Zoo animal welfare assessment: where do we stand?
Open accessAbstract
Zoological institutions, such as zoos and aquariums, have made animal welfare a top priority, as it is not only a moral obligation but also crucial for fulfilling their roles in education and conservation. There is a need for science-based tools to assess and monitor animal welfare in these settings. However, assessing the welfare of zoo animals is challenging due to the diversity of species and lack of knowledge on their specific needs. This review aims to discuss the advantages and disadvantages of existing methodologies for assessing zoo animal welfare through: (1) A critical analysis of the main approaches to zoo animal welfare assessment; (2) A description of the most relevant animal-based welfare indicators for zoo animals with a particular focus on behavioural and physiological indicators; and (3) An identification of areas that require further research.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Species-specific welfare assessment tools offer a refined and more precise evaluation of animal welfare by tailoring assessments to the unique needs, behaviors, and physiological aspects of a particular species.
“These offer a refined and more precise evaluation of animal welfare by tailoring assessments to the unique needs, behaviors, and physiological aspects of a particular species (24).”
From Comparison of animal welfare assessment tools and methodologies: need for an effective approach for captive elephants in Asia (2024) · cites this paper as [24]
Section 3.1 says species-specific protocols are tailored to each species’ biological needs and can use indicators tested for validity and reliability. But it describes these advantages as theoretical and notes that few protocols and validated indicators exist, so it does not establish that the tools generally provide a more precise evaluation. (LLM, conf=0.84)
Experimental — accuracy not yet measuredThis review is the first overview of welfare assessment tools specific to elephants.
“While there have been several reviews of animal welfare frameworks (24–26), to our knowledge, this is the first overview of welfare assessment tools specific to elephants.”
From Comparison of animal welfare assessment tools and methodologies: need for an effective approach for captive elephants in Asia (2024) · cites this paper as [24]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
The use of leukocyte profiles to measure stress in vertebrates: a review for ecologists
Davis, A. K., Maney, D. L., & Maerz, J. C. (2008) · Functional Ecology · doi:10.1111/j.1365-2435.2008.01467.x · Cited by 1,558 · see citing works
Assessment of positive emotions in animals to improve their welfare
Boissy, A., Manteuffel, G., Jensen, M. B., Moe, R. O., Spruijt, B., Keeling, L. J., Winckler, C., Forkman, B., Dimitrov, I., Langbein, J., et al. (2007) · Physiology & Behavior · doi:10.1016/j.physbeh.2007.02.003 · Cited by 1,486 · see citing works
Physiological stress in ecology: lessons from biomedical research
Romero, L. M. (2004) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2004.03.008 · Cited by 1,440 · see citing works
Stereotypies: a critical review
Mason, G. J. (1991) · Animal Behaviour · doi:10.1016/s0003-3472(05)80640-2 · Cited by 1,302 · see citing works
Aubert, G., & Lansdorp, P. M. (2008) · Physiological Reviews · doi:10.1152/physrev.00026.2007 · Cited by 1,188 · see citing works
Animal welfare: concepts and measurement2
Broom, D. M. (1991) · Journal of Animal Science · doi:10.2527/1991.69104167x · Cited by 1,095 · see citing works
Fish welfare: Current issues in aquaculture
Ashley, P. J. (2006) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2006.09.001 · Cited by 1,076 · see citing works
A Scientific Conception of Animal Welfare that Reflects Ethical Concerns
Fraser, D. J., Weary, D. M., Pajor, E. A., & Milligan, B. N. (1997) · Animal Welfare · doi:10.1017/s0962728600019795 · Cited by 1,066 · see citing works
The biology of animal stress: basic principles and implications for animal welfare.
Moberg, G. P. (2000) · CABI Publishing eBooks · doi:10.1079/9780851993591.0000 · Cited by 1,003 · see citing works
The 2020 five domains model: including human-animal interactions in assessments of animal welfare
Mellor, D. J., Beausoleil, N. J., Littlewood, K. E., McLean, A. N., McGreevy, P. D., Jones, B., & Wilkins, C. (2020) · Animals · doi:10.3390/ani10101870 · Cited by 985 · see citing works
Updating Animal Welfare Thinking: Moving beyond the “Five Freedoms” towards “A Life Worth Living”
Mellor, D. (2016) · Animals · doi:10.3390/ani6030021 · Cited by 948 · see citing works
Measuring stress in wildlife: techniques for quantifying glucocorticoids
Sheriff, M. J., Dantzer, B., Delehanty, B., Palme, R., & Boonstra, R. (2011) · Oecologia · doi:10.1007/s00442-011-1943-y · Cited by 919 · see citing works
Current issues in fish welfare
Huntingford, F. A., Adams, C. E., Braithwaite, V. A., Kadri, S., Pottinger, T. G., Sandøe, P., & Turnbull, J. F. (2006) · Journal of Fish Biology · doi:10.1111/j.0022-1112.2006.001046.x · Cited by 873 · see citing works
Measuring Fecal Glucocorticoid Metabolites in Mammals and Birds: The Importance of Validation
TOUMA, C., & PALME, R. (2005) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1343.006 · Cited by 844 · see citing works
Exploration of the hypothalamic–pituitary–adrenal function as a tool to evaluate animal welfare
Mormède, P., Andanson, S., Aupérin, B., Beerda, B., Guemene, D. D., Malmkvist, J., Manteca, X., Manteuffel, G., Prunet, P., van Reenen, C. G., et al. (2007) · Physiology & Behavior · doi:10.1016/j.physbeh.2006.12.003 · Cited by 821 · see citing works
Self-citationAcute phase response in animals: a review.
