Skip to main content
SpringerLink
Log in

Talking to the dead: using Post-mortem data in the assessment of stress in tiger sharks (Galeocerdo cuvier) (Péron and Lesueur, 1822)

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

Sharks are very sensitive to stress and prone to a high mortality rate after capture. Since approximately 50 million of sharks are caught as bycatch every year, and current recommendations to reduce the impact of commercial fishing strongly support immediate release, it is imperative to better understand post-release mortality caused by the stress of capture and handling. Blood samples allow the assessment of stress levels which are valuable tools to reduce mortality in commercial, recreational and scientific fishing, being essential for the improvement in those conservation measures. Biochemical analyses are widely used for sharks as stress indicators, with secondary plasma parameters (lactate, glucose and ions) being the most often employed assays. However, it is virtually impossible to determine baseline plasma parameters in free-ranging sharks, since blood withdrawal involves animal capture and restrain, which are stressful procedures. This study aims at analyzing secondary parameters of five healthy tiger sharks captured with circular hooks and handlines in Fernando de Noronha (Northeastern Brazil) and comparing them with secondary parameters of three dead tiger sharks caught off Recife (also Northeastern Brazil). The results showed that the analysis of some plasma constituents in dead animals may be an efficient tool to assess stress and lethality. However, traditional parameters such as glucose and calcium, need to be used with caution. The results also demonstrated the extreme importance of urea and phosphorus for assessing stress response and mortality in tiger sharks, both parameters frequently neglected and of utmost importance for shark’s homeostasis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Albers C (1970) Acid-base balance. In: Hoar W, Randall DJ (eds) Fish physiology, vol IV. Academic Press Inc., United States pp, pp 173–205

    Google Scholar 

  • Anderson WG (2012) The endocrinology of 1α-hydroxycorticosterone in elasmobranch fish: a review. Comp Biochem Physiol (A) 162(2):73–80. doi:10.1016/j.cbpa.2011.08.015

    Article  CAS  Google Scholar 

  • Andrigueto JM, Peryl L, Minardi I (1990) Nutrição animal: bases e fundamentos da nutrição animal. vol I. Nobel 1, Brazil, p 396

  • Armour KJ, O’Toole LB, Hazon N (1993) The effect of dietary protein restriction on the secretory dynamics of 1α-hydroxycorticosterone and urea in the dogfish, Scyliorhinus canicula: a possible role for 1α-hydroxycorticosterone in sodium retention. J Endocrinol 138(2):275–282. doi:10.1677/joe.0.1380275

    Article  CAS  PubMed  Google Scholar 

  • Awruch CA, Simpfendorfer C, Pankhurst NW (2011) Evaluation and use of a portable field kit for measuring whole-blood lactate in sharks. Mar Freshw Res 62:694–699. doi:10.1071/MF10149

    Article  CAS  Google Scholar 

  • Ballantyne JS (2015) Jaws II: metabolism of elasmobranchs. In: Shadwick RE, Farrell AP, Brauner CJ (eds) Physiology of elasmobranch fishes: internal processes, 1st edn. Academic Press, United States, pp 395–456

    Chapter  Google Scholar 

  • Ballantyne JS (2016) Some of the most interesting things we know, and don’t know, about the biochemistry and physiology of elasmobranch fishes (sharks, skates and rays). Comp Biochem Physiol (B). doi:10.1016/j.cbpb.2016.03.005

    Google Scholar 

  • Ballantyne JS, Robinson JW (2010) Freshwater elasmobranchs: a review of their physiology and biochemistry. J Comp Phys (B) 180(4):475–493. doi:10.1007/s00360-010-0447-0

    Article  Google Scholar 

  • Balmaceda-Aguilera C, Cortes-Campos C, Cifuentes M, Peruzzo B, Mack L, Tapia JC et al (2012) Glucose transporter 1 and monocarboxylate transporters 1, 2, and 4 localization within the glial cells of shark blood-brain-barriers. PLoS One 7(2):e32409

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barton BA, Iwama GK (1991) Physiological changes in fish from stress in aquaculture with emphasis on the response and effects of corticosteroids. Annu Rev Fish Dis 1:3–26. doi:10.1016/0959-8030(91)90019-G

    Article  Google Scholar 

  • Beerkircher LR, Cortes E, Shivji M (2002) Characteristics of shark’s bycatch observed on pelagic loglines off Southeastern United States, 1992–2000. Mar Fish Rev 64(4):40–49

