Article

Do novel insecticides pose a threat to beneficial insects?

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Abstract

Systemic insecticides, such as neonicotinoids, are a major contributor towards beneficial insect declines. This has led to bans and restrictions on neonicotinoid use globally, most noticeably in the European Union, where four commonly used neonicotinoids (imidacloprid, thiamethoxam, clothianidin and thiacloprid) are banned from outside agricultural use. While this might seem like a victory for conservation, restrictions on neonicotinoid use will only benefit insect populations if newly emerging insecticides do not have similar negative impacts on beneficial insects. Flupyradifurone and sulfoxaflor are two novel insecticides that have been registered for use globally, including within the European Union. These novel insecticides differ in their chemical class, but share the same mode of action as neonicotinoids, raising the question as to whether they have similar sub-lethal impacts on beneficial insects. Here, we conducted a systematic literature search of the potential sub-lethal impacts of these novel insecticides on beneficial insects, quantifying these effects with a meta-analysis. We demonstrate that both flupyradifurone and sulfoxaflor have significant sub-lethal impacts on beneficial insects at field-realistic levels of exposure. These results confirm that bans on neonicotinoid use will only protect beneficial insects if paired with significant changes to the agrochemical regulatory process. A failure to modify the regulatory process will result in a continued decline of beneficial insects and the ecosystem services on which global food production relies.

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... Sulfoxaflor exposure can have significant sub-lethal impacts on bumblebee (B. terrestris) reproduction (Siviter et al. 2018a, Siviter et al. 2020Linguadoca et al. 2021) (but see [Siviter et al. 2019]) and flupyradifurone exposure can impair honeybee larval development (Tan et al. 2017, Al Naggar andBaer 2019), and adult behaviour , Tong et al. 2019, Hesselbach et al. 2020 (recently reviewed in [Siviter and Muth 2020]). Novel insecticides could also interact with bee pathogens, for example, bumblebee larvae fed sulfoxaflor in isolation showed no evidence of an increase in larval mortality, but when coexposed to sulfoxaflor, and the common bumblebee parasite Nosema bombi, there was a significant increase in larval mortality (Siviter et al. 2020a). ...
... Sulfoxaflor exposure can have significant sub-lethal impacts on bumblebee (B. terrestris) reproduction (Siviter et al. 2018a, Siviter et al. 2020Linguadoca et al. 2021) (but see [Siviter et al. 2019]) and flupyradifurone exposure can impair honeybee larval development (Tan et al. 2017, Al Naggar andBaer 2019), and adult behaviour , Tong et al. 2019, Hesselbach et al. 2020 (recently reviewed in [Siviter and Muth 2020]). Novel insecticides could also interact with bee pathogens, for example, bumblebee larvae fed sulfoxaflor in isolation showed no evidence of an increase in larval mortality, but when coexposed to sulfoxaflor, and the common bumblebee parasite Nosema bombi, there was a significant increase in larval mortality (Siviter et al. 2020a). ...
... mellifera) fed flupyradifurone and inoculated with N. ceranae had lower survival than unexposed bees, and those exposed to each stressor in isolation (Al Naggar and Baer 2019). While we found no interaction between C. bombi and the neonicotinoid thiamethoxam on bee mortality, future research should focus on understanding how novel insecticides, such as sulfoxaflor and flupyradifurone, interact with common bee parasites (Siviter and Muth 2020). ...
Article
Neonicotinoid insecticides are the most commonly used insecticide in the world and can have significant sub-lethal impacts on beneficial insects, including bumblebees, which are important pollinators of agricultural crops and wild-flowers. This has led to bans on neonicotinoid use in the EU and has resulted in repeated calls for the agrochemical regulatory process to be modified. For example, there is increasing concern about 1) the underrepresentation of wild bees, such as bumblebees, in the regulatory process, and 2) the failure to determine how agrochemicals, such as neonicotinoids, interact with other commonly occurring environmental stressors, such as parasites. Here, we modify an OECD approved lethal dose (LD50) experimental design and coexpose bumblebees (Bombus terrestris) to the neonicotinoid thiamethoxam and the highly prevalent trypanosome parasite Crithidia bombi, in a fully crossed design. We found no difference in the LD50 of thiamethoxam on bumblebees that had or had not been inoculated with the parasite (Crithidia bombi). Furthermore, thiamethoxam dosage did not appear to influence the parasite intensity of surviving bumblebees, and there was no effect of either parasite or insecticide on sucrose consumption. The methodology used demonstrates how existing ring-tested experimental designs can be effectively modified to include other environmental stressors such as parasites. Moving forward, the regulatory process should implement methodologies that assess the interactions between agrochemicals and parasites on non-Apis bees and, in cases when this is not practical, should implement post-regulatory monitoring to better understand the real-world consequences of agrochemical use.
... A victory for conservation of biodiversity was thought when neonicotinoids were banned in Europe (Siviter and Muth, 2020). However, these restrictions to neonicotinoid applications will only benefit biodiversity if newer classes of insecticides are not toxic to non-target insect species. ...
... Beneficial insects face many different stresses caused directly or indirectly by humans that include pesticides, climate change, pathogens, and habitat loss that causes depletion of their nutritional resources and nesting sites. Interaction between multiple stressors can exacerbate negative effects of pesticides (Ricupero et al., 2020;Siviter and Muth, 2020). For instance, the toxic effect of insecticides can be synergized when beneficial insects face hazardous temperatures (Ricupero et al., 2020). ...
... Also, the selection of organisms that should be included in each environmental test should be done on criteria including likeliness of being exposed and ecological importance of the species (Hilbeck et al., 2011). As an example, wild bee species and non-bee insects in ERA should be mandatory (Siviter and Muth, 2020) as they are often present in agricultural fields, and they are key to maintain yields of many crops by making 61% of the visits to crop flowers and sustaining life on Earth (Rader et al., 2015). In chapters 2 and 3, I used hoverflies because they are the most important non-bee pollinators (Rader et al., 2015). ...
... Neonicotinoid exposure also impaired the colony development and foraging performance of bumblebees, which offers a potential mechanism driving the observed downstream effects on reproductive output. We also found genus-level differences, with neonicotinoids impairing Bombus, but not Osmia individual development, highlighting the limitations of generalising results across bee genera (Franklin & Raine, 2019;Siviter & Muth, 2020). Our results confirm that policies that restrict and reduce neonicotinoid use will likely benefit bee populations. ...
... The development of novel systemic insecticides, such as sulfoxaflor and flupyradifurone, that have a similar mode of action to neonicotinoids, offer a direct replacement for neonicotinoids (Brown et al., 2016). While less is known about these novel insecticides, they can impair bee foraging behaviour (Hesselbach et al., 2020;Tong et al., 2019) (but see (Siviter et al., 2019)), reproductive output (Siviter et al., 2018a(Siviter et al., , 2020b and they can also increase bee mortality at field-realistic levels (Siviter et al., 2020a; (recently reviewed in (Siviter & Muth, 2020)). Therefore, while our results confirm that bans on neonicotinoid use will likely benefit wild bee populations, they will only be successful if paired with (1) changes to the agrochemical regulatory process, that ensures novel insecticides do not have a similar sub-lethal effects on non-Apis bees and (2) a reduction in intensive agriculture, and a move towards an integrated pest management approach that promotes biological control, and reduced insecticide use (Colin et al., 2020;Siviter & Muth, 2020). ...
... While less is known about these novel insecticides, they can impair bee foraging behaviour (Hesselbach et al., 2020;Tong et al., 2019) (but see (Siviter et al., 2019)), reproductive output (Siviter et al., 2018a(Siviter et al., , 2020b and they can also increase bee mortality at field-realistic levels (Siviter et al., 2020a; (recently reviewed in (Siviter & Muth, 2020)). Therefore, while our results confirm that bans on neonicotinoid use will likely benefit wild bee populations, they will only be successful if paired with (1) changes to the agrochemical regulatory process, that ensures novel insecticides do not have a similar sub-lethal effects on non-Apis bees and (2) a reduction in intensive agriculture, and a move towards an integrated pest management approach that promotes biological control, and reduced insecticide use (Colin et al., 2020;Siviter & Muth, 2020). A failure to radically change food production, and agrochemical regulation, will result in a continued decline in bee populations that we rely on for functioning eco-systems. ...
Article
Full-text available
Neonicotinoid insecticides can have sub-lethal effects on bees which has led to calls from conservationists for a global ban. In contrast, agrochemical companies argue that neonicotinoids do not harm honeybees at field-realistic levels. However, the focus on honeybees neglects the potential impact on other bee species. We conducted a meta-analysis to assess whether field-realistic neonicotinoid exposure has sub-lethal effects on non-Apis bees. We extracted data from 53 papers (212 effects sizes) and found that it largely consisted of two genera: bumblebees (Bombus) and mason bees (Osmia), highlighting a substantial taxonomic knowledge gap. Neonicotinoid exposure negatively affected reproductive output across all bees and impaired bumblebee colony growth and foraging. Neonicotinoids also reduced Bombus, but not Osmia, individual development (growth and body size). Our results suggest that restrictions on neonicotinoids should benefit bee populations and highlight that the current regulatory process does not safeguard pollinators from the unwanted consequences of insecticide use.
... However, sulfoximines' similarities to neonicotinoids' mode of action (Simon-Delso et al., 2015) and their potential application over vast geographic areas have raised concerns regarding potential adverse effects on non-target organisms (Jiang et al., 2019) and especially on pollinators (Brown et al., 2016). Artificial feeding experiments have recently suggested negative impacts of sulfoxaflor on the reproductive output of bumblebee colonies (Siviter et al., 2018a;Siviter and Muth, 2020). These effects seem to be driven by reduced egg-laying activity and altered larval development (Siviter et al., 2020a(Siviter et al., , 2020b rather than impaired bee-foraging behavior and cognition (Siviter et al., 2019(Siviter et al., , 2018b. ...
... We found indications for resource limitation that might have exacerbated pesticide effects on bumblebee colonies . Our results indicate that sulfoxaflor exposure could be hazardous to bumblebees under field conditions (Siviter and Muth, 2020), even when applied two days before crop bloom. This mitigation strategy might thus be inadequate to eliminate the risk for bumblebees. ...
... This type of insecticides can in fact alter the olfactory learning and working memory, fundamental for foragers to efficiently locate suitable unvisited flowers (Gill and Raine, 2014;Siviter et al., 2018b). However, a recent meta-analysis found no evidence for negative effects of sulfoxaflor exposure on bumblebee cognition and behavior (Siviter and Muth, 2020). In particular, bumblebees exposed to sulfoxaflor did not show impaired foraging performance in a field experiment (Siviter et al., 2018a) or altered cognitive abilities under laboratory conditions (Siviter et al., 2019). ...
Article
Full-text available
Sulfoximines, the next generation systemic insecticides developed to replace neonicotinoids, have been shown to negatively impact pollinator development and reproduction. However, field-realistic studies on sulfoximines are few and consequences on pollination services unexplored. Moreover, the impacts of other agrochemicals such as fungicides, and their combined effects with insecticides remain poorly investigated. Here, we show in a full factorial semi-field experiment that spray applications of both the product Closer containing the insecticide sulfoxaflor and the product Amistar containing the fungicide azoxystrobin, negatively affected the individual foraging performance of bumblebees (Bombus terrestris). Insecticide exposure further reduced colony growth and size whereas fungicide exposure decreased pollen deposition. We found indications for resource limitation that might have exacerbated pesticide effects on bumblebee colonies. Our work demonstrates that field-realistic exposure to sulfoxaflor can adversely impact bumblebees and that applications before bloom may be insufficient as a mitigation measure to prevent its negative impacts on pollinators. Moreover, fungicide use during bloom could reduce bumblebee foraging performance and pollination services.
... Here we investigate the potential effects of two new agrochemicals: sulfoxaflor (Sulf) and flupyradifurone (FPF) on the honey bee gut microbiome. These novel insecticides, which belong to the chemical groups sulfoximines and butenolides respectively, act as selective agonists of Nicotinic Acetyl Choline Receptors (NAChRs) in the same way that neonicotinoids do, and have negative effects on insect pollinators that are substantially comparable to those of neonicotinoids (Siviter and Muth, 2020). ...
... consistent with previous observations that FPF exposure during either larval development or adulthood has a negative impact on honey bee survival (Al Naggar and Baer, 2019;Al Naggar and Paxton, 2021;Guo et al., 2021;Hesselbach et al., 2020;Tosi et al., 2021). A meta-analysis of studies on the potential sub-lethal effects of FPF has also revealed that exposure to field-realistic levels of FPF have significant sub-lethal effects on honey bees (Siviter and Muth, 2020). ...
Article
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.
... This evidence, therefore, suggests that restrictions on the use of neonicotinoids will likely benefit bees (Woodcock et al. 2016). Similarly, novel insecticides, such as flupyradifurone and sulfoxaflor, that are chemically distinct from neonicotinoids, but share a similar mode of action, also have similar sublethal effects on bees (Tong et al. 2019;Siviter and Muth 2020;Siviter et al. 2020aSiviter et al. , 2020b (but see Siviter et al. 2019). The fact that neonicotinoid pesticides are still widely used, and that novel insecticides are similarly harmful, confirms that changes to the agrochemical regulatory process are required if we are to better protect bees and other pollinators from the unwanted consequences of insecticide use (Siviter et al. 2018a, Franklin and Raine 2019, Sgolastra et al. 2020, Siviter and Muth 2020. ...
