The impact of inbreeding and parasitism on bumblebees

Many bumblebee species are suffering from the effects of habitat fragmentation and population isolation. In some cases, populations have lost genetic diversity due to genetic drift and it is possible they are now at heightened risk of extinction. Inbreeding may be particularly costly to bumblebees because, as Hymenoptera, their complementary sex determination system can lead to the production of sterile or inviable diploid males. However, little is known about the effect that diploid male production has on bumblebee colony fitness. Here, the consequences of brother-sister mating in the bumblebee Bombus terrestris are investigated, and the production of diploid males was found to exert considerable costs at the colony level by reducing productivity and survival. Diploid males may therefore act as indicators of the genetic health of populations, and their detection could be used as an informative tool in hymenopteran conservation. Due to the costs associated with inbreeding, selection may have favoured the evolution of kin recognition systems in bumblebees. Data are presented that suggest that B. terrestris can discriminate between kin and non-kin as gynes were less willing to mate with siblings compared to non-relatives. Theory predicts that inbreeding may impose further costs on bumblebees through increased levels of parasitism, but empirical data are scarce. The relationship between population genetic diversity and parasite prevalence is assessed using Hebridean island populations of Bombus muscorum and Bombus jonellus. In the more outbred B. jonellus, there was no relationship between parasite prevalence and population heterozygosity. But prevalence of the gut parasite Crithidia bombi and the tracheal mite Locustacarus buchneri were found to be higher in populations of B. muscorum that had lower genetic diversity. In addition to assessing infection status, the activity of the immune system was assessed in each individual bee. However, there was no relationship between population heterozygosity and these immune parameters. This suggests that, in some Hymenopteran species, as populations lose genetic diversity the impact of parasitism will increase, potentially pushing threatened populations closer to extinction. Therefore, preventing population fragmentation by the creation of suitable habitats and by ensuring connectivity between habitat patches are important aspects of hymenopteran conservation. Finally, this thesis investigates the potential threat of pathogen spread from commercially reared bumblebees used for crop pollination to wild bumblebees. Although no direct evidence for parasite spillover is found, the prevalence of C. bombi was significantly higher in B. terrestris by the end of the season on farms that used commercial bumblebees compared to farms that did not. This high prevalence does suggest that pathogen spillover is a potential threat and it would be preferable to reduce the usage of commercial bumblebees where possible. For example, sowing wild flower mixes could boost natural pollinator populations, which in turn would benefit soft fruit pollination. Overall, this thesis contributes to our knowledge of the consequences of inbreeding in bumblebees and the relationship between genetic diversity and parasite prevalence. It provides a greater understanding of the factors that might be pushing threatened pollinators towards extinction and as a whole provides important information that may inform conservation practitioners, whose aim is to protect the future of our hymenopteran pollinators

Neonicotinoid pesticide limits improvement in buzz pollination by bumblebees

Neonicotinoid pesticides have been linked to global declines of beneficial insects such as bumblebees. Exposure to trace levels of these chemicals causes sub-lethal effects, such as reduced learning and foraging efficiency. Complex behaviours may be particularly vulnerable to the neurotoxic effects of neonicotinoids. Such behaviours may include buzz pollination (sonication), in which pollinators, usually bees, use innate and learned behaviours to generate high-frequency vibrations to release pollen from flowers with specialised anther morphologies. This study assesses the effect of field-realistic, chronic exposure to the widely-used neonicotinoid thiamethoxam on the development of sonication buzz characteristics over time, as well as the collection of pollen from buzz-pollinated flowers. We found that the pollen collection of exposed bees improved less with increasing experience than that of unexposed bees, with exposed bees collecting between 47% and 56% less pollen by the end of 10 trials. We also found evidence of two distinct strategies for maximising pollen collection: (1) extensions to the duration of individual buzzes and (2) extensions of the overall time spent buzzing. We find new complexities in buzz pollination, and conclude that the impacts of field-realistic exposure to a neonicotinoid pesticide may seriously compromise this important ecosystem service

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

Sib-mating does not lead to facultative sex ratio adjustment in the parasitoid wasp, Nasonia vitripennis