Cray, C., Zaias, J., & Altman, N. H. (2009) · PubMed Central · Cited by 816 · see citing works
Broom, D. M., & Johnson, K. G. (2019) · Animal welfare · doi:10.1007/978-3-030-32153-6 · Cited by 788 · see citing works
Mendl, M., Burman, O. H. P., Parker, R. M. A., & Paul, E. S. (2009) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2009.02.023 · Cited by 763 · see citing works
Can’t stop, won’t stop: is stereotypy a reliable animal welfare indicator?
Mason, G., & Latham, N. (2004) · Animal Welfare · doi:10.1017/s096272860001438x · Cited by 718 · see citing works
Mellor, D., & Beausoleil, N. (2015) · Animal Welfare · doi:10.7120/09627286.24.3.241 · Cited by 627 · see citing works
Non-invasive measurement of glucocorticoids: Advances and problems
Palme, R. (2018) · Physiology & Behavior · doi:10.1016/j.physbeh.2018.11.021 · Cited by 614 · see citing works
PALME, R., RETTENBACHER, S., TOUMA, C., EL‐BAHR, S. M., & MÖSTL, E. (2005) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1327.021 · Cited by 598 · see citing works
A modest proposal: displacement activities as an indicator of emotions in primates
Dario Maestripieri, A., Schino, G., Aureli, F., & Troisi, A. (1992) · Animal Behaviour · doi:10.1016/s0003-3472(05)80592-5 · Cited by 583 · see citing works
Measuring Fecal Steroids: Guidelines for Practical Application
PALME, R. (2005) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1343.007 · Cited by 520 · see citing works
STRESS IN FREE-RANGING MAMMALS: INTEGRATING PHYSIOLOGY, ECOLOGY, AND NATURAL HISTORY
Reeder, D. M., & Kramer, K. M. (2005) · Journal of Mammalogy · doi:10.1644/bhe-003.1 · Cited by 467 · see citing works
Dantzer, B., Fletcher, Q. E., Boonstra, R., & Sheriff, M. J. (2014) · Conservation Physiology · doi:10.1093/conphys/cou023 · Cited by 444 · see citing works
A consensus endocrine profile for chronically stressed wild animals does not exist
Dickens, M. J., & Romero, L. M. (2013) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2013.06.014 · Cited by 411 · see citing works
Corticosterone in feathers is a long‐term, integrated measure of avian stress physiology
Bortolotti, G. R., Marchant, T. A., Blas, J., & German, T. N. (2008) · Functional Ecology · doi:10.1111/j.1365-2435.2008.01387.x · Cited by 410 · see citing works
Measuring cortisol, the major stress hormone in fishes
Sadoul, B. C., & Geffroy, B. (2019) · Journal of Fish Biology · doi:10.1111/jfb.13904 · Cited by 399 · see citing works
Assessing the ‘whole animal’: a free choice profiling approach
Wemelsfelder, F., Hunter, T. E. A., Mendl, M., & Lawrence, A. B. (2001) · Animal Behaviour · doi:10.1006/anbe.2001.1741 · Cited by 392 · see citing works
Individual variation in glucocorticoid stress responses in animals
Cockrem, J. F. (2013) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2012.11.025 · Cited by 365 · see citing works
Personality in nonhuman primates: a review and evaluation of past research
Freeman, H. D., & Gosling, S. D. (2010) · American Journal of Primatology · doi:10.1002/ajp.20833 · Cited by 356 · see citing works
Wielebnowski, N. C., Fletchall, N., Carlstead, K., Busso, J. M., & Brown, J. L. (2002) · Zoo Biology · doi:10.1002/zoo.10005 · Cited by 344 · see citing works
The use of hair cortisol for the assessment of stress in animals
Heimbürge, S., Kanitz, E., & Otten, W. (2018) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2018.09.016 · Cited by 329 · see citing works
Anti-glucocorticoid effects of dehydroepiandrosterone (DHEA).
Kalimi, M., Shafagoj, Y., Loria, R., Padgett, D., & Regelson, W. (1994) · Molecular and Cellular Biochemistry · doi:10.1007/bf00925945 · Cited by 328 · see citing works
Behaviour as a tool in the assessment of animal welfare
Dawkins, M. S. (2003) · Zoology · doi:10.1078/0944-2006-00122 · Cited by 294 · see citing works
Lutz, C., Well, A., & Novak, M. (2003) · American Journal of Primatology · doi:10.1002/ajp.10075 · Cited by 285 · see citing works
New directions for zoo animal welfare science
Whitham, J. C., & Wielebnowski, N. (2013) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2013.02.004 · Cited by 273 · see citing works
Romero, L. M., & Butler, L. K. (2007) · International Journal of Comparative Psychology · doi:10.46867/ijcp.2007.20.02.15 · Cited by 267 · see citing works
Measuring zoo animal welfare: theory and practice
Hill, S. P., & Broom, D. M. (2009) · Zoo Biology · doi:10.1002/zoo.20276 · Cited by 252 · see citing works
Acute Phase Proteins in Animals
Cray, C. (2011) · Progress in molecular biology and translational science · doi:10.1016/b978-0-12-394596-9.00005-6 · Cited by 228 · see citing works
Evaluating methods to quantify anthropogenic stressors on wild animals
Tarlow, E. M., & Blumstein, D. T. (2006) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2006.05.040 · Cited by 227 · see citing works
