1 INTRODUCTION

Biodiversity is undergoing a drastic decline worldwide, threatening ecosystems at unprecedented rates (Butchart et al., 2010; Scheffers et al., 2016). Anthropogenic stressors, including land use intensification, pesticides and greenhouse gas emissions, are attributed as dominant causes of this global phenomenon, inducing both an alarming increase of mean temperature (IPCC, 2015) and land cover changes (Lebrun, Thogmartin, Thompson, Dijak, & Millspaugh, 2016). It is now accepted that destruction and degradation of natural ecosystems are occurring, typically leading to smaller and smaller isolated fragments. Such habitat fragmentation constitutes the primary cause of declines in global biodiversity (Pereira et al., 2010; Rands et al., 2010).

Plant–pollinator interactions constitute one of the most iconic examples of mutualistic associations in the living world (Ollerton, Winfree, & Tarrant, 2011; Waser, 2006). Estimations report that more than 300,000 flowering plant species are pollinated by animals worldwide, representing about 87.5% of the estimated species diversity of angiosperms (Ollerton et al., 2011). At the global scale however, plant–pollinator interactions are increasingly at risk of disruption from human activities (Dalsgaard, 2020; Memmot, Craze, Waser, & Price, 2007). Shifts in forb and pollinator phenologies leading to temporal mismatches, non-random species extinctions and loss of spatial co-occurrences between interacting plant–pollinator species constitute key causes of their decline (Burkle, Marlin, & Knight, 2013; Carvell et al., 2017; Gérard, Vanderplanck, Wood, & Michez, 2020; Schleuning et al., 2016).

Among these main flowering plant pollinators, bumblebees (genus Bombus) form an ecologically and economically crucial bee group for numerous wild plant species and food crops, particularly in the Northern Hemisphere (Berenbaum et al., 2007; Cameron & Sadd, 2020). Over the last few decades however, bumblebee decline in both range and abundance has been a substantial concern in the field of pollinator conservation (Kerr et al., 2015). Alarming predictions have recently brought to light the probable impacts of global warming on bumblebee distribution at the European scale, with up to 36% of the European species expected to lose more than 80% of their current range (Rasmont et al., 2015). Moreover, anthropogenic landscape transformation is unanimously considered as one of the leading causes of bumblebee losses at a large scale (Williams & Osborne, 2009) along with parasites and pathogen spillovers, pesticide use (Cameron et al., 2011; Goulson, Nicholls, Botias, & Rotheray, 2008; Graystock et al., 2013; Kerr et al., 2015) and the combination of these different factors (Goulson et al. 2015, Cameron & Sadd, 2020). Locally, bumblebee species diversity is associated with flower-rich grasslands that provide them with continuous supply of forage plants throughout their flight season (Cameron & Sadd, 2020; Vray et al., 2019). In these habitats, bumblebees show preferential foraging on plants providing resources with a specific nutritional balance (Vaudo et al., 2020), which can drastically impact their fitness (Carvell et al., 2017; Vanderplanck, Martinet, et al., 2019; Vanderplanck et al., 2014; Vanderplanck, Roger, et al., 2019). However, despite the growing knowledge on the ecological requirements and causes of decline of bumblebees, the environmental parameters defining their distribution remain largely unknown. Consequently, the consideration of both taxon identity and species-specific habitat is often omitted in current global conservation strategies.

In this study, we focus on the climatic and land cover variables that best predict the distributions of West-Palaearctic bumblebee species. We first explore whether the distribution of bumblebee species can be explained by similar combinations of variables or whether each taxon presents its own specific climatic and land cover requirements. Second, because the climatic and land cover requirements of the different studied species could be at least partly explained by their evolutionary history, we test whether a phylogenetic signal underlies the relative importance of each environmental variable in species distribution models. Thirdly, in order to give insights into a potential prioritization of mitigation strategies based on the ranges and conservation statuses of species, we investigate whether the relative importance of climatic variables in species distribution models is related to species range sizes, population trends or conservation statuses. Finally, we discuss the importance of considering the present findings to further investigate how to set priorities in landscape management for pollinator conservation, at both local and global scales.

2 MATERIALS AND METHODS

3 RESULTS

3.1 Species distribution modelling approaches and areas under the curve

We have performed SDM analyses and generated distribution maps for 68 bumblebee species (see Figure 1 for representative distribution maps, and Figures S3–S4 for all the estimated distribution maps). Most species distribution models are associated with the highest AUC value when based on the first set of analyses, that is analyses performed without filtering on adjacent raster cells. However, for nine species, we obtain higher AUC values with the second set of analyses, that is analyses performed when filtering on adjacent cells. Details on averaged “training” and “test” AUC values are available in the Table S2.

