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A review of welfare indicators for sea turtles undergoing rehabilitation, with emphasis on environmental enrichment

Published online by Cambridge University Press:  01 January 2023

R Diggins*
Affiliation:
College of Public Health, Medical and Veterinary Sciences, James Cook University, 1 Solander Drive, Douglas, QLD 4811, Australia
R Burrie
Affiliation:
College of Public Health, Medical and Veterinary Sciences, James Cook University, 1 Solander Drive, Douglas, QLD 4811, Australia
E Ariel
Affiliation:
College of Public Health, Medical and Veterinary Sciences, James Cook University, 1 Solander Drive, Douglas, QLD 4811, Australia
J Ridley
Affiliation:
College of Public Health, Medical and Veterinary Sciences, James Cook University, 1 Solander Drive, Douglas, QLD 4811, Australia
J Olsen
Affiliation:
College of Public Health, Medical and Veterinary Sciences, James Cook University, 1 Solander Drive, Douglas, QLD 4811, Australia
S Schultz
Affiliation:
College of Public Health, Medical and Veterinary Sciences, James Cook University, 1 Solander Drive, Douglas, QLD 4811, Australia
A Pettett-Willmett
Affiliation:
College of Public Health, Medical and Veterinary Sciences, James Cook University, 1 Solander Drive, Douglas, QLD 4811, Australia
G Hemming
Affiliation:
College of Public Health, Medical and Veterinary Sciences, James Cook University, 1 Solander Drive, Douglas, QLD 4811, Australia
J Lloyd
Affiliation:
College of Public Health, Medical and Veterinary Sciences, James Cook University, 1 Solander Drive, Douglas, QLD 4811, Australia
*
* Contact for correspondence: [email protected]
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Abstract

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For animals undergoing rehabilitation it is vital to monitor welfare in a way that is feasible, practical, and limits stress to the animal. The industry gold standard is to assess welfare under the Five Domains model, including nutrition, environment, physical health, and behaviour as the first four physical domains and mental domain as the fifth. Feasibility and effectiveness of these domains for assessing welfare of sea turtles undergoing rehabilitation were reviewed and it was determined that the mental state can be best assessed through behavioural changes. A scoping review of the literature was conducted using Scopus and Web of Science to investigate use of environmental enrichment devices (EEDs) as a measure of welfare in sea turtles. Behavioural assessments using EEDs were found to be well-documented; however, most EED studies pertained largely to livestock or zoo animals. Furthermore, studies rarely concentrated on reptiles, and specifically sea turtles. Results also showed that certain welfare assessment methods may be less appropriate for short-term captivity experienced during rehabilitation. Additionally, the hospital environment limits the ability to address some of the domains (ie biosecurity, feasibility, safety of turtle, etc, might be compromised). This review shows that only three of the nine environmental enrichment strategies described in the literature suit the specific requirements of sea turtles in rehabilitation: feeding, tactile, and structural. It is documented that turtles display behaviours that would benefit from EEDs and, therefore, more specific studies are needed to ensure the best welfare outcomes for sea turtles undergoing rehabilitation.

Type
Research Article
Copyright
© 2022 Universities Federation for Animal Welfare

References

Addison, DS and Nelson, KA 2000 Recapture of a tagged, captive reared juvenile loggerhead turtle: an example of habituation? Marine Turtle Newsletter 89: 1516Google Scholar
