The Insecticide Imidacloprid Decreases Nannotrigona Stingless Bee Survival and Food Consumption and Modulates the Expression of Detoxification and Immune-Related Genes

Abstract

Stingless bees are ecologically and economically important species in the tropics and subtropics, but there has been little research on the characterization of detoxification systems and immune responses within them. This is critical for understanding their responses to, and defenses against, a variety of environmental stresses, including agrochemicals. Therefore, we studied the detoxification and immune responses of a stingless bee, Nanotrigona perilampoides, which is an important stingless bee that is widely distributed throughout Mexico, including urban areas, and has the potential to be used in commercial pollination. We first determined the LC50 of the neonicotinoid insecticide imidacloprid for foragers of N. perilampoides, then chronically exposed bees for 10 days to imidacloprid at two field-realistic concentrations, LC10 (0.45 ng/µL) or LC20 (0.74 ng/µL), which are respectively 2.7 and 1.3-fold lower than the residues of imidacloprid that have been found in honey (6 ng/g) in central Mexico. We found that exposing N. perilampoides stingless bees to imidacloprid at these concentrations markedly reduced bee survival and food consumption, revealing the great sensitivity of this stingless bee to the insecticide in comparison to honey bees. The expression of detoxification (GSTD1) and immune-related genes (abaecin, defensin1, and hymenopteacin) in N. perilampoides also changed over time in response to imidacloprid. Gene expression was always lower in bees after 8 days of exposure to imidacloprid (LC10 or LC20) than it was after 4 days. Our results demonstrate that N. perilampoides stingless bees are extremely sensitive to imidacloprid, even at low concentrations, and provide greater insight into how stingless bees respond to pesticide toxicity. This is the first study of its kind to look at detoxification systems and immune responses in Mexican stingless bees, an ecologically and economically important taxon.

Evaluation of Afidopyropen Toxicity at Environmentally Relevant Doses to the Asian Honeybee (Apis cerana) Using Physiological and Transcriptome Analysis

“…mellifera workers, and the cumulative toxicity was discovered at 7–8 days followed by the mortalities being dramatically increased and continued until the end of treatment . A similar phenomenon of TRT was observed for the insecticide imidacloprid, and most of the chronic and cumulative toxic effects were detected after 6 days (highest concentration) through laboratory studies on Nannotrigona perilampoides stingless bees . We found a similar trend in mortality from day 5 onward, suggesting that the detoxifying metabolic capacity of A.…”

“…21 A similar phenomenon of TRT was observed for the insecticide imidacloprid, and most of the chronic and cumulative toxic effects were detected after 6 days (highest concentration) through laboratory studies on Nannotrigona perilampoides stingless bees. 40 We found a similar trend in mortality from day 5 onward, suggesting that the detoxifying metabolic capacity of A. cerana bees appeared to have been surpassed or the accumulation of afidopyropen in the bees' bodies was sufficient to cause toxic consequences that increased over time.…”

“…However, when we take into account that bees consumed 0.14 mL of 50% sucrose solution on average each day, we can calculate each newly emerged bee's maximum estimated value LD 50 in 96 h according to Al Naggar et al, 2022. 40 The assessed maximum oral LD 50 was 7.5 μg, which is approximately fifteen times lower than the LD 50 of afidopyropen in A. mellifera (>100 μg/bee). 7 We provide evidence that A. cerana is more sensitive to afidopyropen exposure compared to other species.…”

“…cerana low sensitivity to afidopyropen. However, when we take into account that bees consumed 0.14 mL of 50% sucrose solution on average each day, we can calculate each newly emerged bee’s maximum estimated value LD 50 in 96 h according to Al Naggar et al, 2022 . The assessed maximum oral LD 50 was 7.5 μg, which is approximately fifteen times lower than the LD 50 of afidopyropen in A.…”

Comparison of the Sensitivity of Tetragonisca angustula (Apidae‐Meliponini) and Apis mellifera (Apidae‐Apini) to Three Insecticides (Malathion, Imidacloprid, and Fipronil) Used in Costa Rica

“…Pollination is a crucial ecosystem service to wild plants and crops, and its relevance is well recognized from agronomical, ecological, and economic perspectives (Chaudhary et al, 2015; Guimarães‐Porto et al, 2020; Melathopoulos et al, 2015; Silva et al, 2021). Insects, and particularly bees, are responsible for a significant amount of pollination (Calderone, 2012; Winfree, 2010); conversely, many anthropogenic factors such as habitat destruction, pathogen spread, and agricultural pesticides are known to affect insect pollinators (Abati et al, 2021; Al Naggar et al, 2022; Wagner et al, 2021). For these reasons, bees are a group of major concern within the current global biodiversity crisis (Jacob et al, 2019; Marshman et al, 2019; Wagner, 2020).…”