3.2 Relative importance of climatic and land cover variables in species distribution models

The relative importance of climatic and land cover predictors in each species distribution model is summarized in Figure 2. In addition, response curves obtained for each climatic and land cover predictor are displayed in Figure S5. No clear pattern or species clustering stands out when comparing the relative importance of climatic and land cover variables between species (Figure 2), this latter observation being further confirmed with a principal correspondence analysis based on these same relative importance measures (Figure S6). However, the comparison of species-specific response curve obtained for each environmental variable highlights a series of trends that seem shared by several Bombus species (Figure S5): the probability of occurrence globally tends (a) to increase with grassland coverage, (b) to decrease with both relatively higher temperature and precipitation seasonality and (c) to be maximal around a specific annual mean temperature value. However, for the other environmental variables investigated here, shared trends among species appear less easy to distinguish.

3.5 Range sizes and importance of climatic variables in species distribution models

The link between the total contribution of climatic variables to species distribution models and the approximated range size of the different species is depicted in Figure 3. There is a statistically supported trend (Spearman's rank correlation ρ = 0.399, p-value < .001) for higher total contribution of climatic variables to species distribution models obtained for broadly distributed bumblebee species. When discarding outlier species such as Bombus hyperboreus and B. polaris, that is two species with narrow northern ranges associated with cold temperature, the Spearman rank correlation value increases by ~25% (ρ = 0.496). Overall, widespread species therefore tend to show distribution patterns that are better predicted by temperature and precipitation factors (e.g. the ubiquitous B. hortorum and B. terrestris). Conversely, this involves a higher importance of land cover variables for more narrowly distributed bumblebee species (e.g. the eastern species B. armeniacus and B. sulfureus). Although less frequent, a few widespread bumblebees also seem quite impacted by land cover variables (e.g. B. pascuorum) and some localized ones sometimes predominantly by climatic variables (e.g. the arctic B. hyperboreus and B. polaris).

4 DISCUSSION

Understanding the parameters explaining the distribution of species across broad and restricted geographic scales constitutes a key and common goal in macroecology, biogeography and wildlife conservation (Gaston & Blackburn, 2003; Vandermeer & Goldberg, 2013). Here, we investigate through SDM which climatic and land cover variables are the most important predictors of the distribution of 68 West-Palaearctic bumblebee species. Our results indicate that (a) several environmental variables seem to drive the probability of occurrence of species in the same direction, either negatively (e.g. for higher temperature and precipitation seasonality) or positively (e.g. for grasslands). (b) Although such directional trends can be highlighted, the different species are associated with a continuum of different climatic and land cover requirements, without any clear grouping of species based on the relative importance of each environmental variable as identified by SDM. (c) Except for one (croplands) and almost two other specific land cover variables (snow/ice and wetlands), the distribution of closely phylogenetically related taxa does not tend to be associated with similar environmental variables. (d) Species with distributions mostly predicted by land cover variables would not be, on average, more endangered than species with distributions mostly predicted by land cover variables (or the opposite). (e) The occurrence probability of localized and widespread species is mostly predicted by specific land cover characteristics and climatic conditions, respectively.

The general trend of increased occurrence probability of bumblebees in habitats such as grasslands is not surprising given their propensity to feed on a large spectrum of flowering plants present in these areas (e.g. clovers and thistles; Kleijn & Raemakers, 2008, Vray, Lecocq, Roberts, & Rasmont, 2017, Wood, Gibbs, Graham, & Isaacs, 2019). However, besides such general trends, our results do not reveal any clear phylogenetically related signal underlying their specific environmental requirements. In particular, we only find a significant signal associated with the relative importance of croplands in SDM. Yet, when investigating the phylogenetic tree with tip nodes coloured according to this variable, it remains difficult to distinguish any clear trend associated with the different clades (Figure S7). One exception though is B. confusus, the species with the highest relative importance inferred for croplands (>35%); B. confusus is an isolated taxa within the tree, which could contribute to the significant phylogenetic signal identified for this variable. The association of this species with croplands could confirm the hypothesis that B. confusus historically benefitted from leguminous plants used as crop rotations for agricultural purposes in much of Europe (Folschweiller et al., 2020; Goulson et al., 2008). The loss of such an agricultural tradition, likely combined with an array of other stressors, could likely explain why the species is now threatened in most of its distribution (“vulnerable” in Europe according to the IUCN; Nieto et al., 2014) and has already disappeared from many regions of Europe where it once thrived (e.g. Rasmont et al., 2015). Finally, our results also highlight the difficulty to associate the conservation status of bumblebees with their environmental requirements. In other words, we cannot count on climatic or habitat requirement to clearly define and gather bumblebee species in more or less endangered groups, which complicates the conservation task and further calls for complementing overall conservation plans with species-specific mitigation strategies.