... Similarly, novel insecticides, such as flupyradifurone and sulfoxaflor, that are chemically distinct from neonicotinoids, but share a similar mode of action, also have similar sublethal effects on bees (Tong et al. 2019;Siviter and Muth 2020;Siviter et al. 2020aSiviter et al. , 2020b (but see Siviter et al. 2019). The fact that neonicotinoid pesticides are still widely used, and that novel insecticides are similarly harmful, confirms that changes to the agrochemical regulatory process are required if we are to better protect bees and other pollinators from the unwanted consequences of insecticide use (Siviter et al. 2018a, Franklin and Raine 2019, Sgolastra et al. 2020, Siviter and Muth 2020. ...
Article
Bumblebees are important pollinators of agricultural crops and wildflowers, but many species are in decline. Neonicotinoid insecticides are the most commonly used insecticide globally and can have negative sublethal effects on bumblebee colony growth and reproduction. Individual bumblebees can visit hundreds to thousands of flowers a day to forage for their colony. As such, they are a model species for studying optimal foraging, and small impairments to an individual’s foraging decisions may have compounding effects on the colony’s nutritional intake. We exposed bumblebees (Bombus impatiens) to an acute, field-realistic dose of the neonicotinoid insecticide imidacloprid, before allowing them to forage on an artificial floral array. We found that neonicotinoid-exposed bumblebees made suboptimal foraging decisions, as they were more likely to visit flowers located further apart than control bees. This indicates that for a given flower patch, individual bees exposed to a neonicotinoid will likely use more energy and forage less efficiency than unexposed bees, although further studies that directly measure energetic cost are required to confirm this. Given the robust and growing body of evidence demonstrating negative sublethal effects of neonicotinoids on bees, sublethal assessments on non-Apis bees should be made mandatory within the regulatory process.
... A particular group of insecticides, the neonicotinoids, disperse easily through the environment and are found many kilometers from their target areas. In addition, these pesticides are absorbed in plant tissues, disrupting the pollinator physiology [129][130][131]. Newer insecticides, such as flupyradifurone and sulfoxaflor, were considered good candidates to replace neonicotinoids. ...
... Newer insecticides, such as flupyradifurone and sulfoxaflor, were considered good candidates to replace neonicotinoids. However, recent studies have shown that these insecticides also have non-lethal negative effects on native pollinators [131]. In Chile, agricultural regulation bans the use of certain insecticides [132], but the chemical composition of the approved insecticides has not been tested for non-lethal effects on non-target species. ...
Article
Full-text available
In the last decades, pollinators have drastically declined as a consequence of anthropogenic activities that have local and global impacts. The food industry has been expanding intensive agriculture crops, many of them dependent on animal pollination, but simultaneously reducing native pollinator habitats. Chile is a good example of this situation. Chile is becoming an agro-alimentary powerhouse in Latin America, where intensive agriculture expansion is performed at the expense of natural lands, posing a major threat to biodiversity. Here, we discussed the drivers responsible for the decline of pollinators (including habitat loss, pesticides, invasive species, and climate change) and its synergistic effects. This is particularly critical considering that Chile is a hotspot of endemic bee species locally adapted to specific habitats (e.g., Mediterranean-type ecosystems). However, there is a lack of data and monitoring programs that can provide evidence of their conservation status and contribution to crop yields. Based on our analysis, we identified information gaps to be filled and key threats to be addressed to reconcile crop production and biodiversity conservation. Addressing the local context is fundamental to undertake management and conservation actions with global impact.
... Seed treatments replacing neonicotinoids are currently entering the market in the EU. 38 In 2020 in Sweden, a limited quantity of winter oilseed rape was seed-treated with the systemic insecticide flupyradifurone. Negative effects of these new compounds on beneficial insects have, however, already been reported, 38 making their future regulatory status uncertain. ...
... 38 In 2020 in Sweden, a limited quantity of winter oilseed rape was seed-treated with the systemic insecticide flupyradifurone. Negative effects of these new compounds on beneficial insects have, however, already been reported, 38 making their future regulatory status uncertain. Future strategies for crop protection against insect pests in oilseed rape in the EU should therefore be prepared for a situation in which insecticides will be limited in their availability. ...
Article
Full-text available
There have been great concerns about negative effects on crop production resulting from the ban on insecticide seed treatments containing neonicotinoids. I examine how the neonicotinoid ban has affected crop protection and crop production in oilseed rape (Brassica napus L.) using Sweden as a case study, and compare the Swedish situation to that in leading countries growing winter and spring oilseed rape, respectively. The cropping area of winter and spring oilseed rape in Sweden has increased by ca. 40% to ca. 100’000 ha and decreased by ca. 90% to ca. 4000 ha, respectively following the ban and there are trends for increased pest and disease pressure. Overall, however, the ban has not had any major impacts on the total oilseed rape cropping area or crop yields per hectare of either winter or spring oilseed rape, which is in contrast with the development elsewhere in Europe. In Germany and the United Kingdom for example, the cropping area has decreased following the ban on neonicotinoid seed treatments, attributed to increased insect pest pressure from especially cabbage stem flea beetle, Psylliodes chrysocephala. I conclude that winter oilseed rape has remained a viable crop to grow in Sweden without insecticide seed treatments, but that further investments into integrated pest management will be needed for sustainable insect pest control in oilseed rape in the future. This article is protected by copyright. All rights reserved.
... Nevertheless, resistance to neonicotinoids was reported in different aphid species (Bass et al. 2015). Furthermore, the use of neonicotinoids was restricted in the European Union due to the lack of insect specificity, as well as the significant adverse impacts on beneficial insects (Siviter and Muth 2020). Thus, it is essential to introduce insecticides with a novel mode of action, and a safe environmental profile in A. craccivora management programs. ...
... Flupyradifurone was registered for wide use after the restriction of neonicotinoids (Siviter and Muth 2020). Flupyradifurone belongs to the butenolide insecticide class with fast systemic properties, resulting in the effective control of sucking-pest (Smith and Giurcanu 2013;Coy et al. 2016;Colares et al. 2017). ...
Article
Full-text available
With low-dose stimulation and high-dose inhibition, insecticide-induced hormesis, a biphasic phenomenon, can contribute to pest resurgence. The cowpea aphid, Aphis craccivora (Koch) (Homoptera: Aphididae), is a vital insect that infests legume crops. Its hormesis of flupyradifurone has not been previously established. Age-stage two-sex life analysis is used to investigate the sublethal and transgenerational effects of flupyradifurone on two successive generations of A. craccivora. A leaf-dip bioassay method revealed high toxicity of flupyradifurone against A. craccivora, with lethal concentration 50% value (LC50) of 1.82 mg L⁻¹ after 48 h exposure. Treatment of parent generation (F0) with LC10 and LC25 of flupyradifurone significantly increased the longevity and fecundity of the directly exposed adults. The results of transgenerational effects showed that the treatment of (F0) with LC25 induced significant hormetic effects in progeny generation (F1). Furthermore, flupyradifurone at LC25 significantly enhanced the biological traits, such as intrinsic rate of increase (r), finite rate of increase (λ), and net reproductive rate (R0) compared with the control. Similarly, both LC10 and LC25 induced a significant increase in the mean generation time T (d). Conversely, both treatments caused a significant decrease in the doubling time (DT). Data in the present study demonstrate that the exposure of (F0) to flupyradifurone at LC10 and LC25 enhanced longevity and fecundity in the directly exposed adults of A. craccivora, and induced transgenerational hormesis across the subsequent (F1) generation. These results should be taken into consideration when using flupyradifurone for controlling cowpea aphid.
... However, honeybees that are exposed to Closer during or shortly after its application may be negatively impacted (EFSA, 2019). High degradation rates of sulfoxaflor imply that at the moment of application residue levels are substantially higher with potential implications for honeybees (Cheng et al., 2018;Siviter and Muth, 2020). In fact, recent semi-field studies in which honeybees were either directly exposed to insecticide spray or visited treated flowers in full bloom one day after application, showed that sulfoxaflor or sulfoxaflor-based products (Transform, Closer) increase honeybee mortality, resource consumption and oxidative stress (Chakrabarti et al., 2020;Cheng et al., 2018;Louque, 2018). ...
... Most notably, a large-scale field experiment in Sweden showed strong effects of a neonicotinoid on solitary bees and bumblebees Wintermantel et al., 2018) but not on honeybees (Osterman et al., 2019), even though other studies found no effects of neonicotinoids on wild bees (Thompson et al., 2016;Ruddle et al., 2018). Our results, hence, do not contradict feeding-experiments finding direct effects of sulfoxaflor on bumblebee reproduction (Siviter et al., , 2018 or a meta-analysis showing negative effects of exposure to field-realistic sulfoxaflor doses on bees in general (Siviter and Muth, 2020). This is one of the first studies to experimentally test the effects of a sulfoximine-based insecticide and a fungicide on honeybees under realistic semi-field conditions. ...
Article
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Exposure to pesticides is considered a major threat to bees and several neonicotinoid insecticides were recently banned in cropland within the European Union in light of evidence of their potential detrimental effects. Nonetheless, bees remain exposed to many pesticides whose effects are poorly understood. Recent evidence suggests that one of the most prominent replacements of the banned neonicotinoids – the insecticide sulfoxaflor - harms bees and that fungicides may have been overlooked as a driver of bee declines. Realistic-exposure studies are, however, lacking. Here, we assess the impact of the insecticide Closer (active ingredient: sulfoxaflor) and the widely used fungicide Amistar (a.i.: azoxystrobin) on honeybees in a semi-field study (10 flight cages containing a honeybee colony, for each of three treatments: Closer, Amistar, Control). The products were applied according to label instructions either before (Closer) or during (Amistar) the bloom of purple tansy. We found no significant effects of Closer or Amistar on honeybee colony development or foraging activity. Our study suggests that these pesticides pose no notable risk to honeybees when applied in isolation, following stringent label instructions. The findings on Closer indicate that a safety-period of 5-6 days between application and bloom, which is only prescribed in a few EU member states, may prevent its impacts on honeybees. However, to conclude whether Closer and Amistar can safely be applied, further realistic-exposure studies should examine their effects in combination with other chemical or biological stressors on various pollinator species.
... Flupyradifurone (FPF) (Sivanto™) is a newly developed systemic insecticide as an alternative to neonicotinoids. Although it has been declared that FPF has a favorable safety profile for honey bees and other pollinators, a meta-analysis of systematic literature studies of potential sub-lethal effects of FPF has demonstrated that exposure to field-realistic levels of FPF exhibited significant sub-lethal impacts on honey bees [39]. This study investigated the effects of FPF on the development on larvae as well as foraging ability of foragers who consume the syrup during exposure. ...
Article
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Flupyradifurone (FPF) is a novel systemic nAChR agonist that interferes with signal transduction in the central nervous system of sucking pests. Despite claims that FPF is potentially “bee-safe” by risk assessments, laboratory data have suggested that FPF has multiple sub-lethal effects on individual honey bees. Our study aimed to expand the studies to the effects of field-realistic concentration of FPF. We found a statistically significant decrease in the survival rate of honey bees exposed to FPF, whereas there were no significantly negative effects on larvae development durations nor foraging activity. In addition, we found that the exposed foragers showed significantly higher expression of ApidNT, CYP9Q2, CYP9Q3, and AmInR-2 compared to the CK group (control group), but no alteration in the gene expression was observed in larvae. The exposed newly emerged bees showed significantly higher expression of Defensin and ApidNT. These results indicate that the chronic exposure to the field-realistic concentration of FPF has negligible effects, but more important synergistic and behavioral effects that can affect colony fitness should be explored in the future, considering the wide use of FPF on crops pollinated and visited by honey bees.
... However, there are serious concerns across the globe regarding the dwindling trend in both wild and domesticated pollinator populations, along with the parallel decline in plants that depend on them (Potts et al. 2010;Sánchez-Bayo and Wyckhuys 2019). Besides leveled anthropogenic pressures on natural resources, factors such as the invasive species, emerging microbial diseases, toxic effects of various pesticides are also impacting pollinator populations adversely aggravated by agro-climate change (Pudasaini et al. 2015;Dar et al. 2017;Siviter and Muth 2020). ...
Article
Aesculus indica Colebr. is a monecious, deciduous woody tree species of the temperate regions of the Himalaya. It is cultivated for its commercial use in agro-forestry practices. The present research on pollination biology and conservation of Aesculus indica growing in Kumaon Himalaya was carried out in the temperate forest ecosystem of Lohaghat, Uttarakhand, India. The field experiments were conducted on five randomly selected populations of the study plant during April 2017 to September 2017 to quantify the diversity and foraging behavior of insect visitors and their influence on fruiting success of the plant. Of the total 18 species of insects recorded as floral visitors, 77.78% of the total species belonged to the order Lepidoptera while the rest belonged to the order Hymenoptera. Butterflies foraged the flowers maximum during 10.00–13.00 h, whereas bees were more active during morning times (07.00–10.00 h). The flower handling time and foraging rate as the parameters of foraging behavior varied among insect floral visitors. Butterflies were recorded as the most frequent floral visitors accounting 62.22% of the total floral visits. Experimentally, it was found that Aesculus indica is an ambophilous plant i.e., relying on both wind and insects for its reproductive success, and exhibits psychophilous and melitophilous syndromes for pollination. The overall results on pollination mechanism of the plant would be useful in developing conservation measures for environmental stability in the face of global climate change.