Amorocho, D and Reina, R 2008 Intake passage time, digesta composition and digestibility in East Pacific green turtles (Chelonia mydas agassizii) at Gorgona National Park, Colombian Pacific. Journal of Experimental Marine Biology and Ecology 360: 117124. https://doi.org/10.1016/j.jembe.2008.04.009CrossRefGoogle Scholar
Arena, P, Warwick, C and Steedman, C 2014 Welfare and environmental implications of farmed sea turtles. Journal of Agricultural and Environmental Ethics 27: 309330. https://doi.org/10.1007/s10806-013-9465-8CrossRefGoogle Scholar
Arthur, K, McMahon, K, Limpus, C and Dennison, W 2009 Feeding ecology of green turtles (Chelonia mydas) from Shoalwater Bay, Australia. Marine Turtle Newsletter 123: 612Google Scholar
Balazs, G, Losey, G and Privitera, L 1994 Cleaning symbiosis between the wrasse, Thalassoma dupery, and the green turtle, Chelonia mydas. Copeia 3: 684690. https://doi.org/10.2307/1447184Google Scholar
Bannister, CC, Thomson, AJC and Cuculescu-Santana, M 2021 Can colored object enrichment reduce the escape behavior of captive freshwater turtles? Zoo Biology 40(2): 160168. https://doi.org/10.1002/zoo.21583CrossRefGoogle ScholarPubMed
Barber, JC and Mellen, JD 2013 Animal ethics and welfare. In: Irwin, MD, Stoner, JB and Cobaugh, AM (eds) Zookeeping: An Introduction to the Science and Technology pp 5361. University of Chicago Press: Chicago, USAGoogle Scholar
Barnett, J and Hemsworth, P 2009 Welfare monitoring schemes: using research to safeguard welfare of animals on the farm. Journal of Applied Animal Welfare Science 12: 114131. https://doi.org/10.1080/10888700902719856CrossRefGoogle ScholarPubMed
Bartol, S, Mellgren, R and Musick, J 2003 Visual acuity of juvenile loggerhead sea turtles (Caretta caretta): a behavioral approach. International Journal of Comparative Psychology 16: 143155Google Scholar
Bennett, A 1982 The energetics of reptilian activity. Biology Of The Reptilia 13: 155199Google Scholar
Bjorndal, KA 1980 Nutrition and grazing behavior of the green turtle Chelonia mydas. Marine Biology 56(2): 147154. https://doi.org/10.1007/BF00397131CrossRefGoogle Scholar
Bracke, M and Hopster, H 2006 Assessing the importance of natural behavior for animal welfare. Journal of Agricultural and Environmental Ethics 19: 7789. https://doi.org/10.1007/s10806-005-4493-7CrossRefGoogle Scholar
Brill, R, Balazs, G, Holland, K, Chang, R, Sullivan, S and George, J 1995 Daily movements, habitat use, and submergence intervals of normal and tumor-bearing juvenile green turtles (Chelonia mydas L) within a foraging area in the Hawaiian islands. Journal of Experimental Marine Biology and Ecology 185: 203218. https://doi.org/10.1016/0022-0981(94)00146-5CrossRefGoogle Scholar
Broom, D and Johnson, KJ 1993 Stress and strain, welfare and suffering. In: Broom, D (ed) Stress and Animal Welfare pp 8082. Kluwer Academic Publishers: The Netherlands. https://doi.org/10.1007/978-94-024-0980-2CrossRefGoogle Scholar
Bryant, Z and Kother, G 2015 Environmental enrichment with simple puzzle feeders increases feeding time in fly river turtles (Carettochelys insculpta). Herpetological Bulletin 130: 35Google Scholar
Burghardt, G 2005 Genesis of Animal Play: Testing the Limits. MT Press: Cambridge, UK. https://doi.org/10.7551/mitpress/3229.001.0001Google Scholar
Burghardt, G 2013 Environmental enrichment and cognitive complexity in reptiles and amphibians: concepts, review, and impli-cations for captive populations. Applied Animal Behaviour Science 147(3-4): 286298. https://doi.org/10.1016/j.applanim.2013.04.013CrossRefGoogle Scholar
Burghardt, G, Rosscoe, R and Ward, B 1996 Problem of reptile play: environmental enrichment and play behavior in a captive Nile soft-shelled turtle, Trionyx triunguis. Zoo Biology 15: 223238. https://doi.org/10.1002/(SICI)1098-2361(1996)15:3<223::AID-ZOO3>3.0.CO;2-D3.0.CO;2-D>CrossRefGoogle Scholar
Cabanac, M 1999 Emotion and phylogeny. Journal of Consciousness Studies 6: 176190Google Scholar
