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8 - Measuring Welfare through Behavioral Observation and Adjusting It with Dynamic Environments

from Part II - Captive Care and Management

Published online by Cambridge University Press:  21 December 2018

By
Jason V. Watters ,
Bethany L. Krebs  and
Eridia Pacheco
Edited by
Allison B. Kaufman ,
Meredith J. Bashaw  and
Terry L. Maple
Allison B. Kaufman
Affiliation:
University of Connecticut
Meredith J. Bashaw
Affiliation:
Franklin and Marshall College, Pennsylvania
Terry L. Maple
Affiliation:
Jacksonville Zoo and Gardens
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Summary

Recent years have seen accrediting organizations and their members calling for programs that employ techniques to assess and ensure the welfare of animals living in zoos. Watching animal behavior remains a commonly used approach to assessing animal welfare in captive settings. The two most widely utilized approaches to behavioral assessments of animal welfare are measures of animals’ overall behavioral repertoires and measuring the presence, absence, or intensity of specific indicator behaviors. Here, we discuss the benefits and drawbacks of different approaches to behavioral assessments of animal welfare and suggest several new directions for such assessments in zoo settings. We also discuss the influence of environmental enrichment on animal welfare and methods for best utilizing dynamic enrichments to improve animal welfare.
Type
Chapter
Information
Scientific Foundations of Zoos and Aquariums
Their Role in Conservation and Research
 , pp. 212 - 240
Publisher: Cambridge University Press
Print publication year: 2019

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References

Balsam, P., Sanchez-Castillo, H., Taylor, K., Van Volkinburg, H., & Ward, R. D. (2009). Timing and anticipation: conceptual and methodological approaches. European Journal of Neuroscience, 30(9), 1749–1755.Google Scholar
Bassett, L., & Buchanan-Smith, H. M. (2007). Effects of predictability on the welfare of captive animals. Applied Animal Behaviour Science, 102(3–4), 223–245.CrossRefGoogle Scholar
Bateson, M., & Matheson, S. M. (2007). Performance on a categorisation task suggests that removal of environmental enrichment induces “pessimism” in captive European starlings (Sturnus vulgaris). Animal Welfare, 16(2), 33–36.CrossRefGoogle Scholar
Bethell, E. J. (2015). A “how-to” guide for designing judgment bias studies to assess captive animal welfare. Journal of Applied Animal Welfare Science, 18, S18–S42.Google Scholar
Bloomfield, R. C., Gillespie, G. R., Kerswell, K. J., Butler, K. L., & Hemsworth, P. H. (2015). Effect of partial covering of the visitor viewing area window on positioning and orientation of zoo orangutans: A preference test. Zoo Biology, 34(3), 223–229.CrossRefGoogle ScholarPubMed
Bloomsmith, M. A., & Lambeth, S. P. (1995). Effects of predictable versus unpredictable feeding schedules on chimpanzee behavior. Applied Animal Behaviour Science, 44(1), 65–74.Google Scholar
Boissy, A., & Erhard, H. W. (2014). How Studying Interactions between Animal Emotions, Cognition, and Personality Can Contribute to Improve Farm Animal Welfare. San Diego, CA: Elsevier Academic Press Inc.Google Scholar
Boissy, A., & Lee, C. (2014). How assessing relationships between emotions and cognition can improve farm animal welfare. Revue Scientifique et Technique – Office International Des Epizooties, 33(1), 103–110.Google Scholar
