Fungicide Contamination Reduces Beneficial Fungi in Bee Bread Based on an Area-Wide Field Study in Honey Bee,Apis mellifera, Colonies

Abstract

Fermentation by fungi converts stored pollen into bee bread that is fed to honey bee larvae, Apis mellifera, so the diversity of fungi in bee bread may be related to its food value. To explore the relationship between fungicide exposure and bee bread fungi, samples of bee bread collected from bee colonies pollinating orchards from 7 locations over 2 years were analyzed for fungicide residues and fungus composition. There were detectable levels of fungicides from regions that were sprayed before bloom. An organic orchard had the highest quantity and variety of fungicides, likely due to the presence of treated orchards within bees' flight range. Aspergillus, Penicillium, Rhizopus, and Cladosporium (beneficial fungi) were the primary fungal isolates found, regardless of habitat differences. There was some variation in fungal components amongst colonies, even within the same apiary. The variable components were Absidia, Alternaria, Aureobasidium, Bipolaris, Fusarium, Geotrichum, Mucor, Nigrospora, Paecilomyces, Scopulariopsis, and Trichoderma. The number of fungal isolates was reduced as an effect of fungicide contamination. Aspergillus abundance was particularly affected by increased fungicide levels, as indicated by Simpson's diversity index. Bee bread showing fungicide contamination originated from colonies, many of which showed chalkbrood symptoms.

Negative effects of pesticides on wild bee communities can be buffered by landscape context

“…Conversely, bees foraging in landscapes dominated by agricultural areas where pesticides are applied, will have higher exposure risk even for pollinators surveyed in orchards with low PUI [62]. Interactions between pesticide regime and landscape have been observed previously by comparing bee diversity in organic versus conventional fields, with benefits of organic farming detected only in agriculturally intensified landscapes [70].…”

“…Altered foraging efficiency or nest recognition could decrease offspring production, but so could increased susceptibility of larvae to pesticides if toxins made it into pollen provisions. Honeybee pollen collected from orchards sprayed with fungicides had fewer beneficial fungal species [62], indicating that digestion of pollen masses by larvae may be altered by fungicide exposure if such mutualisms are important for non-Apis nutrition, as well. At present, most laboratory toxicity tests are conducted on eusocial Apis and Bombus.…”

Honeybee Colony Disorder in Crop Areas: The Role of Pesticides and Viruses

“…Studies have already shown the possible modification of microbial composition both at beebread level [62], [72] and at intestinal level [73]. This modification in the composition of microbiota may lead to dysbiosis [74].…”

Trace-level determination of pyrethroid, neonicotinoid and carboxamide pesticides in beeswax using dispersive solid-phase extraction followed by ultra-high-performance liquid chromatography-tandem mass spectrometry

“…Indeed, these molecules are suspected to cause important problems at very low doses and may contribute to bees' death [12]. Another molecule, boscalid, which is a fungicide of the carboxamide family, may be involved in these disorders [41]. Thus, the study of fungicides in beehive matrices is of growing interest to beekeepers and ecotoxicologists.…”