... Similarly, looking beyond parasite-nutrition-chemical interactions to other multi-stressor interactions that may affect pollinators and that occur in real landscapes (for example, including effects of climate extremes, pollution or other population-level effects) is a major challenge that is yet to be addressed. The challenge that the non-additive effects of combined exposure poses for the agrochemical regulatory process is considerable, but our results suggest that it cannot be ignored [36][37][38] . Although testing all stressor combinations for all agrochemicals is not practical, it is simple to predict that certain stressors will often be present in bee populations (for example, deformed wing virus in Apis, Crithidia bombi in Bombus or poor nutrition in both) and thus could reasonably be included in upper tier testing. ...
Article
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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. A meta-analysis of studies in which bees were exposed to combinations of agrochemicals, nutritional stressors and/or parasites revealed evidence for synergistic effects on mortality when bees were exposed to multiple agrochemicals at field-realistic levels.
... The role of native pollinators in providing pollination services to crops (Garibaldi et al., 2013;Kremen et al., 2002) is increasingly important given widespread threats to honeybees, the dominant managed pollinator worldwide (Gill et al., 2016). However, agricultural intensification generally leads to both habitat fragmentation (Ricketts et al., 2008) and increased use of agrochemicals (Iwasaki & Hogendoorn, 2021;Siviter & Muth, 2020). These stresses, along with the shift from native flowering systems to highly seasonal crop floral resources, have meant that many native pollinators are threatened (Winfree, 2010) and, in some cases, have been lost from their natural ranges (Boyle & Philogène, 1983;Brown & Paxton, 2009;Lima & Marchioro, 2021). ...
Article
Supporting and promoting invertebrate diversity within agricultural ecosystems has numerous benefits, including the provision of pollination services. Many insects, including wild pollinators, require floral resources for food and structural habitat for nesting. To support pollinators, research studies and agri‐environment schemes have sought to supplement floral resources, but little is known about the value of different types of nesting habitat enhancements (e.g., trap‐nests or bee hotels). We deployed eight replicates of each of three types (bamboo reed, hardwood block and sand/cement brick) of trap‐nests at five orchards in two apple and cherry growing regions (Bilpin and Orange) in Australia. Both reed and hardwood block trap‐nests attracted a diverse array of invertebrates, such as ants, wasps, spiders and bees, including a cleptoparasitic bee species (Thyreus sp.) not previously recorded in the region. Interestingly, two taxa of native bees (Megachile [Megachile] and Megachile [Eutricharaea]) used the artificial nests and were also observed visiting apple crops. There were significantly more native bees using trap‐nests in Orange (n = 65), where orchards are surrounded by agricultural landscapes, than in Bilpin (n = 2), where orchards are surrounded by native forests. Our findings show that artificial nest enhancements are used by native bees, as well as other nontarget invertebrate taxa, some of which can be predators of bees (ants, wasps, and spiders). Nesting habitat augmentation thus has potential to be used as a conservation tool, especially in areas where nesting sites are limited. However, future studies should also consider measures to reduce colonization by non‐target taxa. To support insect pollinators research studies and agri‐environment schemes have sought to supplement floral resources, but relatively little is known about the value of different types of nesting habitat enhancements (e.g. trap‐nests or bee hotels). We deployed eight replicates of each of three types (bamboo reed, hardwood block and sand/cement brick) of trap‐nests at five orchards in two apple and cherry growing regions (Bilpin and Orange, New South Wales) in Australia. Our research highlights the potential of trap‐nests to support native bees in agricultural landscapes through habitat augmentation, with particular benefits in altered landscapes that have relatively little native habitat.
... The classical approach of combatting agricultural insect pests is via non-selective conventional insecticides. However, their limited target species selectivity has serious disadvantages, including a detrimental impact on environment and human health [229][230][231][232]. In fact, these concerns are increasing and have led to a ban in some commonly used insecticides [233][234][235]. ...
Article
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RNA-mediated pathways form an important regulatory layer of myriad biological processes. In the last decade, the potential of RNA molecules to contribute to the control of agricultural pests has not been disregarded, specifically via the RNA interference (RNAi) mechanism. In fact, several proofs-of-concept have been made in this scope. Furthermore, a novel research field regarding extracellular RNAs and RNA-based intercellular/interorganismal communication is booming. In this article, we review key discoveries concerning extracellular RNAs in insects, insect RNA-based cell-to-cell communication, and plant–insect transfer of RNA. In addition, we overview the molecular mechanisms implicated in this form of communication and discuss future biotechnological prospects, namely from the insect pest-control perspective.
... The application of synthetic insecticides has been one of the most common methods used to control H. armigera; however, multiple cases of resistance to insecticides have been reported in H. armigera populations due to heavy selection pressure (www.pesticideresistance.org) (Mota-Sanchez and Wise 2021). In addition, the use of synthetic insecticides may result in negative environmental impacts, including offtarget effects on beneficial insects (Brühl and Zaller 2019;Siviter and Muth 2020). ...
Article
Bacillus thuringiensis (Bt)-based bioinsecticides and transgenic plants expressing proteins with insecticidal activity (Cry and Vip) have been successfully used in several integrated pest management programs worldwide. Lepidoptera comprise some of the most economically important insect pests of the major agricultural crops. In this study, the toxicity of 150 Bt strains was evaluated against Helicoverpa armigera (Hübner) larvae. Eight strains (426, 520B, 1636, 1641, 1644, 1648, 1657 and 1658) showed high insecticide activity against H. armigera and were therefore tested against Anticarsia gemmatalis (Hübner), Spodoptera cosmioides (Walker), Chrysodeixis includens (Walker), and Diatraea saccharalis (Fabricius) larvae. Our results showed that most of the Bt strains were also toxic to these lepidopteran species. The biochemical and molecular analyses of these strains revealed that they had a similar protein profile; however, their cry and vip gene contents were variable. In addition, the median lethal concentration (LC50) of the selected strains indicated that the strains 1636, 1641, and 1658 were the most effective against H. armigera, showing LC50 values of 185.02, 159.44, and 192.98 ng/cm2, respectively. Our results suggest that the selected Bt strains have great potential to control the lepidopteran pests H. armigera, A. gemmatalis, D. saccharalis, S. cosmioides, and C. includes.
... [2] Originally licensed in 2013 as an effective insecticide at targeting insect pests, it was subsequently banned for use on bee-attractive crops but has since been relicensed based on modifications designed to reduce risk to bee species. [3] However, Siviter and Muth [4] recently presented evidence that sulfoxaflor may have sub-lethal impacts at field-realistic levels on non-target economically important hymenopteran species similar to those resulting from neonicotinoid pesticide exposure. [5] For example, multiple studies examining the impacts of sulfoxaflor exposure on honey bees (Apis mellifera) have revealed increased mortality, [6,7] increased oxidative stress, [6] modulation of host immunocompetence in junction with viral pathogens, [8] and increased Caspase-3 protein levels which are correlated with increased apoptosis. ...
Article
This study investigated the exposure effects of sulfoxaflor, a next-generation sulfoximine insecticide, on the viability, locomotor behavior, and nest-mate interactions of the pavement ant (Tetramorium caespitum). Adult worker ants were exposed to 0, 1, 5, 12.5, 25, or 50 mg/L of sulfoxaflor via oral ingestion for 48 h. This short-term exposure to concentrations as low as 1 mg/L had wide ranging effects on multiple locomotive parameters (average speed, mobile average speed, total travel distance), nest-mate interactions (aggression and antennation), and body morphology (abdominal curving). Exposure to sulfoxaflor for 24 h manifested in decreased locomotion, altered intraspecific interactions and the development of abdominal curvature in the 25 and 50 mg/L treatments. Such alterations in mobility and conspecific behavioral parameters would clearly impact the ability of exposed individuals to successfully satisfy resource demands and presents a risk to colony survival.
... Sulfoxaflor, for example, was reported to negatively impact egg laying in the social bumble bees (Siviter et al., 2018) but did not significantly affect olfactory conditioning and memory (Siviter et al., 2019). The effect caused by this pesticide was recently reviewed for multiple insect species (Siviter and Muth, 2020). However, studies covering the effect of sulfoxaflor on solitary bees seems rare or absent. ...
Article
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Solitary bees are among the most important pollinators worldwide however population declines especially in croplands has been noticed. The novel pesticide sulfoxaflor is a competitive modulator of nicotinic acetylcholine receptors (nAChR) in insects. While there is evidence of a negative impact of neonicotinoids on bees of several social organization levels, our overall knowledge on the impact of sulfoxaflor on bees is poor. Here we present for the first time a study showing effects of field realistic doses of sulfoxaflor on solitary bees. Bees submitted to long term exposure of field realistic doses of sulfoxaflor (5 µg dm-3 , 10 µg dm-3 , 50 µg dm-3) and control were observed regarding their survival rate. Moreover, we recorded metrics related to flower visitation and flight performance. We discover that the highest field realistic dose is lethal to Osmia bicornis along five days of exposure. The effect of sulfoxaflor reduces the outcome of foraging, important features for fruit and seed production of cross-pollinated plant species. Bees exposed to pesticide visited flowers mostly walking rather than flying. Flight performance was also impaired by the pesticide.
... Then, neonicotinoid insecticides have been introduced and became the primary choice to control aphids (Foster et al. 2003). Unfortunately, neonicotinoids have been restricted in the European Union as a result of the lack of insect speci city and the signi cant adverse impacts on bene cial insects (Siviter and Muth 2020). Therefore, it is essential to introduce insecticides with a novel mode of action, and a safe environmental pro le in A. craccivora management programs. ...
Preprint
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Insecticide induced-hormesis, a biphasic phenomenon ,with low-dose stimulation and high-dose inhibition, which effectively contributes to pest resurgence. Although cowpea aphid, Aphis craccivora (Koch) (Homoptera: Aphididae), is the most infection insect to legume crops in Egypt, its’ hormesis to flupyradifurone did not previously establish. Therefore, age-stage two-sex life analysis was used to investigate the sublethal and transgenerational effects of flupyradifurone on two successive generations of A. craccivora . Leaf-dip bioassay method revealed high toxicity of flupyradifurone against A. craccivora with LC 50 value of 1.82 mg L ⁻¹ after 48 h exposure. Treatment of parent generation (F 0 ) with LC 10 and LC 25 of flupyradifurone significantly increased the longevity and fecundity of the directly exposed adults. The results of transgenerational effects showed that treatment of (F 0 ) with LC 25 induced a significant hormetic effects in progeny generation (F 1 ). Furthermore, flupyradifurone at LC 25 significantly enhanced the biological traits such as intrinsic rate of increase (r), finite rate of increase (λ) and net reproductive rate (R 0 ) compared with the control. Similarly, both LC 10 and LC 25 caused a significant increase in the mean generation time T (d). Conversely ,both treatments had a significant decrease in the doubling time (DT). In conclusion, the obtained data demonstrate that exposure of (F 0 ) to flupyradifurone at LC 10 and LC 25 enhanced longevity and fecundity in of the directly exposed adults of A. craccivora and induced transgenerational hormesis across the subsequent (F 1 ) generation. These grades must be taken into consideration when using flupyradifurone against cowpea aphids.
... These uses continue to pollute surface water and soils with neonicotinoids and subsequently pollute wild floral resources. Also, regrettable substitution for outdoor crop protection has occurred with insecticides with similarly high toxicity to pollinators and the same mode of action [15] and new markets for neonicotinoids have opened such as the use in mariculture, including salmon farming (Sea lice medicine approval ratified in EU law). ...
... Pesticide exposure causes harm to wild pollinators as well. In some cases, pesticide exposure causes greater damage to wild pollinators than to honey bees (Biddinger et al. 2013, Cameron & Sadd 2020, Mundy-Heisz et al. 2020, Siviter & Muth 2020, Uhl & Brühl 2019. Thus, the challenges to pollination services posed by parasites, diseases, and pesticides may be greater than generally recognized. ...
... To control A. gossypii, synthetic pesticides have been used by farmers. But the overuse of these chemical products during the past several years has caused many problems such as environmental pollution, harmful to beneficial insects, accumulation of toxicity at different trophic levels, and the emergence of resistance to pesticides [4,5]. Therefore, a need to develop alternative strategies such as entomopathogenic bacterial toxins: Bacillus thuringiensis (Bt) has become necessary. ...
Article
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The objective of this study was to evaluate the insecticidal effect of toxins from Moroccan Bacillus thuringiensis strains (Berliner) (Bt) on Aphis gossypii (Homoptera: Aphididae). Aphis gossypii is one of the most pests of Moroccan crops. Their management is based traditionally on using chemical products. Some of them are well known to be potentially toxic to the environment and human health. Therefore, alternative strategies for aphid management in crops have been developed in recent years, including a biological control using toxins of bacterial strains. In this study, the artificial diet bioassay was used to screen the aphicidal effect of 82 Bt toxins against first instar nymphs and third instar nymphs of A. gossypii. Among the examined Bt strains, eleven showed a high insecticide activity against A. gossypii stages. In addition, the assessment of the lethal concentration (LC50) of selected Bt revealed that the local BtA4, BtA1 and Bt21.6 exhibited higher insecticidal activity against first instar nymphs of A. gossypii (LC50 (BtA4)=0.15, LC50 (BtA1)=0.23 and LC50 (Bt21.6)=0.25 mg/ml) and the selected strains BtB6, BtA10 and Bt21.6 exhibited the relatively best activity third instar nymphs of A. gossypii (LC50 (BtB6)= 0.48, LC50 (BtA10)= 0.79 and LC50 (Bt21.6)= 1.14 mg/ml) of A. gossypii. Therefore, the results of this study indicate that the selected B. thuringiensis strains have great potential to be used in the integrated A. gossypii management.
