Hostname: page-component-77f85d65b8-grvzd Total loading time: 0 Render date: 2026-04-19T09:09:49.141Z Has data issue: false hasContentIssue false
  • English
  • Français

Technical contribution: a cautionary note on the use of behavioural diversity (H-Index) in animal welfare science

Part of: Zoo Animals Collection

Published online by Cambridge University Press:  01 January 2023

KA Cronin  and
SR Ross
KA Cronin*
Affiliation:
Animal Welfare Science Program, Lincoln Park Zoo, 2001 North Clark Street, Chicago, IL 60614, USA
SR Ross
Affiliation:
Lester E Fisher Center for the Study & Conservation of Apes, Lincoln Park Zoo, 2001 North Clark Street, Chicago, IL 60614, USA
*
* Contact for correspondence and requests for reprints: kcronin@lpzoo.org
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the 'Save PDF' action button.

Animal welfare scientists actively seek reliable and practical metrics that can serve as indicators of animal welfare for use with agricultural, laboratory and zoo-housed animals. Behavioural diversity as a welfare concept originated from early welfare scientists linking poor animal welfare with a high proportion of time spent engaged in stereotyped behaviours and little expression of behaviours that would be expected under wild, or natural conditions. Recently, the concept of behavioural diversity as a welfare indicator has been widely adopted and is frequently quantified by the Shannon-Wiener Diversity Index (H-index). However, the H-Index is fraught with theoretical and mathematical limitations when applied to animal welfare. Four key problems with this metric are demonstrated: the metric's responsivity to the size of the behavioural repertoire and the underlying assumption that larger behavioural repertoires reflect better welfare, the sensitivity of the metric to arbitrary decisions about the resolution of behavioural categories, the fact that the calculation of the metric is agnostic to the valence of behaviours, and the metric's susceptibility to the common practice of excluding some behavioural categories. Moving forward, we recommend focusing on validated welfare measures that are sensitive to valence when evaluating animal welfare.

Keywords

animal welfarebehavioural diversityH-indexShannon-Wiener Diversity Indexwelfare metricswell-being

Information

Type
Articles
Information
Animal Welfare , Volume 28 , Issue 2 , May 2019 , pp. 157 - 164
Copyright
© 2019 Universities Federation for Animal Welfare

