Food supplementation affects gut microbiota and immunological resistance to parasites in a wild bird species

Abstract
1. Supplemental feeding can increase the overall health of animals but also can have varying consequences for animals dealing with parasites. Furthermore, the mechanism mediating the effect of food supplementation on host-parasite interactions remains poorly understood.
2. The goal of the study was to determine the effect of food supplementation on host defenses against parasitic nest flies and whether host gut microbiota, which can affect immunity, potentially mediates these relationships. In a fully crossed design, I experimentally manipulated the abundance of parasitic nest flies (Protocalliphora sialia) and food availability then characterized the gut microbiota, immune responses, and nest parasite abundance of nestling eastern bluebirds (Sialia sialis).
3. Food supplemented birds had 75% fewer parasites than unsupplemented birds. Parasite abundance decreased throughout the breeding season for unsupplemented birds, but abundance did not change throughout the season for supplemented birds. Food supplementation increased overall fledging success. Parasitism had a sublethal effects on blood loss, but food supplementation mitigated these effects by increasing parasite resistance via the nestling IgY antibody response.
4. Food supplementation increased the gut bacterial diversity in nestlings, which was negatively related to parasite abundance. Food supplementation also increased the relative abundance of Clostridiumspp. in nestlings, which was positively related to their antibody response and negatively related to parasite abundance.
5. Synthesis and applications. Overall, these results suggest that food supplementation, especially early in the breeding season, increases resistance to parasitism during the early life stage of the host, which could be mediated by the effect of supplementation on the gut microbiota. Wildlife food supplementation is a common pastime for humans worldwide and therefore it is important to determine the consequences of this activity on animal health. Furthermore, supplemental feeding could induce resistance to detrimental parasites (e.g. invasive parasites) in hosts when management of the parasite is not immediately possible.

摘要
1. 补充投喂（supplemental feeding）可提升动物的整体健康状态，但对受寄生虫感染的动物却可能产生多样的影响。此外，介导食物补给对宿主-寄生虫互作效应的调控机制仍知之甚少。
2. 本研究旨在明确食物补给对宿主抵御寄生巢蝇的效应，以及可影响宿主免疫的肠道菌群（gut microbiota）是否潜在介导了这一关联。本研究采用完全交叉实验设计，人为调控寄生巢蝇（Protocalliphora sialia）的种群丰度与食物可获得性，随后对东蓝鸲（Sialia sialis）雏鸟的肠道菌群、免疫应答及巢内寄生虫丰度进行表征分析。
3. 接受食物补给的雏鸟，其体内寄生虫丰度较未补给组低75%。未补给组雏鸟的寄生虫丰度随繁殖季推进逐渐降低，而补给组雏鸟的寄生虫丰度在整个繁殖季无显著变化。食物补给可提升整体雏鸟离巢成功率。寄生感染会引发亚致死性失血，但食物补给可通过增强雏鸟的IgY抗体应答以提升抗寄生虫能力，从而缓解该类效应。
4. 食物补给可提升雏鸟的肠道细菌多样性，该多样性与寄生虫丰度呈负相关。此外，食物补给还可增加雏鸟体内梭菌属（Clostridium spp.）的相对丰度，该类群丰度与雏鸟的抗体应答呈正相关，与寄生虫丰度呈负相关。
5. 综合与应用。总体而言，本研究结果表明，食物补给（尤其在繁殖季早期）可提升宿主早期生命阶段的抗寄生虫能力，该效应或通过补给对肠道菌群的调控作用得以介导。全球范围内，人类开展野生动物补充投喂已是一项常见活动，因此明确该行为对动物健康的影响至关重要。此外，在无法立即开展寄生虫防控的场景下，补充投喂可诱导宿主对有害寄生虫（如入侵性寄生虫）产生抗性。