Recent concern over global pollinator declines has led to considerable research on the effects of pesticides on bees. Although pesticides are typically not encountered at lethal levels in the field, there is growing evidence indicating that exposure to field-realistic levels can have sublethal effects on bees, affecting their foraging behaviour, homing ability and reproductive success. Bees are essential for the pollination of a wide variety of crops and the majority of wild flowering plants, but until now research on pesticide effects has been limited to direct effects on bees themselves and not on the pollination services they provide. Here we show the first evidence to our knowledge that pesticide exposure can reduce the pollination services bumblebees deliver to apples, a crop of global economic importance. Bumblebee colonies exposed to a neonicotinoid pesticide provided lower visitation rates to apple trees and collected pollen less often. Most importantly, these pesticide-exposed colonies produced apples containing fewer seeds, demonstrating a reduced delivery of pollination services. Our results also indicate that reduced pollination service delivery is not due to pesticide-induced changes in individual bee behaviour, but most likely due to effects at the colony level. These findings show that pesticide exposure can impair the ability of bees to provide pollination services, with important implications for both the sustained delivery of stable crop yields and the functioning of natural ecosystems.

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Neonicotinoid pesticide exposure impairs crop pollination services provided by bumblebees

Insecticides are an invaluable pest management tool and anthropogenic stressors of widespread environmental occurrence that are subject to biased perceptions based on the targeted application, market value of use, and regulatory requirements As a result, short-term and simplistic efforts focusing on lethal effects toward individual species and populations prevail Holistic and comprehensive studies exploring rather common sublethal insecticide exposures are rare, particularly considering their potential role in structuring populations and communities in diverse environmental settings and potentially interfering in a range of ecological interactions Studies on insecticide resistance, for example, do not go beyond population-based studies, disregarding temporal and spatial effects in the associated community, and rarely considering the whole of sublethal exposure Some of these knowledge gaps are here recognized and explored

https://digitalcommons.unl.edu/cgi/viewcontent.cgi?article=2998&context=usdaarsfacpub

Sublethal exposure, insecticide resistance, and community stress

Bumblebees are exposed to pesticides applied for crop protection while foraging on treated plants, with increasing evidence suggesting that this sublethal exposure has implications for pollinator declines. The challenges of navigating and learning to manipulate many different flowers underline the critical role learning plays for the foraging success and survival of bees. We assessed the impacts of both acute and chronic exposure to field-realistic levels of a widely applied neonicotinoid insecticide, thiamethoxam, on bumblebee odour learning and memory. Although bees exposed to acute doses showed conditioned responses less frequently than controls, we found no difference in the number of individuals able to learn at field-realistic exposure levels. However, following chronic pesticide exposure, bees exposed to field-realistic levels learnt more slowly and their short-term memory was significantly impaired following exposure to 2.4 ppb pesticide. These results indicate that field-realistic pesticide exposure can have appreciable impacts on learning and memory, with potential implications for essential individual behaviour and colony fitness.

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Bumblebee learning and memory is impaired by chronic exposure to a neonicotinoid pesticide.

The South American tomato pinworm, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae), is an invasive pest difficult to control. Insecticide application is quite common and remains the prevalent control method particularly in open-field cultivation systems. As a result, insecticide resistance to many chemical classes of insecticides has been described both in South America and in Europe. The development of insecticide resistance is relatively fast in this species, and the main mechanisms involved are altered target-site sensitivity and/or enhanced detoxification, depending on the chemical class. However, insecticide resistance mechanisms do not differ between South America and Europe and are mainly due to simple genotype variations leading to high levels of resistance. The presence of resistance alleles at low frequency, especially against newer chemistry, is of major concern, as they tend to spread with the invasions making tomato pinworm particularly difficult to control. The monitoring methods and management programmes developed for the species benefited from the pro-activity of the Insecticide Resistance Action Committee and its country groups, particularly in Brazil and Spain. Bioassay methods were developed, resistance monitoring activities initiated and resistance management guidance was provided. The implementation of integrated control programmes and appropriate resistance management strategies as part of such programs is of utmost importance to keep tomato pinworm infestations under economic damage thresholds, thus guaranteeing sustainable yields.

https://link.springer.com/content/pdf/10.1007%2Fs10340-019-01086-9.pdf

Insecticide resistance in the tomato pinworm Tuta absoluta: patterns, spread, mechanisms, management and outlook

