Inter-aviary distance and visual access influence conservation breeding outcomes in a territorial, endangered bird

Funding for setting up the housing database was provided by the UK’s Biotechnology and Biological Sciences Research Council (BBSRC; grant BB/G023913/2 to C.R.).Species extinctions are becoming a global crisis, affecting biodiversity and ecosystem services, with island populations being particularly vulnerable. In response, conservation managers are increasingly turning to ex situ conservation breeding programs to establish assurance populations and provide a source for release and re-establishment of wild populations. The 'Alalā (Hawaiian crow, Corvus hawaiiensis) is a critically endangered and territorial island corvid that became extinct in the wild in 2002, following a severe and prolonged population decline during the late 20th century. Surviving individuals of the species were brought into captivity to establish an assurance population to serve as a source for reintroduction, which commenced in 2016. We analyzed the extent to which a range of captive housing conditions impact 'Alalā reproductive success, using 19 years of breeding program data. We found that reproductive success was most strongly affected by the distance between aviaries and their closest neighbors and whether breeding pairs had visual access to other adult conspecifics. Pairs located in aviaries that were more spatially isolated and without visual access to conspecifics were more likely to produce fertile eggs than pairs housed in aviaries that were closer to others or those with visual access to other birds. Our results have direct management implications relevant to the design of conservation breeding centers geared towards the recovery of endangered, territorial bird species. Moreover, since suboptimal housing conditions can increase stress levels in captive birds, our findings are also relevant to improving animal welfare for 'Alalā and other species in conservation breeding programs.PostprintPeer reviewe

The influence of pair duration on reproductive success in the monogamous ‘Alalā (Hawaiian crow, Corvus hawaiiensis)

Conservation breeding program practitioners select potential mates in an attempt to maximize pair compatibility and maintain genetic diversity. Therefore, pair duration, or the number of breeding seasons that individuals retain the same mate, is practitioner-determined in these settings. There is a critical need to evaluate whether pair duration influences reproductive success in ex situ assurance populations, particularly for socially monogamous species. The ‘Alalā (Hawaiian crow, Corvus hawaiiensis) is a monogamous forest bird that is currently extinct in the wild. Today, ‘Alalā exist only in human care for intensive conservation breeding. We analyzed breeding program data from 2018-2021 to determine the effects of ‘Alalā pair duration and age on reproduction (nest building, egg laying, hatching, and fledging). We found that pair duration does not influence reproductive outcomes, and thus practitioners can be more proactive when re-pairing birds. Female and male age, on the other hand, influenced the probability of nest building, clutch production, and overall reproductive success. Nest building and clutch production probabilities were high (near 1) and stable as females aged from 2 to ~ 12 years old, declining sharply thereafter. In males, overall reproductive success (from building robust nests to rearing at least one nestling to fledge) increased with age from 2 to ~ 9 years old, peaked and reached an asymptote with males ≳ 9 to ~ 13 years old, and decreased in males ≳ 13 years old. Thus, integrating age into the pair selection process will increase the likelihood of achieving conservation goals. To our knowledge, we are the first to utilize empirical pair duration results to provide specific management recommendations for mate selection in an avian conservation breeding program. Our findings have critical utility for guiding ‘Alalā pairing decisions, and more broadly underscore the importance of evaluating mate retention and selection protocols in other conservation breeding programs

Preliminary observations of tool-processing behaviour in Hawaiian crows Corvus hawaiiensis

This project was funded through a BBSRC David Phillips Fellowship (BB/G023913/2 to C.R.), and a PhD studentship by the BBSRC and the University of St Andrews (to B.K.). Funding for the ‘Alalā conservation breeding programme was provided by the U.S. Fish and Wildlife Service, State of Hawai‘i Division of Forestry and Wildlife, Moore Family Foundation, several anonymous donors, and San Diego Zoo Global.Very few animal species habitually make and use foraging tools. We recently discovered that the Hawaiian crow is a highly skilled, natural tool user. Most captive adults in our experiment spontaneously used sticks to access out-of-reach food from a range of extraction tasks, exhibiting a surprising degree of dexterity. Moreover, many birds modified tools before or during deployment, and some even manufactured tools from raw materials. In this invited addendum article, we describe and discuss these observations in more detail. Our preliminary data, and comparisons with the better-studied New Caledonian crow, suggest that the Hawaiian crow has extensive tool-modification and manufacture abilities. To chart the full extent of the species’ natural tool-making repertoire, we have started conducting dedicated experiments where subjects are given access to suitable raw materials for tool manufacture, but not ready-to-use tools.Publisher PDFPeer reviewe

