Experimental Ecotoxicology Procedures Interfere with Honey Bee Life History.

Apis mellifera was used as a model species for ecotoxicological testing. In the present study, we tested the effects of acetone (0.1% in feed), a solvent commonly used to dissolve pesticides, on bees exposed at different developmental stages (larval and/or adult). Moreover, we explored the potential effect of in vitro larval rearing, a commonly used technique for accurately monitoring worker exposure at the larval stage, by combining acetone exposure and treatment conditions (in vitro larval rearing vs. in vivo larval rearing). We then analyzed the life-history traits of the experimental bees using radio frequency identification technology over three sessions (May, June, and August) to assess the potential seasonal dependence of the solvent effects. Our results highlight the substantial influence of in vitro larval rearing on the life cycle of bees, with a 47.7% decrease in life span, a decrease of 0.9 days in the age at first exit, an increase of 57.3% in the loss rate at first exit, and a decrease of 40.6% in foraging tenure. We did not observe any effect of exposure to acetone at the larval stage on the capacities of bees reared in vitro. Conversely, acetone exposure at the adult stage reduced the bee life span by 21.8% to 60%, decreased the age at first exit by 1.12 to 4.34 days, and reduced the foraging tenure by 30% to 37.7%. Interestingly, we found a significant effect of season on acetone exposure, suggesting that interference with the life-history traits of honey bees is dependent on season. These findings suggest improved integration of long-term monitoring for assessing sublethal responses in bees following exposure to chemicals during both the larval and adult stages. Environ Toxicol Chem 2024;00:1-12. © 2024 The Authors. Environmental Toxicology and Chemistry published by Wiley Periodicals LLC on behalf of SETAC.

Advances and knowledge gaps on climate change impacts on honey bees and beekeeping: A systematic review.

The Western honey bee Apis mellifera is a managed species that provides diverse hive products and contributing to wild plant pollination, as well as being a critical component of crop pollination systems worldwide. High mortality rates have been reported in different continents attributed to different factors, including pesticides, pests, diseases, and lack of floral resources. Furthermore, climate change has been identified as a potential driver negatively impacting pollinators, but it is still unclear how it could affect honey bee populations. In this context, we carried out a systematic review to synthesize the effects of climate change on honey bees and beekeeping activities. A total of 90 articles were identified, providing insight into potential impacts (negative, neutral, and positive) on honey bees and beekeeping. Interest in climate change's impact on honey bees has increased in the last decade, with studies mainly focusing on honey bee individuals, using empirical and experimental approaches, and performed at short-spatial (<10 km) and temporal (<5 years) scales. Moreover, environmental analyses were mainly based on short-term data (weather) and concentrated on only a few countries. Environmental variables such as temperature, precipitation, and wind were widely studied and had generalized negative effects on different biological and ecological aspects of honey bees. Food reserves, plant-pollinator networks, mortality, gene expression, and metabolism were negatively impacted. Knowledge gaps included a lack of studies at the apiary and beekeeper level, a limited number of predictive and perception studies, poor representation of large-spatial and mid-term scales, a lack of climate analysis, and a poor understanding of the potential impacts of pests and diseases. Finally, climate change's impacts on global beekeeping are still an emergent issue. This is mainly due to their diverse effects on honey bees and the potential necessity of implementing adaptation measures to sustain this activity under complex environmental scenarios.

