Applying welfare science to cetacean strandings : a thesis presented in partial fulfilment of the requirements for the degree of Doctor of Philosophy in Zoology at Massey University, Albany, New Zealand

Animal welfare science can provide critical knowledge to inform ethical wildlife management and human intervention efforts. Despite live stranding events being recognised by the International Whaling Commission as a major welfare concern for free-ranging cetaceans, little research has to date, been conducted on stranded cetacean welfare. Live cetacean stranding events offer a quintessential exemplar of wildlife management, where assessment or integration of welfare has been limited in the decision-making process. This thesis contributes new understanding of how welfare science can be applied to cetacean stranding events to inform decision-making processes. Here, the first welfare-centric data regarding live stranded cetaceans is presented. Specifically, this research presents novel contributions to science via: (1) conceptualisation of stranded cetacean welfare and survival likelihood; (2) recognition of key knowledge gaps and concerns that must be addressed to ensure optimal welfare and survival likelihood outcomes; (3) identification of potential valuable and practical indicators for assessing stranded cetacean welfare and survival likelihood; (4) evidenced feasibility of welfare indicator application to live cetacean stranding events; (5) incorporation of indicators to undertake holistic welfare assessments; (6) identification of potential welfare implications of strandings management, including efficacy of euthanasia; and (7) provision of key recommendations and requirements to ensure humane end-of-life outcomes for non-viable stranded cetaceans. This thesis documents inextricable links between animal welfare and survival likelihood of stranded cetaceans and demonstrates a clear need for integration of welfare science alongside conservation biology at live stranding events. Systematic, standardised data collection and welfare-centric assessment of stranded cetaceans can, if applied scientifically, inform intervention decisions, to ensure consistent guidance and improve strandings management to safeguard humane outcomes for affected cetaceans. Collectively, this research provides a significant contribution to the current scientific understanding of stranded cetacean welfare, by providing key knowledge required for the development of a welfare assessment framework that can support decision-making at stranding events

Multi-state open robust design applied to opportunistic data reveals dynamics of wide-ranging taxa: The sperm whale case.

© The Author(s), 2019. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Boys, R. M., Oliveira, C., Perez-Jorgeo, S., Prieto, R., Steiner, L., & Silva, M. A. Multi-state open robust design applied to opportunistic data reveals dynamics of wide-ranging taxa: The sperm whale case. Ecosphere, 10(3), (2019):e02610, doi:10.1002/ecs2.2610.Capture–mark–recapture methods have been extensively used to estimate abundance, demography, and life history parameters of populations of several taxa. However, the high mobility of many species means that dedicated surveys are logistically complicated and expensive. Use of opportunistic data may be an alternative, if modeling takes into account the inevitable heterogeneity in capture probability from imperfect detection and incomplete sampling, which can produce significant bias in parameter estimates. Here, we compare covariate‐based open Jolly‐Seber models (POPAN) and multi‐state open robust design (MSORD) models to estimate demographic parameters of the sperm whale population summering in the Azores, from photo‐identification data collected opportunistically by whale‐watching operators and researchers. The structure of the MSORD also allows for extra information to be obtained, estimating temporary emigration and improving precision of estimated parameters. Estimates of survival from both POPAN and MSORD were high, constant, and very similar. The POPAN model, which partially accounted for heterogeneity in capture probabilities, estimated an unbiased super‐population of ~1470 whales, with annual abundance showing a positive trend from 351 individuals (95% CI: 234–526) in 2010 to 718 (95% CI: 477–1082) in 2015. In contrast, estimates of abundance from MSORD models that explicitly incorporated imperfect detection due to temporary emigration were less biased, more precise, and showed no trend over years, from 275 individuals (95% CI: 188–404) in 2014 to 367 (95% CI: 248–542) in 2012. The MSORD estimated short residence time and an even‐flow temporary emigration, meaning that the probability of whales emigrating from and immigrating to the area was equal. Our results illustrate how failure to account for transience and temporary emigration can lead to biased estimates and trends in abundance, compromising our ability to detect true population changes. MSORD models should improve inferences of population dynamics, especially when capture probability is low and highly variable, due to wide‐ranging behavior of individuals or to non‐standardized sampling. Therefore, these models should provide less biased estimates and more accurate assessments of uncertainty that can inform management and conservation measures.We acknowledge IFAW for providing photo‐identification data from the early period of the study (1987–1993), Biosphere Expeditions and clients of Whale Watch Azores for making data collection possible. We thank Sara Magalhães, Tiago Sá, João Medeiros, Yves Cuenot, Pablo Chevallard Navarro, and numerous volunteers that over the years helped with data collection and organization of the photo‐identification catalogue. We are deeply grateful to Gary White, Bill Kendall, Jim Hines, James Nichols, Paul Conn, and Olivier Gimenez for offering guidance and advice on CMR modeling. We thank Jonathan Gordon for his comments on an earlier version of the manuscript. We are thankful to the three anonymous reviewers for providing very helpful comments. This work was supported by Fundação para a Ciência e Tecnologia (FCT), Azores 2020 Operational Programme, and Fundo Regional da Ciência e Tecnologia (FRCT) through research projects FCT‐Exploratory project (IF/00943/2013/CP1199/CT0001), WATCH IT (Acores‐01‐0145‐FEDER‐000057), and MISTIC SEAS II (GA11.0661/2017/750679/SUB/ENV.C2) co‐funded by FEDER, COMPETE, QREN, POPH, ESF, Portuguese Ministry for Science and Education, and EU‐DG/ENV. The Azores 2020 Operational Programme is funded by the community structural funds ERDF and ESF. We also acknowledge funds provided by FCT to MARE, through the strategic project UID/MAR/04292/2013. Rebecca M Boys is supported by an Estagiar L scholarship, Cláudia Oliveira by a research assistant contract from WATCH IT and Mónica A Silva by an FCT‐Investigator contract (IF/00943/2013), and Rui Prieto by an FCT postdoctoral grant (SFRH/BPD/108007/2015). Mónica A Silva conceptualized the project, acquired funding, administered, and supervised the project. Lisa Steiner, Cláudia Oliveira, Rebecca M Boys, and Mónica A Silva involved in data curation. Rebecca M Boys, Mónica A Silva, Sergi Pérez‐Jorge, and Cláudia Oliveira involved in formal analysis, investigation, and methodology. Rebecca M Boys preparation and visualization of the data. Rebecca M Boys, Mónica A Silva, Sergi Pérez‐Jorge, Rui Prieto wrote the original draft of the manuscript. Rebecca M Boys, Mónica A Silva, Rui Prieto, Sergi Pérez‐Jorge, Cláudia Oliveira, and Lisa Steiner wrote, reviewed, and edited the manuscript

