Lactic acid bacteria (LAB) are well recognized beneficial host-associated members of the microbiota of humans and animals. Yet LAB-associations of invertebrates have been poorly characterized and ...their functions remain obscure. Here we show that honeybees possess an abundant, diverse and ancient LAB microbiota in their honey crop with beneficial effects for bee health, defending them against microbial threats. Our studies of LAB in all extant honeybee species plus related apid bees reveal one of the largest collections of novel species from the genera Lactobacillus and Bifidobacterium ever discovered within a single insect and suggest a long (>80 mya) history of association. Bee associated microbiotas highlight Lactobacillus kunkeei as the dominant LAB member. Those showing potent antimicrobial properties are acquired by callow honey bee workers from nestmates and maintained within the crop in biofilms, though beekeeping management practices can negatively impact this microbiota. Prophylactic practices that enhance LAB, or supplementary feeding of LAB, may serve in integrated approaches to sustainable pollinator service provision. We anticipate this microbiota will become central to studies on honeybee health, including colony collapse disorder, and act as an exemplar case of insect-microbe symbiosis.
The global increase in the proportion of land cultivated with pollinator‐dependent crops implies increased reliance on pollination services. Yet agricultural practices themselves can profoundly ...affect pollinator supply and pollination. Extensive monocultures are associated with a limited pollinator supply and reduced pollination, whereas agricultural diversification can enhance both. Therefore, areas where agricultural diversity has increased, or at least been maintained, may better sustain high and more stable productivity of pollinator‐dependent crops. Given that >80% of all crops depend, to varying extents, on insect pollination, a global increase in agricultural pollinator dependence over recent decades might have led to a concomitant increase in agricultural diversification. We evaluated whether an increase in the area of pollinator‐dependent crops has indeed been associated with an increase in agricultural diversity, measured here as crop diversity, at the global, regional, and country scales for the period 1961–2016. Globally, results show a relatively weak and decelerating rise in agricultural diversity over time that was largely decoupled from the strong and continually increasing trend in agricultural dependency on pollinators. At regional and country levels, there was no consistent relationship between temporal changes in pollinator dependence and crop diversification. Instead, our results show heterogeneous responses in which increasing pollinator dependence for some countries and regions has been associated with either an increase or a decrease in agricultural diversity. Particularly worrisome is a rapid expansion of pollinator‐dependent oilseed crops in several countries of the Americas and Asia that has resulted in a decrease in agricultural diversity. In these regions, reliance on pollinators is increasing, yet agricultural practices that undermine pollination services are expanding. Our analysis has thereby identified world regions of particular concern where environmentally damaging practices associated with large‐scale, industrial agriculture threaten key ecosystem services that underlie productivity, in addition to other benefits provided by biodiversity.
Increasing cultivation of pollinator‐dependent crops has placed a stress on global pollination capacity, which could have been ameliorated by a concomitant increase in agricultural diversification. However, this study reports a relatively weak and decelerating rise in agricultural diversity over time that was largely decoupled from the strong and continually increasing trend in agricultural dependency on pollinators. Particularly worrisome is a rapid expansion of pollinator‐dependent monocultures in several countries of the Americas and Asia that has resulted in a decrease in agricultural diversity. In these regions, reliance on pollinators is increasing, yet agricultural practices that undermine pollination services are expanding.
Urbanisation is an important global driver of biodiversity change, negatively impacting some species groups whilst providing opportunities for others. Yet its impact on ecosystem services is poorly ...investigated. Here, using a replicated experimental design, we test how Central European cities impact flying insects and the ecosystem service of pollination. City sites have lower insect species richness, particularly of Diptera and Lepidoptera, than neighbouring rural sites. In contrast, Hymenoptera, especially bees, show higher species richness and flower visitation rates in cities, where our experimentally derived measure of pollination is correspondingly higher. As well as revealing facets of biodiversity (e.g. phylogenetic diversity) that correlate well with pollination, we also find that ecotones in insect-friendly green cover surrounding both urban and rural sites boost pollination. Appropriately managed cities could enhance the conservation of Hymenoptera and thereby act as hotspots for pollination services that bees provide to wild flowers and crops grown in urban settings.