Brenes, J. C., & Schwarting, R. K. W. (2015). Individual differences in anticipatory activity to food rewards predict cue-induced appetitive 50-kHz calls in rats. Physiology & Behavior, 149, 107–118.Google Scholar
Carlstead, K., Mellen, J., & Kleiman, D. G. (1999). Black rhinoceros (Diceros bicornis) in U.S. zoos: I. Individual behavior profiles and their relationship to breeding success. Zoo Biology, 18(1), 17–34.Google Scholar
Carlstead, K., & Shepherdson, D. (2000). Alleviating stress in zoo animals with environmental enrichment. In Mench, G. P. M. J. A. (Ed.), The Biology of Animal Stress: Basic Principles and Implications for Animal Welfare (pp. 337–349). New York, NY: CABI Publishing.CrossRefGoogle Scholar
Chamove, A. S. (1989). Environmental enrichment: A review. Animal Technology: Journal of the Institute of Animal Technology, 40(3), 155–178.Google Scholar
Chelluri, G. I., Ross, S. R., & Wagner, K. E. (2013). Behavioral correlates and welfare implications of informal interactions between caretakers and zoo-housed chimpanzees and gorillas. Applied Animal Behaviour Science, 147(3–4), 306–315.Google Scholar
Chittka, L., & Jensen, K. (2011). Animal cognition: Concepts from apes to bees. Current Biology, 21(3), R116–R119.Google Scholar
Chitty, J. (2003). Feather plucking in psittacine birds 2. Social, environmental and behavioural considerations. In Practice, 25(9), 550.Google Scholar
Clark, F. E. (2011). Great ape cognition and captive care: Can cognitive challenges enhance well-being? Applied Animal Behaviour Science, 135(1), 1–12.Google Scholar
Clark, F. E. (2013). Marine mammal cognition and captive care: A proposal for cognitive enrichment in zoos and aquariums. Journal of Zoo and Aquarium Research, 1(1), 1–6.Google Scholar
Clegg, I., & Delfour, F. (2018). Cognitive judgement bias is associated with frequency of anticipatory behavior in bottlenose dolphins. Zoo Biology, 37(2), 67–73.Google Scholar
Cunningham, C. L., Gremel, C. M., & Groblewski, P. A. (2006). Drug-induced conditioned place preference and aversion in mice. Nature Protocols, 1(4), 1662–1670.Google Scholar
Davidson, A. J., Tataroglu, O., & Menaker, M. (2005). Circadian effects of timed meals (and other rewards). In Young, M. W. (Ed.), Circadian Rhythms (Vol. 393, pp. 509–523). San Diego, CA: Elsevier Academic Press Inc.Google Scholar
Dudink, S., Simonse, H., Marks, I., de Jonge, F. H., & Spruijt, B. M. (2006). Announcing the arrival of enrichment increases play behaviour and reduces weaning-stress-induced behaviours of piglets directly after weaning. Applied Animal Behaviour Science, 101(1–2), 86–101.Google Scholar
Escobar, C., Martinez-Merlos, M. T., Angeles-Castellanos, M., Minana, M. D., & Buijs, R. M. (2007). Unpredictable feeding schedules unmask a system for daily resetting of behavioural and metabolic food entrainment. European Journal of Neuroscience, 26(10), 2804–2814.CrossRefGoogle ScholarPubMed
Fanselow, M. S. (1980). Conditional and unconditional components of post-shock freezing. The Pavlovian Journal of Biological Science: Official Journal of the Pavlovian, 15(4), 177–182.Google Scholar
Franks, B., Champagne, F. A., & Higgins, E. T. (2013). How enrichment affects exploration trade-offs in rats: Implications for welfare and well-being. PLoS ONE, 8(12), e83578.Google Scholar
Garner, J. P., Meehan, C. L., Famula, T. R., & Mench, J. A. (2006). Genetic, environmental, and neighbor effects on the severity of stereotypies and feather picking in orange-winged Amazon parrots (Amazona amazonica): An epidemiological study. Applied Animal Behaviour Science, 96(1), 153–168.Google Scholar