Among invertebrates, less than 1% of described species have been assessed for threat by the International Union for Conservation of Nature (IUCN), and ~40% of assessed ones are threatened (Dirzo et al., 2014). In this context, bumblebees constitute a relevant study case of widespread and declining insect pollinators. Substantial declining trends are identified among >45% of European bumblebees, of which nearly a quarter is threatened (Nieto et al., 2014). Various parameters underline this decline, but as in many insect groups, habitat degradation is credited as a major factor (Sánchez-Bayo & Wyckhuys, 2019). By reducing foraging and nesting opportunities, urbanization and intensified agricultural practices constitute key factors in the decline of pollinators and, in particular, in those associated with particular habitats. In this context, our results depict the important role of land cover parameters, suggesting that habitat degradation and/or fragmentation does not impact all taxa in the same way, and is likely to only moderately impact broadly distributed species compared to more localized species, which are more dependent on habitat characteristics.

The present results therefore highlight the need to develop conservation strategies at the appropriate geographic scale, differentiating local versus global action plans. At a local scale, geographically restricted species can be protected by landscape management offering an adequate vegetation structure for nesting, foraging, mating and overwintering, that is that suit the species-specific requirements in terms of land cover and nutrition (Vaudo, Tooker, Grozinger, & Patch, 2015; Wood et al., 2019). Such suitable habitats, which should typically exhibit a low to null exposure to land use stressors such as pesticides (Kenna et al., 2019), overgrazing (Xie, Williams, & Tang, 2008) and invasive species (which might only attract the most common species; Vanderplanck, Roger, et al., 2019), also need to be connected to other stepping stone habitats by ecological corridors. These ecological corridors allow a proper food foraging, gene flow and potentially population movements (Black, 2018, Forister, Pelton, & Black, 2019). Planting floral strips that provide adequate floral resources (e.g. clovers) for bumblebees could be efficient in landscapes that are dominated by intensive agriculture, although their efficiency can be context-dependent and could mostly benefit species that are already common (Wood, Holland, Hughes, & Goulson, 2015). To overcome this problem, action plans must be implemented locally based on red lists or up-to-date atlases in order to prioritize areas where target species are endangered by climatic or land use changes (Drossart et al., 2019, Folschweiller et al., 2020). A distinct example of encouraged prioritizations is those of arctic taxa such as B. hyperboreus and B. polaris, two species that show an important association with climatic variables (Figure 2) while also presenting a restricted distribution (Figure 3). Their small distribution range could however simply be a result of the physical impossibility to extend further north. Conversely, in our analysed timeline, such cold-adapted taxa could have already partly suffered from a decline in their original wider distribution. This hypothesis is supported by current data given that both species are now categorized as “vulnerable” at the continental scale (Nieto et al., 2014).

At larger scales, governments need to promote policies that strengthen pesticide regulations to address landscape contamination, for instance, by banning the cosmetic use of pest control products, or by rewarding farmers for adopting organic, diversified and ecologically intensified farming practices with price incentives and technical support (Dicks et al., 2016; Graystock et al., 2013). In this process, educating and raising awareness of the public are a key step to encourage societies to apply these strategies, for instance, by supporting the dissemination of scientific research to general audiences (Michez, Rasmont, Terzo, & Vereecken, 2019). This can be achieved with the creation of areas that constitute both a shelter for wild bees as well as hotspots of public awareness, such as nature reserves (e.g. Folschweiller et al., 2019). Public involvement can subsequentially help long-term monitoring projects that are strongly relevant for local and large-scale studies (Neuwirth, Neumayer, & Wallner, 2020; Wilson, Pan, General, & Koch, 2020). At continental scales, further effort should be done by authorities to minimize carbon use (e.g. to limit the increase of average temperature), to implement robust mitigation strategies that help protecting and restoring habitats across anthropogenically transformed pieces of land and to trend public towards purchasing food grown using environmental-friendly measures, pleasing both ecosystems and humans. In a time when approximately 40% of global land use is devoted to agriculture, global policies should be applied to rethink our approach to land use and incorporate the conservation of pollinator diversity as equally important as that of other resources (Roser & Richie, 2019; Forister et al., 2019).

