Abstract
Simple Summary
Safeguarding animal welfare in research is crucial for ethical and legislative compliance as well as the integrity of scientific data. It is, therefore, essential that researchers working with animals across all fields of life sciences have an understanding of how to assess animal welfare, including their behaviour, health, and physiology. This study looked into the education of ecologists, wildlife biologists, and conservation managers in Europe, Canada, the USA, Australia, and New Zealand and found that very few universities offered specific courses on animal welfare, and these courses were often optional rather than required. These results highlight the need for universities to provide more formal and mandatory education on animal welfare to better prepare future researchers studying and managing wildlife. By improving education in this area, we can ensure that researchers have the necessary knowledge and skills to work with wildlife in a responsible and compassionate way.
Abstract
Animal welfare is a subject of increasing scientific and ethical concern in today’s society, crucial for the well-being of animals used in research and the integrity of scientific data. Equipping researchers in the life science disciplines with a science-based knowledge of animal welfare, behaviour, physiology, and health is, therefore, essential. Nevertheless, previous studies evaluating animal welfare education focused on veterinary, laboratory, or farm animal science. Consequently, the aim of this study was, for the very first time, to map the prevalence of animal welfare courses in the university education of ecologists, wildlife biologists, and conservation managers in Europe, Canada, the USA, Australia, and New Zealand. A comprehensive assessment of 1548 universities was conducted, resulting in the identification of 596 relevant programs at the bachelor’s and master’s levels. Analysis of the curricula revealed that only 1% of the programs offered a formal course on animal welfare, while 65% provided courses on animal behaviour, 59% on animal physiology, and 34% on animal health. However, the majority of these courses were listed as electives rather than mandatory components of the programs. These results underscore the need for universities to incorporate more formal and obligatory education in animal welfare in order to better prepare future ecologists, wildlife biologists, and conservation managers for the challenges of working with wildlife.
Keywords: 3Rs principles, animal welfare, animal behaviour, animal physiology, animal health, education, wildlife welfare
1. Introduction
Understanding and protecting the many different species that live on Earth depend heavily on research in ecology, wildlife biology, and species conservation. This research offers insightful information on population dynamics, animal behaviour, ecological processes, and the effects of human activity on wildlife [1,2,3,4,5]. However, many conventional conservation research and management techniques might inadvertently inflict harm on the very animals they aim to protect. For instance, wildlife research can include chasing, darting, and capture methods as well as mutilations (e.g., through toe- or fin-clipping) for identification and tissue sampling, tagging, marking, and hot- or freeze-branding, considered to be necessary to gain more knowledge about animals’ biology or behaviour [6]. Additionally, animal welfare issues arise in species management, either with the removal of unwanted species with lethal means or with translocations and reintroductions, which include harm caused by capture, group separation, or stress of the source animals [7,8,9]. Furthermore, the welfare of individuals within socially complex species and genetically depauperate populations can be profoundly impacted, underscoring the importance of post-release welfare monitoring [10].
While wildlife research and conservation efforts are critically important, we should, nevertheless, be cognisant of potential animal welfare implications that might arise within these endeavours and attempt to mitigate them [11]. Inadequate knowledge and training in animal welfare can result in unintended harm to the animals involved in research and management, not only compromising the well-being of animals but also potentially undermining the validity of research outcomes [6]. Furthermore, legislations in many countries worldwide make it a prerequisite for research on vertebrate and some invertebrate animals to implement the 3Rs principles [12]: replacing the use of animals in experiments with other approaches whenever possible, reducing the number of animals used whilst ensuring the statistical power, and refining the experiments to minimise pain, suffering, distress, or lasting harm. The implementation of the 3Rs principles is stipulated within the EU by the Directive 2010/63/EU, in the USA in the USDA Animal Welfare Regulations [13], in Australia in a national standard unifying the different States’ Regulations [14], and in New Zealand in the Animal Welfare Act 1999. Therefore, anyone conducting research on animals has the ethical, scientific, as well as legal obligation to minimise animal welfare impacts. A crucial prerequisite for upholding good animal welfare standards is, however, a thorough understanding of animal behaviour and knowledge of physiological stress and health concepts [15].
