Projected decline in European bumblebee populations in the twenty-first century.

Habitat degradation and climate change are globally acting as pivotal drivers of wildlife collapse, with mounting evidence that this erosion of biodiversity will accelerate in the following decades1-3. Here, we quantify the past, present and future ecological suitability of Europe for bumblebees, a threatened group of pollinators ranked among the highest contributors to crop production value in the northern hemisphere4-8. We demonstrate coherent declines of bumblebee populations since 1900 over most of Europe and identify future large-scale range contractions and species extirpations under all future climate and land use change scenarios. Around 38-76% of studied European bumblebee species currently classified as 'Least Concern' are projected to undergo losses of at least 30% of ecologically suitable territory by 2061-2080 compared to 2000-2014. All scenarios highlight that parts of Scandinavia will become potential refugia for European bumblebees; it is however uncertain whether these areas will remain clear of additional anthropogenic stressors not accounted for in present models. Our results underline the critical role of global change mitigation policies as effective levers to protect bumblebees from manmade transformation of the biosphere.

Global patterns in bumble bee pollen collection show phylogenetic conservation of diet.

Bumble bees (Bombus) are a group of eusocial bees with a strongly generalised feeding pattern, collecting pollen from many different botanical families. Though predominantly generalists, some bumble bee species seem to have restricted dietary choices. It is unclear whether restricted diets in bumble bees are inherent or a function of local conditions due to a lack of data for many species across different regions. The objective of this study was to determine whether bumble bee species displayed specific patterns of pollen collection, and whether patterns were influenced by phylogenetic relatedness or tongue length, a trait known to be associated with structuring floral visitation. Bumble bee pollen collection patterns were quantified from 4,132 pollen loads taken from 58 bumble bee species, representing 24% of the pollen-collecting diversity of this genus. Phylogenetic trait mapping showed a conserved pattern of dietary dissimilarity across species, but not for dietary breadth. Dietary dissimilarity was driven by collection of Fabaceae, with the most similar species collecting around 50%-60% of their diet from this botanical family. The proportion of the diet collected from Fabaceae also showed a conserved phylogenetic signal. Greater collection of Fabaceae was associated with longer tongue lengths, with shorter tongued species focusing on alternative botanical families. However, this result was largely driven by phylogenetic relatedness, not tongue length per se. These results demonstrate that, though generalists, bumble bees are still subject to dietary restrictions that constrain their foraging choices. These dietary constraints have implications for their persistence should their core resources decline in abundance.

Global effects of extreme temperatures on wild bumblebees.

Climate plays a key role in shaping population trends and determining the geographic distribution of species because of limits in species' thermal tolerance. An evaluation of species tolerance to temperature change can therefore help predict their potential spatial shifts and population trends triggered by ongoing global warming. We assessed inter- and intraspecific variations in heat resistance in relation to body mass, local mean temperatures, and evolutionary relationships in 39 bumblebee species, a major group of pollinators in temperate and cold ecosystems, across 3 continents, 6 biomes, and 20 regions (2386 male specimens). Based on experimental bioassays, we measured the time before heat stupor of bumblebee males at a heatwave temperature of 40 °C. Interspecific variability was significant, in contrast to interpopulational variability, which was consistent with heat resistance being a species-specific trait. Moreover, cold-adapted species are much more sensitive to heat stress than temperate and Mediterranean species. Relative to their sensitivity to extreme temperatures, our results help explain recent population declines and range shifts in bumblebees following climate change.

Efectos Globales de las Temperaturas Extremas sobre Abejorros Silvestres Resumen El clima juega un papel importante en la configuración de las tendencias poblacionales y en la determinación de la distribución geográfica de las especies debido a los límites de la tolerancia térmica y al agua que tiene cada especie. Por lo tanto, una evaluación de la tolerancia de las especies al cambio térmico puede ayudar a predecir los potenciales cambios espaciales y las tendencias poblacionales detonadas por el calentamiento global en curso. Evaluamos las variaciones inter- e intraespecíficas de la resistencia al calor en relación con la masa corporal, temperaturas locales promedio y las relaciones evolutivas para 39 especies de abejorros, un grupo primordial de polinizadores en ecosistemas templados y fríos, en tres continentes, seis biomas y 20 regiones (2,386 especímenes machos). Con base en bioanálisis experimentales, medimos el tiempo previo al letargo por calor de los abejorros machos a temperaturas de 40 °C, típicas de una ola de calor. La variabilidad interespecífica fue significativa, en contraste con la variabilidad interpoblacional, lo cual fue consistente con el hecho de que la resistencia al calor sea una característica específica de la especie. Además, las especies adaptadas al frío son mucho más sensibles al estrés por calor que las especies de clima templado o Mediterráneo. En relación con la sensibilidad a las temperaturas extremas, nuestros resultados ayudan a explicar las recientes declinaciones poblacionales y cambios en la distribución de los abejorros posteriores al cambio climático.

