Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-28T01:58:16.212Z Has data issue: false hasContentIssue false
  • English
  • Français

Applying welfare science to bottlenose dolphins (Tursiops truncatus)

Published online by Cambridge University Press:  01 January 2023

ILK Clegg ,
CE Van Elk  and
F Delfour
ILK Clegg*
Affiliation:
Laboratoire d’Ethologie Expérimentale et Comparée EA4443, Université Paris 13, Villetaneuse, France Equipe Delphinarium, Parc Astérix, BP8, 60128 Plailly, France
CE Van Elk
Affiliation:
Dolfinarium Harderwijk, Strandboulevard 1, 3841 AB Harderwijk, The Netherlands
F Delfour
Affiliation:
Laboratoire d’Ethologie Expérimentale et Comparée EA4443, Université Paris 13, Villetaneuse, France Equipe Delphinarium, Parc Astérix, BP8, 60128 Plailly, France
*
* Contact for correspondence and requests for reprints: [email protected]
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 science is a burgeoning field, but research on cetaceans (whales, dolphins and porpoises) is lacking. Bottlenose dolphins (Tursiops truncatus) are the most well-known and studied cetaceans, particularly in captivity, and thus are used in this review as a model for other cetacean species. Despite the public interest and need for such research, studies specifically investigating dolphin welfare are lacking. This review uses the three broad categories of behaviour, health, and cognition, to discuss how dolphin welfare has been assessed thus far, and could be assessed in future. We present welfare indicators validated in other species that could be applied to dolphins, including innovative measures, such as cognitive appraisal of emotions. We provide a summary of practical recommendations for validating the indicators of bottlenose dolphin welfare. This paper aims to stimulate further research into dolphin welfare which could improve the lives of the animals themselves and ultimately support regulatory decisions. We recommend uniting expertise in cetology and welfare science in order to develop a holistic approach to dolphin welfare assessment.

Keywords

affective statesanimal-based measuresanimal welfarebottlenose dolphinscetaceanswelfare assessment
Type
Articles
Information
Animal Welfare , Volume 26 , Issue 2 , May 2017 , pp. 165 - 176
Copyright
© 2017 Universities Federation for Animal Welfare

References

Atkinson, S, Crocker, D, Houser, D and Mashburn, K 2015 Stress physiology in marine mammals: how well do they fit the terrestrial model? Journal of Comparative Physiology B: 1-24. https://doi.org/10.1007/s00360-015-0901-0CrossRefGoogle Scholar
Barber, JC 2009 Programmatic approaches to assessing and improving animal welfare in zoos and aquariums. Zoo Biology 28:519–530. https://doi.org/10.1002/zoo.20260Google ScholarPubMed
Barnard, S, Pedernera, C, Candeloro, L, Ferri, N, Velarde, A and Dalla Villa, P 2016 Development of a new welfare assess-ment protocol for practical application in long-term dog shelters. The Veterinary Record 178: 18CrossRefGoogle Scholar
Bel'kovich, VM, Ivanova, EE, Kozarovitsky, LB, Novikova, EV and Kharitonov, SP 1991 Dolphin play behavior in the open sea. In: Pryor, K and Norris, KS (eds) Dolphin Societies: Discoveries and Puzzles pp 67–77. University of California Press: London, UKGoogle Scholar
Blois-Heulin, C, Rochais, C, Camus, S, Fureix, C, Lemasson, A, Lunel, C, Bézard, E and Hausberger, M 2015 Animal welfare: Could adult play be a false friend? Animal Behavior and Cognition 2: 156–185CrossRefGoogle Scholar
Blokhuis, HJ 2008 International cooperation in animal welfare: the Welfare Quality®project. Acta Veterinaria Scandinavica 50: S10. https://doi.org/10.1186/1751-0147-50-S1-S10CrossRefGoogle Scholar
Boissy, A, Manteuffel, G, Jensen, MB, Moe, RO, Spruijt, B, Keeling, LJ and Aubert, A 2007 Assessment of positive emotions in animals to improve their welfare. Physiology & Behavior 92:375–397. https://doi.org/10.1016/j.physbeh.2007.02.003CrossRefGoogle ScholarPubMed
Brando, SICA 2010 Advances in husbandry training in marine mammal care programs. International Journal of Comparative Psychology 23: 777–791CrossRefGoogle Scholar
Broom, DM 1991 Assessing welfare and suffering. Behavioural Processes 25: 117–123. https://doi.org/10.1016/0376-6357(91)90014-QCrossRefGoogle ScholarPubMed
Broom, DM 2010 Animal welfare: an aspect of care, sustainabili-ty, and food quality required by the public. Journal of Veterinary Medical Education 37: 83–88. https://doi.org/10.3138/jvme.37.1.83CrossRefGoogle Scholar