The ethical imperative to address these concerns through education is increasingly recognised. While significant attention has been directed towards advocating for the integration of animal welfare courses within veterinary and animal science curricula [16,17,18,19,20], the training of ecologists, wildlife biologists, and conservation managers has been neglected. For instance, a recent study [21] reported that the availability of animal welfare courses for ecologists might be low, with only 38% of respondents in a survey stating that the topic of animal welfare was covered in their training and education. Although veterinarians could play a crucial role in ensuring the welfare of animals, they may not always be integral members of ecological research or conservation management teams. In 2013, Cattet [22] assessed 11 representative wildlife journals and found that only 26 out of 100 articles with an animal welfare focus included a co-author with a veterinary degree. Therefore, nurturing a foundational understanding of animal welfare principles becomes indispensable for ecologists and wildlife or conservation biologists who regularly interact with wildlife.
Despite this pressing need, a comprehensive evaluation of the prevalence of animal welfare courses in ecology, wildlife biology, and species conservation-related programs has not been attempted before. For that reason, the aim of this study was, for the first time, to explore the extent to which universities in Europe, Australia, New Zealand, Canada, and the USA have incorporated courses related to animal welfare, behaviour, physiology, and health into the curricula of programs training future ecologists, wildlife biologists, and conservation managers.
2. Materials and Methods
To assess the prevalence of courses relevant to animal welfare, I surveyed bachelor’s or master’s-level programs offered at universities in Europe, North America, and Oceania. This focus on developed countries with a similar level of animal welfare protection enabled a global comparison. The assessment was conducted between April and June 2023. Universities were identified through the university lists outlined on Wikipedia [23]. Universities with a clear medical, veterinary, law, business, or other unrelated focus—based on their name—were excluded from the evaluation. If the university offered a program likely to train ecologists, wildlife biologists, or conservation managers, for example, a bachelor’s or master’s degree in biodiversity, conservation biology, ecology, environmental biology, marine biology, organismal biology, wildlife biology, wildlife conservation, wildlife management, or zoology, the curriculum of this program was assessed for the presence of courses on animal welfare, animal behaviour, animal physiology, or animal health [24]. If the option to choose elective subjects was listed but without specification, the university’s course catalogue was examined to search for relevant elective subjects. The search was performed through a combination of reading through the catalogue and using a search function in order to minimise the chance of reporting false negatives. For classification, I followed the methodology described in Shivley et al. [25]: for a course to be categorised as an animal welfare course, its title needed to contain the term welfare or well-being. Courses in the animal behaviour area had to have the term behaviour, behavioural, or ethology in their title. For courses categorised as animal physiology, the term physiology, stress, or endocrinology had to be included in the title. Lastly, for courses in the animal health category, the term health, disease, or parasitology had to be present in the title. Descriptive statistics were implemented to summarise the results [25]. Fisher’s exact test was used to assess any potential influence of the region and education level (bachelor’s vs. master’s) on the prevalence of courses. This type of test was chosen to accommodate for low expected frequencies. The significance for all levels was set at p < 0.05, and p values were corrected for multiple testing using the Benjamini–Hochberg FDR method [26]. All statistical analyses were conducted in R 4.1.3 [27] integrated in RStudio 2022.02.1 [28].
3. Results
In total, 1548 universities were assessed across 33 countries (Table 1 and Tables S1 and S2). Excluded were universities that offered programs in general biology without a relevant specialisation or no wildlife-related programs (N = 802), environmental science programs focused entirely on abiotic aspects of the environment (N = 58), or programs without a curriculum available online (N = 92). As a curriculum was considered a list of subjects outlined on the program’s website. In total, 596 universities offered programs related to wildlife research and had their curricula accessible (Table 1 and Table S1; Figure 1). Only 8 of the 596 programs provided a formal course on animal welfare—2 of them as a mandatory course, 6 of them as an elective course (Table 2; Figure 2). A course on animal behaviour was offered at 385 programs, as a compulsory at 33 of them, and as an optional course at 352 (Table 2; Figure 2). An animal physiology course was listed in the curriculum of 351 programs: in 50 as a mandatory and in 301 as an elective course (Table 2; Figure 2). Animal health courses were included in 205 programs, out of which the courses in 11 programs were mandatory, and the courses in 194 programs were optional (Table 2; Figure 2). There was a statistically significant difference among regions, with all types of courses being most prevalent in North America (p < 0.001). Furthermore, the courses were more likely to be present at the bachelor’s level than at the master’s level: animal welfare courses were 4.23 times (p = 0.05), animal behaviour courses were 0.3 times (p < 0.001), animal physiology courses were 0.173 times (p < 0.001), and animal physiology courses were 0.432 times more likely to be present (p < 0.001).