    Google Scholar 

  • Bone Q (1988) Muscles and locomotion. In: Shuttleworth TJ (ed) Physiology of elasmobranch fishes. Springer, Berlin, pp 99–141

    Chapter  Google Scholar 

  • Bonga SW (1997) The stress response in fish. Physiol Rev 77(3):591–625

    Google Scholar 

  • Boonstra R (2004) Coping with changing northern environments: the role of the stress axis in birds and mammals. Integr Comp Biol 44(2):95–108. doi:10.1093/icb/44.2.95

    Article  PubMed  Google Scholar 

  • Braithwaite VA, Ebbesson LOE (2014) Pain and stress responses in farmed fish. Rev Sci Tech 33(1):245–253

    CAS  PubMed  Google Scholar 

  • Brajon S, Laforest JP, Schmitt O, Devillers N (2016) A preliminary study of the effects of individual response to challenge tests and stress induced by humans on learning performance of weaned piglets (Sus scrofa). Behav Process 129:27–36. doi:10.1016/j.beproc.2016.05.007

    Article  Google Scholar 

  • Brooks EJ, Sloman KA, Liss S, Hassan-Hassanein L, Danylchuk AJ, Cooke SJ, Mandelman JW, Skomal GB, Sims DW, Suski CD (2011) The stress physiology of extended duration tonic immobility in the juvenile lemon shark, Negaprion brevirostris (Poey 1868). J Exp Mar BiolEcol 409:351–360. doi:10.1016/j.jembe.2011.09.017

    Article  Google Scholar 

  • Brooks EJ, Mandelman JW, Sloman KA, Liss S, Danylchuk AJ, Cooke SJ, Skomal GB, Philipp DP, Sims DW, Suski CD (2012) The physiological response of the Caribbean reef shark (Carcharhinus perezi) to longline capture. Comp Biochem Physiol (A) 162:94–100. doi:10.1016/j.cbpa.2011.04.012

    Article  CAS  Google Scholar 

  • Cannon WB (1929) Organization for physiological homeostasis. Physiol Rev 400:399–431

    Google Scholar 

  • Cliff G, Thurman GD (1984) Pathological and physiological effects of stress during capture and transport in the juvenile dusky shark, Carcharhinus obscurus. Comp Biochem Physiol (A) 78:167–173. doi:10.1016/0300-9629(84)90111-7

    Article  Google Scholar 

  • Cockrem JF (2013) Individual variation in glucocorticoid stress responses in animals. Gen Comp Endocrinol 181:45–58. doi:10.1016/j.ygcen.2012.11.025

    Article  CAS  PubMed  Google Scholar 

  • Crowder LB, Murawski SA (1998) Fisheries bycatch: implications for management. Fisheries 23(6):8–17. doi:10.1577/15488446(1998)023<0008:FBIFM>2.0.CO;2

    Article  Google Scholar 

  • Davies RWD, Cripps SJ, Nickson A, Porter G (2009) Defining and estimating global marine fisheries bycatch. Mar Policy 33(4):661–672. doi:10.1016/j.marpol.2009.01.003

    Article  Google Scholar 

  • de Roos R, de Roos CC (1978) Elevation of plasma glucose levels by catecholamines in elasmobranch fish. Gen Comp Endocrinol 34:447–452. doi:10.1016/0016-6480(78)90285-X

    Article  Google Scholar 

  • de Roos R, deRoos CC, Werner CS, Werner H (1985) Plasma levels of glucose, alanine, lactate, and β-hydroxybutyrate in the unfed spiny dogfish (Squalus acanthias) after surgery and following mammalian insulin infusion. Gen Comp Endocrinol 58:28–43. doi:10.1016/0016-6480(85)90133-9

    Article  Google Scholar 

  • Deck CA, LeMoine CMR, Walsh PJ (2016) Phylogenetic analysis and tissue distribution of elasmobranch glucose transporters and their response to feeding. Biol Open. doi:10.1242/bio.016709

    PubMed  PubMed Central  Google Scholar 

  • Dulvy NK, Baum JK, Clarke S, Compagno LJ, Cortes E, Domingo A et al (2008) You can swim but you can’t hide: the global status and conservation of oceanic pelagic sharks and rays. Aquat Conserv Mar Freshw Ecosyst 18(5):459–482. doi:10.1002/aqc.975