... In some cases, pesticide exposure causes greater damage to wild pollinators than to honey bees (Biddinger et al. 2013;Cameron & Sadd 2020;Goulson et al. 2015;Mundy-Heisz et al. Preprint;Siviter & Muth 2020;Uhl & Brühl 2019). Thus, the challenges to pollination services posed by parasites, diseases, and pesticides may be greater than generally recognized. ...
Preprint
Full-text available
Many food crops rely on pollination by animals. Historically, wind and wild organisms provided pollination as an ecosystem service that varied across agroecological zones, cropping systems, and time. The value of these pollination services is likely substantial but has not been estimated reliably. More recently, pollination services in major crop-producing regions have been provided through organized markets, primarily the rental of honey bees. The sustainability of commercially provided pollination services is being challenged by parasites, diseases, pesticide exposures, poor nutrition, and Colony Collapse Disorder. Economic analyses indicate that honey bee rental markets have been able to adjust to those challenges, at least to date. Understanding the future sustainability of rental markets requires greater knowledge of the contributions of wild pollinators, optimal management of pollination services from wild and managed organisms, and the value of pollination services provided by wild and managed organisms. Expected final online publication date for the Annual Review of Resource Economics, Volume 13 is October 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
... The impact of insecticides, most notably neonicotinoids, on natural insect populations has often been mentioned as one of the most important drivers for insect decline as these substances are meant to kill insects (6,(19)(20)(21)(22). Neonicotinoids were first introduced in 1991 and are currently the most widely used class of insecticides globally (23,24). ...
Article
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There is an ongoing unprecedented loss in insects, both in terms of richness and biomass. The usage of pesticides, especially neonicotinoid insecticides, has been widely suggested to be a contributor to this decline. However, the risks of neonicotinoids to natural insect populations have remained largely unknown due to a lack of field-realistic experiments. Here, we used an outdoor experiment to determine effects of field-realistic concentrations of the commonly applied neonicotinoid thiacloprid on the emergence of naturally assembled aquatic insect populations. Following application, all major orders of emerging aquatic insects (Coleoptera, Diptera, Ephemeroptera, Odonata, and Trichoptera) declined strongly in both abundance and biomass. At the highest concentration (10 µg/L), emergence of most orders was nearly absent. Diversity of the most species-rich family, Chironomidae, decreased by 50% at more commonly observed concentrations (1 µg/L) and was generally reduced to a single species at the highest concentration. Our experimental findings thereby showcase a causal link of neonicotinoids and the ongoing insect decline. Given the urgency of the insect decline, our results highlight the need to reconsider the mass usage of neonicotinoids to preserve freshwater insects as well as the life and services depending on them.
... www.nature.com/scientificreports/ negative impacts on beneficial insects 3 . A soil-borne bacterium, Bacillus thuringiensis (Bt), produces various insecticidal proteins (cry toxins), which have been used widely against many pests and until now, numerous cry toxins have been transformed in cotton 4 . ...
Article
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Transgenic technology played a crucial role in developing insect-resistant plants resulting in the reduced application of pesticides. This article reports the expression of two cry proteins (Cry3Bb1 and Cry3) in cotton for enhanced resistance against chewing insect pests. The aforementioned genes were synthetically developed and were cloned under appropriate regulatory sequences followed by transformation into Eagle-2 genotype (Gossypium hirsutum) of cotton through shoot apex-cut Agro-infiltration. The transgene integration was validated by polymerase chain reaction using primers flanking the aforementioned cry genes. Transgene expression was assessed by qRT-PCR using GADPH as a reference gene. The relative fold expression analyses revealed the highest expression of the transgene(s) in M1 plants, which is a 4.5-fold expression (Cry3 + Cry3Bb1) followed by M3 (fold expression, 3.0) (Cry3Bb1) and M2 (fold expression, 2.5) (Cry3) transformants of cotton. The confirmed transgenic plants were exposed to insect pests, pink bollworm (Pectinophora gossypiella), and army bollworm (Helicoverpa armigera). Bioassay results revealed that 60% mortality was observed against pink bollworm, and 75% mortality was observed against army bollworm in transgenic plants containing both Cry3Bb1 and Cry3 genes (M1 transgenic plants). In M2 transgenic plants containing only the Cry3Bb1 gene, the mortality was observed to be 40% in the pink bollworm population, whereas 45% mortality was observed in the army bollworm population. In the case of M3 transgenic plants containing single gene-Cry3, the mortality was 20% in the pink bollworm population, whereas 30% mortality was observed in the army bollworm population. Almost no mortality was observed in non-transgenic Eagle-2 control plants. Hence, the developed cotton transformants have improved resistance against chewing insect pests.
... The new compounds include flupyradifurone and sulfoxaflor (the first butanolide and sulfoximine-based insecticides, respectively) which have been registered for agricultural use [37]. Emerging evidence indicates that field-realistic exposure to these new chemical classes also has substantial sublethal effects on bees and predatory arthropods [38], and therefore will have effects on non-target species that are similar to those of neonicotinoids. ...
Article
We present the results of our 13th annual horizon scan of issues likely to impact on biodiversity conservation. Issues are either novel within the biological conservation sector or could cause a substantial step-change in impact, either globally or regionally. Our global panel of 26 scientists and practitioners identified 15 issues that we believe to represent the highest priorities for tracking and action. Many of the issues we identified, including the impact of satellite megaconstellations and the use of long-distance wireless energy transfer, have both elements of threats and emerging opportunities. A recent state-sponsored application to commence deep-sea mining represents a significant step-change in impact. We hope that this horizon scan will increase research and policy attention on the highlighted issues.
... This has prompted policy makers to reduce the environmental damage of synthetic pesticides such as neonicotinoids (Gross, 2013;Stokstad, 2018). Subsequently, novel synthetic insecticides were registered for use in the agricultural sector and it seems likely that non-target organisms will continue to receive similar negative impacts (Siviter and Muth, 2020). This collective evidence suggests that significant changes to pest control standards are necessary to bring this process to a halt. ...
Article
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Worldwide biodiversity decline is caused by multiple factors, including pesticides. Aside from their applications in agriculture, the uptake of pesticides in urban gardens is widespread. Here, we review the potential of controlling pests of ornamental garden plants, like the boxtree moth Cydalima perspectalis Walker, 1859 (Lepidoptera: Crambidae), using entomopathogenic nematodes (Heterorhabdidae & Steinernematidae). Nematode biocontrol is highly suitable, particularly for small-scale control such as in boxtree plantings. Boxtree (Buxus spp.) is an ornamental shrub widely used in public and private grounds across Europe. Over the past decade boxtree has suffered heavily from the destructive boxtree moth, an invasive and persistent pest species of East-Asian origin. Widespread application of insecticides has been effective, yet resistance to these compounds is accumulating. The dense foliage of boxtree shrubs facilitates the correct tuning of moisture and temperature conditions required for nematode mediated pest control. Warm weather, without direct sunlight, on moist to wet foliage appear to be the most suitable conditions. We conclude that the use of entomopathogenic nematodes for controlling pests, such as the boxtree moth, may limit damage to horticulture and provide a safe and environmentally friendly form of control in urban spaces.
... Numerous researchers have documented the loss of arthropod biomass and diversity in various locations around the world , Sánchez-Bayo and Wyckhuys 2019, Eggleton 2020, Wagner 2020). More specifically, declines have been attributed to land-use intensification (Sorg et al. 2013, Hallmann et al. 2017, Seibold et al. 2019, agricultural intensification (Raven and Wagner 2020), insecticide use (Hallmann et al. 2014, Siviter andMuth 2020), climate change Garcia 2018, 2019;Harris et al. 2019;Raven and Wagner 2020), and light pollution (Grubisic et al. 2018). Sánchez-Bayo and Wyckhuys (2019) predict up to 40% of the world's insect species may go extinct over the next few decades. ...
Article
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The longleaf pine Pinus palustris Miller (Pinales: Pinaceae) ecosystem once covered as many as 37 million hectares across the southeastern United States. Through fire suppression, development, and conversion to other plantation pines, this coverage has dwindled to fewer than 2 million hectares. A recent focus on the restoration of this ecosystem has revealed its complex and biologically diverse nature. Arthropods of the longleaf pine ecosystem are incredibly numerous and diverse—functionally and taxonomically. To provide clarity on what is known about the species and their functional roles in longleaf pine forests, we thoroughly searched the literature and found nearly 500 references. In the end, we tabulated 51 orders 477 families, 1,949 genera, and 3,032 arthropod species as having been stated in the scientific literature to occur in longleaf pine ecosystems. The body of research we drew from is rich and varied but far from comprehensive. Most work deals with land management objective associated taxa such as pests of pine, pests of—and food for—wildlife (red-cockaded woodpecker, northern bobwhite quail, gopher tortoise, pocket gopher, etc.), and pollinators of the diverse plant understory associated with longleaf pine. We explored the complex role frequent fire (critical in longleaf pine management) plays in determining the arthropod community in longleaf pine, including its importance to rare and threatened species. We examined known patterns of abundance and occurrence of key functional groups of longleaf pine-associated arthropods. Finally, we identified some critical gaps in knowledge and provide suggestions for future research into this incredibly diverse ecosystem.
... While this resulted in the banning of three neonicotinoids for outside use in the EU, these insecticides are still widely used around the world, and research into their impact continues. At the same time, new insecticides have been introduced and examined for their possible impacts Siviter et al., 2018;Siviter and Muth, 2020). With the recognition that interactions between stressors might play a key role in reducing bee health (e.g., Vanbergen et al., 2013), it is perhaps no surprise that most interaction studies have included insecticides as one of the stressors. ...
Article
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There is clear evidence for wild insect declines globally. Habitat loss, climate change, pests, pathogens and environmental pollution have all been shown to cause detrimental effects on insects. However, interactive effects between these stressors may be the key to understanding reported declines. Here, we review the literature on pesticide and pathogen interactions for wild bees, identify knowledge gaps, and suggest avenues for future research fostering mitigation of the observed declines. The limited studies available suggest that effects of pesticides most likely override effects of pathogens. Bees feeding on flowers and building sheltered nests, are likely less adapted to toxins compared to other insects, which potential susceptibility is enhanced by the reduced number of genes encoding detoxifying enzymes compared with other insect species. However, to date all 10 studies using a fully-crossed design have been conducted in the laboratory on social bees using Crithidia spp. or Nosema spp., identifying an urgent need to test solitary bees and other pathogens. Similarly, since laboratory studies do not necessarily reflect field conditions, semi-field and field studies are essential if we are to understand these interactions and their potential effects in the real-world. In conclusion, there is a clear need for empirical (semi-)field studies on a range of pesticides, pathogens, and insect species to better understand the pathways and mechanisms underlying their potential interactions, in particular their relevance for insect fitness and population dynamics. Such data are indispensable to drive forward robust modelling of interactive effects in different environmental settings and foster predictive science. This will enable pesticide and pathogen interactions to be put into the context of other stressors more broadly, evaluating their relative importance in driving the observed declines of wild bees and other insects. Ultimately, this will enable the development of more effective mitigation measures to protect bees and the ecosystem services they supply.
... Nowadays, environmental concerns have prompted a reduction in insecticides to control agricultural pests [36]. Thus, European Union authorities have restricted or even banned several active ingredients belonging to different action groups in recent decades [37][38][39]. Nevertheless, preventive agricultural practices can be a helpful substitute and/or supplement for citrus growers in integrated crop management, in order to reduce the use of chemical pest control. ...
Article
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The Mediterranean Basin is the second highest citrus growing region in the world behind China. Citrus trees are known to produce several flush shoots per year, particularly during the spring–summer season. Farmers endeavor to reduce the growth of summer shoots by means of hand pruning, especially those located at the top of the tree, as most of these shoots become vigorous, nutrient consuming, non-productive, and attractive to several pests. Furthermore, hand pruning substantially increases the costs of citrus orchards production. This research was therefore intended to study new different treatments to control spring–summer flush shoots and thus reduce growers’ investments in citrus production. Six different treatments were applied in two experimental and high density orange orchards over two consecutive years: (1) control; (2) topping (mechanical pruning); (3) dichlorprop-p; (4) triclopyr; (5) topping + dichlorprop-p; and (6) topping + triclopyr. The treatment of dichlorprop-p alone reduced the number of summer young shoots in both years. Moreover, these applications did not negatively affect yield or fruit quality. These mechanical methodologies help citrus growers manage the density of flush shoots and reduce hand labor costs in citrus orchards.
... Recent studies suggest sub-lethal effects of field-realistic sulfoxaflor exposure (i.e., exposure levels likely encountered by insects in agriculture) on reproduction, larval development, food consumption and foraging performance in social bumblebees (Bombus terrestris) and honeybees (Apis mellifera) (Siviter and Muth, 2020;Li et al., 2021;Linguadoca et al., 2021;Tamburini et al., 2021a, but see Tamburini et al., 2021b), while impacts on solitary bees, particularly under (semi-)natural conditions, remain largely unexplored (Boff et al., 2021). Since solitary and social bees differ in their physiologies, e.g., detoxification abilities (Hayward et al., 2019), and life-history traits, their sensitivities and levels of pesticide exposure can differ substantially (Arena and Sgolastra, 2014;Sgolastra et al., 2019). ...