Table 1.
Region | Country | Universities Assessed | Relevant Programs |
---|---|---|---|
Europe | Austria | 5 | 5 |
Europe | Belgium | 5 | 3 |
Europe | Bulgaria | 4 | 0 |
Europe | Croatia | 5 | 1 |
Europe | Cyprus | 4 | 1 |
Europe | Czech Republic | 8 | 6 |
Europe | Denmark | 4 | 0 |
Europe | Estonia | 3 | 1 |
Europe | Finland | 5 | 3 |
Europe | France | 32 | 14 |
Europe | Germany | 47 | 22 |
Europe | Greece | 4 | 2 |
Europe | Hungary | 6 | 0 |
Europe | Ireland | 6 | 3 |
Europe | Italy | 33 | 15 |
Europe | Latvia | 2 | 1 |
Europe | Lithuania | 3 | 0 |
Europe | Malta | 1 | 0 |
Europe | Netherlands | 7 | 7 |
Europe | Norway | 12 | 7 |
Europe | Poland | 19 | 2 |
Europe | Portugal | 10 | 7 |
Europe | Romania | 6 | 1 |
Europe | Slovakia | 6 | 4 |
Europe | Slovenia | 1 | 1 |
Europe | Spain | 31 | 9 |
Europe | Sweden | 11 | 5 |
Europe | Switzerland | 12 | 4 |
Europe | UK | 14 | 14 |
North America | Canada | 72 | 37 |
North America | USA | 1127 | 391 |
Oceania | Australia | 35 | 23 |
Oceania | New Zealand | 8 | 7 |
Table 2.
Europe | North America | Oceania | BSc/BA | MSc/MA | |
---|---|---|---|---|---|
Animal welfare | |||||
Mandatory | 1 | 0 | 1 | 1 | 1 |
Optional | 4 | 1 | 1 | 3 | 3 |
None | 133 | 427 | 28 | 476 | 112 |
Animal behaviour | |||||
Mandatory | 16 | 13 | 4 | 21 | 12 |
Optional | 48 | 291 | 13 | 316 | 36 |
None | 74 | 124 | 13 | 143 | 68 |
Animal physiology | |||||
Mandatory | 15 | 31 | 4 | 39 | 11 |
Optional | 26 | 268 | 7 | 282 | 19 |
None | 97 | 129 | 19 | 159 | 86 |
Animal health | |||||
Mandatory | 6 | 3 | 2 | 5 | 6 |
Optional | 28 | 165 | 1 | 176 | 18 |
None | 104 | 260 | 27 | 299 | 92 |
4. Discussion
4.1. Prevalence of Animal Welfare Courses
This survey across 33 countries revealed that the availability of courses in animal welfare, animal behaviour, animal physiology, and animal health in university programs educating aspiring ecologists, wildlife biologists, and conservation managers is limited (Table 2; Figure 2). These findings are congruent with the results of a previous study reporting that animal welfare courses are not prevalent in the education of ecologists but would be appreciated [21]. The results show that bachelor’s level programs were more likely to incorporate animal welfare-related courses compared to master’s degrees. This might be a reflection of the more focused nature of master’s level programs, which often prioritise advanced topics relevant to a student’s chosen specialisation. It is nevertheless crucial that animal welfare education is included in both bachelor’s and master’s programs to ensure that all future ecologists, wildlife biologists, and conservation managers possess a well-rounded understanding of the subject.
