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Redefining human-animal relationships: an evaluation of methods to allow their empirical measurement in zoos

Published online by Cambridge University Press:  01 January 2023

F Patel ,
K Whitehouse-Tedd  and
SJ Ward
F Patel
Affiliation:
School of Animal, Rural and Environmental Sciences, Nottingham Trent University, Southwell NG25 0QF, UK
K Whitehouse-Tedd
Affiliation:
School of Animal, Rural and Environmental Sciences, Nottingham Trent University, Southwell NG25 0QF, UK
SJ Ward*
Affiliation:
School of Animal, Rural and Environmental Sciences, Nottingham Trent University, Southwell NG25 0QF, UK
*
* Contact for correspondence: samantha.ward@ntu.ac.uk
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Abstract

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Scientific studies of human-animal interactions (HAIs) and how these develop into human-animal relationships (HARs) now represent some of the most significant contributions to animal welfare science. However, due to the current definition of HAR, studies have only been able to measure HAIs and infer its impact on HARs and animal welfare. Here, we redefine HARs as a series of repeated HAIs between two individuals known to each other, the nature of which is influenced by their historical HAIs and where consideration to the content, quality and the pattern of the interactions is also vital. With a new definition, it is now feasible to empirically measure HARs, however, first, it is important to evaluate current methods utilised in animal industries to allow standardisation across HAR research in zoos. Here, we review the current methods that have been used to assess HAIs in animals and determine their overall suitability for measuring HARs and their use in a zoo environment. Literature searches were conducted using the search terms ‘human-animal’ AND ‘interaction’, ‘human-animal’ AND ‘relationship’, ‘human-animal’ AND ‘bond’. Subsequently, ‘zoo’, ‘companion’, ‘agriculture’, ‘laboratory’ and ‘wild’ were added to each combination yielding five potential methods to evaluate. These methods were assessed according to a panel of indicators including reliability, robustness, practical application and feasibility for use in a zoo environment. Results indicated that the methods utilising ‘latency’, ‘qualitative behaviour assessment’ and the ‘voluntary approach test’ were potentially viable to assess HARs in a zoo environment and could subsequently contribute to the assessment of welfare implications of these HARs for the animals involved. These methods now require empirical testing and comparisons within a zoo environment.

Keywords

animal welfarebehaviourhuman-animal-interactionshuman-animal-relationshipsmethodzoo
Type
Articles
Information
Animal Welfare , Volume 28 , Issue 3 , August 2019 , pp. 247 - 259
Copyright
© 2019 Universities Federation for Animal Welfare

References

Baird, BA, Kuhar, CW, Lukas, KE, Amendolaginea, LA, Fuller, GA, Nemet, J, Willis, MA and Schooka, MW 2016 Program animal welfare: Using behavioral and physiological meas-ures to assess the well-being of animals used for education pro-grams in zoos. Applied Animal Welfare Science 176: 150–162. https://doi.org/10.1016/j.applanim.2015.12.004CrossRefGoogle Scholar
Baker, KC 2004 Benefits of positive human interaction for social-ly housed chimpanzees. Animal Welfare 13(2): 23910.1017/S0962728600026981CrossRefGoogle Scholar
Barongi, R, Fisken, FA, Parker, M and Gusset, M 2015 Committing to conservation: the world zoo and aquarium conservation strategy. WAZA Executive Office: Gland, SwitzerlandGoogle Scholar