    Article  Google Scholar 

  • Edwards JR (1988) The determinants and consequences of coping with stress. In: Coopre CL, Payn R (eds) Causes, coping consequences of stress at work, chichester. Wiley, New York, pp 233–266

    Google Scholar 

  • FAO (2011) International guidelines on bycatch management and reduction of discards. Food and agriculture organization of the United Nations (FAO), Rome/Roma, p 73

  • Foo JTW, Lam TJ (1993) Serum cortisol response to handling stress and the effect of cortisol implantation on testosterone level in the tilapia Oreocrhomis mossambicus. Aquaculture 11(5):145–158. doi:10.1016/0044-8486(93)90365-6

    Article  Google Scholar 

  • Frick LH, Reina RD, Walker TI (2010) Stress related physiological changes and post-release survival of Port Jackson sharks (Heterodontusportusjacksoni) and gummy sharks (Mustelusantarcticus) following gill-net and longline capture in captivity. J Exp Mar Biol Ecol 385:29–37. doi:10.1016/j.jembe.2010.01.013

    Article  Google Scholar 

  • Gallagher A, Serafy J, Cooke S, Hammerschlag N (2014) Physiological stress response, reflex impairment, and survival of five sympatric shark species following experimental capture and release. Mar Ecol Prog Ser 496:207–218. doi:10.3354/meps10490

    Article  Google Scholar 

  • Gutierrez J, Carrillo M, Zanuy S, Planas J (1984) Daily rhythms of insulin and glucose levels in the plasma of sea bass Dicentrarchuslabrax after experimental feeding. Gen Comp Endocrinol 55(3):393–397. doi:10.1016/0016-6480(84)90009-1

    Article  CAS  PubMed  Google Scholar 

  • Hammerschlag N (2006) Osmoregulation in elasmobranchs: a review for fish biologists, behaviourists and ecologists. Mar Freshw Behav Physiol 39(3):209–228. doi:10.1080/10236240600815820

    Article  CAS  Google Scholar 

  • Hazin FHV, Afonso AS (2013) A green strategy for shark attack mitigation off Recife, Brazil. Anim Conserv 17(4):287–296. doi:10.1111/acv.12096

    Article  Google Scholar 

  • Hazon N, Henderson IW (1984) Secretory dynamics of 1α-hydroxycorticosterone in the elasmobranch fish, Scyliorhinus canicula. J Endocrinol 103(2):205–211. doi:10.1677/joe.0.1030205

    Article  CAS  PubMed  Google Scholar 

  • Heberer C, Aalbers SA, Bernal D, Kohin S, DiFiore B, Sepulveda CA (2010) Insights into catch-and-release survivorship and stress-induced blood biochemistry of common thresher sharks (Alopiasvulpinus) captured in the southern California recreational fishery. Fish Res 106:495–500. doi:10.1016/j.fishres.2010.09.024

    Article  Google Scholar 

  • Hoffmayer ER, Parsons GR (2001) The physiological response to capture and handling stress in the Atlantic sharpnose shark, Rhizoprionodonterraenovae. Fish Physiol Biochem 25:277–285. doi:10.1023/A:1023210620904

    Article  Google Scholar 

  • Hoffmayer ER, Hendon JM, Parsons GR (2012) Seasonal modulation in the secondary stress response of a carcharhinid shark, Rhizoprionodon terraenovae. Comp Biochem Physiol (A) 162(2):81–87. doi:10.1016/j.cbpa.2011.05.002

    Article  CAS  Google Scholar 

  • Hoffmayer ER, Hendon JM, Parsons GR, Driggers WB, Campbell MD (2015) A comparison of single and multiple stressor protocols to assess acute stress in a coastal shark species, Rhizoprionodonterraenovae. Fish Physiol Biochem 41(5):1253–1260. doi:10.1007/s10695-015-0083-4

    Article  CAS  PubMed  Google Scholar 

  • Hyatt MW, Anderson PA, O’Donnell PM (2016) Behavioral release condition score of bull and bonnethead sharks as a coarse indicator of stress. J Coast Res (in press). doi:10.2112/JCOASTRES-D-15-00108.1

  • Idler DR, Truscott B (1966) 1α-hydroxycorticosterone from cartilaginous fish: a new adrenal steroid in blood. J Fish Res Board Can 23(4):615–619. doi:10.1139/f66-053

