TitleLinden (Tilia cordata) associated bumble bee mortality: Metabolomic analysis of nectar and bee muscle.
Publication TypeJournal Article
Year of Publication2019
AuthorsLande C, Rao S, Morré JT, Galindo G, Kirby J, Reardon PN, Bobe G, Stevens JFrederik
JournalPLoS One
Date Published2019
KeywordsAlkaloids, Animals, Bees, Cholinesterase Inhibitors, Feeding Behavior, Metabolome, Muscles, Plant Nectar, Tilia

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.

Alternate JournalPLoS ONE
PubMed ID31291287
PubMed Central IDPMC6619659
Grant ListS10 OD018518 / OD / NIH HHS / United States
S10 RR022589 / RR / NCRR NIH HHS / United States
S10 RR027878 / RR / NCRR NIH HHS / United States