{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T01:33:21Z","timestamp":1760146401304,"version":"build-2065373602"},"reference-count":47,"publisher":"MDPI AG","issue":"11","license":[{"start":{"date-parts":[[2024,10,29]],"date-time":"2024-10-29T00:00:00Z","timestamp":1730160000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Biology"],"abstract":"<jats:p>Background: Leopard sharks (Triakis semifasciata) are abundant, coastal, eastern Pacific, mesopredatory sharks and are frequently managed in aquariums and zoos. Medical examinations are a routine part of good husbandry practices, but the handling protocols vary greatly between facilities. In this study, we compared the physiological stress responses of T. semifasciata associated with manual restraint and sedated handling under parallel holding and handling procedures in a 10 min interval. Methods: Blood was collected and analyzed for the hematocrit (Hct), lactate, glucose, beta-hydroxybutyrate (\u03b2-HB), pH, blood gasses, 1\u03b1-hydroxycorticosterone (1\u03b1-OHB), and corticosterone (B). Results: Overall, a minimal physiological stress response was observed in both groups. However, statistically significant increases in the PCO2, \u03b2-HB and lactate occurred, while the pHTC, SO2, and BE decreased over time in the manual-restraint group. In the sedated group, the B, PCO2, and lactate increased while the pHTC, SO2, and base excess (BE) decreased over time. When comparing treatments, the sedated group had a higher B and PCO2 TC and a lower pHTC, BE, and SO2 than the manual-restraint group at the second time point. Conclusions: This study indicates that manual restraint is comparable to the described sedation in T. semifasciata for minimally invasive procedures. The overall results show that this species had low physiological stress responses to both methods.<\/jats:p>","DOI":"10.3390\/biology13110878","type":"journal-article","created":{"date-parts":[[2024,10,29]],"date-time":"2024-10-29T06:29:57Z","timestamp":1730183397000},"page":"878","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Comparison of Physiological Stress Indices in Anesthetized and Manually Restrained Leopard Sharks, Triakis semifasciata"],"prefix":"10.3390","volume":"13","author":[{"given":"Meghan M.","family":"Holst","sequence":"first","affiliation":[{"name":"Aquatic Health Program, School of Veterinary Medicine, Department of Anatomy, Physiology, and Cell Biology, University of California, One Shields Avenue, Davis, CA 95616, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2224-6434","authenticated-orcid":false,"given":"Catharine J.","family":"Wheaton","sequence":"additional","affiliation":[{"name":"Disney\u2019s Animals, Science and Environment, Disney\u2019s Animal Kingdom<sup>\u00ae<\/sup> and the Seas with Nemo and Friends<sup>\u00ae<\/sup>, Lake Buena Vista, FL 32830, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4806-552X","authenticated-orcid":false,"given":"Alexandra N.","family":"Schoen","sequence":"additional","affiliation":[{"name":"Department of Biology, University of Winnipeg, Winnipeg, MB R3B SE9, Canada"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jill V.","family":"Spangenberg","sequence":"additional","affiliation":[{"name":"Animal Care Department, Aquarium of the Bay, San Francisco, CA 94133, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Kevin T.","family":"McEligot","sequence":"additional","affiliation":[{"name":"Animal Care Department, Aquarium of the Bay, San Francisco, CA 94133, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Melissa L.","family":"Schouest","sequence":"additional","affiliation":[{"name":"Animal Care Department, Aquarium of the Bay, San Francisco, CA 94133, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Charlene M.","family":"Burns","sequence":"additional","affiliation":[{"name":"Disney\u2019s Animals, Science and Environment, Disney\u2019s Animal Kingdom<sup>\u00ae<\/sup> and the Seas with Nemo and Friends<sup>\u00ae<\/sup>, Lake Buena Vista, FL 32830, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3396-6082","authenticated-orcid":false,"given":"Natalie D.","family":"Mylniczenko","sequence":"additional","affiliation":[{"name":"Disney\u2019s Animals, Science and Environment, Disney\u2019s Animal Kingdom<sup>\u00ae<\/sup> and the Seas with Nemo and Friends<sup>\u00ae<\/sup>, Lake Buena Vista, FL 32830, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2024,10,29]]},"reference":[{"key":"ref_1","unstructured":"Coyle, S.D., Durborow, R.W., and Tidwell, J.H. (2004). Anesthetics in Aquaculture (No. 3900), Southern Regional Aquaculture Center, Kentucky State University."