Abstract
Populations of honey bees and other pollinators have declined worldwide in recent years. A variety of stressors have been implicated as potential causes, including agricultural pesticides. Neonicotinoid insecticides, which are widely used and highly toxic to honey bees, have been found in previous analyses of honey bee pollen and comb material. However, the routes of exposure have remained largely undefined. We used LC/MS-MS to analyze samples of honey bees, pollen stored in the hive and several potential exposure routes associated with plantings of neonicotinoid treated maize. Our results demonstrate that bees are exposed to these compounds and several other agricultural pesticides in several ways throughout the foraging period. During spring, extremely high levels of clothianidin and thiamethoxam were found in planter exhaust material produced during the planting of treated maize seed. We also found neonicotinoids in the soil of each field we sampled, including unplanted fields. Plants visited by foraging bees (dandelions) growing near these fields were found to contain neonicotinoids as well. This indicates deposition of neonicotinoids on the flowers, uptake by the root system, or both. Dead bees collected near hive entrances during the spring sampling period were found to contain clothianidin as well, although whether exposure was oral (consuming pollen) or by contact (soil/planter dust) is unclear. We also detected the insecticide clothianidin in pollen collected by bees and stored in the hive. When maize plants in our field reached anthesis, maize pollen from treated seed was found to contain clothianidin and other pesticides; and honey bees in our study readily collected maize pollen. These findings clarify some of the mechanisms by which honey bees may be exposed to agricultural pesticides throughout the growing season. These results have implications for a wide range of large-scale annual cropping systems that utilize neonicotinoid seed treatments.
Highlights
Pollinator health is receiving increased attention as both managed pollinators and native pollinator populations decline worldwide [1,2,3]
Soil collected from areas near our test site revealed that neonicotinoid insecticide residues were present in all samples tested (Table 1), with clothianidin occurring in each field sampled
Maize pollen was frequently collected by foraging honey bees while it was available: maize pollen comprised over 50% of the pollen collected by bees, by volume, in 10 of 20 samples
Summary
Pollinator health is receiving increased attention as both managed pollinators (i.e. honey bees) and native pollinator populations decline worldwide [1,2,3]. Pesticide exposure has received significant attention and recently-published analyses of pollen from managed bees located near agricultural environments demonstrated that many agricultural chemicals (including insecticides, miticides, fungicides and herbicides) are detectable in honey bee wax and pollen samples [5,6]. Of the many compounds detected, the neo-nicotinoid group has arguably received the most attention These compounds act as nicotinic acetylcholine receptor agonists in insects, causing persistent excitation of these receptors and eventually death [7]. This study was initiated in response to reports of bee kills at Indiana apiaries in spring of 2010 These reports coincided with the peak period of maize planting in the area [11]. A herbicide that is commonly used in maize production and is relatively non-toxic to honey bees [12]
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