Production, usage, and comprehension in animal vocalizations
Seyfarth, R. M., & Cheney, D. L. (2009) · Brain and Language · doi:10.1016/j.bandl.2009.10.003 · Cited by 225 · see citing works
The sources of convergence between measures of apathy and depression
Marin, R. S., Firinciogullari, S., & Biedrzycki, R. C. (1993) · Journal of Affective Disorders · doi:10.1016/0165-0327(93)90040-q · Cited by 213 · see citing works
The 24/7 approach to promoting optimal welfare for captive wild animals
Brando, S., & Buchanan-Smith, H. M. (2018) · Behavioural Processes · doi:10.1016/j.beproc.2017.09.010 · Cited by 194 · see citing works
Behavioral Diversity as a Potential Indicator of Positive Animal Welfare
Miller, L. J., Vicino, G. A., Sheftel, J., & Lauderdale, L. K. (2020) · Animals · doi:10.3390/ani10071211 · Cited by 193 · see citing works
Interpreting indices of physiological stress in free-living vertebrates
Johnstone, C. P., Reina, R. D., & Lill, A. (2012) · Journal of Comparative Physiology B · doi:10.1007/s00360-012-0656-9 · Cited by 191 · see citing works
What Is so Positive about Positive Animal Welfare?—A Critical Review of the Literature
Lawrence, A. B., Vigors, B., & Sandøe, P. (2019) · Animals · doi:10.3390/ani9100783 · Cited by 188 · see citing works
INVITED REVIEW: The usefulness of measuring glucocorticoids for assessing animal welfare
Ralph, C. R., & Tilbrook, A. J. (2016) · Journal of Animal Science · doi:10.2527/jas.2015-9645 · Cited by 179 · see citing works
Müller, C., Jenni‐Eiermann, S., & Jenni, L. (2010) · Functional Ecology · doi:10.1111/j.1365-2435.2010.01816.x · Cited by 175 · see citing works
On Comparing the Behaviour of Zoo Housed Animals with Wild Conspecifics as a Welfare Indicator
Veasey, J. S., Waran, N. K., & Young, R. J. (1996) · Animal Welfare · doi:10.1017/s0962728600018297 · Cited by 173 · see citing works
Statement on the use of animal‐based measures to assess the welfare of animals
(AHAW), E. P. O. A. H. A. W. (2012) · EFSA Journal · doi:10.2903/j.efsa.2012.2767 · Cited by 165 · see citing works
Davis, A. K., & Maney, D. L. (2018) · Methods in Ecology and Evolution · doi:10.1111/2041-210x.13020 · Cited by 164 · see citing works
Assessing reptile welfare using behavioural criteria
Warwick, C., Arena, P. C., Lindley, S., Jessop, M., & Steedman, C. (2013) · In Practice · doi:10.1136/inp.f1197 · Cited by 159 · see citing works
Overall assessment of animal welfare: strategy adopted in Welfare Quality®
Botreau, R., Veissier, I., & Perny, P. (2009) · Animal Welfare · doi:10.1017/s0962728600000762 · Cited by 150 · see citing works
Watters, J. V., & Powell, D. (2011) · Zoo Biology · doi:10.1002/zoo.20379 · Cited by 141 · see citing works
Cumulative stress in research animals: Telomere attrition as a biomarker in a welfare context?
Melissa Bateson, B. (2015) · BioEssays · doi:10.1002/bies.201500127 · Cited by 140 · see citing works
Feather damaging behaviour in parrots: A review with consideration of comparative aspects
van Zeeland, Y. R. A., Spruit, B. M., Rodenburg, T. B., Riedstra, B., van Hierden, Y. M., Buitenhuis, B., Korte, S. M., & Lumeij, J. T. (2009) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2009.09.006 · Cited by 139 · see citing works
Gormally, B. M. G., & Romero, L. M. (2020) · Functional Ecology · doi:10.1111/1365-2435.13648 · Cited by 136 · see citing works
Vocalisations in farm animals: A step towards positive welfare assessment
Laurijs, K. A., Briefer, E. F., Reimert, I., & Webb, L. E. (2021) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2021.105264 · Cited by 135 · see citing works
Animal-based welfare monitoring: using keeper ratings as an assessment tool
Whitham, J. C., & Wielebnowski, N. (2009) · Zoo Biology · doi:10.1002/zoo.20281 · Cited by 134 · see citing works
Meehan, C. L., Millam, J. R., & Mench, J. A. (2003) · Applied Animal Behaviour Science · doi:10.1016/s0168-1591(02)00192-2 · Cited by 129 · see citing works
Maple, T. L., & Perdue, B. M. (2013) · Animal welfare · doi:10.1007/978-3-642-35955-2 · Cited by 126 · see citing works
Effects of acute stressors on nociception, adrenocortical responses and behavior of dairy cows
Herskin, M. S., Munksgaard, L., & Ladewig, J. (2004) · Physiology & Behavior · doi:10.1016/j.physbeh.2004.08.027 · Cited by 123 · see citing works
Searching for behavioral indicators of welfare in zoos: Uncovering anticipatory behavior
Watters, J. V. (2014) · Zoo Biology · doi:10.1002/zoo.21144 · Cited by 120 · see citing works
Rault, J., van den Munkhof, M. H., & Buisman‐Pijlman, F. T. A. (2017) · Frontiers in Psychology · doi:10.3389/fpsyg.2017.01521 · Cited by 118 · see citing works
Clegg, I. L. K., Borger-Turner, J. L., & Eskelinen, H. C. (2015) · Animal Welfare · doi:10.7120/09627286.24.3.267 · Cited by 118 · see citing works
How Abnormal Is the Behaviour of Captive, Zoo-Living Chimpanzees?
