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).