Broom, DM and Johnson, KG 1993 Stress and Animal Welfare. Chapman & Hall: London, UK. https://doi.org/10.1007/978-94-024-0980-2CrossRefGoogle Scholar
Buchanan-Smith, HM, Griciute, J, Daoudi, S, Leonardi, R and Whiten, A 2013 Interspecific interactions and welfare impli-cations in mixed species communities of capuchin (Sapajus apella) and squirrel monkeys (Saimiri sciureus) over 3 years. Applied Animal Behaviour Science 147: 324–333. https://doi.org/10.1016/j.applan-im.2013.04.004CrossRefGoogle Scholar
Butterworth, A, Brakes, P, Vail, CS and Reiss, D 2013 A vet-erinary and behavioral analysis of dolphin killing methods current-ly used in the ‘drive hunt’ in Taiji, Japan. Journal of Applied Animal Welfare Science 16: 184–204. https://doi.org/10.1080/10888705.2013.768925CrossRefGoogle Scholar
Butterworth, A, Clegg, I and Bass, C 2012 Untangled-marine debris: a global picture of the impact on animal welfare and of animal-focused solutions. World Society for the Protection of Animals International: London, UKGoogle Scholar
Castellote, M and Fossa, F 2006 Measuring acoustic activity as a method to evaluate welfare in captive beluga whales (Delphinapterus leucas). Aquatic Mammals 32: 325. https://doi.org/10.1578/AM.32.3.2006.325CrossRefGoogle Scholar
Cattet, M, Boulanger, J, Stenhouse, G, Powell, RA and Reynolds-Hogland, MJ 2008 An evaluation of long-term capture effects in ursids: implications for wildlife welfare and research. Journal of Mammalogy 89(4): 973–990. https://doi.org/10.1644/08-MAMM-A-095.1CrossRefGoogle Scholar
Ceta-base 2011 Captive Cetaceans, Living Population. Ceta-Base: United States & Canada. http://www.ceta-base.com/publications/cetaceans-captive-us-canada-2011.pdfGoogle Scholar
Christiansen, F and Lusseau, D 2015 Linking behavior to vital rates to measure the effects of non-lethal disturbance on wildlife. Conservation Letters 8: 424–431. https://doi.org/10.1111/conl.12166CrossRefGoogle Scholar
Clapham, PJ, Leimkuhler, E and Gray, BK 1995 Do humpback whales exhibit lateralized behaviour? Animal Behaviour 50: 73–82. https://doi.org/10.1006/anbe.1995.0222CrossRefGoogle Scholar
Clark, FE 2013 Marine mammal cognition and captive care: A proposal for cognitive enrichment in zoos and aquariums. Journal of Zoo and Aquarium Research 1: 1–6Google Scholar
Clegg, ILK, Borger-Turner, JL and Eskelinen, HC 2015 C-Well: The development of a welfare assessment index for captive bottlenose dolphins (Tursiops truncatus). Animal Welfare 24: 267–282. https://doi.org/10.7120/09627286.24.3.267CrossRefGoogle Scholar
Connor, RC, Smolker, R and Bejder, L 2006 Synchrony, social behaviour and alliance affiliation in Indian Ocean bottlenose dol-phins, Tursiops aduncus. Animal Behaviour 72: 1371–1378. https://doi.org/10.1016/j.anbehav.2006.03.014CrossRefGoogle Scholar
Connor, RC, Wells, R, Mann, J and Read, A 2000 The bot-tlenose dolphin: social relationships in a fission-fusion society. In: Mann, J, Connor, R, Tyack, P and Whitehead, H (eds) Cetacean Societies: Field Studies of Whales and Dolphins pp 91–126. University of Chicago Press: Chicago, IL, USAGoogle Scholar
Dantzer, R 1988 Les Emotions. Presses Universitaires de France: Paris, FranceGoogle Scholar
Dawkins, MS 1980 Animal Suffering: The Science of Animal Welfare. Chapman and Hall: London, UK. https://doi.org/10.1007/978-94-009-5905-7CrossRefGoogle Scholar
Dawkins, MS 1998 Evolution and animal welfare. Quarterly Review of Biology 305-328. https://doi.org/10.1086/420307CrossRefGoogle Scholar
Dawkins, MS 2004 Using behaviour to assess animal welfare. Animal Welfare 13: 3–7Google Scholar
Dawkins, MS 2006 A user's guide to animal welfare science. Trends in Ecology and Evolution 21: 77–82. https://doi.org/10.1016/j.tree.2005.10.017CrossRefGoogle ScholarPubMed
Dawkins, M 2015 Chapter two: 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
Delfour, F 2006 Marine mammals in front of the mirror, or from body experiences to self-recognition. Cognitive ethological methodology combined with a phenomenological questioning. Journal of Aquatic Mammals 32: 517–527. https://doi.org/10.1578/AM.32.4.2006.517CrossRefGoogle Scholar
Delfour, F 2010 Marine mammals enact individual worlds. International Journal of Comparative Psychology 23: 792–810CrossRefGoogle Scholar