Birkett, L. P., & Newton‐Fisher, N. E. (2011) · PLoS ONE · doi:10.1371/journal.pone.0020101 · Cited by 111 · see citing works
Carbajal, A., Reyes‐López, F. E., Talló-Parra, O., López‐Béjar, M., & Tort, L. (2019) · Aquaculture · doi:10.1016/j.aquaculture.2019.04.005 · Cited by 108 · see citing works
The sources of convergence between measures of apathy and depression
Marin, R. S., Firinciogullari, S., & Biedrzycki, R. C. (1993) · Journal of Affective Disorders · doi:10.1016/0165-0327(93)90072-r · Cited by 105 · see citing works
An animal welfare risk assessment process for zoos
Sherwen, S. L., Hemsworth, L. M., Beausoleil, N. J., Embury, A., & Mellor, D. J. (2018) · Animals · doi:10.3390/ani8080130 · Cited by 105 · see citing works
Hands-on and hands-off measurement of stress.
Cook, C. J., Mellor, D. J., Harris, P. J., Ingram, J. R., & Matthews, L. R. (2000) · CABI Publishing eBooks · doi:10.1079/9780851993591.0123 · Cited by 100 · see citing works
Staley, M., Conners, M. G., Hall, K., & Miller, L. J. (2018) · Hormones and Behavior · doi:10.1016/j.yhbeh.2018.04.011 · Cited by 100 · see citing works
Status of animal welfare research in zoos and aquariums: Where are we, where to next?
Binding, S., Farmer, H., Krusin, L., & Cronin, K. A. (2020) · The Journal of zoo and aquarium research · doi:10.19227/jzar.v8i3.505 · Cited by 98 · see citing works
Miller, L. J., Pisacane, C., & Vicino, G. A. (2016) · Animal Welfare · doi:10.7120/09627286.25.3.325 · Cited by 93 · see citing works
Stoinski, T. S., Jaicks, H. F., & Drayton, L. A. (2012) · Zoo Biology · doi:10.1002/zoo.20425 · Cited by 91 · see citing works
Kalliokoski, O., Jellestad, F., & Murison, R. (2019) · Scientific Reports · doi:10.1038/s41598-019-48517-2 · Cited by 87 · see citing works
Beyond Glucocorticoids: Integrating Dehydroepiandrosterone (DHEA) into Animal Welfare Research
Whitham, J. C., Bryant, J. L., & Miller, L. J. (2020) · Animals · doi:10.3390/ani10081381 · Cited by 86 · see citing works
Miller, L. J. (2012) · Zoo Biology · doi:10.1002/zoo.20411 · Cited by 84 · see citing works
Development of a behavioural welfare assessment tool for routine use with captive elephants
Yon, L., Williams, E., Harvey, N. D., & Asher, L. (2019) · PLoS ONE · doi:10.1371/journal.pone.0210783 · Cited by 83 · see citing works
Lukas, K. E. (1999) · Applied Animal Behaviour Science · doi:10.1016/s0168-1591(98)00239-1 · Cited by 77 · see citing works
Mendl, M. (2001) · Nature · doi:10.1038/35065194 · Cited by 73 · see citing works
Assessing Animal Welfare with Behavior: Onward with Caution
Watters, J. V., Krebs, B. L., & Eschmann, C. L. (2021) · Journal of Zoological and Botanical Gardens · doi:10.3390/jzbg2010006 · Cited by 73 · see citing works
Blubber cortisol qualitatively reflects circulating cortisol concentrations in bottlenose dolphins
Champagne, C. D., Kellar, N. M., Crocker, D. E., Wasser, S. K., Booth, R. K., Trego, M. L., & Houser, D. S. (2016) · Marine Mammal Science · doi:10.1111/mms.12352 · Cited by 72 · see citing works
Cognitive Bias in Zoo Animals: An Optimistic Outlook for Welfare Assessment
Clegg, I. L. K. (2018) · Animals · doi:10.3390/ani8070104 · Cited by 71 · see citing works
Vera, F., Zenuto, R. R., & Antenucci, C. D. (2017) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2017.01.010 · Cited by 69 · see citing works
Repeatability of glucocorticoid hormones in vertebrates: a meta-analysis
Schoenemann, K. L., & Bonier, F. (2018) · PeerJ · doi:10.7717/peerj.4398 · Cited by 66 · see citing works
Reproductive Sciences in Animal Conservation
(2019) · Advances in Experimental Medicine and Biology · doi:10.1007/978-3-030-23633-5 · Cited by 64 · see citing works
Morfeld, K. A., Lehnhardt, J., Alligood, C. A., Bolling, J., & Brown, J. L. (2014) · PLoS ONE · doi:10.1371/journal.pone.0093802 · Cited by 63 · see citing works
The translational study of apathy—an ecological approach
Cathomas, F., Hartmann-Riemer, M. N., Seifritz, E., Pryce, C. R., & Kaiser, S. (2015) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2015.00241 · Cited by 61 · see citing works
FUNCTIONAL ANALYSIS AND TREATMENT OF SELF‐INJURY IN A CAPTIVE OLIVE BABOON
Dorey, N. R., Rosales‐Ruiz, J., Smith, R. G., & Lovelace, B. (2009) · Journal of Applied Behavior Analysis · doi:10.1901/jaba.2009.42-785 · Cited by 60 · see citing works