Article
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Pesticide exposure is considered a major driver of pollinator decline and the use of neonicotinoid insecticides has been restricted by regulatory authorities due to their risks for pollinators. Impacts of new alternative sulfoxamine-based compounds on solitary bees and their potential interactive effects with other commonly applied pesticides in agriculture remain unclear. Here, we conducted a highly replicated full-factorial semi-field experiment with the solitary bee Osmia bicornis, an important pollinator of crops and wild plants in Europe, and Phacelia tanacetifolia as a model crop. We show that spray applications of the insecticide sulfoxaflor (product Closer) and the fungicide azoxystrobin (product Amistar), both alone and combined, had no significant negative impacts on adult female survival or the production, mortality, sex ratio and body size of offspring when sulfoxaflor was applied five days before crop flowering. Our results indicate that for O. bicornis (1) the risk of adverse impacts of sulfoxaflor (Closer) on fitness is small when applied at least five days before crop flowering and (2) that azoxystrobin (Amistar) has a low potential of exacerbating sulfoxaflor effects under field-realistic conditions.
... Pollinators are responsible for around 35% of the world's food production through pollination process (Potts et al., 2016). Beneficial insects and natural enemies are efficient biocontrol agents and crop pollinators to our agroecosystem (Siviter and Muth, 2020). ...
Article
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Beneficial insects have inevitable contributions for pollination and natural pest control in agriculture. But farmers are struggling to boost up the crop production with chemical application in controlling insect pests enormously without knowing the ultimate consequences. Asia covers 59% of the world's total insecticide usage. Insecticidal exposures share different modes of action with parasitoids and predators. They affect the survival of insects, reduce the capacity of reproduction, change insect behavior, alter the host's availability for parasitism or predation, and sometimes cause direct death. Among the different pesticides, clothianidin and pyridaben recorded in decreasing 86.44% and 83.54% of the honeybee population (86.44 and 83.54%) indicating their toxicity to the bee pollinators reduction. Dimethoate causes the total mortality of aphid parasitoid Aphidius ervi. while Azadirachtin showed 40.43% emergence rate at the dose of LC25 for both the male and female insects, and pyrethrum insecticides have sublethal effects on the lifespan of Chelonus oculator. The nicotinoids, pyrethroid, and organophosphorus groups have a residual impact on the nectar and pollen biology. Residues of imidacloprid @ 19.7μg/kg found in pollen and 6.0μg/kg in honey those potentially affecting on the bee activity. Moreover, sulfoxaflor exposure has extensive sub-lethal effects on wasps, especially available as beneficial insect in the crop fields. This study findings revealed the necessities for future research on the harmful effects of synthetic and natural insecticides on the beneficial insects. Furthermore, it has been suggested that Integrated pest management (IPM) that involves sustainable ecosystem-based pest management techniques Might be an effective and efficient alternative of the insecticides for conserving the beneficial insects in the agroecosystem for the betterment of our future generations.
Article
Ecological interactions between plants and insects are of paramount importance for the maintenance of biodiversity and ecosystem functioning. Herbicides have been long considered a threat to plant and insect populations, but global increases in intensive agriculture and availability of herbicide‐resistant crops have intensified concerns about their full impact on biodiversity. Here, we argue that exposure to sublethal herbicide doses has the potential to alter plant‐insect interactions as a result of disruptions in their chemical communication. This is because herbicides interfere with biosynthetic pathways and phytohormones involved in the production of several classes of plant volatiles that mediate plant‐insect chemical communication. Sublethal herbicide doses can modify morphological and life history plant traits and affect interactions with insects. However, the potential changes in plant volatiles and their consequences for plant‐insect chemical communication have not yet received as much attention. We discuss how target‐site (disruptors of primary metabolism) and non‐target site (synthetic‐auxins) herbicides could alter the production of plant volatiles and disrupt plant‐insect chemical communication. We suggest research avenues to fill in the current gap in our knowledge that might derive recommendations and applied solutions to minimize herbicides’ impacts on plant‐insect interactions and biodiversity. This article is protected by copyright. All rights reserved.
Article
Bees are vital pollinators of crops and wildflowers and as such, wild bee declines threaten food security and functioning ecosystems. One driver of bee declines is the use of systemic insecticides, such as commonly used neonicotinoids. However, rising pest resistance to neonicotinoids, and restrictions on their use in the EU, has increased the demand for replacement insecticides to control crop pests. Flupyradifurone is a novel systemic insecticide that is thought to be relatively ‘bee safe’ although it can be present in the nectar and pollen of bee-attractive crops. Bumblebees rely on learning to forage efficiently, and thus detriments to learning performance may have downstream consequences on their ability to forage. While neonicotinoids negatively influence bumblebee learning and memory, whether this is also the case for their replacements is unclear. Here, we exposed bumblebees (Bombus impatiens) to an acute, field-realistic dose of flupyradifurone before training them to learn either an olfactory or colour association. We found that flupyradifurone impaired bumblebees' learning and memory performance in both olfactory and visual modalities. Flupyradifurone-treated bees were also less motivated to feed. Given the similarity between the detriments to cognition found here and those previously reported for neonicotinoids, this implies that these insecticides may have similar sub-lethal effects on bees. Restrictions on neonicotinoid use are therefore unlikely to benefit bees if novel insecticides like flupyradifurone are used as an alternative, highlighting that current agrochemical risk assessments are not protecting bees from the unwanted consequences of pesticide use. Sub-lethal assessments on non-Apis bees should be made mandatory in agrochemical regulation to ensure that novel insecticides are indeed ‘bee safe’.
Article
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 indirect 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’.
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Pesticides primarily affect target organisms via direct toxicity, but may also alter the feeding behaviors of surviving individuals in ways that alter their effect on host plants. The latter impact is especially important when pests can transmit plant pathogens. The Mediterranean (MED) population of the sweetpotato whitefly Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae) transmits Tomato yellow leaf curl virus (TYLCV), a pathogen that can be economically devastating in field and greenhouse cropping systems. We first assessed the impact of sublethal (LC15) and label concentrations of flupyradifurone, a butenolide-derived insecticide, on the feeding behavior of TYLCV-infected MED on tomato. We next measured the effect of flupyradifurone on plant TYLCV load, vector transmission efficiency, and MED survival. Both the LC15 and label flupyradifurone concentrations dramatically altered MED feeding and caused the near cessation of both salivation and phloem ingestion (necessary for viral transmission and acquisition, respectively). Both concentrations also significantly reduced plant TYLCV load, and the label rate of flupyradifurone sharply decreased TYLCV transmission while killing >99% of MED. As the first report of pesticide-induced changes in the feeding behavior of viruliferous Bemisia, our findings highlight the potential importance of chemically driven feeding cessation in the control of TYLCV and other Bemisia-transmitted plant pathogens.
Article
The aim was to determine, for the first time, concentrations of 7 neonicotinoids (NEOs) and 5 metabolites in Sus scrofa from hunting areas in north-eastern Poland and assess the risk to consumers eating boar meat. 42 wild boar muscle samples were collected over a one-year period. The concentrations of 12 NEOs were determined by a fully validated LC-ESI-MS/MS protocol based on ultrasonic, freezing and cleanup EMR–lipid sample preparation. NEOs were present in over 83% of samples, 17% had no residue, and one pesticide was present in 36% of samples. Most often found were: clothianidin (35%), acetamiprid and imidacloprid (33%), thiacloprid (31%), thiamethoxam (9%), and the average concentrations were (ng g⁻¹): thiacloprid 6.2 > imidacloprid 5.7 > acetamiprid 4.6 > clothianidin 2.2 > thiacloprid 1.6 > thiamethoxam 1.0. Multi-residue samples were found, one with 7 and one with 5 NEOs. Two NEOs were present in 24%; 3 in 39% and 4 in 10% of samples. In the metabolic degradation of acetamiprid, imidacloprid and thiacloprid, it was observed that metabolites account for no more than 8.5% of the measured parent substance. Acetamiprid-n-desmethyl was noted most often (21%). Due to the detection of NEOs in a large proportion of samples, chronic and acute risk assessment were performed. The estimated chronic and acute risk for consumers from NEOs neonicotinoids through the consumption of wild boar was very low and amounted to respectively 0.02% of ADI and 0.86% of ARfD.
Article
The present work is the first extensive study of large-scale pesticides research in wild animals. The investigation covered three game species: wild boar (n=42), roe deer (n=79) and deer (n=15) collected from north-eastern Poland. To characterize the 480 pesticides in muscle samples, LC-GC-MS/MS techniques were used. A total of 28 compounds were detected: 5 neonicotinoids, 6 organochlorine and 5 other insecticides, 9 fungicides and 4 herbicides, in the range of 0.1-85.3 ng g⁻¹. Over four hundred detections were done. The highest mean concentrations were as follows: anthraquinone (85.3 ng g⁻¹)>DDT-p,p’ (4.6 ng g⁻¹)>imidacloprid (4.3 ng g⁻¹)>permethrin (3.6 ng g⁻¹)>thiacloprid (2.8 ng g⁻¹). DDT and metabolites were the most frequently detected, followed by acetamiprid, tebuconazole, clothianidin and imidacloprid. Overall, 92% samples with residues were recorded, including 100% of wild boar, 88% of roe deer and 86% of deer. More than one pesticide (up to 9) was found in over 73% of the tested samples. The estimated chronic and acute risk to consumers of venison were very low (below 1% ADI and ARfD). This interdisciplinary study may be helpful for estimating ecological risk to wild animals and risk to consumers of wild animal products, and also as a source of biomonitoring data.
Article
The accumulating scientific evidence on global insect and pollinator decline is fuelling calls for pollinator conservation policies. A broad range of regulating and incentivising policies is undoubtedly needed to address the diverse threats to pollinator abundance and diversity, but implementing policies and regulations is beset by socio-political challenges. Lessons could be learned from the past and current applications of concepts central to biodiversity conservation. Given the uncertainties and data gaps, the concept of the Precautionary Principle (PP) is particularly important. The PP means that when it is scientifically plausible that human activities may lead to morally unacceptable harm, actions shall be taken to avoid or diminish that harm: uncertainty should not be an excuse to delay action. This paper reviews the role of the PP in pollinator conservation. The current research front is fragmented: the PP is briefly mentioned as relevant in literature on biodiversity conservation because of the scientific uncertainties regarding insect decline and their diverse drivers. A separate strand of literature contains studies on specific cases where the PP has played a role in the regulation of specific threats to pollinators: systemic insecticides and global trade in bees. Although limited to two significant threats to pollinator abundance and diversity, these studies provide important lessons on the challenges of implementing precautionary pollinator conservation policies and underline socio-political aspects of the ‘human-dimensions’ of pollinator conservation. Specifically, they highlight that ambiguity is a greater challenge than scientific uncertainty, which may be heightened when policies are intended to regulate specific economic sectors. We suggest that more attention should be paid to the discrepancy between the PP as formally included in policies or regulations and its inadequate implementation (too little too late) in a context of scientific uncertainty and societal conflict.
Article
Crops that offer multiple types of value, for example, in terms of economy, culture, and health, frequently lack information on the basic ecological interactions that play a significant role in their persistence. Chayote (Sechium edule, Cucurbitaceae), a widespread squash valued for its nutritious fruit, is one example. We aimed at describing the assemblage of flower visitors to this crop at 2400 m where stingless bees, reported as the main pollinators, are naturally absent. We implemented flower exclusions, performed field observations, and inspection of pollen loads of captured visitors to be able to draw distinctions between primary and secondary pollinators. We recorded a total of 60 species or morphospecies of insects visiting the flowers. Bees, wasps, and flies, present in all sites and consistently carrying abundant pollen, are the main pollinators of S. edule at high altitudes. Our study adds to the building evidence of the fundamental role that native bees and wasps play as crop pollinators in subsistence farming. Basic ecological knowledge is essential to inform agricultural management policies and to foresee preventable food scarcity problems, especially in view of climate change scenarios that predict drastic alterations in plant geographical distributions.
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Essential oils (EOs) are increasingly used as biopesticides due to their insecticidal potential. This study addresses their non-target effects on a biological control agent: the egg parasitoid Trichogramma evanescens. In particular, we tested whether EOs affected parasitoid fitness either directly, by decreasing pre-imaginal survival, or indirectly, by disrupting parasitoids' orientation abilities. The effect of Anise, Fennel, Sweet orange, Basil, Coriander, Oregano, Peppermint, Mugwort, Rosemary and Thyme EOs were studied on five strains of T. evanescens. Specific experimental setups were developed, and data obtained from image analysis were interpreted with phenomenological models fitted with Bayesian inference. Results highlight the fumigant toxicity of EOs on parasitoid development. Anise, Fennel, Basil, Coriander, Oregano, Peppermint and Thyme EOs are particularly toxic and drastically reduce the emergence rate of T. evanescens. Most EOs also affect parasitoid behavior: (i) Basil, Coriander, Oregano, Peppermint, Mugwort and Thyme EOs are highly repellent for naive female parasitoids; (ii) Anise and Fennel EOs can have repellent to attractive effects depending on strains; and (iii) Sweet orange, Oregano and Rosemary EOs have no detectable impact on orientation behavior. This study shows that EOs fumigation have non-target effects on egg parasitoids. This highlights the need to cautiously precise the deployment framework of biopesticides in an agroecological perspective.