La abeja occidental Apis mellifera es una especie manejada que proporciona diversos productos de la colmena y servicios de polinización, los cuales son cruciales para plantas silvestres y cultivos en todo el mundo. En distintos continentes se han registrado altas tasas de mortalidad, las cuales son atribuidas a diversos factores, como el uso de pesticidas, plagas, enfermedades y falta de recursos florales. Además, el cambio climático ha sido identificado como un potencial factor que afecta negativamente a los polinizadores, pero aún no está claro cómo podría afectar a las poblaciones de abejas melíferas. En este contexto, realizamos una revisión sistemática de la literatura disponible para sintetizar los efectos del cambio climático en las abejas melíferas y las actividades apícolas. En total, se identificaron 90 artículos que proporcionaron información sobre los posibles efectos (negativos, neutros y positivos) en las abejas melíferas y la apicultura. El interés por el impacto del cambio climático en las abejas melíferas ha aumentado en la última década, con estudios centrados principalmente en individuos de abejas melíferas, utilizando enfoques empíricos y experimentales y realizados a escalas espaciales (<10 km) y temporales (<5 años) cortas. Además, los análisis ambientales fueron basaron principalmente en datos a corto plazo (meteorológicos) y se concentraron sólo en algunos países. Variables ambientales como la temperatura, las precipitaciones y el viento fueron ampliamente estudiadas y tuvieron efectos negativos generalizados sobre distintos aspectos biológicos y ecológicos de las abejas melíferas. Además, las reservas alimenticias, las interacciones planta-polinizador, la mortalidad, la expresión génica y el metabolismo se vieron afectados negativamente. Entre los vacios de conocimiento cabe mencionar la falta de estudios a nivel de colmenar y apicultor, la escasez de estudios de predicción y percepción, la escasa representación de las grandes escalas espaciales y a mediano plazo, el déficit de análisis climáticos y la escasa comprensión de los impactos potenciales de plagas y enfermedades. Por último, las repercusiones del cambio climático en la apicultura mundial siguen siendo un tema emergente, que debe estudiarse en los distintos países. Esto se debe principalmente a sus diversos efectos sobre las abejas melíferas y a la necesidad potencial de aplicar medidas de adaptación para mantener esta actividad crucial en escenarios medioambientales complejos.

The genome of the blind bee louse fly reveals deep convergences with its social host and illuminates Drosophila origins.

Social insects' nests harbor intruders known as inquilines,1 which are usually related to their hosts.2,3 However, distant non-social inquilines may also show convergences with their hosts,4,5 although the underlying genomic changes remain unclear. We analyzed the genome of the wingless and blind bee louse fly Braula coeca, an inquiline kleptoparasite of the western honey bee, Apis mellifera.6,7 Using large phylogenomic data, we confirmed recent accounts that the bee louse fly is a drosophilid8,9 and showed that it had likely evolved from a sap-breeder ancestor associated with honeydew and scale insects' wax. Unlike many parasites, the bee louse fly genome did not show significant erosion or strict reliance on an endosymbiont, likely due to a relatively recent age of inquilinism. However, we observed a horizontal transfer of a transposon and a striking parallel evolution in a set of gene families between the honey bee and the bee louse fly. Convergences included genes potentially involved in metabolism and immunity and the loss of nearly all bitter-tasting gustatory receptors, in agreement with life in a protective nest and a diet of honey, pollen, and beeswax. Vision and odorant receptor genes also exhibited rapid losses. Only genes whose orthologs in the closely related Drosophila melanogaster respond to honey bee pheromone components or floral aroma were retained, whereas the losses included orthologous receptors responsive to the anti-ovarian honey bee queen pheromones. Hence, deep genomic convergences can underlie major phenotypic transitions during the evolution of inquilinism between non-social parasites and their social hosts.

Insect-Mediated Pollination of Strawberries in an Urban Environment.

Pollination services provided by a diversity of pollinators are critical in agriculture because they enhance the yield of many crops. However, few studies have assessed pollination services in urban agricultural systems. We performed flower-visitor observations and pollination experiments on strawberries (Fragaria × ananassa) in an urban area near Paris, France, in order to assess the effects of (i) insect-mediated pollination service and (ii) potential pollination deficit on fruit set, seed set, and fruit quality (size, weight, and malformation). Flower-visitor observations revealed that the pollinator community solely comprised unmanaged pollinators, despite the presence of beehives in the surrounding landscape. Based on the pollination experiments, we found that the pollination service mediated by wild insects improved the fruit size as a qualitative value of production, but not the fruit set. We also found no evidence of pollination deficit in our urban environment. These results suggest that the local community of wild urban pollinators is able to support strawberry crop production and thus plays an important role in providing high-quality, local, and sustainable crops in urban areas.