Williams, E., Chadwick, C., Yon, L., & Asher, L. (2018) · Animal Welfare · doi:10.7120/09627286.27.3.235 · Cited by 59 · see citing works
Dantzer, B., Westrick, S. E., & van Kesteren, F. (2016) · Integrative and Comparative Biology · doi:10.1093/icb/icw051 · Cited by 57 · see citing works
Orban, D. A., Soltis, J. M., Perkins, L., & Mellen, J. D. (2017) · Zoo Biology · doi:10.1002/zoo.21366 · Cited by 57 · see citing works
Baxter, E., & Plowman, A. B. (2001) · Animal Welfare · doi:10.1017/s0962728600024052 · Cited by 57 · see citing works
Small, T. W., Bebus, S. E., Bridge, E. S., Elderbrock, E. K., Ferguson, S. M., Jones, B. C., & Schoech, S. J. (2017) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2017.01.028 · Cited by 56 · see citing works
An analysis of regurgitation and reingestion in captive chimpanzees
Baker, K. C., & Easley, S. P. (1996) · Applied Animal Behaviour Science · doi:10.1016/0168-1591(96)01061-1 · Cited by 54 · see citing works
Identification of Acute Phase Proteins and Assays Applicable in Nondomesticated Mammals
Bertelsen, M. F., Kjelgaard-Hansen, M. J., Grøndahl, C., Heegaard, P. M. H., & Jacobsen, S. E. (2009) · Journal of Zoo and Wildlife Medicine · doi:10.1638/2007-0125.1 · Cited by 53 · see citing works
Factors Influencing Scratching Behaviour in Long-Tailed Macaques (Macaca fascicularis)
Pavani, S., Maestripieri, D., Schino, G., Turillazzi, P. G., & Scucchi, S. (1991) · Folia Primatologica · doi:10.1159/000156561 · Cited by 52 · see citing works
Animal Welfare and Resistance to Disease: Interaction of Affective States and the Immune System
Düpjan, S., & Dawkins, M. S. (2022) · Frontiers in Veterinary Science · doi:10.3389/fvets.2022.929805 · Cited by 50 · see citing works
Reconsidering coprophagy as an indicator of negative welfare for captive chimpanzees
Hopper, L. M., Freeman, H. D., & Ross, S. R. (2016) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2016.01.002 · Cited by 48 · see citing works
Role of oxytocin in improving the welfare of farm animals — A review
Chen, S., & Sato, S. (2016) · Asian-Australasian Journal of Animal Sciences · doi:10.5713/ajas.15.1058 · Cited by 46 · see citing works
Nature calls: intelligence and natural foraging style predict poor welfare in captive parrots
Mellor, E., Kinkaid, H. M., Mendl, M., Cuthill, I. C., van Zeeland, Y. R. A., & Mason, G. J. (2021) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2021.1952 · Cited by 46 · see citing works
Can sleep behaviour be used as an indicator of stress in group-housed rats (Rattus norvegicus)?
Abou-Ismail, U., Burman, O., Nicol, C. J., & Mendl, M. (2007) · Animal Welfare · doi:10.1017/s0962728600031298 · Cited by 42 · see citing works
Cronin, K. A., & Ross, S. R. (2019) · Animal Welfare · doi:10.7120/09627286.28.2.157 · Cited by 42 · see citing works
Neindre, P. L., Bernard, É., Boissy, A., Boivin, X., Calandreau, L., Delon, N., Deputte, B. L., Desmoulin‐Canselier, S., Dunier, M., Faivre, N., et al. (2017) · EFSA Supporting Publications · doi:10.2903/sp.efsa.2017.en-1196 · Cited by 42 · see citing works
Berkvens, C. N., Hyatt, C. V., Gilman, C. I., Pearl, D. L., Barker, I. K., & Mastromonaco, G. F. (2013) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2013.08.011 · Cited by 41 · see citing works
Huber, N., Marasco, V., Painer, J., Vetter, S. G., Göritz, F., Kaczensky, P., & Walzer, C. (2019) · Frontiers in Veterinary Science · doi:10.3389/fvets.2019.00105 · Cited by 39 · see citing works
Edwards, K. L., Bansiddhi, P., Paris, S., Galloway, M., & Brown, J. L. (2019) · Conservation Physiology · doi:10.1093/conphys/coy077 · Cited by 36 · see citing works
Diana, A., Salas, M., Pereboom, Z., Mendl, M., & Norton, T. (2021) · Animals · doi:10.3390/ani11113048 · Cited by 36 · see citing works
Self-citationSalas, M., Manteca, X., Abáigar, T., Delclaux, M., Enseñat, C., Martínez‐Nevado, E., Quevedo, M. Á., & Fernández-Bellón, H. (2018) · Animals · doi:10.3390/ani8070111 · Cited by 33 · see citing works
Self-citationCarbajal, A., Soler, P., Talló-Parra, O., Isasa, M., Echevarría, C. A., López-Béjar, M., & Vinyoles, D. (2019) · Animals · doi:10.3390/ani9110939 · Cited by 33 · see citing works
Animal-based indicators to assess welfare in zoo animals.
