Age‐dependent effects of developmental experience on morphology, performance, dispersal and survival in a translocated, endangered species

Abstract

1. While ex situ breeding programs are critical tools for species recovery, translocations using animals reared under human care can face low success rates, often related to increased dispersal and reduced survival. These issues may be related to a mismatch between ex situ environments and natural habitats. Natal habitat preference induction, wherein individuals seek out habitat similar to that they experienced during development, may provide one explanation for this phenomenon. While exposure to naturalistic environments and pre-release training can mitigate these issues, there may be developmental windows within which these sorts of experiences are most transformative.2. We characterized the impacts of environmental experience at different developmental stages on morphology, performance and post-translocation dispersal and survival in the endangered mountain yellow-legged frog Rana muscosa. We exposed frogs of different ages (N = 146 one-year-olds, hereafter juveniles; N = 110 two-year-olds, hereafter subadults) to different water flow regimes to mimic stream conditions of reintroduction sites. We measured morphology and swimming performance before and after treatment. Frogs were translocated into the wild and monitored to collect data on movement and survival.3. Stream experience resulted in significantly longer proportional limb lengths and improved swimming performance for juvenile but not subadult frogs. 4. After translocation, stream experienced subadults exhibited significantly lower post-release movement than control subadults. There was no effect of treatment on juvenile movement, which was significantly higher than in subadults.5. Stream experience significantly boosted apparent survival for juveniles but not subadults, but subadults exhibited higher survival overall.6. Synthesis and applications. Our results suggest that early-life experience with naturalistic conditions in ex situ facilities can significantly impact morphology, performance and post-translocation movement and survival, and that the effects are age dependent. Pre-release training is a vital component of

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

“…Our results underscore the importance of tailoring pre‐translocation environments and experience to particular developmental stages (Tetzlaff et al ., 2019; Hammond et al ., 2022). The optimal time at which to expose animals to predators depends not just on the species' ecology and the age at which they are released, but also on the delay between pre‐release treatments and translocation.…”

“…We used a single two‐striped garter snake Thamnophis hammondii , housed in a separate room from the frogs for all predator stimuli. This species co‐occurs with R. muscosa and has been documented preying upon reintroduced frogs (Hammond et al ., 2022). We have not observed this species at the release site that was used for this study (the site to be used was unknown when developing the project), though there are observations at nearby locations.…”

“…Early life stages can also act as key, flexible periods in which external cues may trigger phenotypic trajectories that are adaptive in different environments (Moran, 1992; Bohenek & Resetarits, 2018). In the context of ex‐situ breeding programs, it is critical to consider such developmental impacts to avoid phenotypic mismatches, wherein traits associated with human‐managed rearing are maladapted for natural environments (Stringwell et al ., 2014; Clarke, Fraser, & Purchase, 2016), with critical consequences for reintroduction success (Tetzlaff, Sperry, & DeGregorio, 2019; Hammond et al ., 2022).…”

“…Here, we use an ex‐situ breeding and translocation program for the endangered mountain yellow‐legged frog Rana muscosa as an opportunity to evaluate whether early life experience with predators impacts post‐translocation outcomes. R. muscosa is predated upon by many species, with resulting impacts on translocation success (Hammond et al ., 2022). We tested whether, during the tadpole stage, R. muscosa exhibits morphological, behavioral, and developmental changes after exposure to a natural predator, the two‐striped garter snake Thamnophis hammondii .…”

Translocation in a fragmented river provides demographic benefits for imperiled fishes

“…Translocation above barriers can aid conservation by augmenting populations and mitigating the effects of habitat fragmentation and loss within a species' native range. Translocations might be useful where managers desire to accomplish multiple objectives, such as providing access to important habitats upstream of barriers for native species while precluding dispersal by invasive species (e.g., Rahel & McLaughlin, 2018), creating population redundancy for imperiled species (Healy et al, 2020; Johnson et al, 2022), expanding or augmenting a species' distribution in fragmented ecosystems (Harig & Fausch, 2002; Nissen et al, 2023; White et al, 2003), or aiding in the recovery of species in rapid decline (Hammond et al, 2022; Sheller et al, 2006). Studies of conservation translocations have focused on birds and mammals, with fewer studies on fishes (reviewed by Bubac et al, 2019), and defining success can be difficult if objectives are not explicitly stated a priori (Bubac et al, 2019; Ewen et al, 2014; Minckley, 1995).…”