Increasing the Awareness of Animal Welfare Science in Marine Mammal Conservation: Addressing Language, Translation and Reception Issues

Integrating welfare principles into conservation strategy is an emerging synthesis that encourages consideration of individual animals’ quality of life in research, policies and law. However, these principles have gained limited traction in marine compared to terrestrial animal conservation. This manuscript investigates several factors that may be contributing to this disparity. In order to gauge current understanding of animal welfare science principles by marine mammal researchers and other stakeholders, a “Welfare in the Wild” workshop was convened at the 32nd European Cetacean Society conference (La Spezia, Italy, April 2018). The workshop was attended by 30 participants who completed pre- and post-workshop surveys on animal welfare principles. The survey results highlight a range of different views about exactly what animal welfare science is and how it can be applied to marine mammals. Specifically, participants’ definitions appeared to vary depending on the type of employment or research they engaged in, indicating a need for an interdisciplinary common language. Secondly, we analysed the peer-reviewed literature in order to ascertain where marine mammal publications exploring welfare were being published. From 1950 to July 2020, a total of 299 articles featured both marine mammal taxa (one or more) and the word welfare in the title, abstract or keywords. This represents just 0.96% of the total peer-reviewed published papers on marine mammal taxa (n = 31,221) during the same period. When examining articles published within “Welfare and Ethics” (n = 6133) and “Aquatic-focused” (n = 139,352) journals, just 1.2% (n = 71) and 0.04% (n = 57) of articles, respectively, featured the word welfare when examining marine mammals. With the aim of exploring how explicitly including welfare evaluations in marine mammal research and management can benefit conservation outcomes, we framed our workshop and quantitative literature review findings to provide practical solutions to the language, translation and reception issues of this burgeoning cross-disciplinary collaboration

Deathly Silent: Exploring the Global Lack of Data Relating to Stranded Cetacean Euthanasia

The compromised state of stranded cetaceans means that euthanasia is often required. However, current knowledge and implementation of euthanasia methods remain highly variable, with limited data on the practicalities and welfare impacts of procedures. This study evaluated the available published data on cetacean euthanasia, highlighting knowledge gaps and providing direction to improve stranded cetacean welfare. A total of 2147 peer-reviewed articles describing marine mammal euthanasia were examined. Of these 3.1% provided details on the method used, with 91% employing chemical methods. Two countries, the United Kingdom (UK) and New Zealand (NZ), provided euthanasia reports to the International Whaling Commission (IWC) between 2007 and 2020. Methods employed were reported for 78.3% and 100% of individual cetaceans euthanised in the UK and NZ, respectively. In the UK, chemical euthanasia was most common (52%), whilst in NZ only ballistics methods were used. Few data were available about time to death/insensibility (TTD); 0.5% of peer-reviewed articles provided TTD, whilst TTD was reported for 35% of individuals in the UK and for 98% in NZ. However, IWC reports lacked detail on how death/insensibility were assessed, with multiple individuals “presumed instantly” killed. Overall, the findings highlight the lack of available information on cetacean euthanasia, and suggest increased data collection and the application of appropriate methods to improve welfare

