G. Christopher Cutler

Insecticide-induced hormesis and arthropod pest management.

Ecological backlashes such as insecticide resistance, resurgence and secondary pest outbreaks are frequent problems associated with insecticide use against arthropod pest species. The last two have been particularly important in sparking interest in the phenomenon of insecticide-induced hormesis within entomology and acarology. Hormesis describes a biphasic dose-response relationship that is characterized by a reversal of response between low and high doses of a stressor (e.g. insecticides). Although the concept of insecticide-induced hormesis often does not receive sufficient attention, or has been subject to semantic confusion, it has been reported in many arthropod pest species and natural enemies, and has been linked to pest outbreaks and potential problems with insecticide resistance. The study of hormesis remains largely neglected in entomology and acarology. Here, we examined the concept of insecticide-induced hormesis in arthropods, its functional basis and potential fitness consequences, and its importance in arthropod pest management and other areas.

Insects, Insecticides and Hormesis: Evidence and Considerations for Study

Insects are ubiquitous, crucial components of almost all terrestrial and fresh water ecosystems. In agricultural settings they are subjected to, intentionally or unintentionally, an array of synthetic pesticides and other chemical stressors. These ecological underpinnings, the amenability of insects to laboratory and field experiments, and our strong knowledgebase in insecticide toxicology, make the insect-insecticide model an excellent one to study many questions surrounding hormesis. Moreover, there is practical importance for agriculture with evidence of pest population growth being accelerated by insecticide hormesis. Nevertheless, insects have been underutilized in studies of hormesis. Where hormesis hypotheses have been tested, results clearly demonstrate stimulatory effects on multiple taxa as measured through several biological endpoints, both at individual and population levels. However, many basic questions are outstanding given the myriad of chemicals, responses, and ecological interactions that are likely to occur.

A large-scale field study examining effects of exposure to clothianidin seed-treated canola on honey bee colony health, development, and overwintering success

In summer 2012, we initiated a large-scale field experiment in southern Ontario, Canada, to determine whether exposure to clothianidin seed-treated canola (oil seed rape) has any adverse impacts on honey bees. Colonies were placed in clothianidin seed-treated or control canola fields during bloom, and thereafter were moved to an apiary with no surrounding crops grown from seeds treated with neonicotinoids. Colony weight gain, honey production, pest incidence, bee mortality, number of adults, and amount of sealed brood were assessed in each colony throughout summer and autumn. Samples of honey, beeswax, pollen, and nectar were regularly collected, and samples were analyzed for clothianidin residues. Several of these endpoints were also measured in spring 2013. Overall, colonies were vigorous during and after the exposure period, and we found no effects of exposure to clothianidin seed-treated canola on any endpoint measures. Bees foraged heavily on the test fields during peak bloom and residue analysis indicated that honey bees were exposed to low levels (0.5–2 ppb) of clothianidin in pollen. Low levels of clothianidin were detected in a few pollen samples collected toward the end of the bloom from control hives, illustrating the difficulty of conducting a perfectly controlled field study with free-ranging honey bees in agricultural landscapes. Overwintering success did not differ significantly between treatment and control hives, and was similar to overwintering colony loss rates reported for the winter of 2012–2013 for beekeepers in Ontario and Canada. Our results suggest that exposure to canola grown from seed treated with clothianidin poses low risk to honey bees.

Green peach aphid, Myzus persicae (Hemiptera: Aphididae), reproduction during exposure to sublethal concentrations of imidacloprid and azadirachtin.

BACKGROUND Resurgence of insect pests following insecticide applications is often attributed to natural enemy disturbance, but hormesis could be an alternative or additional mechanism. Green peach aphid, Myzus persicae (Sulzer), is an important insect pest of many crops worldwide that may be exposed to sublethal insecticide concentrations over time. Here, the hypothesis that exposure to low concentrations of imidacloprid and azadirachtin can induce hormetic responses in M. persicae is tested in the laboratory. RESULTS When insects were exposed to potato leaf discs dipped in sublethal concentrations of insecticide, almost all measured endpoints-adult longevity, F1 production, F1 survival and F2 production-were affected, and a statistically significant (P < 0.05) stimulatory response was recorded for F2 production following exposure to imidacloprid. No other measures for hormesis were statistically significant, but other trends of hormetic response were consistently observed. CONCLUSIONS Given that variable distribution and degradation of insecticides in the field would result in a wide range of concentrations over time and space, these laboratory experiments suggest that exposure to sublethal concentrations of imidacloprid and azadirachtin could stimulate reproduction in M. persicae.