4.2. Importance of Animal Welfare Education
There are several reasons why animal welfare courses should be included in education across all life science disciplines. First, animal welfare is an important ethical issue that is relevant to all fields that involve animal use, such as veterinary medicine, animal science, and wildlife biology [16]. The relevance for ecologists, wildlife biologists, and conservation managers stems from the potential animal welfare impact of commonly used research and management methods. For instance, the mere act of capture can induce substantial stress for free-living animals not accustomed to human contact [29], potentially leading to capture myopathy—a stress-associated metabolic disorder [9,30]. Also, blood sampling, toe-clipping, and attachment of radio transmitters have been reported to increase mortality, induce inflammation, or disrupt normal behaviour [31,32,33]. Apart from animal welfare considerations, robust scientific practices dictate that animals involved in research should remain unaffected by harm in terms of their physical, physiological, and behavioural well-being [34]. Any deviations from this norm can introduce alterations in an individual’s condition that may consequently influence the credibility, consistency, and replicability of experimental and observational outcomes [35]. Because of the above-mentioned animal welfare issues as well as animal protection regulations, many studies in ecology, wildlife biology, or species conservation projects are conducted by multidisciplinary teams. The participation of veterinarians, in particular, can greatly enhance the welfare of animals involved in research; however, this is not always the case [22]. The potential absence of experts in veterinary science highlights the importance of providing everyone involved in wildlife research and management with the knowledge and tools to mitigate potential risks to the animals.
Second, students who have a clear understanding of animal welfare issues early in their education are better equipped to make informed ethical decisions in their future careers [36,37]. The education should include not only an introduction to animal welfare and the most important concepts, such as Five Freedoms and Five Domains [38,39], but also the application of physiological, behavioural, and health indicators to situations that the students are most likely to encounter in their profession. For this reason, a collaboration between universities and zoos, wildlife parks, and nature reserves would be beneficial for the students to learn how to apply theoretical understanding of animal welfare in practice.
Third, animal welfare is of growing concern for the general public, and having a basic understanding of animal welfare issues can help scientists communicate their work to the public more effectively and transparently [11,20,40]. Some research and conservation management projects had to be halted in the past due to disagreement and outrage among the local communities [41,42].
Finally, incorporating animal welfare courses into life science curricula can help to promote a culture of respect and responsibility towards animals in the scientific community, leading to better animal care and more ethical research practices [43,44,45].
4.3. Recommendations and Future Directions
It is highly recommended that animal welfare be included as a mandatory subject in wildlife degree programs to fill the current vacuum. To guarantee that upcoming ecologists, wildlife biologists, and conservation managers receive thorough training in animal welfare, this integration should take place at both the undergraduate and graduate levels [16,46,47]. Educational institutions can emphasise the significance of animal welfare by giving it the same priority in the curriculum as other important topics in wildlife research and management, classifying it as a core subject [48]. Additionally, governmental and regulatory organisations, as well as wildlife research and conservation societies and scientific journals, ought to encourage and promote the inclusion of animal welfare education by acknowledging it as a crucial element of wildlife research and conservation [34].
It might be argued that students can be taught about animal welfare through informal discussions with lecturers and supervisors. While this could be a useful approach, it poses a couple of challenges: (1) the lecturer may not have received any animal welfare training either, and (2) the student might not understand the significance of the subject matter [49]. Consequently, some form of formal training in animal welfare is necessary and also provides transparency of what is being taught [25,49]. Furthermore, the importance of safeguarding animal welfare for ethical as well as scientific reasons should grant the subject a prominent place in the curriculum as a standalone course.
It is important to note that due to differences in attitudes towards animals, the course content related to animal welfare might vary between countries. As pointed out by Illmann et al. [50], countries with a rich tradition of animal welfare research may emphasise the fundamental scientific basis of animal welfare, including physiology and ethology, whereas, in countries that implement EU animal welfare policies but have less involvement in research, the focus may be more on practical aspects like legal issues and/or animal welfare assessment. Given the interdisciplinary nature of animal welfare, the incorporation of educators from various fields could provide valuable enrichment to the educational experience within each domain. The inclusion of guest speakers, particularly those engaged in roles spanning animal welfare, ecological research, and management, could further enhance the educational environment. The exact content of the courses should be investigated in future studies.
Implementing animal welfare education within ecology and wildlife conservation programs may face challenges and resistance. Scarce resources, curriculum restrictions, and opposition from established academic systems are some of the potential obstacles [51]. To overcome them, it is crucial to engage in proactive communication with academic institutions, faculty members, and other stakeholders. Support for integrating animal welfare education into wildlife degree programs can be gained by presenting arguments that are supported by data [21,52], highlighting successful examples from other institutions and programs [19,53,54], and emphasising the scientific and ethical necessity and the beneficial effects on research outcomes [6,10,22].
