Tracking Epidermal Cortisol and Oxytocin in Managed Bottlenose Dolphins as Potential Non-Invasive Physiological Welfare Indicators
Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Ethics Statement
2.2. Study Area and Individuals
2.3. Sample Collection and Preparation
2.4. Sample Storage, Preparation, and Hormone Extraction
2.5. Hormone Detection and Assay Validation
2.6. Data Collection and Individual Welfare Profiling Based on Aquarium Reports
2.7. Data Management
2.8. Statistical Analyses
3. Results
3.1. Assay Validation
3.2. Descriptive Overview, Individual Variation, and Correlation of Epidermal Cortisol and Oxytocin Concentrations
3.3. Descriptive Analysis of Environmental and Welfare-Related Predictors
3.4. Effects of Environmental and Welfare-Related Predictors on Epidermal Cortisol Concentrations at Different Time Lags
3.5. Effects of Environmental and Welfare-Related Predictors on Epidermal Oxytocin Concentrations at Different Time Lags
4. Discussion
4.1. Assay and Method Validation
4.2. Descriptive Overview and Correlation Between Epidermal Cortisol and Oxytocin Concentrations
4.3. Effects of Environmental and Welfare-Related Predictors on Epidermal Cortisol Concentrations
4.4. Effects of Environmental and Welfare-Related Predictors on Epidermal Oxytocin Concentrations
4.5. Effects of Temporal Dynamics of Cortisol and Oxytocin Incorporation into the Epidermis
4.6. Study Limitations and Future Directions
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Abbreviations
ACTH | Adrenocorticotropic hormone |
ECC | Epidermal cortisol concentration |
EOC | Epidermal oxytocin concentration |
HPA | Hypothalamic–pituitary–adrenal axis |
KW | Kruskal–Wallis |
LM | Linear Model |
References
- Clegg, I.L.K. What does the future hold for the public display of cetaceans? J. Appl. Anim. Ethics Res. 2021, 3, 240–278. [Google Scholar] [CrossRef]
- Grimm, D. Are dolphins too smart for captivity? Science 2011, 332, 526–529. [Google Scholar] [CrossRef] [PubMed]
- van der Meer, L.; Kasdan, I.; Galvin, J. The importance of evidence, animal-based measures, and the rule of law to ensure good animal welfare. Aquat. Mamm. 2018, 44, 142–149. [Google Scholar] [CrossRef]
- Avila, I.C.; Kaschner, K.; Dormann, C.F. Current global risks to marine mammals: Taking stock of the threats. Biol. Conserv. 2018, 221, 44–58. [Google Scholar] [CrossRef]
- Whitham, J.C.; Wielebnowski, N.C. New directions for zoo animal welfare science. Appl. Anim. Behav. Sci. 2013, 147, 247–260. [Google Scholar] [CrossRef]
- Brando, S.; Broom, D.M.; Acasuso-Rivero, C.; Clark, F. Optimal marine mammal welfare under human care: Current efforts and future directions. Behav. Process. 2018, 156, 16–36. [Google Scholar] [CrossRef]
- Clegg, I.L.K.; Butterworth, A. Assessing the welfare of cetacea. In Marine Mammal Welfare; Butterworth, A., Ed.; Springer: Cham, Switzerland, 2017; pp. 183–211. [Google Scholar] [CrossRef]
- Clegg, I.L.K.; Rödel, H.G.; Mercera, B.; Van der Heul, S.; Schrijvers, T.; De Laender, P.; Delfour, F. Dolphins’ willingness to participate (WtP) in positive reinforcement training as a potential welfare indicator, where WtP predicts early changes in health status. Front. Psychol. 2019, 10, 2112. [Google Scholar] [CrossRef]
- Kagan, R.; Carter, S.; Allard, S. A universal animal welfare framework for zoos. J. Appl. Anim. Welf. Sci. 2015, 18 (Suppl. S1), S1–S10. [Google Scholar] [CrossRef]
- Miller, L.J.; Mellen, J.; Greer, T.; Kuczaj, S.A. The effects of education programmes on Atlantic bottlenose dolphin (Tursiops truncatus) behaviour. Anim. Welf. 2011, 20, 159–172. [Google Scholar] [CrossRef]
- Broom, D.M.; Johnson, K.G. Stress and Animal Welfare: Key Issues in the Biology of Humans and Other Animals, 2nd ed.; Springer: Cham, Switzerland, 2019. [Google Scholar] [CrossRef]
- Moberg, G.P. (Ed.) Biological response to stress: Key to assessment of animal well-being? In Animal Stress; American Physiological Society: Bethesda, MD, USA, 1985; pp. 27–49. [Google Scholar] [CrossRef]
- Reeder, D.M.; Kramer, K.M. Stress in free-ranging mammals: Integrating physiology, ecology and natural history. J. Mammal. 2005, 86, 225–235. [Google Scholar] [CrossRef]
- Ralph, C.R.; Tilbrook, A.J. The hypothalamo–pituitary–adrenal axis and sex steroid interactions: Implications for sexual function and fertility. Front. Endocrinol. 2016, 7, 156. [Google Scholar] [CrossRef]
- Sapolsky, R.M.; Romero, L.M.; Munck, A.U. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr. Rev. 2000, 21, 55–89. [Google Scholar] [CrossRef]
- Rault, J.L.; van den Munkhof, M.; Buisman-Pijlman, F.T. Oxytocin as an indicator of psychological and social well-being in domesticated animals: A critical review. Front. Psychol. 2017, 8, 1521. [Google Scholar] [CrossRef]
- Hruby, V.J.; Chow, M.S.; Smith, D.D. Conformational and structural considerations in oxytocin-receptor binding and biological activity. Annu. Rev. Pharmacol. Toxicol. 1990, 30, 501–534. [Google Scholar] [CrossRef] [PubMed]
- Lee, H.J.; Macbeth, A.H.; Pagani, J.H.; Young, W.S. Oxytocin: The great facilitator of life. Prog. Neurobiol. 2009, 88, 127–151. [Google Scholar] [CrossRef] [PubMed]
- Chang, S.W.C.; Barter, J.W.; Ebitz, R.B.; Watson, K.K.; Platt, M.L. Inhaled oxytocin amplifies both vicarious reinforcement and self reinforcement in rhesus macaques. Proc. Natl. Acad. Sci. USA 2012, 109, 959–964. [Google Scholar] [CrossRef] [PubMed]
- Ross, H.E.; Young, L.J. Oxytocin and the neural mechanisms regulating social cognition and affiliative behavior. Front. Neuroendocrinol. 2009, 30, 534–547. [Google Scholar] [CrossRef]
- Churchland, P.S.; Winkielman, P. Modulating social behavior with oxytocin: How does it work? What does it mean? Horm. Behav. 2012, 61, 392–399. [Google Scholar] [CrossRef]
