Correction: Behavioural ethogram to inform ex-situ initiatives for a critically endangered Bird: the case of the Plains-wanderer

Monique Van Sluys^1*Yvette Pauligk²Alicia Burns³Mark O'Riordan⁴Richard Matkovics⁵Chris Hartnett⁶Benjamin James Pitcher^7,8

• ¹Taronga Institute of Science and Learning, Taronga Conservation Society Australia, Mosman, Australia
• ²Life Sciences, Werribee Open Range Zoo, Werribee, Australia
• ³Cluster of excellence Science of Intelligence, Berlin, Germany
• ⁴Conservation Division, Taronga Western Plains Zoo, Dubbo, Australia
• ⁵Taronga Zoo Sydney, Mosman, Australia
• ⁶Zoos Victoria, Parkville, Australia
• ⁷Taronga Institute of Science and Learning, Mosman, Australia
• ⁸Macquarie University Faculty of Science and Engineering, Macquarie Park, Australia

The functional importance of animal behaviour for the success and effectiveness of conservation management projects has been increasingly recognised in recent years (Greggor et al., 2019;Greggor et al., 2020). Conservation breeding and translocation programs have been established to safeguard species from extinction and set up viable breeding populations for future releases, and a vital element to increase the probability of success of these programs is the understanding of the target species' behaviour (Berger-Tal et al., 2019). A thorough understanding of behaviour is essential to a species recovery's efforts (Sutherland, 1998), not only to inform management and husbandry decisions, but critically, to ensure optimal survival of released animals and their offspring. Zoos play a critical role in the recovery of threatened wildlife due to their husbandry, welfare, veterinary and research skillset, and the opportunities they create for in-depth analysis of animal behaviour. The establishment of a successful zoo-based breeding population for conservation purposes relies on a great understanding of the species biology, behaviour, physiology, and dietary requirements, among others (Sutherland, 1998).At the early stages of an ex-situ breeding program for endangered species, when there's little evidence of husbandry requirements, or a desire to know more about the species' responses to husbandry and management (Rose and Riley, 2021), the understanding of species-specific behaviours becomes critical. An ethogram is a basic tool to the understanding of animal behaviour by clearly defining, describing, and classifying distinct behaviours commonly exhibited by a species (Fern et al., 2022). Defining animal behaviour requires careful observation and the use of measurable markers to quantify those behaviours. At the early stages of an ex-situ breeding program for endangered species, when there is a lack of evidence for the care of that species in the breeding institution, or a desire to know more about the species' responses to husbandry and management (Rose and Riley, 2021), the understanding of species-specific behaviours becomes critical. By first observing behaviour and attempting to interpret their function, animal carers will be able to use this knowledge to adjust husbandry practices and improve welfare and conservation outcomes.Multiple facilities or institutions may be involved in recovery breeding programs. This is desirable to share risk across several locations but is also often a necessity due to resource limitations and geographical spread. These facilities may have different staff, husbandry procedures and routines, as well as different enclosures and environmental conditions, all of which can lead to variations in both the behaviour of animals and how information is recorded and interpreted. To ensure successful breeding and reintroduction programs we needit is important to understand behaviour and establish universal, standardised ethograms that can be used by multiple programs and institutions to compare behaviours of both wild and captive populations and understand breeding behaviour to increase the likelihood of success. Without information on the triggers of breeding and reproductive success, including both behavioural and environmental triggers, efforts to curb the current decline in population numbers are severely hindered.An ethogram is a basic tool to the understanding of animal behaviour. An ethogram clearly defines, describes, and classifies distinct behaviours commonly exhibited by a species (Fern et al., 2022).When all partner institutions refer to the same behaviours, it increases objectivity and allows for comparisons among them. Recent calls for consistency in defining and coding animal behaviour have stemmed from variation in how behaviours are defined within and across species, which could have implications for reproducibility and comparability of results (Fern et al., 2022). Ethograms are also relevant for identifying and advising on age-related issues that might compromise the welfare of individual birds.The Plains-wanderer, Pedionomus torquatus, is a ground-dwelling, native grassland specialist bird endemic to Australia (Baker-Gabb et al., 2016), and the sole member of the Pedionomidae