Context-dependent medicinal effects of anabasine and infection-dependent toxicity in bumble bees

Background
Floral phytochemicals are ubiquitous in nature, and can function both as antimicrobials and as insecticides. Although many phytochemicals act as toxins and deterrents to consumers, the same chemicals may counteract disease and be preferred by infected individuals. The roles of nectar and pollen phytochemicals in pollinator ecology and conservation are complex, with evidence for both toxicity and medicinal effects against parasites. However, it remains unclear how consistent the effects of phytochemicals are across different parasite lineages and environmental conditions, and whether pollinators actively self-medicate with these compounds when infected.
Approach
Here, we test effects of the nectar alkaloid anabasine, found in Nicotiana, on infection intensity, dietary preference, and survival and performance of bumble bees (Bombus impatiens). We examined variation in the effects of anabasine on infection with different lineages of the intestinal parasite Crithidia under pollen-fed and pollen-starved conditions.
Results
We found that anabasine did not reduce infection intensity in individual bees infected with any of four Crithidia lineages that were tested in parallel, nor did anabasine reduce infection intensity in microcolonies of queenless workers. In addition, neither anabasine nor its isomer, nicotine, was preferred by infected bees in choice experiments, and infected bees consumed less anabasine than did uninfected bees under no-choice conditions. Furthermore, anabasine exacerbated the negative effects of infection on bee survival and microcolony performance. Anabasine reduced infection in only one experiment, in which bees were deprived of pollen and post-pupal contact with nestmates. In this experiment, anabasine had antiparasitic effects in bees from only two of four colonies, and infected bees exhibited reduced—rather than increased—phytochemical consumption relative to uninfected bees.
Conclusions
Variation in the effect of anabasine on infection suggests potential modulation of tritrophic interactions by both host genotype and environmental variables. Overall, our results demonstrate that Bombus impatiens prefer diets without nicotine and anabasine, and suggest that the medicinal effects and toxicity of anabasine may be context dependent. Future research should identify the specific environmental and genotypic factors that determine whether nectar phytochemicals have medicinal or deleterious effects on pollinators.

背景
花源植物化学物（floral phytochemicals）在自然界中广泛分布，兼具抗菌与杀虫双重功效。尽管多数植物化学物会对取食者产生毒性并起到驱避作用，但这类物质同样可以对抗病害，且会被受感染的取食者所偏好。花蜜与花粉中的植物化学物在传粉昆虫生态学与保护生物学中的作用机制十分复杂，既有研究证实其可对寄生虫产生毒性，也有研究表明其具备药用功效。然而，目前仍不清楚植物化学物的作用效果在不同寄生虫谱系与环境条件下是否具有一致性，也不清楚受感染的传粉昆虫是否会主动利用这类化合物进行自我药疗。

研究方法
本研究旨在探究烟草属（Nicotiana）植物中存在的花蜜生物碱假木贼碱（anabasine）对北美大黄蜂（Bombus impatiens）的感染强度、取食偏好、存活情况与生长表现的影响。我们分别在喂食花粉与禁食花粉的条件下，探究了假木贼碱对不同谱系肠道寄生虫锥虫属（Crithidia）感染情况的影响差异。

结果
研究发现，无论对同时受试的4个锥虫谱系感染的单个蜜蜂，还是无蜂王工蜂组成的微型蜂群，假木贼碱均未降低其感染强度。此外，在选择饲喂实验中，受感染的蜜蜂既不偏好假木贼碱，也不偏好其异构体尼古丁；而在非选择饲喂条件下，受感染蜜蜂摄入的假木贼碱量低于未感染蜜蜂。进一步而言，假木贼碱会加重感染对蜜蜂存活及微型蜂群生长表现的负面影响。仅在一项实验中，假木贼碱降低了蜜蜂的感染强度：该实验中蜜蜂被剥夺花粉，且成虫后无法与巢伴接触。在该实验中，仅来自4个蜂群中的2个蜂群的蜜蜂，其感染情况会被假木贼碱抑制；且与未感染蜜蜂相比，受感染蜜蜂的植物化学物摄入量反而有所降低。

结论
假木贼碱对感染的作用存在差异，这表明宿主基因型与环境变量均可能调控三营养级互作关系。总体而言，本研究结果证实北美大黄蜂（Bombus impatiens）更倾向于不含尼古丁与假木贼碱的食物，同时表明假木贼碱的药用功效与毒性可能依赖于具体情境。未来研究应明确具体的环境与基因型因素，以此判断花蜜中的植物化学物对传粉昆虫究竟会产生药用还是有害影响。