Fundamental Concepts, Knowledge Gaps and Key Concerns Relating to Welfare and Survival of Stranded Cetaceans

Wildlife management can influence animal welfare and survival, although both are often not explicitly integrated into decision making. This study explores fundamental concepts and key concerns relating to the welfare and survival of stranded cetaceans. Using the Delphi method, the opinions of an international, interdisciplinary expert panel were gathered, regarding the characterisation of stranded cetacean welfare and survival likelihood, knowledge gaps and key concerns. Experts suggest that stranded cetacean welfare should be characterised based on interrelated aspects of animals’ biological function, behaviour, and mental state and the impacts of human interventions. The characterisation of survival likelihood should reflect aspects of stranded animals’ biological functioning and behaviour as well as a 6-month post-re-floating survival marker. Post-release monitoring was the major knowledge gap for survival. Welfare knowledge gaps related to diagnosing internal injuries, interpreting behavioural and physiological parameters, and euthanasia decision making. Twelve concerns were highlighted for both welfare and survival likelihood, including difficulty breathing and organ compression, skin damage and physical traumas, separation from conspecifics, and suffering and stress due to stranding and human intervention. These findings indicate inextricable links between perceptions of welfare state and the likely survival of stranded cetaceans and demonstrate a need to integrate welfare science alongside conservation biology to achieve effective, ethical management at strandings

Identification of potential welfare and survival indicators for stranded cetaceans through international, interdisciplinary expert opinion

Management of live cetacean strandings generally focuses on refloating animals, yet there is a lack of scientific data to inform decision-making. Valid indicators that are practical to measure are needed to assess welfare status and survival likelihood for stranded cetaceans. The Delphi method was applied to gather international and interdisciplinary expert opinion to provide face validity to potential indicators of stranded cetacean welfare and survival likelihood. Two online questionnaires were conducted. In the first questionnaire these experts identified potential indicators of stranded cetacean welfare and survival likelihood. These indicators were subsequently scored by the same experts in questionnaire two, based on their value for assessing welfare/survival likelihood and being practical to measure. Indicators considered valuable and practical for assessing welfare and survival likelihood at strandings included animal-based indices of body and skin condition, signs of physical trauma, respiration rate and various behaviours. Resource-/management-based indicators related mainly to human intervention and should be correlated with animal-based indices to provide relevant evaluations. Importantly, inextricable links between welfare and survival for stranded cetaceans are emphasized, with 90% of indicators being similar for both. Investigations into these indicators should be conducted to develop a practical, science-based assessment framework to inform decision-making during stranding events

Categories of potential indicators generated from expert opinion from Identification of potential welfare and survival indicators for stranded cetaceans through international, interdisciplinary expert opinion

Themes of welfare and survival likelihood indicators based on reflexive thematic analysis of expert opinions from questionnaire 1, transcribed as intelligent verbati

Potential affective experiences of stranded cetaceans as identified via expert opinion from Identification of potential welfare and survival indicators for stranded cetaceans through international, interdisciplinary expert opinion

All expert suggestions, transcribed as intelligent verbatim, of affective experience or cause of observed welfare status indicator from questionnaire

Results of the linear discriminant analysis (LDA) from Identification of potential welfare and survival indicators for stranded cetaceans through international, interdisciplinary expert opinion

Management of live cetacean strandings generally focuses on refloating animals, yet there is a lack of scientific data to inform decision-making. Valid indicators that are practical to measure are needed to assess welfare status and survival likelihood for stranded cetaceans. The Delphi method was applied to gather international and interdisciplinary expert opinion to provide face validity to potential indicators of stranded cetacean welfare and survival likelihood. Two online questionnaires were conducted. In the first questionnaire these experts identified potential indicators of stranded cetacean welfare and survival likelihood. These indicators were subsequently scored by the same experts in questionnaire two, based on their value for assessing welfare/survival likelihood and being practical to measure. Indicators considered valuable and practical for assessing welfare and survival likelihood at strandings included animal-based indices of body and skin condition, signs of physical trauma, respiration rate and various behaviours. Resource-/management-based indicators related mainly to human intervention and should be correlated with animal-based indices to provide relevant evaluations. Importantly, inextricable links between welfare and survival for stranded cetaceans are emphasized, with 90% of indicators being similar for both. Investigations into these indicators should be conducted to develop a practical, science-based assessment framework to inform decision-making during stranding events

Information sheet provided to participants from Identification of potential welfare and survival indicators for stranded cetaceans through international, interdisciplinary expert opinion

Information sheet provided to invited participants to take part in the study gathering expert opinions on the assessment of stranded cetacean welfare and survival likelihood