Delfour, F and Beyer, H 2012 Assessing the effectiveness of environmental enrichment in bottlenose dolphins (Tursiops trunca-tus). Zoo Biology 31: 137–150. https://doi.org/10.1002/zoo.20383Google Scholar
Delfour, F and Marten, K 2006 Lateralized visual behavior in bottlenose dolphins (Tursiops truncatus) performing audio-visual tasks: The right visual field advantage. Behavioural Processes 71: 41–50. https://doi.org/10.1016/j.beproc.2005.09.005CrossRefGoogle ScholarPubMed
Désiré, L, Boissy, A and Veissier, I 2002 Emotions in farm ani-mals: a new approach to animal welfare in applied ethology. Behavioural Processes 60: 165–180. https://doi.org/10.1016/S0376-6357(02)00081-5CrossRefGoogle Scholar
Dierauf, L and Gulland, FM 2001 CRC Handbook of Marine Mammal Medicine, Second Edition. CRC Press: Boca Raton, FL, USA. https://doi.org/10.1201/9781420041637CrossRefGoogle Scholar
Dudzinski, KM 2010 Overlap between information gained from complementary and comparative studies of captive and wild dol-phins. International Journal of Comparative Psychology 23: 566–586CrossRefGoogle Scholar
EAZA 2015 European Association of Zoos and Aquaria's (EAZA) European StudBook for bottlenose dolphins. Information provided by Cornelis van Elk, current European StudBook keeper for bot-tlenose dolphins, December 2015Google Scholar
Esch, HC, Sayigh, LS, Blum, JE and Wells, RS 2009 Whistles as potential indicators of stress in bottlenose dolphins (Tursiops truncatus). Journal of Mammalogy 90: 638–650. https://doi.org/10.1644/08-MAMM-A-069R.1CrossRefGoogle Scholar
Fair, PA, Schaefer, AM, Romano, TA, Bossart, GD, Lamb, SV and Reif, JS 2014 Stress response of wild bottlenose dolphins (Tursiops truncatus) during capture-release health assessment studies. General and Comparative Endocrinology 206: 203–212. https://doi.org/10.1016/j.ygcen.2014.07.002CrossRefGoogle ScholarPubMed
Fraser, D, Weary, DM, Pajor, EA and Milligan, BN 1997 A scientific conception of animal welfare that reflects ethical con-cerns. Animal Welfare 6: 187–205Google Scholar
Galhardo, L, Appleby, MC, Waran, NK and Dos Santos, ME 1996 Spontaneous activities of captive performing bottlenose dol-phins (Tursiops truncatus). Animal Welfare 5: 373–389Google Scholar
Gonyou, HW 1994 Why the study of animal behavior is associated with the animal welfare issue. Journal of Animal Science 72: 2171–2177CrossRefGoogle Scholar
Greene, WE, Melillo-Sweeting, K and Dudzinski, KM 2011 Comparing object play in captive and wild dolphins. International Journal Comparative Psychology 24: 292–306CrossRefGoogle Scholar
Grimm, D 2011 Are dolphins too smart for captivity? Science 332: 526–529. https://doi.org/10.1126/science.332.6029.526CrossRefGoogle ScholarPubMed
Gygax, L 1993 Spatial movement patterns and behaviour of two captive bottlenose dolphins (Tursiops truncatus): absence of stereo-typed behaviour or lack of definition? Applied Animal Behaviour Science 38: 337–344. https://doi.org/10.1016/0168-1591(93)90031-JCrossRefGoogle Scholar
Heiler, J, Elwen, SH, Kriesell, HJ and Gridley, T 2016 Changes in bottlenose dolphin whistle parameters related to vessel pres-ence, surface behaviour and group composition. Animal Behaviour 117: 167–177. https://doi.org/10.1016/j.anbehav.2016.04.014CrossRefGoogle Scholar
Held, SD and Špinka, M 2011 Animal play and animal welfare. Animal Behaviour 81: 891–899. https://doi.org/10.1016/j.anbe-hav.2011.01.007CrossRefGoogle Scholar
Herman, LM and Tavolga, WN 1980 The communication sys-tems of cetaceans. In: Herman, L (ed) Cetacean Behavior: Mechanisms and Functions pp 149–209. John Wiley and Sons: New York, NY, USAGoogle Scholar
Herzing, DL 1996 Vocalizations and associated underwater behav-ior of free-ranging Atlantic spotted dolphins, Stenella frontalis and bottlenose dolphins, Tursiops truncatus. Aquatic Mammals 22: 61–80Google Scholar
Hill, H and Lackups, M 2010 Journal publication trends regarding cetaceans found in both wild and captive environments: what do we study and where do we publish? International Journal of Comparative Psychology 23: 414–534Google Scholar
Hill, H and Ramirez, D 2014 Adults play but not like their young: the frequency and types of play by belugas (Delphinapterus leucas) in human care. Animal Behavior and Cognition 1: 166–185. https://doi.org/10.12966/abc.05.07.2014CrossRefGoogle Scholar
Hill, SP and Broom, DM 2009 Measuring zoo animal welfare: theory and practice. Zoo Biology 28: 531–544. https://doi.org/10.1002/zoo.20276Google ScholarPubMed