Shift in size of bumblebee queens over the last century.

Species can respond differently when facing environmental changes, such as by shifting their geographical ranges or through plastic or adaptive modifications to new environmental conditions. Phenotypic modifications related to environmental factors have been mainly explored along latitudinal gradients, but they are relatively understudied through time despite their importance for key ecological interactions. Here we hypothesize that the average bumblebee queen body size has changed in Belgium during the last century. Based on historical and contemporary databases, we first tested if queen body sizes changed during the last century at the intraspecific level among four common bumblebee species and if it could be linked to global warming and/or habitat fragmentation as well as by the replacement by individuals from new populations. Then, we assessed body size changes at the community level, among 22 species, taking into account species population trends (i.e. increasing, stable or decreasing relative abundance). Our results show that the average queen body size of all four bumblebee species increased over the last century. This size increase was significantly correlated to global warming and habitat fragmentation, but not explained by changes in the population genetic structure (i.e. colonization). At the community level, species with stable or increasing relative abundance tend to be larger than declining species. Contrary to theoretical expectations from Bergmann's rule (i.e. increasing body size in colder climates), temperature does not seem to be the main driver of bumblebee body size during the last century as we observed the opposite body size trend. However, agricultural intensification and habitat fragmentation could be alternative mechanisms that shape body size clines. This study stresses the importance of considering alternative global change factors when assessing body size change.

Long-term effects of global change on occupancy and flight period of wild bees in Belgium.

Global change affects species by modifying their abundance, spatial distribution, and activity period. The challenge is now to identify the respective drivers of those responses and to understand how those responses combine to affect species assemblages and ecosystem functioning. Here we correlate changes in occupancy and mean flight date of 205 wild bee species in Belgium with temporal changes in temperature trend and interannual variation, agricultural intensification, and urbanization. Over the last 70 years, bee occupancy decreased on average by 33%, most likely because of agricultural intensification, and flight period of bees advanced on average by 4 days, most likely because of interannual temperature changes. Those responses resulted in a synergistic effect because species which increased in occupancy tend to be those that have shifted their phenologies earlier in the season. This leads to an overall advancement and shortening of the pollination season by 9 and 15 days respectively, with lower species richness and abundance compared to historical pollinator assemblages, except at the early start of the season. Our results thus suggest a strong decline in pollination function and services.

The interplay of climate and land use change affects the distribution of EU bumblebees.

Bumblebees in Europe have been in steady decline since the 1900s. This decline is expected to continue with climate change as the main driver. However, at the local scale, land use and land cover (LULC) change strongly affects the occurrence of bumblebees. At present, LULC change is rarely included in models of future distributions of species. This study's objective is to compare the roles of dynamic LULC change and climate change on the projected distribution patterns of 48 European bumblebee species for three change scenarios until 2100 at the scales of Europe, and Belgium, Netherlands and Luxembourg (BENELUX). We compared three types of models: (1) only climate covariates, (2) climate and static LULC covariates and (3) climate and dynamic LULC covariates. The climate and LULC change scenarios used in the models include, extreme growth applied strategy (GRAS), business as might be usual and sustainable European development goals. We analysed model performance, range gain/loss and the shift in range limits for all bumblebees. Overall, model performance improved with the introduction of LULC covariates. Dynamic models projected less range loss and gain than climate-only projections, and greater range loss and gain than static models. Overall, there is considerable variation in species responses and effects were most pronounced at the BENELUX scale. The majority of species were predicted to lose considerable range, particularly under the extreme growth scenario (GRAS; overall mean: 64% ± 34). Model simulations project a number of local extinctions and considerable range loss at the BENELUX scale (overall mean: 56% ± 39). Therefore, we recommend species-specific modelling to understand how LULC and climate interact in future modelling. The efficacy of dynamic LULC change should improve with higher thematic and spatial resolution. Nevertheless, current broad scale representations of change in major land use classes impact modelled future distribution patterns.