Battini, M, Andreoli, E, Barbieri, S and Mattiello, S 2011 Long-term stability of avoidance distance tests for on-farm assess-ment of dairy cow relationship to humans in alpine traditional hus-bandry systems. Applied Animal Behaviour Science 135(4): 267–270. https://doi.org/10.1016/j.applanim.2011.10.013CrossRefGoogle Scholar
Battini, M, Barbieri, S, Waiblinger, S and Mattiello, S 2016 Validity and feasibility of Human-Animal Relationship tests for on-farm welfare assessment in dairy goats. Applied Animal Behaviour Science 178: 32–39. https://doi.org/10.1016/j.applanim.2016.03.012CrossRefGoogle Scholar
Boissy, A and Bouissou, MF 1988 Effects of early handling on heifers’ subsequent reactivity to humans and to unfamiliar situations, Applied Animal Behaviour Science 22: 259–273. https://doi.org/10.1016/0168-1591(88)90051-2CrossRefGoogle Scholar
Brajon, S, Laforest, JP, Bergeron, R, Tallet, C and Devillers, N 2015 The perception of humans by piglets: recognition of familiar handlers and generalisation to unfamiliar humans. Animal Cognition 18(6): 1299–1316. https://doi.org/10.1007/s10071-015-0900-2CrossRefGoogle ScholarPubMed
Breuer, K, Hemsworth, PH and Coleman, GJ 2003 The effect of positive or negative handling on the behavioural and physiolog-ical responses of nonlactating heifers. Applied Animal Behaviour Science 84: 3–22. https://doi.org/10.1016/S0168-1591(03)00146-1CrossRefGoogle Scholar
Burrow, HM and Corbet, NJ 2000 Genetic and environmental factors affecting temperament of zebu and zebu-derived beef cat-tle grazed at pasture in the tropics. Australian Journal of Agricultural Research 55: 155–162. https://doi.org/10.1071/AR99053CrossRefGoogle Scholar
Carlstead, K 2009 A comparative approach to the study of keep-er-animal relationships in the Zoo. Zoo Biology 28: 589–608. https://doi.org/10.1002/zoo.20289Google Scholar
Carlstead, K, Fraser, J, Bennett, C and Kleiman, DG 1999b Black rhinoceros (Diceros bicornis) in US Zoos: II Behavior, breeding success, and mortality in relation to housing facilities. Zoo Biology 18(1): 35–52. https://doi.org/10.1002/(SICI)1098-2361(1999)18:1<35::AID-ZOO5>3.0.CO;2-L3.0.CO;2-L>CrossRefGoogle Scholar
Carlstead, K, Mellen, J and Kleiman, DG 1999a Black rhinoc-eros (Diceros bicornis) in US zoos: I Individual behavior profiles and their relationship to breeding success. Zoo Biology 18: 17–34. https://doi.org/10.1002/(SICI)1098-2361(1999)18:1<17::AID-ZOO4>3.0.CO;2-K Carlstead, K, Paris, S and Brown, JL 2019 Good keeper-ele-phant relationships in North American zoos are mutually benefi-cial to welfare. Applied Animal Behaviour Science 211: 103–111. https://doi.org/10.1016/j.applanim.2018.11.0033.0.CO;2-K>CrossRefGoogle Scholar
Caroprese, M, Napolitano, F, Boivin, X, Albenzio, M, Annicchiarico, G and Sevi, A 2012 Development of affinity to the stockperson in lambs from two breeds. Physiology & Behavior 105(2): 251–256. https://doi.org/10.1016/j.physbeh.2011.08.027CrossRefGoogle Scholar
Carrasco, L, Colell, M, Calvo, M, Abello, MT, Velasco, M and Posada, S 2009 Benefits of training/playing therapy in a group of captive lowland gorillas (Gorilla gorilla gorilla). Animal Welfare 18: 9–1910.1017/S0962728600000026CrossRefGoogle Scholar
Chamove, AS, Hosey, GR and Schaetzel, P 1988 Visitors excite primates in zoos. Zoo Biology 7: 359–369. https://doi.org/10.1002/zoo.1430070407CrossRefGoogle Scholar
Chelluri, GI, Ross, SR and Wagner, KE 2013 Behavioral cor-relates and welfare implications of informal interactions between caretakers and zoo-housed chimpanzees and gorillas. Applied Animal behaviour Science 147(3-4): 306–315. https://doi.org/10.1016/j.applanim.2012.06.008CrossRefGoogle Scholar