- Gerber, L.; Connor, R.C.; Allen, S.J.; Horlacher, K.; King, S.L.; Sherwin, W.B.; Willems, E.P.; Wittwer, S.; Krützen, M. Social integration influences fitness in allied male dolphins. Curr. Biol. 2022, 32, 1664–1669.e3. [Google Scholar] [CrossRef]
- Seyfarth, R.M.; Cheney, D.L. The evolutionary origins of friendship. Annu. Rev. Psychol. 2012, 63, 153–177. [Google Scholar] [CrossRef]
- Crockford, C.; Wittig, R.M.; Langergraber, K.E.; Ziegler, T.E.; Zuberbühler, K.; Deschner, T. Endogenous peripheral oxytocin measures can give insight into the dynamics of social relationships: A review. Front. Behav. Neurosci. 2014, 8, 68. [Google Scholar] [CrossRef]
- Champagne, C.D.; Kellar, N.M.; Crocker, D.E.; Wasser, S.K.; Booth, R.K.; Trego, M.L.; Houser, D.S. Blubber cortisol qualitatively reflects circulating cortisol concentrations in bottlenose dolphins. Mar. Mamm. Sci. 2017, 33, 134–153. [Google Scholar] [CrossRef]
- Champagne, C.D.; Houser, D.S.; Costa, D.P.; Crocker, D.E. Comprehensive endocrine response to acute stress in the bottlenose dolphin from serum, blubber, and feces. Gen. Comp. Endocrinol. 2018, 266, 178–193. [Google Scholar] [CrossRef] [PubMed]
- Agustí, C.; Manteca, X.; García-Párraga, D.; Tallo-Parra, O. Validating a non-invasive method for assessing cortisol concentrations in scraped epidermal skin from common bottlenose dolphins and belugas. Animals 2024, 14, 1377. [Google Scholar] [CrossRef] [PubMed]
- Trumble, S.J.; Norman, S.A.; Crain, D.D.; Mansouri, F.; Winfield, Z.C.; Sabin, R.; Potter, C.W.; Gabriele, C.M.; Usenko, S. Baleen whale cortisol levels reveal a physiological response to 20th-century whaling. Nat. Commun. 2018, 9, 4587. [Google Scholar] [CrossRef]
- Henderson, G.L. Mechanisms of drug incorporation into hair. Forensic Sci. Int. 1993, 63, 19–29. [Google Scholar] [CrossRef]
- Bechshoft, T.; Wright, A.J.; Styrishave, B.; Houser, D.S. Measuring and validating concentrations of steroid hormones in the skin of bottlenose dolphins. Conserv. Physiol. 2020, 8, coaa032. [Google Scholar] [CrossRef]
- Wong, C.H.; Tsai, M.A.; Ko, F.C.; Wang, J.H.; Xue, Y.J.; Yang, W.C. Skin cortisol and acoustic activity: Potential tools to evaluate stress and welfare in captive cetaceans. Animals 2023, 13, 1521. [Google Scholar] [CrossRef]
- Agustí, C.; Guix, L.; Carbajal, A.; Domingo, M.; López-Béjar, M.; Manteca, X.; Tallo-Parra, O. Physiological welfare indicators in wild cetaceans: Epidermal cortisol and oxytocin concentrations in stranded striped dolphins. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2025, 301, 111793. [Google Scholar] [CrossRef]
- Cirillo, N.; Prime, S.S. Keratinocytes synthesize and activate cortisol: First characterization of a novel epidermal glucocorticoid system. J. Cell. Biochem. 2011, 112, 1499–1505. [Google Scholar] [CrossRef]
- Robinson, K.J.; Ternes, K.; Hazon, N.; Wells, R.S.; Janik, V.M. Bottlenose dolphin calves have multi-year elevations of plasma oxytocin compared to all other age classes. Gen. Comp. Endocrinol. 2020, 286, 113323. [Google Scholar] [CrossRef]
- Jeong, Y.K.; Oh, Y.I.; Song, K.H.; Seo, K.W. Evaluation of salivary vasopressin as an acute stress biomarker in healthy dogs with stress due to noise and environmental challenges. BMC Vet. Res. 2020, 16, 331. [Google Scholar] [CrossRef]
- Gröschl, M. Current status of salivary hormone analysis. Clin. Chem. 2008, 54, 1759–1769. [Google Scholar] [CrossRef] [PubMed]
- Deing, V.; Roggenkamp, D.; Kühnl, J.; Gruschka, A.; Stäb, F.; Wenck, H.; Bürkle, A.; Neufang, G. Oxytocin modulates proliferation and stress responses of human skin cells: Implications for atopic dermatitis. Exp. Dermatol. 2013, 22, 399–405. [Google Scholar] [CrossRef] [PubMed]
- López-Arjona, M.; Tecles, F.; Mateo, S.V.; Contreras-Aguilar, M.D.; Martínez-Miró, S.; Cerón, J.J.; Martínez-Subiela, S. A procedure for oxytocin measurement in hair of pig: Analytical validation and a pilot application. Biology 2021, 10, 527. [Google Scholar] [CrossRef]
- Hunt, K.E.; Moore, M.J.; Rolland, R.M.; Kellar, N.M.; Hall, A.J.; Kershaw, J.; Raverty, S.A.; Davis, C.E.; Yeates, L.C.; Fauquier, D.A.; et al. Overcoming the challenges of studying conservation physiology in large whales: A review of available methods. Conserv. Physiol. 2013, 1, cot006. [Google Scholar] [CrossRef]
- Beaulieu, M. Capturing wild animal welfare: A physiological perspective. Biol. Rev. 2024, 99, 1–22. [Google Scholar] [CrossRef]
- Mellor, D.J.; Beausoleil, N.J. Extending the ‘Five Domains’ model for animal welfare assessment to incorporate positive welfare states. Anim. Welf. 2015, 24, 241–253. [Google Scholar] [CrossRef]
- Mellor, D.J.; Beausoleil, N.J.; Littlewood, K.E.; McLean, A.N.; McGreevy, P.D.; Jones, B.; Wilkins, C. The 2020 Five Domains Model: Including human–animal interactions in assessments of animal welfare. Animals 2020, 10, 1870. [Google Scholar] [CrossRef]
- Goymann, W. On the use of non-invasive hormone research in uncontrolled, natural environments: The problem with sex, diet, metabolic rate and the individual. Methods Ecol. Evol. 2012, 3, 757–765. [Google Scholar] [CrossRef]
- Touma, C.; Palme, R. Measuring fecal glucocorticoid metabolites in mammals and birds: The importance of validation. Ann. N. Y. Acad. Sci. 2005, 1046, 54–74. [Google Scholar] [CrossRef]
- Kucheravy, C.; Trana, M.R.; Watt, C.A.; Ferguson, S. Blubber cortisol in four Canadian beluga whale populations is unrelated to diet. Mar. Ecol. Prog. Ser. 2022, 698, 171–183. [Google Scholar] [CrossRef]
- Trana, M.R.; Roth, J.D.; Tomy, G.T.; Anderson, W.G.; Ferguson, S.H. Increased blubber cortisol in ice-entrapped beluga whales (Delphinapterus leucas). Polar Biol. 2016, 39, 1563–1569. [Google Scholar] [CrossRef]
