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

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

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 criticised 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 771ppb in pollen and up to 561ppb in nectar. The image of thiacloprid as a relatively benign neonicotinoid should now be questioned

Incidental mosquitocidal effect of an ivermectin mass drug administration on Anopheles farauti conducted for scabies control in the Solomon Islands.

Background: The Solomon Islands is targeting elimination of malaria by 2030. The dominant vector is the predominantly exophagic, exophilic Anopheles farauti sensu strictu. This biting behaviour limits the efficacy of conventional vector control tools and highlights the need for new strategies. When administered to humans ivermectin has been shown to have a mosquitocidal effect. Mass drug administration (MDA) with ivermectin is an emerging strategy in the control of scabies. In this study we explored any incidental effect of ivermectin MDA conducted for scabies control on mosquitoes. Methods: MDA for scabies was conducted in three villages. We performed human landing catches and measured 5-day mortality amongst Anopheles mosquitoes caught before and after MDA. Cox regression was used to calculate hazard ratios (HR) for mortality between mosquitoes caught before and after MDA. Results: There was a significant increase in 5-day mortality in anopheline mosquitoes caught post-MDA which was highest on the day of MDA itself (HR 4.2 95% CI 1.8 to 10.1, p=0.001) and the following day (HR 4.4 95% CI 1.8 to 10.8, p=0.002) compared to mosquitoes caught before MDA. Conclusions: This study shows a possible mosquitocidal effect of ivermectin MDA conducted for scabies control. Studies with a larger sample size with clinical as well as entomological outcomes should be conducted in this population

Field-potential evidence for extrasynaptic alterations in the hippocampal CA1 pyramidal cell population during paired-pulse potentiation

The mechanisms of paired-pulse potentiation of the CA1 pyramidal cell population were examined by determining input-output relations for control and potentiated responses originating from the activation of radiatum fibers in the hippocampal slice preparation. Two types of potentiation for synchronously discharging pyramidal cells (population spike) were observed. In the first type, the potentiation of the population spike was found to be a combination of synaptic and extrasynaptic factors. This form of potentiation was observed in 16 of 28 slices. In the second type, the potentiation of the population spike was attributed entirely to the potentiation of summated dendritic depolarizations (population EPSP). This synaptic process of potentiation was observed in 12 of 28 slices. The involvement of only extrasynaptic mechanisms in the paired-pulse potentiation of the population spike was not observed. For the potentiation originating from a combination of synaptic and extrasynaptic mechanisms, 60% of the potentiation of the population spike was a result of synaptic factors and 40% could be attributed to extrasynaptic factors. These results support the concept that alterations in the excitability of postsynaptic neurons serve as a component of the mechanisms of paired-pulse potentiation in the radiatum fiber-CA1 pyramidal cell system.Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/25247/1/0000689.pd

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

Monitoring neonicotinoid exposure for bees in rural and peri-urban areas of the UK 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 UK 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

Ornamental plants on sale to the public are a significant source of pesticide residues with implications for the health of pollinating insects

Garden centres frequently market nectar- and pollen-rich ornamental plants as “pollinator-friendly”, however these plants are often treated with pesticides during their production. There is little information on the nature of pesticide residues present at the point of purchase and whether these plants may actually pose a threat to, rather than benefit, the health of pollinating insects. Using mass spectrometry analyses, this study screened leaves from 29 different ‘bee-friendly’ plants for 8 insecticides and 16 fungicides commonly used in ornamental production. Only two plants (a Narcissus and a Salvia variety) did not contain any pesticide and 23 plants contained more than one pesticide, with some species containing mixtures of 7 (Ageratum houstonianum) and 10 (Erica carnea) different agrochemicals. Neonicotinoid insecticides were detected in more than 70% of the analysed plants, and chlorpyrifos and pyrethroid insecticides were found in 10% and 7% of plants respectively. Boscalid, spiroxamine and DMI-fungicides were detected in 40% of plants. Pollen samples collected from 18 different plants contained a total of 13 different pesticides. Systemic compounds were detected in pollen samples at similar concentrations to those in leaves. However, some contact (chlorpyrifos) and localised penetrant pesticides (iprodione, pyroclastrobin and prochloraz) were also detected in pollen, likely arising from direct contamination during spraying. The neonicotinoids thiamethoxam, clothianidin and imidacloprid and the organophosphate chlorpyrifos were present in pollen at concentrations between 6.9 and 81 ng/g and at levels that overlap with those known to cause harm to bees. The net effect on pollinators of buying plants that are a rich source of forage for them but simultaneously risk exposing them to a cocktail of pesticides is not clear. Gardeners who wish to gain the benefits without the risks should seek uncontaminated plants by growing their own from seed, plant-swapping or by buying plants from an organic nursery