Effects of insecticides used in strawberries on stingless bees Melipona quadrifasciata and Tetragonisca fiebrigi (Hymenoptera: Apidae)

Abstract

The use of pesticides is considered one of the most important threats to pollinators, especially since they are widely used in agriculture for pest control. In the last years, several studies have reported severe secondary effects on various bee species, including exotic and native bees. In this study, lethal (mortality) and sublethal (locomotor activity) effects of insecticides and acaricides used in strawberries in Brazil (abamectin, novaluron, spinetoram, and thiamethoxam) were evaluated on the native stingless bees Melipona quadrifasciata and Tetragonisca fiebrigi. The results showed that the effects varied significantly according to the pesticide, type of exposure (oral or topical), and bee species. Through oral exposure, M. quadrifasciata was more susceptible to all insecticides except for abamectin, while in topical exposure, T. fiebrigi was more sensitive. Thiamethoxam followed by spinetoram and abamectin were the most lethal, regardless of species or exposure route; novaluron was not harmful at the highest tested dose. The locomotor activity of bees was altered in the presence of sublethal doses (LC 10 and LC 50 ) of all insecticides. Spinetoram and abamectin can be as much as toxic as thiamethoxam against M. quadrifasciata and T. fiebrigi in laboratory experiments. These findings should be confirmed in field experiments to define possibilities to combine pest control and pollinator management. In crops like strawberries, the selectivity of native pollinators should be considered.

Biopesticides and insect pollinators: Detrimental effects, outdated guidelines, and future directions

“…Spinosad and spinoteram (another fermentation product of Saccharopolyspora spinosa) can prove highly toxic to these bees. In particular, a considerable reduction in adult survival after exposure to spinosyns was documented for M. quadrifasciata (Barbosa et al, 2015b;Piovesan et al, 2020), Partamona helleri (Tomé et al, 2015;dos Santos Araujo et al, 2019a), Plebeia emerina (Padilha et al, 2019), Plebeia lucii (Marques et al, 2020), Scaptotrigona xanthotricha (Tomé et al, 2015), and Tetragonisca fiebrigi (Padilha et al, 2020;Piovesan et al, 2020). In addition to the lethal effect, a plethora of sublethal effects on different developmental stages were demonstrated in several studies (Figs.…”

“…Exposure at the larval stage caused a delay in development and induced microbial and morphological changes in the midgut of P. helleri workers as well as alterations in their activity (dos Santos Araujo et al, 2019b). Spinosad exposure produced deformed pupae and impaired locomotor and flight ability in emerged adults of M. quadrifasciata (Barbosa et al, 2015b;Piovesan et al, 2020). Exposure of M. quadrifasciata workers also caused a decrease in the expression of the immune-related gene vitellogenin and an increase in the number of circulating hemocytes (Viana et al, 2020).…”

Acute toxicity of the insecticide abamectin and the fungicide difenoconazole (individually and in mixture) to the tropical stingless bee Melipona scutellaris

“…In addition, contact toxicity tests with A. mellifera evaluating technical abamectin indicate a higher sensitivity than that of M. scutellaris exposed to Kraft 36 EC (Table 2). Eventually, the toxicity value will vary significantly depending on the pesticide (technical substance or formulated product), type of exposure (oral or topical), and bee species evaluated (Piovesan et al 2020).…”

“…Given the above, the vast majority of available bee toxicity data have been derived with A. mellifera (Fig. 1; Cham et al 2019;Piovesan et al 2020;Sgolastra et al 2020). Other bee species have thus received considerably less attention.…”

“…Both pesticides are authorized for use in a wide variety of crops in Brazil that depend on pollination (do Prado et al 2020). Subsequently, stingless bees may be exposed to these pesticides both through direct contact with air-suspended molecules and indirectly through the ingestion of pesticide residues present in nectar, pollen or water (MAPA 2021;Piovesan et al 2020). De Oliveira et al (2016, for example, reported that there can be significant transfer of abamectin present in the surrounding atmosphere to pollen.…”