Abstract
Linden (Tilia spp.), a profusely flowering temperate tree that provides bees with vital pollen and nectar, has been associated with bumble bee (Bombus spp.) mortality in Europe and North America. Bee deaths have been attributed, with inadequate evidence, to toxicity from mannose in nectar or starvation due to low nectar in late blooming linden. Here, we investigated both factors via untargeted metabolomic analyses of nectar from five T. cordata trees beneath which crawling/dead bumble bees (B. vosnesenskii) were observed, and of thoracic muscle of 28 healthy foraging and 29 crawling bees collected from linden trees on cool mornings (< 30°C). Nectar contained the pyridine alkaloid trigonelline, a weak acetylcholinesterase inhibitor, but no mannose. Principal component analysis of muscle metabolites produced distinct clustering of healthy and crawling bees, with significant differences (P<0.05) in 34 of 123 identified metabolites. Of these, TCA (Krebs) cycle intermediates were strongly represented (pathway analysis; P<0.01), suggesting that the central metabolism is affected in crawling bees. Hence, we propose the following explanation: when ambient temperature is low, bees with energy deficit are unable to maintain the thoracic temperature required for flight, and consequently fall, crawl, and ultimately, die. Energy deficit could occur when bees continue to forage on linden despite limited nectar availability either due to loyalty to a previously energy-rich source or trigonelline-triggered memory/learning impairment, documented earlier with other alkaloids. Thus, the combination of low temperature and nectar volume, resource fidelity, and alkaloids in nectar could explain the unique phenomenon of bumble bee mortality associated with linden.
Highlights
Bees provide critical pollination services in diverse landscapes, and are vital to global economy, food security, and environmental health
At any given time, not every linden tree causes bee mortality, and that not every bee that forages on a linden tree dies
In the thoracic muscles of healthy and crawling bees collected from linden trees in 2016 and 2017, one hundred and fifteen features detected with liquid chromatography–tandem mass spectrometry (LC-MS/MS) matched records in the IROA library of metabolite standards
Summary
Bees provide critical pollination services in diverse landscapes, and are vital to global economy, food security, and environmental health. There have been reports of declines in bee populations due to loss of foraging resources and nesting habitats, pathogens, and pesticides [1,2,3,4,5]. Risks associated with foraging behaviors are critical as bees spend considerable time seeking food resources. Amino acids, lipids, vitamins, and minerals are obtained by bees from floral nectar and pollen to meet their metabolic needs [8,9,10], and the availability of flowers that can provide these resources throughout the life cycle of the colony is critical
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