Cabanac, M and Bernieri, C 2000 Behavioral rise in body tem-perature and tachycardia by handling of a turtle (Clemmys insculp-ta). Behavioral Processes 49: 6168. https://doi.org/10.1016/S0376-6357(00)00067-XCrossRefGoogle Scholar
Caldwell, D 1962 Growth measurements of young captive Atlantic sea turtles in temperate waters. Contributions in Science 50: 18. https://doi.org/10.5962/p.241045CrossRefGoogle Scholar
Case, B, Lewbart, G and Doerr, P 2005 The physiological and behav-ioral impacts of and preference for an enriched environment in the eastern box turtles (Terrapene carolina carolina). Applied Animal Behaviour Science 92: 353365. https://doi.org/10.1016/j.applanim.2004.11.011CrossRefGoogle Scholar
Claxton, AM 2011 The potential of the human–animal relation-ship as an environmental enrichment for the welfare of zoo-housed animals. Applied Animal Behaviour Science 133(1-2): 110. https://doi.org/10.1016/j.applanim.2011.03.002CrossRefGoogle Scholar
Clegg, IL, Borger-Turner, JL and Eskelinen, HC 2015 C-Well: The development of a welfare assessment index for captive bot-tlenose dolphins (Tursiops truncatus). Animal Welfare 24(3): 267282. https://doi.org/10.7120/09627286.24.3.267CrossRefGoogle Scholar
Davis, K 2009 Sociality, cognition and social learning in turtles ( Emydidae). Dissertation, Tenessee Research and Creative Exchange, USAGoogle Scholar
Davis, K and Burghardt, G 2012 Long-term retention of visual tasks by two species of emydid turtles, Pseudemys nelsoni and Trachemys scripta. Journal of Comparative Psychology 126: 213223. https://doi.org/10.1037/a0027827CrossRefGoogle ScholarPubMed
Davis, A, Maney, D and Maerz, J 2008 The use of leukocyte pro-files to measure stress in vertebrates: A review for ecologists. Functional Ecology 22(5): 760772. https://doi.org/10.1111/j.1365-2435.2008.01467.xCrossRefGoogle Scholar
Dawkins, MS 2008 The science of animal suffering. Ethology 114: 937945. https://doi.org/10.1111/j.1439-0310.2008.01557.xCrossRefGoogle Scholar
de Azevedo, CS, Cipreste, CF and Young, RJ 2007 Environmental enrichment: a GAP analysis. Applied Animal Behaviour Science 102(3-4): 329343. https://doi.org/10.1016/j.applanim.2006.05.034CrossRefGoogle Scholar
Deem, SL and Harris, HS 2017 Nutrition. In: Manire, CA, Norton, TM and Stacy, BA (eds) Sea Turtle Health and Rehabilitation pp 945953. J Ross Publishing, Incorporated: FL, USAGoogle Scholar
Eagan, T 2019 Evaluation of enrichment for reptiles in zoos. Journal of Applied Animal Welfare Science 22(1): 6977. https://doi.org/10.1080/10888705.2018.1490182CrossRefGoogle ScholarPubMed
Englefield, B, Blackman, SA, Starling, M and McGreevy, PD 2019 A review of Australian animal welfare legislation, regulation, codes of practice, and policy, and their influence on stakeholders caring for wildlife and the animals for whom they care. Animals 9(6): 335. https://doi.org/10.3390/ani9060335CrossRefGoogle ScholarPubMed
Fagen, R 1981 Animal Play Behavior. Oxford University Press: New York, USAGoogle Scholar
Farm Animal Welfare Council 1993 Second report on priorities for research and development in farm animal welfare. Farm Animal Welfare Council, MAFF: Tolworth, UKGoogle Scholar
Flint, J, Flint, M, Limpus, CJ and Mills, P 2017 Status of marine turtle rehabilitation in Queensland. PeerJ 5: e3132. https://doi.org/10.7717/peerj.3132CrossRefGoogle ScholarPubMed
Garner, J 2005 Part II: stereotypic behaviours as pathologies. In: Mason, G and Rushen, J (eds) Stereotypic Animal Behaviour: Fundamentals and Applications to Welfare, Second Edition. CABI Publishing: Cambridge, UKGoogle Scholar
Glazebrook, JS, Campbell, RSF and Blair, D 1989 Studies on cardiovascular fluke (Digenea: Spirorchiidae) infections in sea turtles from the Great Barrier Reef, Queensland, Australia. Journal of Comparative Pathology 101(3): 231250. https://doi.org/10.1016/0021-9975(89)90033-9CrossRefGoogle ScholarPubMed