Variability in Sexual Pheromones Questions their Role in Bumblebee Pre-Mating Recognition System.

Sex-specific chemical secretions have been widely used as diagnostic characters in chemotaxonomy. The taxonomically confused group of bumblebees has reaped the benefit of this approach through the analyses of cephalic labial gland secretions (CLGS). Most of currently available CLGS descriptions concern species from the West-Palearctic region but few from the New World. Here, the CLGS of four East-Palearctic species Bombus deuteronymus, B. filchnerae, B. humilis, and B. exil (subgenus Thoracobombus) are analysed. Our results show high levels of variability in the major compounds in B. exil. In contrast, we describe a low differentiation in CLGS compounds between B. filchnerae and its phylogenetically closely related taxon B. muscorum. Moreover, the chemical profiles of B. filchnerae and B. muscorum are characterized by low concentrations of the C16 component, which is found in higher concentrations in the other Thoracobombus species. This raises the possibility that courtship behavior as well as environmental constraints could affect the role of the bumblebee males' CLGS.

Impact of pollen resources drift on common bumblebees in NW Europe.

Several bee species are experiencing significant population declines. As bees exclusively rely on pollen for development and survival, such declines could be partly related to changes in their host plant abundance and quality. Here, we investigate whether generalist bumblebee species, with stable population trends over the past years, adapted their diets in response to changes in the distribution and chemical quality of their pollen resources. We selected five common species of bumblebee in NW Europe for which we had a precise description of their pollen diet through two time periods ('prior to 1950' and '2004-2005'). For each species, we assessed whether the shift in their pollen diet was related with the changes in the suitable area of their pollen resources. Concurrently, we evaluated whether the chemical composition of pollen resources changed over time and experimentally tested the impact of new major pollen species on the development of B. terrestris microcolonies. Only one species (i.e. B. lapidarius) significantly included more pollen from resources whose suitable area expanded. This opportunist pattern could partly explain the expansion of B. lapidarius in Europe. Regarding the temporal variation in the chemical composition of the pollen diet, total and essential amino acid contents did not differ significantly between the two time periods while we found significant differences among plant species. This result is driven by the great diversity of resources used by bumblebee species in both periods. Our bioassay revealed that the shift to new major pollen resources allowed microcolonies to develop, bringing new evidence on the opportunist feature of bumblebee in their diets. Overall, this study shows that the response to pollen resource drift varies among closely related pollinators, and a species-rich plant community ensures generalist species to select a nutrient-rich pollen diet.

Growth Rate of Bumblebee Larvae is Related to Pollen Amino Acids.

The use of Bombus terrestris L. commercial colonies for outdoor and greenhouse crop pollination is currently widespread. Colony breeding includes bumblebee feeding, mostly by using the honeybee pollen loads of diverse palynological composition. Because the chemical content of pollen is highly variable, the choice of commercial blend should not be random but has to be carefully selected to ensure the optimal development of workers and then pollination efficacy. In this work, we compared the impact of three common commercial blends on the development of bumblebee microcolonies, namely, Actinidia deliciosa L., Cistus sp., and Salix sp. We focus on amino acids (i.e., composition and amount), as they are currently used as an indicator of diet performance. Five parameters were used to determine microcolonies growth rate: 1) number of eggs, 2) number of alive larvae, 3) number of ejected larvae, 4) number of pupae, and 5) total number of offspring. Syrup collection was also monitored to estimate energetic requirement for colony growth. Results revealed that the three commercial blends chemically differed in their amino acid contents, with those displaying higher concentrations (i.e., Salix sp. and A. deliciosa) accelerating microcolony development along with an increase of syrup collection. The advantages of rearing bumblebee commercial colonies using a pollen diet with an optimal amino acid content are discussed.

First Chemical Analysis and Characterization of the Male Species-Specific Cephalic Labial-Gland Secretions of South American Bumblebees.