family.The species is critically endangered and considered of high conservation significance (BirdLife International, 2022;Jetz et al., 2014;McClure et al., 2023). It has the third highest EDGE score for a bird species (McClure et al., 2023) reflecting both the high evolutionary distinctiveness and extinction probability of the species. The closest related species to the Plains-wanderer are South American seedsnipes (Olson and Steadman, 1981). Population declines in the wild have mostly been associated with the conversion of native grasslands to crops and dense introduced pastures (Commonwealth of Australia, 2016) and climate extremes, both drought and excessive wet years (Antos andSchultz, 2019, Parker et al., 2021). Current population estimates across its range suggest a wild population of less than 500 individuals and trending downward (Antos and Schultz, 2019).Plains-wanderers are solitary and occupy home ranges of about 12ha (Baker-Gabb et al., 1990); Uuncommon among birds, females are larger and more conspicuous than the males. Plains-wanderers are considered polyandrous, and the male takes the major role in incubating and caring for the young (Bennett, 1983). Recent tracking of Plains-wanderers provided critical information about habitat use for different behaviours and times of daythe Plains-wanderer tends to forage in denser grassland patches than those preferred as nocturnal roosting sites (Nugent et al., 2022). Due to the elusive nature of the Plains-wanderer and resulting challenges with direct observations, little is known about its behavioural repertoire (Bennett, 1983, Baker-Gabb 1988;Nugent et al., 2022), limited to published notes of chance encounters (Purnell 1915, Hopton andCarpenter 2021) or as unpublished anecdotal records.As part of the recovery efforts for the Plains-wanderer (Commonwealth of Australia, 2016), an exsitu conservation breeding program was established to safeguard the species from extinction and set up a viable breeding population for future translocations to its original range. Specifically, the Recovery Plan (Commonwealth of Australia, 2016) identifies developing and implementing a robust, targeted, conservation breeding strategy as a priority conservation action. This initiative is a joint program across five zoological institutions, supported by the Plains-wanderer National Recovery Team. The goal of the ex-situ breeding program is to provide 15-20 years of respite from the current high risk of extinction, while appropriate site-based conservation actions are implemented. A thorough understanding of Plains-wanderer behaviour is essential to this recovery plan, not only to inform management and husbandry decisions, but critically, to ensure optimum survival of released birds and their offspring. While information can be gathered from wild populations, for this cryptic species, the ex-situ population provides a unique opportunity to observe, document and better understand detailed data about the behaviour of the species, particularly its breeding behaviour, including can only be gathered from intense behavioural monitoring. The ex-situ population therefore provides a unique opportunity to observe and better understand different aspects of male-female interactions, courtship behaviour, and parental care of wild birds which would otherwise be logistically difficult to observe of wild birds. Further, a thorough understanding of these behaviours from both wild-caught and zoo-bred birds will allow us can be used to 'benchmark' wild-type behaviours to assess potential changes over time in behaviour over time attributable to a captive environment and inform adaptive management of the program. An initial ethogram and activity budget describing the behaviour of zoo-based birds at Werribee Open Range Zoo (Victoria, Australia) has already been described by Pauligk (2020) and provides the crucial starting point from which we develop our ethogram here.We combine behaviour observations from video footage from three different zoo-based breeding population across NSW and Victoria and establish a basic ethogram from birds Plains-wanderer collected from the wild (potential founders). Building on the initial report by Pauligk (2020), herein we describe the main behavioural repertoire that makes up the ethogram of the critically endangered Plains-wanderer. It is hoped this information will support the species' ex-situ management to ensure that individuals of the insurance population maintain natural behaviours and are as suitable as possible for release. We further aim to discuss the application of ethograms in the management of ex-situ breeding program and provide a framework that can be applied in other recovery programs.Wild adult Plains wanderers (n=25) were brought into three separate breeding facilities (Taronga Zoo, Sydney; Taronga Western Plains Zoo, Dubbo; and Werribee Open Range Zoo, Werribee) between June 2017-2020. Wild birds were located and captured during nocturnal spotlight surveys from a slow moving (<5 km/hr) vehicle. While Plains-wanderers are typically