Gordon, AN, Kelly, WR and Lester, RJG 1993 Epizootic mor-tality of free-living green turtles, Chelonia mydas, due to coccidio-sis. Journal of Wildlife Diseases 29(3): 490494. https://doi.org/10.7589/0090-3558-29.3.490CrossRefGoogle Scholar
Gregory, L, Gross, T, Bolten, A, Bjorndal, K and Guillette, L 1996 Plasma corticosterone concentrations associated with acute captivity stress in the loggerhead sea turtle (Caretta caretta). General and Comparative Endocinology 104(3): 312320. https://doi.org/10.1006/gcen.1996.0176CrossRefGoogle Scholar
Guy, AJ, Curnoe, D and Banks, PB 2013 A survey of current mammal rehabilitation and release practices. Biodiversity and Conservation 22(4): 825837. https://doi.org/10.1007/s10531-013-0452-1CrossRefGoogle Scholar
Hall, RJ, Robson, SK and Ariel, E 2018 Colour vision of green turtle (Chelonia mydas) hatchlings: do they still prefer blue under water? PeerJ 6: e5572. https://doi.org/10.7717/peerj.5572CrossRefGoogle ScholarPubMed
Hart, K and Fujisaki, I 2010 Satellite tracking reveals habitat use by juvenile green sea turtles, Chelonia mydas, in the Everglades, Florida, USA. Endangered Species Research 11: 221232. https://doi.org/10.3354/esr00284CrossRefGoogle Scholar
Hawkings, M and Willemsen, M 2004 Environmental enrichment for amphibians and reptiles. ASZK Reptile Enrichment Workshop. Zoological Parks Board of NSW. Thylacinus vol 28, no 3. http://tester.enrichment.org/MiniWebs/Australasia/workshop01.pdfGoogle Scholar
Heithaus, M, McLash, J, Frid, A, Dill, L and Marshall, G 2002 Novel insights into green sea turtle behaviour using animal-borne video cam-eras. Journal of the Marine Biological Association of the United Kingdom 82: 10491050. https://doi.org/10.1017/S0025315402006689CrossRefGoogle Scholar
Hoopes, LA, Koutsos, EA and Norton, TM 2017 Nutrition. In: Manire, CA, Norton, TM and Stacy, BA (eds) Sea Turtle Health & Rehabilitation pp 6390. J Ross Publishing, Incorporated: FL, USAGoogle Scholar
Hoy, J, Murray, P and Tribe, A 2010 Thirty years later: enrich-ment practices for captive mammals. Zoo Biology 29: 303316. https://doi.org/10.1002/zoo.20254CrossRefGoogle Scholar
Hunt, KE, Innis, CJ, Kennedy, AE, McNally, KL, Davis, DG, Burgess, EA and Merigo, C 2016 Assessment of ground trans-portation stress in juvenile Kemp's Ridley sea turtles (Lepidochelys kempii). Conservation Physiology 4(1). https://doi.org/10.1093/con-phys/cov071CrossRefGoogle Scholar
Hutchins, M 2006 Death at the zoo: the media, science, and real-ity. Zoo Biology 25: 101115. https://doi.org/10.1002/zoo.20085CrossRefGoogle Scholar
Jessop, T 2001 Modulation of the adrenocortical stress response in marine turtles (Cheloniidae): evidence for a hormonal tactic maximizing maternal reproductive investment. Journal of Zoology 254: 5765. https://doi.org/10.1017/S0952836901000553CrossRefGoogle Scholar
Jessop, T, Knapp, R, Whittier, J and Limpus, C 2002a Dynamic endocrine responses to stress: evidence for energetic constraints and sta-tus dependence in breeding male green turtles. General and Comparative Endocrinology 129: 5967. https://doi.org/10.1006/gcen.2001.7769CrossRefGoogle Scholar
Jessop, T, Limpus, C and Whittier, J 2002b Nocturnal activity in the green sea turtle alters daily profiles of melatonin and corticos-terone. Hormones and Behaviour 41: 357365. https://doi.org/10.1006/hbeh.2002.1775CrossRefGoogle Scholar
Jessop, TS, Sumner, JM, Limpus, CJ and Whittier, JM 2004 Interplay between plasma hormone profiles, sex and body condition in immature hawksbill turtles (Eretmochelys imbricata) subject-ed to a capture stress protocol. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 137(1): 197204. https://doi.org/10.1016/j.cbpb.2003.09.029CrossRefGoogle ScholarPubMed
