Large variability in response to projected climate and land-use changes among European bumblebee species.

Bumblebees (Bombus ssp.) are among the most important wild pollinators, but many species have suffered from range declines. Land-use change, agricultural intensification, and the associated loss of habitat have been identified as drivers of the observed dynamics, amplifying pressures from a changing climate. However, these drivers are still underrepresented in continental-scale species distribution modeling. Here, we project the potential distribution of 47 European bumblebee species in 2050 and 2080 from existing European-scale distribution maps, based on a set of climate and land-use futures simulated through a regional integrated assessment model and consistent with the RCP-SSP scenario framework. We compare projections including (1) dynamic climate and constant land use (CLIM); (2) constant climate and dynamic land use (LU); and (3) dynamic climate and dynamic land use (COMB) to disentangle the effects of land use and climate change on future habitat suitability, providing the first rigorous continental-scale assessment of linked climate-land-use futures for bumblebees. We find that direct climate impacts, although variable across species, dominate responses for most species, especially under high-end climate change scenarios (up to 99% range loss). Land-use impacts are highly variable across species and scenarios, ranging from severe losses (up to 75% loss) to considerable gains (up to 68% gain) of suitable habitat extent. Rare species thereby tend to be disproportionally affected by both climate and land-use change. COMB projections reveal that land use may amplify, attenuate, or offset changes to suitable habitat extent expected from climate impact depending on species and scenario. Especially in low-end climate change scenarios, land use has the potential to become a game changer in determining the direction and magnitude of range changes, indicating substantial potential for targeted conservation management.

Chernobyl-level radiation exposure damages bumblebee reproduction: a laboratory experiment.

The consequences for wildlife of living in radiologically contaminated environments are uncertain. Previous laboratory studies suggest insects are relatively radiation-resistant; however, some field studies from the Chernobyl Exclusion Zone report severe adverse effects at substantially lower radiation dose rates than expected. Here, we present the first laboratory investigation to study how environmentally relevant radiation exposure affects bumblebee life history, assessing the shape of the relationship between radiation exposure and fitness loss. Dose rates comparable to the Chernobyl Exclusion Zone (50-400 µGy h-1) impaired bumblebee reproduction and delayed colony growth but did not affect colony weight or longevity. Our best-fitting model for the effect of radiation dose rate on colony queen production had a strongly nonlinear concave relationship: exposure to only 100 µGy h-1 impaired reproduction by 30-45%, while further dose rate increases caused more modest additional reproductive impairment. Our data indicate that the practice of estimating effects of environmentally relevant low-dose rate exposure by extrapolating from high-dose rates may have considerably underestimated the effects of radiation. If our data can be generalized, they suggest insects suffer significant negative consequences at dose rates previously thought safe; we therefore advocate relevant revisions to the international framework for radiological protection of the environment.

Mainstreaming biodiversity: A review of national strategies.

Biodiversity is suffering dramatic declines across the globe, threatening the ability of ecosystems to provide the services on which humanity depends. Mainstreaming biodiversity into the plans, strategies and policies of different economic sectors is key to reversing these declines. The importance of this mainstreaming is recognized by the Convention on Biological Diversity (CBD) and its Aichi targets. Individual countries can implement the goals of the CBD through their National Biodiversity Strategies and Action Plans (NBSAPs), which aim to, inter alia, support the mainstreaming of biodiversity into the policies of key economic sectors, such as agriculture, forestry and fisheries. This paper investigates the performance of countries at incorporating biodiversity mainstreaming into their post-2010 NBSAPs. We conduct a large-scale review of 144 NBSAPs against five criteria and calculate a national-level indicator for comparing levels of mainstreaming among countries. Our results show that developing countries, particularly those in Africa, have higher scores, indicating that they have a higher awareness of the importance of biodiversity mainstreaming. Developing nations were also more likely to involve a greater range of stakeholders in the NBSAP development process, whilst developed nations were less likely to give specific details about the monetary contributions of biodiversity to their economies. Overall, our findings suggest that biodiversity mainstreaming remains a challenge across much of the world, but that progress in some areas can provide direction and momentum in the future.

