Department of Crop and Soil Science, Oregon State University, Corvallis, Oregon, United States of America.
Department of Chemistry, Oregon State University, Corvallis, Oregon, United States of America.
PLoS One. 2019 Jul 10;14(7):e0218406. doi: 10.1371/journal.pone.0218406. eCollection 2019.
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.
椴树（Tilia spp.）是一种开花繁茂的温带树木，为蜜蜂提供重要的花粉和花蜜，与欧洲和北美的熊蜂（Bombus spp.）死亡有关。由于花蜜中的甘露糖或由于晚开花的椴树花蜜含量低而导致的饥饿，蜜蜂的死亡归因于证据不足的毒性。在这里，我们通过对五棵 T. cordata 树下爬行/死亡的熊蜂（B. vosnesenskii）和从凉爽早晨（<30°C）的椴树上采集的 28 只健康觅食和 29 只爬行蜜蜂的胸部肌肉进行非靶向代谢组学分析，调查了这两个因素。花蜜中含有吡啶生物碱三叶草碱，这是一种弱乙酰胆碱酯酶抑制剂，但不含甘露糖。肌肉代谢物的主成分分析产生了健康和爬行蜜蜂的明显聚类，在 123 种鉴定的代谢物中有 34 种存在显著差异（P<0.05）。其中，三羧酸（Krebs）循环中间体含量较高（途径分析；P<0.01），表明爬行蜜蜂的中央代谢受到影响。因此，我们提出以下解释：当环境温度较低时，能量不足的蜜蜂无法维持飞行所需的胸部温度，因此会坠落、爬行，最终死亡。当蜜蜂继续在椴树上觅食，尽管花蜜供应有限，它们可能会因为对以前富含能量的来源的忠诚或三叶草碱引发的记忆/学习障碍而继续觅食，以前有其他生物碱记录了这一点。因此，低温和花蜜量、资源保真度以及花蜜中的生物碱的结合可以解释与椴树相关的独特的熊蜂死亡现象。
