In the Old World, sandfly species of the genus Phlebotomus are known vectors of Leishmania, Bartonella and several viruses. Recent sandfly catches and autochthonous cases of leishmaniasis hint on spreading tendencies of the vectors towards Central Europe. However, studies addressing potential future distribution of sandflies in the light of a changing European climate are missing. Here, we modelled bioclimatic envelopes using MaxEnt for five species with proven or assumed vector competence for Leishmania infantum, which are either predominantly located in (south-) western (Phlebotomus ariasi, P. mascittii and P. perniciosus) or south-eastern Europe (P. neglectus and P. perfiliewi). The determined bioclimatic envelopes were transferred to two climate change scenarios (A1B and B1) for Central Europe (Austria, Germany and Switzerland) using data of the regional climate model COSMO-CLM. We detected the most likely way of natural dispersal (“least-cost path”) for each species and hence determined the accessibility of potential future climatically suitable habitats by integrating landscape features, projected changes in climatic suitability and wind speed. Results indicate that the Central European climate will become increasingly suitable especially for those vector species with a current south-western focus of distribution. In general, the highest suitability of Central Europe is projected for all species in the second half of the 21st century, except for P. perfiliewi. Nevertheless, we show that sandflies will hardly be able to occupy their climatically suitable habitats entirely, due to their limited natural dispersal ability. A northward spread of species with south-eastern focus of distribution may be constrained but not completely avoided by the Alps. Our results can be used to install specific monitoring systems to the projected risk zones of potential sandfly establishment. This is urgently needed for adaptation and coping strategies against the emerging spread of sandfly-borne diseases.
Globally, the number of vector-borne infections in humans and animals increases rapidly, meanwhile causing almost one third of all cases of emerging infectious diseases [1]. In the Old World, sandfly species of the genus Phlebotomus serve as vectors for sandfly-borne pathogens such as Leishmania, Bartonella and several viruses (e. g. Phlebovirus, Vesiculovirus and Orbivirus) [2]–[4]. Sandfly-borne diseases and in particular visceral leishmaniasis are a main public health concern [5], which demands more attention in science and policy [6]. While the spatial distribution of leishmaniasis seems to expand in southern parts of Europe [7], [8], first cases of autochthonous origin are recently reported from Central Europe [9]–[11], where this disease was not endemic in the past. The presence of sandflies as vectors is mainly regulated by the species' climatic requirements on temperature and humidity or soil moisture, respectively [3], [12]–[15]. Temperature and humidity are also the main factors impacting the altitudinal structure of sandfly occurrences [16]. It is known that sandflies react very sensitive to wind speed and prefer breeding sites sheltered from wind [17]–[20]. Beyond that, high wind speed decreases or even excludes flight activity [17], [21]. For the purpose of inferring geographic distribution for sandflies, the advantages of ecological niche models have been demonstrated on the example of Lutzomyia species (Lutzomyia spp.) in the New World [22]. For the first time, Peterson and Shaw [23] integrated climate change scenarios in order to project future distribution of Lutzomyia spp. in Brazil. Recently, range expansions for sandflies of the genus Lutzomyia have also been projected for North America in the face of climate change [24]. For Europe, surprisingly, only few studies estimated the risk of potential range expansions of sandflies in the face of climate change (e. g. [25], [26]). The need for such studies is supported by the first sandflies catches in Central Europe. P. mascittii has been caught in Austria on the frontier to Slovenia [27]. Furthermore, P. mascittii is reported from the “Upper Rhine Valley” in the outermost southwest of Germany near the French border [28]. P. perniciosus seems to be established in the German state of “Rhineland-Palatinate” [29]. These findings may either indicate spreading tendencies from Mediterranean regions or range expansion from small Central European refugial areas, which may have already been occupied by the species during the Holocene climate optimum about 6,500 years ago [30]. Possibly, sandflies has occupied more areas in the past than it was noticed. For Austria, establishment of sandflies in formerly non-endemic areas can be expected already by moderately increasing temperatures in the 21st century [25]. Recently, Fischer et al. [26] estimated potential temperature-derived establishment of sandflies in Germany by transferring the required temperature during their activity phase and annual mean temperature for persistence to the expected future climate conditions in Germany using data of a spatio-temporal highly resolved regional climate model. But up to now, projections of the current and climate-driven potential future distribution of Phlebotomus spp. which additionally consider species-specific dispersal ability are missing. As climate is expected to change rapidly in the 21st century, sandflies are forced to react promptly. Here, we close this gap of knowledge and hypothesise:
It is well known that species dispersal ability is dependent on the environment and varies strongly with landscape structure [53]. In order to make projections more realistic according to spatial characteristics, we used a least-cost path analysis based on graph theory [54]–[56] to determine the most likely way for Phlebotomus spp. to move across a spatio-temporally changing landscape. The path function indicates the least efforts (“costs”) for a species in moving through any particular cell in the respective landscape [57]–[59]. Least-cost path analyses are frequently used to determine potential dispersal pathways for mammals [60]–[63] but have also been applied to insects [58].