Jones, TT, Salmon, M, Wyneken, J and Johnson, C 2000 Rearing leatherback hatchlings: protocols, growth and survival. Marine Turtle Newsletter 90: 36Google Scholar
Kanghae, H, Thongprajukaew, K, Inphrom, S, Malawa, S, Sandos, P, Sotong, P and Boonsuk, K 2021 Enrichment devices for green turtles (Chelonia mydas) reared in captivity programs. Zoo Biology 40(5): 407416. https://doi.org/10.1002/zoo.21613CrossRefGoogle ScholarPubMed
Krams, I, Vrublevska, J, Cirule, D, Kivleniece, I, Krama, T, Rantala, MJ, Sild, E and Hõrak, P 2012 Heterophil/lymphocyte ratios predict the magnitude of humoral immune response to a novel antigen in great tits (Parus major). Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 161(4): 422428. https://doi.org/10.1016/j.cbpa.2011.12.018CrossRefGoogle ScholarPubMed
Lambert, H, Carder, G and D’Cruze, N 2019 Given the cold shoulder: A review of the scientific literature for evidence of reptile sentience. Animals 9(10): 821. https://doi.org/10.3390/ani9100821CrossRefGoogle Scholar
Latham, N 2010 Chapter 6. Brief introduction to welfare assess-ment: A ‘Toolbox’ of techniques. In: Hubrecht R and Kirkwood JK (eds) The UFAW Handbook on the Care and Management of Laboratory and Other Research Animals, Chapter 6. Brief introduction to welfare assess-ment: A ‘Toolbox’ of techniques. In: Hubrecht R and Kirkwood JK (eds) The UFAW Handbook on the Care and Management of Laboratory and Other Research Animals, Wiley: West Sussex, UKGoogle Scholar
Levy, Y, King, R and Aizenberg, I 2005 Holding a live leatherback turtle in Israel: lessons learned. Marine Turtle Newsletter 107: 78Google Scholar
Limpus, C and Limpus, D 2000 Mangroves in the diet of Chelonia mydas in Queensland, Australia. Marine Turtle Newsletter 89: 1315Google Scholar
Limpus, CJ, Limpus, DJ, Savige, M and Shearer, D 2012 Health assessment of green turtles in south and central Queensland following extreme weather impacts on coastal habitat during 2011. Department of Environment and Heritage Protection: QLD, AustraliaGoogle Scholar
Lloyd, J, Ariel, E, Adams, D and Owens, L 2012 Environmental enrichment for sea turtles in rehabilitation: preliminary study. Proceedings of the 8th National Australian Wildlife Rehabilitation Conference. 16-20 July 2012,Townsville, QLD, AustraliaGoogle Scholar
Lopez, J, Gomez, Y, Rodriguez, F, Broglio, C, Vargas, J and Salas, C 2001 Spatial learning in turtles. Animal Cognition 4: 4959. https://doi.org/10.1007/s100710100091Google Scholar
Manire, CA, Norton, TM, Walsh, MT and Campbell, LA 2017 Buoyancy disorders. In: Manire, CA, Norton, TM and Stacy, BA (eds) Sea Turtle Health & Rehabilitation pp 4560. J Ross Publishing, Incorporated: FL, USAGoogle Scholar
Maple, T and Perdue, B 2013 Zoo Animal Welfare. Springer: Heidelberg, New York, Dordrecht, London. https://doi.org/10.1007/978-3-642-35955-2CrossRefGoogle Scholar
March, DT, Marshall, K, Swan, G, Gerlach, T, Smith, H, Blyde, D, Ariel, E, Christidis, L and Kelaher, BP 2021 The use of echocardiography as a health assessment tool in green sea turtles (Chelonia mydas). Australian Veterinary Journal 99(1-2): 4654. https://doi.org/10.1111/avj.13039CrossRefGoogle ScholarPubMed
March, DT, Vinette-Herrin, K, Peters, A, Ariel, E, Blyde, D, Hayward, D, Christidis, L and Kelaher, BP 2018 Hematologic and biochemical characteristics of stranded green sea turtles. Journal of Veterinary Diagnostic Investigation 30(3): 423429. https://doi.org/10.1177/1040638718757819CrossRefGoogle ScholarPubMed
Mason, G 1991 Stereotypies: a critical review. Animal Behaviour 41: 10151037. https://doi.org/10.1016/S0003-3472(05)80640-2CrossRefGoogle Scholar
Mason, G and Latham, N 2004 Can't stop, won't stop: is stereo-typy a reliable animal welfare indicator? Animal Welfare 13: 5769Google Scholar