Gottlieb, D. H., Coleman, K., & McCowan, B. (2013). The effects of predictability in daily husbandry routines on captive rhesus macaques (Macaca mulatta). Applied Animal Behaviour Science, 143(2–4), 117–127.Google Scholar
Gottlieb, D. H., Ghirardo, S., Minier, D. E., Sharpe, N., Tatum, L., & McCowan, B. (2011). Efficacy of 3 types of foraging enrichment for rhesus macaques (Macaca mulatta). Journal of the American Association for Laboratory Animal Science, 50(6), 888–894.Google Scholar
Grindlinger, H. M. (1991). Compulsive feather picking in birds. Archives of General Psychiatry, 48(9), 857–857.Google Scholar
Gunn, D., & Morton, D. B. (1995). Inventory of the behaviour of New Zealand white rabbits in laboratory cages. Applied Animal Behaviour Science, 45(3), 277–292.Google Scholar
Hall, L. E., Robinson, S., & Buchanan-Smith, H. M. (2015). Refining dosing by oral gavage in the dog: A protocol to harmonise welfare. Journal of Pharmacological and Toxicological Methods, 72, 35–46.Google Scholar
Harding, E. J., Paul, E. S., & Mendl, M. (2004). Animal behaviour: Cognitive bias and affective state. Nature, 427(6972), 312–312.Google Scholar
Harley, H. E., Fellner, W., & Stamper, M. A. (2010). Cognitive research with dolphins (Tursiops truncatus) at Disney’s The Seas: A program for enrichment, science, education, and conservation. International Journal of Comparative Psychology, 23(3), 331–343.CrossRefGoogle Scholar
Herbert, P. L., & Bard, K. (2000). Orangutan use of vertical space in an innovative habitat. Zoo Biology, 19(4), 239–251.Google Scholar
Herrelko, E. S., Buchanan-Smith, H. M., & Vick, S.-J. (2015). Perception of available space during chimpanzee introductions: Number of accessible areas is more important than enclosure size. Zoo Biology, 34(5), 397–405.Google Scholar
Hill, J. O., Pavlik, E. J., Smith, G. L., Burghardt, G. M., & Coulson, P. B. (1976). Species-characteristic responses to catnip by undomesticated felids. Journal of Chemical Ecology, 2(2), 239–253.Google Scholar
Hughes, B. O., & Duncan, I. J. H. (1988). The notion of ethological “need,” models of motivation and animal welfare. Animal Behaviour, 36(6), 1696–1707.Google Scholar
Imfeld-Mueller, S., & Hillmann, E. (2012). Anticipation of a food ball increases short-term activity levels in growing pigs. Applied Animal Behaviour Science, 137(1–2), 23–29.Google Scholar
Inglis, I. R., Langton, S., Forkman, B., & Lazarus, J. (2001). An information primacy model of exploratory and foraging behaviour. Animal Behaviour, 62(3), 543–557.Google Scholar
Jensen, A. L. M., Delfour, F., & Carter, T. (2013). Anticipatory behavior in captive bottlenose dolphins (Tursiops truncatus): A preliminary study. Zoo Biology, 32(4), 436–444.Google Scholar
Kirkwood, J. K., & Hubrecht, R. (2001). Animal consciousness, cognition and welfare. Animal Welfare, 10(1), 5–17.Google Scholar
Krebs, B. L., & Watters, J. V. (2016). Using technology driven environments to promote animal well-being in zoos. Paper presented at the Human Computer Interactions, San Jose, CA.Google Scholar
Krebs, B. L., & Watters, J. V. (2017). Simple but temporally unpredictable puzzles are cognitive enrichment. Animal Behavior and Cognition, 4(1), 119–134.Google Scholar
Krebs, B. L., Torres, E., Chesney, C., Kantoniemi Moon, V., & Watters, J. V. (2017). Applying behavioral conditioning to identify anticipatory behaviors. Journal of Applied Animal Welfare Science, 20(2), 155–175.Google Scholar
