Behavioral responses across a mosaic of ecosystem states restructure a sea otter-urchin trophic cascade

Consumer and predator foraging behavior can impart profound trait-mediated constraints on community regulation that scale-up to influence the structure and stability of ecosystems. Here we demonstrate how the behavioral response of an apex predator to changes in prey behavior and condition can dramatically alter the role and relative contribution of top-down forcing, depending on the spatial organization of ecosystem states. In this study, a rapid and dramatic decline in the abundance of a meso-predator (Pycnopodia helianthoides) and primary producer (Macrocystis pyrifera, ‘kelp’) coincided with a fundamental change in purple sea urchin (Strongylocentrotus purpuratus) foraging behavior and condition, resulting in a spatial mosaic of kelp forests interspersed with patches of sea urchin barrens. We show that this mosaic of adjacent alternative ecosystem states led to an increase in the number of sea otters (Enhydra lutris nereis) specializing on urchin prey, a population-level increase in urchin consumption, and an increase in sea otter survivorship. We further show that the spatial distribution of sea otter foraging effort for urchin prey was not directly linked to high prey density, but rather was predicted by the distribution of energetically profitable prey. Therefore, we infer that spatially explicit sea otter foraging enhances the resistance of remnant forests to overgrazing, but does not directly contribute to the resilience (recovery) of forests. These results highlight the role of consumer and predator trait-mediated responses to resource mosaics that are common throughout natural ecosystems and enhance understanding of reciprocal feedbacks between top-down and bottom-up forcing on the regional stability of ecosystems.

消费者与捕食者的觅食行为，可通过性状介导的调控机制对群落结构施加深刻约束，该效应可跨尺度放大，进而影响生态系统的结构与稳定性。本研究揭示了顶级捕食者（apex predator）针对猎物行为与状态变化所做出的行为响应，如何依循生态系统状态的空间分布格局，显著改变下行驱动（top-down forcing）的作用角色与相对贡献。
本研究中，一种中型捕食者（meso-predator，向日葵海星*Pycnopodia helianthoides*）与初级生产者（primary producer，巨藻*Macrocystis pyrifera*，俗称海带林，kelp）的丰度出现快速且剧烈的下降，与此同时紫海胆（*Strongylocentrotus purpuratus*）的觅食行为与生理状态发生了根本性转变，最终形成了海带林与海胆荒斑交错分布的空间镶嵌格局。
研究表明，这种相邻交替生态系统状态形成的镶嵌格局，使得专门捕食海胆的海獭（*Enhydra lutris nereis*）数量有所增加，海獭种群的海胆捕食量整体提升，同时海獭的存活率也得到提高。
本研究进一步发现，海獭针对海胆猎物的觅食活动空间分布，并非直接与高猎物密度相关，而是由能量收益最优的猎物分布格局所决定。据此我们推断，具有空间特异性的海獭觅食行为，可增强剩余海带林对过度啃食的抵抗力，但无法直接促进森林生态系统的恢复力（recovery，即恢复能力）。
本研究结果凸显了消费者与捕食者针对自然生态系统中普遍存在的资源镶嵌格局所产生的性状介导响应的重要作用，并加深了我们对下行驱动与上行驱动（bottom-up forcing）之间的双向反馈如何影响生态系统区域稳定性的理解。