    Article  CAS  Google Scholar 

  • Kirschner LB (1993) The energetics of osmotic regulation in ureotelic and hypoosmotic fishes. J Exp Zool 267:19–26. doi:10.1002/jez.1402670104

    Article  CAS  Google Scholar 

  • Mandelman JW, Farrington MA (2007) The physiological status and mortality associated with otter-trawl capture, transport, and captivity of an exploited elasmobranch, Squalus acanthias. ICES J Mar Sci 64:122–130. doi:10.1093/icesjms/fsl003

    CAS  Google Scholar 

  • Mandelman JW, Skomal GB (2009) Differential sensitivity to capture stress assessed by blood acid–base status in five carcharhinid sharks. J Com Physiol B 179:267–277. doi:10.1007/s00360-008-0306-4

    Article  Google Scholar 

  • Manire C, Hueter R, Hull E, Spieler R (2001) Serological changes associated with gill-net capture and restraint in three species of sharks. Trans Am Fish Soc 130:1038–1048. doi:10.1577/1548-8659(2001)130<1038:SCAWGN>2.0.CO;2

    Article  Google Scholar 

  • Manire CA, Rasmussen LEL, Maruska KP, Tricas TC (2007) Sex, seasonal, and stress-related variations in elasmobranch corticosterone concentrations. Comp Biochem Physiol (A) 148(4):926–935. doi:10.1016/j.cbpa.2007.09.017

    Article  Google Scholar 

  • Marshall WS (2003) Rapid regulation of NaCl secretion by estuarine teleost fish: coping strategies for short-duration freshwater exposures. BBA Rev Biomambranes 1618(2):95–105. doi:10.1016/j.bbamem.2003.10.015

    Article  CAS  Google Scholar 

  • Marshall WS, Grosell M (2006) Ion transport, osmoregulation, and acid-base balance. In: Evans DH, Claiborne JB, Currie S (eds) The physiology of fishes. CRC Press, Boca Raton, pp 177–230

    Google Scholar 

  • Marshall H, Field L, Afiadata A, Sepulveda C, Skomal G, Bernal D (2012) Hematological indicators of stress in longline-captured sharks. Comp Biochem Physiol A 162:121–129. doi:10.1016/j.cbpa.2012.02.008

    Article  CAS  Google Scholar 

  • Mommsen TP, Vijayan MM, Moon TW (1999) Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Rev Fish Biol Fish 9:211–268. doi:10.1023/A:1008924418720

    Article  Google Scholar 

  • Morgan A, Burgess GH (2007) At-vessel fishing mortality for six species of sharks caught in the northwest Atlantic and Gulf of Mexico. In: Proceedings of the 59th annual conference of the gulf and caribbean fisheries institute, 19, pp 123–130

  • Moyes CD, Fragoso N, Musyl MK, Brill RW (2006) Predicting post release survival in large pelagic fish. Trans Am Fish Soc 135:1389–1397. doi:10.1577/T05-224.1

    Article  Google Scholar 

  • Neves KR, Graciolli FG, Dos Reis LM, Pasqualucci CA, Moyses RM, Jorgetti V (2004) Adverse effects of hyperphosphatemia on myocardial hypertrophy, renal function, and bone in rats with renal failure. Kidney Int 66(6):2237–2244. doi:10.1111/j.1523-1755.2004.66013.x

    Article  CAS  PubMed  Google Scholar 

  • Pickering AD, Pottinger TG, Christie P (1982) Recovery of the brown trout, Salmo trutta L., from acute handling stress: a time-course study. J Fish Biol 20(2):229–244. doi:10.1111/j.1095-8649.1982.tb03923.x

    Article  Google Scholar 

  • Pikering AD, Pottinger TG (1995) Biochemical effects of stress. In: Hochachka PW, Mommsen TP (eds) Environmental and ecological biochemistry. Elsevier, Amsterdam, pp 349–379

    Chapter  Google Scholar 

  • Pozhitkov AE, Neme R, Domazet-Loso T, Leroux B, Soni S, Tautz D, Noble PA (2016) Thanatotranscriptome: genes actively expressed after organismal death. BioRxiv. doi:10.1101/058305

    Google Scholar 

  • Rasmussen LEL, Crow GL (1993) Serum corticosterone concentrations in immature captive whitetip reef sharks, Triaenodon obesus. J Exp Zool 267(3):283–287. doi:10.1002/jez.1402670306