4.4. Study Limitations
In discussing the implications of the results, it is important to acknowledge the limitations inherent in the chosen methodology. The classification of courses based solely on their titles may not provide a comprehensive representation of the actual content and depth of animal welfare education. While every effort was made to categorise courses accurately, it is possible that some relevant courses were excluded. Furthermore, animal welfare courses that cater to ecologists might be provided by some veterinary faculties. Due to feasibility considerations, this study did not account for these nuances, and a more comprehensive search delving deeper into the actual content and pedagogy might provide more accurate estimates.
Another limitation is the focus on developed, higher-income countries, which prevents the generalisability of the results at a global scale. The findings of this study may not be directly applicable to developing countries, in which the educational system, resources, and priorities might be significantly different. The insights and recommendations mentioned could nevertheless provide some guidance for universities across the globe that aspire to improve animal welfare education.
5. Conclusions
Animal welfare should be an integral part of the education of all researchers who work with animals. However, this first overview of wildlife-related programs across several continents revealed that this subject remains neglected. This is a serious problem that needs to be addressed. Academic institutions and governing bodies should support the inclusion of animal welfare education in order to help create a new generation of ecologists, wildlife biologists, and conservation managers with the knowledge, abilities, and moral compass necessary to conduct research that upholds both animal welfare and the long-term conservation of wildlife populations.
Acknowledgments
I would like to thank Ivo Wallimann-Helmer for his support.
Supplementary Materials
The following supporting information can be downloaded at https://www.mdpi.com/article/10.3390/ani13182907/s1. Table S1: List of assessed programs at universities in Europe, Canada, USA, Australia, and New Zealand; Table S2: List of universities evaluated but not included.
Institutional Review Board Statement
Not applicable.
Informed Consent Statement
Not applicable.
Data Availability Statement
The data presented in this study are available in the Supplementary Materials and upon request from the corresponding author.
Conflicts of Interest
The author declares no conflict of interest.
Funding Statement
This research received no external funding.
Footnotes
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References
- 1.Mulatu K.A., Mora B., Kooistra L., Herold M. Biodiversity monitoring in changing tropical forests: A review of approaches and new opportunities. Remote Sens. 2017;9:1059. doi: 10.3390/rs9101059. [DOI] [Google Scholar]
- 2.Zemanova M.A., Broennimann O., Guisan A., Knop E., Heckel G. Slimy invasion: Climatic niche and current and future biogeography of Arion slug invaders. Divers. Distrib. 2018;24:1627–1640. doi: 10.1111/ddi.12789. [DOI] [Google Scholar]
- 3.Farrell M.J., Govender D., Hajibabaei M., van der Bank M., Davies J. Next generation wildlife monitoring: A comparison of eDNA and camera trapping in Kruger National Park, South Africa. Genome. 2020;60:933. [Google Scholar]
- 4.Williams D.R., Balmford A., Wilcove D.S. The past and future role of conservation science in saving biodiversity. Conserv. Lett. 2020;13:e12720. doi: 10.1111/conl.12720. [DOI] [Google Scholar]
- 5.Zemanova M.A., Ramp D. Genetic structure and gene flow in eastern grey kangaroos in an isolated conservation reserve. Diversity. 2021;13:570. doi: 10.3390/d13110570. [DOI] [Google Scholar]
- 6.Zemanova M.A. Towards more compassionate wildlife research through the 3Rs principles: Moving from invasive to non-invasive methods. Wildl. Biol. 2020;1:wlb.00607. doi: 10.2981/wlb.00607. [DOI] [Google Scholar]
