breeding under pressure: corticosterone is associated with reproductive investment under fluctuating predation risk in a long-lived sea duck

Phenotypic plasticity may enable individuals to cope with predictable and unpredictable environments during their life-cycle. In that context, studying glucocorticoids – corticosterone (CORT) in birds – is relevant because of their primary role in allostasis. Higher baseline CORT levels are classically associated with environmental constraints and lower fitness (the CORT-fitness hypothesis). However, in some environments, higher baseline CORT levels can promote reproduction, therefore being associated with higher fitness (the CORT-adaptation hypothesis). These two hypotheses have been tested in multiple systems, but rarely in a context of fluctuating predation threat.

We used a long-term individual-based monitoring of baseline CORT levels in female common eiders Somateria mollissima (nCORT = 1537; nindividual = 790; 2009-2022) to disentangle the context-dependent links between environmental conditions, CORT and fitness. Importantly, the study population has been facing a drastic increase in predation pressure over the past decades, linked to the recovery of the white-tailed eagle Haliaeetus albicilla. Additionally, eiders breed on open or forested islands, further affecting adult and nest predation risk. This system allowed us to disentangle the relative contributions of within- and among-individual variation in baseline CORT levels under predation.

Supporting the CORT-adaptation hypothesis, baseline CORT levels were positively associated with reproductive investment (clutch size), age and hatching success. By partitioning within- and among-individual effects, we showed that at the individual level, CORT flexibly increased with clutch size and age. Females displaying higher CORT levels were more successful, suggesting a link between CORT and individual quality.

At both the population and individual levels, baseline CORT levels decreased over the study period. This decrease was correlated with an increase in predation risk. Females had reduced baseline CORT when nesting under high eagle abundance or adult predation risk (within-individual effect). Interestingly, apparent plasticity towards adult predation risk was only observed on open islands, likely reflecting habitat-dependent strategies.

Consistent with the CORT-adaptation hypothesis, we show that changes in predation regime not only correlate with changes in reproductive investment, but also with rapid plastic adjustment of glucocorticoid levels and therefore individual strategies to cope with predation risk. Given the correlative nature of our study, we encourage further experimental studies testing for a causal relationship between predation and corticosterone levels.

表型可塑性（Phenotypic plasticity）可使生物个体在生命周期内应对可预测与不可预测的环境变化。在此研究背景下，针对糖皮质激素（glucocorticoids）——鸟类体内的皮质酮（corticosterone, CORT）——的研究具有重要意义，因其在应变稳态（allostasis）中发挥核心调控作用。经典理论认为，较高的基础皮质酮水平与环境约束加剧及适合度下降相关，即皮质酮-适合度假说（CORT-fitness hypothesis）。然而在部分环境中，较高的基础皮质酮水平可促进繁殖过程，进而与更高的个体适合度挂钩，即皮质酮-适应假说（CORT-adaptation hypothesis）。上述两种假说已在多个研究系统中得到验证，但极少在波动的捕食风险背景下开展相关检验。

我们依托2009年至2022年间的长期个体水平监测数据，分析了雌性普通绒鸭（Somateria mollissima）的基础皮质酮水平（皮质酮样本量n_CORT=1537；个体样本量n_individual=790），以厘清环境条件、皮质酮水平与个体适合度之间的情境依赖关联。值得注意的是，过去数十年间，该研究种群面临的捕食压力随白尾海雕（Haliaeetus albicilla）种群恢复而急剧升高。此外，绒鸭的繁殖栖息地可分为开阔岛屿与林岛两类，这一差异进一步影响了成体与鸟巢的捕食风险。本研究系统使得我们得以解析捕食压力下，基础皮质酮水平的个体内变异与个体间变异的相对贡献。

研究结果支持皮质酮-适应假说：基础皮质酮水平与繁殖投入（窝卵数（clutch size））、个体年龄及孵化成功率（hatching success）呈显著正相关。通过拆分个体内与个体间效应，我们发现，在个体层面，皮质酮水平随窝卵数与年龄的增加而灵活升高。基础皮质酮水平更高的雌性个体繁殖成功率也更高，这表明皮质酮水平与个体质量存在显著关联。

在种群与个体两个层面，基础皮质酮水平均随研究周期推进呈现下降趋势。该下降趋势与捕食风险的升高呈显著相关性。当雌性在海雕密度较高或成体捕食风险较高的环境中筑巢时，其基础皮质酮水平会显著降低（个体内效应）。有趣的是，针对成体捕食风险的表观可塑性仅在开阔岛屿生境中被观测到，这可能反映了栖息地依赖的应对策略差异。

与皮质酮-适应假说一致，我们的研究表明，捕食格局的变化不仅与繁殖投入的改变相关，还与糖皮质激素水平的快速塑性调整及个体应对捕食风险的策略变化相关。鉴于本研究属于相关性观测研究，我们呼吁后续开展实验性研究，以检验捕食压力与皮质酮水平之间的因果关系。