Chronic exposure to a common biopesticide is detrimental to individuals and colonies of the paper wasp Polistes versicolor.

Risk assessments of agrochemicals on non-target insects are biased in studies with surrogate groups, such as pollinators. In social insects, such investigations are generally restricted to lethal tests with adults maintained individually, simulating a non-realistic scenario. Here, we performed a holistic approach to resemble a chronic field exposure of Polistes versicolor (Hymenoptera: Vespidae) to a common biopesticide. These wasps are predators that perform biological control in the agroecosystems. Wasps were chronically subjected to the ingestion of different concentrations of azadirachtin. The neonicotinoid imidacloprid was used as a positive control. For the first time, we demonstrated that the biopesticide azadirachtin is detrimental for individual and colony survival and impairs colony reproduction of a social wasp maintained in the laboratory. Our data also indicated that neonicotinoid imidacloprid is harmful to wasps and their colonies. Therefore, the concomitant use of azadirachtin and paper wasps in integrated pest management strategies should be carefully evaluated, because the constant use of this pesticide can be detrimental for social wasps, possibly reducing biological control.

Toxicological assessments of agrochemical effects on stingless bees (Apidae, Meliponini).

Bee pollination is crucial for ecosystem maintenance and crop production. The ubiquity of bee pollinators in agricultural landscapes frequently results in their exposure to agrochemicals, which has been associated with their decline. Stingless bees are wild pollinators restricted to the Pantropical region, and like honey bees, are suffering colony losses. However, stingless bees and honey bees do not show the same behaviors, therefore, methods used for risk assessment of honey bees cannot be utilized on stingless bees. Herein, we describe protocols to standardize methods that allow for the exploration of lethal and sublethal effects of agrochemicals via acute and chronic exposure of stingless bees. The in vitro rearing used for chronic exposure from the egg to the adult stage proved to be effective in obtaining relevant screenings. In addition, we performed a meta-analysis and summarized the results of toxicological studies conducted with the protocols described. The meta-analyses indicated a reduction in survival under acute and chronic exposures to agrochemicals, and revealed that our protocols for toxicological assessments did not have publication bias for either acute or chronic exposure. These findings proved that these standardized protocols are reliable for toxicological research on stingless bee.

Effects of Spinosad, Imidacloprid, and Lambda-cyhalothrin on Survival, Parasitism, and Reproduction of the Aphid Parasitoid Aphidius colemani.

Insecticides can affect biological control by parasitoids. Here, we examined the lethal and sublethal effects of two conventional insecticides, imidacloprid and lambda-cyhalothrin, and a reduced-risk bioinsecticide, spinosad, on the aphid parasitoid Aphidius colemani Viereck (Hymenoptera: Braconidae). Concentration-mortality curves generated from insecticide residue bioassays found that wasps were nearly 20-fold more susceptible to spinosad than imidacloprid and lambda-cyhalothrin. Imidacloprid and lambda-cyhalothrin compromised adult parasitoid longevity, but not as dramatically as spinosad: concentrations >200 ng spinosad/cm2 reduced wasp longevity by half. Imidacloprid and lambda-cyhalothrin also compromised aphid parasitism by wasps. Although increasing imidacloprid concentrations led to increased host viability and reduced progeny production, lambda-cyhalothrin did not affect viability of parasitized hosts or parasitoid progeny production in a dose-dependent manner. Our results demonstrate that reduced risk bioinsecticide products like spinosad can be more toxic to biological control agents than certain conventional insecticides.

Spinosad- and Deltamethrin-Induced Impact on Mating and Reproductive Output of the Maize Weevil Sitophilus zeamais.

Assessments of acute insecticide toxicity frequently focus on the lethal effects on individual arthropod pest species and populations neglecting the impacts and consequences of sublethal exposure. However, the sublethal effects of insecticides may lead to harmful, neutral, or even beneficial responses that may affect (or not) the behavior and sexual fitness of the exposed insects. Intriguingly, little is known about such effects on stored product insect pests in general and the maize weevil in particular. Thus, we assessed the sublethal effects of spinosad and deltamethrin on female mate-searching, mating behavior, progeny emergence, and grain consumption by maize weevils. Insecticide exposure did not affect the resting time, number of stops, and duration of mate-searching by female weevils, but their walking velocity was compromised. Maize weevil couples sublethally exposed to deltamethrin and spinosad exhibited altered reproductive behavior (walking, interacting, mounting, and copulating), but deltamethrin caused greater impairment. Curiously, higher grain consumption and increased progeny emergence were observed in deltamethrin-exposed insects, suggesting that this pyrethroid insecticide elicits hormesis in maize weevils that may compromise control efficacy by this compound. Although spinosad has less of an impact on weevil reproductive behavior than deltamethrin, this bioinsecticide also benefited weevil progeny emergence, but did not affect grain consumption. Therefore, our findings suggest caution using either compound, and particularly deltamethrin, for controlling the maize weevil, as they may actually favor this species population growth when in sublethal exposure requiring further assessments. The same concern may be valid for other insecticides as well, what deserves future attention.

Leaf Fertilizers Affect Survival and Behavior of the Neotropical Stingless Bee Friesella schrottkyi (Meliponini: Apidae: Hymenoptera).