- Ramirez, K. Marine mammal training: The history of training animals for medical behaviors and keys to their success. Vet. Clin. N. Am. Exot. Anim. Pract. 2012, 15, 413–423. [Google Scholar] [CrossRef] [PubMed]
- Würsig, B.; Thewissen, J.G.M.; Kovacs, K.M. (Eds.) Encyclopedia of Marine Mammals, 3rd ed.; Academic Press: London, UK, 2018. [Google Scholar]
- Yeates, L.C.; Houser, D.S. Thermal tolerance in bottlenose dolphins (Tursiops truncatus). J. Exp. Biol. 2008, 211, 3249–3257. [Google Scholar] [CrossRef]
- European Association for Aquatic Mammals (EAAM). Standards and Guidelines for the Management of Aquatic Mammals Under Human Care, 2021 ed.; EAAM: Brussels, Belgium, 2019. [Google Scholar]
- López-Arjona, M.; Tecles, F.; Mateo, S.V.; Contreras-Aguilar, M.D.; Martínez-Miró, S.; Cerón, J.J.; Martínez-Subiela, S. Measurement of cortisol, cortisone and 11β-hydroxysteroid dehydrogenase type 2 activity in hair of sows during different phases of the reproductive cycle. Vet. J. 2020, 259, 105458. [Google Scholar] [CrossRef]
- Reimers, T.J.; Lamb, S.V. Radioimmunoassay of hormones in laboratory animals for diagnostics and research. Lab. Anim. 1991, 20, 32–38. [Google Scholar]
- Clegg, I.L.; Borger-Turner, J.L.; Eskelinen, H.C. C-Well: The development of a welfare assessment index for captive bottlenose dolphins (Tursiops truncatus). Anim. Welf. 2015, 24, 267–282. [Google Scholar] [CrossRef]
- Baumgartner, K.; Hüttner, T.; Clegg, I.L.K.; Hartmann, M.G.; Garcia-Párraga, D.; Manteca, X.; Delfour, F. Dolphin-WET—Development of a welfare evaluation tool for bottlenose dolphins (Tursiops truncatus) under human care. Animals 2024, 14, 701. [Google Scholar] [CrossRef]
- Boys, R.M.; Beausoleil, N.J.; Pawley, M.D.; Littlewood, K.E.; Betty, E.L.; Stockin, K.A. Fundamental concepts, knowledge gaps and key concerns relating to welfare and survival of stranded cetaceans. Diversity 2022, 14, 338. [Google Scholar] [CrossRef]
- Harvey, A.M.; Beausoleil, N.J.; Ramp, D.; Mellor, D.J. Mental experiences in wild animals: Scientifically validating measurable welfare indicators in free-roaming horses. Animals 2023, 13, 1507. [Google Scholar] [CrossRef] [PubMed]
- Johnson, S.P.; Venn-Watson, S.K.; Cassle, S.E.; Smith, C.R.; Jensen, E.D.; Ridgway, S.H. Use of phlebotomy treatment in Atlantic bottlenose dolphins with iron overload. J. Am. Vet. Med. Assoc. 2009, 235, 194–200. [Google Scholar] [CrossRef] [PubMed]
- Waples, K.A.; Gales, N.J. Evaluating and minimising social stress in the care of captive bottlenose dolphins (Tursiops aduncus). Zoo Biol. 2002, 21, 5–26. [Google Scholar] [CrossRef]
- Couquiaud, L. Whales, dolphins, and porpoises: Presentation of the cetaceans. Aquat. Mamm. 2005, 31, 288–310. [Google Scholar] [CrossRef]
- Colitz, C.M.H.; Bailey, J.E.; Mejia-Fava, J.C. Cetacean and pinniped ophthalmology. In CRC Handbook of Marine Mammal Medicine, 3rd ed.; Gulland, F.M.D., Dierauf, L.A., Whitman, K.L., Eds.; CRC Press: Boca Raton, FL, USA, 2018; pp. 517–536. [Google Scholar]
- Graham, M.S.; Dow, P.R. Dental care for a captive killer whale (Orcinus orca). Zoo Biol. 1990, 9, 325–330. [Google Scholar] [CrossRef]
- Venn-Watson, S.K.; Daniels, R.; Smith, C.R. Thirty year retrospective evaluation of pneumonia in a bottlenose dolphin (Tursiops truncatus) population. Dis. Aquat. Organ. 2012, 99, 237–242. [Google Scholar] [CrossRef]
- St. Leger, J.A.; Raverty, S.; Mena, A. Cetacea. In Pathology of Wildlife and Zoo Animals; Terio, K.A., McAloose, D., St. Leger, J., Eds.; Academic Press: Cambridge, MA, USA, 2018; pp. 533–568. [Google Scholar] [CrossRef]
- Gulland, F.M.D.; Dierauf, L.A.; Whitman, K.L. (Eds.) CRC Handbook of Marine Mammal Medicine, 3rd ed.; CRC Press: Boca Raton, FL, USA, 2018. [Google Scholar]
- Kuczaj, S.A.; Highfill, L.E.; Makecha, R.N.; Byerly, H.C. Why do dolphins smile? A comparative perspective on dolphin emotions and emotional expressions. In Emotions of Animals and Humans: Comparative Perspectives; Watanabe, S., Kuczaj, S.A., Eds.; Springer: Tokyo, Japan, 2013; pp. 63–85. [Google Scholar] [CrossRef]
- Delfour, F.; Monreal-Pawlowsky, T.; Vaicekauskaite, R.; Pilenga, C.; Garcia-Parraga, D.; Rödel, H.G.; García Caro, N.; Perlado Campos, E.; Mercera, B. Dolphin welfare assessment under professional care: “Willingness to participate”, an indicator significantly associated with six potential “alerting factors”. J. Zool. Bot. Gard. 2020, 1, 42–60. [Google Scholar] [CrossRef]
- Huettner, T.; Dollhaeupl, S.; Simon, R.; Baumgartner, K.; von Fersen, L. Activity budget comparisons using long-term observations of a group of bottlenose dolphins (Tursiops truncatus) under human care: Implications for animal welfare. Animals 2021, 11, 2107. [Google Scholar] [CrossRef]
- Nollens, H.H.; Venn-Watson, S.; Gili, C.; McBain, J.F. Cetacean medicine. In CRC Handbook of Marine Mammal Medicine, 3rd ed.; Gulland, F.M.D., Dierauf, L.A., Whitman, K.L., Eds.; CRC Press: Boca Raton, FL, USA, 2018; pp. 887–908. [Google Scholar]
- Hicks, B.D.; St Aubin, D.J.S.; Geraci, J.R.; Brown, W.R. Epidermal growth in the bottlenose dolphin (Tursiops truncatus). J. Investig. Dermatol. 1985, 85, 60–63. [Google Scholar] [CrossRef]
- Zmijewski, M.A.; Slominski, A.T. Neuroendocrinology of the skin: An overview and selective analysis. Dermato-Endocrinology 2011, 3, 3–10. [Google Scholar] [CrossRef]
- Quintana, D.S.; Westlye, L.T.; Smerud, K.T.; Mahmoud, R.A.; Andreassen, O.A.; Djupesland, P.G. Saliva oxytocin measures do not reflect peripheral plasma concentrations after intranasal oxytocin administration in men. Horm. Behav. 2018, 102, 85–92. [Google Scholar] [CrossRef]
- R Core Team. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2024; Available online: https://www.R-project.org/ (accessed on 2 March 2025).
