The potential for parasite spill-back from commercial bumblebee colonies: a neglected threat to wild bees?

Commercially-reared bumblebee colonies provide pollination services to numerous crop species globally. These colonies may harbour parasites which can spill-over to wild bee species. However, the potential for parasites to spread from wild to commercial bumblebees, which could then lead to parasite spill-back, is poorly understood. To investigate this, parasite-free commercial Bombus terrestris audax colonies, which are used commercially for strawberry pollination, were placed into seasonal strawberry crops for either 6- or 8-week blocks across two key time periods, early spring and early summer. Bumblebees were removed from colonies weekly and screened for the presence of parasites. In the early spring placement, only one parasite, the highly virulent neogregarine Apicystis bombi, was detected at a low prevalence (0.46% across all bees screened). In contrast, all colonies placed in the crop in the early summer became infected. A trypanosome, Crithidia bombi, and A. bombi were the most prevalent parasites across all samples, reaching peak prevalence in screened bees of 39.39% and 18.18% respectively at the end of the experimental period. The prevalence of A. bombi was greater than most UK records from wild bumblebees, suggesting that commercial colonies could enhance levels of A. bombi infection in wild bees through spill-back. Studies on larger geographical scales with different commercial colony densities are required to fully assess spill-back risk. However, seasonal management, to minimise spill-back opportunities, and treatment of commercial colonies to prevent infection, could be implemented to manage the potential risks of parasite spill-back to wild bees. Implications for insect conservation Our results show that commercial bumblebee populations do pick up infections, most likely from wild bees, and that these infections can reach prevalences where they may pose a threat to wild bees via parasite spill-back. More research is required to clarify the extent of this potential threat. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s10841-021-00322-x.

Agrochemicals interact synergistically to increase bee mortality.

Global concern over widely documented declines in pollinators1-3 has led to the identification of anthropogenic stressors that, individually, are detrimental to bee populations4-7. Synergistic interactions between these stressors could substantially amplify the environmental effect of these stressors and could therefore have important implications for policy decisions that aim to improve the health of pollinators3,8,9. Here, to quantitatively assess the scale of this threat, we conducted a meta-analysis of 356 interaction effect sizes from 90 studies in which bees were exposed to combinations of agrochemicals, nutritional stressors and/or parasites. We found an overall synergistic effect between multiple stressors on bee mortality. Subgroup analysis of bee mortality revealed strong evidence for synergy when bees were exposed to multiple agrochemicals at field-realistic levels, but interactions were not greater than additive expectations when bees were exposed to parasites and/or nutritional stressors. All interactive effects on proxies of fitness, behaviour, parasite load and immune responses were either additive or antagonistic; therefore, the potential mechanisms that drive the observed synergistic interactions for bee mortality remain unclear. Environmental risk assessment schemes that assume additive effects of the risk of agrochemical exposure may underestimate the interactive effect of anthropogenic stressors on bee mortality and will fail to protect the pollinators that provide a key ecosystem service that underpins sustainable agriculture.

Varietal and seasonal differences in the effects of commercial bumblebees on fruit quality in strawberry crops.

Both wild and managed pollinators significantly contribute to global food production by providing pollination services to crops. Colonies of commercially-reared honey bees and bumblebees are two of the largest groups of managed pollinators. Bumblebees in particular are increasingly used on soft fruit crops, such as strawberry, an economically important crop globally. Despite the use of commercial bumblebees in strawberry crops, there is little quantitative evidence that they provide a benefit to farmers. Given the negative impacts that commercial colonies can have on wild bee populations, it is vital that the benefits of commercial bumblebees are quantified, so reasoned management decisions can be made that provide maximum benefit to both farmers and wild bees. In this study, commercial colonies of the UK native subspecies Bombus terrestris audax were placed into June-bearer (flowering March-April, varieties 'Malling Centenary' and 'Flair') and everbearer (flowering May-June) strawberry polytunnels on a soft-fruit farm in the south east of England, and opened and closed at weekly intervals. The flower-visiting assemblage inside polytunnels was quantified, and fruit was harvested and quality assessed. In the June-bearer variety Malling Centenary, the presence of commercial bumblebees increased the amount of high commercial grade fruit by 25%. In contrast, no benefit of commercial bees on pollination or fruit quality was observed in the June-bearer variety Flair and the everbearer crop. The increase in quality of fruit in the Malling Centenary crop may be driven by the higher B. terrestris audax flower visitation rates seen in this crop in combination with varietal differences in pollination dependency. The number of flower visits by wild pollinators was not a well-supported predictor of strawberry quality, thus the benefit they provide in this system remains to be elucidated. The results presented here suggest that commercial bumblebees can greatly increase the quality and subsequent value of a strawberry crop, when deployed on a suitable variety at a time when wild pollinator numbers are low. However, the results also raise the possibility that commercial colonies do not always provide the benefits to strawberry crops that they are thought to. For growers to make informed decisions on commercial bumblebee use, further research is required into the effect of commercial bumblebees on the major strawberry varieties, in different locations and seasons. This study is an important step in gaining this understanding.