- 7.Bosson C.O., Palme R., Boonstra R. Assessing the impact of live-capture, confinement, and translocation on stress and fate in eastern gray squirrels. J. Mammal. 2013;94:1401–1411. doi: 10.1644/13-MAMM-A-046.1. [DOI] [Google Scholar]
- 8.Harrington L.A., Moehrenschlager A., Gelling M., Atkinson R.P.D., Hughes J., Macdonald D.W. Conflicting and complementary ethics of animal welfare considerations in reintroductions. Conserv. Biol. 2013;27:486–500. doi: 10.1111/cobi.12021. [DOI] [PubMed] [Google Scholar]
- 9.Breed D., Meyer L.C.R., Steyl J.C.A., Goddard A., Burroughs R., Kohn T.A. Conserving wildlife in a changing world: Understanding capture myopathy—A malignant outcome of stress during capture and translocation. Conserv. Physiol. 2020;7:coz027. doi: 10.1093/conphys/coz027. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Zemanova M.A. Non-domesticated terrestrial species. In: Knight A., Phillips C., Sparks P., editors. Routledge Handbook of Animal Welfare. 1st ed. Routledge; London, UK: 2022. pp. 271–281. [Google Scholar]
- 11.Paquet P.C., Darimont C.T. Wildlife conservation and animal welfare: Two sides of the same coin? Anim. Welf. 2010;19:177–190. doi: 10.1017/S0962728600001433. [DOI] [Google Scholar]
- 12.Russell W.M.S., Burch R.L. The Principles of Humane Experimental Technique. Volume 1 Methuen; London, UK: 1959. [Google Scholar]
- 13.National Institutes of Health . Institutional Animal Care and Use Committee Guidebook. 2nd ed. US Department of Health and Human Services; Bethesda, MD, USA: 2002. [Google Scholar]
- 14.National Health and Medical Research Council . Australian Code of Practice for the Care and Use of Animals for Scientific Purposes. 8th ed. NHMRC; Canberra, ACT, Australia: 2013. [Google Scholar]
- 15.Friend T.H. Teaching animal welfare in the land grant universities. J. Anim. Sci. 1990;68:3462–3467. doi: 10.2527/1990.68103462x. [DOI] [PubMed] [Google Scholar]
- 16.Broom D.M. Animal welfare education: Development and prospects. J. Vet. Med. Educ. 2005;32:438–441. doi: 10.3138/jvme.32.4.438. [DOI] [PubMed] [Google Scholar]
- 17.Hazel S.J., Signal T.D., Taylor N. Can teaching veterinary and animal-science students about animal welfare affect their attitude toward animals and human-related empathy? J. Vet. Med. Educ. 2011;38:74–83. doi: 10.3138/jvme.38.1.74. [DOI] [PubMed] [Google Scholar]
- 18.Hewson C.J., Baranyiova E., Broom D.M., Cockram M.S., Galindo F., Hanlon A.J., Hanninen L., Lexer D., Mellor D.J., Molento C.F.M., et al. Approaches to teaching animal welfare at 13 veterinary schools worldwide. J. Vet. Med. Educ. 2005;32:422–437. doi: 10.3138/jvme.32.4.422. [DOI] [PubMed] [Google Scholar]
- 19.Mota-Rojas D., Orihuela A., Strappini-Asteggiano A., Cajiao-Pachon M.N., Aguera-Buendia E., Mora-Medina P., Ghezzi M., Alonso-Spilsbury M. Teaching animal welfare in veterinary schools in Latin America. Int. J. Vet. Sci. Med. 2018;6:131–140. doi: 10.1016/j.ijvsm.2018.07.003. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.De Briyne N., Vidović J., Morton D.B., Magalhães-Sant’Ana M. Evolution of the teaching of animal welfare science, ethics and law in European veterinary schools (2012–2019) Animals. 2020;10:1238. doi: 10.3390/ani10071238. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Zemanova M.A. Making room for the 3Rs principles of animal use in ecology: Potential issues identified through a survey. Eur. J. Ecol. 2021;7:18–39. doi: 10.17161/eurojecol.v7i2.14683. [DOI] [Google Scholar]
- 22.Cattet M.R.L. Falling through the cracks: Shortcomings in the collaboration between biologists and veterinarians and their consequences for wildlife. ILAR J. 2013;54:33–40. doi: 10.1093/ilar/ilt010. [DOI] [PubMed] [Google Scholar]
- 23.Wikipedia List of Universities and Colleges by Country. [(accessed on 3 April 2023)]. Available online: https://en.wikipedia.org/wiki/Lists_of_universities_and_colleges_by_country.