Mason, G, Clubb, R, Latham, N and Vickery, S 2007 Why and how should we use environmental enrichment to tackle stereo-typic behaviour? Applied Animal Behaviour Science 102(3-4): 163188. https://doi.org/10.1016/j.applanim.2006.05.041CrossRefGoogle Scholar
Mason, G and Mendl, M 1993 Why is there no simple way of measuring animal welfare? Animal Welfare 2: 301319Google Scholar
Mason, G and Veasey, JS 2010 How should the psychological well-being of zoo elephants be objectively investigated? Zoo Biology 29(2): 237255. https://doi.org/10.1002/zoo.20256CrossRefGoogle ScholarPubMed
Meager, JJ and Limpus, C 2012 Marine wildlife stranding and mortality database annual report 2011 III. Marine Turtle. Conservation Technical and Data Report 3: 146Google Scholar
Mellen, J and MacPhee, M 2001 Philosophy of environmental enrichment: past, present and future. Zoo Biology 20: 211226. https://doi.org/10.1002/zoo.1021CrossRefGoogle Scholar
Mellgren, R and Mann, M 1998 What can a green sea turtle learn? In: Abreu-Grobois, F, Briseño-Dueñas, R, Márquez, R and Sarti, L (eds) Proceedings of the Eighteenth International Sea Turtle Symposium. US Department of Commerce, NOAA Tech Memo. NMFS-SEFSC-436 pp 7980. 3-7 March 1998, Mazatlán, Sinaloa, México. http://aquaticcommons.org/2131/1/Fish_TM_436.pdfGoogle Scholar
Mellor, DJ 2017 Operational details of the Five Domains model and its key applications to the assessment and management of ani-mal welfare. Animals 7: 60. https://doi.org/10.3390/ani7080060CrossRefGoogle Scholar
Mellor, DJ and Beausoleil, NJ 2015 Extending the ‘Five Domains’ model for animal welfare assessment to incorporate positive welfare states. Animal Welfare 24(3): 241. https://doi.org/10.7120/09627286.24.3.241CrossRefGoogle Scholar
Mellor, DJ and Reid, CSW 1994 Concepts of animal well-being and predicting the impact of procedures on experimental animals. Improving the Well-being of Animals in the Research Environment 3-18. https://www.wellbeingintlstudiesrepository.org/cgi/viewcontent.cg i?article=1006&context=exprawelGoogle Scholar
Melvin, SD, March, DT, Marshall, K, Carroll, AR and van de Merwe, JP 2021 Improving rehabilitation outcomes using metabolomics: Health, recovery and biomarkers of mortality in sick and injured green turtles (Chelonia mydas). Biological Conservation 254: 108943. https://doi.org/10.1016/j.biocon.2020.108943CrossRefGoogle Scholar
Monreal-Pawlowsky, T, Marco-Cabedo, V, Membrive, GP, Sanjose, J, Fuentes, O, Jimenez, E and Manteca, X 2017 Environmental enrichment facilitates release and survival of an injured loggerhead sea turtle (Caretta caretta) after ten years in captivity. Journal of Zoo and Aquarium Research 5: 182186Google Scholar
Newberry, R 1995 Environmental enrichment: increasing the bio-logical relevance of captive environments. Applied Animal Behaviour Science 44: 229243. https://doi.org/10.1016/0168-1591(95)00616-ZCrossRefGoogle Scholar
Norton, T 2005 Sea turtle conservation in Georgia and an overview of the Georgia Sea Turtle Center on Jekyll Island, Georgia. Georgia Journal of Science 63: 208231Google Scholar
Ogden, J, Robinson, L, Witlock, K, Daganhardt, H and Cebula, R 1983 Diel foraging patterns in juvenile green turtles (Chelonia mydas) in St Croix United States Virgin Islands. Journal of Experimental Marine Biology and Ecology 66: 199205. https://doi.org/10.1016/0022-0981(83)90160-0CrossRefGoogle Scholar
Phillips, C, Jiang, Z, Hatton, A, Tribe, A, Bouar, M, Guerlin, M and Murray, P 2011 Environmental enrichment for captive eastern blue-tongue lizards, Tiliqua scincoides. Animal Welfare 20: 377384Google Scholar
Schofield, G, Katselidis, K, Pantis, J, Dimopoulos, P and Hays, G 2007 Female-female aggression: structure of interaction and outcome in loggerhead sea turtles. Marine Ecology Progress Series 336: 267274. https://doi.org/10.3354/meps336267CrossRefGoogle Scholar