Transgenerational shifts in reproduction hormesis in green peach aphid exposed to low concentrations of imidacloprid.

Hormesis is a biphasic phenomenon that in toxicology is characterized by low-dose stimulation and high-dose inhibition. It has been observed in a wide range of organisms in response to many chemical stressors, including insects exposed to pesticides, with potential repercussions for agriculture and pest management. To address questions related to the nature of the dose-response and potential consequences on biological fitness, we examined transgenerational hormesis in the green peach aphid, Myzus persicae, when exposed to sublethal concentrations of the insecticide imidacloprid. A hormetic response in the form of increased reproduction was consistently observed and a model previously developed to test for hormesis adequately fit some of our data. However, the nature of the dose-response differed within and across generations depending upon the duration and mode of exposure. Decreased reproduction in intermediate generations confirmed that fitness tradeoffs were a consequence of the hormetic response. However, recovery to levels of reproduction equal to that of controls in subsequent generations and significantly greater total reproduction after four generations suggested that biological fitness was increased by exposure to low concentrations of the insecticide, even when insects were continuously exposed to the stressor. This was especially evident in a greenhouse experiment where the instantaneous rate of population increase almost doubled and total aphid production more than quadrupled when aphids were exposed to potato plants systemically treated with low amounts of imidacloprid. Our results show that although fitness tradeoffs do occur with hormetic responses, this does not necessarily compromise overall biological fitness.

Risk to Pollinators from the Use of Chlorpyrifos in the United States

CPY is an organophosphorus insecticide that is widely used in North American agriculture. It is non-systemic, comes in several sprayable and granular formulations,and is used on a number of high-acreage crops on which pollinators can forage,including tree fruits, alfalfa, corn, sunflower, and almonds. Bees (Apoidea) are the most important pollinators of agricultural crops in North America and were the main pollinators of interest in this risk assessment.The conceptual model identified a number of potential exposure pathways for pollinators, some more significant than others. CPY is classified as being highly toxic to honey bees by direct contact exposure. However, label precautions and good agricultural practices prohibit application of CPY when bees are flying and/or when flowering crops or weeds are present in the treatment area. Therefore, the risk of CPY to pollinators through direct contact exposure should be small. The main hazards for primary exposure for honey bees are dietary and contact exposure from flowers that were sprayed during application and remain available to bees after application. The main pathways for potential secondary exposure to CPY is through pollen and nectar brought to the hive by forager bees and the sublethal body burden of CPY carried on forager bees. Foraging for other materials, including water or propolis, does not appear to be an important exposure route. Since adult forager honey bees are most exposed, their protection from exposure via pollen, honey, and contact with plant surfaces is expected to be protective of other life stages and castes of honey bees.Tier- I approaches to estimate oral exposure to CPY through pollen and nectar/honey, the principle food sources for honey bees, suggested that CPY poses a risk to honey bees through consumption of pollen and nectar. However, a Tier-2 assessment of concentrations reported in pollen and honey from monitoring work in North America indicated there is little risk of acute toxicity from CPY through consumption of these food sources.Several models were also used to estimate upper-limit exposure of honey bees to CPY through consumption of water from puddles or dew. All models suggest that the risk of CPY is below the LOC for this pathway. Laboratory experiments with field-treated foliage, and semi-field and field tests with honey bees, bumble bees,and alfalfa leaf cutting bees indicate that exposure to foliage, pollen and/or nectar is hazardous to bees up to 3 d after application of CPY to a crop. Pollinators exposed to foliage, pollen or nectar after this time should be minimally affected.Several data gaps and areas of uncertainty were identified, which apply to CPYand other foliar insecticides. These primarily concern the lack of exposure and toxicological data on non-Apis pollinators. Overall, the rarity of reported bee kill incidents involving CPY indicates that compliance with the label precautions and good agricultural practice with the product is the norm in North American agriculture.Overall, we concluded that, provided label directions and good agricultural practices are followed, the use of CPY in agriculture in North America does not present an unacceptable risk to honeybees.