Discovery of species-wide tool use in the Hawaiian crow

Funding from the Biotechnology and Biological Sciences Research Council, UK (BBSRC; grant BB/G023913/2 to C.R., and studentship to B.C.K.), the University of St Andrews (C.R.), JASSO (S.S.), and the Royal Society of London (M.B.M.). Funding for thecaptive ‘Alala propagation programme was provided by the U.S. Fish and Wildlife Service, Hawai‘i Division of Forestry and Wildlife, Moore Family Foundation, Marisla Foundation, several anonymous donors, and San Diego Zoo Global.Only a handful of bird species are known to use foraging tools in the wild1. Amongst them, the New Caledonian crow (Corvus moneduloides) stands out with its sophisticated tool-making skills2, 3. Despite considerable speculation, the evolutionary origins of this species’ remarkable tool behaviour remain largely unknown, not least because no naturally tool-using congeners have yet been identified that would enable informative comparisons4. Here we show that another tropical corvid, the ‘Alalā (C. hawaiiensis; Hawaiian crow), is a highly dexterous tool user. Although the ‘Alalā became extinct in the wild in the early 2000s, and currently survives only in captivity5, at least two lines of evidence suggest that tool use is part of the species’ natural behavioural repertoire: juveniles develop functional tool use without training, or social input from adults; and proficient tool use is a species-wide capacity. ‘Alalā and New Caledonian crows evolved in similar environments on remote tropical islands, yet are only distantly related6, suggesting that their technical abilities arose convergently. This supports the idea that avian foraging tool use is facilitated by ecological conditions typical of islands, such as reduced competition for embedded prey and low predation risk4, 7. Our discovery creates exciting opportunities for comparative research on multiple tool-using and non-tool-using corvid species. Such work will in turn pave the way for replicated cross-taxonomic comparisons with the primate lineage, enabling valuable insights into the evolutionary origins of tool-using behaviour.PostprintPeer reviewe

Neratinib in the extended adjuvant treatment of patients from Asia with early-stage HER2+ breast cancer after trastuzumab-based therapy: exploratory analyses from the phase III ExteNET trial

published_or_final_versio

DataSheet_1_The influence of pair duration on reproductive success in the monogamous ‘Alalā (Hawaiian crow, Corvus hawaiiensis).zip

Conservation breeding program practitioners select potential mates in an attempt to maximize pair compatibility and maintain genetic diversity. Therefore, pair duration, or the number of breeding seasons that individuals retain the same mate, is practitioner-determined in these settings. There is a critical need to evaluate whether pair duration influences reproductive success in ex situ assurance populations, particularly for socially monogamous species. The ‘Alalā (Hawaiian crow, Corvus hawaiiensis) is a monogamous forest bird that is currently extinct in the wild. Today, ‘Alalā exist only in human care for intensive conservation breeding. We analyzed breeding program data from 2018-2021 to determine the effects of ‘Alalā pair duration and age on reproduction (nest building, egg laying, hatching, and fledging). We found that pair duration does not influence reproductive outcomes, and thus practitioners can be more proactive when re-pairing birds. Female and male age, on the other hand, influenced the probability of nest building, clutch production, and overall reproductive success. Nest building and clutch production probabilities were high (near 1) and stable as females aged from 2 to ~ 12 years old, declining sharply thereafter. In males, overall reproductive success (from building robust nests to rearing at least one nestling to fledge) increased with age from 2 to ~ 9 years old, peaked and reached an asymptote with males ≳ 9 to ~ 13 years old, and decreased in males ≳ 13 years old. Thus, integrating age into the pair selection process will increase the likelihood of achieving conservation goals. To our knowledge, we are the first to utilize empirical pair duration results to provide specific management recommendations for mate selection in an avian conservation breeding program. Our findings have critical utility for guiding ‘Alalā pairing decisions, and more broadly underscore the importance of evaluating mate retention and selection protocols in other conservation breeding programs.</p