Monitoring Neonicotinoid Exposure for Bees in Rural and Peri-urban Areas of the U.K. during the Transition from Pre- to Post-moratorium.

Concerns regarding the impact of neonicotinoid exposure on bee populations recently led to an EU-wide moratorium on the use of certain neonicotinoids on flowering crops. Currently, evidence regarding the impact, if any, the moratorium has had on bees' exposure is limited. We sampled pollen and nectar from bumblebee colonies in rural and peri-urban habitats in three U.K. regions: Stirlingshire, Hertfordshire, and Sussex. Colonies were sampled over three years: prior to the ban (2013), during the initial implementation when some seed-treated winter-sown oilseed rape was still grown (2014), and following the ban (2015). To compare species-level differences, in 2014 only, honeybee colonies in rural habitats were also sampled. Over half of all samples were found to be contaminated ( n = 408), with thiamethoxam being the compound detected at the highest concentrations in honeybee- (up to 2.29 ng/g in nectar in 2014, median ≤ 0.1 ng/g, n = 79) and bumblebee-collected pollen and nectar (up to 38.77 ng/g in pollen in 2013, median ≤ 0.12 ng/g, n = 76). Honeybees were exposed to higher concentrations of neonicotinoids than bumblebees in 2014. While neonicotinoid exposure for rural bumblebees declined post-ban (2015), suggesting a positive impact of the moratorium, the risk of neonicotinoid exposure for bumblebees in peri-urban habitats remained largely the same between 2013 and 2015.

The Neonicotinoid Insecticide Thiacloprid Impacts upon Bumblebee Colony Development under Field Conditions.

The impacts of pesticides, and in particular of neonicotinoids, on bee health remain much debated. Many studies describing negative effects have been criticized as the experimental protocol did not perfectly simulate real-life field scenarios. Here, we placed free-flying bumblebee colonies next to raspberry crops that were either untreated or treated with the neonicotinoid thiacloprid as part of normal farming practice. Colonies were exposed to the raspberry crops for a two week period before being relocated to either a flower-rich or flower-poor site. Overall, exposed colonies were more likely to die prematurely, and those that survived reached a lower final weight and produced 46% fewer reproductives than colonies placed at control farms. The impact was more marked at the flower-rich site (all colonies performed poorly at the flower poor site). Analysis of nectar and pollen stores from bumblebee colonies placed at the same raspberry farms revealed thiacloprid residues of up to 771 ppb in pollen and up to 561 ppb in nectar. The image of thiacloprid as a relatively benign neonicotinoid should now be questioned.

Sex allocation theory reveals a hidden cost of neonicotinoid exposure in a parasitoid wasp.

Sex allocation theory has proved to be one the most successful theories in evolutionary ecology. However, its role in more applied aspects of ecology has been limited. Here we show how sex allocation theory helps uncover an otherwise hidden cost of neonicotinoid exposure in the parasitoid wasp Nasonia vitripennis. Female N. vitripennis allocate the sex of their offspring in line with Local Mate Competition (LMC) theory. Neonicotinoids are an economically important class of insecticides, but their deployment remains controversial, with evidence linking them to the decline of beneficial species. We demonstrate for the first time to our knowledge, that neonicotinoids disrupt the crucial reproductive behaviour of facultative sex allocation at sub-lethal, field-relevant doses in N. vitripennis. The quantitative predictions we can make from LMC theory show that females exposed to neonicotinoids are less able to allocate sex optimally and that this failure imposes a significant fitness cost. Our work highlights that understanding the ecological consequences of neonicotinoid deployment requires not just measures of mortality or even fecundity reduction among non-target species, but also measures that capture broader fitness costs, in this case offspring sex allocation. Our work also highlights new avenues for exploring how females obtain information when allocating sex under LMC.

Genetic diversity, parasite prevalence and immunity in wild bumblebees.