Hoy, JM, Murray, PJ and Tribe, A 2010 Thirty years later: enrichment practices for captive mammals. Zoo Biology 29: 303–316. https://doi.org/10.1002/zoo.20254CrossRefGoogle ScholarPubMed
Innes, WS, DeMaster, DP, Rodriguez, A and Crowder, LB 2005 Survival rates of marine mammals in captivity: Temporal trends and institutional analysis. Sixteenth Biennial Conference on the Biology of Marine Mammals pp 136. 12-16 December 2005, San Diego, CA, USAGoogle Scholar
Janik, VM and Sayigh, LS 2013 Communication in bottlenose dolphins: 50 years of signature whistle research. Journal of Comparative Physiology A 199: 479–489. https://doi.org/10.1007/s00359-013-0817-7CrossRefGoogle ScholarPubMed
Jensen, A-L, Delfour, F and Carter, T 2013 Anticipatory behaviour in captive bottlenose dolphins (Tursiops truncatus): A preliminary study. Zoo Biology 32: 436–444. https://doi.org/10.1002/zoo.21077CrossRefGoogle ScholarPubMed
Jiang, Y, Luck, M and Parsons, ECM 2007 Public awareness, edu-cation, and marine mammals in captivity. Tourism Review International 11: 237–249. https://doi.org/10.3727/154427207783948829CrossRefGoogle Scholar
Joblon, MJ, Pokras, MA, Morse, B, Harry, CT, Rose, KS, Sharp, SM, Niemeyer, ME, Patchett, KM, Sharp, WB and Moore, MJ 2014 Body condition scoring system for Delphinids based on short-beaked common dolphins (Delphinus delphis). Journal of Marine Animals and Their Ecology 7: 5–13Google Scholar
Johnson, SP, Venn-Watson, SK, Cassle, SE, Smith, CR, Jensen, ED and Ridgway, SH 2009 Use of phlebotomy treat-ment in Atlantic bottlenose dolphins with iron overload. Journal of the American Veterinary Medical Association 235: 194–200. https://doi.org/10.2460/javma.235.2.194CrossRefGoogle Scholar
Jordan, B 2005 Science-based assessment of animal welfare: wild and captive animals. Revue Scientifique et Technique (International Office of Epizootics) 24: 515-528. https://doi.org/10.20506/rst.24.2.1588CrossRefGoogle Scholar
Joseph, B and Antrim, J 2010 Special considerations for the maintenance of marine mammals in captivity. In: Kleiman, DG, Thompson, KV and Kirk Baer, C (eds) Wild Mammals in Captivity: Principles and Techniques for Zoo Management, 2nd Edition pp 181–216. The University of Chicago Press: Chicago, IL, USAGoogle Scholar
Joseph, BE, Cornell, LH, Simpson, JG, Migaki, G and Griner, L 1986 Pulmonary aspergillosis in three species of dolphin. Zoo Biology 5: 301–308. https://doi.org/10.1002/zoo.1430050308CrossRefGoogle Scholar
Karenina, K, Giljov, A, Baranov, V, Osipova, L and Krasnova, V 2010 Visual laterality of calf-mother interactions in wild whales. PLoS ONE 5: e13787. https://doi.org/10.1371/journal.pone.0013787CrossRefGoogle ScholarPubMed
Karenina, K, Giljov, A, Ivkovich, T, Burdin, A and Malashichev, Y 2013 Lateralization of spatial relationships between wild mother and infant orcas, Orcinus orca. Animal Behavior 86: 1225–1231. https://doi.org/10.1016/j.anbe-hav.2013.09.025CrossRefGoogle Scholar
Kuczaj, S, Lacinak, T, Fad, O, Trone, M, Solangi, M and Ramos, J 2002 Keeping environmental enrichment enriching. International Journal of Comparative Psychology 15: 127–137CrossRefGoogle Scholar
Kuczaj, S and Makecha, R 2008 The role of play in the evolution and ontogeny of contextually flexible communication. In: Oller, K and Griebel, U (eds) Evolution of Communicative Flexibility pp 253–278. MIT Press: Cambridge, USA. https://doi.org/10.7551/mitpress/9780262151214.003.0012CrossRefGoogle Scholar
Kuczaj, SA and Eskelinen, HC 2014 Why do dolphins play. Animal Behavior and Cognition 1: 113–127. https://doi.org/10.12966/abc.05.03.2014Google Scholar
Kuczaj, SA, Highfill, LE, Makecha, RN and Byerly, HC 2013 Why do dolphins smile? A comparative perspective on dolphin emotions and emotional expressions. In: Watanabe, S and Kuczaj, S (eds) Emotions of Animals and Humans: Comparative Perspectives pp 63–85. Springer: New York, NY, USAGoogle Scholar
Leliveld, LM, Langbein, J and Puppe, B 2013 The emergence of emotional lateralization: evidence in non-human vertebrates and implications for farm animals. Applied Animal Behaviour Science 145: 1–14. https://doi.org/10.1016/j.applanim.2013.02.002CrossRefGoogle Scholar
Lilly, JC 1963 Distress call of the bottlenose dolphin: stimuli and evoked behavioral responses. Science 139: 116–118. https://doi.org/10.1126/science.139.3550.116CrossRefGoogle ScholarPubMed