Summary
The ability to forage and return home is essential to the success of bees as both foragers and pollinators. Pesticide exposure may cause behavioural changes that interfere with these processes, with consequences for colony persistence and delivery of pollination services.
We investigated the impact of chronic exposure (5–43 days) to field-realistic levels of a neonicotinoid insecticide (2·4 ppb thiamethoxam) on foraging ability, homing success and colony size using radio frequency identification (RFID) technology in free-flying bumblebee colonies.
Individual foragers from pesticide-exposed colonies carried out longer foraging bouts than untreated controls (68 vs. 55 min). Pesticide-exposed bees also brought back pollen less frequently than controls indicating reduced foraging performance.
A higher proportion of bees from pesticide-exposed colonies returned when released 1 km from their nests; this is potentially related to increased orientation experience during longer foraging bouts. We measured no impact of pesticide exposure on homing ability for bees released from 2 km, or when data were analysed overall.
Despite a trend for control colonies to produce more new workers earlier, we found no overall impacts of pesticide exposure on whole colony size.
Synthesis and applications. This study shows that field-realistic neonicotinoid exposure can have impacts on both foraging ability and homing success of bumblebees, with implications for the success of bumblebee colonies in agricultural landscapes and their ability to deliver crucial pollination services. Pesticide risk assessments should include bee species other than honeybees and assess a range of behaviours to elucidate the impact of sublethal effects. This has relevance for reviews of neonicotinoid risk assessment and usage policy world-wide.

https://besjournals.onlinelibrary.wiley.com/doi/pdf/10.1111/1365-2664.12689

Investigating the impacts of field-realistic exposure to a neonicotinoid pesticide on bumblebee foraging, homing ability and colony growth

Hormesis, a biphasic dose response whereby exposure to low doses of a stressor can stimulate biological processes, has been reported in many organisms, including pest insects when they are exposed to low doses of a pesticide. However, awareness of the hormesis phenomenon seems to be limited among bee researchers, in spite of the increased emphasis of late on pollinator toxicology and risk assessment. In this commentary, we show that there are several examples in the literature of substances that are toxic to bees at high doses but stimulatory at low doses. Appreciation of the hormetic dose response by bee researchers will improve our fundamental understanding of how bees respond to low doses of chemical stressors, and may be useful in pollinator risk assessment. © 2015 Society of Chemical Industry

Can poisons stimulate bees? Appreciating the potential of hormesis in bee–pesticide research

Hormesis, a biphasic phenomenon characterized by low-dose stimulation and high-dose inhibition following exposure to stress, has been reported in many different insects exposed to low doses of pesticide. Using green peach aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae), and the insecticide imidacloprid as a model, we tested whether or not there were changes in expression of genes involved in insecticide detoxification and general stress when aphids were exposed over multiple generations in a greenhouse setting to imidacloprid concentrations that induced hormetic responses. We also wanted to know whether exposure to insecticide concentrations that induce reproductive hormesis impacted the insect’s ability to cope with a subsequent stressor. The instantaneous rate of increase and total reproductive output of aphids developing on potato plants treated with 0.25 µg imidacloprid L−1 was significantly greater than that on control plants. Treatments of 0.25 and 2.5 µg imidacloprid L−1 significantly increased or decreased expression of genes for E4-esterase, cytochrome P450-CYP6CY3, and Hsp60 in aphids, with variation within and across generations. Third-generation aphids from plants treated with 0.25 µg imidacloprid L−1 survived longer than control aphids when subsequently subjected to food/water stress, but not when subsequently exposed to a LC20 of another insecticide. Our results indicate insecticide-induced reproduction hormesis in M. persicae is accompanied by intermittent changes in expression of detoxification and stress-coping genes, and that it can prime the insect to cope with subsequent stress.

Sublethal concentrations of imidacloprid increase reproduction, alter expression of detoxification genes, and prime Myzus persicae for subsequent stress

Hormesis and insects: Effects and interactions in agroecosystems.

BACKGROUND
Hormetic preconditioning, whereby exposure to mild stress primes an organism to better tolerate subsequent stress, is well documented. It is unknown if exposure to hormetic concentrations of insecticide can trans-generationally prime insects to better tolerate insecticide exposure, or whether exposure to hormetic concentrations of insecticide can induce mutations in genes responsible for insecticide resistance. Using the aphid Myzus persicae (Sulzer) and insecticide imidacloprid as a model, we examined if exposure to mildly toxic and hormetic concentrations of imidacloprid reduced aphid susceptibility to insecticides across four generations, and whether such exposures induced mutations in the imidacloprid binding site in post-synaptic nicotinic acetylcholine receptors.

RESULTS
Chronic, multigenerational exposure of aphids to hormetic concentrations of imidacloprid primed offspring to better survive exposure to certain concentrations of imidacloprid, but not exposure to spirotetramat, an insecticide with a different mode of action. Exposure to hormetic and mildly toxic concentrations of imidacloprid did not result in mutations in any of the examined nicotinic acetylcholine receptor subunits.

CONCLUSION
Our findings demonstrate that exposure to hormetic concentrations of insecticide can prime insects to better withstand subsequent chemical stress, but this is dependent upon the insecticide exposure scenario, and may be subtle over generations.

Rachel R. Rix

Papers

Can poisons stimulate bees? Appreciating the potential of hormesis in bee–pesticide research

Sublethal concentrations of imidacloprid increase reproduction, alter expression of detoxification genes, and prime Myzus persicae for subsequent stress

Hormesis and insects: Effects and interactions in agroecosystems.

Does multigenerational exposure to hormetic concentrations of imidacloprid precondition aphids for increased insecticide tolerance

Pesticide-Induced Hormesis in Arthropods: Towards Biological Systems