Combined Effects of Pesticides and Electromagnetic-Fields on Honeybees: Multi-Stress Exposure.

Daniela Lupi,Antonio Lavazza,Giovanni Zambon,Marco Palamara Mesiano,Mario Colombo,Paolo Tremolada,Maria Beatrice Boniotti,Agnese Adani,Roberto Giacchini,Paolo Parenti,Roberto Benocci,Stefano Bassi

doi:10.3390/insects12080716

Abstract

Simple SummaryMulti-stress conditions are considered the most putative cause of honeybee decline. The ongoing reduction of domestic and natural pollinators is considered a very severe signal of the current loss of biodiversity, and it requires a broad research effort to clarify the causes. In this research, the combined effects of two possible stress sources for bees, pesticides and electromagnetic fields (multi-stress conditions) were analyzed by a field trial. After one year of monitoring, a complex picture of several induced effects was present, especially in the multi-stress site, such as disease appearance (American foulbrood), higher mortality in the underbaskets (common to pesticide-stress site), behavioral alterations (queen changes, excess of both drone-brood deposition and honey storage) and biochemical anomalies (higher ALP activity at the end of the season). The multi-stress site showed the worst health condition of the bee colonies, with only one alive at the end of the experimentation out of the four ones present at the beginning.Honeybee and general pollinator decline is extensively reported in many countries, adding new concern to the general biodiversity loss. Many studies were addressed to assess the causes of pollinator decline, concluding that in most cases multi-stress effects were the most probable ones. In this research, the combined effects of two possible stress sources for bees, pesticides and electromagnetic fields (multi-stress conditions), were analyzed in the field. Three experimental sites were chosen: a control one far from direct anthropogenic stress sources, a pesticide-stress site and multi-stress one, adding to the same exposure to pesticides the presence of an electromagnetic field, coming from a high-voltage electric line. Experimental apiaries were monitored weekly for one year (from April 2017 to April 2018) by means of colony survival, queen activity, storage and brood amount, parasites and pathogens, and several biomarkers in young workers and pupae. Both exposure and effect biomarkers were analysed: among the first, acetylcholinesterase (AChE), catalase (CAT), glutathione S-transferase (GST) and alkaline phosphatase (ALP) and Reactive Oxygen Species (ROS); and among the last, DNA fragmentation (DNAFRAGM) and lipid peroxidation (LPO). Results showed that bee health conditions were the worst in the multi-stress site with only one colony alive out of the four ones present at the beginning. In this site, a complex picture of adverse effects was observed, such as disease appearance (American foulbrood), higher mortality in the underbaskets (common to pesticide-stress site), behavioral alterations (queen changes, excess of honey storage) and biochemical anomalies (higher ALP activity at the end of the season). The overall results clearly indicate that the multi-stress conditions were able to induce biochemical, physiological and behavioral alterations which severely threatened bee colony survival.

Highlights

The hive is a complex system regulated by many biological, chemical and nutritional factors; all the specimens contribute to the family maintenance by a highly coordinated activity
The loss of one hive in the control site resulted in a quite high mortality because of the low number of replicates (1 of 4, 25%), but we evaluate that this collapse was not due to the site characteristics but to an external event due to a new queen coming from market following the loss of the pre-existing queen during the mating flight
This research evidenced that both stress caused negative impacts on exposed colonies, due to disease appearance (American foulbrood), mortality in the underbaskets and behavioral alterations

Summary

Introduction

The hive is a complex system regulated by many biological, chemical and nutritional factors; all the specimens contribute to the family maintenance by a highly coordinated activity. This equilibrium is daily at risk as workers patrol an environment highly modified and full of anthropogenic pollutants, especially in more developed countries. When honeybees are exposed simultaneously to multiple chemicals they may exhibit, as a consequence, synergistic, additive or antagonistic effects [11,27,28]; pesticides may have a fundamental role in compromising colony health and increasing the susceptibility of the colony to pests and pathogens [7,29,30]

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