Through laboratory experiments in which treatments were administered singly or in combination to individual insects, we recorded harmful effects of FPF and pathogens on honey bee survival and immune ...gene expression. Though we found no evidence of synergistic interactions among stressors on either honey bee survival or viral load, the combined treatment SULF and DWV‐B led to a synergistic up‐regulation of dicer‐like gene expression. We conclude that common viral pathogens pose a major threat to honey bees whilst co‐exposure to these novel nACHR insecticides does not significantly exacerbate viral impacts on host survival in the laboratory.
Summary
The decline of insect pollinators threatens global food security. A major potential cause of decline is considered to be the interaction between environmental stressors, particularly between exposure to pesticides and pathogens. To explore pesticide–pathogen interactions in an important pollinator insect, the honey bee, we used two new nicotinic acetylcholine receptor agonist insecticides (nACHRs), flupyradifurone (FPF) and sulfoxaflor (SULF), at sublethal and field‐realistic doses in a fully crossed experimental design with three common viral honey bee pathogens, Black queen cell virus (BQCV) and Deformed wing virus (DWV) genotypes A and B. Through laboratory experiments in which treatments were administered singly or in combination to individual insects, we recorded harmful effects of FPF and pathogens on honey bee survival and immune gene expression. Though we found no evidence of synergistic interactions among stressors on either honey bee survival or viral load, the combined treatment SULF and DWV‐B led to a synergistic upregulation of dicer‐like gene expression. We conclude that common viral pathogens pose a major threat to honey bees, while co‐exposure to these novel nACHR insecticides does not significantly exacerbate viral impacts on host survival in the laboratory.
The gut microbiome plays an important role in bee health and disease. But it can be disrupted by pesticides and in-hive chemicals, putting honey bee health in danger. We used a controlled and fully ...crossed laboratory experimental design to test the effects of a 10-day period of chronic exposure to field-realistic sublethal concentrations of two nicotinic acetylcholine receptor agonist insecticides (nACHRs), namely flupyradifurone (FPF) and sulfoxaflor (Sulf), and a fungicide, azoxystrobin (Azoxy), individually and in combination, on the survival of individual honey bee workers and the composition of their gut microbiota (fungal and bacterial diversity). Metabarcoding was used to examine the gut microbiota on days 0, 5, and 10 of pesticide exposure to determine how the microbial response varies over time; to do so, the fungal ITS2 fragment and the V4 region of the bacterial 16S rRNA were targeted. We found that FPF has a negative impact on honey bee survival, but interactive (additive or synergistic) effects between either insecticide and the fungicide on honey bee survival were not statistically significant. Pesticide treatments significantly impacted the microbial community composition. The fungicide Azoxy substantially reduced the Shannon diversity of fungi after chronic exposure for 10 days. The relative abundance of the top 10 genera of the bee gut microbiota was also differentially affected by the fungicide, insecticides, and fungicide-insecticide combinations. Gut microbiota dysbiosis was associated with an increase in the relative abundance of opportunistic pathogens such as Serratia spp. (e.g. S. marcescens), which can have devastating consequences for host health such as increased susceptibility to infection and reduced lifespan. Our findings raise concerns about the long-term impact of novel nACHR insecticides, particularly FPF, on pollinator health and recommend a novel methodology for a refined risk assessment that includes the potential effects of agrochemicals on the gut microbiome of bees.
Display omitted
•Novel insecticide flupyradifurone reduced honey bee longevity.•Pesticide treatments affected the composition of host microbiome communities.•The Shannon diversity of the fungal microbiome was decreased by fungicide treatment.•Dysbiosis of the gut microbiota was seen as an increase in relative abundance of opportunistic pathogens.
A microbiome silver bullet for honey bees Paxton, Robert J
Science (American Association for the Advancement of Science),
01/2020, Letnik:
367, Številka:
6477
Journal Article
Recenzirano
A genetically engineered honey bee gut bacterium knocks down two major bee threats
The western honey bee (
Apis mellifera
) brings tangible benefits to humans as an important pollinator and insights ...into social evolution as a model organism. Yet, despite close scientific scrutiny, it is under global threat from a range of stressors (
1
) that are unlikely to diminish with global change. Chief among these are pests and pathogens, remedies to which are either ineffective, short-term, expensive, or impractical. On page 573 of this issue, Leonard
et al.
(
2
) reveal a hidden microbiological key to fight these pests and pathogens: genetically modified honey bee gut bacteria tailored to induce host RNA interference (RNAi)–based defense (
3
) that is effective, long-term, potentially cheap, and easy to apply. This important approach may not only provide a solution to many of the honey bee's woes, it also offers a new functional genomic toolkit with which to dissect the molecular intricacies of honey bees and their societies.