Mann, J, Connor, RC, Tyack, PL and Whitehead, H 2000 Cetacean Societies: Field Studies of Dolphins and Whales. University of Chicago Press: Chicago, IL, USAGoogle Scholar
Mann, J and Kemps, C 2003 The effects of provisioning on maternal care in wild bottlenose dolphins, Shark Bay, Australia. Books Online 2006: 304–320Google Scholar
Maple, TL 2007 Toward a science of welfare for animals in the zoo. Journal of Applied Animal Welfare Science 10: 63–70. https://doi.org/10.1080/10888700701277659CrossRefGoogle Scholar
Mason, GJ 1991 Stereotypies: a critical review. Animal Behaviour 41: 1015–1037. https://doi.org/10.1016/S0003-3472(05)80640-2CrossRefGoogle Scholar
Mason, GJ and Latham, NR 2004 Can't stop, won't stop: is stereo-typy a reliable animal welfare indicator? Animal Welfare 13: 57–69Google Scholar
Mason, GJ and Rushen, J 2008 Stereotypic Animal Behaviour: Fundamentals and Applications to Welfare. CABI: Wallingford, UKGoogle Scholar
Mason, GJ and Veasey, JS 2010 How should the psychological well-being of zoo elephants be objectively investigated? Zoo Biology 29: 237–255. https://doi.org/10.1002/zoo.20256CrossRefGoogle ScholarPubMed
Maze-Foley, K and Wursig, B 2002 Patterns of social affiliation and group composition for bottlenose dolphins (Tursiops trunca-tus) in San Luis Pass, Texas. Gulf of Mexico Science 20: 122–134CrossRefGoogle Scholar
McCowan, B, Marino, L, Vance, E, Walke, L and Reiss, D 2000 Bubble ring play of bottlenose dolphins (Tursiops truncatus): implications for cognition. Journal of Comparative Psychology 114:98. https://doi.org/10.1037/0735-7036.114.1.98CrossRefGoogle ScholarPubMed
Meehan, CL and Mench, JA 2007 The challenge of challenge: can problem solving opportunities enhance animal welfare? Applied Animal Behaviour Science 102: 246–261. https://doi.org/10.1016/j.applanim.2006.05.031CrossRefGoogle Scholar
Mendl, M, Burman, OH, Parker, RM and Paul, ES 2009 Cognitive bias as an indicator of animal emotion and welfare: emerging evidence and underlying mechanisms. Applied Animal Behaviour Science 118: 161–181. https://doi.org/10.1016/j.applan-im.2009.02.023CrossRefGoogle Scholar
Mendl, M, Burman, OH and Paul, ES 2010 An integrative and functional framework for the study of animal emotion and mood. Proceedings of the Royal Society of London B: Biological Sciences 277:2895–2904. https://doi.org/10.1098/rspb.2010.0303Google Scholar
Miller, LJ, Kuczaj, S and Herzing, D 2011a Stereotypic behav-ior in wild marine carnivores? Zoo Biology 30: 365–370. https://doi.org/10.1002/zoo.20347CrossRefGoogle Scholar
Miller, SJ, Mellen, J, Greer, T and Kuczaj, SA 2011b The effects of education programmes on Atlantic bottlenose dolphin (Tursiops truncatus) behaviour. Animal Welfare 20: 159–172Google Scholar
Millman, ST 2007 Sickness behaviour and its relevance to animal welfare assessment at the group level. Animal Welfare 16: 123–125Google Scholar
Moberg, GP and Mench, JA 2000 Biology of Animal Stress: Basic Principles and Implications for Animal Welfare. CABI Publishing: Wallingford, UK. https://doi.org/10.1079/9780851993591.0000CrossRefGoogle Scholar
Mononen, J, Moller, SH, Hansen, SW, Hovland, AL, Koistinen, T, Lidfors, L, Malkmvist, J and Ahola, L 2012 The development of on-farm welfare assessment protocols for foxes and mink: the WelFur project. Animal Welfare 21: 363–371. https://doi.org/10.7120/09627286.21.3.363CrossRefGoogle Scholar
Möstl, E and Palme, R 2002 Hormones as indicators of stress. Domestic Animal Endocrinology 23: 67–74. https://doi.org/10.1016/S0739-7240(02)00146-7CrossRefGoogle ScholarPubMed
Müller, M and Bossley, M 2002 Solitary bottlenose dolphins in comparative perspective. Aquatic Mammals 28: 298–307Google Scholar
Neto, MP, Silveira, M and dos Santos, ME 2016 Training bot-tlenose dolphins to overcome avoidance of environmental enrich-ment objects in order to stimulate play activities. Zoo Biology 35:210–215. https://doi.org/10.1002/zoo.21282CrossRefGoogle Scholar
Newberry, RC 1995 Environmental enrichment: increasing the biological relevance of captive environments. Applied Animal Behaviour Science 44: 229–243. https://doi.org/10.1016/0168-1591(95)00616-ZCrossRefGoogle Scholar
Ohl, F and van der Staay, FJ 2012 Animal welfare: At the inter-face between science and society. The Veterinary Journal 192: 13–19. https://doi.org/10.1016/j.tvjl.2011.05.019CrossRefGoogle Scholar
