Bees and the pollination services they deliver are beneficial to both food crop production, and for reproduction of many wild plant species. Bee decline has stimulated widespread interest in ...assessing hazards and risks to bees from the environment in which they live. While there is increasing knowledge on how the use of broad-spectrum insecticides in agricultural systems may impact bees, little is known about effects of other pesticides (or plant protection products; PPPs) such as herbicides and fungicides, which are used more widely than insecticides at a global scale. We adopted a systematic approach to review existing research on the potential impacts of fungicides and herbicides on bees, with the aim of identifying research approaches and determining knowledge gaps. While acknowledging that herbicide use can affect forage availability for bees, this review focussed on the potential impacts these compounds could have directly on bees themselves. We found that most studies have been carried out in Europe and the USA, and investigated effects on honeybees. Furthermore, certain effects, such as those on mortality, are well represented in the literature in comparison to others, such as sub-lethal effects. More studies have been carried out in the lab than in the field, and the impacts of oral exposure to herbicides and fungicides have been investigated more frequently than contact exposure. We suggest a number of areas for further research to improve the knowledge base on potential effects. This will allow better assessment of risks to bees from herbicides and fungicides, which is important to inform future management decisions around the sustainable use of PPPs.
Exposure to Plant Protection Products, PPPs, (fungicides, herbicides and insecticides) is a significant stressor for bees and other pollinators, and has recently been the focus of intensive debate ...and research. Specifically, exposure through contaminated pollen and nectar is considered pivotal, as it presents the highest risk of PPP exposure across all bee species. However, the actual risk that multiple PPP residues might pose to non-target species is difficult to assess due to the lack of clear evidence of their actual concentrations. To consolidate the existing knowledge of field-realistic residues detected in pollen and nectar directly collected from plants, we performed a systematic literature review of studies over the past 50 years (1968–2018). We found that pollen was the matrix most frequently evaluated and, of the compounds investigated, the majority were detected in pollen samples. Although the overall most studied category of PPPs were the neonicotinoid insecticides, the compounds with the highest median concentrations of residues in pollen were: the broad spectrum carbamate carbofuran (1400 ng/g), the fungicide and nematicide iprodione (524 ng/g), and the organophosphate insecticide dimethoate (500 ng/g). In nectar, the highest median concentration of PPP residues detected were dimethoate (1595 ng/g), chlorothalonil (76 ng/g), and the insecticide phorate (53.5 ng/g). Strong positive correlation was observed between neonicotinoid residues in pollen and nectar of cultivated plant species. The maximum concentrations of several compounds detected in nectar and pollen were estimated to exceed the LD50s for honey bees, bumble bees and four solitary bee species, by several orders of magnitude. However, there is a paucity of information for the biggest part of the world and there is an urgent need to expand the range of compounds evaluated in PPP studies.
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Cultivation of mass flowering entomophilous crops benefits from the presence of managed and wild pollinators, who visit flowers to forage on pollen and nectar. However, management of these crops ...typically includes application of pesticides, the presence of which may pose a hazard for pollinators foraging in an agricultural environment. To determine the levels of potential exposure to pesticides, their presence and concentration in pollen and nectar need assessing, both within and beyond the target crop plants. We selected ten pesticide compounds and one metabolite and analysed their occurrence in a crop (Brassica napus) and a wild plant (Rubus fruticosus agg.), which was flowering in field edges. Nectar and pollen from both plants were collected from five spring and five winter sown B. napus fields in Ireland, and were tested for pesticide residues, using QuEChERS and Liquid Chromatography tandem mass spectrometry (LC-MS/MS). Pesticide residues were detected in plant pollen and nectar of both plants. Most detections were from fields with no recorded application of the respective compounds in that year, but higher concentrations were observed in recently treated fields. Overall, more residues were detected in B. napus pollen and nectar than in the wild plant, and B. napus pollen had the highest mean concentration of residues. All matrices were contaminated with at least three compounds, and the most frequently detected compounds were fungicides. The most common compound mixture was comprised of the fungicides azoxystrobin, boscalid, and the neonicotinoid insecticide clothianidin, which was not recently applied on the fields. Our results indicate that persistent compounds like the neonicotinoids, should be continuously monitored for their presence and fate in the field environment. The toxicological evaluation of the compound mixtures identified in the present study should be performed, to determine their impacts on foraging insects that may be exposed to them.
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•Pesticide residues in plant pollen and nectar may pose a hazard for pollinators.•We evaluated the pesticide residues in a crop and a wild plant species in Ireland.•Most detections were in fields with no recent application of the compounds detected.•Azoxystrobin, boscalid and clothianidin was the most common compound mixture.•Clothianidin was detected in both plant species several years after its application.