Inbreeding and a consequent loss of genetic diversity threaten small, isolated populations. One mechanism by which genetically impoverished populations may become extinct is through decreased immunocompetence and higher susceptibility to parasites. Here, we investigate the relationship between immunity and inbreeding in bumblebees, using Hebridean island populations of Bombus muscorum. We sampled nine populations and recorded parasite prevalence and measured two aspects of immunity: the encapsulation response and levels of phenoloxidase (PO). We found that prevalence of the gut parasite Crithidia bombi was higher in populations with lower genetic diversity. Neither measure of immune activity was correlated with genetic diversity. However, levels of PO declined with age and were also negatively correlated with parasite abundance. Our results suggest that as insect populations lose heterozygosity, the impact of parasitism will increase, pushing threatened populations closer to extinction.

Impacts of inbreeding on bumblebee colony fitness under field conditions.

BACKGROUND: Inbreeding and the loss of genetic diversity are known to be significant threats to small, isolated populations. Hymenoptera represent a special case regarding the impact of inbreeding. Haplodiploidy may permit purging of deleterious recessive alleles in haploid males, meaning inbreeding depression is reduced relative to diploid species. In contrast, the impact of inbreeding may be exacerbated in Hymenopteran species that have a single-locus complementary sex determination system, due to the production of sterile or inviable diploid males. We investigated the costs of brother-sister mating in the bumblebee Bombus terrestris. We compared inbred colonies that produced diploid males and inbred colonies that did not produce diploid males with outbred colonies. Mating, hibernation and colony founding took place in the laboratory. Once colonies had produced 15 offspring they were placed in the field and left to forage under natural conditions. RESULTS: The diploid male colonies had a significantly reduced fitness compared to regular inbred and outbred colonies; they had slower growth rates in the laboratory, survived for a shorter time period under field conditions and produced significantly fewer offspring overall. No differences in success were found between non-diploid male inbred colonies and outbred colonies. CONCLUSION: Our data illustrate that inbreeding exacts a considerable cost in Bombus terrestris through the production of diploid males. We suggest that diploid males may act as indicators of the genetic health of populations, and that their detection could be used as an informative tool in hymenopteran conservation. We conclude that whilst haplodiploids may suffer less inbreeding depression than diploid species, they are still highly vulnerable to population fragmentation and reduced genetic diversity due to the extreme costs imposed by the production of diploid males.

Larval exposure to the neonicotinoid imidacloprid impacts adult size in the farmland butterfly Pieris brassicae.

Populations of farmland butterflies have been suffering from substantial population declines in recent decades. These declines have been correlated with neonicotinoid usage both in Europe and North America but experimental evidence linking these correlations is lacking. The potential for non-target butterflies to be exposed to trace levels of neonicotinoids is high, due to the widespread contamination of agricultural soils and wild plants in field margins. Here we provide experimental evidence that field realistic, sub-lethal exposure to the neonicotinoid imidacloprid negatively impacts the development of the common farmland butterfly Pieris brassicae. Cabbage plants were watered with either 0, 1, 10, 100 or 200 parts per billion imidacloprid, to represent field margin plants growing in contaminated agricultural soils and these were fed to P. brassicae larvae. The approximate digestibility (AD) of the cabbage as well as behavioural responses by the larvae to simulated predator attacks were measured but neither were affected by neonicotinoid treatment. However, the duration of pupation and the size of the adult butterflies were both significantly reduced in the exposed butterflies compared to the controls, suggesting that adult fitness is compromised through exposure to this neonicotinoid.

Niche partitioning in a sympatric cryptic species complex.

Competition theory states that multiple species should not be able to occupy the same niche indefinitely. Morphologically, similar species are expected to be ecologically alike and exhibit little niche differentiation, which makes it difficult to explain the co-occurrence of cryptic species. Here, we investigated interspecific niche differentiation within a complex of cryptic bumblebee species that co-occur extensively in the United Kingdom. We compared the interspecific variation along different niche dimensions, to determine how they partition a niche to avoid competitive exclusion. We studied the species B. cryptarum, B. lucorum, and B. magnus at a single location in the northwest of Scotland throughout the flight season. Using mitochondrial DNA for species identification, we investigated differences in phenology, response to weather variables and forage use. We also estimated niche region and niche overlap between different castes of the three species. Our results show varying levels of niche partitioning between the bumblebee species along three niche dimensions. The species had contrasting phenologies: The phenology of B. magnus was delayed relative to the other two species, while B. cryptarum had a relatively extended phenology, with workers and males more common than B. lucorum early and late in the season. We found divergent thermal specialisation: In contrast to B. cryptarum and B. magnus, B. lucorum worker activity was skewed toward warmer, sunnier conditions, leading to interspecific temporal variation. Furthermore, the three species differentially exploited the available forage plants: In particular, unlike the other two species, B. magnus fed predominantly on species of heather. The results suggest that ecological divergence in different niche dimensions and spatio-temporal heterogeneity in the environment may contribute to the persistence of cryptic species in sympatry. Furthermore, our study suggests that cryptic species provide distinct and unique ecosystem services, demonstrating that morphological similarity does not necessarily equate to ecological equivalence.

