Is a strobilurin fungicide capable of inducing histopathological effects on the midgut and Malpighian tubules of honey bees?

Abstract

Bees that forage in agricultural plantations and surroundings are exposed to pesticide residues, which can cause sublethal effects in individuals and consequently compromise the performance of the colony. Regarding the honey bees, beekeepers can be hampered by decreased production of honey and other bee products. Although the effects of insecticides on bees are widely studied for obvious reasons, there is growing evidence that fungicides, too, are not harmless to bees. However, further studies are needed on the effects caused by fungicide residues present in pollen and nectar which are collected and consumed by honey bees. For this reason, we aimed to perform a histopathological diagnosis and cell death immunolabeling in the midgut and Malpighian tubules of Africanized honey bee workers throughout continuous oral exposure (24 h, 48 h, 72 h, 96 h) to low concentrations of picoxystrobin (9 ppb and 18 ppb), a strobilurin fungicide. Although there were no histopathological effects on the Malpighian tubules, an organ that plays a role in excretion, these effects were observed in the midgut of bees exposed to both concentrations of picoxystrobin. Morphological alterations, as well as positive-labeling for cell death, were observed in the midgut of exposed bees over time (from 24 to 96 h after the beginning of exposure). Although the data have shown evidence of intestinal epithelial renewal in response to cytotoxic effects, i.e., recovery after short-time exposure, this organ may have its nutrient absorption functions compromised in the long-term, which may lead to symptoms of malnutrition and affect the individual’s performance, which could, in turn, affect the whole colony.

Keywords:

• Apis mellifera
• cell death
• newly emerged workers
• picoxystrobin

Disclosure statement

No potential conflict of interest was reported by the authors.

Additional information

Funding

This research had financial support from “Fundação de Amparo à Pesquisa do Estado de São Paulo” (FAPESP: 2014/04697-9) and CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) through a master’s degree scholarship for the first author. Authors thank Profa. Dra. Letícia Silva Souto from LADIVE (UFSCar, Sorocaba) for the availability of the microtome (FAPESP: 2015/01424-4, 2017/21097-3), and the PPGBMA (USCar, Sorocaba) for the availability of the Laser Scanning Confocal Microscopy (Pró-Equipamentos: 3420/2013-17, 2610/2014-90), allocated in DBio (Departamento de Biologia da UFSCar, Sorocaba). Authors thanks PTS (Parque Tecnologico de Sorocaba) by infrastructure for bioassays. Our gratitude also goes out to Dr. Osmar Malaspina from CEIS (UNESP, Rio Claro) and the beekeeper Edson Sampaio (COAPIS).