Economic costs of the invasive Yellow-legged hornet on honey bees.

Biological invasions have ecological impacts worldwide with potential massive economic costs. Among other ecosystem services such as nitrogen cycle, carbon sequestration and primary production, invasive alien species are particularly known to impact pollination. By predating honey bees (Apis mellifera), the invasive Yellow-legged hornet (Vespa velutina nigrithorax) increases the mortality risk of European bee colonies; however, little is known about its economic costs. We developed an analytic process combining large-scale field data, niche modelling techniques and agent-based models to spatially assess the ecological and economic impacts of the Yellow-legged hornet on honey bees and beekeeping in France. In particular, we estimated (i) the hornet-related risk of bee colony mortality, (ii) the economic cost of colony loss for beekeepers and (iii) the economic impact of livestock replacement compared to honey revenues at regional and national scales. We estimated an overall density of 1.08 hornet nest/km2 in France, based on the field record of 1260 nests over a searched area of 28,348 km2. However, this predator density was heterogeneously spread out across the country as well as the distribution of managed honey bee colonies. Overall, this hornet-related risk of bee colony mortality could reach up to 29.2 % of the beekeepers' livestock at national scale each year in high predation scenario. This national cost could reach as much as € 30.8 million per year due to colony loss, which represents for beekeepers an economic impact of livestock replacement of 26.6 % of honey revenues. Our results suggest non-negligible ecological and economic impacts of the invasive Yellow-legged hornet on honey bees and beekeeping activities. Moreover, this study meets the urgent need for more numerous and accurate economic estimations, necessary to calculate the impact of biological invasions on biodiversity and human goods, with a view to enhance policies of biodiversity conservation.

Density of predating Asian hornets at hives disturbs the 3D flight performance of honey bees and decreases predation success.

Automated 3D image-based tracking systems are new and promising devices to investigate the foraging behavior of flying animals with great accuracy and precision. 3D analyses can provide accurate assessments of flight performance in regard to speed, curvature, and hovering. However, there have been few applications of this technology in ecology, particularly for insects. We used this technology to analyze the behavioral interactions between the Western honey bee Apis mellifera and its invasive predator the Asian hornet, Vespa velutina nigrithorax. We investigated whether predation success could be affected by flight speed, flight curvature, and hovering of the Asian hornet and honey bees in front of one beehive. We recorded a total of 603,259 flight trajectories and 5175 predator-prey flight interactions leading to 126 successful predation events, representing 2.4% predation success. Flight speeds of hornets in front of hive entrances were much lower than that of their bee prey; in contrast to hovering capacity, while curvature range overlapped between the two species. There were large differences in speed, curvature, and hovering between the exit and entrance flights of honey bees. Interestingly, we found hornet density affected flight performance of both honey bees and hornets. Higher hornet density led to a decrease in the speed of honey bees leaving the hive, and an increase in the speed of honey bees entering the hive, together with more curved flight trajectories. These effects suggest some predator avoidance behavior by the bees. Higher honey bee flight curvature resulted in lower hornet predation success. Results showed an increase in predation success when hornet number increased up to 8 individuals, above which predation success decreased, likely due to competition among predators. Although based on a single colony, this study reveals interesting outcomes derived from the use of automated 3D tracking to derive accurate measures of individual behavior and behavioral interactions among flying species.

Bee and non-bee pollinator importance for local food security.

Pollinators are critical for food security; however, their contribution to the pollination of locally important crops is still unclear, especially for non-bee pollinators. We reviewed the diversity, conservation status, and role of bee and non-bee pollinators in 83 different crops described either as important for the global food market or of local importance. Bees are the most commonly recorded crop floral visitors. However, non-bee pollinators are frequently recorded visitors to crops of local importance. Non-bee pollinators in tropical ecosystems include nocturnal insects, bats, and birds. Importantly, nocturnal pollinators are neglected in current diurnal-oriented research and are experiencing declines. The integration of non-bee pollinators into scientific studies and conservation agenda is urgently required for more sustainable agriculture and safeguarding food security for both globally and locally important crops.

