Discussion
Phenotypic traits involved in arduous or risky components of life history can exert strong selective pressure. Animals bred in captivity for release to the wild as a conservation intervention should ideally conform to optimal phenotypes for surviving these challenges (Crateset al. 2022). In this study, I present the first multi-species evaluation of the prevalence and fitness impact of captive wing phenotypes among birds. I found the wing shapes of captive birds differed to wild conspecifics in a quarter of species examined. These changes usually involved the most distal primary feathers forming the wing tip or the secondary feather length. Wing tip shape determines flight performance (Lockwood et al. 1998; Swaddle & Lockwood 2003), but whether the changes I report result in impaired flight ability remains unclear. However, this possibility is supported by evidence that a shorter P10 in released juvenile captive orange-bellied parrots incurred a fitness cost. Juveniles with wild wing phenotypes were more than twice as likely to survive the first year of life than individuals with only a 1mm shorter P10. This is the first demonstration that altered wing phenotypes are widespread among captive-bred birds and that these changes incur a fitness cost post release.
Orange-bellied parrots are the beneficiary of careful genetic management and professional husbandry techniques in the large-scale, professional captive-breeding for reintroduction program (Pritchard et al.2022). Despite this care, subtle changes to wing phenotypes emerged in captivity (Stojanovic et al. 2021), despite similarities in other components of phenotype like overall body size (Stojanovic et al.2019). Juvenile orange-bellied parrots face a gauntlet of obstacles to survival of their first year of life (Stojanovic et al. 2020b; Stojanovic et al. 2022) – perhaps the likely increase in drag of a rounder wing tip (Tucker 1995; Minias et al. 2015) is enough to further disadvantage captive phenotypes during long flights. At the breeding ground, post-release survival of captive-bred parrots is very high (Smales et al. 2000), indicating stronger selection occurs during migration when juveniles are developing their survival skills and physical endurance.
My results raise important new questions both for orange-bellied parrots and other conservation breeding programs more generally. Firstly, why is the length of flight feathers of birds so plastic among so many species? Whether wing shape is under genetic control or shaped by the environment is not clear, and clarifying the importance of these potential forces on feather development may provide insight into how to correct captive wing phenotypes. Second, why are the distal feathers so prone to change? The forces exerted by flight are greatest at the wing tip (Lockwood et al.1998) and many species in this study had altered P10 lengths (both significant and indicative effects). Investigating the relationship between feather development and curtailed flight in captive environments may help explain why distal flight feather length is plastic. Third, can individuals with captive wing phenotypes revert to a wild phenotype? If feather growth is at least partly affected by environment, it is conceivable that individuals with captive wing phenotypes could be experimentally manipulated before release to optimize wing shape (e.g. with flight training). Fourth, why do captive wing phenotypes incur a fitness cost, and is this universal? Rounded wing tips produce more drag than pointed ones (Lockwood et al. 1998), but the direct consequences of captive wing phenotypes on migration success is unknown, especially because the changes I report here vary in their magnitude among species. Understanding the aerodynamic cost of captive wing phenotypes is important for optimizing survival of captive-bred migratory birds.
Captive phenotypes vary from obvious to subtle deviations from the optimal wild type. I show a mere 1mm reduction in the length of a single feather significantly elevates juvenile mortality. This surprising consequence of a seemingly trivial phenotypic change is an important reminder that captive breeding for conservation is not straightforward. Importantly, the changes to wing shape I report would go unnoticed using indices of wing shape such as the hand wing index (Sheard et al.2020) because LW and LP (which are important for calculating this index) were unaffected by captivity. This result reaffirms that detailed surveillance is crucial for detecting subtle deviations from the wild phenotype. Ensuring that captive animals are in optimal condition for life in the wild is especially crucial for species that experience strong phenotypic selection from some component of life history (Davis et al. 2020; Crates et al. 2022). However, surveillance for altered captive phenotypes is negligible despite the risks that these changes pose to the success of release programs (Crates et al. 2022). I argue captive breeding programs should (i) clearly identify components of phenotype that could impose strong selection (e.g. migration, traits associated with foraging such as the ability to capture/subdue prey, exaggerated sexual signals), (ii) establish baseline information about variation in wild phenotypes for identified traits, (iii) surveil captive populations for extreme variance in these traits, (iv) where changes are detected, identify the mechanisms driving them, and (v) quantify the impacts of captive phenotypes on release success. Rapid post-release mortality of phenotypically maladapted animals is a waste of conservation resources, may not benefit wild populations and is ethically problematic. This may be overcome by focusing on the phenotypic quality (not quantity) of animals produced so that the likelihood of post-release survival is increased (Crates et al. 2022). Given the wide diversity of taxa held in zoological collections globally (Conde et al. 2011), this study is likely only the tip of an iceberg of subtle phenotypic changes are overlooked among captive-bred animals. Implementing the five steps above is a good start for identifying the scale and magnitude of this conservation challenge, which is likely to become increasingly important as the global extinction crisis forces more species into captive breeding programs (IUCN Conservation planning specialist group 2020).