Wagner Faria Barbosa

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.

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.

Side Effects of Fungicides Used in Cucurbitaceous Crop on Trichogrammaatopovirilia Oatman & Platner (Hymenoptera: Trichogramatidae)

Trichogramma spp. (Hymenoptera: Trichogrammatidae) can control Diaphania hyalinata Linnaeus (Lepidoptera: Pyralidae). On the other hand, pesticides may reduce the efficiency of natural enemies. The objective was to evaluate the side-effects of fungicides used in the production of cucurbitaceous crops on Trichogramma atopovirilia Oatman & Platner parasitizing D. hyalinata eggs. The fungicides used in bioassays were: azoxystrobin (0.08 g active ingredient [ai] L -1 ), chlorothalonil (2.00 g ai L -1 ), mancozeb (1.60 g ai L -1 ), tebuconazole (0.25 g ai L -1 ) and thiophanate-methyl (0.49 g ai L -1 ). Cardboards with 30 D. hyalinata eggs previously immersed in fungicide solutions and distilled water (control) were offered separately to 20 newly emerged T. atopovirilia females in glass tubes. Parasitism, parasitism reduction, emergence, sex ratio, and number of individuals per egg were evaluated. The fungicides chlorothalonil, thiophanate-methyl and tebuconazole reduced parasitism of T. atopovirilia by 43.37, 27.64 and 18.51%, respectively. However, parasitism with azoxystrobin (79.21%) was higher than the control (67.37%) (P ≤ 0.05). Chlorothalonil, thiophanate-methyl and tebuconazole reduced emergence by 73.77, 75.62 and 79.35% (P ≤ 0.05), respectively. Azoxystrobin and thiophanate-methyl reduced the sex ratio by 0.77 and 0.76 (P ≤ 0.05), respectively. Fungicides did not reduce the number of individuals per egg. The fungicides azoxystrobin and mancozeb were selective for T. atopovirilia for most studied parameters suggesting that these products must have the priority in crop disease management to allow efficient biological control of T. atopovirilia against D. hyalinata.

Azadirachtin-induced antifeeding in Neotropical stingless bees

The ongoing debate regarding the role of pesticides in the global decline of bee populations is increasing the demand for use of biopesticides, compounds generally believed to be less harmful to pollinators. However, there is lack of evidence justifying such perceptions, particularly regarding native pollinator species like Neotropical stingless bees. Here, we investigated whether azadirachtin, a neem-based biopesticide, causes significant lethal and sublethal effects on adult workers of the Neotropical stingless bee species Melipona quadrifasciata and Partamona helleri. Susceptibility to azadirachtin varied with several factors, including the route of exposure, the concentration of the biopesticide, and the bee species. We found that although azadirachtin did not affect worker bee mortality, flight, or respiration rate, it did, however, induce a significant antifeeding effect on the stingless bee species.

Mating behavior of the predator Podisus nigrispinus (Heteroptera: Pentatomidae) under exposure to neem: Comportamiento de apareamiento del depredador Podisus nigrispinus (Heteroptera: Pentatomidae) expuesto al neem

La preservacion de los enemigos naturales es la base fundamental para el manejo integrado de las plagas. Los insecticidas botanicos han demostrado un bajo impacto sobre los artropodos beneficos en relacion a la supervivencia. Se desarrollo un estudio para evaluar el efecto del insecticida botanico neem (Azadirachta indica A. Juss.; Meliaceae) sobre el comportamiento de apareamiento del chinche depredador Podisus nigrispinus (Heteroptera: Pentatomidae). Se expusieron adultos virgenes de 5-7 dias de edad, separados por sexo, a residuos secos de este extracto. Machos y hembras virgenes entre 5 y 7 d de edad fueron expuestos a la azadiractina, por contacto directo con superficies tratadas. Los tratamientos fueron: machos y hembras no tratados; macho tratado y hembra no tratada; macho no tratado y hembra tratada y macho y hembras tratadas. Los resultados demostraron que la azadiractina afecto la duracion de la primera copula (test de Wilcoxon, χ2 = 13.38, df = 3, p = 0.004) lo que se traduce en un alto tiempo medio efectivo de copula (EATM50) en el tratamiento en que solo la hembra fue tratada con azadiractina. Esta constatacion apunta a un efecto subletal de la azadiractina sobre el comportamiento de apareamiento de P. nigrispinus que probablemente compromete su reproduccion.