Silvestre, A 2014 How to assess stress in reptiles. Journal of Exotic Pet Medicine 23: 240243. https://doi.org/10.1053/j.jepm.2014.06.004CrossRefGoogle Scholar
Smith, B and Litchfield, C 2010 An empirical case study examining effectiveness of environmental enrichment in two captive aus-tralian sea lions (Neophoca cinera). Journal of Applied Animal Welfare Science 13:407416. https://doi.org/10.1080/10888700903371863CrossRefGoogle Scholar
Stabenau, EK and Vietti, K 2003 The physiological effects of multiple forced submergences in loggerhead sea turtles (Caretta caretta). Fishery Bulletin 101(4): 889899Google Scholar
Stamper, AM, Harms, CA and Lewbart, GA 2017 Environment/water quality/biosecurity. In: Manire, CA, Norton, TM and Stacy, BA (eds) Sea Turtle Health & Rehabilitation pp 4560. J Ross Publishing, Incorporated: FL, USAGoogle Scholar
Tetzlaff, SJ, Sperry, JH and DeGregorio, BA 2018 Captive-reared juvenile box turtles innately prefer naturalistic habitat: Implications for translocation. Applied Animal Behaviour Science 204: 128133. https://doi.org/10.1016/j.applanim.2018.03.007CrossRefGoogle Scholar
Tetzlaff, SJ, Sperry, JH and DeGregorio, BA 2019a Trade-offs with growth and behavior for captive box turtles head-started with environmental enrichment. Diversity 11: 40. https://doi.org/10.3390/d11030040CrossRefGoogle Scholar
Tetzlaff, SJ, Sperry, JH, Kingsbury, BA and DeGregorio, BA 2019b Captive-rearing duration may be more important than environmental enrichment for enhancing turtle head-starting suc-cess. Global Ecology and Conservation 20: e00797. https://doi.org/10.1016/j.gecco.2019.e00797CrossRefGoogle Scholar
Therrien, C, Gaster, L, Cunningham-Smith, P and Manire, A 2007 Experimental evaluation of environmental enrichment of sea turtles. Zoo Biology 26: 407416. https://doi.org/10.1002/zoo.20145CrossRefGoogle Scholar
Tynes, VV 2010 Behavior of Exotic Pets. John Wiley & Sons: USAGoogle Scholar
Van de Merve, J, Ibrahim, K, Lee, S and Whittier, J 2009 Habitat use by green turtles (Chelonia mydas) nesting in Peninsular Malaysia: local & regional conservation implications. Wildlife Research 36: 367645. https://doi.org/10.1071/WR09099Google Scholar
Warwick, C, Arena, P, Lindley, S, Jessop, M and Steedman, C 2013 Assessing reptile welfare using behavioral criteria. In Practice 35: 123131. https://doi.org/10.1136/inp.f1197CrossRefGoogle Scholar
Whitham, J and Wielebnowski, N 2009 Animal-based welfare monitoring: using keeper ratings as an assessment tool. Zoo Biology 28: 545560. https://doi.org/10.1002/zoo.20281Google ScholarPubMed
Wickins-Drazilova, D 2006 Zoo animal welfare. Journal of Agricultural and Environmental Ethics 19: 2736. https://doi.org/10.1007/s10806-005-4380-2CrossRefGoogle Scholar
Wilkinson, A, Chan, H and Hall, G 2007 Spatial learning and mem-ory in the tortoise (Geochelone carbonaria). Journal of Comparative Psychology 121(4): 412418. https://doi.org/10.1037/0735-7036.121.4.412CrossRefGoogle ScholarPubMed
Wilkinson, A, Coward, S and Hall, G 2009 Visual and response-based navigation in the tortoise (Geochelone carbonaria). Animal Cognition 12: 779787. https://doi.org/10.1007/s10071-009-0237-9CrossRefGoogle ScholarPubMed
Wood, J and Wood, F 1981 Growth and digestibility for the green turtle (Chelonia mydas) fed diets containing varying protein levels. Aquaculture 25: 269274. https://doi.org/10.1016/0044-8486(81)90188-5CrossRefGoogle Scholar
Young, RJ 2013 Environmental Enrichment for Captive Animals. John Wiley & Sons: USAGoogle Scholar
Zamzow, J 1998 Cleaning symbioses between Hawaiian reef fish-es and green sea turtles, Chelonia mydas. In: Abreu-Grobois, FA, Briseño-Dueñas, R, Márquez, R and Sarti, L (eds) Proceedings of the Eighteenth International Sea Turtle Symposium. US Dep Commerce. NOAA Tech Memo NMFS-SEFSC-436 pp 235237. http://aquaticcom-mons.org/2131/1/Fish_TM_436.pdfGoogle Scholar