- 24.Zemanova M.A. More training in animal ethics needed for European biologists. Bioscience. 2017;67:301–305. doi: 10.1093/biosci/biw177. [DOI] [Google Scholar]
- 25.Shivley C.B., Garry F.B., Kogan L.R., Grandin T. Survey of animal welfare, animal behavior, and animal ethics courses in the curricula of AVMA Council on Education-accredited veterinary colleges and schools. Javma—J. Am. Vet. Med. Assoc. 2016;248:1165–1170. doi: 10.2460/javma.248.10.1165. [DOI] [PubMed] [Google Scholar]
- 26.Benjamini Y., Hochberg Y. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J. R. Stat. Society Ser. B (Methodol.) 1995;57:289–300. doi: 10.1111/j.2517-6161.1995.tb02031.x. [DOI] [Google Scholar]
- 27.R Core Team R: A Language and Environment for Statistical Computing. [(accessed on 15 March 2022)]. Available online: http://www.R-project.org.
- 28.RStudio Team RStudio: Integrated Development for R. [(accessed on 15 March 2022)]. Available online: http://www.rstudio.com/
- 29.Wilson R.P., McMahon C.R. Measuring devices on wild animals: What constitutes acceptable practice? Front. Ecol. Environ. 2006;4:147–154. doi: 10.1890/1540-9295(2006)004[0147:MDOWAW]2.0.CO;2. [DOI] [Google Scholar]
- 30.Marco I., Mentaberre G., Ponjoan A., Bota G., Mañosa S., Lavín S. Capture myopathy in little bustards after trapping and marking. J. Wildl. Dis. 2006;42:889–891. doi: 10.7589/0090-3558-42.4.889. [DOI] [PubMed] [Google Scholar]
- 31.Brooks C., Bonyongo C., Harris S. Effects of global positioning system collar weight on zebra behavior and location error. J. Wildl. Manag. 2008;72:527–534. doi: 10.2193/2007-061. [DOI] [Google Scholar]
- 32.Brown M.B., Brown C.R. Blood sampling reduces annual survival in cliff swallows (Petrochelidon pyrrhonota) Auk. 2009;126:853–861. doi: 10.1525/auk.2009.09048. [DOI] [Google Scholar]
- 33.Phillott A.D., McDonald K.R., Skerratt L.F. Inflammation in digits of unmarked and toe-tipped wild hylids. Wildl. Res. 2011;38:204–207. doi: 10.1071/WR10154. [DOI] [Google Scholar]
- 34.Field K.A., Paquet P.C., Artelle K., Proulx G., Brook R.K., Darimont C.T. Publication reform to safeguard wildlife from researcher harm. PLoS Biol. 2019;17:e3000193. doi: 10.1371/journal.pbio.3000193. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 35.Garner J.P. Stereotypies and other abnormal repetitive behaviors: Potential impact on validity, reliability, and replicability of scientific outcomes. ILAR. 2005;46:106–117. doi: 10.1093/ilar.46.2.106. [DOI] [PubMed] [Google Scholar]
- 36.Freire R., Phillips C.J.C., Verrinder J.M., Collins T., Degeling C., Fawcett A., Fisher A.D., Hazel S., Hood J., Johnson J., et al. The importance of animal welfare science and ethics to veterinary students in Australia and New Zealand. J. Vet. Med. Educ. 2017;44:208–216. doi: 10.3138/jvme.1215-191R. [DOI] [PubMed] [Google Scholar]
- 37.Hernandez E., Fawcett A., Brouwer E., Rau J., Turner P.V. Speaking up: Veterinary ethical responsibilities and animal welfare issues in everyday practice. Animals. 2018;8:15. doi: 10.3390/ani8010015. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 38.Mellor D.J. Updating animal welfare thinking: Moving beyond the “Five Freedoms” towards “A Life Worth Living”. Animals. 2016;6:21. doi: 10.3390/ani6030021. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 39.Mellor D.J. Operational details of the Five Domains Model and its key applications to the assessment and management of animal welfare. Animals. 2017;7:60. doi: 10.3390/ani7080060. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 40.Alonso M.E., González-Montaña J.R., Lomillos J.M. Consumers’ concerns and perceptions of farm animal welfare. Animals. 2020;10:385. doi: 10.3390/ani10030385. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 41.Perry D., Perry G. Improving interactions between animal rights groups and conservation biologists. Conserv. Biol. 2008;22:27–35. doi: 10.1111/j.1523-1739.2007.00845.x. [DOI] [PubMed] [Google Scholar]
