Penelope R. Whitehorn

Neonicotinoid pesticide reduces bumble bee colony growth and queen production.

Bad News for Bees Neonicotinoid insecticides were introduced in the early 1990s and have become one of the most widely used crop pesticides in the world. These compounds act on the insect central nervous system, and they have been shown to be persistent in the environment and in plant tissues. Recently, there have been controversial connections made between neonicotinoids and pollinator deaths, but the mechanisms underlying these potential deaths have remained unknown. Whitehorn et al. (p. 351, published online 29 March) exposed developing colonies of bumble bees to low levels of the neonicotinoid imidacloprid and then released them to forage under natural conditions. Treated colonies displayed reduced colony growth and less reproductive success, and they produced significantly fewer queens to found subsequent generations. Henry et al. (p. 348, published online 29 March) documented the effects of low-dose, nonlethal intoxication of another widely used neonicotinoid, thiamethoxam, on wild foraging honey bees. Radio-frequency identification tags were used to determine navigation success of treated foragers, which suggested that their homing success was much reduced relative to untreated foragers. Bumble bee colonies produce many fewer queens after exposure to a widely used insecticide. 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.

Conclusions of the Worldwide Integrated Assessment on the risks of neonicotinoids and fipronil to biodiversity and ecosystem functioning

The side effects of the current global use of pesticides on wildlife, particularly at higher levels of biological organization: populations, communities and ecosystems, are poorly understood (Kohler and Triebskorn 2013). Here, we focus on one of the problematic groups of agrochemicals, the systemic insecticides fipronil and those of the neonicotinoid family. The increasing global reliance on the partly prophylactic use of these persistent and potent neurotoxic systemic insecticides has raised concerns about their impacts on biodiversity, ecosystem functioning and ecosystem services provided by a wide range of affected species and environments. The present scale of use, combined with the properties of these compounds, has resulted in widespread contamination of agricultural soils, freshwater resources, wetlands, non-target vegetation and estuarine and coastal marine systems, which means that many organisms inhabiting these habitats are being repeatedly and chronically expose...

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.

BackgroundInbreeding 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.ResultsThe 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.ConclusionOur 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.

Kin recognition and inbreeding reluctance in bumblebees

Inbreeding frequently has a costly impact on fitness, thus selection has favoured the evolution of kin recognition and inbreeding avoidance behaviour in many species. As haplodiploid Hymenoptera, bumblebees are susceptible to additional costs of inbreeding due to their single-locus complementary sex determination (sl-CSD) system, which means that incest can result in the production of costly diploid males. Here we test whether Bombus terrestris reproductives are able to discriminate between kin and non-kin and whether their willingness to mate is adjusted accordingly. We found that B. terrestris reproductives took significantly longer to mate with siblings compared to non-relatives. This indicates that this species exhibits kin recognition and uses this information to determine mating behaviour.ZusammenfassungBei vielen Tierarten führt die Paarung mit nahen Verwandten bei den Nachkommen zu einer geringerer Fitness, ein Phänomen, das als Inzuchtdepression bekannt ist. Solche Arten sollten daher in der Lage sein, ihre Verwandten zu erkennen und eine Paarung mit ihnen zu vermeiden. Das Ziel dieses Experimentes war es zu prüfen, ob Hummeln aus der Art Bombus terrestris ihre Verwandten erkennen können, da Hummeln allgemein als besonders anfällig gegenüber Inzuchteffekte gelten. Dies vor allem deshalb, da aufgrund der genetischen Strukturen im Hummelvolk die Paarung zwischen verwandten Individuen zu diploiden Männchen führen kann. Diploide Männchen sind steril und werden auf Kosten der fleißigen Arbeiterinnen produziert, wodurch das Hummelvolk geschwächt wird. Daher sollte die natürliche Selektion zu Verwandtschaftserkennung und Inzuchtvermeidung führen, um die Kosten für die Produktion diploider Männchen zu umgehen. Das Paarungsexperiment wurde in einem großen Flugkäfig (70 cm × 70 cm × 70 cm) aus Gaze durchgeführt und den jungen Königinnen wurden entweder ihre Brüder oder unverwandte Männchen als Paarungspartner angeboten. Die Bereitschaft der Königinnen sich mit ihren Brüdern bzw. den unverwandten Männchen zu paaren wurde ermittelt, indem die Zeitspanne zwischen dem Freilassen der Paarungspartner (Königin und Männchen) und der erfolgreichen Kopulation gemessen wurde. Durchschnittlich 10,8 Minuten (± 0,94) vergingen, bis eine Verwandtenpaarung stattfand, während im Durchschnitt lediglich 4,5 Minuten (± 1,15) für eine Paarung zwischen nicht verwandten Partnern benötigt wurden. Diese Ergebnisse lassen vermuten, dass B. terrestris die Fähigkeit zur Verwandtschaftserkennung besitzt und entsprechend dem Verwandtschaftsgrad das Paarungsverhalten ändert. Weitere Untersuchungen sollten die Mechanismen der Verwandtschaftserkennung aufklären.

Influence of urbanisation on the prevalence of protozoan parasites of bumblebees

1. Increasing urbanisation is often cited as a cause of declining biodiversity, but for bumblebees there is evidence that urban populations of some species such as Bombus terrestris L. may be more dense than those found in agricultural landscapes, perhaps because gardens provide plentiful floral resources and nesting opportunities.

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.

Investigating the impact of deploying commercial Bombus terrestris for crop pollination on pathogen dynamics in wild bumble bees

Summary The use of commercial bumble bees for crop pollination has been implicated in the decline of wild bumble bees through the spread of pathogens. This study investigates whether diseases from commercial bumble bees threaten native species in the UK. We sampled bumble bees from ten soft fruit farms: five that deploy commercial Bombus terrestris and five that do not. Each farm was visited monthly throughout the summer and workers of B. terrestris, B. pratorum, B. pascuorumand B. lapidarius were captured. The faeces of these bees were inspected for the gut microparasites Crithidia spp., Nosema bombi and Apicystis bombi. Prevalence was defined as the proportion of individuals infected and abundance was defined as the number of pathogen cells per volume of bumble bee faeces. The prevalence of A. bombi and N. bombi was too low to analyse. The prevalence and abundance of Crithidia spp. was significantly different among bumble bee species. Overall, the prevalence of Crithidia spp. was initially lower on farms deploying commercial bumble bees, possibly due to a dilution effect caused by the high density of imported bees. Crithidia spp. prevalence in Bombus terrestris, however, rose sharply on commercial farms at the end of the season. One potential explanation is that commercial bumble bees contract the local pathogen, which is then rapidly transmitted among them due to the high bee density. Whilst our data provide no evidence of pathogen spillover to wild species, it would be premature to conclude with certainty that commercial colonies do not represent a disease risk to native bees in the UK and we urge further studies into this phenomenon.

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.

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.