The ongoing concern about bee decline has largely focused on honey bees and neonicotinoid insecticides, while native pollinators such as Neotropical stingless bees and agrochemicals such as other insecticide groups, pesticides in general, and fertilizers-especially leaf fertilizers-remain neglected as potential contributors to pollination decline. In an effort to explore this knowledge gap, we assessed the lethal and sublethal behavioral impact of heavy metal-containing leaf fertilizers in a native pollinator of ecological importance in the Neotropics: the stingless bee Friesella schrottkyi (Friese). Two leaf fertilizers-copper sulfate (24% Cu) and a micronutrient mix (Arrank L: 5% S, 5% Zn, 3% Mn, 0.6% Cu, 0.5% B, and 0.06% Mo)-were used in oral and contact exposure bioassays. The biopesticide spinosad and water were used as positive and negative controls, respectively. Copper sulfate compromised the survival of stingless bee workers, particularly with oral exposure, although less than spinosad under contact exposure. Sublethal exposure to both leaf fertilizers at their field rates also caused significant effects in exposed workers. Copper sulfate enhanced flight take-off on stingless bee workers, unlike workers exposed to the micronutrient mix. There was no significant effect of leaf fertilizers on the overall activity and walking behavior of worker bees. No significant effect was observed for the respiration rate of worker bees under contact exposure, but workers orally exposed to the micronutrient mix exhibited a reduced respiration rate. Therefore, leaf fertilizers do affect F. schrottkyi , what may also occur with other stingless bees, potentially compromising their pollination activity deserving attention.

Biopesticide-induced behavioral and morphological alterations in the stingless bee Melipona quadrifasciata.

Because of their natural origin, biopesticides are assumed to be less harmful to beneficial insects, including bees, and therefore their use has been widely encouraged for crop protection. There is little evidence, however, to support this ingrained notion of biopesticide safety to pollinators. Because larval exposure is still largely unexplored in ecotoxicology and risk assessment on bees, an investigation was performed on the lethal and sublethal effects of a diet treated with 2 bioinsecticides, azadirachtin and spinosad, on the stingless bee, Melipona quadrifasciata, which is one of the most important pollinators in the Neotropics. Survival of stingless bee larvae was significantly compromised at doses above 210 ng a.i./bee for azadirachtin and 114 ng a.i./bee for spinosad. No sublethal effect was observed on larvae developmental time, but doses of both compounds negatively affected pupal body mass. Azadirachtin produced deformed pupae and adults as a result of its insect growth regulator properties, but spinosad was more harmful and produced greater numbers of deformed individuals. Only spinosad compromised walking activity of the adult workers at doses as low as 2.29 ng a.i./bee, which is 1/5000 of the maximum field recommended rate. In conclusion, the results demonstrated that bioinsecticides can pose significant risks to native pollinators with lethal and sublethal effects; future investigations are needed on the likelihood of such effects under field conditions.

Pesticides and reduced-risk insecticides, native bees and pantropical stingless bees: pitfalls and perspectives.

Although invertebrates generally have a low public profile, the honey bee, Apis mellifera L., is a flagship species whose popularity likely derives from the products it provides and its perceived ecological services. Therefore, the raging debate regarding honey bee decline has surpassed the realm of beekeepers, academia, industry and regulatory agencies and now also encompasses non-governmental agencies, media, fiction writers and the general public. The early interest and concern about honey bee colony collapse disorder (CCD) soon shifted to the bigger issue of pollinator decline, with a focus on the potential involvement of pesticides in such a phenomenon. Pesticides were previously recognised as the potential culprits of the reported declines, particularly the neonicotinoid insecticides owing to their widespread and peculiar use in agriculture. However, the evidence for the potential pivotal role of these neonicotinoids in honey bee decline remains a matter of debate, with an increased recognition of the multifactorial nature of the problem and the lack of a direct association between the noted decline and neonicotinoid use. The focus on the decline of honey bee populations subsequently spread to other species, and bumblebees became another matter of concern, particularly in Europe and the United States. Other bee species, ones that are particularly important in other regions of the world, remain the object of little concern (unjustifiably so). Furthermore, the continuous focus on neonicotinoids is also in need of revision, as the current evidence suggests that a broad spectrum of compounds deserve attention. Here we address both shortcomings.

Spinosad in the native stingless bee Melipona quadrifasciata: regrettable non-target toxicity of a bioinsecticide.

The risks imposed by novel insecticides, mainly bioinsecticides, are largely unknown despite their increased use and their perceived environmental safety, which is based on their natural origin. Furthermore, unlike honeybees, native pollinator species have received little attention. In the present study, the lethal and sublethal effects of the neonicotinoid imidacloprid and the bioinsecticide spinosad were assessed in the stingless bee species Meliponaquadrifasciata, an important native pollinator in the Neotropical region. The adult stingless bee workers exhibited high oral insecticide susceptibility, with LD50s of 23.54 and 12.07 ng a.i./bee for imidacloprid and spinosad, respectively. Imidacloprid also impaired worker respiration and overall group activity and flight, while spinosad significantly impaired only worker flight despite exhibiting higher oral toxicity to adult workers than imidacloprid. These findings indicate the hazardous nature not only of imidacloprid but also the bioinsecticide spinosad to adult workers of the native pollinator M. quadrifasciata. Therefore, bioinsecticides should not be exempted from risk assessment analysis due to their lethal and sublethal components.