Orbach, DN, Packard, JM, Piwetz, S and Würsig, B 2015 Sex-specific variation in conspecific-acquired marking prevalence among dusky dolphins (Lagenorhynchus obscurus). Canadian Journal of Zoology 93: 383–390. https://doi.org/10.1139/cjz-2014-0302CrossRefGoogle Scholar
Ortiz, RM and Worthy, GAJ 2000 Effects of capture on adre-nal steroid and vasopressin concentrations in free-ranging bot-tlenose dolphins (Tursiops truncatus). Comparative Biochemistry and Physiology Part A 125: 317–324. https://doi.org/10.1016/S1095-6433(00)00158-6CrossRefGoogle ScholarPubMed
Overstrom, NA 1983 Association between burst-pulse sounds and aggressive behavior in captive Atlantic bottlenosed dolphins (Tursiops truncatus). Zoo Biology 2: 93–103. https://doi.org/10.1002/zoo.1430020203CrossRefGoogle Scholar
Pace, DS 2000 Fluke: made bubble rings as toys in bottlenose dolphin calves (Tursiops truncatus). Aquatic Mammals 26: 57–64Google Scholar
Pack, AA 2010 The synergy of laboratory and field studies of dol-phin behavior and cognition. International Journal of Comparative Psychology 23: 538–565CrossRefGoogle Scholar
Parsons, KM, Durban, JW, Claridge, DE, Herzing, DL, Balcomb, KC and Noble, LR 2006 Population genetic structure of coastal bottlenose dolphins (Tursiops truncatus) in the northern Bahamas. Marine Mammal Science 22: 276–298. https://doi.org/10.1111/j.1748-7692.2006.00019.xCrossRefGoogle Scholar
Paul, ES, Harding, EJ and Mendl, M 2005 Measuring emotional processes in animals: the utility of a cognitive approach. Neuroscience & Biobehavioral Reviews 29: 469–491. https://doi.org/10.1016/j.neubiorev.2005.01.002CrossRefGoogle ScholarPubMed
Paulos, RD, Trone, M and Kuczaj SA, II 2010 Play in wild and captive cetaceans. International Journal of Comparative Psychology 23: 701–722CrossRefGoogle Scholar
Pedernera-Romano, C, Valdez, RA, Singh, S, Chiappa, X, Romano, MC and Galindo, F 2006 Salivary cortisol in captive dolphins (Tursiops truncatus): a non-invasive. Animal Welfare 15: 359–362Google Scholar
Perelberg, A and Schuster, R 2009 Bottlenose dolphins (Tursiops truncatus) prefer to cooperate when petted: Integrating proximate and ultimate explanations ii. Journal of Comparative Psychology 123: 45–55. https://doi.org/10.1037/a0013585CrossRefGoogle ScholarPubMed
Pettis, HM, Rolland, RM, Hamilton, PK, Brault, S, Knowlton, AR and Kraus, SD 2004 Visual health assessment of North Atlantic right whales (Eubalaena glacialis) using photographs. Canadian Journal of Zoology 82: 8–19. https://doi.org/10.1139/z03-207Google Scholar
Pryor, K and Norris, KS 1998 Dolphin Societies: Discoveries and Puzzles. University of California Press: London, UKGoogle Scholar
Reif, JS, Fair, PA, Adams, J, Joseph, B, Kilpatrick, DS, Sanchez, R, Goldstein, JD, Townsend, FI Jr, McCulloch, SD, Mazzoil, M, Zolman, ES, Hansen, LJ and Bossart, GD 2008 Evaluation and comparison of the health status of Atlantic bot-tlenose dolphins from the Indian River Lagoon, Florida, and Charleston, South Carolina. Journal of the American Veterinary Medical Association 233: 299–307. https://doi.org/10.2460/javma.233.2.299CrossRefGoogle ScholarPubMed
Reiss, D and Marino, L 2001 Mirror self-recognition in the bot-tlenose dolphin: A case of cognitive convergence. Proceedings of the National Academy of Sciences 98: 5937–5942. https://doi.org/10.1073/pnas.101086398CrossRefGoogle Scholar
Roche, JR, Friggens, NC, Kay, JK, Fisher, MW, Stafford, KJ and Berry, DP 2009 Invited review: Body condition score and its asso-ciation with dairy cow productivity, health, and welfare. Journal of Dairy Science 92: 5769–5801. https://doi.org/10.3168/jds.2009-2431CrossRefGoogle Scholar
Roe, E, Buller, H and Bull, J 2011 The performance of farm ani-mal assessment. Animal Welfare 20: 69–78Google Scholar
Rogers, LJ 2002 Lateralization in vertebrates: its early evolution, general pattern, and development. Advances in the Study of Behavior, Vol 31 pp 107–161. Academic Press Inc: San Diego, CA, USA. https://doi.org/10.1016/S0065-3454(02)80007-9Google Scholar
Rogers, LJ 2010 Relevance of brain and behavioural lateralization to animal welfare. Applied Animal Behaviour Science 127: 1–11. https://doi.org/10.1016/j.applanim.2010.06.008CrossRefGoogle Scholar
Rushen, J, Butterworth, A and Swanson, JC 2011 Animal behavior and well-being symposium: farm animal welfare assur-ance: science and application. Journal of Animal Science 89: 1219–1228. https://doi.org/10.2527/jas.2010-3589CrossRefGoogle Scholar