In an agricultural environment, where crops are treated with pesticides, bees are likely to be exposed to a range of chemical compounds in a variety of ways. The extent to which different bee species ...are affected by these chemicals, largely depends on the concentrations and type of exposure. We quantified the presence of selected pesticide compounds in the pollen of two different entomophilous crops; oilseed rape (Brassica napus) and broad bean (Vicia faba). Sampling was performed in 12 sites in Ireland and our results were compared with the pollen loads of honey bees and bumble bees actively foraging on those crops in those same sites. Detections were compound specific, and the timing of pesticide application in relation to sampling likely influenced the final residue contamination levels. Most detections originated from compounds that were not recently applied on the fields, and samples from B. napus fields were more contaminated compared to those from V. faba fields. Crop pollen was contaminated only with fungicides, honey bee pollen loads contained mainly fungicides, while more insecticides were detected in bumble bee pollen loads. The highest number of compounds and most detections were observed in bumble bee pollen loads, where notably, all five neonicotinoids assessed (acetamiprid, clothianidin, imidacloprid, thiacloprid, and thiamethoxam) were detected despite the no recent application of these compounds on the fields where samples were collected. The concentrations of neonicotinoid insecticides were positively correlated with the number of wild plant species present in the bumble bee-collected pollen samples, but this relationship could not be verified for honey bees. The compounds azoxystrobin, boscalid and thiamethoxam formed the most common pesticide combination in pollen. Our results raise concerns about potential long-term bee exposure to multiple residues and question whether honey bees are suitable surrogates for pesticide risk assessments for all bee species.
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•Pesticide residues in various pollen types may pose a hazard for pollinators.•We evaluated the pesticide residues in crop, honey bee and bumble bee pollen.•Following the BeeREX model no risk was identified for honey bees.•Azoxystrobin, boscalid and thiamethoxam was the most common compound mix.•Different contamination patterns were observed between different bee taxa.
•Urban multi-floral honeys had a higher total phenolic content than rural honeys.•Heather honey had the highest total phenolic content of all Irish honeys.•Irish heather honey had a higher total ...phenolic content than Manuka honey.•Irish heather honey had similar physiochemical characteristics to Manuka honey.
The composition of honey influences how beneficial it is to human health. This study evaluated the physiochemical properties and total phenolic content (TPC) of single vs. multi-floral Irish and selected international honeys, and whether properties varied according to hive location. Oilseed rape honey had the lowest TPC of Irish unifloral honeys. Heather honey had the highest TPC, similar to Manuka honey (Mean ± SD = 68.16 ± 2.73 and 62.43 ± 10.03 respectively), and the TPC of ivy honey was approximately half that of heather. Urban multi-floral honeys contained higher TPC (28.26 ± 13.63) than rural honeys (20.32 ± 11.54). Physiochemical properties varied according to floral origin, and whether hives were in urban or rural sites. Irish heather honey had similar physiochemical characteristics to Manuka honey. This first examination of Irish honey confirms that TPC and physiochemical properties vary with honey type and hive location, and suggests that Irish heather honey should be examined for potential health benefits.
Despite a substantial increase in scientific, public and political interest in pollinator health and many practical conservation efforts, incorporating initiatives across a range of scales and ...sectors, pollinator health continues to decline. We review existing pollinator conservation initiatives and define their common structural elements. We argue that implementing effective action for pollinators requires further scientific understanding in six key areas: (i) status and trends of pollinator populations; (ii) direct and indirect drivers of decline, including their interactions; (iii) risks and co-benefits of pollinator conservation actions for ecosystems; (iv) benefits of pollinator conservation for society; (v) the effectiveness of context-specific, tailored, actionable solutions; and (vi) integrated frameworks that explicitly link benefits and values with actions to reverse declines. We propose use of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services (IPBES) conceptual framework to link issues and identify critical gaps in both understanding and action for pollinators. This approach reveals the centrality of addressing the recognized
drivers of decline, such as patterns of global trade and demography, which are frequently overlooked in current pollinator conservation efforts. Finally, we discuss how existing and new approaches in research can support efforts to move beyond these shortcomings in pollinator conservation initiatives. This article is part of the theme issue 'Natural processes influencing pollinator health: from chemistry to landscapes'.
Declines in insect pollinators across Europe have raised concerns about the supply of pollination services to agriculture. Simultaneously, EU agricultural and biofuel policies have encouraged ...substantial growth in the cultivated area of insect pollinated crops across the continent. Using data from 41 European countries, this study demonstrates that the recommended number of honeybees required to provide crop pollination across Europe has risen 4.9 times as fast as honeybee stocks between 2005 and 2010. Consequently, honeybee stocks were insufficient to supply >90% of demands in 22 countries studied. These findings raise concerns about the capacity of many countries to cope with major losses of wild pollinators and highlight numerous critical gaps in current understanding of pollination service supplies and demands, pointing to a pressing need for further research into this issue.