Urbanization is a global phenomenon with major effects on species, the structure of community functional traits and ecological interactions. Body size is a key species trait linked to metabolism, ...life‐history and dispersal as well as a major determinant of ecological networks. Here, using a well‐replicated urban–rural sampling design in Central Europe, we investigate the direction of change of body size in response to urbanization in three common bumblebee species, Bombus lapidarius, Bombus pascuorum and Bombus terrestris, and potential knock‐on effects on pollination service provision. We found foragers of B. terrestris to be larger in cities and the body size of all species to be positively correlated with road density (albeit at different, species‐specific scales); these are expected consequences of habitat fragmentation resulting from urbanization. High ambient temperature at sampling was associated with both a small body size and an increase in variation of body size in all three species. At the community level, the community‐weighted mean body size and its variation increased with urbanization. Urbanization had an indirect positive effect on pollination services through its effects not only on flower visitation rate but also on community‐weighted mean body size and its variation. We discuss the eco‐evolutionary implications of the effect of urbanization on body size, and the relevance of these findings for the key ecosystem service of pollination.
Bees are considered to be threatened globally, with severe overwinter losses of the most important commercial pollinator, the Western honeybee, a major concern in the Northern Hemisphere. Emerging ...infectious diseases have risen to prominence due to their temporal correlation with colony losses. Among these is Deformed wing virus (DWV), which has been frequently linked to colony mortality. We now provide evidence of a strong statistical association between overwintering colony decline in the field and the presence of DWV genotype-B (DWV-B), a genetic variant of DWV that has recently been shown to be more virulent than the original DWV genotype-A. We link the prevalence of DWV-B directly to a quantitative measure of overwinter decline (workforce mortality) of honeybee colonies in the field. We demonstrate that increased prevalence of virus infection in individual bees is associated with higher overwinter mortality. We also observed a substantial reduction of infected colonies in the spring, suggesting that virus-infected individuals had died during the winter. Our findings demonstrate that DWV-B, plus possible A/B recombinants exhibiting DWV-B at PCR primer binding sites, may be a major cause of elevated overwinter honeybee loss. Its potential emergence in naïve populations of bees may have far-reaching ecological and economic impacts.
Urbanization is considered a global threat to biodiversity; the growth of cities results in an increase in impervious surfaces, soil and air pollution, fragmentation of natural vegetation and ...invasion of non-native species, along with numerous environmental changes, including the heat island phenomenon. The combination of these effects constitutes a challenge for both the survival and persistence of many native species, while also imposing altered selective regimes. Here, using 110 314 single nucleotide polymorphisms generated by restriction-site-associated DNA sequencing, we investigated the genome-wide effects of urbanization on putative neutral and adaptive genomic diversity in a major insect pollinator, Bombus lapidarius, collected from nine German cities and nine paired rural sites. Overall, genetic differentiation among sites was low and there was no obvious genome-wide genetic structuring, suggesting the absence of strong effects of urbanization on gene flow. We nevertheless identified several loci under directional selection, a subset of which was associated with urban land use, including the percentage of impervious surface surrounding each sampling site. Overall, our results provide evidence of local adaptation to urbanization in the face of gene flow in a highly mobile insect pollinator.
Cross-species transmission of a pathogen from a reservoir to a recipient host species, spillover, can have major impacts on biodiversity, domestic species and human health.
(DWV) is a panzootic RNA ...virus in honeybees that is causal in their elevated colony losses, and several correlative field studies have suggested spillover of DWV from managed honeybees to wild bee species such as bumblebees. Yet unequivocal demonstration of DWV spillover is lacking, while spillback, the transmission of DWV from a recipient back to the reservoir host, is rarely considered. Here, we show in fully crossed laboratory experiments that the transmission of DWV (genotype A) from honeybees to bumblebees occurs readily, yet we neither detected viral transmission from bumblebees to honeybees nor onward transmission from experimentally infected to uninoculated bumblebees. Our results support the potential for viral spillover from honeybees to other bee species in the field when robbing resources from heterospecific nests or when visiting the same flowers. They also underscore the importance of studies on the virulence of DWV in wild bee species so as to evaluate viral impact on individual and population fitness as well as viral adaption to new host species.