Kuczaj, S., Lacinak, T., Fad, O., Trone, M., Solangi, M., & Ramos, J. (2002). Keeping environmental enrichment enriching. International Journal of Comparative Psychology, 15(2), 127–137.Google Scholar
Laule, G. E. (2003). Positive reinforcement training and environmental enrichment: Enhancing animal well-being. Journal of the American Veterinary Medical Association, 223(7), 969–973.Google Scholar
MacDonald, S. E., & Ritvo, S. (2016). Comparative cognition outside the laboratory. Comparative Cognition & Behavior Reviews, 11, 49–61.CrossRefGoogle Scholar
Makowska, I. J., & Weary, D. M. (2016). Differences in anticipatory behaviour between rats (Rattus norvegicus) housed in standard versus semi-naturalistic laboratory environments. PLoS ONE, 11, e0147595.Google Scholar
Manteuffel, G., Langbein, J., & Puppe, B. (2009a). From operant learning to cognitive enrichment in farm animal housing: bases and applicability. Animal Welfare, 18(1), 87–95.Google Scholar
Manteuffel, G., Langbein, J., & Puppe, B. (2009b). Increasing farm animal welfare by positively motivated instrumental behaviour. Applied Animal Behaviour Science, 118(3–4), 191–198.Google Scholar
Mason, G. J. (1991). Stereotypies: A critical review. Animal Behaviour, 41(6), 1015–1037.Google Scholar
Meehan, C. L., & Mench, J. A. (2007). The challenge of challenge: Can problem solving opportunities enhance animal welfare? Applied Animal Behaviour Science, 102(3–4), 246–261.Google Scholar
Meehan, C. L., Millam, J. R., & Mench, J. A. (2003). Foraging opportunity and increased physical complexity both prevent and reduce psychogenic feather picking by young Amazon parrots. Applied Animal Behaviour Science, 80(1), 71–85.Google Scholar
Mellor, D. J., Hunt, S., & Gusset, M. (Eds.) (2015). Caring for Wildlife: The World Zoo and Aquarium Animal Welfare Strategy. Gland: WAZA Executive Office.Google Scholar
Mench, J. A. (1998). Environmental enrichment and the importance of exploratory behavior. In Shepherdson, D. J., Mellen, J. D., & Hutchins, M. (Eds.), Second Nature: Environmental Enrichment for Captive Animals (pp. 30–46). Washington, DC: Smithsonian Institution Press.Google Scholar
Mendl, M., Burman, O. H. P., Parker, R. M. A., & Paul, E. S. (2009). Cognitive bias as an indicator of animal emotion and welfare: Emerging evidence and underlying mechanisms. Applied Animal Behaviour Science, 118(3), 161–181.Google Scholar
Mistlberger, R. E. (1994). Circadian food-anticipatory activity: Formal models and physiological mechanisms. Neuroscience & Biobehavioral Reviews, 18(2), 171–195.Google Scholar
Mistlberger, R. E. (2009). Food-anticipatory circadian rhythms: Concepts and methods. European Journal of Neuroscience, 30(9), 1718–1729.Google Scholar
Morimura, N. (2006). Cognitive enrichment in chimpanzees: An approach of welfare entailing an animal’s entire resources. In Matsuzawa, T., Tomonaga, M., & Tanaka, M. (Eds.), Cognitive Development in Chimpanzees (pp. 368–391). Tokyo: Springer Tokyo.Google Scholar
Newberry, R. C. (1995). Environmental enrichment: Increasing the biological relevance of captive environments. Applied Animal Behaviour Science, 44(2), 229–243.Google Scholar
Novak, M. A., Kinsey, J. H., Jorgensen, M. J., & Hazen, T. J. (1998). Effects of puzzle feeders on pathological behavior in individually housed rhesus monkeys. American Journal of Primatology, 46(3), 213–227.Google Scholar
