Imidacloprid-Induced Impairment of Mushroom Bodies and Behavior of the Native Stingless Bee Melipona quadrifasciata anthidioides

Abstract

Declines in pollinator colonies represent a worldwide concern. The widespread use of agricultural pesticides is recognized as a potential cause of these declines. Previous studies have examined the effects of neonicotinoid insecticides such as imidacloprid on pollinator colonies, but these investigations have mainly focused on adult honey bees. Native stingless bees (Hymenoptera: Apidae: Meliponinae) are key pollinators in neotropical areas and are threatened with extinction due to deforestation and pesticide use. Few studies have directly investigated the effects of pesticides on these pollinators. Furthermore, the existing impact studies did not address the issue of larval ingestion of contaminated pollen and nectar, which could potentially have dire consequences for the colony. Here, we assessed the effects of imidacloprid ingestion by stingless bee larvae on their survival, development, neuromorphology and adult walking behavior. Increasing doses of imidacloprid were added to the diet provided to individual worker larvae of the stingless bee Melipona quadrifasciata anthidioides throughout their development. Survival rates above 50% were only observed at insecticide doses lower than 0.0056 µg active ingredient (a.i.)/bee. No sublethal effect on body mass or developmental time was observed in the surviving insects, but the pesticide treatment negatively affected the development of mushroom bodies in the brain and impaired the walking behavior of newly emerged adult workers. Therefore, stingless bee larvae are particularly susceptible to imidacloprid, as it caused both high mortality and sublethal effects that impaired brain development and compromised mobility at the young adult stage. These findings demonstrate the lethal effects of imidacloprid on native stingless bees and provide evidence of novel serious sublethal effects that may compromise colony survival. The ecological and economic importance of neotropical stingless bees as pollinators, their susceptibility to insecticides and the vulnerability of their larvae to insecticide exposure emphasize the importance of studying these species.

The ontogenetic saga of a social brain

“…The morphogenetic field of the MBs is thus formed by concentric layers of proliferative cells. Knowledge of the development of the MBs and other honeybee brain regions such as the optic lobes (Marco Antônio and Hartfelder 2016) has broad scientific interest given that, for example, pesticides used in agriculture to control insects target the brains of larval bees (Tomé et al 2012;Tavares et al 2015). The ontogenetic saga of a social brain Using phalloidin and DAPI staining of wholemount brains, Moda et al (2013) showed clear peduncular organisation in worker larvae in the L5F phase.…”

Consumption of the neonicotinoid thiamethoxam during the larval stage affects the survival and development of the stingless bee, Scaptotrigona aff. depilis

“…However, Kremen et al (2002), Del Sarto et al (2005) and Tomé et al (2015) highlighted the importance of native pollinators in the context of insecticide use in agriculture. Despite their importance as native pollinators in Brazil, the first and only study to date that addressed the exposure of stingless bees during the larval stage to insecticides was published by Tomé et al (2012). In their study, the authors observed several adverse effects of the neonicotinoid imidacloprid on Melipona quadrifasciata anthidioides .…”

Quantification of larval food and its pollen content in the diet of stingless bees – subsidies for toxicity bioassays studies

“…In addition, as each stingless bee larva ingests the entire quantity of food provided, it is possible to know the full dose of ingested toxin (Tomé et al, 2012). In this context, this study provides a foundation for future experiments of stingless bee exposure to potentially toxic substances through the larval food.…”

“…In this context, this study provides a foundation for future experiments of stingless bee exposure to potentially toxic substances through the larval food. Furthermore, in vitro bioassays with stingless bees, for instance, require previously the amount of larval food to be placed on ELISA plates, as evidenced by Tomé et al (2012) and Lima et al (2013). Thus, besides the information of pollen quantifying, the results of the total food content consumed by larvae provided herein, may be used as subsidies for these types of bioassays in stingless bees.…”