easy to approach, not flighty and able to be captured by hand, a lightweight insect net (with a padded rim and small mesh) was used to capture the birds, which were transported to the breeding facilities in customised transport boxes. The behavioural observations were initiated soon after each bird was brought into the holding facilities to capture as much wild representative behaviour as possible. Due to their cryptic behaviour, Plains-wanderer are difficult to observe directly therefore, to allow for husbandry monitoring of the birds, all aviaries were fitted with CCTV cameras operating for 24 hours (about 50% of the cameras had night vision capabilities). , and tThe behaviours were analysed by remote monitoring and review of the CCTV cameras footage.During the observation period (2017-2020) birds were housed individually or in pairs in designated aviaries that varied in size from 2.8m x 3.2m x 2.4m to 4.0m x 4.0m x 4.0m, vegetated with plant species typical of Plains-wanderer habitat to emulate conditions in the wild. Birds are usually held in pairs This configuration could change for management purposes (e.g.or s birds held in small single-sex groups (3-4 birds) in each aviary). and this configuration may change for management purposes.Initial behavioural observations were obtained from CCTV cameras recording for 24 hours, 7 days a week in each aviary across the three sites within the first 12 months of the first wild birds arriving at the breeding population. Overall, more than 10,000 hours of footage was reviewed across the three institutions to establish the ethogram. Birds were out of sight or hidden from view for large portions of the recordings, therefore behaviours were described from ad lib samples when a bird was visible as opposed to fixed-time scan sampling.During the description of behaviours and development of the ethogram, the footage and descriptions of behaviours were exchanged between the institutions to validate their meaning and seek common description (as a proxy for interobserver reliability).The ethogram presented here now includes several four breeding seasons' worth of displays from both male and female birds, as well as calling and social interactions, and general maintenance behaviour. Overall, more than 10,000 hours of footage was reviewed across the three institutions to establish the ethogram.From the initial data, results indicate that most mating and reproductive-related behaviours occur during the twilight hours, with many displays between birds occurring between early morning (dawn) and evening (dusk). Although only a subset of the behaviour has been analysed due to the extensive surveillance system, and the cryptic nature of the species, pin-pointing this time of day for analysis going forward is already a valuable outcome.Forty-four different behaviours were described in the ethogram compiled by Pauligk (2020), with an additional category of 'other behaviours' describing less frequently observed behaviours.Here we grouped some of these behaviours into five broad functional categories (Sexual, Communication, Anti-predator, Maintenance, Movement) and discuss some of the most typical ones (Table 1). Videos of specific behaviours can be found in the supplementary material.Building on an initial framework by Pauligk (2020), hHere we establish an ethogram of 'wild-type' behaviour that has been observed in wild-born Plains-wanderers brought into the ex-situ breeding program. The behaviours described here are by no means exhaustive, however due to their relative regularity between individuals and across institutions and between individuals, we suggest these behaviours provide the main repertoire as seen in wild Plains-wanderer. In some cases where function is currently speculative, we have tried to include form as a means of avoiding possible confusion when assessing behaviour going forward. The development of the ethogram allowed for consistency and standardisation of the behaviours' description and meaning to ensure objectivity and uniformity of terminology. Thus, they can be used as a benchmark of wild behaviours against which the behaviour of birds within the ex-situ population can be compared.There is no detailed description of Plains-wanderer behaviours in the wild which prevents comparisons with the behaviours exhibited by the birds in the ex-situ population. However, as the behaviours described in the ethogram were based on observations of wild birds collected for the insurance population and recorded soon after their transition into the ex-situ program, we assume they are representative of the behavioural suite exhibited by Plains-wanderer in natural habitats. For example, observations of mating behaviours during the twilight hours mirror observations made during field-based activities (David Parker, pers.obs.). Further, Plains-wanderer commonly consumed water droplets on leaves after rain or irrigation, not just from water bowls provided, which suggests this is how they access water in the wild.The establishment of this ethogram is especially