Owen, M. A., Swaisgood, R. R., Czekala, N. M., & Lindburg, D. G. (2005). Enclosure choice and well-being in giant pandas: Is it all about control? Zoo Biology, 24(5), 475–481.Google Scholar
Panksepp, J. (2005). Affective consciousness: Core emotional feelings in animals and humans. Consciousness and Cognition, 14(1), 30–80.Google Scholar
Poole, T. B. (1987). Social behavior of a group of orangutans (Pongo pygmaeus) on an artificial island in Singapore Zoological Gardens. Zoo Biology, 6(4), 315–330.Google Scholar
Puppe, B., Ernst, K., Schön, P. C., & Manteuffel, G. (2007). Cognitive enrichment affects behavioural reactivity in domestic pigs. Applied Animal Behaviour Science, 105(1–3), 75–86.Google Scholar
Renner, M. J., & Rosenzweig, M. R. (1986). Object interactions in juvenile rats (Rattus norvegicus): Effects of different experiential histories. Journal of Comparative Psychology, 100(3), 229–236.Google Scholar
Richter, S. H., Schick, A., Hoyer, C., Lankisch, K., Gass, P., & Vollmayr, B. (2012). A glass full of optimism: Enrichment effects on cognitive bias in a rat model of depression. Cognitive, Affective, & Behavioral Neuroscience, 12(3), 527–542.Google Scholar
Rimpley, K., & Buchanan-Smith, H. M. (2013). Reliably signalling a startling husbandry event improves welfare of zoo-housed capuchins (Sapajus apella). Applied Animal Behaviour Science, 147(1–2), 205–213.Google Scholar
Ross, S. R. (2006). Issues of choice and control in the behaviour of a pair of captive polar bears (Ursus maritimus). Behavioural Processes, 73(1), 117–120.CrossRefGoogle ScholarPubMed
Rushen, J. (1996). Using aversion learning techniques to assess the mental state, suffering, and welfare of farm animals. Journal of Animal Science, 74(8), 1990–1995.Google Scholar
Sambrook, T. D., & Buchanan-Smith, H. M. (1997). Control and complexity in novel object enrichment. Animal Welfare, 6(3), 207–216.Google Scholar
Shepherdson, D. (1994). The role of environmental enrichment in the captive breeding and reintroduction of endangered species. In Olney, P. J. S., Mace, G. M., & Feistner, A. T. C. (Eds.), Creative Conservation: Interactive management of wild and captive animals (pp. 167–177). Dordrecht: Springer Netherlands.Google Scholar
Shepherdson, D., Lewis, K. D., Carlstead, K., Bauman, J., & Perrin, N. (2013). Individual and environmental factors associated with stereotypic behavior and fecal glucocorticoid metabolite levels in zoo housed polar bears. Applied Animal Behaviour Science, 147(3), 268–277.Google Scholar
Solis-Salazar, T., Martinez-Merlos, M. T., Angeles-Castellanos, M., Mendoza, J., & Escobar, C. (2005). Behavioral and physiological adaptations in rats during food-entrainment. Biological Rhythm Research, 36(1–2), 99–108.Google Scholar
Spruijt, B. M., van den Bos, R., & Pijlman, F. T. A. (2001). A concept of welfare based on reward evaluating mechanisms in the brain: Anticipatory behaviour as an indicator for the state of reward systems. Applied Animal Behaviour Science, 72(2), 145–171.Google Scholar
Stephan, F. K. (2002). The “other” circadian system: Food as a zeitgeber. Journal of Biological Rhythms, 17(4), 284–292.Google Scholar
Swaisgood, R. R., & Shepherdson, D. J. (2005). Scientific approaches to enrichment and stereotypies in zoo animals: what’s been done and where should we go next? Zoo Biology, 24(6), 499–518.Google Scholar
Tarou, L. R., & Bashaw, M. J. (2007). Maximizing the effectiveness of environmental enrichment: Suggestions from the experimental analysis of behavior. Applied Animal Behaviour Science, 102(3–4), 189–204.Google Scholar