Manteca, X., Amat, M., Salas, M., & Temple, D. (2016) · CABI Reviews · doi:10.1079/pavsnnr201611010 · Cited by 32 · see citing works
Self-citationIndividual differences in chimpanzee reconciliation relate to social switching behaviour
Webb, C. E., Franks, B., Romero, T., Higgins, E. T., & de Waal, F. Β. Μ. (2014) · Animal Behaviour · doi:10.1016/j.anbehav.2014.01.014 · Cited by 31 · see citing works
Guindre‐Parker, S. (2018) · Integrative and Comparative Biology · doi:10.1093/icb/icy048 · Cited by 28 · see citing works
Zoo-based amphibian research and conservation breeding programs
Browne, R. K., Wolfram, K., García, G., Bagaturov, M. F., & Pereboom, Z. (2011) · Zenodo (CERN European Organization for Nuclear Research) · doi:10.5281/zenodo.13712179 · Cited by 27 · see citing works
Cortisol: often not the best indicator of stress and poor welfare
Broom, D. M. (2017) · Physiology News · doi:10.36866/pn.107.30 · Cited by 25 · see citing works
Monclús, L., Carbajal, A., Talló-Parra, O., Sabés‐Alsina, M., Darwich, L., Molina‐López, R. A., & López‐Béjar, M. (2017) · Journal für Ornithologie · doi:10.1007/s10336-016-1424-5 · Cited by 24 · see citing works
Measuring peripheral oxytocin and vasopressin in nonhuman primates
Ziegler, T. E. (2018) · American Journal of Primatology · doi:10.1002/ajp.22871 · Cited by 24 · see citing works
Skovlund, C. R., Kirchner, M. K., Moos, L. W., Alsted, N., Manteca, X., Talló-Parra, O., Stelvig, M., & Forkman, B. (2021) · Animal Welfare · doi:10.7120/09627286.30.1.001 · Cited by 24 · see citing works
Self-citationMiller, L. J., & Tobey, J. R. (2012) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2012.07.011 · Cited by 20 · see citing works
Krebs, B. L., Chudeau, K. R., Eschmann, C. L., Tu, C. W., Pacheco, E., & Watters, J. V. (2022) · Frontiers in Veterinary Science · doi:10.3389/fvets.2022.972217 · Cited by 17 · see citing works
Laméris, D. W., Verspeek, J., Salas, M., Staes, N., Torfs, J. R. R., Eens, M., & Stevens, J. M. G. (2022) · Animals · doi:10.3390/ani12213002 · Cited by 11 · see citing works
Self-citationRacciatti, D. S., Feld, A., Rial, L. A., Blanco, C., & Tallo-Parra, O. (2022) · Frontiers in Veterinary Science · doi:10.3389/fvets.2022.1033821 · Cited by 11 · see citing works
Directions in animal enclosure use studies
Brereton, J. E. (2020) · The Journal of zoo and aquarium research · doi:10.19227/jzar.v8i1.330 · Cited by 10 · see citing works
Kalliokoski, O., Jellestad, F., & Murison, R. (2018) · bioRxiv · doi:10.1101/375667 · Cited by 4
Flagged first, then by citations
Research works printed but not linked: 8
- [13]Tallo-Parra O. Delfour F. von Fersen L. Garcia-Párraga D. Manteca X. Moneal-Pawlowsky T. Pilenga C. Ternes K. Clegg I.L.K. Garcia Hartmann M. Dolphin-WET (Welfare Evaluation Tool): A New Conceptual Framework for Welfare Evaluation of Bottlenose Dolphins (Tursiops truncatus) under Human Care Proceedings of the EAZA Annual Conference Valencia, Spain 17–21 September 2019
- [22]Watters J.V. Krebs B.L. Pacheco E. Measuring Welfare through Behavioral Observation and Adjusting It with Dynamic Environments Scientific Foundations of Zoos and Aquariums Cambridge University Press Cambridge, UK 2019 212 240
- [32]Hosey G. Melfi V. Behaviour P.S. Zoo Animals: Behaviour, Management and Welfare Oxford University Press Oxford, UK 2009 82 128
- [73]Paul-Murphy J. Molter C. Overview of Animal Welfare in Zoos Fowler’s Zoo and Wild Animal Medicine Current Therapy, Volume 9 Elsevier St. Louis, MO, USA 2019 64 72
- [94]Staley M. Miller L.J. Salivary Bioscience and Research on Animal Welfare and Conservation Science Salivary Bioscience Springer International Publishing Cham, Switzerland 2020 675 708
- [110]Fraser D. Understanding Animal Welfare: The Science in Its Cultural Context Wiley-Blackwell Publishing, Inc. Oxford, UK 2008 978-1-405-13695-2
- [113]Schreck C.B. Tort L. Farrell A.P. Brauner C.J. Biology of Stress in Fish Academic Press Cambridge, MA, USA 2016 9780128027288
- [124]Swanberg S.E. Telomeres and Telomerase in Birds Conn’s Handbook of Models for Human Aging Elsevier Cambridge, MA, USA 2018 313 322 9780128113530
Cited by
Sorted by citations
Beer, H. N., Shrader, T. C., Schmidt, T. B., & Yates, D. T. (2023) · Journal of Zoological and Botanical Gardens · doi:10.3390/jzbg4040046 · Cited by 40 · see citing works
Kelly, R. J., Freeman, M. S., & Rose, P. E. (2025) · Frontiers in Ethology · doi:10.3389/fetho.2025.1517294 · Cited by 20 · see citing works
Utilizing vocalizations to gain insight into the affective states of non-human mammals
Whitham, J. C., & Miller, L. J. (2024) · Frontiers in Veterinary Science · doi:10.3389/fvets.2024.1366933 · Cited by 19 · see citing works
Baumgartner, K., Hüttner, T., Clegg, I. L. K., Hartmann, M. G., García‐Párraga, D., Manteca, X., Mercera, B., Monreal‐Pawlowsky, T., Pilenga, C., Ternes, K., et al. (2024) · Animals · doi:10.3390/ani14050701 · Cited by 17 · see citing works
Self-citationKhan, E. A., Rizwan, M., Wang, Y., Munir, F., & Hua, J. (2025) · Veterinary Sciences · doi:10.3390/vetsci12080733 · Cited by 16 · see citing works
Соколенко, С. В., Sokolenko, Y. V., Van, Y. L., Ozymok, M. O., Kobal, I., & Соколенко, В. Л. (2024) · Regulatory Mechanisms in Biosystems · doi:10.15421/0224111 · Cited by 10 · see citing works
Behavioral factors linking sustainability and animal welfare in dairy farming
Mohammadzadeh, M., Hayati, D., & Valizadeh, N. (2025) · Scientific Reports · doi:10.1038/s41598-025-10260-2 · Cited by 10 · see citing works
Ghimire, R., Brown, J. L., Thitaram, C., & Bansiddhi, P. (2024) · Frontiers in Veterinary Science · doi:10.3389/fvets.2024.1370909 · Cited by 8 · see citing works
“These offer a refined and more precise evaluation of animal welfare by tailoring assessments to the unique needs, behaviors, and physiological aspects of a particular species (24).”