Pre-release training, predator interactions and evidence for persistence of anti-predator behavior in reintroduced `alalā, Hawaiian crow

Animal translocations commonly fail due to predation after release, especially if animals are reared in human care, away from natural predation pressure. Anti-predator training can be a useful tool for combating the predator naivety of released animals, but its effective implementation requires attention to numerous details. We present the step-by-step development of an anti-predator training regime, tailored to the critically endangered `alalā (Corvus hawaiiensis). `Alalā are the last remaining corvid species of the Hawaiian islands, and historically the level of predation they experienced from the Hawaiian hawk, `io (Buteo solitarius) is unclear. However, one factor thought to compromise outcomes of earlier attempts to reintroduce `alalā in the 1990′s was predation by `io, motivating the development of anti-predator training for recent `alalā releases. We documented evidence for what appears to be competent anti-predator behavior in conservation-bred `alalā, with a range of behavioral strategies for coping with `io observed during a series of controlled presentations of `io and `io-related stimuli. These behavioral responses included vigilance, alarm calling, and mobbing during experimental trials conducted in release training aviaries. Our results did not conclusively establish that anti-predator learning occurred as a result of the training, or that the training produced enhanced survival. However, following release, `io-`alalā encounters were observed on more than 35 occasions, and `alalā responses mirrored those observed pre-release, including the first ever recorded mobbing interactions by juvenile flocks of `alalā in the wild. While it is unclear the extent to which training encouraged these species-appropriate anti-predator responses, their occurrence suggests that the `alalā has retained and can express defensive behavioral strategies. By documenting the design process, training execution and behavioral outcomes in `alalā, we highlight details that other reintroduction programs may need to consider when preparing animals for reintroduction alongside natural predators

Reduction of genetic diversity in ‘Alalā (Hawaiian crow; <em>Corvus hawaiiensis</em>) between the late 1800s and the late 1900s

Genetic and genomic data are increasingly used to aid conservation management of endangered species by providing insights into evolutionary histories, factors associated with extinction risks, and potential for future adaptation. For the ‘Alalā, or Hawaiian crow (Corvus hawaiiensis), genetic concerns include negative correlations between inbreeding and hatching success. However, it is unclear if low genetic diversity and inbreeding depression are consequences of a historical population bottleneck, or if ‘Alalā had historically low genetic diversity that predated human influence, perhaps as a result of earlier declines or founding events. In this study, we applied a hybridization-based sequence capture to generate a genome-wide single nucleotide polymorphism (SNP) dataset for comparing historical specimens collected in the 1890s, when ‘Alalā were more numerous, to samples taken between 1973 and 1998, when ‘Alalā population densities were near the lowest documented levels in the wild, prior to all individuals being collected for captive rearing. We found low genome-wide diversity in both sample groups, however, the modern sample group (1973 to 1998 cohort) exhibited relatively fewer polymorphic alleles, a lower proportion of polymorphic loci, and lower observed heterozygosity, consistent with a population decline and potential bottleneck effects. These results combined with a current low population size highlight the importance of continued efforts by conservation managers to mitigate inbreeding and maintain founder representation to preserve what genetic diversity remains

A High-Quality, Long-Read De Novo Genome Assembly to Aid Conservation of Hawaiiʻs Last Remaining Crow Species

Genome-level data can provide researchers with unprecedented precision to examine the causes and genetic consequences of population declines, which can inform conservation management. Here, we present a high-quality, long-read, de novo genome assembly for one of the world&rsquo;s most endangered bird species, the ʻAlalā (Corvus hawaiiensis; Hawaiian crow). As the only remaining native crow species in Hawaiʻi, the ʻAlalā survived solely in a captive-breeding program from 2002 until 2016, at which point a long-term reintroduction program was initiated. The high-quality genome assembly was generated to lay the foundation for both comparative genomics studies and the development of population-level genomic tools that will aid conservation and recovery efforts. We illustrate how the quality of this assembly places it amongst the very best avian genomes assembled to date, comparable to intensively studied model systems. We describe the genome architecture in terms of repetitive elements and runs of homozygosity, and we show that compared with more outbred species, the ʻAlalā genome is substantially more homozygous. We also provide annotations for a subset of immunity genes that are likely to be important in conservation management, and we discuss how this genome is currently being used as a roadmap for downstream conservation applications