Contrasting patterns of richness, abundance, and turnover in mountain bumble bees and their floral hosts.

Environmental gradients generate and maintain biodiversity on Earth. Mountain slopes are among the most pronounced terrestrial environmental gradients, and the elevational structure of species and their interactions can provide unique insight into the processes that govern community assembly and function in mountain ecosystems. We recorded bumble bee-flower interactions over 3 years along a 1400-m elevational gradient in the German Alps. Using nonlinear modeling techniques, we analyzed elevational patterns at the levels of abundance, species richness, species ß-diversity, and interaction ß-diversity. Though floral richness exhibited a midelevation peak, bumble bee richness increased with elevation before leveling off at the highest sites, demonstrating the exceptional adaptation of these bees to cold temperatures and short growing seasons. In terms of abundance, though, bumble bees exhibited divergent species-level responses to elevation, with a clear separation between species preferring low versus high elevations. Overall interaction ß-diversity was mainly caused by strong turnover in the floral community, which exhibited a well-defined threshold of ß-diversity rate at the tree line ecotone. Interaction ß-diversity increased sharply at the upper extreme of the elevation gradient (1800-2000 m), an interval over which we also saw steep decline in floral richness and abundance. Turnover of bumble bees along the elevation gradient was modest, with the highest rate of ß-diversity occurring over the interval from low- to mid-elevation sites. The contrast between the relative robustness bumble bee communities and sensitivity of plant communities to the elevational gradient in our study suggests that the strongest effects of climate change on mountain bumble bees may be indirect effects mediated by the responses of their floral hosts, though bumble bee species that specialize in high-elevation habitats may also experience significant direct effects of warming.

Towards integrated pest and pollinator management in tropical crops.

Biotic pollination and pest control are two critical insect-mediated ecosystem services that support crop production. Although management of both services is usually treated separately, the new paradigm of Integrated Pest and Pollinator Management (IPPM) suggests synergetic benefits by considering them together. We reviewed the management practices in two major tropical perennial crops: cocoa and coffee, to assess IPPM applications under the tropics. We found potential synergies and antagonisms among crop pest and pollination management, however, very few studies considered these interactions. Interestingly, we also found management practices focusing mainly on a single service mediated by insects although species can show multiple ecological functions as pests, natural enemies, or pollinators. The tropics represent a promising area for the implementation of IPPM and future research should address this concept to move towards a more sustainable agriculture.

Delayed effects of a single dose of a neurotoxic pesticide (sulfoxaflor) on honeybee foraging activity.

Pesticide risk-assessment guidelines for honeybees (Apis mellifera) generally require determining the acute toxicity of a chemical over the short-term through fix-duration tests. However, potential long-lasting or delayed effects resulting from an acute exposure (e.g. a single dose) are often overlooked, although the modification of a developmental process may have life-long consequences. To investigate this question, we exposed young honeybee workers to a single sublethal field-realistic dose of a neurotoxic pesticide, sulfoxaflor, at one of two amounts (16 or 60 ng), at the moment when they initiated orientation flights (preceding foraging activity). We then tracked in the field their flight activity and lifespan with automated life-long monitoring devices. Both amounts of sulfoxaflor administered reduced the total number of flights but did not affect bee survival and flight duration. When looking at the time series of flight activity, effects were not immediate but delayed until foraging activity with a decrease in the daily number of foraging flights and consequently in their total number (24 and 33% less for the 16 and 60 ng doses, respectively). The results of our study therefore blur the general assumption in honeybee toxicology that acute exposure results in immediate and rapid effects and call for long-term recording and/or time-to-effect measurements, even upon exposure to a single dose of pesticide.

Effects of temperature and photoperiod on the seasonal timing of Western honey bee colonies and an early spring flowering plant.

