Fear changes traits and increases survival: a meta‐analysis evaluating the efficacy of antipredator training in captive‐rearing programs

Abstract

Captive rearing is commonly used to support efforts to restore extirpated or diminished wild populations. Many rearing programs include antipredator training in an effort to reduce post-release mortality due to predation, but the value such training adds to restoration efforts is not fully understood. Analyses of antipredator training impacts often focus on changes in prey following training and not the actual effects when prey are exposed to predators. Studies also commonly assess prey traits instead of fitness. However, changes in prey following training may not translate to desired increase in fitness upon release for a selfsustaining population. To consider these relationships, we identified studies that analyzed changes in organisms following both training and lethal exposure to predators. Notably, we identified only 12 studies that analyzed outcomes in both training and lethal exposure settings and found the majority of measurements focused on traits. Although meta-analysis indicated that antipredator training changed prey traits and increased prey survival, relationships between changes in traits and fitness could not be assessed given the rarity of studies that included both outcomes. While these results support the general use of antipredator training, they also suggest that trait changes cannot be reliably used as proxies for fitness impacts. Future work should seek to more clearly measure impacts on fitness and determine when changes in traits can truly be used as a surrogate for training efficacy. These issues reflect recent concerns regarding research on non-consumptive effects and highlight potential avenues for future collaborative research on fear.

Early life experience with predators impacts development, behavior, and post‐translocation outcomes in an endangered amphibian

“…Our study also highlights the importance of data on wild baselines as a point of comparison for ex‐situ behaviors. The majority of previous predator‐training studies in ex situ programs do not evaluate post‐release outcomes (Edwards et al ., 2021; Zhu et al ., 2022); but see (van Heezik, Seddon, & Maloney, 1999; Shier & Owings, 2006; Shier & Owings, 2007; Gaudioso et al ., 2011; D'Anna et al ., 2012; Moseby, Cameron, & Crisp, 2012; Lopes et al ., 2017; Farnsley et al ., 2018; Edwards et al ., 2021; Greggor et al ., 2021; Zhu et al ., 2022). Work is needed to show not just that animals can change their behavior in response to anti‐predator training, but also that such behavioral changes match wild‐type behaviors to result in enhanced survival in the wild.…”

“…Predation is a major cause of mortality in conservation translocations across taxonomic groups (Berger‐Tal, Blumstein, & Swaisgood, 2020). Predator exposure and/or training regimes are among the most common forms of pre‐release “life skills” development (Greggor, Price, & Shier, 2019), with many studies showing the efficacy of such treatments (Shier & Owings, 2006; Tetzlaff et al ., 2019; Zhu et al ., 2022). However, the optimal timing of exposure to predators is often unclear.…”

“…However, the optimal timing of exposure to predators is often unclear. Moreover, even when learning is demonstrated in predator‐training studies, the effects of training on fitness and post‐release outcomes often remain unquantified (Edwards et al ., 2021; Zhu et al ., 2022). In some species, training, and learning may be less critical than developmental “switches.” For example, in amphibians, exposure to predator cues during the tadpole stage can induce changes in morphology, behavior, and fitness (Van Buskirk, McCollum, & Werner, 1997).…”

The fitness consequences of wildlife conservation translocations: a meta-analysis

“…We use the term enrichment broadly to refer to a variety of supportive measures 14 employed by ACTs to offset any maladaptive behavior, physiology, or physical injury incurred during captivity and/or translocation 23,41 . Some examples include fostering pre-release organisms with experienced conspecifics 42 , simulating in situ environments with naturalistic enclosures or antipredator training 43 , implementing a soft-release phase where supplemental feeding and/or shelter are provided 44 , or simply reducing the length of the captive phase 26,45 . Literature reviews suggest that enriched ESR cohorts are more successful post-release compared to un-enriched cohorts 14,23 , but the lack of a wild-reference group in the synthesized findings makes it difficult to conclude whether enrichment strategies produce translocated organisms that are indistinguishable from wild conspecifics with respect to post-release fitness 46 .…”

“…These syntheses are an invaluable resource for applied conservation and management, but their largely narrative format is not conducive to quantitative synthesis across broad and multifactorial datasets while accounting for bias and heterogeneity among studies. Meta-analysis is well equipped to gauge translocation efficacy based on the postrelease performance of animal subjects 23,43,[49][50][51] . Previous meta-analyses are limited to comparisons among translocated cohorts and fail to include a wild-reference group (but see 22 ), therefore, they cannot address whether translocated individuals are as capable as their wild conspecifics at contributing to population viability.…”