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Determination of how neonicotinoid ingestion affects the foraging behaviour of flower-visiting animals, and using Optimal Foraging Theory to assess the nature and extent of consequent changes to foraging efficiency, provide a novel approach for understanding how neonic ingestion affects the cognitive abilities of these animals, and their ultimate reproductive success. Neonicotinoids (neonics for short) are used worldwide as insecticides to protect agricultural crops, but may be ingested by non-target flower-visiting animals, such as bees, with negative impacts on their cognitive abilities and consequent adverse effects on their foraging behaviour, reproduction and pollination services. Optimal Foraging Theory may help to understand such effects as it hypothesises that nectar-feeding animals, including bees, will adopt foraging behaviour that maximises net rate of energy intake. Simple models of foraging movements exist but require further development to be useful in this regard. Observed movement patterns could then be compared with predicted patterns, derived from such models, and compared between neonicotinoid-affected and control individuals, with the expectation that control individuals will forage optimally, while neonicotinoid-affected individuals will not exhibit such behaviour and will exhibit reduced foraging success. However, there has been little attempt to develop and test predictions for cognitive foragers, like bees, that are moving between flowers or flower clusters, potentially limiting our ability to manage neonic-use to control agricultural pests. Addressing this gap should lead to enhanced knowledge and understanding of the impacts of neonics on non-target animals, along with other possible flow-on environmental impacts, including possible reductions in pollinator abundance and hence the harvest yields of crops requiring pollination, and could lead to refinements in policy and procedure for future use of neonics to control agricultural pests. The same issues apply to other insecticides and to interactions amongst insecticides.
Article
Abstract 1) Many wild bee species interact with soil either as a nesting substrate or material. These soil interactions create a risk of exposure to agrochemicals such as imidacloprid or other neonicotinoid pesticides that can persist in soil for months after application. At the landscape level, concentrations of imidacloprid residue in soil are limited to the immediate treatment area, and thus risks to soil-interacting bees could be low if they avoid contaminated soils. 2) We utilized Osmia lignaria (Say), a solitary cavity nesting bee which collects mud to partition and seal nests, and conducted two laboratory experiments to test whether nesting females select or avoid soils containing various levels of imidacloprid residue. For the first experiment, we assessed behavioral responses of females to treated soil utilizing a choice arena and pairing various choices of soil with imidacloprid residues ranging between 0 and 780 ppb. For the second experiment, we developed a laboratory assay to assess soil selection of actively nesting O. lignaria, by providing choices of contaminated soil between 0 and 100 ppb and 0 and 1,000 ppb to nesting females. 3) We found no evidence that O. lignaria females avoided any level of imidacloprid contamination, even at the highest residue level (1,000 ppb) in both the experiments, which may have implications for risk. The in situ nesting methodology developed in this study has future applications for research on soil or pollen preferences of cavity nesting Osmia species, and potential for breeding of O. lignaria in laboratory.
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Insecticides are pesticides used to control insects in agriculture, ornamental gardens, homes, and veterinary medicine. Although the toxic effects on the environment and the health of living beings are not fully understood, these pesticides have become the first options for crop protection in agriculture. After herbicides, insecticides are the most extensively used pesticides in agriculture, with large quantities consumed on every continent, primarily in America. Chlorpyrifos, carbaryl, and imidacloprid are among the top ten most used insecticides. Amidst organophosphates, chlorpyrifos has been reported to be used in over fifty food crops. Carbaryl is a carbamate employed as an insecticide, fungicide, herbicide, and nematicide. Similarly, neonicotinoids are the most used insecticide on a global scale. Neonicotinoids include imidacloprid, the second most frequently used pesticide, surpassed only by glyphosate. It is used because it is less toxic to humans. However, insects appear to be less resistant to its compounds. Evidence suggests that these insecticides persist in soils for a long time and have neurotoxic effects in animal species not intended to receive its consequences. Thus, this chapter’s aim is to describe these three pesticides effects and contrast them with the most recent findings regarding their neurotoxic effects in various animal species.
Article
Sulfoxaflor and flupyradifurone, two pesticides belonging to sulfoximins and butenolides, are widely used to treat crops and fruits. In order to amplify the detection of pollutants, we aimed to identify also molecules deriving from the parent pesticides. We studied their photoinduced transformation and identified their main transformation products by applying a laboratory simulation and by employing HPLC-HRMS to characterize them. We detected three transformation products from sulfoxaflor, whose formation involved the conversion of cyanamide group into a ureic group and the detachment of the side chain. Flupyradifurone transformation proceeded through the formation of seven transformation products and three of them were recognized in this study for the first time; it involved hydroxylation and breakage of the molecule with the detachment of the pyridine or furan ring. These results will allow enlarging the extent of TPs to be screened in food matrices. Pesticides and their transformation products were then determined in 67 samples of fruits, leaves, honey and pollen by applying QuECHERs for sample pre-treatment and HPLC-MS/MS for their quantification. The presence of flupyradifurone was detected in different samples of honey at concentration level of 10–15 μg/kg.
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Few human data on exposure and toxicity are available on neonicotinoids and neonicotinoid-like compounds (NNIs), an important group of insecticides worldwide. Specifically, exposure assessment of humans by biomonitoring remains a challenge due to the lack of appropriate biomarkers. We investigated the human metabolism and metabolite excretion in urine of acetamiprid (ACE), clothianidin (CLO), flupyradifurone (FLUP), imidacloprid (IMI), sulfoxaflor (SULF), thiacloprid (THIAC) and thiamethoxam (THIAM) after single oral dosages at the currently acceptable daily intake levels of the European Food Safety Authority. Consecutive post-dose urine samples were collected up to 48 h. Suspect screening of tentative metabolites was carried out by liquid chromatography–high-resolution mass spectrometry. Screening hits were identified based on their accurate mass, isotope signal masses and ratios, product ion spectra, and excretion kinetics. We found, with the exception of SULF, extensive metabolization of NNIs to specific metabolites which were excreted next to the parent compounds. Overall, 24 metabolites were detected with signal intensities indicative of high metabolic relevance. Phase-I metabolites were predominantly derived by mono-oxidation (such as hydroxy-FLUP, -IMI, and -THIAC) and by oxidative N-desalkylation (such as N-desdifluoroethyl-FLUP and N-desmethyl-ACE, -CLO and -THIAM). IMI-olefin, obtained by dehydration of hydroxylated IMI, was identified as a major metabolite of IMI. SULF was excreted unchanged in urine. Previously reported metabolites of NNIs such as 6-chloronicotinic acid or 2-chlorothiazole-4-carboxylic acid and their glycine derivatives were detected either at low signal intensities or not at all and seem less relevant for human biomonitoring. Our highly controlled approach provides specific insight into the human metabolism of NNIs and suggests suitable biomarkers for future exposure assessment at environmentally relevant exposures.
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Insect nervous systems offer unique advantages for studying interactions between sensory systems and behavior, given their complexity with high tractability. By examining the neural coding of salient environmental stimuli and resulting behavioral output in the context of environmental stressors, we gain an understanding of the effects of these stressors on brain and behavior and provide insight into normal function. The implication of neonicotinoid (neonic) pesticides in contributing to declines of nontarget species, such as bees, has motivated the development of new compounds that can potentially mitigate putative resistance in target species and declines of nontarget species. We used a neuroethologic approach, including behavioral assays and multineuronal recording techniques, to investigate effects of imidacloprid (IMD) and the novel insecticide sulfoxaflor (SFX) on visual motion-detection circuits and related escape behavior in the tractable locust system. Despite similar LD 50 values, IMD and SFX evoked different behavioral and physiological effects. IMD significantly attenuated collision avoidance behaviors and impaired responses of neural populations, including decreases in spontaneous firing and neural habituation. In contrast, SFX displayed no effect at a comparable sublethal dose. These results show that neonics affect population responses and habituation of a visual motion detection system. We propose that differences in the sublethal effects of SFX reflect a different mode of action than that of IMD. More broadly, we suggest that neuroethologic assays for comparative neurotoxicology are valuable tools for fully addressing current issues regarding the proximal effects of environmental toxicity in nontarget species.
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Dramatic losses of pollinating insects have become of global concern, as they threaten not only key ecosystem services but also human food production. Recent research provided evidence that interactions between ecological stressors are drivers of declining pollinator health and responsible for observed population collapses. We used the honeybee Apis mellifera and conducted a series of experiments to test for long-term effects of a single short exposure to the agricultural pesticide flupyradifurone to a second environmental stressor later in life. To do this, we exposed individuals during their larval development or early adulthood to sublethal dosages of flupyradifurone (0.025 μg for larvae and 0.645 μg for imagos), either pure or as part of an agricultural formulation (Sivanto). We afterwards exposed bees to a second ecological stressor infecting individuals with 10,000 spores of the fungal gut parasite Nosema ceranae. We found that pesticide exposures significantly reduced survival of bees and altered the expression of several immune and detoxification genes. The ability of bees to respond to these latter effects differed significantly between colonies, offering opportunities to breed bees with elevated levels of pesticide tolerance in the future. We conclude that short episodes of sublethal pesticide exposures during development are sufficient to trigger effects later in life and could therefore contribute to the widespread declines in bee health.
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1.Honeybees (Apis mellifera) and other pollinating insects suffer from pesticides in agricultural landscapes. Flupyradifurone is the active ingredient of a novel pesticide by the name of “Sivanto”, introduced by Bayer AG (Crop Science Division, Monheim am Rhein, Germany). It is recommended against sucking insects and marketed as "harmless" to honeybees. Flupyradifurone binds to nicotinergic acetylcholine receptors like neonicotinoids, but it has a different mode of action. So far, little is known on how sublethal flupyradifurone doses affect honeybees. 2.We chronically applied a sublethal and field realistic concentration of flupyradifurone to test for long‐term effects on flight behavior using radio frequency identification (RFID). We examined Hematoxylin/Eosin stained brains of flupyradifurone‐treated bees to investigate possible changes in brain morphology and brain damage. 3.A field realistic flupyradifurone dose of approximately 1.0 μg/bee/day significantly increased mortality. Pesticide‐treated bees initiated foraging earlier than control bees. No morphological damage in the brain was observed. 4.Synthesis and applications. The early onset of foraging induced by a chronical application of flupyradifurone could be disadvantageous for honeybee colonies, reducing the period of in‐hive tasks and life expectancy of individuals. Radio frequency identification technology (RFID) is a valuable tool for studying pesticide effects on life‐time foraging behavior of insects.
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Bees are exposed to a wide range of multiple chemicals “chemical mixtures” from anthropogenic (e.g. plant protection products or veterinary products) or natural origin (e.g. mycotoxins, plant toxins). Quantifying the relative impact of multiple chemicals on bee health compared with other environmental stressors (e.g. varroa, viruses, and nutrition) has been identified as a priority to support the development of holistic risk assessment methods. Here, extensive literature searches and data collection of available laboratory studies on combined toxicity data for binary mixtures of pesticides and non-chemical stressors has been performed for honey bees (Apis mellifera), wild bees (Bombus spp.) and solitary bee species (Osmia spp.). From 957 screened publications, 14 publications provided 218 binary mixture toxicity data mostly for acute mortality (lethal dose: LD50) after contact exposure (61%), with fewer studies reporting chronic oral toxicity (20%) and acute oral LC50 values (19%). From the data collection, available dose response data for 92 binary mixtures were modelled using a Toxic Unit (TU) approach and the MIXTOX modelling tool to test assumptions of combined toxicity i.e. concentration addition (CA), and interactions (i.e. synergism, antagonism). The magnitude of interactions was quantified as the Model Deviation Ratio (MDR). The CA model applied to 17% of cases while synergism and antagonism were observed for 72% (MDR > 1.25) and 11% (MDR
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Recent reports of local extinctions of arthropod species 1 , and of massive declines in arthropod biomass 2 , point to land-use intensification as a major driver of decreasing biodiversity. However, to our knowledge, there are no multisite time series of arthropod occurrences across gradients of land-use intensity with which to confirm causal relationships. Moreover, it remains unclear which land-use types and arthropod groups are affected, and whether the observed declines in biomass and diversity are linked to one another. Here we analyse data from more than 1 million individual arthropods (about 2,700 species), from standardized inventories taken between 2008 and 2017 at 150 grassland and 140 forest sites in 3 regions of Germany. Overall gamma diversity in grasslands and forests decreased over time, indicating loss of species across sites and regions. In annually sampled grasslands, biomass, abundance and number of species declined by 67%, 78% and 34%, respectively. The decline was consistent across trophic levels and mainly affected rare species; its magnitude was independent of local land-use intensity. However, sites embedded in landscapes with a higher cover of agricultural land showed a stronger temporal decline. In 30 forest sites with annual inventories, biomass and species number-but not abundance-decreased by 41% and 36%, respectively. This was supported by analyses of all forest sites sampled in three-year intervals. The decline affected rare and abundant species, and trends differed across trophic levels. Our results show that there are widespread declines in arthropod biomass, abundance and the number of species across trophic levels. Arthropod declines in forests demonstrate that loss is not restricted to open habitats. Our results suggest that major drivers of arthropod decline act at larger spatial scales, and are (at least for grasslands) associated with agriculture at the landscape level. This implies that policies need to address the landscape scale to mitigate the negative effects of land-use practices.