Invasive alien plants can compete with native plants for resources, and may ultimately decrease native plant diversity and/or abundance in invaded sites. This could have consequences for native ...mutualistic interactions, such as pollination. Although invasive plants often become highly connected in plant-pollinator interaction networks, in temperate climates they usually only flower for part of the season. Unless sufficient alternative plants flower outside this period, whole-season floral resources may be reduced by invasion. We hypothesized that the cessation of flowering of a dominant invasive plant would lead to dramatic, seasonal compositional changes in plant-pollinator communities, and subsequent changes in network structure. We investigated variation in floral resources, flower-visiting insect communities, and interaction networks during and after the flowering of invasive Rhododendron ponticum in four invaded Irish woodland sites. Floral resources decreased significantly after R. ponticum flowering, but the magnitude of the decrease varied among sites. Neither insect abundance nor richness varied between the two periods (during and after R. ponticum flowering), yet insect community composition was distinct, mostly due to a significant reduction in Bombus abundance after flowering. During flowering R. ponticum was frequently visited by Bombus; after flowering, these highly mobile pollinators presumably left to find alternative floral resources. Despite compositional changes, however, network structural properties remained stable after R. ponticum flowering ceased: generality increased, but quantitative connectance, interaction evenness, vulnerability, H'2 and network size did not change. This is likely because after R. ponticum flowering, two to three alternative plant species became prominent in networks and insects increased their diet breadth, as indicated by the increase in network-level generality. We conclude that network structure is robust to seasonal changes in floral abundance at sites invaded by alien, mass-flowering plant species, as long as alternative floral resources remain throughout the season to support the flower-visiting community.
The impact of neonicotinoid insecticides on insect pollinators is highly controversial. Sublethal concentrations alter the behaviour of social bees and reduce survival of entire colonies. However, ...critics argue that the reported negative effects only arise from neonicotinoid concentrations that are greater than those found in the nectar and pollen of pesticide-treated plants. Furthermore, it has been suggested that bees could choose to forage on other available flowers and hence avoid or dilute exposure. Here, using a two-choice feeding assay, we show that the honeybee, Apis mellifera, and the buff-tailed bumblebee, Bombus terrestris, do not avoid nectar-relevant concentrations of three of the most commonly used neonicotinoids, imidacloprid (IMD), thiamethoxam (TMX), and clothianidin (CLO), in food. Moreover, bees of both species prefer to eat more of sucrose solutions laced with IMD or TMX than sucrose alone. Stimulation with IMD, TMX and CLO neither elicited spiking responses from gustatory neurons in the bees' mouthparts, nor inhibited the responses of sucrose-sensitive neurons. Our data indicate that bees cannot taste neonicotinoids and are not repelled by them. Instead, bees preferred solutions containing IMD or TMX, even though the consumption of these pesticides caused them to eat less food overall. This work shows that bees cannot control their exposure to neonicotinoids in food and implies that treating flowering crops with IMD and TMX presents a sizeable hazard to foraging bees.
Summary
Invasive non‐native plants form interactions with native species and have the potential to cause direct and indirect impacts on those species, as well as the functioning of invaded ...ecosystems.
Many entomophilous invasive plants form interactions with resident pollinators; sometimes, these interactions are necessary for the reproductive success of the invader. However, the direct role native pollinators play in plant invasion is not well understood and varies according to invasive plant traits, including breeding system and pollination syndrome.
The majority of studies addressing impacts on plant–pollinator mutualisms have focussed on the indirect impacts of plant invasion for native plant pollination. Fewer studies have focussed on the direct effects of invasive plants on native flower visitors.
Impacts of invasive plants on native pollinators can occur at a range of scales: from the individual flower visitors (in terms of nutrition, health and fitness), to populations (size, density and growth rates), communities (richness, diversity and composition) and community‐level interactions (insect–flower interaction networks). Most research to date has focussed on community‐level impacts, with almost nothing known about the effects of invaders on native flower visitor individuals or populations.
Invasive plant traits, including reward quantity and quality, spatial and temporal availability and accessibility, modulate effects on native flower visitors, and thus, different plant species have different impacts. Similarly, flower visitors do not all respond in the same way to invasive plants. Thus, generalizations are difficult to make, but understanding impacts at the individual and population level for different visitor taxa is key to explaining community‐level impacts.
There have been varied approaches to determining impacts, with most studies attempting to compare invaded vs. non‐invaded habitats. The pros and cons of different approaches are discussed.
Since it is impractical to study every invasive plant in every ecological context in which it occurs, we recommend a better understanding of relevant individual‐level traits to predict direct interactions between invasive plants and native pollinators.
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