AUC-values yielded in high scores for five species (Table 1). Binominal tests indicated that tests points are predicted better by the model than a random prediction with the same factional predicted area at the significance level p<0. 01. Similarity between current and projected climate is analysed by MESS-analysis. Highest similarity in projections is indicated for southern parts of Germany, the northernmost regions of Switzerland as well as for eastern and north-eastern parts of Austria. Instead, lowest similarity exists for alpine regions and northern Germany. However, our projections seem not to be biased by non-analogue climate. In general, climatic suitability can be expected to increase for all species in the 21st century (Figure 3 and S1, Table 3 and S1). This is in accordance with the first part of our first hypothesis assuming increasing climatic suitability for the species in Central Europe. Nevertheless, we cannot completely verify the second part of our first hypothesis of more favourable conditions in the (south-) westernmost parts of Central Europe for species with current (south-) western focus of European distribution and the opposite for species which are currently distributed in (south-) eastern parts of Europe. Overall, projections based on the A1B scenario (Table 3) represent higher suitability for species in comparison to projection of the B1 scenario (Table S1). Nevertheless, the spatial patterns of potential climatically suitable habitats remain to be the same for both scenarios. The detailed annotation of climatic suitability in the following refers to the A1B scenario. In general, projections hint on spreading tendencies for all studied Phlebotomus spp. to areas where they have not occurred so far in both scenarios (Figure 4 and S2). Nevertheless, sandfly species will not be able to become established in all climatically suitable areas of Central Europe according to the limited natural dispersal ability. The detected dispersal pathways show some differences between the two applied scenarios, in contrast to the modelled climatic suitability, where just temporal but no spatial variations are pointed out. The first part of our second hypothesis that species with current (south-) western focus of distribution are likely to disperse eastwards can be affirmed only for P. perniciosus but not for P. ariasi and for P. mascittii. We cannot confirm the part of the second hypothesis that the Alps will prohibit completely a northward spread for the species which are currently distributed in (south-) eastern European regions. However, it is very likely that the Alps will decelerate the range expansion.
Our aim was to determine future occurrences of five Phlebotomus spp. with spreading tendencies in the face of a changing climate. These sandflies serve as proven or assumed (P. mascittii) vectors of Leishmania infantum causing the leishmaniasis. Knowledge concerning the potential future presence of disease vectors is a first step towards an accurate and efficient risk assessment of vector-borne diseases [72]. Conventional static bioclimatic niche modelling can be extended by novel avenues for instance regarding species-specific abilities to disperse [73]. Therefore, we integrated species-specific dispersal pathways to the detected climatically suitable habitats. Within this study, we focus on active and natural dispersal of the species and excluded potential human assistance for range expansions, for instance via the transport of subtropical plants containing eggs or larvae in the moist substrate. However, these effects are not clearly understood and hence not included in this analysis. The results of this study represent the minimum range expansion of Phlebotomus spp. that is only related to active and natural movement in a changing environment without potential human-assistance. Our results suggest that the development of Central European climate will increasingly support suitable habitats for phlebotomine sandflies. This general trend will become even more pronounced in the second half of the 21st century. We project sandfly establishment in formerly non-endemic areas. This will additionally increase the risk of emerging sandfly-borne diseases in Central Europe such as leishmaniasis. Nevertheless, it is unlikely that sandflies will reach and occupy the provided climatically suitable habitats entirely. During the upcoming years, a spatial focus of surveillance regarding potential new-establishment of Phlebotomus spp. with current south- (western) focus of distribution should be directed for western parts of the German state “North Rhine-Westphalia”. These species may additionally occupy the regions around the “Lake Constance” (southern part of Germany and northern part of Switzerland). Furthermore, Switzerland must be aware on potential sandfly occurrences around the river valley of the “Aare” and the “Lac dé Neuchâtel’ already within some years. In Austria, especially the south-eastern states “Carinthia’, “Styria’ and “Burgenland’ seem to be at risk by new-infestations due to the spreading tendencies of P. mascittii and P. ariasi. In the case of sandfly species with current south (-eastern) focus of distribution (P. neglectus and P. perfiliewi), the canton “Ticino” in southern