In addition, our results predominantly point out the crucial importance of being careful when considering conservation strategies for a group as a whole and show the urge to start focusing on the requirements of species by themselves. Indeed, the absence of clear species clustering in terms of relative importance of land cover variables in our species distribution models suggests the complex range of mitigation strategies that such pollinator insects would require for their survival in evolving landscapes impacted by human activities. Moreover, the lack of association between IUCN status and trends and the species’ environmental requirements highlight that conservation strategies must integrate both climatic and habitat measures. Although red lists of endangered species already warn of the specific conservation statuses of organisms (e.g. Nieto et al., 2014; Settele et al., 2008), many action plans perpetuate the very limited idea of finding general strategies (“butterfly conservation” or “bumblebee conservation”). Although these ideas can constitute adequate starting points for further strategic thinking, it is now acknowledged that global changes can show very distinct impacts on living organisms within a single monophyletic group, from highly beneficial (increasing a distribution range) to highly deleterious (leading to extinction) depending on the species (Kerr et al., 2015; Marshall et al., 2018; Prŷs-Jones, 2019). In addition to global warming, the increased agricultural intensification and habitat fragmentation have been shown to be involved in species-specific phenotypic changes in bumblebee queens over the last century (Gérard, Martinet, et al., 2020). Such species-specific responses to habitat changes are also dietary, for instance, following the drastic drift of pollen resources that occurred in the second half of the 20th century (Roger et al., 2017). Conversely, responses to urbanization have also been shown to be taxon-specific, with different functional groups of pollinators dominating in different urban landscapes (Threlfall et al., 2015). Cities have, for instance, been shown to host a lower proportion of dietary specialist bees (Hernandez, Frankie, & Thorp, 2009).

In the light of these various fates, we therefore argue in favour of appropriate species-specific and geographically adapted mitigation plans for wildlife conservation. We encourage projects such as “Saving the Yellow bumblebee” (Bombus distinguendus), led by the UK’s Bumblebee Conservation Trust (www.bumblebeeconservation.org). This kind of conservation programme presents several qualities that reflect our position on adapted conservation strategies, including (a) the focus on a bumblebee species that has shown a drastic decline over the last century in Europe, (b) the adequate focus on important habitat types (e.g. machair) that host the remaining populations of the target species, (c) the participation of many volunteers who get involved in establishing the current distribution of this declining bumblebee and (d) the provision of free management advice and follow-up support to landowners and farmers, helping them to implement beneficial land management.

Very general (i.e. untargeted) action plans and landscape management are often likely to benefit only the most common species, therefore not resolving any issue about the endangered species of that group if they are not already present in the habitat (Wood et al., 2015). This major problem is currently amplified by the unregulated movements of managed pollinators (including bumblebees) within and between countries (Bartomeus, Molina, Hidalgo-Galiana, & Ortego, 2020; Dicks et al., 2016), implying an unwanted increase in abundance of species that are already ubiquitous in the wild. Representative examples of inappropriate strategies for a group instead of taxa conservation include the installation of honeybee hives in an effort to “save the bees,” or attempts to “enhance habitats” using alien plants that could end up favouring bees that are already common. Altogether, the counterproductive consequences of some very general action plans further underline the importance of targeted species-related conservation strategies. As shown in our results, monophyletic groups such as Bombus show a wide panel of natural requirements that can globally not be predicted by a phylogenetic inference.

More broadly and all across wildlife (e.g. Nelson et al., 2019; Rejmánek, 2018; Thomas, Simcox, & Clarke, 2009), the current context of global losses in species diversity must encourage the recognition of taxa as distinct entities associated with particular habitats and therefore requiring precise measures that cannot always be readily pooled with those of other taxa. In practice, trade-offs between conservation measures trying to capture a maximum of taxa with a poorer specificity and strategies specifically prioritizing fewer taxa still constitute critical debates in the field of conservation. In addition, much work combining other threats faced by biodiversity (e.g. invasive species, pesticides and parasite spillover) remains to be done to deeper our understanding of local and global patterns of population and species decline. We hope this study will provide further encouragement to explore the requirements of species and boost the development of appropriate mitigation strategies for wildlife.

AUTHORS’ CONTRIBUTIONS

G.G. and S.D. designed the study. S.D. performed the data analyses. G.G. and S.D. interpreted the results. D.M. and P.R. contributed to reagents and materials. G.G. and S.D. wrote the first draft of the manuscript. All authors discussed the results, edited and approved the content of the manuscript.

BIOSKETCH

All authors share interest in understanding the responses of wildlife to ongoing climate change and the loss of suitable habitat. In particular, the authors carry out research on the evolutionary history and conservation of wild bees.