The evolution of signals and reproductive traits involved in the pre-mating recognition has been in focus of abundant research in several model species, such as bumblebees (genus Bombus). However, the most-studied bumblebee reproductive trait, the male cephalic labial gland secretions (CLGS), remains unknown among bumblebee species from South America. In this study, the CLGS of five South American bumblebees of the subgenera Thoracobombus (Bombus excellens and B. atratus) and Cullumanobombus (B. rubicundus, B. hortulanus, and B. melaleucus) were investigated, by comparing the chemical compositions of their secretions to those of closely related European species. The results showed an obvious interspecific differentiation in both subgenera. The interspecific differentiation among the species of the Thoracobombus subgenus involved different compounds present at high contents (main compounds), while those of the Cullumanobombus subgenus shared the same main components. This suggests that among the species of the Cullumanobombus subgenus, the differentiation in minor components could lead to species discrimination.

Scent of a break-up: phylogeography and reproductive trait divergences in the red-tailed bumblebee (Bombus lapidarius).

BACKGROUND: The Pleistocene climatic oscillations are considered as a major driving force of intraspecific divergence and speciation. During Ice Ages, populations isolated in allopatric glacial refugia can experience differentiation in reproductive traits through divergence in selection regimes. This phenomenon may lead to reproductive isolation and dramatically accentuates the consequences of the climatic oscillations on species. Alternatively, when reproductive isolation is incomplete and populations are expanding again, further mating between the formerly isolated populations can result in the formation of a hybrid zone, genetic introgression or reinforcement speciation through reproductive trait displacements. Therefore changes in reproductive traits driven by population movements during climatic oscillations can act as an important force in promoting pre-zygotic isolation. Notwithstanding, divergence of reproductive traits has not been approached in the context of climatic oscillations. Here we investigate the impact of population movements driven by climatic oscillations on a reproductive trait of a bumblebee species (Bombus lapidarius). We characterise the pattern of variation and differentiation across the species distribution (i) with five genes (nuclear and mitochondrial), and (ii) in the chemical composition of male marking secretions (MMS), a key trait for mate attraction in bumblebees. RESULTS: Our results provide evidence that populations have experienced a genetic allopatric differentiation, in at least three main refugia (the Balkans, Centre-Eastern Europe, and Southern Italy) during Quaternary glaciations. The comparative chemical analyses show that populations from the Southern Italian refugium have experienced MMS differentiation and an incipient speciation process from another refugium. The meeting of Southern Italian populations with other populations as a result of range expansion at a secondary contact zone seems to have led to a reinforcement process on local MMS patterns. CONCLUSIONS: This study suggests that population movement during Quaternary climatic oscillations can lead to divergence in reproductive traits by allopatric differentiation during Ice Ages and by reinforcement during post-glacial recolonization.

Species richness declines and biotic homogenisation have slowed down for NW-European pollinators and plants.

Concern about biodiversity loss has led to increased public investment in conservation. Whereas there is a widespread perception that such initiatives have been unsuccessful, there are few quantitative tests of this perception. Here, we evaluate whether rates of biodiversity change have altered in recent decades in three European countries (Great Britain, Netherlands and Belgium) for plants and flower visiting insects. We compared four 20-year periods, comparing periods of rapid land-use intensification and natural habitat loss (1930-1990) with a period of increased conservation investment (post-1990). We found that extensive species richness loss and biotic homogenisation occurred before 1990, whereas these negative trends became substantially less accentuated during recent decades, being partially reversed for certain taxa (e.g. bees in Great Britain and Netherlands). These results highlight the potential to maintain or even restore current species assemblages (which despite past extinctions are still of great conservation value), at least in regions where large-scale land-use intensification and natural habitat loss has ceased.

The new annotated checklist of the wild bees of Europe (Hymenoptera: Anthophila).

At a time when nature conservation has become essential to ensure the long-term sustainability of our environment, it is widely acknowledged that conservation actions must be implemented within a solid taxonomic framework. In preparation for the upcoming update of the IUCN Red List, we here update the European checklist of the wild bees (sensu the IUCN geographical framework). The original checklist, published in 2014, was revised for the first time in 2017. In the present revision, we add one genus, four subgenera and 67 species recently described, 40 species newly recorded since the latest revision (including two species that are not native to Europe), 26 species overlooked in the previous European checklists and 63 published synonymies. We provide original records for eight species previously unknown to the continent and, as original taxonomic acts, we provide three new synonyms, we consider two names as nomina nuda, ten names as nomina dubia, three as species inquirenda, synonymize three species and exclude 40 species from the previous checklist. Around a hundred other taxonomic changes and clarifications are also included and discussed. The present work revises the total number of genera for IUCN Europe to 77 and the total number of species to 2,138. In addition to specifying the taxonomic changes necessary to update the forthcoming Red List of European bees, we discuss the sampling and taxonomic biases that characterise research on the European bee fauna and highlight the growing importance of range expansions and species invasions.