Clarke, T, Pluske, JR and Fleming, PA 2016 Are observer ratings influenced by prescription? A comparison of Free Choice Profiling and Fixed List methods of Qualitative Behavioural Assessment. Applied Animal Behaviour Science 177: 77–83. https://doi.org/10.1016/j.applanim.2016.01.022CrossRefGoogle Scholar
Collins, CK and Marples, NM 2016 The effects of zoo visitors on a group of Western lowland gorillas (Gorilla gorilla gorilla) before and after the birth of an infant at Dublin Zoo. International Zoo Yearbook 50(1): 183–192. https://doi.org/10.1111/izy.12111CrossRefGoogle Scholar
Dalla Costa, E, Dai, F, Murray, LAM, Guazzetti, S, Canali, E and Minero, M 2015 A study on validity and reliability of on-farm tests to measure human–animal relationship in horses and don-keys. Applied Animal Behaviour Science 163: 110–121. https://doi.org/10.1016/j.applanim.2014.12.007CrossRefGoogle Scholar
de Oliveira, D, da Costa, MJP, Zupan, M, Rehn, T and Keeling, LJ 2015 Early human handling in non-weaned piglets: Effects on behaviour and body weight. Applied Animal Behaviour Science 164: 56–63. https://doi.org/10.1016/j.applanim.2015.01.002CrossRefGoogle Scholar
de Passillé, AM and Rushen, J 2005 Can we measure human-animal interactions in on-farm animal welfare assessment? Some unresolved issues. Applied Animal Behaviour Science 92: 193–209. https://doi.org/10.1016/j.applanim.2005.05.006CrossRefGoogle Scholar
Ebinghaus, A, Ivemeyer, S, Lauks, V, Santos, L and Brugemann, K 2017 How to measure dairy cows’ responsive-ness towards humans in breeding and welfare assessments? A comparison of selected behavioural measures and existing breeding traits. Applied Animal Behaviour Science 196: 22–29. https://doi.org/10.1016/j.applanim.2017.07.006CrossRefGoogle Scholar
Ellingsen, K, Coleman, GJ, Lund, V and Mejdell, CM 2014 Using qualitative behaviour assessment to explore the link between stockperson behaviour and dairy calf behaviour. Applied Animal Behaviour Science 153: 10–17. https://doi.org/10.1016/j.applanim.2014.01.011CrossRefGoogle Scholar
Ellingsen, K, Zanella, AJ, Bjerkås, E and Indrebø, A 2010 The relationship between empathy, perception of pain and attitudes toward pets among Norwegian dog owners. Anthrozoös 23(3): 231–243. https://doi.org/10.2752/175303710X12750451258931CrossRefGoogle Scholar
Estep, DQ and Hetts, S 1992 Interactions, relationships and bonds: the conceptual basis for scientist-animal relations. In: Davis, H and Balfour, AD (eds) The Inevitable Bond: Examining Scientist-Animal Interactions pp 6–26. CAB International: Cambridge, UKGoogle Scholar
Fravel, L 2003 Critics question zoos’ commitment to conservation. National Geographic News. http://news.nationalg eographic.com/news/2003/11/1113_031113_zoorole.htmlGoogle Scholar
Gartner, MC and Powel, D 2011 Personality assessment in snow leopards (Uncia uncia). Zoo Biology 29: 1–15Google Scholar
Heidenreich, B 2007 An introduction to positive reinforcement training and its benefits. Journal of Exotic Pet Care Medicine 16(1): 19–23. https://doi.org/10.1053/j.jepm.2006.11.005CrossRefGoogle Scholar
Hemsworth, PH, Barnett, JL and Coleman, GJ 1993 The human-animal relationship in agriculture and its consequences for the animal. Animal Welfare 2(1): 33–5110.1017/S096272860001544XCrossRefGoogle Scholar
Hemsworth, PH and Coleman, GJ 1998 Human-Livestock Interactions. CABI: Wallingford, UKGoogle Scholar
Hinde, RA 1976 Interactions, relationships and social structure. Man 11(1): 1–17. https://doi.org/10.2307/2800384CrossRefGoogle Scholar
Hosey, G 2008 A preliminary model of human-animal relation-ships in the zoo. Applied Animal Behaviour Science 109(2): 105–127. https://doi.org/10.1016/j.applanim.2007.04.013CrossRefGoogle Scholar