References

Boissy, A, Manteuffel, G, Jensen, MB, Moe, RO, Spruijt, B, Keeling, LJ, Winckler, C, Forkman, B, Dimitrov, I, Langbein, J and Bakken, M 2007 Assessment of positive emotions in ani-mals to improve their welfare. Physiology & Behavior 92: 375–397. https://doi.org/10.1016/j.physbeh.2007.02.003CrossRefGoogle Scholar
Bracke, MB and Hopster, H 2006 Assessing the importance of natural behavior for animal welfare. Journal of Agricultural and Environmental Ethics 19: 77–89. https://doi.org/10.1007/s10806-005-4493-7CrossRefGoogle Scholar
Brando, S and Buchanan-Smith, HM The 24/7 approach to promoting optimal welfare for captive wild animals. Behavioural Processes 156: 83–95. https://doi.org/10.1016/j.beproc.2017.09.010CrossRefGoogle Scholar
Broom, DM 1988 The scientific assessment of animal welfare. Applied Animal Behaviour Science 20: 5–19. https://doi.org/10.1016/0168-1591(88)90122-0CrossRefGoogle Scholar
Brown, M, Carbone, L, Conlee, KM, Dawkins, MS, Duncan, IJ, Fraser, D, Griffin, G, Hampshire, VA, Lambert, LA, Mench, JA and Morton, D 2006 Report of the working group on animal distress in the laboratory. Lab Animal 35: 26. https://doi.org/10.1038/laban0906-26CrossRefGoogle Scholar
Brown, SM, Klaffenbock, M, Nevison, IM and Lawrence, AB 2015 Evidence for litter differences in play behaviour in pre-weaned pigs. Applied Animal Behaviour Science 172: 17–25. https://doi.org/10.1016/j.applanim.2015.09.007CrossRefGoogle ScholarPubMed
Carter, GG and Wilkinson, GS 2015 Intranasal oxytocin increases social grooming and food sharing in the common vam-pire bat Desmodus rotundus. Hormones and Behaviour 75: 150–153. https://doi.org/10.1016/j.yhbeh.2015.10.006CrossRefGoogle ScholarPubMed
Charmoy, K, Sullivan, T and Miller, LJ 2015 Impact of differ-ent forms of environmental enrichment on foraging and activity levels in gorillas, Gorilla gorilla gorilla. Animal Behavior and Cognition 2: 233–240. https://doi.org/10.12966/abc.08.03.2015CrossRefGoogle Scholar
Clark, FE and Melfi, VA 2012 Environmental enrichment for a mixed-species nocturnal mammal exhibit. Zoo Biology 31: 397–413. https://doi.org/10.1002/zoo.20380CrossRefGoogle ScholarPubMed
Collins, C, Quirke, T, Overy, L, Flannery, K and O’Riordan, R 2016 The effect of the zoo setting on the behavioural diversity of captive gentoo penguins and the implications for their educational potential. Journal of Zoo and Aquarium Research 4: 85–90Google Scholar
Dawkins, MS 2004 Using behaviour to assess animal welfare. Animal Welfare 13: S3–S7Google Scholar
Dawkins, MS 2015 Animal welfare and the paradox of animal consciousness. Advances in the Study of Behavior 47: 5–38. https://doi.org/10.1016/bs.asb.2014.11.001CrossRefGoogle Scholar
Duncan, IJ and Petherick, JC 1991 The implications of cognitive processes for animal welfare. Journal of Animal Science 691: 5017–5022. https://doi.org/10.2527/1991.69125017xGoogle Scholar
Fàbregas, MC, Guillén-Salazar, F and Garcés-Narro, C 2012 Do naturalistic enclosures provide suitable environments for zoo animals? Zoo Biology 31: 362–373. https://doi.org/10.1002/zoo.20404CrossRefGoogle ScholarPubMed
Farm Animal Welfare Council 1992 The Five Freedoms. Farm Animal Welfare Council: London, UKGoogle Scholar
Fraser, D 1995 Science values and animal welfare: exploring the ‘inextricable connection’ Animal Welfare 4: 103–117Google Scholar
Fraser, D 2008 Toward a global perspective on farm animal wel-fare. Applied Animal Behaviour Science 113: 330–339. https://doi.org/10.1016/j.applanim.2008.01.011CrossRefGoogle Scholar
Fraser, D and Duncan, IJ 1998 Pleasures, pains, and animal wel-fare: toward a natural history of affect. Animal Welfare 7: 383–396Google Scholar
Frézard, A and Pape, GL 2003 Contribution to the welfare of captive wolves Canis lupus lupus: a behavioral comparison of six wolf packs. Zoo Biology 22: 33–44. https://doi.org/10.1002/zoo.10070CrossRefGoogle Scholar
Galhardo, L, Correia, J and Oliveira, RF 2008 The effect of substrate availability on behavioural and physiological indicators of welfare in the African cichlid Oreochromis mossambicus. Animal Welfare 17: 239–254Google Scholar
Gonyou, HW 1994 Why the study of animal behavior is associ-ated with the animal welfare issue. Journal of Animal Science 72:2171–2177. https://doi.org/10.2527/1994.7282171xCrossRefGoogle Scholar
Griffin, AS, Diquelou, M and Perea, M 2014 Innovative prob-lem solving in birds: a key role of motor diversity. Animal Behaviour 92: 221–227. https://doi.org/10.1016/j.anbehav.2014.04.009CrossRefGoogle Scholar
Hancocks, D 1980 Bringing nature into the zoo: inexpensive solutions for zoo environments. International Journal for the Study of Animal Problems 13: 170–177Google Scholar
Hirt, H and Wechsler, B 1994 Behavioural diversity as a meas-ure of welfare: a study in pigs. Applied Animal Behaviour Science 40:82–83. https://doi.org/10.1016/0168-1591(94)90108-2CrossRefGoogle Scholar
Izzo, GN, Bashaw, MJ and Campbell, JB 2011 Enrichment and individual differences affect welfare indicators in squirrel monkeys Saimiri sciureus. Journal of Comparative Psychology 125: 347–352. https://doi.org/10.1037/a0024294CrossRefGoogle ScholarPubMed
Keeling, LJ, Rushen, J and Duncan, IJ 2011 Understanding ani-mal welfare. In: Appleby, MC, Mench, JA, Olsson, IAS and Hughes, BO (eds) Animal Welfare pp 13–26. Cambridge University Press: Cambridge, UK. https://doi.org/10.1079/9781845936594.0013Google Scholar