BackgroundAnimal–Visitor Interactions in Zoos and Aquariums: A Systematic Review
Lin, G.-Y., Ng, K. C. H., & Fernandez, E. J. (2025) · Animals · doi:10.3390/ani15131924 · Cited by 6 · see citing works
Martin, S., Stafford, G., & Miller, D. S. (2024) · Animals · doi:10.3390/ani14050736 · Cited by 6 · see citing works
Comparing Manual and Automated Spatial Tracking of Captive Spider Monkeys Using Heatmaps
Lund, S. M., Gammelgård, F., Nielsen, J., Larsen, L. L. N., Christensen, N., Hansen, S. P., Kristensen, T., Rodkjær, H. H. Ø., Sivagnanasundram, S. M., Thomsen, B. Ø., et al. (2025) · Animals · doi:10.3390/ani15203056 · Cited by 5 · see citing works
Simplifying the Animal Welfare Assessment Grid for enhanced accessibility
Kim, J., Choi, J.-H., Ryu, H., & Kang, H. (2024) · Frontiers in Veterinary Science · doi:10.3389/fvets.2024.1459560 · Cited by 4 · see citing works
Alonso-Almorox, P., Blanco, A., Fiorito, C., Sierra, E., Suárez‐Santana, C. M., Consoli, F., Arbelo, M., Grandía-Guzmán, R., Molpeceres-Diego, I., Gomez, A., et al. (2025) · Animals · doi:10.3390/ani15050735 · Cited by 4 · see citing works
Understanding animal introductions and welfare in zoos: A scoping review
Martinez, C. C., James-Aldridge, V., McWhorter, T. J., & Fernandez, E. J. (2025) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2025.106737 · Cited by 3 · see citing works
From concept to action: Operationalising animal welfare strategies in zoos and aquaria
Partoon, J., Sherwen, S. L., Smith, M., Riley, L. M., & Whittaker, A. L. (2025) · Animal Welfare · doi:10.1017/awf.2025.10053 · Cited by 3 · see citing works
Baotic, A. (2025) · Frontiers in Conservation Science · doi:10.3389/fcosc.2025.1590562 · Cited by 3 · see citing works
Higgs, S., Huck, M., Sheffield, D., & Fido, D. (2025) · Journal of Zoological and Botanical Gardens · doi:10.3390/jzbg6040061 · Cited by 2 · see citing works
Automated Activity Tracking and Space Use Monitoring of Captive Jaguars with Machine Learning
Larsen, L. L. N., Christensen, N., Kristensen, T., Faddersbøll, T. L., Lassen, A. R. W., Rasmussen, B., Pagh, S., & Pertoldi, C. (2026) · Animals · doi:10.3390/ani16101504 · Cited by 2 · see citing works
Plácido, M., Talló-Parra, O., & Salas, M. (2024) · Journal of Applied Animal Welfare Science · doi:10.1080/10888705.2024.2409158 · Cited by 2 · see citing works
Self-citationModification of Domestic Animal Lameness Scales for Use in Asiatic Black Bears (Ursus thibetanus)
Hunter-Ishikawa, M., Nakatani, J. Y., & Miller, D. S. (2023) · Animals · doi:10.3390/ani13213302 · Cited by 2 · see citing works
Cooper‐Rogers, B., Klingner, P., Hanson, S. L., Partoon, J., & Fernandez, E. J. (2026) · Zoo Biology · doi:10.1002/zoo.70089 · Cited by 2 · see citing works
Nightly space use of African ungulates in zoos
Gübert, J., & Dierkes, P. W. (2024) · Discover Animals · doi:10.1007/s44338-024-00039-6 · Cited by 1 · see citing works
Gartland, K. N., Bovee, E., & Fuller, G. A. (2025) · American Journal of Primatology · doi:10.1002/ajp.70005 · Cited by 1 · see citing works
George, A. J., Tull, S., & Rose, P. E. (2025) · Zoo Biology · doi:10.1002/zoo.70001 · Cited by 1 · see citing works
Environmental and biological drivers of movement activity in Callimico goeldii under zoo conditions
Nieckarz, Z., Nowicki, J., Lasko, M., & Pawlak, K. (2025) · Scientific Reports · doi:10.1038/s41598-025-18540-7 · Cited by 1 · see citing works
Geijtenbeek, J. W., van den Berg, L. M., & Roth, T. S. (2026) · Animal Welfare · doi:10.1017/awf.2026.10086 · Cited by 1 · see citing works
Arbogast, D. M., Freeman, E. W., Donelan, E. M., Jones, M. K., Rispoli, L. A., Roth, T. L., & Metrione, L. C. (2026) · Theriogenology Wild · doi:10.1016/j.therwi.2026.100155 · Cited by 1 · see citing works
Yamamoto, T., Kakizaki, T., Takashima, Y., Tsunesumi, H., & Yoda, K. (2025) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2025.106633 · Cited by 1 · see citing works
Identification and Validation of Operational Pain Indicators in Anurans
González, S., Caiozzi, A., Cabeza, O., & Cañon–Jones, H. (2025) · Journal of Zoological and Botanical Gardens · doi:10.3390/jzbg6040049 · Cited by 1 · see citing works
Ensuring species’ survival and longevity: The role of modern zoos