Switzerland must be alert. According to our results, especially the regions around “Lago Maggiore” and “Lago di Lugano” should be monitored systematically. Furthermore, the Austrian regions neighbouring Slovenia and Hungary should be prepared for the establishment of these sandfly species in the near future. The main limitation in our projections refers to the accuracy of georeferencing maps of sandfly distribution. We have chosen an algorithm that is capable to cope with this source of uncertainty [48]. Expectedly, improved model projections would arise with geographically more accurate point data. However, the intension of this paper is rather to provide a methodological approach. Recently, it has been pointed out that pixel values of predictor variables in close proximity will be highly correlated, which would reduce the effect of inaccuracy in spatial data set of species occurrences [74]. Furthermore, when comparing the reports for cases of autochthonous leishmaniasis in regions that were considered as being non-endemic (e. g. [9]) with documented presence records of sandflies leads to the assumption that sandflies may be wider distributed than realised. However, as it is unknown which species acted in such regions as vectors, only documented presence records at the species level of the Phlebotomus spp. can reasonably be integrated. Assuming climate is generally considered to be suitable for the permanent establishment of populations, the presence of Phlebotomus spp. is additionally dependent on land cover e. g. forest, agriculture and urban areas [75], [76]. In this study, we integrated altitudinal structures such as river valleys and mountain ridges in least-cost path analysis. In order to recalculate wind speed we additionally integrated land cover data as surface roughness to decelerate near-surface wind speed. Climate change may contribute to alterations in land use and cover, due to warming, changes of precipitation regimes and increases of climatic extreme events such as droughts or floods. This is likely to affect the spatial structure of agricultural systems. In addition to direct climatic impacts, these changes of land cover will additionally affect the spread and distribution of sandflies. However, land cover and land use changes depend on complex processes of decision making under specific political and economical conditions [77] and are hence difficult to project. Therefore land use and cover were considered to remain constant in this study. In general, biotic interactions such as predation or competition are crucial for species distribution [78]. The modifications of the ecological links or networks of an organism by climate change can substantially alter the realised niche of species population [79]. In Germany, P. perniciosus and P. mascittii do not co-exist at the same locations [29]. This can be a result of diverging invasion pathways or of competitive exclusion in the respective regions. Unfortunately, knowledge on biotic interactions of sandflies is scarce. Furthermore, one has to bear in mind that presence of phlebotomine sandflies is dependent on humans and their social factors, for instance living conditions [80], [81]. However, all these factors become more important for species distribution on smaller spatial scales than applied in this study [82], [83]. Concerning the least-cost analysis for species movement it has to be noted that the attributed costs are based on assumptions and/or preliminary observations and hence may not include all of the relevant factors [55], [61]. For instance, it is questionable whether humans assist in the spread of sandflies. Nevertheless, in comparison to mosquitoes, direct human effects on dispersal are of minor importance. Furthermore, the species movement behaviour must not necessarily be optimal or well adapted in human-modified landscapes [53]. Especially dispersal behaviour of individuals between populations may differ from the general tendency at the metapopulation level [58]. Besides the effects of changes in long-term climatic conditions used in this study, extreme weather events are expected to increase in Europe [84]. This will influence organisms and ecosystems remarkably [85], [86]. It has been shown that climatic variability in general [87] and extreme weather events such as floods particularly affect sandfly occurrences [88]. In order to integrate weather extremes in a satisfactory quality within climatic projections, a further downscaling of their spatial resolution to the local scale is required [89]. This is the only way to account for the contribution of weather extremes on disease vectors in risk analysis. Bioclimatic envelope models are powerful tools to envisage potential responses in species distribution to climate change from regional to global scales [82], [90]. They can be seen as a useful first filter for approximations of the impact of climate change on the species distribution [82], [91]. A well-adapted modelling approach is required to project climate change effects on species [44]. Therefore, we selected MaxEnt as algorithm, due to better performances in comparison with further presence-only and (pseudo-) presence-only algorithms (see chapter Model runs for details). Results yielded in high model quality