- Bechshøft, T.Ø.; Wright, A.J.; Weisser, J.J.; Teilmann, J.; Dietz, R.; Hansen, M.; Björklund, E.; Styrishave, B. Developing a new research tool for use in free-ranging cetaceans: Recovering cortisol from harbour porpoise skin. Conserv. Physiol. 2015, 3, cov016. [Google Scholar] [CrossRef] [PubMed]
- Jung, Y.; Yoo, G.; Yang, K.; Yoon, M. Exploring the relationship between plasma and salivary levels of oxytocin, vasopressin, and cortisol in beagles: A preliminary study. Domest. Anim. Endocrinol. 2025, 92, 106937. [Google Scholar] [CrossRef] [PubMed]
- Hoge, E.A.; Pollack, M.H.; Kaufman, R.E.; Zak, P.J.; Simon, N.M. Oxytocin levels in social anxiety disorder. CNS Neurosci. Ther. 2008, 14, 165–170. [Google Scholar] [CrossRef] [PubMed]
- Taylor, S.E.; Saphire-Bernstein, S.; Seeman, T.E. Are plasma oxytocin in women and plasma vasopressin in men biomarkers of distressed pair-bond relationships? Psychol. Sci. 2010, 21, 3–7. [Google Scholar] [CrossRef]
- Chen, S.; Sato, S. Role of oxytocin in improving the welfare of farm animals—A review. Asian-Australas. J. Anim. Sci. 2017, 30, 449–454. [Google Scholar] [CrossRef]
- Sutherland, M.A.; Tops, M. Possible involvement of oxytocin in modulating the stress response in lactating dairy cows. Front. Psychol. 2014, 5, 951. [Google Scholar] [CrossRef]
- Romero, L.M. Seasonal changes in plasma glucocorticoid concentrations in free-living vertebrates. Gen. Comp. Endocrinol. 2002, 128, 1–24. [Google Scholar] [CrossRef]
- Boggs, A.S.; Ragland, J.M.; Zolman, E.S.; Schock, T.B.; Morey, J.S.; Galligan, T.M.; Schwacke, L.H. Remote blubber sampling paired with liquid chromatography–tandem mass spectrometry for steroidal endocrinology in free-ranging bottlenose dolphins (Tursiops truncatus). Gen. Comp. Endocrinol. 2019, 281, 164–172. [Google Scholar] [CrossRef]
- Funasaka, N.; Yoshioka, M.; Suzuki, M.; Ueda, K.; Miyahara, H.; Uchida, S. Seasonal difference of diurnal variations in serum melatonin, cortisol, testosterone, and rectal temperature in Indo-Pacific bottlenose dolphins (Tursiops aduncus). Aquat. Mamm. 2011, 37, 433–442. [Google Scholar] [CrossRef]
- Wells, R.S.; Hohn, A.A.; Scott, M.D.; Sweeney, J.C.; Townsend, F.I., Jr.; Allen, J.B.; Fauquier, D.A.; Rowles, T.K. Life history, reproductive, and demographic parameters for bottlenose dolphins (Tursiops truncatus) in Sarasota Bay, Florida. Front. Mar. Sci. 2025, 12, 1531528. [Google Scholar] [CrossRef]
- Biancani, B. Use of Faecal Samples to Monitor the Oestrous Cycle, Reproductive Status and Adrenal Gland Activity in the Bottlenose Dolphin (Tursiops truncatus). Ph.D. Thesis, University of Padua, Padua, Italy, 2008. Available online: http://paduaresearch.cab.unipd.it/363/ (accessed on 15 March 2025).
- Mercera, K.; Pilot-Storck, F.; Mercera, B.; Gilbert, C.; Delfour, F. Exploration of fecal glucocorticoid metabolites in the bottlenose dolphin (Tursiops truncatus) under human care by enzyme immunoassay. Aquat. Mamm. 2021, 47, 227–238. [Google Scholar] [CrossRef]
- Noren, D.P.; Williams, T.M.; Berry, P.; Butler, E. Thermoregulation during swimming and diving in bottlenose dolphins, Tursiops truncatus. J. Comp. Physiol. B 1999, 169, 93–99. [Google Scholar] [CrossRef] [PubMed]
- Hosey, G.; Melfi, V.; Pankhurst, S. Zoo Animals: Behaviour, Management and Welfare; Oxford University Press: New York, NY, USA, 2009. [Google Scholar]
- Quadros, S.; Goulart, V.D.; Passos, L.; Vecci, M.A.; Young, R.J. Zoo visitor effect on mammal behaviour: Does noise matter? Appl. Anim. Behav. Sci. 2014, 156, 78–84. [Google Scholar] [CrossRef]
- Iwata, E.; Terayama, H.; Ishikawa, H.; Suzuki, S.; Sakaguchi, R.; Takahashi, E.; Asaki, H. Analysis of the behavioral characteristics and plasma cortisol levels in captive dolphins participating in human–dolphin interaction programs. Anim. Behav. Manag. 2022, 58, 182–193. [Google Scholar]
- Matsushiro, M.; Kurono, H.; Yamamoto, K.; Kooriyama, T. Cortisol changes in bottlenose dolphins in the dolphin interactive program. Jpn. J. Vet. Res. 2021, 69, 99–108. [Google Scholar] [CrossRef]
- Delfour, F.; Vaicekauskaite, R.; García-Párraga, D.; Pilenga, C.; Serres, A.; Brasseur, I.; Pascaud, A.; Perlado-Campos, E.; Sánchez-Contreras, G.J.; Baumgartner, K.; et al. Behavioural diversity study in bottlenose dolphin groups and its implications for welfare assessments. Animals 2021, 11, 1715. [Google Scholar] [CrossRef]
- Serres, A.; Robeck, T.; Deng, X.; Steinman, K.; Hao, Y.; Wang, D. Social, reproductive and contextual influences on fecal glucocorticoid metabolites in captive Yangtze finless porpoises (Neophocaena asiaeorientalis asiaeorientalis) and bottlenose dolphins (Tursiops truncatus). J. Zool. Bot. Gard. 2020, 1, 24–41. [Google Scholar] [CrossRef]
- Bruni, G.; Dal Pra, P.; Dotti, M.T.; Segre, G. Plasma ACTH and cortisol levels in benzodiazepine treated rats. Pharmacol. Res. Commun. 1980, 12, 163–175. [Google Scholar] [CrossRef]
- Tormey, W.P.; Dolphin, C.; Darragh, A.S. The effects of diazepam on sleep, and on the nocturnal release of growth hormone, prolactin, ACTH, and cortisol. Br. J. Clin. Pharmacol. 1979, 8, 90–92. [Google Scholar] [CrossRef]
- Fukuda, M.; Takazawa, S.; Nakagome, K.; Iwanami, A.; Hata, A.; Kasai, K.; Hiramatsu, K.I. Decreased plasma cortisol level during alprazolam treatment of panic disorder: A case report. Prog. Neuropsychopharmacol. Biol. Psychiatry 1998, 22, 909–915. [Google Scholar] [CrossRef]