Sex ratio theory predicts that in haplodiploid species, females should lay a relatively more female-biased offspring sex ratio when they mate with a sibling compared with when they mate with a non-relative. This is because in haplodiploids, inbreeding leads to females having greater relatedness to daughters relative to sons. This prediction has only been tested in the parasitoid waspNasonia vitripennis, where no support for this prediction was found. However, a limitation of this previous work is that it was carried out with only two females laying eggs per patch. This is a problem, because in this case the predicted difference in the offspring sex ratio is small and therefore hard to detect. We addressed this problem by utilizing a situation in which larger sex ratio differences are predicted – five females laying eggs per patch. Consistent with the previous results, we also found that the offspring sex ratio laid by a female was not influenced by whether she mated with a sibling or non-relative. Meta-analysis of all the experiments we have undertaken confirms this pattern. This failure to respond to the identity of a mating partner suggests females are unable to discriminate kin and is a relatively rare example of maladaptive sex allocation

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

P.R.W. was funded by the University of Stirling, C.V.B. and S.M.G. were funded by Nuffield Research Placements and N.C., J.G. and D.M.S. were funded by NERC (NE/J024481/1).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.Publisher PDFPeer reviewe

The effects of climate and land use on British bumblebees:Findings from a decade of citizen-science observations

Bumblebees are important pollinators but are suffering from population declines due to land use intensification and climate change. In-depth knowledge of species' relationships with different land use and climate variables is invaluable to guide conservation efforts, as well as enable predictions to be made about the impacts of future changes in these variables. Here we use 10 years of bumblebee abundance data from the UK, collected by citizen scientists as part of the BeeWalk scheme, to investigate associations between 14 bumblebee species and various land use, habitat and climate variables. National-scale land cover and climate data were complemented with observer-collected habitat data. Bumblebee presence and abundance showed strong relationships with environmental variables. However, interspecific variation was far stronger than commonalities, which suggests that targeted conservation work is required to effectively safeguard particular species. Within species, we found evidence of different habitat associations between reproductive and worker castes. The results also showed that wetland and riparian habitats had consistently positive associations with a number of species, while semi-natural, arable and urban areas had strongly species-specific associations. Synthesis and applications. This study reveals strong effects of specific habitats occurring within broad land cover types on the presence and abundance of bumblebees, with several distinct habitats having importance for different species and castes. Consequently, conservation efforts need to be carefully tailored to particular species. Nevertheless, reversing the loss of semi-natural areas such as wetlands may be the single most generally effective action for bumblebee conservation while improving habitats in urban and arable areas could benefit particular (rare) species. Our results also suggest that the combination of long-term, detailed monitoring data of both species and habitats, here collected by citizen scientists, with remotely sensed landcover and climate data is essential to extend knowledge of species' habitat requirements and to support future research and conservation.</p

The effects of climate and land use on British bumblebees: Findings from a decade of citizen‐science observations

Bumblebees are important pollinators but are suffering from population declines due to land use intensification and climate change. In-depth knowledge of species' relationships with different land use and climate variables is invaluable to guide conservation efforts, as well as enable predictions to be made about the impacts of future changes in these variables. Here we use 10 years of bumblebee abundance data from the UK, collected by citizen scientists as part of the BeeWalk scheme, to investigate associations between 14 bumblebee species and various land use, habitat and climate variables. National-scale land cover and climate data were complemented with observer-collected habitat data. Bumblebee presence and abundance showed strong relationships with environmental variables. However, interspecific variation was far stronger than commonalities, which suggests that targeted conservation work is required to effectively safeguard particular species. Within species, we found evidence of different habitat associations between reproductive and worker castes. The results also showed that wetland and riparian habitats had consistently positive associations with a number of species, while semi-natural, arable and urban areas had strongly species-specific associations. Synthesis and applications. This study reveals strong effects of specific habitats occurring within broad land cover types on the presence and abundance of bumblebees, with several distinct habitats having importance for different species and castes. Consequently, conservation efforts need to be carefully tailored to particular species. Nevertheless, reversing the loss of semi-natural areas such as wetlands may be the single most generally effective action for bumblebee conservation while improving habitats in urban and arable areas could benefit particular (rare) species. Our results also suggest that the combination of long-term, detailed monitoring data of both species and habitats, here collected by citizen scientists, with remotely sensed landcover and climate data is essential to extend knowledge of species' habitat requirements and to support future research and conservation.</p

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 non-linear 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 generalised, 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