criteria, emphasised by threshold-dependent and independent criteria for Phlebotomus spp. In order to cope with the general uncertainty in species distribution modelling regarding the climatic evolvement [78], we projected the climatic suitability based on two IPCC [37] scenarios (A1B and B1) that best illustrate the respective storyline. We choose bioclimatic variables that are considered to be biologically meaningful variables for model input. Our projections of future climatic suitability refer to data of the European regional climate model CCLM, which is nested into the well-established global climate model ECHAM5 [35]. In comparison to their driving global models, regional patterns of climate change are projected more precisely, which enhances the quality of climate impact studies [36]. For instance, global climate models fail particularly in replication of observed wind speeds. Obviously, projections of changes in wind speed profit from downscaling to the regional level [92]. Furthermore, potential regions with non-analogue climatic conditions and where hence projections are inappropriate were excluded via MESS-analysis. Evidently, the consideration of the dispersal capacity of insects in a changing climate improves the quality of projections of species distribution [93]. Hence, we combined projected climatic suitability in the 21st century with dispersal ability for five Phlebotomus spp. We practiced least-cost analysis for future movement patterns by including temporarily stable (elevation, landscape features) and variable factors (wind speed and development of climatic suitability). This allows integrating and combining expert knowledge on sandfly ecology and biology with statistical methods. In doing so, potential species-specific dispersal pathways can be pointed out. This offers the opportunity to distinguish between climatically suitable habitats that can be reached by invasive species and those that are not accessible to them. The proposed method for the detection of dispersal pathways can be applied to other invasive and mobile disease vectors in the face of climate change. For this purpose, however, species-specific cost surfaces have to be generated. The Alps, for instance, may not be seen as crucial natural barrier for the mainly human-assisted spread of invasive mosquitoes such as the Asian tiger mosquito (Aedes albopictus). However, they are an efficient natural barrier for other species. Here, we provide a powerful methodological approach to extend conventional bioclimatic envelope modelling of disease vectors by species specific dispersal ability. Our findings promise more realistic projections concerning the vector species future distributions. We identify those Central European regions that are especially exposed to the emerging threat of disease vectors in the light climate change. For the modelling of hitherto neglected vector-connected risks, expertise from various scientific disciplines has been taken into account. Proactive monitoring activities and development of feasible adaptation strategies are required before the establishment of disease vectors may take place. Hence, those analyses help to focus control programmes on specific areas at risk on a regional scale. Due to the identification of spatial hot-spots for such activities, cost- and time-efficient surveillance strategies can be developed. This enables target-orientated counteractions directed against the suggested spread of disease vectors in time. Consequently, the risk of disease transmission in formerly non-endemic areas can be reduced. Once disease vectors such as sandflies are established, vector control and disease prevention have proven to be limited.
Growing evidence exists on the emergence of sandfly-borne diseases in the light of climate change. Determining the principle responses of phlebotomine sandflies to climatic changes supports our understanding of future regions that will be threatened by new-establishments of this important group of disease vectors. The aim of this paper is to combine projected climatic suitability for five Phlebotomus species in Central Europe (Austria, Germany and Switzerland) for different time-periods during the 21st century with their potential spreading capacity to disperse to climatically suitable areas. We indicate that the Central European climate will develop toward the preferred bioclimatic niche of the species, especially from mid-century onwards. Nevertheless, we also elucidate within this study that sandflies will hardly be able to occupy the whole areas that will provide suitable climatic conditions due to their limited natural dispersal ability. Our approach provides a framework to combine statistical modelling techniques with expert knowledge on species ecology. Indications of future occurrences of disease vectors may help to initiate surveillance systems in specific regions at an early stage of risk exposure. Hence, the threat of the climate-driven spatial extension of disease vectors and consequently of potentially emerging vector-borne diseases can be counteracted.
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Combining Climatic Projections and Dispersal Ability: A Method for Estimating the Responses of Sandfly Vector Species to Climate Change