Temperature and photoperiod are important Zeitgebers for plants and pollinators to synchronize growth and reproduction with suitable environmental conditions and their mutualistic interaction partners. Global warming can disturb this temporal synchronization since interacting species may respond differently to new combinations of photoperiod and temperature under future climates, but experimental studies on the potential phenological responses of plants and pollinators are lacking. We simulated current and future combinations of temperature and photoperiod to assess effects on the overwintering and spring phenology of an early flowering plant species (Crocus sieberi) and the Western honey bee (Apis mellifera). We could show that increased mean temperatures in winter and early spring advanced the flowering phenology of C. sieberi and intensified brood rearing activity of A. mellifera but did not advance their brood rearing activity. Flowering phenology of C. sieberi also relied on photoperiod, while brood rearing activity of A. mellifera did not. The results confirm that increases in temperature can induce changes in phenological responses and suggest that photoperiod can also play a critical role in these responses, with currently unknown consequences for real-world ecosystems in a warming climate.

Grassland-to-crop conversion in agricultural landscapes has lasting impact on the trait diversity of bees.

CONTEXT: Global pollinator decline has motivated much research to understand the underlying mechanisms. Among the multiple pressures threatening pollinators, habitat loss has been suggested as a key-contributing factor. While habitat destruction is often associated with immediate negative impacts, pollinators can also exhibit delayed responses over time. OBJECTIVES: We used a trait-based approach to investigate how past and current land use at both local and landscape levels impact plant and wild bee communities in grasslands through a functional lens. METHODS: We measured flower and bee morphological traits that mediate plant-bee trophic linkage in 66 grasslands. Using an extensive database of 20 years of land-use records, we tested the legacy effects of the landscape-level conversion of grassland to crop on flower and bee trait diversity. RESULTS: Land-use history was a strong driver of flower and bee trait diversity in grasslands. Particularly, bee trait diversity was lower in landscapes where much of the land was converted from grassland to crop long ago. Bee trait diversity was also strongly driven by plant trait diversity computed with flower traits. However, this relationship was not observed in landscapes with a long history of grassland-to-crop conversion. The effects of land-use history on bee communities were as strong as those of current land use, such as grassland or mass-flowering crop cover in the landscape. CONCLUSIONS: Habitat loss that occurred long ago in agricultural landscapes alters the relationship between plants and bees over time. The retention of permanent grassland sanctuaries within intensive agricultural landscapes can offset bee decline.

Measuring ontogenetic shifts in central-place foragers: A case study with honeybees.

Measuring time-activity budgets over the complete individual life span is now possible for many animals with the recent advances of life-long individual monitoring devices. Although analyses of changes in the patterns of time-activity budgets have revealed ontogenetic shifts in birds or mammals, no such technique has been applied to date on insects. We tested an automated breakpoint-based procedure to detect, assess and quantify shifts in the temporal pattern of the flight activities in honeybees. We assumed that the learning and foraging stages of honeybees will differ in several respects, to detect the age at onset of foraging (AOF). Using an extensive dataset covering the life-long monitoring of 1,167 individuals, we compared the AOF outputs with the more conventional approaches based on arbitrary thresholds. We further evaluated the robustness of the different methods comparing the foraging time-activity budget allocations between the presumed foragers and confirmed foragers. We revealed a clear-cut learning-foraging ontogenetic shift that differs in duration, frequency and time of occurrence of flights. Although AOF appeared to be highly plastic among bees, the breakpoint-based procedure seems better capable to detect it than arbitrary threshold-based methods that are unable to deal with inter-individual variation. We developed the aof r-package including a broad range of examples with both simulated and empirical datasets to illustrate the simplicity of use of the procedure. This simple procedure is generic enough to be derived from any individual life-long monitoring devices recording the time-activity budgets, and could propose new ecological applications of bio-logging to detect ontogenetic shifts in the behaviour of central-place foragers.

Science communication is needed to inform risk perception and action of stakeholders.