Hosey, G and Melfi, V 2014 Human-animal interactions, relationships and bonds: A review and analysis of the literature. International Journal of Comparative Psychology 27(1): 117–14210.46867/ijcp.2014.27.01.01CrossRefGoogle Scholar
Jezierski, T, Jaworski, Z and Gorecka, A 1999 Effects of han-dling on behaviour and heart rate in Konik horses: Comparison of stable and forest reared youngstock. Applied Animal Behaviour Science 62(1): 1–11. https://doi.org/10.1016/S0168-1591(98)00209-3CrossRefGoogle Scholar
Jones, RB 1997 Fear and distress. In: Appleby, MC and Hughes, BO (eds) Animal Welfare pp 75–87. CAB International: Wallingford, UKGoogle Scholar
Keeling, LJ 1995 Spacing behaviour and an ethological approach to assessing optimal space allocations for laying hens. Applied Animal Behaviour Science 44: 71–186. https://doi.org/10.1016/0168-1591(95)00612-VCrossRefGoogle Scholar
Korte, SM, Ruesink, W and Blokhuis, HJ 1999 Heart rate vari-ability during manual restraint in chicks from high and low feath-er pecking lines of laying hens. Physiology and Behaviour 65: 649–652. https://doi.org/10.1016/S0031-9384(98)00206-6CrossRefGoogle Scholar
Lensink, BJ, Raussi, S, Boivin, X, Pyykkönen, M and Veissier, I 2001 Reactions of calves to handling depend on housing condition and previous experience with humans. Applied Animal Behaviour Science 70(3): 187–199. https://doi.org/10.1016/S0168-1591(00)00152-0CrossRefGoogle ScholarPubMed
Marchant, JN, Burfoot, A, Corning, S and Broom, DM 1997 The ‘human approach test’: a test of fearfulness or investigatory behaviour. Proceedings of the 31st International Congress of the International Society for Applied Ethology pp 182. 13-16 August 1997, Prague, Czech RepublicGoogle Scholar
Marinelli, L, Adamelli, S, Normando, S and Bono, G 2007 Quality of life of the pet dog: Influence of owner and dog's char-acteristics. Applied Animal Behaviour Science 108(1): 143–156. https://doi.org/10.1016/j.applanim.2006.11.018CrossRefGoogle Scholar
Martin, RA and Melfi, V 2016 A comparison of zoo animal behavior in the presence of familiar and unfamiliar people. Journal of Applied Animal Welfare Science: 19(3): 234–244. https://doi.org/10.1080/10888705.2015.1129907CrossRefGoogle ScholarPubMed
McBride, G, James, JW and Soffner, RN 1963 Social forces determining spacing and head orientation in a flock of domestic hens. Nature 197: 1272–1273. https://doi.org/10.1038/1971272a0CrossRefGoogle Scholar
McMillan, FD 2000 Quality of life in animals. Journal of American Veterinary Medicine Association 216: 1904–1910. https://doi.org/10.2460/javma.2000.216.1904CrossRefGoogle ScholarPubMed
Meehan, CL, Mench, JA, Carlstead, K and Hogan, JN 2016 Determining connections between the daily lives of zoo elephants and their welfare: an epidemiological approach. PLoS ONE 11(7): e0158124. https://doi.org/10.1371/journal.pone.0158124CrossRefGoogle ScholarPubMed
Mellen, JD 1991 Factors influencing reproductive success in small captive exotic felids (Felis spp): a multiple regression analysis. Zoo Biology 10(2): 95–110. https://doi.org/10.1002/zoo.1430100202CrossRefGoogle Scholar
Morton, DB 2000 A systematic approach for establishing humane endpoints. Ilar Journal 41(2): 80–86. https://doi.org/10.1093/ilar.41.2.80CrossRefGoogle ScholarPubMed
Napolitano, F, De Rosa, G, Braghieri, A, Grasso, F, Bordi, A and Wemelsfelder, F 2008 The qualitative assessment of responsiveness to environmental challenges in horses and ponies. Applied Animal Behaviour Science 109: 342. https://doi.org/10.1016/j.applanim.2007.03.009CrossRefGoogle Scholar