Bumblebee olfactory learning affected by task allocation but not by a trypanosome parasite.

Parasites can induce behavioural changes in their host organisms. Several parasite species are known to infect bumblebees, an important group of pollinators. Task allocation within bumblebee colonies can also cause differences in behaviour. Thus, task allocation may lead to context-dependent impacts of parasites on host behaviour. This study uses Bombus terrestris and its gut trypanosome Crithidia bombi, to investigate the effects of parasitism, task allocation (foraging or nest-work) and their interactions, on olfactory learning. Prior to undergoing the olfactory learning task, bees were orally infected with a field-realistic dose of C. bombi, and observed to determine task allocation. Parasitism did not significantly affect olfactory learning, but task allocation did, with foragers being significantly more likely to learn than nest bees. There was no significant interaction between parasitism and task. These results suggest that C. bombi is unlikely to affect pollination services via changes in olfactory learning of its host if bees are under no environmental or nutritional stress. However, wild and commercial colonies are likely to face such stressors. Future studies in the field are needed to extrapolate our results to real world effects.

The database of the PREDICTS (Projecting Responses of Ecological Diversity In Changing Terrestrial Systems) project.

The PREDICTS project-Projecting Responses of Ecological Diversity In Changing Terrestrial Systems (www.predicts.org.uk)-has collated from published studies a large, reasonably representative database of comparable samples of biodiversity from multiple sites that differ in the nature or intensity of human impacts relating to land use. We have used this evidence base to develop global and regional statistical models of how local biodiversity responds to these measures. We describe and make freely available this 2016 release of the database, containing more than 3.2 million records sampled at over 26,000 locations and representing over 47,000 species. We outline how the database can help in answering a range of questions in ecology and conservation biology. To our knowledge, this is the largest and most geographically and taxonomically representative database of spatial comparisons of biodiversity that has been collated to date; it will be useful to researchers and international efforts wishing to model and understand the global status of biodiversity.

Global effects of land use on local terrestrial biodiversity.

Human activities, especially conversion and degradation of habitats, are causing global biodiversity declines. How local ecological assemblages are responding is less clear--a concern given their importance for many ecosystem functions and services. We analysed a terrestrial assemblage database of unprecedented geographic and taxonomic coverage to quantify local biodiversity responses to land use and related changes. Here we show that in the worst-affected habitats, these pressures reduce within-sample species richness by an average of 76.5%, total abundance by 39.5% and rarefaction-based richness by 40.3%. We estimate that, globally, these pressures have already slightly reduced average within-sample richness (by 13.6%), total abundance (10.7%) and rarefaction-based richness (8.1%), with changes showing marked spatial variation. Rapid further losses are predicted under a business-as-usual land-use scenario; within-sample richness is projected to fall by a further 3.4% globally by 2100, with losses concentrated in biodiverse but economically poor countries. Strong mitigation can deliver much more positive biodiversity changes (up to a 1.9% average increase) that are less strongly related to countries' socioeconomic status.

The PREDICTS database: a global database of how local terrestrial biodiversity responds to human impacts.

Biodiversity continues to decline in the face of increasing anthropogenic pressures such as habitat destruction, exploitation, pollution and introduction of alien species. Existing global databases of species' threat status or population time series are dominated by charismatic species. The collation of datasets with broad taxonomic and biogeographic extents, and that support computation of a range of biodiversity indicators, is necessary to enable better understanding of historical declines and to project - and avert - future declines. We describe and assess a new database of more than 1.6 million samples from 78 countries representing over 28,000 species, collated from existing spatial comparisons of local-scale biodiversity exposed to different intensities and types of anthropogenic pressures, from terrestrial sites around the world. The database contains measurements taken in 208 (of 814) ecoregions, 13 (of 14) biomes, 25 (of 35) biodiversity hotspots and 16 (of 17) megadiverse countries. The database contains more than 1% of the total number of all species described, and more than 1% of the described species within many taxonomic groups - including flowering plants, gymnosperms, birds, mammals, reptiles, amphibians, beetles, lepidopterans and hymenopterans. The dataset, which is still being added to, is therefore already considerably larger and more representative than those used by previous quantitative models of biodiversity trends and responses. The database is being assembled as part of the PREDICTS project (Projecting Responses of Ecological Diversity In Changing Terrestrial Systems - http://www.predicts.org.uk). We make site-level summary data available alongside this article. The full database will be publicly available in 2015.