A meta-analysis of non-consumptive predator effects in arthropods: the influence of organismal and environmental characteristics

Non-consumptive effects (NCEs) – changes in prey behavior or physiology in response to predator threat – are common and can be as strong as consumptive effects. However, our knowledge of NCEs in arthropod systems is lacking. Factors related to study organism and environment have the potential to influence the occurrence and magnitude of NCEs in arthropod systems. While factors such as coevolutionary history of natural enemies and their prey, predator cue, predator or prey feeding mode, and refuge availability have been theoretically and empirically examined, no trends have been proposed for arthropods. We compiled 62 studies, yielding 128 predator–prey interactions, which explicitly examined NCEs in experiments where arthropods were identified to species, using a previously published database of papers from 1990 to 2005 and a new database of papers published from 2006 to 2015. Using these data, we conducted a meta-analysis to explore the influence of organismal and environmental characteristics on the magnitude of predator NCEs. Our analysis addressed the following three questions. 1) Does predator–prey coevolution give rise to stronger NCEs than when predator and prey species did not coevolve? 2) What influence does habitat type and refuge availability have on NCEs? 3) How do predator characteristics (cue type, hunting mode and life stage) and prey characteristics (mobility, life stage, specialization, gregariousness and feeding mode) influence NCEs? We found that while NCEs were similar across most measured characteristics, NCEs on prey activity were significantly stronger when predator and prey shared an evolutionary history. Our results support growing evidence that NCEs have a negative effect on prey traits and that behavioral NCEs are stronger than physiological ones. Additional studies are needed to be confident in any emerging patterns, therefore we identify key gaps in the literature on NCEs in arthropod systems and discuss ideas for moving forward.

非消耗效应（Non-consumptive effects, NCEs）——指猎物因感知捕食者威胁而发生的行为或生理变化——广泛存在，其影响强度可与消耗效应（consumptive effects）相当。然而，当前学界对节肢动物（arthropod）系统中非消耗效应的认知仍存在不足。与研究对象及环境相关的因子，均可能影响节肢动物系统中非消耗效应的发生与强度。尽管天敌与猎物的协同进化历史、捕食者信号、捕食者或猎物的取食模式，以及庇护所可获得性等因子，已在理论与实证层面得到探讨，但目前尚未针对节肢动物系统提出相关规律总结。我们整合了62项研究，涵盖128组捕食者-猎物相互作用，所有研究均通过物种水平鉴定的节肢动物实验，明确考察了非消耗效应；数据来源包括1990年至2005年的已公开论文数据库，以及2006年至2015年新建的论文数据库。基于上述数据集，我们开展了元分析（meta-analysis），以探究生物与环境特征对捕食者介导的非消耗效应强度的影响。本研究旨在解答以下三个核心问题：1）相较于捕食者与猎物未发生协同进化的情形，二者的协同进化是否会产生更强的非消耗效应？2）生境类型与庇护所可获得性对非消耗效应存在何种影响？3）捕食者特征（信号类型、捕食模式与生活史阶段）以及猎物特征（移动性、生活史阶段、特化程度、集群性与取食模式）如何影响非消耗效应？研究结果显示，尽管多数测定特征下的非消耗效应并无显著差异，但当捕食者与猎物共享进化历史时，对猎物活动的非消耗效应显著更强。本研究结果进一步佐证了日益增多的实证证据，即非消耗效应对猎物性状存在负面影响，且行为性非消耗效应的强度显著高于生理性非消耗效应。由于现有研究尚不足以支撑对新兴规律的确定性总结，因此我们明确了节肢动物系统中非消耗效应相关研究的关键空白，并对后续研究方向提出了具体构想。