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Sulfoximine-based insecticides, such as sulfoxaflor, are of increasing global importance and have been registered for use in 81 countries, offering a potential alternative to neonicotinoid insecticides.Previous studies have demonstrated that sulfoxaflor exposure can have a negative impact on the reproductive output of bumblebee colonies, but the specific life-history variables that underlie these effects remain unknown.Here, we used a microcolony-based protocol to assess the sub-lethal effects of chronic sulfoxaflor exposure on egg laying, larval production, ovary development, sucrose consumption, and mortality in bumblebees. Following a pre-registered design, we exposed colonies to sucrose solutions containing 0, 5, 10 and 250ppb of sulfoxaflor. Exposure at 5 ppb has been previously shown to negatively impact colony reproductive success.Our results showed that sulfoxaflor exposure at 5 ppb (lowest exposure tested) reduced the number of eggs found within the microcolonies (Hedge's d = -0.37), with exposed microcolonies also less likely to produce larvae (Hedge's d = -0.36). Despite this, we found no effect of sulfoxaflor exposure on ovarian development. Sulfoxaflor-exposed bumblebees consumed less sucrose solution, potentially driving the observed reduction in egg laying. Policy implications. Regulatory bodies such as the European Food Safety Authority (EFSA) are under increasing pressure to consider the potential impact of insecticides on wild bees, such as bumblebees, but sublethal effects can go undetected at lower-tier testing. In identifying just such an effect for bumblebees exposed to sulfoxaflor, this study highlights that microcolony-based protocols are a useful tool that could be implemented within an ecotoxicology framework. Furthermore, the results provide evidence for potentially negative consequences of pollinator exposure to an insecticide that is currently undergoing the licensing process in several EU member states.
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Recent research has shown that several managed bee species have specific P450 enzymes that are preadapted to confer intrinsic tolerance to some insecticides including certain neonicotinoids. However, the universality of this finding across managed bee pollinators is unclear. Here we show that the alfalfa leafcutter bee, Megachile rotundata, lacks such P450 enzymes and is >2,500-fold more sensitive to the neonicotinoid thiacloprid and 170-fold more sensitive to the butenolide insecticide flupyradifurone than other managed bee pollinators. These findings have important implications for the safe use of insecticides in crops where M. rotundata is used for pollination, and ensuring that regulatory pesticide risk assessment frameworks are protective of this species.
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Pesticide use is one of the main causes of pollinator declines in agricultural ecosystems. Traditionally, most laboratory studies on bee ecotoxicology test acute exposure to single compounds. However, under field conditions, bees are often chronically exposed to a variety of chemicals, with potential synergistic effects. We studied the effects of field-realistic concentrations of three pesticides measured in pollen and nectar of commercial melon fields on the solitary bee Osmia bicornis L. We orally exposed females of this species throughout their life span to 8 treatments combining two neonicotinoid insecticides (acetamiprid, imidacloprid) and a triazole fungicide (myclobutanil) via pollen and sugar syrup. We measured pollen and syrup consumption, longevity, ovary maturation and thermogenesis. Pesticide intake was three orders of magnitude higher via syrup than pollen. At the tested concentrations, no synergistic effects emerged, and we found no effects on longevity and ovary maturation. However, all treatments containing imidacloprid resulted in suppressed syrup consumption and drastic decreases in thoracic temperature and bee activity. Our results have important implications for pesticide regulation. If we had measured only lethal effects we would have wrongly concluded that the pesticide combinations containing imidacloprid were safe to O. bicornis. The incorporation of tests specifically intended to detect sublethal effects in bee risk assessment schemes should be an urgent priority. In this way, the effects of pesticide exposure on the dynamics of bee populations in agroecosystems will be better assessed. Bees, both wild and managed, play an essential role in crop pollination and food production stability 1-3. Yet, especially in intensively farmed areas, bee populations often face adverse environmental conditions, including destruction of nesting habitats, scarcity of floral resources and intensive pesticide presence 4-7 .
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Currently honeybees are the sole model insect pollinator for regulatory pesticide risk assessments globally. Here we question whether this surrogacy approach provides adequate protection against potential non-target impacts of pesticide exposure for the wide diversity of insect pollinators on which agricultural production and wild plant ecosystems depend.
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Systemic insecticides such as neonicotinoids and sulfoximines can be present in the nectar and pollen of treated crops, through which foraging bees can become acutely exposed. Research has shown that acute, field realistic dosages of neonicotinoids can negatively influence bee learning and memory, with potential consequences for bee behaviour. As legislative reassessment of neonicotinoid use occurs globally, there is an urgent need to understand the potential risk of other systemic insecticides. Sulfoxaflor, the first branded sulfoximine-based insecticide, has the same mode of action as neonicotinoids, and may potentially replace them over large geographical ranges. Here we assessed the impact of acute sulfoxaflor exposure on performance in two paradigms that have previously been used to illustrate negative impacts of neonicotinoid pesticides on bee learning and memory. We assayed whether acute sulfoxaflor exposure influences (a) olfactory conditioning performance in both bumblebees ( Bombus terrestris ) and honeybees ( Apis mellifera ), using a proboscis extension reflex assay, and (b) working memory performance of bumblebees, using a radial-arm maze. We found no evidence to suggest that sulfoxaflor influenced performance in either paradigm. Our results suggest that despite a shared mode of action between sulfoxaflor and neonicotinoid-based insecticides, widely-documented effects of neonicotinoids on bee cognition may not be observed with sulfoxaflor, at least at acute exposure regimes.
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Pollination is a critical ecosystem service underpinning the productivity of agricultural systems across the world. Wild insect populations provide a substantial contribution to the productivity of many crops and seed set of wild flowers. However, large-scale evidence on species-specific trends among wild pollinators are lacking. Here we show substantial inter-specific variation in pollinator trends, based on occupancy models for 353 wild bee and hoverfly species in Great Britain between 1980 and 2013. Furthermore, we estimate a net loss of over 2.7 million occupied 1 km² grid cells across all species. Declines in pollinator evenness suggest that losses were concentrated in rare species. In addition, losses linked to specific habitats were identified, with a 55% decline among species associated with uplands. This contrasts with dominant crop pollinators, which increased by 12%, potentially in response agri-environment measures. The general declines highlight a fundamental deterioration in both wider biodiversity and non-crop pollination services.
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Neonicotinoids are widely-used pesticides implicated in the decline of bees, known to have sub-lethal effects on bees’ foraging and colony performance. One proposed mechanism for these negative effects is impairment to bees’ ability to learn floral associations. However, the effects of neonicotinoids on learning performance have largely been addressed using a single protocol, where immobilized bees learn an association based on a single sensory modality. We thus have an incomplete understanding of how these pesticides affect bee learning in more naturalistic foraging scenarios. We carried out the first free-foraging study into the effects of acute exposure of a neonicotinoid (imidacloprid) on bumblebees’ (Bombus impatiens) ability to learn associations with visual stimuli. We uncovered dose-dependent detrimental effects on motivation to initiate foraging, amount of nectar collected, and initiation of subsequent foraging bouts. However, we did not find any impairment to bees’ ability to learn visual associations. While not precluding the possibility that other forms of learning are impaired, our findings suggest that some of the major effects of acute neonicotinoid exposure on foraging performance may be due to motivational and/or sensory impairments. In light of these findings, we discuss more broadly how pesticide effects on pollinator cognition might be studied.
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The honeybee (Apis mellifera L.) is an important pollinator and a model for pesticide effects on insect pollinators. The effects of agricultural pesticides on honeybee health have therefore raised concern. Bees can be exposed to multiple pesticides that may interact synergistically, amplifying their side effects. Attention has focused on neonicotinoid pesticides, but flupyradifurone (FPF) is a novel butenolide insecticide that is also systemic and a nicotinic acetylcholine receptor (nAChR) agonist. We therefore tested the lethal and sublethal toxic effects of FPF over different seasons and worker types, and the interaction of FPF with a common SBI fungicide, propiconazole. We provide the first demonstration of adverse synergistic effects on bee survival and behaviour (poor coordination, hyperactivity, apathy) even at FPF field-realistic doses (worst-case scenarios). Pesticide effects were significantly influenced by worker type and season. Foragers were consistently more susceptible to the pesticides (4-fold greater effect) than in-hive bees, and both worker types were more strongly affected by FPF in summer as compared with spring. Because risk assessment (RA) requires relatively limited tests that only marginally address bee behaviour and do not consider the influence of bee age and season, our results raise concerns about the safety of approved pesticides, including FPF. We suggest that pesticide RA also test for common chemical mixture synergies on behaviour and survival.
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Honeybees and other pollinators are threatened by changing landscapes and pesticides resulting from intensified agriculture. In 2018 the European Union prohibited the outdoor use of three neonicotinoid insecticides due to concerns about pollinators. A new pesticide by the name of “Sivanto” was recently released by Bayer AG. Its active ingredient flupyradifurone binds to the nicotinic acetylcholine receptor (AchR) in the honeybee brain, similar to neonicotinoids. Nevertheless, flupyradifurone is assumed to be harmless for honeybees and can even be applied on flowering crops. So far, only little has been known about sublethal effects of flupyradifurone on honeybees. Intact motor functions are decisive for numerous behaviors including foraging and dancing. We therefore selected a motor assay to investigate in how far sublethal doses of this pesticide affect behavior in young summer and long-lived winter honeybees. Our results demonstrate that flupyradifurone (830 µmol/l) can evoke motor disabilities and disturb normal motor behavior after a single oral administration (1.2 µg/bee). These effects are stronger in long-lived winter bees than in young summer bees. After offering an equal amount of pesticide (1.0–1.75 µg) continuously over 24 h with food the observed effects are slighter. For comparisons we repeated our experiments with the neonicotinoid imidacloprid. Intriguingly, the alterations in behavior induced by this pesticide (4 ng/bee) were different and longer-lasting compared to flupyradifurone, even though both substances bind to nicotinic acetylcholine receptors.
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Abstract In accordance with Article 6 of Regulation (EC) No 396/2005, the applicant Dow AgroSciences submitted a request to the competent national authority in Ireland to modify the existing maximum residue levels (MRLs) for the active substance sulfoxaflor in various crops, including limes imported from Australia. The data submitted in support of the request were found to be sufficient to derive MRL proposals for limes, cauliflowers, Brussels sprouts, kales, spinaches and similar leaves, herbs and edible flowers, beans without pods, peas with pods, oat, rye and triticale (wheat). Adequate analytical methods for enforcement are available to control the residues of sulfoxaflor on the commodities under consideration. Based on the risk assessment results, EFSA concluded that the use of sulfoxaflor according to the intended good agricultural practices is unlikely to present a risk to consumers’ health.
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Current pesticide risk assessment for bees relies on a single (social) species, the western honey bee, Apis mellifera L. (Hymenoptera: Apidae). However, most of the >20,000 bee species worldwide are solitary. Differences in life history traits between solitary bees (SB) and honey bees (HB) are likely to determine differences in routes and levels of pesticide exposure. The objectives of this review are to: 1) compare SB and HB life history traits relevant for risk assessment; 2) summarize current knowledge about levels of pesticide exposure for SB and HB; 3) identify knowledge gaps and research needs; 4) evaluate whether current HB risk assessment schemes cover routes and levels of exposure of SB; and 5) identify potential SB model species for risk assessment. Most SB exposure routes seem well covered by current HB risk assessment schemes. Exceptions to this are exposure routes related to nesting substrates and nesting materials used by SB. Exposure via soil is of particular concern because most SB species nest underground. Six SB species (Hymenoptera: Megachilidae-Osmia bicornis L., O. cornifrons Radoszkowski, O. cornuta Latreille, O. lignaria Say, Megachile rotundata F., and Halictidae-Nomia melanderi Cockerell) are commercially available and could be used in risk assessment. Of these, only N. melanderi nests underground, and the rest are cavity-nesters. However, the three Osmia species collect soil to build their nests. Life history traits of cavity-nesting species make them particularly suitable for semifield and, to a lesser extent, field tests. Future studies should address basic biology, rearing methods and levels of exposure of ground-nesting SB species.
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A number of studies indicate that tropical arthropods should be particularly vulnerable to climate warming. If these predictions are realized, climate warming may have a more profound impact on the functioning and diversity of tropical forests than currently anticipated. Although arthropods comprise over two-thirds of terrestrial species, information on their abundance and extinction rates in tropical habitats is severely limited. Here we analyze data on arthropod and insectivore abundances taken between 1976 and 2012 at two midelevation habitats in Puerto Rico’s Luquillo rainforest. During this time, mean maximum temperatures have risen by 2.0 °C. Using the same study area and methods employed by Lister in the 1970s, we discovered that the dry weight biomass of arthropods captured in sweep samples had declined 4 to 8 times, and 30 to 60 times in sticky traps. Analysis of long-term data on canopy arthropods and walking sticks taken as part of the Luquillo Long-Term Ecological Research program revealed sustained declines in abundance over two decades, as well as negative regressions of abundance on mean maximum temperatures. We also document parallel decreases in Luquillo’s insectivorous lizards, frogs, and birds. While El Niño/Southern Oscillation influences the abundance of forest arthropods, climate warming is the major driver of reductions in arthropod abundance, indirectly precipitating a bottom-up trophic cascade and consequent collapse of the forest food web.
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Pollinators in agroecosystems are often exposed to pesticide mixtures. Even at low concentrations, the effects of these mixtures on bee populations are difficult to predict due to potential synergistic interactions. In this paper, we orally exposed newly emerged females of the solitary beeOsmia bicornis to environmentally realistic levels of clothianidin (neonicotinoid insecticide) and propiconazole (fungicide), singly and in combination. The amount of feeding solution consumed was highest in bees exposed to the neonicotinoid, and lowest in bees exposed to the pesticide mixture. Ovary maturation and longevity of bees of the neonicotinoid and the fungicide treatments did not differ from those of control bees. By contrast, bees exposed to the pesticide mixture showed slow ovary maturation and decreased longevity. We found a synergistic interaction between the neonicotinoid and the fungicide on survival probability. We also found an interaction between treatment and emergence time (an indicator of physiological condition) on longevity. Longevity was negatively correlated to physiological condition only in the fungicide and the mixture treatments. Delayed ovary maturation and premature death imply a shortened nesting period (highly correlated to fecundity in Osmia). Our findings provide a mechanism to explain the observed dynamics of solitary bee populations exposed to multiple chemical residues in agricultural environments.