Napolitano, F, De Rosa, G, Grasso, F and Wemelsfelder, F 2012 Qualitative behaviour assessment of dairy buffaloes (Bubalus bubalis). Applied Animal Behaviour Science 141(3): 91–100. https://doi.org/10.1016/j.applanim.2012.08.002CrossRefGoogle Scholar
O’Haire, M 2010 Companion animals and human health: Benefits, challenges, and the road ahead. Journal of Veterinary Behavior 5:226–234. https://doi.org/10.1016/j.jveb.2010.02.002CrossRefGoogle Scholar
Pizzutto, CS, Nichi, M, Correa, SR, Ades, C and Guimaraes, MABV 2007 Reduction of abnormal behavior in a gorilla (Gorilla gorilla gorilla) through social interaction with a human being. Laboratory Primate Newsletter 46(3): 6–9Google Scholar
Podberscek, A, Blackshaw, J and Beattie, A 1991 The effects of repeated handling by familiar and unfamiliar people on rabbits in individual cages and group pens. Applied Animal Behaviour Science 28: 365–373. https://doi.org/10.1016/0168-1591(91)90168-WCrossRefGoogle Scholar
Renner, MJ and Kelly, AL 2006 Behavioral decisions for managing social distance and aggression in captive polar bears (Ursus maritimus). Journal of Applied Animal Welfare Science 9(3): 233–239. https://doi.org/10.1207/s15327604jaws0903_5CrossRefGoogle ScholarPubMed
Rousing, T and Waiblinger, S 2004 Evaluation of on-farm methods for testing the human-animal relationship in dairy herds with cubicle loose housing systems: test-retest and inter-observ-er reliability and consistency to familiarity of test person. Applied Animal Behaviour Science 85: 215–231. https://doi.org/10.1016/j.applanim.2003.09.014CrossRefGoogle Scholar
Rushen, J, Taylor, AA and de Passillé, AM 1999 Domestic ani-mals’ fear of humans and its effect on their welfare. Applied Animal Behaviour Science 65(3): 285–303. https://doi.org/10.1016/S0168-1591(99)00089-1CrossRefGoogle Scholar
Rutherford, KMD, Donald, RD, Lawrence, AB and Wemelsfelder, F 2012 Qualitative Behavioural Assessment of emotionality in pigs. Applied Animal Behaviour Science 139: 218–224. https://doi.org/10.1016/j.applanim.2012.04.004CrossRefGoogle ScholarPubMed
Sherwen, SL, Magrath, MJL, Butler, KL and Hemsworth, PH 2015 Little penguins, Eudyptula minor show increased avoid-ance, aggression and vigilance in response to zoo visitors. Applied Animal Behaviour Science 168: 71–76. https://doi.org/10.1016/j.applanim.2015.04.007CrossRefGoogle Scholar
Sherwen, SL, Magrath, MJL, Butler, KL, Phillips, CJC and Hemsworth, PH 2014 A multi-enclosure study investigating the behavioural response of meerkats to zoo visitors. Applied Animal Behaviour Science 156: 70–77. https://doi.org/10.1016/j.applan-im.2014.04.012CrossRefGoogle Scholar
Smith, JJ 2014 Human-animal relationships in zoo-housed orang-utans (P. abelii) and gorillas (G.g. gorilla): The effects of familiarity. American Journal of Primatology 76 (10): 942–955. https://doi.org/10.1002/ajp.22280CrossRefGoogle Scholar
Søndergaard, E and Halekoh, U 2003 Young horses’ reactions to humans in relation to handling and social environment. Applied Animal Behaviour Science 84: 265–280. https://doi.org/10.1016/j.applanim.2003.08.011CrossRefGoogle Scholar
Species360 2016 Species360.orgGoogle Scholar
Stricklin, WR, Graves, HB and Wilson, L 1979 Some theoret-ical and observed relationships of fixed and portable spacing behaviours of animals. Applied Animal Ethology 5: 201–214. https://doi.org/10.1016/0304-3762(79)90056-7CrossRefGoogle Scholar
Thompson, VD 1989 Behavioural response of 12 ungulate species in captivity to the presence of humans. Zoo Biology 8: 275–297. https://doi.org/10.1002/zoo.1430080308CrossRefGoogle Scholar
Vitztum, C and Urbanik, J 2016 Assessing the dog: A theoreti-cal analysis of the companion animal's actions in human-animal interactions. Society and Animals 24(2): 172–185. https://doi.org/10.1163/15685306-12341399CrossRefGoogle Scholar