- Gram, L.; Christensen, P. Benzodiazepine suppression of cortisol secretion: A measure of anxiolytic activity? Pharmacopsychiatry 1986, 19, 19–22. [Google Scholar] [CrossRef] [PubMed]
- Mody, I.; Maguire, J. The reciprocal regulation of stress hormones and GABA(A) receptors. Front. Cell Neurosci. 2012, 6, 4. [Google Scholar] [CrossRef] [PubMed]
- Kastelein, R.A.; Bakker, M.J.; Jennings, N.; Covi-Dijkhuizen, J. Evaluating the use of diazepam in stranded dolphins and porpoises for husbandry and veterinary purposes. Aquat. Mamm. 2023, 49, 94–103. [Google Scholar] [CrossRef]
- Fischer, B.D.; Licata, S.C.; Edwankar, R.V.; Wang, Z.J.; Huang, S.; He, X.; Yu, J.; Zhou, H.; Johnson, E.M., Jr.; Cook, J.M. Anxiolytic-like effects of 8-acetylene imidazobenzodiazepines in a rhesus monkey conflict procedure. Neuropharmacology 2010, 59, 612–618. [Google Scholar] [CrossRef] [PubMed]
- Rowlett, J.K.; Platt, D.M.; Lelas, S.; Atack, J.R.; Dawson, G.R. Different GABAA receptor subtypes mediate the anxiolytic, abuse-related, and motor effects of benzodiazepine-like drugs in primates. Proc. Natl. Acad. Sci. USA 2005, 102, 915–920. [Google Scholar] [CrossRef]
- Kezar, S.M.; Baker, K.C.; Russell-Lodrigue, K.E.; Bohm, R.P. Single-dose diazepam administration improves pairing success of unfamiliar adult male rhesus macaques (Macaca mulatta). J. Am. Assoc. Lab. Anim. Sci. 2022, 61, 173–180. [Google Scholar] [CrossRef]
- Winslow, J.T.; Noble, P.L.; Lyons, C.K.; Sterk, S.M.; Insel, T.R. Rearing effects on cerebrospinal fluid oxytocin concentration and social buffering in rhesus monkeys. Neuropsychopharmacology 2003, 28, 910–918. [Google Scholar] [CrossRef]
- Champagne, C.D.; Crocker, D.E.; Fowler, M.A.; Houser, D.S. Fasting physiology of the pinnipeds: The challenges of fasting while maintaining high energy expenditure and nutrient delivery for lactation. In Comparative Physiology of Fasting, Starvation, and Food Limitation; McCue, M.D., Ed.; Springer: Berlin, Germany, 2012; pp. 309–336. [Google Scholar] [CrossRef]
- Guinet, C.; Servera, N.; Mangin, S.; Georges, J.Y.; Lacroix, A. Change in plasma cortisol and metabolites during the attendance period ashore in fasting lactating subantarctic fur seals. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2004, 137, 523–531. [Google Scholar] [CrossRef]
- Agustí, C.; Carbajal, A.; Olvera-Maneu, S.; Domingo, M.; Lopez-Bejar, M. Blubber and serum cortisol concentrations as indicators of the stress response and overall health status in striped dolphins. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2022, 272, 111268. [Google Scholar] [CrossRef]
- Kershaw, J.L.; Sherrill, M.; Davison, N.J.; Brownlow, A.; Hall, A.J. Evaluating morphometric and metabolic markers of body condition in a small cetacean, the harbor porpoise (Phocoena phocoena). Ecol. Evol. 2017, 7, 3494–3506. [Google Scholar] [CrossRef] [PubMed]
- Bergendahl, M.; Vance, M.L.; Iranmanesh, A.; Thorner, M.O.; Veldhuis, J.D. Fasting as a metabolic stress paradigm selectively amplifies cortisol secretory burst mass and delays the time of maximal nyctohemeral cortisol concentrations in healthy men. J. Clin. Endocrinol. Metab. 1996, 81, 692–699. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Exton, J.H.; Corbin, J.G.; Harper, S.C. Control of gluconeogenesis in liver. V. Effects of fasting, diabetes, and glucagon on lactate and endogenous metabolism in the perfused rat liver. J. Biol. Chem. 1972, 247, 4996–5003. [Google Scholar] [CrossRef] [PubMed]
- Hainer, V.; Stich, V.; Kunesova, M.; Parizkova, J.; Zak, A.; Wernischova, V. Effect of 4-wk treatment of obesity by very-low-calorie diet on anthropometric, metabolic, and hormonal indexes. Am. J. Clin. Nutr. 1992, 56, 281S–282S. [Google Scholar] [CrossRef]
- Wabitsch, M.; Hauner, H.; Heinze, E.; Böckmann, A.; Benz, R.; Mayer, H.; Teller, W. Body fat distribution and steroid hormone concentrations in obese adolescent girls before and after weight reduction. J. Clin. Endocrinol. Metab. 1995, 80, 3469–3475. [Google Scholar] [CrossRef]
- Johnstone, A.M.; Faber, P.; Andrew, R.; Gibney, E.R.; Elia, M.; Lobley, G.; Walker, B.R. Influence of short-term dietary weight loss on cortisol secretion and metabolism in obese men. Eur. J. Endocrinol. 2004, 150, 185–194. [Google Scholar] [CrossRef]
- Broom, D.M. Cortisol: Often not the best indicator of stress and poor welfare. Physiol. News 2017, 107, 30–32. [Google Scholar] [CrossRef]
- Bergfelt, D.R.; Vences, M.; Smallcomb, M.; Sanchez-Okrucky, R.; Canales, R. Circulating concentrations of cortisol encompassing controlled cessation of suckling during weaning under managed care in cow and calf bottlenose dolphins (Tursiops truncatus). Aquat. Mamm. 2023, 49, 362–372. [Google Scholar] [CrossRef]
- Ugaz, C.; Valdez, R.A.; Romano, M.C.; Galindo, F. Behavior and salivary cortisol in captive dolphins. J. Vet. Behav. 2013, 8, 285–290. [Google Scholar] [CrossRef]
- Biancani, B.; Da Dalt, L.; Gallina, G.; Capolongo, F.; Gabai, G. Fecal cortisol radioimmunoassay to monitor adrenal gland activity in the bottlenose dolphin (Tursiops truncatus) under human care. Mar. Mamm. Sci. 2017, 33, 1014–1034. [Google Scholar] [CrossRef]
- Goldstein, J.D.; Schaefer, A.M.; McCulloch, S.D.; Fair, P.A.; Bossart, G.D.; Reif, J.S. Clinicopathologic findings from Atlantic bottlenose dolphins (Tursiops truncatus) with cytologic evidence of gastric inflammation. J. Zoo Wildl. Med. 2012, 43, 730–738. [Google Scholar] [CrossRef]