Seletividade de inseticidas, recomendados para cucurbitáceas para Trichogramma atopovirilia Oatman & Platner (Hymenoptera: Trichogrammatidae) em condições de laboratório

Selectivity of pesticides used in cucurbits to Trichogramma atopovirilia Oatman & Platner (Hymenoptera: Trichogrammatidae) The cucurbit borers Diaphania spp. are major cucurbit pests, causing losses of up to 100% in production. Biological control with the parasitoid Trichogramma is an alternative for reducing the use of insecticides. The objective of this study was to evaluate the selectivity of the active ingredients abamectin, chlorfenapyr and thiacloprid to Trichogramma atopovirilia Oatman & Platner (Hymenoptera: Trichogrammatidae). For this purpose, 20 newly emerged females of T. atopovirilla were confined individually in glass tubes (2.5 cm diameter x 8.5 cm in length), with 30 eggs of Diaphania hyalinata (Linnaeus) (Lepidoptera: Pyralidae) glued on a small cardboard strip that was previously immersed for five seconds in chemical solution. The active ingredients abamectin, chlorfenapyr and thiacloprid did not af fect the T. atopovirilia parasitism. However, chlorfenapyr reduced larval emergence. Abamectin and thiacloprid can be therefore recommended for the Integrated Pest Management, as they proved to be the most selective to T. atopovirilia in D. hyalinata eggs.

Variations in circulating hemocytes are affected by age and caste in the stingless bee Melipona quadrifasciata

The insect immune system faces various challenges; particularly in social bees, caste system and age polyethism expose individuals to numerous environmental and working conditions. However, little is known about how cellular defenses in social bees may be organized to respond to a variety of immune challenges. Here, we describe the morphological features and the total and differential counts of hemocytes in different female classes (newly emerged workers, nurses, foragers, and virgin queens) of the eusocial stingless bee Melipona quadrifasciata. Granulocytes and prohemocytes were, respectively, the most and the least abundant cells among all classes of females. Furthermore, there were more prohemocytes in virgin queens than in foragers. The total number of hemocytes was smaller in foragers, whereas the largest number was observed in nurse workers. This reduced amount of hemocytes in foragers might allow energy savings to perform colony activities such as foraging and defense. Foragers also had the biggest hemocytes (either prohemocytes, granulocytes, or plasmatocytes) in comparison to the other classes of females, which might have arisen as a compensation for the reduction in number of these cells during aging. These results suggest that profiles of hemocytes of M. quadrifasciata vary according to the caste and age of this eusocial bee.

Acute and oral exposure to imidacloprid does not affect the number of circulating hemocytes in the stingless bee Melipona quadrifasciata post immune challenge

In the present work, the effects of the neonicotinoid imidacloprid formulation on the total hemocyte counts (THC) and differential hemocyte counts (DHC) were investigated in foraging workers of the stingless bee Melipona quadrifasciata under (or not) the challenge with the bacteria Escherichia coli. The THC was not altered with the insecticide exposure and/or bacterial infection. However, the DHC of the bees changed with the imidacloprid exposure and/or bacterial infection. The number of prohemocytes (stem cells) increased in bees exposed to imidacloprid, but it did not change after the bacterial infection. The number of plasmatocytes (phagocytic cells) increased in imidacloprid-exposed and uninfected bees and decreased in infected bees regardless of the exposure to imidacloprid. On the other hand, there was a reduction of granulocytes, the most active immune cells, after imidacloprid exposure and an increase of granulocytes after the infection. Previous studies have shown that the neonicotinoids exposure can impair the immune system of bees. Our findings showed that the relative number of granulocytes declined with imidacloprid exposure, but the overall capacity of hemocyte responses in terms of total numbers after bacterial infection persisted even after the insecticide exposure.

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.