Farming with Alternative Pollinators benefits pollinators, natural enemies, and yields, and offers transformative change to agriculture.

Low- and middle-income countries cannot afford reward-based land sparing for wildflower strips to combat pollinator decline. Two small-grant projects assessed, if an opportunity-cost saving land-sharing approach, Farming with Alternative Pollinators, can provide a method-inherent incentive to motivate farmers to protect pollinators without external rewards. The first large-scale Farming-with-Alternative-Pollinators project used seven main field crops in 233 farmer fields of four agro-ecosystems (adequate rainfall, semi-arid, mountainous and oasis) in Morocco. Here we show results: higher diversity and abundance of wild pollinators and lower pest abundance in enhanced fields than in monocultural control fields; the average net-income increase per surface is 121%. The higher income is a performance-related incentive to enhance habitats. The income increase for farmers is significant and the increase in food production is substantial. Higher productivity per surface can reduce pressure on (semi)-natural landscapes which are increasingly used for agriculture. Land-use change additionally endangers biodiversity and pollinators, whereas this new pollinator-protection approach has potential for transformative change in agriculture.

The bees of Lebanon (Hymenoptera: Apoidea: Anthophila).

The study of wild bees has markedly increased in recent years due to their importance as pollinators of crops and wild plants, and this interest has been accentuated by increasing evidence of global declines in their abundance and species richness. Though best studied in Europe and North America, knowledge on the current state of wild bees is scarce in regions where they are particularly diversified, such as the Mediterranean basin. The eastern Mediterranean country of Lebanon, located at the heart of the Levant in a biodiversity hotspot, is particularly poorly studied. The aim of this paper is to produce a first annotated checklist of the wild bees of Lebanon from new and museum collections, literature records, and verified occurrences from online databases. The present list totals 573 species for Lebanon of which 289 are reported for the first time, but the estimated diversity is likely to be closer to 700. Preliminary information on local distributions and flower records are also presented. The local species assemblages indicate affinities with montane habitats of the Mediterranean and Anatolia and the semi-arid habitats of the Levant and north Africa. This study also encourages further research on local wild bee faunas and the use of this knowledge for conservation purposes.

Contribution to the knowledge of the bumblebee fauna of Afghanistan (Hymenoptera, Apidae, Bombus Latreille).

Bumblebees (Hymenoptera: Apidae: genus Bombus Latreille, 1802) constitute an important group of pollinators for many wild plants and crops in north temperate regions and South America. Although knowledge of these insects has been increasing over the last decades, some geographic areas remain poorly studied and additions to the knowledge of their faunas are infrequent. Afghanistan is one example of a country that is currently underrepresented in the scientific literature despite its high species diversity. For this study, more than 420 new occurrence records were gathered for 17 bumblebee species belonging to all eight subgenera recorded in the country, including the first record of a species closely related to the B longipennis group. Additionally, the first standardized database for Afghan bees is launched, which we hope will be enriched in the future to allow further assessments of population trends for the bumblebees of Afghanistan. Finally, the previously published species records for the country are discussed considering the most recent taxonomic revisions of the genus and key perspectives are highlighted for further work in this understudied country and neighboring regions.

An update and revision of the Andrena fauna of Morocco (Hymenoptera, Apoidea, Andrenidae) with the description of eleven new North African species.