- Fair, P.A.; Schaefer, A.M.; Romano, T.A.; Bossart, G.D.; Lamb, S.V.; Reif, J.S. Stress response of wild bottlenose dolphins (Tursiops truncatus) during capture–release health assessment studies. Gen. Comp. Endocrinol. 2014, 206, 203–212. [Google Scholar] [CrossRef] [PubMed]
- Galligan, T.M.; Schwacke, L.H.; Houser, D.S.; Wells, R.S.; Rowles, T.; Boggs, A.S. Characterization of circulating steroid hormone profiles in the bottlenose dolphin (Tursiops truncatus) by liquid chromatography–tandem mass spectrometry (LC–MS/MS). Gen. Comp. Endocrinol. 2018, 263, 80–91. [Google Scholar] [CrossRef] [PubMed]
- Hart, L.B.; Wells, R.S.; Kellar, N.; Balmer, B.C.; Hohn, A.A.; Lamb, S.V.; Schwacke, L.H. Adrenal hormones in common bottlenose dolphins (Tursiops truncatus): Influential factors and reference intervals. PLoS ONE 2015, 10, e0127432. [Google Scholar] [CrossRef] [PubMed]
- Monreal-Pawlowsky, T.; Carbajal, A.; Tallo-Parra, O.; Sabés-Alsina, M.; Monclús, L.; Almunia, J.; Lopez-Bejar, M. Daily salivary cortisol levels in response to stress factors in captive common bottlenose dolphins (Tursiops truncatus): A potential welfare indicator. Vet. Rec. 2017, 180, 593. [Google Scholar] [CrossRef]
- Yang, W.C.; Chen, C.F.; Chuah, Y.C.; Zhuang, C.R.; Chen, I.H.; Mooney, T.A.; Stott, J.; Blanchard, M.; Jen, I.F.; Chou, L.S. Anthropogenic sound exposure-induced stress in captive dolphins and implications for cetacean health. Front. Mar. Sci. 2021, 8, 606736. [Google Scholar] [CrossRef]
- Ashley, N.T.; Barboza, P.S.; Macbeth, B.J.; Janz, D.M.; Cattet, M.R.L.; Booth, R.K.; Wasser, S.K. Glucocorticosteroid concentrations in feces and hair of captive caribou and reindeer following adrenocorticotropic hormone challenge. Gen. Comp. Endocrinol. 2011, 172, 382–391. [Google Scholar] [CrossRef]
- Sandøe, P.; Corr, S.A.; Lund, T.B.; Forkman, B. Aggregating animal welfare indicators: Can it be done in a transparent and ethically robust way? Anim. Welf. 2019, 28, 67–76. [Google Scholar] [CrossRef]
- Dickens, M.J.; Romero, L.M. A consensus endocrine profile for chronically stressed wild animals does not exist. Gen. Comp. Endocrinol. 2013, 191, 177–189. [Google Scholar] [CrossRef]
- Noda, K.; Aoki, M.; Akiyoshi, H.; Asaki, H.; Ogata, T.; Yamauchi, K.; Shimada, T.; Ohashi, F. Effect of bovine lactoferrin on the immune responses of captive bottlenosed dolphins (Tursiops truncatus) being transported over long distances. Vet. Rec. 2006, 159, 885–888. [Google Scholar] [CrossRef]
- Cavanaugh, J.; Carp, S.B.; Rock, C.M.; French, J.A. Oxytocin modulates behavioral and physiological responses to a stressor in marmoset monkeys. Psychoneuroendocrinology 2016, 66, 22–30. [Google Scholar] [CrossRef] [PubMed]
- Bienboire-Frosini, C.; Bracco, E.; Chabaud, C.; Pageat, P. Inaccuracies in oxytocin assays: The Trojan horse of solid-phase extraction procedures? Psychoneuroendocrinology 2024, 160, 106865. [Google Scholar] [CrossRef]
- McCullough, M.E.; Churchland, P.S.; Mendez, A.J. Problems with measuring peripheral oxytocin: Can the data on oxytocin and human behavior be trusted? Neurosci. Biobehav. Rev. 2013, 37, 1485–1492. [Google Scholar] [CrossRef]
- Rault, J.L. Effects of positive and negative human contacts and intranasal oxytocin on cerebrospinal fluid oxytocin. Psychoneuroendocrinology 2016, 69, 60–66. [Google Scholar] [CrossRef] [PubMed]
- Uvnäs-Moberg, K.; Gross, M.M.; Calleja-Agius, J.; Turner, J.D. The yin and yang of the oxytocin and stress systems: Opposites, yet interdependent and intertwined determinants of lifelong health trajectories. Front. Endocrinol. 2024, 15, 1272270. [Google Scholar] [CrossRef]
- Russell, E.; Koren, G.; Rieder, M.; Van Uum, S.H.M. The detection of cortisol in human sweat: Implications for measurement of cortisol in hair. Ther. Drug Monit. 2012, 34, 512–515. [Google Scholar] [CrossRef]
- Hunt, K.E.; Lysiak, N.S.; Moore, M.; Rolland, R.M. Longitudinal progesterone profiles in baleen from female North Atlantic right whales (Eubalaena glacialis) match known calving history. Conserv. Physiol. 2014, 2, cou029. [Google Scholar] [CrossRef] [PubMed]
- Pondeljak, N.; Lugović-Mihić, L. Stress-induced interaction of skin immune cells, hormones, and neurotransmitters. Clin. Ther. 2020, 42, 757–770. [Google Scholar] [CrossRef]
- Slominski, A.; Wortsman, J.; Tuckey, R.C.; Paus, R. Differential expression of HPA axis homolog in the skin. Mol. Cell. Endocrinol. 2007, 265–266, 143–149. [Google Scholar] [CrossRef]
- Skobowiat, C.; Slominski, A.T. UVB activates hypothalamic–pituitary–adrenal axis in C57BL/6 mice. J. Investig. Dermatol. 2015, 135, 1638–1648. [Google Scholar] [CrossRef]
- Cook, N.J. Minimally invasive sampling media and the measurement of corticosteroids as biomarkers of stress in animals. Can. J. Anim. Sci. 2012, 92, 227–259. [Google Scholar] [CrossRef]
- Palme, R. Non-invasive measurement of glucocorticoids: Advances and problems. Physiol. Behav. 2019, 199, 229–243. [Google Scholar] [CrossRef]
- Heistermann, M.; Palme, R.; Ganswindt, A. Comparison of different enzyme immunoassays for assessment of adrenocortical activity in primates based on fecal analysis. Am. J. Primatol. 2006, 68, 257–273. [Google Scholar] [CrossRef]
