Predicting bee community responses to land-use changes: Effects of geographic and taxonomic biases.

Land-use change and intensification threaten bee populations worldwide, imperilling pollination services. Global models are needed to better characterise, project, and mitigate bees' responses to these human impacts. The available data are, however, geographically and taxonomically unrepresentative; most data are from North America and Western Europe, overrepresenting bumblebees and raising concerns that model results may not be generalizable to other regions and taxa. To assess whether the geographic and taxonomic biases of data could undermine effectiveness of models for conservation policy, we have collated from the published literature a global dataset of bee diversity at sites facing land-use change and intensification, and assess whether bee responses to these pressures vary across 11 regions (Western, Northern, Eastern and Southern Europe; North, Central and South America; Australia and New Zealand; South East Asia; Middle and Southern Africa) and between bumblebees and other bees. Our analyses highlight strong regionally-based responses of total abundance, species richness and Simpson's diversity to land use, caused by variation in the sensitivity of species and potentially in the nature of threats. These results suggest that global extrapolation of models based on geographically and taxonomically restricted data may underestimate the true uncertainty, increasing the risk of ecological surprises.

Mapping species distributions: a comparison of skilled naturalist and lay citizen science recording.

To assess the ability of traditional biological recording schemes and lay citizen science approaches to gather data on species distributions and changes therein, we examined bumblebee records from the UK's national repository (National Biodiversity Network) and from BeeWatch. The two recording approaches revealed similar relative abundances of bumblebee species but different geographical distributions. For the widespread common carder (Bombus pascuorum), traditional recording scheme data were patchy, both spatially and temporally, reflecting active record centre rather than species distribution. Lay citizen science records displayed more extensive geographic coverage, reflecting human population density, thus offering better opportunities to account for recording effort. For the rapidly spreading tree bumblebee (Bombus hypnorum), both recording approaches revealed similar distributions due to a dedicated mapping project which overcame the patchy nature of naturalist records. We recommend, where possible, complementing skilled naturalist recording with lay citizen science programmes to obtain a nation-wide capability, and stress the need for timely uploading of data to the national repository.

Emerging dangers: deadly effects of an emergent parasite in a new pollinator host.

There is growing concern about the threats facing many pollinator populations. Emergent diseases are one of the major threats to biodiversity and a microsporidian parasite, Nosema ceranae, has recently jumped host from the Asian to the Western honeybee, spreading rapidly worldwide, and contributing to dramatic colony losses. Bumblebees are ecologically and economically important pollinators of conservation concern, which are likely exposed to N. ceranae by sharing flowers with honeybees. Whilst a further intergeneric jump by N. ceranae to infect bumblebees would be potentially serious, its capacity to do this is unknown. Here we investigate the prevalence of N. ceranae in wild bumblebees in the UK and determine the infectivity of the parasite under controlled conditions. We found N. ceranae in all seven wild bumblebee species sampled, and at multiple sites, with many of the bees having spores from this parasite in their guts. When we fed N. ceranae spores to bumblebees under controlled conditions, we confirmed that the parasite can infect bumblebees. Infections spread from the midgut to other tissues, reduced bumblebee survival by 48% and had sub-lethal effects on behaviour. Although spore production appeared lower in bumblebees than in honeybees, virulence was greater. The parasite N. ceranae therefore represents a real and emerging threat to bumblebees, with the potential to have devastating consequences for their already vulnerable populations.

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.

Two bee-pollinated plant species show higher seed production when grown in gardens compared to arable farmland.

BACKGROUND: Insect pollinator abundance, in particular that of bees, has been shown to be high where there is a super-abundance of floral resources; for example in association with mass-flowering crops and also in gardens where flowering plants are often densely planted. Since land management affects pollinator numbers, it is also likely to affect the resultant pollination of plants growing in these habitats. We hypothesised that the seed or fruit set of two plant species, typically pollinated by bumblebees and/or honeybees might respond in one of two ways: 1) pollination success could be reduced when growing in a floriferous environment, via competition for pollinators, or 2) pollination success could be enhanced because of increased pollinator abundance in the vicinity. METHODOLOGY/PRINCIPAL FINDINGS: We compared the pollination success of experimental plants of Glechoma hederacea L. and Lotus corniculatus L. growing in gardens and arable farmland. On the farms, the plants were placed either next to a mass-flowering crop (oilseed rape, Brassica napus L. or field beans, Vicia faba L.) or next to a cereal crop (wheat, Triticum spp.). Seed set of G. hederacea and fruit set of L. corniculatus were significantly higher in gardens compared to arable farmland. There was no significant difference in pollination success of G. hederacea when grown next to different crops, but for L. corniculatus, fruit set was higher in the plants growing next to oilseed rape when the crop was in flower. CONCLUSIONS/SIGNIFICANCE: The results show that pollination services can limit fruit set of wild plants in arable farmland, but there is some evidence that the presence of a flowering crop can facilitate their pollination (depending on species and season). We have also demonstrated that gardens are not only beneficial to pollinators, but also to the process of pollination.

Estimation of bumblebee queen dispersal distances using sibship reconstruction method.

Dispersal ability is a key determinant of the propensity of an organism to cope with habitat fragmentation and climate change. Here we quantify queen dispersal in two common bumblebee species in an arable landscape. Dispersal was measured by taking DNA samples from workers in the spring and summer, and from queens in the following spring, at 14 sites across a landscape. The queens captured in the spring must be full sisters of workers that were foraging in the previous year. A range of sibship reconstruction methods were compared using simulated data sets including or no genotyping errors. The program Colony gave the most accurate reconstruction and was used for our analysis of queen dispersal. Comparison of queen dispersion with worker foraging distances was used to take into account an expected low level of false identification of sister pairs which might otherwise lead to overestimates of dispersal. Our data show that Bombus pascuorum and B. lapidarius queens can disperse by at least 3 and 5 km, respectively. These estimates are consistent with inferences drawn from studies of population structuring in common and rare bumblebee species, and suggest that regular gene flow over several kilometres due to queen dispersal are likely to be sufficient to maintain genetic cohesion of ubiquitous species over large spatial scales whereas rare bumblebee species appear unable to regularly disperse over distances greater than 10 km. Our results have clear implications for conservation strategies for this important pollinator group, particularly when attempting to conserve fragmented populations.

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.