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"549","DOI":"10.1016\/S0044-8486(03)00111-X","article-title":"The efficacy of metomidate, clove oil, Aqui-STM and Benzoak\u00ae as anaesthetics in Atlantic salmon (Salmo salar L.) smolts, and their potential stress-reducing capacity","volume":"221","author":"Iversen","year":"2003","journal-title":"Aquaculture"},{"key":"ref_3","unstructured":"Smith, M., Warmolts, D., Thoney, D., Hueter, R., Murray, M., and Ezcurra, J. (2017). The Elasmobranch Husbandry Manual II: Recent Advances in the Care of Sharks, Rays and their Relatives, Ohio Biological Survey, Inc."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"S96","DOI":"10.7589\/52.2S.S96","article-title":"Effectiveness of the anesthetic AQUI-S\u00ae 20E in marine finfish and elasmobranchs","volume":"52","author":"Silbernagel","year":"2016","journal-title":"J. Wildl. Dis."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"774","DOI":"10.1139\/cjz-2017-0093","article-title":"Are 3 minutes good enough for obtaining baseline physiological samples from teleost fish?","volume":"96","author":"Lawrence","year":"2018","journal-title":"Can. J. Zool."},{"key":"ref_6","unstructured":"Pickering, A.D. (1981). Stress and Fish, Academic."},{"key":"ref_7","unstructured":"Hochachka, P.W., and Mommsen, T.P. (1995). Biochemical effects of stress. Environmental and Ecological Biochemistry, Elsevier."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"coab067","DOI":"10.1093\/conphys\/coab067","article-title":"Simulated heatwave and fishing stressors alter corticosteroid and energy balance in neonate blacktip reef sharks, Carcharhinus melanopterus","volume":"9","author":"Schoen","year":"2021","journal-title":"Conserv. Physiol."},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Schreck, C.B., and Moyle, P.B. (1990). Stress and acclimation. Methods for Fish Biology, American Fish Society.","DOI":"10.47886\/9780913235584"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"591","DOI":"10.1152\/physrev.1997.77.3.591","article-title":"The stress response in fish","volume":"77","year":"1997","journal-title":"Physiol. Rev."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"796","DOI":"10.1093\/icesjms\/fsx191","article-title":"Integrating reflexes with physiological measures to evaluate coastal shark stress response to capture","volume":"75","author":"Jerome","year":"2018","journal-title":"ICES J. Mar. Sci."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"146","DOI":"10.1016\/j.cbpa.2011.10.002","article-title":"The physiological response to anthropogenic stressors in marine elasmobranch fishes: A review with a focus on the secondary response","volume":"162","author":"Skomal","year":"2012","journal-title":"Comp. Biochem. Physiol. A Mol. Integr. Physiol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1577\/M08-031.1","article-title":"The Physiological Response of Port Jackson Sharks and Australian Swellsharks to Sedation, Gill-Net Capture, and Repeated Sampling in Captivity","volume":"29","author":"Frick","year":"2009","journal-title":"North Am. J. Fish. Manag."},{"key":"ref_14","unstructured":"Fuller, L.N. (2019). Description and alleviation of the stress response in Atlantic sharpnose sharks (Rhizoprionodon terraenovae), White-spotted bamboo sharks (Chiloscyllium plagiosum), and Golden Shiners (Notemigonus crysoleucas). [Ph.D. Dissertation, University of Mississippi]."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/B978-0-12-801286-4.00001-0","article-title":"Elasmobranch cardiovascular system","volume":"Volume 34","author":"Brill","year":"2015","journal-title":"Fish Physiology"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1016\/j.cbpa.2011.08.015","article-title":"The endocrinology of 1\u03b1-hydroxycorticosterone in elasmobranch fish: A review","volume":"162","author":"Anderson","year":"2012","journal-title":"Comp. Biochem. Physiol. A Mol. Integr. Physiol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"703","DOI":"10.1016\/S0305-0491(97)00272-1","article-title":"Jaws: The Inside Story. The Metabolism of Elasmobranch Fishes","volume":"118","author":"Ballantyne","year":"1997","journal-title":"Comp. Biochem. Physiol. B Biochem. Mol. Biol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"395","DOI":"10.1016\/B978-0-12-801286-4.00007-1","article-title":"Metabolism of elasmobranchs (Jaws II)","volume":"Volume 