Chanyandura, A., ALOTAIBA, A. M., Alqahtani, H. A., & ALHAJERI, M. M. (2025) · Animal Reports · doi:10.64636/ar.34 · Cited by 1 · see citing works
Fernández-Sánchez, M., Barros-García, C., & Garzón, M. (2026) · Frontiers in Veterinary Science · doi:10.3389/fvets.2026.1736943 · Cited by 1 · see citing works
Yamamoto, T., Adachi, D., Kakizaki, T., Takashima, Y., Tsunesumi, H., & Yoda, K. (2026) · Zoo Biology · doi:10.1002/zoo.70072 · Cited by 1 · see citing works
Marques, G. N., Cruz, J. T., Pinto, M., Leal, M. O., Flanagan, C. A., Urbani, N., & de Carvalho, L. M. (2023) · Journal of Zoological and Botanical Gardens · doi:10.3390/jzbg4040056 · Cited by 1 · see citing works
Gandia, K. M., Elliott, J., Girling, S. J., Kessler, S. E., & Buchanan‐Smith, H. M. (2024) · Animals · doi:10.3390/ani14152223 · Cited by 1 · see citing works
Environmental Control of Pacing in Cougars
Fahlmann, E. A. (2023) · doi:10.12794/metadc2256952
(2024) · Frontiers research topics · doi:10.3389/978-2-8325-5519-4
Arbuatti, A., Spiezio, C., Martino, G. D., & Lucidi, P. (2026) · Frontiers in Ethology · doi:10.3389/fetho.2026.1784527
Worup, A. M., Sonne, A. S., Kudahl, J., Jacobsen, J. H., Pagh, S., Faddersbøll, T. L., & Pertoldi, C. (2026) · Animals · doi:10.3390/ani16081165
Palacios, D. A., Gartland, K. N., Andrus, M., Vassallo, M., & Fuller, G. A. (2026) · Discover Animals · doi:10.1007/s44338-026-00190-2
Rose, P. E., Azogu‐Sepe, I., Clifforde, L. M., Harley, J. J., Hunt, K., Kelly, R. J., de Figueiredo, R. L., Partoon, J., Stanley, C. R., & Whiteside, M. (2026) · Frontiers in Veterinary Science · doi:10.3389/fvets.2026.1793169
Kang, H. (2026) · Frontiers in Veterinary Science · doi:10.3389/fvets.2026.1814857
Caracterización de la biodiversidad de fauna en el bioparque Yanacocha
Pérez, I. E. F., López, W. F. N., Licuy, N. D. S., & López, D. L. C. (2026) · Horizontes Amazónicos · doi:10.67321/2gxa2f16
Gartland, K. N., Bovee, E., Reed, A. N., & Fuller, G. A. (2026) · American Journal of Primatology · doi:10.1002/ajp.70183
Carbajal, A., Serres‐Corral, P., Horta, E., Monreal‐Pawlowsky, T., & López‐Béjar, M. (2026) · Marine Mammal Science · doi:10.1111/mms.70272
Animal welfare or animal well-being: A review of terminological use in zoo research and practice
Stratford, L., Murray, L., Edwards, K. L., & Holmes, L. (2026) · Animal Welfare · doi:10.1017/awf.2026.10108
Racciatti, D. S., Talló-Parra, O., Manteca, X., Blanco, C. J., & Ferrari, H. R. (2026) · Animals · doi:10.3390/ani16193122
Self-citationKim, J.-Y., Lee, W., Jeong, D.-W., & Kim, M.-G. (2026) · Frontiers in Ethology · doi:10.3389/fetho.2026.1919787
Vaca, E. F. T., & Torres, O. P. N. (2026) · ConcienciaDigital · doi:10.33262/concienciadigital.v9i4.3797
Shedding light: an evidence-based approach to adapting cognitive bias tests for reptiles
Turner, J. T., Fernandez, E. J., & Whittaker, A. L. (2026) · Biology Letters · doi:10.1098/rsbl.2026.0318
- Authors
- Tallo-Parra, O., Salas, M., & Manteca, X.
- Affiliations
- School of Veterinary Science, Universitat Autònoma de Barcelona, Campus UAB, 08193 Barcelona, Spain
- Royal Zoological Society of Antwerp (BE)
- Universitat Autònoma de Barcelona (ES)
- Corresponding author
- Manteca, Xavier
- Venue
- Animals
- Publisher
- MDPI AG
- Published
- 2023-06-12
- Volume
- 13
- Issue
- 12
- Pages
- 1966
- ISSN
- 2076-2615 (ISSN-L)
- PMC
- PMC10294817
- OpenAlex
- W4380485712
- Cited by
- 45
- References
- 124
- Citations by year
- 2026: 16 · 2025: 16 · 2024: 9 · 2023: 4
- FWCI
- 2.06
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Animals (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Dipòsit Digital de Documents de la UAB (Universitat Autònoma de Barcelona) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Flemish Government
- Topics
- Health Sciences › Veterinary › Small Animals › Animal Behavior and Welfare Studies
- Health Sciences › Veterinary › Small Animals › Veterinary Pharmacology and Anesthesia
- Social Sciences › Psychology › Social Psychology › Primate Behavior and Ecology
- Keywords
- zoo animal welfare, animal welfare assessment, welfare indicators, behavioural indicators, physiological parameters, zoos and aquariums, captive animals
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review