeand four months over the southern UK. The annual 50   N( a )( b )( c )( d  )( e )(  f  )40   N50   N40   N50   N40   N50   N40   N50   N40   N50   N40   N020   E020   E020   E020   E020   E020   Esuitablehigh risk medium risk low risk no suitabilitysuitability908070605025weeks252118161411 Figure 3. Observed climate suitability of   A. albopictus   based on different models (rows) and for two different time periods (col-umns). ( a  , b ) The climate suitability is calculated based on model 1 for ( a  ) 1960–1989 and ( b ) 1990–2009. ( c  , d  ) The climatesuitability is based on model 2. This is carried out for ( c  ) 1960–1989 and ( d  ) 1990–2009. ( e  ,  f   ) Weeks of adult mosquito activityfor ( e  ) 1960–1989 and (  f   ) 1990–2009 based on model 3. See §2 for further details. Asian tiger mosquito climate suitability   C. Caminade  et al  . 5 J. R. Soc. Interface   on October 3, 2017http://rsif.royalsocietypublishing.org/ Downloaded from
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