Stakeholders are critical environmental managers in human-dominated landscapes. In some contexts, stakeholders can be forced to personally act following their own observations and risk perception instead of science recommendation. In particular, biological invasions need rapid control actions to reduce potential socio-ecological impacts, while science-based risk assessments are rather complex and time-delayed. Although they can lead to important detrimental effects on biodiversity, potential time-delayed disconnections between stakeholders' action and science recommendations are rarely studied. Using the case study of western European beekeepers controlling the invasive Asian hornet Vespa velutina nigrithorax for its suspected impact on honey bee colonies, we analysed mechanisms underlying personal actions of stakeholders and how they evolved in science disconnection. Personal actions of stakeholders were causal-effect linked with their risk observation but disconnected to time-delayed science predictions and recommendations. Unfortunately, these science-disconnected actions also led to dramatic impacts on numerous species of the local entomofauna. These results highlight the need to improve mutual risk communication between science and action in the early-stages of management plans to improve the sustainably of stakeholders' practices.

Honeybee lifespan: the critical role of pre-foraging stage.

Assessing the various anthropogenic pressures imposed on honeybees requires characterizing the patterns and drivers of natural mortality. Using automated lifelong individual monitoring devices, we monitored worker bees in different geographical, seasonal and colony contexts creating a broad range of hive conditions. We measured their life-history traits and notably assessed whether lifespan is influenced by pre-foraging flight experience. Our results show that the age at the first flight and onset of foraging are critical factors that determine, to a large extent, lifespan. Most importantly, our results indicate that a large proportion (40%) of the bees die during pre-foraging stage, and for those surviving, the elapsed time and flight experience between the first flight and the onset of foraging is of paramount importance to maximize the number of days spent foraging. Once in the foraging stage, individuals experience a constant mortality risk of 9% and 36% per hour of foraging and per foraging day, respectively. In conclusion, the pre-foraging stage during which bees perform orientation flights is a critical driver of bee lifespan. We believe these data on the natural mortality risks in honeybee workers will help assess the impact of anthropogenic pressures on bees.

Limitation of complementary resources affects colony growth, foraging behavior, and reproduction in bumble bees.

Resource availability in agricultural landscapes has been disturbed for many organisms, including pollinator species. Abundance and diversity in flower availability benefit bee populations; however, little is known about which of protein or carbohydrate resources may limit their growth and reproductive performance. Here, we test the hypothesis of complementary resource limitation using a supplemental feeding approach. We applied this assumption with bumble bees (Bombus terrestris), assuming that colony growth and reproductive performance should depend on the continuous supply of carbohydrates and proteins, through the foraging for nectar and pollen, respectively. We placed wild-caught bumble bee colonies along a landscape gradient of seminatural habitats, and monitored the colonies' weight, foraging activity, and reproductive performance during the whole colony cycle. We performed supplemental feeding as an indicator of landscape resource limitation, using a factorial design consisting of the addition of sugar water (carbohydrate, supplemented or not) crossed by pollen (protein, supplemented or not). Bumble bee colony dynamics showed a clear seasonal pattern with a period of growth followed by a period of stagnation. Higher abundance of seminatural habitats resulted in reducing the proportion of pollen foragers relative to all foragers in both periods, and in improving the reproductive performance of bumble bees. Interestingly, the supplemental feeding of sugar water positively affected the colony weight during the stagnation period, and the supplemental feeding of pollen mitigated the landscape effect on pollen collection investment. Single and combined supplementation of sugar water and pollen increased the positive effect of seminatural habitats on reproductive performance. This study reveals a potential colimitation in pollen and nectar resources affecting foraging behavior and reproductive performance in bumble bees, and indicates that even in mixed agricultural landscapes with higher proportions of seminatural habitats, bumble bee populations face resource limitations. We conclude that the seasonal management of floral resources must be considered in conservation to support bumble bee populations and pollination services in farmlands.

Honeybees generalize among pollen scents from plants flowering in the same seasonal period.