34","author":"Ballantyne","year":"2015","journal-title":"Fish Physiology"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"457","DOI":"10.1016\/0039-128X(67)90100-6","article-title":"1\u03b1-hydroxycorticosterone: Synthesis in vitro and properties of an interrenal steroid in the blood of cartilaginous fish (Genus Raja)","volume":"9","author":"Idler","year":"1967","journal-title":"Steroids"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"113799","DOI":"10.1016\/j.ygcen.2021.113799","article-title":"Energy and corticosteroid mobilization following an induced stress response in an elasmobranch fish, the North Pacific spiny dogfish (Squalus acanthias suckleyi)","volume":"310","author":"Schoen","year":"2021","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1016\/j.ygcen.2018.01.028","article-title":"Challenges, pitfalls and surprises: Development and validation of a monoclonal antibody for enzyme immunoassay of the steroid 1\u03b1-hydroxycorticosterone in elasmobranch species","volume":"265","author":"Wheaton","year":"2018","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"113440","DOI":"10.1016\/j.ygcen.2020.113440","article-title":"Measurement of 1\u03b1 hydroxycorticosterone in the Japanese banded houndshark, Triakis scyllium, following exposure to a series of stressors","volume":"292","author":"Iki","year":"2020","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1023\/A:1023287123495","article-title":"Effect of temperature on oxygen consumption of the leopard shark, Triakis semifasciata","volume":"66","author":"Miklos","year":"2003","journal-title":"Environ. Biol. Fishes"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"210","DOI":"10.1242\/jeb.031781","article-title":"Proteomic and physiological responses of leopard sharks (Triakis semifasciata) to salinity change","volume":"213","author":"Dowd","year":"2010","journal-title":"J. Exp. Biol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1242\/jeb.151.1.161","article-title":"Blood respiratory properties and the effect of swimming on blood gas transport in the leopard shark Triakis semifasciata","volume":"151","author":"Graham","year":"1990","journal-title":"J. Experim"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1242\/jeb.00741","article-title":"Postprandial response of gastric pH in leopard sharks (Triakis semifasciata) and its use to study foraging ecology","volume":"207","author":"Papastamatiou","year":"2004","journal-title":"J. Exp. Biol."},{"key":"ref_27","unstructured":"Moe, M.A. (2009). Marine Aquarium Handbook, Beginner to Breeder, Green Turtle Publications."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"553","DOI":"10.1111\/j.1439-0426.2012.01950.x","article-title":"Review Tricaine methane-sulfonate (MS-222) application in fish anaesthesia","volume":"28","author":"Popovic","year":"2012","journal-title":"J. Appl. Ichthyol."},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Von Krogh, K., Higgins, J., Saavedra Torres, Y., and Mocho, J.-P. (2021). Screening of Anaesthetics in Adult Zebrafish (Danio rerio) for the Induction of Euthanasia by Overdose. Biology, 10.","DOI":"10.3390\/biology10111133"},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"F\u00e9lix, L., Correia, R., Sequeira, R., Ribeiro, C., Monteiro, S., Antunes, L., Silva, J., Ven\u00e2ncio, C., and Valentim, A. (2021). MS-222 and Propofol Sedation during and after the Simulated Transport of Nile tilapia (Oreochromis niloticus). Biology, 10.","DOI":"10.3390\/biology10121309"},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Br\u00f8nstad, A. (2022). Good Anesthesia Practice for Fish and Other Aquatics. Biology, 11.","DOI":"10.3390\/biology11091355"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"117","DOI":"10.2460\/javma.241.1.117","article-title":"Evaluation of critical care blood analytes assessed with a point-of-care portable blood analyzer in wild and aquarium-housed elasmobranchs and the influence of phlebotomy site on results","volume":"241","author":"Naples","year":"2012","journal-title":"J. Am. Vet. Med. Assoc."},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Bates, D., M\u00e4chler, M., Bolker, B., and Walker, S. (2014). Fitting Linear Mixed-Effects Models using lme4. arXiv.","DOI":"10.18637\/jss.v067.i01"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1080\/01621459.1991.10475006","article-title":"Generalized Linear Models With Random Effects; A Gibbs Sampling Approach","volume":"86","author":"Zeger","year":"1991","journal-title":"J. Am. Stat. Assoc."