Kistler, C, Hegglin, D, Wurbel, H and Konig, B 2009 Feeding enrichment in an opportunistic carnivore: The red fox. Applied Animal Behaviour Science 116: 260–265. https://doi.org/10.1016/j.applanim.2008.09.004CrossRefGoogle Scholar
Lyon, M and Robbins, T 1975 The action of central nervous sys-tem stimulant drugs: A general theory concerning amphetamine effects. In: Essman, W and Valzelli, L (eds) Current Developments in Psychopharmacology Vol 2 pp 81–163. Spectrum: New York, NY, USAGoogle Scholar
Major, CA, Kelly, BJ, Novak, MA, Davenport, MD, Stonemetz, KM and Meyer, JS 2009 The anxiogenic drug FG7142 increases self-injurious behavior in male rhesus monkeys Macaca mulatta. Life Sciences 85: 753–758. https://doi.org/10.1016/j.lfs.2009.10.003CrossRefGoogle ScholarPubMed
Mason, G and Mendl, M 1993 Why is there no simple way of measuring animal welfare? Animal Welfare 24: 301–319Google Scholar
Mason, GJ and Latham, NR 2004 Can't stop won't stop: is stereotypy a reliable animal welfare indicator? Animal Welfare 13: S57–S70Google Scholar
Mellor, DJ 2015 Positive animal welfare states and reference standards for welfare assessment. New Zealand Veterinary Journal 63: 17–23. https://doi.org/10.1080/00480169.2014.926802CrossRefGoogle ScholarPubMed
Mellor, DJ 2016 Updating animal welfare thinking: Moving beyond the ‘Five Freedoms’ towards ‘a life worth living’. Animals 6: 21. https://doi.org/10.3390/ani6030021CrossRefGoogle Scholar
Mendl, M, Brooks, J, Basse, C, Burman, O, Paul, E, Blackwell, E and Casey, R 2010 Dogs showing separation-related behav-iour exhibit a ‘pessimistic'cognitive bias. Current Biology 20: R839–R840. https://doi.org/10.1016/j.cub.2010.08.030CrossRefGoogle ScholarPubMed
Miller, LJ, Mellen, J, Greer, T and Kuczaj, SA 2011 The effects of education programmes on Atlantic bottlenose dolphin Tursiops truncatus behavior. Animal Welfare 20: 159–172Google Scholar
Miller, LJ, Pisacane, CB and Vicino, GA 2016 Relationship between behavioural diversity and faecal glucocorticoid metabo-lites: a case study with cheetahs Acinonyx jubatus. Animal Welfare 25: 325–329. https://doi.org/10.7120/09627286.25.3.325CrossRefGoogle Scholar
Napolitano, F, Knierim, U, Grass, F and De Rosa, G 2009 Positive indicators of cattle welfare and their applicability to on-farm protocols. Italian Journal of Animal Science 8: 355–365. https://doi.org/10.4081/ijas.2009.s1.355CrossRefGoogle Scholar
Neal Webb, SJ, Hau, J and Schapiro, SJ 2018 Captive chim-panzee (Pan troglodytes) behavior as a function of space per animal and enclosure type. American Journal of Primatology 80: e22749. https://doi.org/10.1002/ajp.22749CrossRefGoogle ScholarPubMed
Pomerantz, O, Terkel, J, Suomi, SJ and Paukner, A 2012 Stereotypic head twirls, but not pacing, are related to a ‘pes-simistic’-like judgment bias among captive tufted capuchins (Cebus apella). Animal Cognition 15: 689–698. https://doi.org/10.1007/s10071-012-0497-7CrossRefGoogle Scholar
Rabin, LA 2003 Maintaining behavioural diversity in captivity for con-servation: natural behaviour management. Animal Welfare 12: 85–94Google Scholar
Razal, CB, Bryant, J and Miller, LJ 2017 Monitoring the behav-ioral and adrenal activity of giraffe Giraffa camelopardalis to assess welfare during seasonal housing changes. Animal Behavior and Cognition 4: 154–168. https://doi.org/10.12966/abc.03.05.2017CrossRefGoogle Scholar
Rygula, R, Pluta, H and Popik, P 2012 Laughing rats are opti-mistic. PLOS One 7: e51959. https://doi.org/10.1371/journal.pone.0051959CrossRefGoogle Scholar
Shannon, C and Weaver, W 1949 The Mathematical Study of Communication. University of Illinois Press: Urbana, IL, USA.Google Scholar
Shannon, CE 1948 A mathematical theory of communication. Bell System Technical Journal 27: 379–423. https://doi.org/10.1002/j.1538-7305.1948.tb01338.xCrossRefGoogle Scholar
Shepherdson, DJ, Carlstead, K, Mellen, JD and Seidensticker, J 1993 The influence of food presentation on the behavior of small cats in confined environments. Zoo Biology 12:203–216. https://doi.org/10.1002/zoo.1430120206CrossRefGoogle Scholar
Stolba, A, Baker, N and Wood-Gush, DGM 1983 The charac-terisation of stereotyped behaviour in stalled sows by informational redundancy. Behaviour 87: 157–182. https://doi.org/10.1163/156853983X00417CrossRefGoogle Scholar
Tannenbaum, J 1991 Ethics and animal welfare: The inextrica-ble connection. Journal of the American Veterinary Medical Association 198: 1360–1376Google ScholarPubMed
Veasey, JS, Waran, NK and Young, RJ 1996 On comparing the behaviour of zoo housed animals with wild conspecifics as a wel-fare indicator. Animal Welfare 5: 139–153Google Scholar
Vickery, S and Mason, G 2004 Stereotypic behavior in Asiatic black and Malayan sun bears. Zoo Biology 23: 409–430. https://doi.org/10.1002/zoo.20027CrossRefGoogle Scholar
Wemelsfelder, F, Haskell, M, Mendl, MT, Calvert, S and Lawrence, AB 2000 Diversity of behaviour during novel object tests is reduced in pigs housed in substrate-impover-ished conditions. Animal Behaviour 60: 385–394. https://doi.org/10.1006/anbe.2000.1466CrossRefGoogle ScholarPubMed
Wittig, RM, Crockford, C, Deschner, T, Langergraber, KE, Ziegler, TE and Zuberbühler, K 2014 Food sharing is linked to urinary oxytocin levels and bonding in related and unrelated wild chimpanzees. Proceedings of the Royal Society, Series B 281: 20133096. https://doi.org/10.1098/rspb.2013.3096Google ScholarPubMed