Effects of pesticide-adjuvant combinations used in almond orchards on olfactory responses to social signals in honey bees (Apis mellifera)

Abstract

Abstract Exposure to agrochemical sprays containing pesticides and tank-mix adjuvants has been implicated in post-bloom mortality, particularly of brood, in honey bee colonies brought into California almond orchards for pollination. Although adjuvants are generally considered to be biologically inert, some adjuvants have exhibited toxicity and sublethal effects, including decreasing survival rates of next-generation queens. Honey bees have a highly developed olfactory system to detect and discriminate among social signals. To investigate the impact of pesticide-adjuvant combinations on honey bee signal perception, we performed electroantennography assays to assess alterations in their olfactory responsiveness to the brood ester pheromone (BEP), the volatile larval pheromone β-ocimene, and the alarm pheromone 2-heptanone. These assays aimed to uncover potential mechanisms underlying changes in social behaviors and reduced brood survival after pesticide exposure. We found that combining the adjuvant Dyne-Amic with the fungicide Tilt (propiconazole) and the insecticide Altacor (chlorantraniliprole) synergistically enhanced olfactory responses to three concentrations of BEP and as well exerted dampening and compensatory effects on responses to 2-heptanone and β-ocimene, respectively. In contrast, exposure to adjuvant alone or the combination of fungicide and insecticide had no effect on olfactory responses to BEP at most concentrations but altered responses to β-ocimene and 2-heptanone. Exposure to Dyne-Amic, Altacor, and Tilt increased BEP signal amplitude, indicating potential changes in olfactory receptor sensitivity or sensilla permeability to odorants. Given that, in a previous study, next-generation queens raised by nurses exposed to the same treated pollen experienced reduced survival, these new findings highlight the potential disruption of social signaling in honey bees and its implications for colony reproductive success.