},{"key":"ref_35","unstructured":"Length, R.V., Banfai, B., Bolker, B., Buerkner, P., Gin\u00e9-V\u00e1zquez, I., Herve, M., Jung, M., Love, J., Miguez, F., and Piaskowski, J. (2024, October 09). emmeans: Estimated Marginal Means, aka Least-Squares Means. Available online: https:\/\/cran.r-project.org\/web\/packages\/emmeans\/index.html."},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Mylniczenko, N., Clauss, T., and Stamper, M. (2014). Elasmobranchs and holocephalans. Zoo Animal and Wildlife Immobilization and Anesthesia, John Wiley & Sons, Inc.","DOI":"10.1002\/9781118792919.ch16"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"94","DOI":"10.1016\/j.cbpa.2011.04.012","article-title":"The physiological response of the Caribbean reef shark (Carcharhinus perezi) to longline capture","volume":"162","author":"Brooks","year":"2012","journal-title":"Comp. Biochem. Physiol. A Mol. Integr. Physiol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"207","DOI":"10.3354\/meps10490","article-title":"Physiological stress response, reflex impairment, and survival of five sympatric shark species following experimental capture and release","volume":"496","author":"Gallagher","year":"2014","journal-title":"Mar. Ecol. Prog. Ser."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"267","DOI":"10.1007\/s00360-008-0306-4","article-title":"Differential sensitivity to capture stress assessed by blood acid-base status in five carcharhinid sharks","volume":"179","author":"Mandelman","year":"2009","journal-title":"J. Comp. Physiol. B"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1016\/j.cbpa.2012.02.008","article-title":"Hematological indicators of stress in longline-captured sharks","volume":"162","author":"Marshall","year":"2012","journal-title":"Comp. Biochem. Physiol. A Mol. Integr. Physiol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1419","DOI":"10.1056\/NEJMra1711860","article-title":"Diagnostic Use of Base Excess in Acid\u2013Base Disorders","volume":"378","author":"Berend","year":"2018","journal-title":"N. Engl. J. Med."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"236","DOI":"10.1644\/BHE-001.1","article-title":"Equipped for life: The adaptive role of the stress axis in male mammals","volume":"86","author":"Boonstra","year":"2005","journal-title":"J. Mammal."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"cou037","DOI":"10.1093\/conphys\/cou037","article-title":"Validation of the i-STAT system for the analysis of blood parameters in fish","volume":"2","author":"Harter","year":"2014","journal-title":"Conserv. Physiol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"cov002","DOI":"10.1093\/conphys\/cov002","article-title":"Validation of the i-STAT system for the analysis of blood gases and acid\u2013base status in juvenile sandbar shark (Carcharhinus plumbeus)","volume":"3","author":"Harter","year":"2015","journal-title":"Conserv. Physiol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1577\/H10-012.1","article-title":"Blood gas, Oxygen Saturation, pH, and Lactate Values in Elasmobranch Blood Measured with a Commercially Available Portable Clinical analyzer and Standard Laboratory Instruments","volume":"22","author":"Gallagher","year":"2010","journal-title":"J. Aquat. Anim. Health"},{"key":"ref_46","unstructured":"Mylniczenko, N., Smukall, M.J., and Wheaton, C.J. (2019, January 18\u201322). Measurement of Serum 1\u03b1-hydroxycorticosterone (1\u03b1OH-B), the Elasmobranch Stress Hormone, in Select Shark Species. Proceedings of the 50th Annual IAAAM Conference, Durban, South Africa."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"251","DOI":"10.1016\/B978-0-12-802728-8.00007-2","article-title":"The stress and stress mitigation effects of exercise: Cardiovascular, metabolic, and skeletal muscle adjustments","volume":"Volume 35","author":"Rodnick","year":"2016","journal-title":"Fish Physiology"}],"container-title":["Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2079-7737\/13\/11\/878\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T16:22:43Z","timestamp":1760113363000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2079-7737\/13\/11\/878"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,10,29]]},"references-count":47,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2024,11]]}},"alternative-id":["biology13110878"],"URL":"https:\/\/doi.org\/10.3390\/biology13110878","relation":{},"ISSN":["2079-7737"],"issn-type":[{"type":"electronic","value":"2079-7737"}],"subject":[],"published":{"date-parts":[[2024,10,29]]}}}