- Wasser, S.K.; Hunt, K.E.; Brown, J.L.; Cooper, K.; Crockett, C.M.; Bechert, U.; Monfort, S.L. A generalized fecal glucocorticoid assay for use in a diverse array of nondomestic mammalian and avian species. Gen. Comp. Endocrinol. 2000, 120, 260–275. [Google Scholar] [CrossRef] [PubMed]
- Keckeis, K.; Lepschy, M.; Schöpper, H.; Moser, L.; Troxler, J.; Palme, R. Hair cortisol: A parameter of chronic stress? Insights from a radiometabolism study in guinea pigs. J. Comp. Physiol. B 2012, 182, 985–996. [Google Scholar] [CrossRef] [PubMed]
Domain | Welfare Indicator | Description | Type Contribution to Welfare State (Positive/Negative) and Inferred Affective States (Domain 5) | References |
---|---|---|---|---|
Domain 1: Nutrition | Three-month mild weight loss | Calculation of the Body Weight Oscillation Score (BWOS) was performed by determining the difference between the maximum and minimum body weight over a three-month period, dividing this value by the average body weight, and multiplying by 100. A BWOS exceeding 5% was considered indicative of mild weight loss. In our results, BWOS ranged from 5% to 13.5%, with a maximum three-month weight loss of 13.5% of average body weight. Dolphins were voluntarily weighed approximately once per month using a scale located outside the pool. To obtain daily body weight values for calculating BWOS, weights were interpolated between consecutive measurements, assuming a gradual and continuous weight change throughout each interval. | Negative; long-term hunger, weakness | [54] |
Reduced food intake | Measure of the percentage of fish consumed daily by each animal, defined as days when intake was below 90% of the total food offered (recorded in kg). | Negative; short-term hunger, malaise | [8,57,58] | |
Domain 2: Environment | Social isolation | Observations of dolphins kept alone and separated from their social group for extended periods, resulting in impeded affiliative interactions and reduced opportunities for social behaviors. | Negative; loneliness, insecurity, anxiety | [58,59] |
Domain 3: Health | Incidence of eye lesions | Observations of eye opacities, corneal scars, color changes, or any other indicators of eye lesions or diseases. | Negative; malaise, pain, sickness, exhaustion, and, where applicable, breathlessness | [53,60] |
Incidence of oral and dental conditions | Observations of dental wear, fractures, missing teeth, gingivitis, tongue injuries, fungal lesions, or mucosal lesions, including records of previous oral diseases. | [53,61] | ||
Incidence of respiratory diseases | Observations of blowhole secretions, odors, unusual sounds, or changes in respiratory rate, along with diagnosis of respiratory infections or diseases. | [53,62] | ||
Incidence of gastrointestinal diseases | Observations of signs indicating gastrointestinal dysfunction, including records of gastric and fecal abnormalities, cytological evaluations, cultures, and parasitological examinations. | [15,63] | ||
Incidence of renal conditions | Observations of renal abnormalities, including blood chemistry and urinalysis results. | [53,64] | ||
Incidence of skin lesions and diseases | Observations of viral, fungal, or bacterial skin lesions, wounds, discoloration, or other abnormalities. | [53,64] | ||
Domain 4: Behavioral Interactions | Negative social integration | Observations of limited or absent engagement with a novel social group, or the emergence of agonistic interactions after attempted integration. | Negative; anger, anxiety, fear, insecurity | [53,58] |
Presence of mild or low-intensity agonistic behaviors | Observations of agonistic social events or states (e.g., chasing, biting, jaw clapping), including the presence of new rake marks. | [53,58] | ||
Regurgitation | Observations of individuals ejecting a full fish or a mixture of water and fish remnants, often followed by re-swallowing the same material. | Negative; boredom, depression, anxiety | [54] | |
Foreign body ingestion | Observations of individuals ingesting non-food objects, or documentation of the item’s removal. | [59] | ||
Presence of socio-sexual behaviors | Observations of dolphins engaging in socio-sexual behaviors, including genital inspection or contact, or movements in close genital proximity. | Positive; affectionate sociability, excitation/playfulness, sexually gratified | [53,54] | |
Positive social integration | Observations of affiliative social events or states (e.g., gentle approaches, synchronous swimming, playful contact) following integration with a novel social group. | [7,65] | ||
Domain 5: Mental state | Willingness to participate in training sessions (positive human–animal relationship) | Daily records of willingness to participate in sessions as rated on a 5-point scale (0 to 4) representing incremental dolphin’s motivation and enthusiasm during training sessions. | Low: anxiety, fear, insecurity, non-compliant, avoidance High: calm, confident, feels in control, compliantly responsive, seeks contact, bonded with humans | [8,66,67] |
Predictor | Description |
---|---|
Negative welfare indicators | Weekly sum of daily scores of the Negative welfare indicators variable, which includes the cumulative daily presence of the following welfare indicators: Reduced food intake, Social isolation, Incidence of eye lesions, Incidence of oral and dental conditions, Incidence of respiratory diseases, Incidence of gastrointestinal diseases, Incidence of renal conditions, Incidence of skin lesions and diseases, Negative social integration, Presence of mild or low-intensity agonistic behaviors, Regurgitation, and Foreign body ingestion |