Floral Sonication is an Innate Behaviour in Bumblebees that can be Fine-Tuned with Experience in Manipulating Flowers.

Bumblebees demonstrate an extensive capacity for learning complex motor skills to maximise exploitation of floral rewards. This ability is well studied in nectar collection but its role in pollen foraging is less well understood. Floral sonication is used by bees to extract pollen from some plant species with anthers which must be vibrated (buzzed) to release pollen. Pollen removal is determined by sonication characteristics including frequency and amplitude, and thus the ability to optimise sonication should allow bees to maximise the pollen collection. We investigated the ability of the buff-tailed bumblebee (Bombus terrestris) to modify the frequency and amplitude of their buzzes with increasing experience manipulating flowers of the buzz-pollinated plant Solanum rostratum. We analysed flight and feeding vibrations generated by naïve workers across feeding bouts. Feeding buzzes were of a higher frequency and a lower amplitude than flight buzzes. Both flight and feeding buzzes had reduced amplitudes with increasing number of foraging trips. However, the frequency of their feeding buzzes was reduced significantly more than their flight buzzes as bumblebee workers gained experience manipulating flowers. These results suggest that bumblebees are able to modify the characteristics of their buzzes with experience manipulating buzz-pollinated flowers. We discuss our findings in the context of bumblebee learning, and the current understanding of the optimal sonication characteristics for releasing pollen in buzz-pollinated species. Our results present a tantalising insight into the potential role of learning in floral sonication, paving the way for future research in this area.

Bergmann's Body Size Rule Operates in Facultatively Endothermic Insects: Evidence from a Complex of Cryptic Bumblebee Species.

According to Bergmann's rule we expect species with larger body size to inhabit locations with a cooler climate, where they may be well adapted to conserve heat and resist starvation. This rule is generally applied to endotherms. In contrast, body size in ectothermic invertebrates has been suggested to follow the reverse ecogeographic trend: these converse Bergmann's patterns may be driven by the ecological constraints of shorter season length and lower food availability in cooler high latitude locations. Such patterns are particularly common in large insects due to their longer development times. As large and facultatively endothermic insects, bumblebees could thus be expected to follow either trend. In this investigation, we studied body size of three bumblebee species over a large spatial area and investigated whether interspecific trends in body size correspond to differences in their distribution consistent with either Bergmann's or a converse Bergmann's rule. We examined the body size of queens, males and workers of the Bombus lucorum complex of cryptic bumblebee species from across the whole of Great Britain. We found interspecific differences in body size corresponding to Bergmann's rule: queens and males of the more northerly distributed, cool-adapted, species were largest. In contrast, the mean body size of the worker caste did not vary between the three species. These differences in body size may have evolved under selection pressures for thermoregulation or starvation resistance. We suggest that this case study in facultatively endothermic insects may help clarify the selection pressures governing Bergmann rule trends more generally.

Neonicotinoid pesticide reduces bumble bee colony growth and queen production.

Growing evidence for declines in bee populations has caused great concern because of the valuable ecosystem services they provide. Neonicotinoid insecticides have been implicated in these declines because they occur at trace levels in the nectar and pollen of crop plants. We exposed colonies of the bumble bee Bombus terrestris in the laboratory to field-realistic levels of the neonicotinoid imidacloprid, then allowed them to develop naturally under field conditions. Treated colonies had a significantly reduced growth rate and suffered an 85% reduction in production of new queens compared with control colonies. Given the scale of use of neonicotinoids, we suggest that they may be having a considerable negative impact on wild bumble bee populations across the developed world.