When honey bees (Apis mellifera) feed on flowers, they extend their proboscis to absorb the nectar, i.e. they perform the proboscis extension response (PER). The presence of pollen and/or nectar can be associated with odors, colors or visual patterns, which allows honey bees to recognize food sources in the environment. Honey bees can associate similar, though different, stimuli with the presence of food; i.e. honey bees discriminate and generalize among stimuli. Here, we evaluated generalization among pollen scents from six different plant species. Experiments were based on the PER conditioning protocol over two phases: (1) conditioning, in which honey bees associated the scent of each pollen type with sucrose, and (2) test, in which honey bees were presented with a novel scent, to evaluate generalization. Generalization was evinced by honey bees extending their proboscis to a novel scent. The level of PER increased over the course of the conditioning phase for all pollen scents. Honey bees generalized pollen from Pyracantha coccinea and from Hypochaeris radicata These two plants have different amounts of protein and are not taxonomically related. We observed that the flowering period influences the olfactory perceptual similarity and we suggest that both pollen types may share volatile compounds that play key roles in perception. Our results highlight the importance of analyzing the implications of the generalization between pollen types of different nutritional quality. Such studies could provide valuable information for beekeepers and agricultural producers, as the generalization of a higher quality pollen can benefit hive development, and increase pollination and honey production.

The Conservation of Native Honey Bees Is Crucial.

Recent studies have emphasized the role of the western honey bee, Apis mellifera, as a managed agricultural species worldwide, but also as a potential threat to endangered wild pollinators. This has resulted in the suggestion that honey bees should be regulated in natural areas to conserve wild pollinators. We argue that this perspective fails to appreciate the multifaceted nature of honey bees as native or introduced species with either managed or wild colonies. Wild populations of A. mellifera are currently imperiled, and natural areas are critical for the conservation of local subspecies and genotypes. We propose that a differentiation between managed and wild populations is required and encourage integrated conservation planning for all endangered wild bees, including A. mellifera.

Exposure to pollen-bound pesticide mixtures induces longer-lived but less efficient honey bees.

Due to the widespread use of pesticides and their persistence in the environment, non-target organisms are chronically exposed to mixtures of toxic residues. Fungicides, herbicides and insecticides are all found at low doses in the diet of pollinators such as honey bees, but due to the lack of data on the toxicological effects of these mixtures, determining their risk is difficult to assess. We therefore developed a study combining the identification of common pollen-bound pesticide mixtures associated with poor colony development and tested their effects on bee behavior and physiology. We exposed bees to the identified pesticide mixtures during the first days of their adult life, a crucial period for physiological development. Using optic bee counters we recorded the behavior of bees throughout their lives and identified two pesticide mixtures that delay the onset of foraging and slow-down foraging activity. Furthermore, one of these mixtures hampers pollen foraging. As bee longevity is strongly influenced by the time spent foraging, bees exposed to these pesticide mixtures outlived control bees. Physiological analysis revealed that perturbations of the energetic metabolism preceded the altered behavior. In conclusion, we found that early-life exposure to low doses of pesticide mixtures can have long-term effects that translate into longer-lived but slower and less efficient bees. These surprising findings contrast with the commonly reported increase in bee mortality upon pesticide exposure, and demonstrate that exposure that may seem harmless (e.g., very low doses, pesticides not intended to kill insects) can have undesirable effects on non-target organisms.

Towards an integrated species and habitat management of crop pollination.

Pollination deficits are widespread in current agriculture, so improving management for crop pollination is critical. Here we review the two most common management approaches to enhance crop pollination, species and habitat management, by providing referenced lists of successful examples. We pinpoint that these approaches have been studied in isolation from each other, with little discussion on potential synergies and trade-offs between them. The potential costs of species management (e.g., loss of biodiversity due to biological invasion), as well as the potential benefits to managed pollinator species from habitat restoration, are rarely quantified. An integrative approach to crop pollination should be implemented, accounting for the cost and benefits (including those beyond crop production) and interactions of species and habitat management.