Russell, JA 2003 Core affect and the psychological construction of emotion. Psychological Review 110: 145. https://doi.org/10.1037/0033-295X.110.1.145CrossRefGoogle ScholarPubMed
Sakai, M, Hishii, T, Takeda, S and Kohshima, S 2006 Laterality of flipper rubbing behaviour in wild bottlenose dolphins (Tursiops aduncus): Caused by asymmetry of eye use? Behavioural Brain Research 170: 204–210. https://doi.org/10.1016/j.bbr.2006.02.018CrossRefGoogle ScholarPubMed
Samuels, A and Gifford, T 1997 A quantitative assessment of dominance relations among bottlenose dolphins. Marine Mammal Science 13: 70–99. https://doi.org/10.1111/j.1748-7692.1997.tb00613.xCrossRefGoogle Scholar
Schusterman, R, Thomas, JA and Wood, FG 2013 Dolphin Cognition and Behavior: A Comparative Approach. Psychology Press: London, UKCrossRefGoogle Scholar
Schwacke, LH, Smith, CR, Townsend, FI, Wells, RS, Hart, LB, Balmer, BC and Rowles, TK 2014 Health of common bot-tlenose dolphins (Tursiops truncatus) in Barataria Bay, Louisiana, following the Deepwater Horizon oil spill. Environmental Science and Technology 48: 93–103. https://doi.org/10.1021/es403610fCrossRefGoogle ScholarPubMed
Scott, EM, Mann, J, Watson-Capps, JJ, Sargeant, BL and Connor, RC 2005 Aggression in bottlenose dolphins: evidence for sexual coercion, male-male competition, and female tolerance through analysis of tooth-rake marks and behaviour. Behaviour 142: 21–44. https://doi.org/10.1163/1568539053627712Google Scholar
Selye, H 1975 Stress and distress. Comprehensive Therapy 1: 9–13Google ScholarPubMed
Siegford, JM 2013 Multidisciplinary approaches and assessment techniques to better understand and enhance zoo nonhuman ani-mal welfare. Journal of Applied Animal Welfare Science 16: 300–318. https://doi.org/10.1080/10888705.2013.827914CrossRefGoogle Scholar
Silber, GK and Fertl, D 1995 Intentional beaching by bottlenose dolphins (Tursiops truncatus) in the Colorado River Delta, Mexico. Aquatic Mammals 21: 183–186Google Scholar
Small, RJ and DeMaster, DP 1995 Survival of five species of captive marine mammals. Marine Mammal Science 11: 209–226. https://doi.org/10.1111/j.1748-7692.1995.tb00519.xCrossRefGoogle Scholar
Smolker, R, Richards, A, Connor, RC, Mann, J and Berggren, P 1997 Sponge carrying by dolphins (Delphinidae, Tursiops spp): a foraging specialization involving tool use? Ethology 103: 454–465. https://doi.org/10.1111/j.1439-0310.1997.tb00160.xCrossRefGoogle Scholar
Sneddon, LU, Elwood, RW, Adamo, SA and Leach, MC 2014 Defining and assessing animal pain. Animal Behaviour 97: 201–212. https://doi.org/10.1016/j.anbehav.2014.09.007CrossRefGoogle Scholar
Sobel, N, Supin, AY and Myslobodsky, MS 1994 Rotational swimming tendencies in the dolphin (Tursiops truncatus). Behavioural Brain Research 65: 41–45. https://doi.org/10.1016/0166-4328(94)90071-XCrossRefGoogle ScholarPubMed
Spruijt, BM, van den Bos, R and Pijlman, FT 2001 A concept of welfare based on reward evaluating mechanisms in the brain: anticipatory behaviour as an indicator for the state of reward sys-tems. Applied Animal Behaviour Science 72: 145–171. https://doi.org/10.1016/S0168-1591(00)00204-5CrossRefGoogle Scholar
Stockin, KA, Lusseau, D, Binedell, V, Wiseman, N and Orams, MB 2008 Tourism affects the behavioural budget of the common dolphin Delphinus spp. in the Hauraki Gulf, New Zealand. Marine Ecology-Progress Series 355: 287. https://doi.org/10.3354/meps07386CrossRefGoogle Scholar
Swaisgood, RR 2007 Current status and future directions of applied behavioral research for animal welfare and conservation. Applied Animal Behaviour Science 102: 139–162. https://doi.org/10.1016/j.applanim.2006.05.027CrossRefGoogle Scholar
Tamaki, N, Morisaka, T and Taki, M 2006 Does body contact contribute towards repairing relationships? The association between flipper-rubbing and aggressive behavior in captive bot-tlenose dolphins. Behavioural Processes 73: 209–215. https://doi.org/10.1016/j.beproc.2006.05.010CrossRefGoogle ScholarPubMed
Thomson, CA and Geraci, JR 1986 Cortisol, aldosterone, and leucocytes in the stress response of bottlenose dolphins, Tursiops truncatus. Canadian Journal of Fisheries and Aquatic Sciences 43:1010–1016. https://doi.org/10.1139/f86-125CrossRefGoogle Scholar