Presence of socio-sexual behaviors | Weekly sum of daily scores of Presence of socio-sexual behaviors |
Positive social integration | Weekly sum of daily scores of Positive social interactions |
Three-month mild weight loss | Weekly sum of daily scores of Weight loss over a three-month period |
Diazepam administration | Weekly sum of daily scores of diazepam administration |
Spring | Weeks containing within 21 March–20 June |
Summer | Weeks within 21 June–20 September |
Fall | Weeks within 21 September–20 December |
Peak season | Weeks within 1 July–31 August 2019 |
Closure period | Weeks within 12 March–30 June 2020 |
Predictor | Mean (Scale 0–7) | SD | Median | Min. | Max. |
---|---|---|---|---|---|
Negative welfare indicators (normalized) * | 0.19 | 0.21 | 0.142 | 0 | 1.214 |
Presence of socio-sexual behaviors | 0.15 | 0.48 | 0 | 0 | 3 |
Positive social integration | 0.43 | 0.91 | 0 | 0 | 6 |
Three-month mild weight loss | 0.34 | 1.43 | 0 | 0 | 7 |
Diazepam administration | 1.60 | 2.87 | 0 | 0 | 7 |
Spring | 1.91 | 3.12 | 0 | 0 | 7 |
Summer | 1.59 | 2.94 | 0 | 0 | 7 |
Fall | 1.58 | 2.93 | 0 | 0 | 7 |
Peak season | 0.65 | 2.02 | 0 | 0 | 7 |
Closure period | 1.08 | 2.48 | 0 | 0 | 7 |
Season | Mean ± SD (°C) | Winter (p Value) | Spring (p Value) | Summer (p Value) | Fall (p Value) |
---|---|---|---|---|---|
Winter | 20.8 ± 0.89 | - | 0.26 | <0.001 | <0.001 |
Spring | 21.4 ± 1.93 | 0.26 | - | <0.001 | <0.001 |
Summer | 23.2 ± 1.09 | <0.001 | <0.001 | - | <0.001 |
Fall | 22.6 ± 0.70 | <0.001 | <0.001 | <0.001 | - |
Predictors | Time Lag in Days (Estimates) | |||||||
---|---|---|---|---|---|---|---|---|
20–26 | 27–33 | 34–40 | 41–47 | 48–54 | 55–61 | 62–68 | 69–75 | |
Negative Welfare Indicators | 0.014 | −0.017 | −0.025 | 0.028 | −0.037 | −0.08 | −0.042 | −0.015 |
Presence of socio-sexual behaviors | −0.026 | 0.039 | 0.015 | −0.029 | −0.028 | 0.049 | 0.023 | 0.040 |
Positive social integration | 0.129. | 0.083 | 0.035 | −0.044 | 0.085 | −0.003 | 0.017 | 0.035 |
Three-month mild weight loss | −0.050 | −0.038 | 0.003 | −0.033 | −0.095 | −0.179 ** | −0.224 *** | −0.206 ** |
Diazepam administration | −0.108 | −0.148. | −0.136. | −0.178 * | −0.229 ** | −0.132. | −0.126. | −0.116 |
Spring | −0.065 | −0.091 | −0.079 | −0.053 | −0.052 | −0.045 | 0.035 | 0.067 |
Summer | 0.1563 | 0.194. | 0.174. | 0.233 * | 0.158 | 0.204 * | 0.316 ** | 0.322 *** |
Fall | 0.170 * | 0.142. | 0.146. | 0.136. | 0.119 | 0.108 | 0.076 | 0.095 |
Peak season | −0.013 | −0.083 | −0.035 | −0.065 | 0.048 | 0.007 | −0.027 | −0.070 |
Closure period | −0.066 | −0.001 | 0.024 | 0.048 | 0.120 | 0.038 | −0.022 | 0.014 |
Predictors | Time Lag (Estimates) | |||||||
---|---|---|---|---|---|---|---|---|
20–26 | 27–33 | 34–40 | 41–47 | 48–54 | 55–61 | 62–68 | 69–75 | |
Negative welfare indicators | −5.140 * | −2.353 | −3.195 | −1.373 | −0.912 | −0.319 | −2.433 | −1.813 |
Presence of socio-sexual behaviors | 2.139 | −0.232 | −1.55 | −3.579 | −2.214 | −0.463 | 3.135 | −2.434 |
Positive social integration | −0.494 | 1.040 | −0.197 | −2.949 | −0.368 | 1.763 | 2.85 | −1.155 |
Three-month mild weight loss | 0.753 | −0.855 | −1.419 | −1.252 | −0.362 | −3.126 | −3.883. | −3.761. |
Diazepam administration | 5.702 * | 4.673. | 3.924 | 3.951 | 0.986 | 0.550 | 0.155 | 0.813 |
Spring | −2.577 | −2.244 | 0.669 | 1.812 | −0.159 | 0.189 | 1.688 | 4.921. |
Summer | −1.054 | −0.565 | −1.759 | −0.712 | −1.377 | 1.167 | 5.095 | 5.606. |
Fall | 5.133 * | 4.607. | 5.696 * | 6.069 * | 4.614. | 4.893. | 4.372. | 5.903 * |
Peak season | 4.918. | 4.469 | 6.468 * | 6.508 * | 5.923. | 4.441 | 0.094 | −0.030 |
Closure period | −2.959 | −3.848 | −4.678 | −5.235. | −3.719 | −5.059. | −5.502 * | −6.745 ** |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2025 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Agustí, C.; Talló-Parra, O.; Tejero-Caballo, E.; Garcia-Parraga, D.; López-Arjona, M.; Álvaro-Álvarez, T.; Joaquín-Cerón, J.; Manteca, X. Tracking Epidermal Cortisol and Oxytocin in Managed Bottlenose Dolphins as Potential Non-Invasive Physiological Welfare Indicators. Animals 2025, 15, 2628. https://doi.org/10.3390/ani15172628
Agustí C, Talló-Parra O, Tejero-Caballo E, Garcia-Parraga D, López-Arjona M, Álvaro-Álvarez T, Joaquín-Cerón J, Manteca X. Tracking Epidermal Cortisol and Oxytocin in Managed Bottlenose Dolphins as Potential Non-Invasive Physiological Welfare Indicators. Animals. 2025; 15(17):2628. https://doi.org/10.3390/ani15172628
Chicago/Turabian StyleAgustí, Clara, Oriol Talló-Parra, Enrique Tejero-Caballo, Daniel Garcia-Parraga, Marina López-Arjona, Teresa Álvaro-Álvarez, José Joaquín-Cerón, and Xavier Manteca. 2025. "Tracking Epidermal Cortisol and Oxytocin in Managed Bottlenose Dolphins as Potential Non-Invasive Physiological Welfare Indicators" Animals 15, no. 17: 2628. https://doi.org/10.3390/ani15172628
APA StyleAgustí, C., Talló-Parra, O., Tejero-Caballo, E., Garcia-Parraga, D., López-Arjona, M., Álvaro-Álvarez, T., Joaquín-Cerón, J., & Manteca, X. (2025). Tracking Epidermal Cortisol and Oxytocin in Managed Bottlenose Dolphins as Potential Non-Invasive Physiological Welfare Indicators. Animals, 15(17), 2628. https://doi.org/10.3390/ani15172628