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

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.

Mulch type and moisture level affect pupation depth of Rhagoletis mendax Curran (Diptera: Tephritidae) in the laboratory

Mulching can be beneficial for organic highbush blueberry production, but its effects on insect pests have received little attention. For pests that pupate in soil, depth may affect pupation success due to differences in temperature and moisture, mortality factors such as predation, or efficacy of controls such as insecticidal soil drenches. We examined how mulch type and moisture affect pupation depth for Rhagoletis mendax Curran (blueberry maggot), an important pest of blueberries. In laboratory studies, pupation depth was measured in wood waste compost, uncomposted pine needles, soil and sand, each at dry, field moisture levels and wet, 99% water holding capacity conditions. Pupation occurred more deeply but with greater variability in pine needle mulch compared to compost mulch, soil, or sand. Approximately 50% of maggots pupated on the surface of wet soil, however, maggots burrowed more deeply in wet than in dry pine needles. Moisture level did not significantly affect pupation depth in compost or sand. Some larvae unexpectedly escaped the stacks of cups used to assess pupation depth or died before forming a puparium. Less than 70% of stacks with dry pine needles contained pupae, and fewer pupae were recovered from wet than dry compost and soil. These results suggest that mulch material and/or moisture levels can have significant impacts on R. mendax pupation depth with potential implications for its management.

Host-finding ability of three entomopathogenic nematode isolates in the presence of plant roots

The effect of plant roots on the host-finding ability of three isolates of entomopathogenic nematodes (EPN), Heterorhabditis bacteriophora D-H-Da1, Steinernema sp. Dongrae and Steinernema sp. BJ was studied. In Petri dish experiments the overall response of the infective juveniles (IJ) of these isolates differed from one another, but all were attracted to a Galleria mellonella larva and to a tomato seedling when either of these targets was presented with a blank control. The BJ and D-H-Da1 IJ aggregated more around a tomato root than a G. mellonella larva when these targets were presented separately, but showed no preference for a G. mellonella-tomato seedling combination over a blank control. Dongrae IJ showed no preference for a G. mellonella larva or tomato seedling when each was presented simultaneously in the same Petri dish. In experiments in pots of soil, plant roots did not affect the host-finding ability of Dongrae IJ. In contrast, compared to control pots with no roots, roots of bean plants hindered the ability of BJ IJ to infect a G. mellonella larva, but tomato roots increased host-finding by D-H-Da1 IJ. Roots of certain plant species modify the host-finding ability of EPN, but the extent and direction of the response varied with the EPN applied.

Gene Expression during Imidacloprid-Induced Hormesis in Green Peach Aphid

Imidacloprid-induced hormesis in the form of stimulated reproduction has previously been reported in green peach aphid, Myzus persicae. Changes in gene expression accompanying this hormetic response have not been previously investigated. In this study, expression of stress response (Hsp60), dispersal (OSD, TOL and ANT), and developmental (FPPS I) genes were examined for two generations during imidacloprid-induced reproductive stimulation in M. persicae. Global DNA methylation was also measured to test the hypothesis that changes in gene expression are heritable. At hormetic concentrations, down-regulation of Hsp60 was followed by up-regulation of this gene in the subsequent generation. Likewise, expression of dispersal-related genes and FPPS I varied with concentration, life stage, and generation. These results indicate that reproductive hormesis in M. persicae is accompanied by a complex transgenerational pattern of up- and down-regulation of genes that likely reflects trade-offs in gene expression and related physiological processes during the phenotypic dose-response. Moreover, DNA methylation in second generation M. persicae occurred at higher doses than in first-generation aphids, suggesting that heritable adaptability to low doses of the stressor might have occurred.