Troisi, A. (2002). Displacement activities as a behavioral measure of stress in nonhuman primates and human subjects. Stress, 5(1), 47–54.Google Scholar
Valuska, A. J., Leighty, K. A., Schutz, P. J., Ferrie, G. M., Sky, C. C., & Bettinger, T. L. (2013). The use of visual barriers to reduce aggression among a group of marabou storks (Leptoptilos crumeniferus). Zoo Biology, 32(6), 648–651.Google Scholar
van den Bos, R., Meijer, M. K., van Renselaar, J. P., van der Harst, J. E., & Spruijt, B. M. (2003). Anticipation is differently expressed in rats (Rattus norvegicus) and domestic cats (Felis silvestris catus) in the same Pavlovian conditioning paradigm. Behavioural Brain Research, 141(1), 83–89.Google Scholar
van der Harst, J. E., Fermont, P. C. J., Bilstra, A. E., & Spruijt, B. M. (2003). Access to enriched housing is rewarding to rats as reflected by their anticipatory behaviour. Animal Behaviour, 66, 493–504.Google Scholar
van der Kolk, B. A. (1988). The trauma spectrum: The interaction of biological and social events in the genesis of the trauma response. Journal of Traumatic Stress, 1(3), 273–290.CrossRefGoogle Scholar
van der Kolk, B. A., & Saporta, J. (1991). The biological response to psychic trauma: Mechanisms and treatment of intrusion and numbing. Anxiety Research, 4(3), 199–212.Google Scholar
Watters, J. V. (2009). Toward a predictive theory for environmental enrichment. Zoo Biology, 28(6), 608–622.Google Scholar
Watters, J. V. (2014). Searching for behavioral indicators of welfare in zoos: Uncovering anticipatory behavior. Zoo Biology, 33(4), 251–256.Google Scholar
Watters, J. V., Margulis, S. W., & Atsalis, S. (2009). Behavioral monitoring in zoos and aquariums: A tool for guiding husbandry and directing research. Zoo Biology, 28(1), 35–48.Google Scholar
Watters, J. V., Miller, J. T., & Sullivan, T. J. (2011). Note on optimizing environmental enrichment: A study of fennec fox and zoo guests. Zoo Biology, 30(6), 647–654.CrossRefGoogle ScholarPubMed
Watters, J. V., & Powell, D. M. (2011). Measuring animal personality for use in population management in zoos: Suggested methods and rationale. Zoo Biology, 31(1), 1–12.Google Scholar
Watters, J. V., et al. (2015). Assessing quality of life in geriatric zoo animals. WAZA Magazine, 16, 37–40.Google Scholar
Weiss, S. J. (2007). Neurobiological alterations associated with traumatic stress. Perspectives in Psychiatric Care, 43(3), 114–122.Google Scholar
Wells, D. L. (2009). Sensory stimulation as environmental enrichment for captive animals: A review. Applied Animal Behaviour Science, 118(1–2), 1–11.Google Scholar
Whitham, J. C., & Wielebnowski, N. (2013). New directions for zoo animal welfare science. Applied Animal Behaviour Science, 147(3–4), 247–260.Google Scholar
Wichman, A., Keeling, L. J., & Forkman, B. (2012). Cognitive bias and anticipatory behaviour of laying hens housed in basic and enriched pens. Applied Animal Behaviour Science, 140(1–2), 62–69.Google Scholar
Wojciechowski, S. (2004). Introducing a fourth primate species to an established mixed-species exhibit of African monkeys. Zoo Biology, 23(2), 95–108.Google Scholar
Yeates, J. W., & Main, D. C. (2008). Assessment of positive welfare: A review. The Veterinary Journal, 175(3), 293–300.Google Scholar
Zebunke, M., Puppe, B., & Langbein, J. (2013). Effects of cognitive enrichment on behavioural and physiological reactions of pigs. Physiology & Behavior, 118, 70–79.Google Scholar

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