Ugaz, C, Valdez, RA, Romano, MC and Galindo, F 2013 Behavior and salivary cortisol of captive dolphins (Tursiops trunca-tus) kept in open and closed facilities. Journal of Veterinary Behavior: Clinical Applications and Research 8: 285–290. https://doi.org/10.1016/j.jveb.2012.10.006CrossRefGoogle Scholar
Veasey, J 2006 Concepts in the care and welfare of captive ele-phants. International Zoo Yearbook 40: 63–79. https://doi.org/10.1111/j.1748-1090.2006.00063.xCrossRefGoogle Scholar
Veissier, I, Butterworth, A, Bock, B and Roe, E 2008 European approaches to ensure good animal welfare. Applied Animal Behaviour Science. 113: 279-297. https://doi.org/10.1016/j.applanim.2008.01.008CrossRefGoogle Scholar
Venn-Watson, SK, Jensen, ED and Ridgway, SH 2011 Evaluation of population health among bottlenose dolphins (Tursiops truncatus) at the United States Navy Marine Mammal Program. Journal of the American Veterinary Medical Association 238:356–360. https://doi.org/10.2460/javma.238.3.356CrossRefGoogle ScholarPubMed
Ventre, J and Jett, J 2015 Killer whales, theme parks and contro-versy: an exploration of the evidence. In: Markwell, K (ed) Animals and Tourism: Understanding Diverse Relationships. Channel View Productions: Bristol, UKGoogle Scholar
Vicino, GA and Marcacci, ES 2015 Intensity of play behavior as a potential measure of welfare: A novel method for quantifying the integrated intensity of behavior in African elephants. Zoo Biology 34: 492–496. https://doi.org/10.1002/zoo.21238CrossRefGoogle ScholarPubMed
Walker, MD, Duggen, G, Roulston, N, Van Slack, AG and Mason, G 2012 Negative affective states and their effects on mor-bidity, mortality and longevity. Animal Welfare 21: 497–509. https://doi.org/10.7120/09627286.21.4.497CrossRefGoogle Scholar
Waples, KA and Gales, NJ 2002 Evaluating and minimising social stress in the care of captive bottlenose dolphins (Tursiops adun-cus). Zoo Biology 21: 5–26. https://doi.org/10.1002/zoo.10004CrossRefGoogle Scholar
Watters, JV 2014 Searching for behavioral indicators of welfare in zoos: Uncovering anticipatory behavior. Zoo Biology 33: 251–256. https://doi.org/10.1002/zoo.21144CrossRefGoogle ScholarPubMed
Weary, DM, Niel, L, Flower, FC and Fraser, D 2006 Identifying and preventing pain in animals. Applied Animal Behaviour Science 100: 64–76. https://doi.org/10.1016/j.applanim.2006.04.013Google Scholar
Webster, J 2005 Animal Welfare: Limping towards Eden. Blackwell Publishing Ltd: Oxford, UK. https://doi.org/10.1002/9780470751107CrossRefGoogle Scholar
Welfare Quality® 2009a Welfare Quality® Assessment Protocol for Cattle (Fattening Cattle, Dairy cows, Veal Calves). Welfare Quality® Consortium: Lelystad, The NetherlandsGoogle Scholar
Welfare Quality® 2009b Welfare Quality® Assessment Protocol for Pigs. Welfare Quality®Consortium: Lelystad, The NetherlandsGoogle Scholar
Welfare Quality® 2009c Welfare Quality® Assessment Protocol for Poultry. Welfare Quality® Consortium: Lelystad, The NetherlandsGoogle Scholar
Wells, RS 1991 The role of long-term study in understanding the social structure of a bottlenose dolphin community. In: Pryor, K and Norris, KS (eds) Dolphin Societies: Discoveries and Puzzles pp 199–225. University of California Press: London, UKGoogle Scholar
Wells, RS 2009 Learning from nature: bottlenose dolphin care and husbandry. Zoo Biology 28: 635–651. https://doi.org/10.1002/zoo.20252Google ScholarPubMed
Wells, RS and Scott, MD 1999 Bottlenose dolphin: Tursiops trun-catus (Montagu, 1821). In: Ridgway, SH and Harrison, R (eds) Handbook of Marine Mammals: The Second Book of Dolphins and Porpoises pp 137–182. Academic Press: San Diego, CAGoogle Scholar
Whitham, JC and Wielebnowski, N 2013 New directions for zoo animal welfare science. Applied Animal Behaviour Science 147:247–260. https://doi.org/10.1016/j.applanim.2013.02.004CrossRefGoogle Scholar
Würbel, H and Garner, JP 2007 Refinement of rodent research through environmental enrichment and systematic randomization. NC3Rs 9: 1–9Google Scholar
Yaman, S, von Fersen, L, Dehnhardt, G and Güntürkün, O 2003 Visual lateralization in the bottlenose dolphin (Tursiops trun-catus): Evidence for a population asymmetry? Behavioural Brain Research 142: 109–114. https://doi.org/10.1016/S0166-4328(02)00385-6CrossRefGoogle ScholarPubMed
Yeates, JW and Main, DCJ 2008 Assessment of positive wel-fare: a review. The Veterinary Journal 175: 293–300. https://doi.org/10.1016/j.tvjl.2007.05.009CrossRefGoogle Scholar