- 42.Grimm D. PETA targets early-career wildlife researcher. Science. 2017;357:1087. doi: 10.1126/science.357.6356.1087. [DOI] [PubMed] [Google Scholar]
- 43.Vucetich J.A., Nelson M.P. What are 60 warblers worth? Killing in the name of conservation. Oikos. 2007;116:1267–1278. doi: 10.1111/j.0030-1299.2007.15536.x. [DOI] [Google Scholar]
- 44.Costello M.J., Beard K.H., Corlett R.T., Cumming G.S., Devictor V., Loyola R., Maas B., Miller-Rushing A.J., Pakeman R., Primack R.B. Field work ethics in biological research. Biol. Conserv. 2016;203:268–271. doi: 10.1016/j.biocon.2016.10.008. [DOI] [Google Scholar]
- 45.Bruskotter J.T., Vucetich J.A., Dietsch A., Slagle K.M., Brooks J.S., Nelson M.P. Conservationists’ moral obligations toward wildlife: Values and identity promote conservation conflict. Biol. Conserv. 2019;240:108296. doi: 10.1016/j.biocon.2019.108296. [DOI] [Google Scholar]
- 46.Siegford J.M., Bernardo T.M., Malinowski R.P., Laughlin K., Zanella A.J. Integrating animal welfare into veterinary education: Using an online, interactive course. J. Vet. Med. Educ. 2005;32:497–504. doi: 10.3138/jvme.32.4.497. [DOI] [PubMed] [Google Scholar]
- 47.Lord L.K., Millman S.T., Carbone L., Cook N., Fisher A., McKeegan D., Morton D., Pajor E., Peralta J.M., Robertson S.A., et al. A model curriculum for the study of animal welfare in colleges and schools of veterinary medicine. JAVMA. 2017;250:632–640. doi: 10.2460/javma.250.6.632. [DOI] [PubMed] [Google Scholar]
- 48.Colonius T., Swoboda J. Student perspectives on animal-welfare education in American veterinary medical curricula. J. Vet. Med. Educ. 2010;37:56–60. doi: 10.3138/jvme.37.1.56. [DOI] [PubMed] [Google Scholar]
- 49.Main D.C.J., Thornton P., Kerr K. Teaching animal welfare science, ethics, and law to veterinary students in the United Kingdom. J. Vet. Med. Educ. 2005;32:505–508. doi: 10.3138/jvme.32.4.505. [DOI] [PubMed] [Google Scholar]
- 50.Illmann G., Keeling L., Melisova M., Simeckova M., Ilieski V., Winckler C., Kostal L., Meunier-Salaun M.C., Mihina S., Spoolder H., et al. Mapping farm animal welfare education at university level in Europe. Anim. Welf. 2014;23:401–410. doi: 10.7120/09627286.23.4.401. [DOI] [Google Scholar]
- 51.Beaver B.V. Introduction: Animal welfare education, a critical time in veterinary medicine. J. Vet. Med. Educ. 2005;32:419–421. doi: 10.3138/jvme.32.4.419. [DOI] [PubMed] [Google Scholar]
- 52.Pejman N., Kallas Z., Reig L., Velarde A., Moreno M., Magnani D., Protopapadaki V., Ribikauskas V., Ribikauskienė D., Dalmau A. Should animal welfare be included in educational programs? Attitudes of secondary and university students from eight EU countries. J. Appl. Anim. Welf. Sci. 2023;26:341–360. doi: 10.1080/10888705.2021.1969931. [DOI] [PubMed] [Google Scholar]
- 53.Abood S.K., Siegford J.M. Student perceptions of an animal-welfare and ethics course taught early in the veterinary curriculum. J. Vet. Med. Educ. 2012;39:136–141. doi: 10.3138/jvme.0911.093R1. [DOI] [PubMed] [Google Scholar]
- 54.Johnson J., Collins T., Degeling C., Fawcett A., Fisher A.D., Freire R., Hazel S.J., Hood J., Lloyd J., Phillips C.J.C., et al. The first shared online curriculum resources for veterinary undergraduate learning and teaching in animal welfare and ethics in Australia and New Zealand. Animals. 2015;5:395–406. doi: 10.3390/ani5020362. [DOI] [PMC free article] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Data Availability Statement
The data presented in this study are available in the Supplementary Materials and upon request from the corresponding author.