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Intensive agriculture currently relies on pesticides to maximize crop yield1,2. Neonicotinoids are the most widely used insecticides globally3, but increasing evidence of negative impacts on important pollinators4-9 and other non-target organisms10 has led to legislative reassessment and created demand for the development of alternative products. Sulfoximine-based insecticides are the most likely successor11, and are either licensed for use or under consideration for licensing in several worldwide markets3, including within the European Union12, where certain neonicotinoids (imidacloprid, clothianidin and thiamethoxam) are now banned from agricultural use outside of permanent greenhouse structures. There is an urgent need to pre-emptively evaluate the potential sub-lethal effects of sulfoximine-based pesticides on pollinators11, because such effects are rarely detected by standard ecotoxicological assessments, but can have major impacts at larger ecological scales13-15. Here we show that chronic exposure to the sulfoximine-based insecticide sulfoxaflor, at dosages consistent with potential post-spray field exposure, has severe sub-lethal effects on bumblebee (Bombus terrestris) colonies. Field-based colonies that were exposed to sulfoxaflor during the early growth phase produced significantly fewer workers than unexposed controls, and ultimately produced fewer reproductive offspring. Differences between the life-history trajectories of treated and control colonies first became apparent when individuals exposed as larvae began to emerge, suggesting that direct or indirect effects on a small cohort may have cumulative long-term consequences for colony fitness. Our results caution against the use of sulfoximines as a direct replacement for neonicotinoids. To avoid continuing cycles of novel pesticide release and removal, with concomitant impacts on the environment, a broad evidence base needs to be assessed prior to the development of policy and regulation.
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Most insecticides are insect neurotoxins. Evidence is emerging that sublethal doses of these neurotoxins are affecting the learning and memory of both wild and managed bee colonies, exacerbating the negative effects of pesticide exposure and reducing individual foraging efficiency. Variation in methodologies and interpretation of results across studies has precluded the quantitative evaluation of these impacts that is needed to make recommendations for policy change. It is not clear whether robust effects occur under acute exposure regimes (often argued to be more field‐realistic than the chronic regimes upon which many studies are based), for field‐realistic dosages, and for pesticides other than neonicotinoids. Here we use meta‐analysis to examine the impact of pesticides on bee performance in proboscis extension‐based learning assays, the paradigm most commonly used to assess learning and memory in bees. We draw together 104 (learning) and 167 (memory) estimated effect sizes across a diverse range of studies. We detected significant negative effects of pesticides on learning and memory (i) at field realistic dosages, (ii) under both chronic and acute application, and (iii) for both neonicotinoid and non‐neonicotinoid pesticides groups. We also expose key gaps in the literature that include a critical lack of studies on non‐Apis bees, on larval exposure (potentially one of the major exposure routes), and on performance in alternative learning paradigms. Policy implications. Procedures for the registration of new pesticides within EU member states now typically require assessment of risks to pollinators if potential target crops are attractive to bees. However, our results provide robust quantitative evidence for subtle, sublethal effects, the consequences of which are unlikely to be detected within small‐scale prelicensing laboratory or field trials, but can be critical when pesticides are used at a landscape scale. Our findings highlight the need for long‐term postlicensing environmental safety monitoring as a requirement within licensing policy for plant protection products.
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Urbanization represents a rapidly growing driver of land-use change. While it is clear that urbanization impacts species abundance and diversity, direct effects of urban land use on animal reproductive success are rarely documented. Here, we show that urban land use is linked to long-term colony reproductive output in a key pollinator. We reared colonies from wild-caught bumblebee (Bombus terrestris) queens, placed them at sites characterized by varying degrees of urbanization from inner city to rural farmland and monitored the production of sexual offspring across the entire colony cycle. Our land-use cluster analysis identified three site categories, and this categorization was a strong predictor of colony performance. Crucially, colonies in the two clusters characterized by urban development produced more sexual offspring than those in the cluster dominated by agricultural land. These colonies also reached higher peak size, had more food stores, encountered fewer parasite invasions and survived for longer. Our results show a link between urbanization and bumblebee colony reproductive success, supporting the theory that urban areas provide a refuge for pollinator populations in an otherwise barren agricultural landscape.
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Due to intensive agriculture honeybees are threatened by various pesticides. The use of one group of them, the neonicotinoids, was recently restricted by the European Union. These chemicals bind to the nicotinic acetylcholine receptor (nAchR) in the honeybee brain. Recently, Bayer AG released a new pesticide by the name of "Sivanto" against sucking insects. It is assumed to be harmless for honeybees, although its active ingredient, flupyradifurone, binds nAchR similar to the neonicotinoids. We investigated if this pesticide affects the taste for sugar and cognitive performance in honeybee foragers. These bees are directly exposed to the pesticide while foraging for pollen or nectar. Our results demonstrate that flupyradifurone can reduce taste and appetitive learning performance in honeybees foraging for pollen and nectar, although only the highest concentration had significant effects. Most likely, honeybee foragers will not be exposed to these high concentrations. Therefore, the appropriate use of this pesticide is considered safe for honeybees, at least with respect to the behaviors studied here.
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Relatively little attention has focused on how pesticides may affect Asian honey bees, which provide vital crop pollination services and are key native pollinators. We therefore studied the effects of a relatively new pesticide, flupyradifurone (FLU), which has been developed, in part, because it appears safer for honey bees than neonicotinoids. We tested the effects of FLU on Apis cerana olfactory learning in larvae (lower dose of 0.033 µg/larvae/day over 6 days) and, in a separate experiment, adults (lower dose of 0.066 µg/adult bee/day) at sublethal, field-realistic doses given over 3 days. A worst-case field-realistic dose is 0.44 µg/bee/day. Learning was tested in adult bees. The lower larval dose did not increase mortality, but the lower adult dose resulted in 20% mortality. The lower FLU doses decreased average olfactory learning by 74% (larval treatment) and 48% (adult treatment) and reduced average memory by 48% (larval treatment) and 22% (adult treatment) as compared to controls. FLU at higher doses resulted in similar learning impairments. The effects of FLU, a pesticide that is reported to be safer than neonicotinoids for honey bees, thus deserve greater attention.
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New information on the lethal and sublethal effects of neonicotinoids and fipronil on organisms is presented in this review, complementing the previous Worldwide Integrated Assessment (WIA) in 2015. The high toxicity of these systemic insecticides to invertebrates has been confirmed and expanded to include more species and compounds. Most of the recent research has focused on bees and the sublethal and ecological impacts these insecticides have on pollinators. Toxic effects on other invertebrate taxa also covered predatory and parasitoid natural enemies and aquatic arthropods. Little new information has been gathered on soil organisms. The impact on marine and coastal ecosystems is still largely uncharted. The chronic lethality of neonicotinoids to insects and crustaceans, and the strengthened evidence that these chemicals also impair the immune system and reproduction, highlights the dangers of this particular insecticidal class (neonicotinoids and fipronil), with the potential to greatly decrease populations of arthropods in both terrestrial and aquatic environments. Sublethal effects on fish, reptiles, frogs, birds, and mammals are also reported, showing a better understanding of the mechanisms of toxicity of these insecticides in vertebrates and their deleterious impacts on growth, reproduction, and neurobehaviour of most of the species tested. This review concludes with a summary of impacts on the ecosystem services and functioning, particularly on pollination, soil biota, and aquatic invertebrate communities, thus reinforcing the previous WIA conclusions (van der Sluijs et al. 2015).
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Modern humans live in an “exploded” network with unusually large circles of trust that form due to prosociality toward unfamiliar people (i.e. xenophilia). In a set of experiments we demonstrate that semi-free ranging bonobos (Pan paniscus) – both juveniles and young adults – also show spontaneous responses consistent with xenophilia. Bonobos voluntarily aided an unfamiliar, non-group member in obtaining food even when he/she did not make overt requests for help. Bonobos also showed evidence for involuntary, contagious yawning in response to videos of yawning conspecifics who were complete strangers. These experiments reveal that xenophilia in bonobos can be unselfish, proactive and automatic. They support the first impression hypothesis that suggests xenophilia can evolve through individual selection in social species whenever the benefits of building new bonds outweigh the costs. Xenophilia likely evolved in bonobos as the risk of intergroup aggression dissipated and the benefits of bonding between immigrating members increased. Our findings also mean the human potential for xenophilia is either evolutionarily shared or convergent with bonobos and not unique to our species as previously proposed.
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Global declines in insects have sparked wide interest among scientists, politicians, and the general public. Loss of insect diversity and abundance is expected to provoke cascading effects on food webs and to jeopardize ecosystem services. Our understanding of the extent and underlying causes of this decline is based on the abundance of single species or taxo-nomic groups only, rather than changes in insect biomass which is more relevant for ecological functioning. Here, we used a standardized protocol to measure total insect biomass using Malaise traps, deployed over 27 years in 63 nature protection areas in Germany (96 unique location-year combinations) to infer on the status and trend of local entomofauna. Our analysis estimates a seasonal decline of 76%, and midsummer decline of 82% in flying insect biomass over the 27 years of study. We show that this decline is apparent regardless of habitat type, while changes in weather, land use, and habitat characteristics cannot explain this overall decline. This yet unrecognized loss of insect biomass must be taken into account in evaluating declines in abundance of species depending on insects as a food source, and ecosystem functioning in the European landscape.
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The widespread contamination of a significant proportion of the planet’s land and water with pesticides is undeniable. While this takes place, innumerable species of animals associated with agricultural landscapes are declining at rates that may put them on the brink to extinction in the span of a lifetime. It is evident, therefore, that our current risk assessment of agrochemicals has failed to protect the environment. A new framework is proposed here that combines the mandatory introduction of new toxicity endpoints with a more logical assessment of risks within the existing tiered approach. Chronic toxicity tests designed to detect time-cumulative effects should be a requirement for assessing delayed mortality as well as population endpoints that are crucial for the recovery and survival of species, such as fecundity. Exposure assessments should ensure that field monitoring data integrate both the highest and average levels of residues, as the former levels determine the main ecological impacts. The first tier of the risk assessment should comprise an evaluation of short-term mortality (as currently done by a hazard quotient on acute toxicity) and of the lethality after chronic exposure to sublethal levels. Chemicals that pass this tier should be assessed in a second tier whereby the crucial population endpoints are evaluated. Unless there is evidence of recovery with no negative effects on reproduction of the species tested, a chemical should not be registered. Further tiers of assessment, including sublethal effects, community effects tested in model ecosystems (i.e. microcosms, mesocoms) and field trials can still be used as supporting evidence, as it is currently done.
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Pollinators are in global decline and agricultural pesticides are a potential driver of this. Recent studies have suggested that pesticides may significantly impact bumblebee colonies—an important and declining group of pollinators. Here, we show that colony-founding queens, a critical yet vulnerable stage of the bumblebee lifecycle, are less likely to initiate a colony after exposure to thiamethoxam, a neonicotinoid insecticide. Bombus terrestris queens were exposed to field-relevant levels of thiamethoxam and two natural stressors: the parasite Crithidia bombi and varying hibernation durations. Exposure to thiamethoxam caused a 26% reduction in the proportion of queens that laid eggs, and advanced the timing of colony initiation, although we did not detect impacts of any experimental treatment on the ability of queens to produce adult offspring during the 14-week experimental period. As expected from previous studies, the hibernation duration also had an impact on egg laying, but there was no significant interaction with insecticide treatment. Modelling the impacts of a 26% reduction in colony founding on population dynamics dramatically increased the likelihood of population extinction. This shows that neonicotinoids can affect this critical stage in the bumblebee lifecycle and may have significant impacts on population dynamics.
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Neonicotinoid seed dressings have caused concern world-wide. We use large field experiments to assess the effects of neonicotinoid-treated crops on three bee species across three countries (Hungary, Germany, and the United Kingdom). Winter-sown oilseed rape was grown commercially with either seed coatings containing neonicotinoids (clothianidin or thiamethoxam) or no seed treatment (control). For honey bees, we found both negative (Hungary and United Kingdom) and positive (Germany) effects during crop flowering. In Hungary, negative effects on honey bees (associated with clothianidin) persisted over winter and resulted in smaller colonies in the following spring (24% declines). In wild bees (Bombus terrestris and Osmia bicornis), reproduction was negatively correlated with neonicotinoid residues. These findings point to neonicotinoids causing a reduced capacity of bee species to establish new populations in the year following exposure.
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Experiments linking neonicotinoids and declining bee health have been criticized for not simulating realistic exposure. Here we quantified the duration and magnitude of neonicotinoid exposure in Canadatextquoterights corn-growing regions and used these data to design realistic experiments to investigate the effect of such insecticides on honey bees. Colonies near corn were naturally exposed to neonicotinoids for up to 4 monthstextemdashthe majority of the honey beetextquoterights active season. Realistic experiments showed that neonicotinoids increased worker mortality and were associated with declines in social immunity and increased queenlessness over time. We also discovered that the acute toxicity of neonicotinoids to honey bees doubles in the presence of a commonly encountered fungicide. Our work demonstrates that field-realistic exposure to neonicotinoids can reduce honey bee health in corn-growing regions.
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Imidacloprid is the most widely used insecticide in agriculture. In this study, we used feeding methods to simulate in-hive exposures of formulated imidacloprid (Advise® 2FL) alone and mixtures with six representative pesticides for different classes. Advise, fed at 4.3 mg/L (equal to maximal residue detection o