Morocco has a diverse bee fauna, but one that has also been relatively understudied in recent years. Here a revision of the species-rich genus Andrena is presented that reveals eleven new species for science and substantially improves our understanding of North African Andrena. From Morocco, Andrena (Aciandrena) semiadesus Wood, sp. nov., Andrena (Aciandrena) triangulivalvis Wood sp. nov., Andrena (Campylogaster) sparsipunctata Wood sp. nov., Andrena (Carandrena) hebescens Wood sp. nov., Andrena (Cnemidandrena) niveofacies Wood sp. nov., Andrena (incertae sedis) tenebricorpus Wood sp. nov., Andrena (Notandrena) acutidentis Wood sp. nov., Andrena (Poliandrena) breviceps Wood sp. nov., and Andrena (Poliandrena) farinosoides Wood sp. nov. are described and their ecology is discussed. Andrena (Aciandrena) astrella Warncke, 1975 is synonymised with Andrena (Aciandrena) fulica Warncke, 1974 syn. nov. The unknown female of Andrena (Nobandrena) ounifa Warncke, 1974, and the unknown male of Andrena (Poliandrena) guichardi Warncke, 1980 are described. Andrena (incertae sedis) gafsensis Wood sp. nov. from Tunisia is described due to its similarity to Andrena tenebricorpus. Andrena (Poecilandrena) nigriclypeus Wood sp. nov. from Algeria is also described as it was collected within 10 km of the Moroccan border. A further 18 species are recorded in Morocco for the first time. Andrena (Melandrena) nitida (Müller, 1776) and Andrena (Notandrena) nitidiuscula Schenck, 1853 are removed from the Moroccan list due to historic problems in the application of these names to Mediterranean taxa.

Loss of pollinator specialization revealed by historical opportunistic data: Insights from network-based analysis.

We are currently facing a large decline in bee populations worldwide. Who are the winners and losers? Generalist bee species, notably those able to shift their diet to new or alternative floral resources, are expected to be among the least vulnerable to environmental change. However, studies of interactions between bees and plants over large temporal and geographical scales are limited by a lack of historical records. Here, we used a unique opportunistic century-old countrywide database of bee specimens collected on plants to track changes in the plant-bee interaction network over time. In each historical period considered, and using a network-based modularity analysis, we identified some major groups of species interacting more with each other than with other species (i.e. modules). These modules were related to coherent functional groups thanks to an a posteriory trait-based analysis. We then compared over time the ecological specialization of bees in the network by computing their degree of interaction within and between modules. "True" specialist species (or peripheral species) are involved in few interactions both inside and between modules. We found a global loss of specialist species and specialist strategies. This means that bee species observed in each period tended to use more diverse floral resources from different ecological groups over time, highly specialist species tending to enter/leave the network. Considering the role and functional traits of species in the network, combined with a long-term time series, provides a new perspective for the study of species specialization.

The wild bees (Hymenoptera: Apoidea) of Morocco.

Morocco is a well known hot-spot of biodiversity in the Mediterranean basin. While some taxa like vascular plants are relatively well recorded, important groups of pollinators like bees are still understudied. This article presents an updated checklist of the bee species of Morocco and includes a summary of global and regional distribution of each species. A total of 961 species belonging to six bee families and 68 genera are recorded: Andrenidae (8 genera, 217 species); Apidae (15 genera, 241 species); Colletidae (2 genera, 74 species), Halictidae (12 genera, 144 species), Megachilidae (28 genera, 271 species) and Melittidae (3 genera, 14 species). Among them, 67 species are recorded for the first time in Morocco. Around 70% of the bee fauna of Morocco consists of widespread Palaearctic species. Only 18% of Moroccan species recorded are restricted to North Africa and 8% are Moroccan single-country endemics (81 species). Afrotropical elements in the Moroccan fauna are few, with only 3% of Morocco species co-occuring in that region. This checklist is intended to stimulate new regional research on bees including their taxonomy and biogeography. As many groups of bees have been understudied, discovery of new species for science and new records for the country can be expected. Additional research including inventorying, monitoring, and integrative taxonomic studies are needed to develop a comprehensive strategy for bee conservation in Morocco.

Sexual attraction: a review of bumblebee male pheromones.

Males of many bumblebee species exhibit a conspicuous pre-mating behavior with two distinct behavioral components: scent marking and patrol flying. The marking pheromone is produced by the cephalic part of the labial gland (CLG). As far as is known, the CLG secretion is species specific, and it usually consists of two types of compounds: (i) straight-chain aliphatic alcohols, aldehydes or esters, and (ii) acyclic mono-, sesqui- and diterpenes (alcohols or acetates). Here, we summarize data from the literature reporting chemical composition of the CLG secretions of more than 80 bumblebee species. Similarities and differences within and between subgenera are discussed in the context of biosynthetic pathways and evolution.