Waiblinger, S, Boivin, X, Pederson, V, Tosi, M, Janczak, AM, Visser, EK and Jones, RB 2006 Assessing the human-animal relationship in farmed species: A critical review. Applied Animal Behaviour Science 101: 185–242. https://doi.org/10.1016/j.applan-im.2006.02.001CrossRefGoogle Scholar
Waiblinger, S, Menke, C and Fölsch, DW 2003 Influences on the avoidance and approach behaviour of dairy cows towards humans on 35 farms. Applied Animal Behaviour Science 84(1): 23–39. https://doi.org/10.1016/S0168-1591(03)00148-5CrossRefGoogle Scholar
Waiblinger, S, Menke, C, Korff, J and Bucher, A 2004 Previous handling and gentle interactions affect behaviour and heart rate of dairy cows during a veterinary procedure. Applied Animal Behaviour Science 85(1): 31–42. https://doi.org/10.1016/j.applanim.2003.07.002CrossRefGoogle Scholar
Walsh, F 2009 Human-animal bonds I: The relational significance of companion animals. Family Process 48(4): 462–480. https://doi.org/10.1111/j.1545-5300.2009.01296.xCrossRefGoogle ScholarPubMed
Ward, SJ and Melfi, V 2013 The implications of husbandry training on zoo animal response rates. Applied Animal Behaviour Science 147(1): 179–185. https://doi.org/10.1016/j.applanim.2013.05.008CrossRefGoogle Scholar
Ward, SJ and Melfi, V 2015 Keeper-animal interactions: Differences between the behaviour of zoo animals affect stock-manship. PLOS One 10(10): e0140237. https://doi.org/10.1371/journal.pone.0140237CrossRefGoogle Scholar
Wemelsfelder, F, Hunter, EA, Mendl, MT and Lawrence, AB 2000 The spontaneous qualitative assessment of behavioural expressions in pigs: first explorations of a novel methodology for integrative animal welfare measurement. Applied Animal Behaviour Science 67: 193–215. https://doi.org/10.1016/S0168-1591(99)00093-3CrossRefGoogle ScholarPubMed
Wemelsfelder, F, Hunter, TEA, Mendl, MT and Lawrence, AB 2001 Assessing the ‘whole animal’: a free choice profiling approach. Animal Behaviour 62: 209–220. https://doi.org/10.1006/anbe.2001.1741CrossRefGoogle Scholar
Wemelsfelder, F and Lawrence, AB 2001 Qualitative assess-ment of animal behaviour as an on-farm welfare-monitoring tool. Acta Agriculturae Scandinavica Section A51: 21–22. https://doi.org/10.1080/090647001316923018CrossRefGoogle Scholar
Wemelsfelder, F, Millard, F, Rosa, G and Napolitano, F 2009 Qualitative behaviour assessment. In: Forkman, B, and Keeling, L (eds) Assessment of Animal Welfare Measures for Dairy Cattle, Beef Bulls and Veal Calves pp 21. Cardiff University: Cardiff, UKGoogle Scholar
Wielebnowski, NC 1999 Behavioral differences as predictors of breeding status in captive cheetahs. Zoo Biology 18(4): 335–349. https://doi.org/10.1002/(SICI)1098-2361(1999)18:4<335::AID-ZOO8>3.0.CO;2-X3.0.CO;2-X>CrossRefGoogle Scholar
Wielebnowski, NC, Fletchall, N, Carlstead, K, Busso, JM and Brown, JL 2002 Non-inasive assessment of adrenal activity associated with husbandry and behavioural factors in the north american clouded leopard population. Zoo Biology 21: 77–98. https://doi.org/10.1002/zoo.10005CrossRefGoogle Scholar
Windschnurer, I, Boivin, and Waiblinger, S 2009 Reliability of an avoidance distance test for the assessment of animals’ responsive-ness to humans and a preliminary investigation of its association with farmers attitudes on bull fattening farms. Applied Animal Behaviour Science 117: 117–127. https://doi.org/10.1016/j.applanim.2008.12.013CrossRefGoogle Scholar
Zentall, TR 2006 Imitation: Definitions, evidence, and mechanisms. Animal Cognition 9: 335–353. https://doi.org/10.1007/s10071-006-0039-2CrossRefGoogle ScholarPubMed
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