relevant as the Plains-wanderer recovery program is reaching the next stage of trialling wild translocations to boost natural populations. Considering that the phenotypic quality of captive-bred animals is critical in determining the success of reintroduction programs (Tripovich et al., 2021;Crates et al., 2022), the more we understand and agree on typical behaviours the more informed/evidence-based decisions will be about release cohorts or release candidate suitability.There is no detailed description of Plains-wanderer behaviours in the wild which prevents comparisons with the behaviours exhibited by the birds in the ex-situ population. However, as the behaviours described in the ethogram were based on observations of wild birds collected for the insurance population and recorded soon after their transition into the ex-situ program, we assume they are representative of the behavioural suite exhibited by Plains-wanderer in natural habitats.Identifying the behavioural factors that determine current and future reproductive success is the obvious next step when analysing Plains-wanderer behaviour. Currently data is being collated from all successful mating events across all institutions to retrospectively determine which factors may have contributed to successful mating. Once these factors are established, we can investigate the role that behavioural matching and mate-choice has on factors such as clutch size and chick health.Recent evidence has shown that incorporating behavioural compatibility and mate-choice into breeding programs enhances reproductive output and survivorship (Hartnett et al., 2018;Martin-Wintle et al., 2018). Further, it is known that captivity can cause changes in important life history and behavioural traits in various species over time (Crates et al., 2022), thus putting individuals earmarked for release potentially at a disadvantage upon reintroduction to the wild. A full grasp on typical behaviours will inform management decisions regarding the most suitable candidates for release as well as the release protocol. For example, the Regent Honeyeater (Anthochaera phrygia), another critically endangered Australian bird currently being managed through a conservation breeding program, has been bred in zoos for approximately 20 years and over 400 individuals released to the wild. Over that time changes have been observed in the vocalisations of the species both in captivity and the wild, likely due to both small populations limiting learning opportunities and mimicry of other, more abundant species (Crates et al., 2022). A recent study (Appleby et al., 2023) indicated that female Regent Honeyeaters tend to prefer songs of males they are familiar with. Further, analysis of the fitness of released individuals highlighted the importance of song tutoring, as well as complex pre-release zoo habitats (Tripovich et al., 2021). Behavioural management has now been implemented to monitor and enhance the fitness of birds and assist in selecting release candidates.The detailed behavioural observations and resulting development of the Plains-wanderer ethogram provide a consistent framework for using typical behaviours as benchmarks to inform release candidate selection. For example, by comparing behaviours observed as part of the ongoing husbandry (such as foraging) to behaviours when pre-release changes are introduced (such as consistent foraging behaviour when scatter feed is increased or changes in behaviour following attachment of a tracking device), then birds that are behaviourally suitable for release, in addition to being demographically and genetically suitable, can be confirmed. These traits may include the inability to recognise natural foods or predators, or deficient locomotor skills and/or spatial awareness, which, if recognised in advance, may provide an opportunity to address potential deficiencies in a release cohort by, for example, introducing pre-release training. Whether this is the case for bird species is largely unknown and thus this project provides a unique opportunity to intensively monitor the behaviour of birds from the time they enter the ex-situ population, to the time their descendants can be released.As ex-situ breeding programs increasingly become an essential component of the recovery efforts for 'at-risk' wildlife, all information on typical aspects of the species biology is essential, especially for evolutionary unique species for which relying on 'proxy' species is difficult, as is the case for the Plains-wanderer. The systematic description of behaviours in ethograms brings rigour and consistency to ex-situ breeding programs by removing inherent subjectivity and variation due to different stakeholders. Further, the implementation of systematic behaviour observations and descriptions allow for monitoring if and how behaviour changes over time. This would allow for adaptive management changes within the breeding program to avoid behavioural changes within a captive environment and ensure birds for release are as behaviourally sound as possible.