    Article  CAS  Google Scholar 

  • Rasmussen LEL, Gruber SH (1993) Serum concentrations of reproductively-related circulating steroid hormones in the free-ranging lemon shark, Negaprion brevirostris. In: Demski LS, Wourms JP (eds) The reproduction and development of sharks, skates, rays and ratfishes. Springer, Dordrecht, pp 167–174

    Chapter  Google Scholar 

  • R Development Core Team (2016) R: a language and environment for statistical computing. Vienna, Austria. www.r-project.org

  • Romero ML, Butler LK (2007) Endocrinology of stress. Int J Comp Psychol 20(2):89–95

    Google Scholar 

  • Routley MH, Nilsson GE, Renshaw GMC (2002) Exposure to hypoxia primes the respiratory and metabolic responses of the epaulette shark to progressive hypoxia. Comp Biochem Physiol (A) 131:313–321. doi:10.1016/S1095-6433(01)00484-6

    Article  Google Scholar 

  • Skomal GB (2006) The physiological effects of capture stress on post-release survivorship of sharks, tunas and marlins. Boston, Massachusetts: Boston University, PhD dissertation, p 294

  • Skomal GB (2007) Evaluating the physiological and physical consequences of capture on post-release survivorship in large pelagic fishes. Fish Manag Ecol 14:81–89. doi:10.1111/j.1365-2400.2007.00528.x

    Article  Google Scholar 

  • Skomal GB, Bernal D (2010) Physiological responses to stress in sharks. In: Carrier J, Musick J, Heithaus M (eds) Sharks and their relatives II: biodiversity, adaptive physiology, and conservation. CRC Press, Boca Raton, pp 459–490

    Chapter  Google Scholar 

  • Skomal GB, Mandelman JW (2012) The physiological response to anthropogenic stressors in marine elasmobranch fishes: a review with a focus on the secondary response. Comp Biochem Physiol (A) 162:146–155. doi:10.1016/j.cbpa.2011.10.002

    Article  CAS  Google Scholar 

  • Skomal G, Lobel PS, Marshall G (2007) The use of animal-borne imaging to assess post release behavior as it relates to capture stress in grey reef sharks, Carcharhinus amblyrhynchos. Mar Technol Soc J 41:44–48. doi:10.4031/002533207787441999

    Article  Google Scholar 

  • Smith MFL (1992) Capture and transportation of elasmobranchs, with emphasis on the grey nurse shark, Carcharias taurus. Aust J Mar Freshw Res 43:325–343. doi:10.1071/MF9920325

    Article  CAS  Google Scholar 

  • Smith MFL, Marshall A, Correia JP, Rupp J (2004) Elasmobranch transport techniques and equipment. In: Smith M, Warmolts D, Thoney D, Heuter R (eds) The Elasmobranch husbandry manual: captive care of sharks, rays and their relatives, The Ohio Biological Society, Columbus, OH, pp 105–131

  • Speers-Roesch B, Treberg JR (2010) The unusual energy metabolism of elasmobranch fishes. Comp Biochem Physiol (A) 155:417–434. doi:10.1016/j.cbpa.2009.09.031

    Article  Google Scholar 

  • Speers-Roesch B, Richards JG, Brauner CJ, Farrell AP, Hickey AJR, Wang YS, Renshaw GMC (2012) Hypoxia tolerance in elasmobranchs I. Critical oxygen tension as a measure of blood oxygen transport during hypoxia exposure. J Exp Biol 215:93–102. doi:10.1242/jeb.059642

    Article  CAS  PubMed  Google Scholar 

  • Thomas PM, Pankhurst NW, Bremner HA (1999) The effect of stress and exercise on post-mortem biochemistry of Atlantic salmon and rainbow trout. J Fish Biol 54(6):1177–1196. doi:10.1111/j.1095-8649.1999.tb02047.x

    Article  CAS  Google Scholar 

  • Treberg JR, Speers-Roesch B (2016) Does the physiology of chondrichthyan fishes constrain their distribution in the deep-sea? J Exp Biol 219:615–625. doi:10.1242/jeb.128108

    Article  PubMed  Google Scholar 

  • Vitousek MN, Jenkins BR, Safran RJ (2014) Stress and success: individual differences in the glucocorticoid stress response predict behavior and reproductive success under high predation risk. Horm Behav 66(5):812–819. doi:10.1016/j.yhbeh.2014.11.004

    Article  CAS  PubMed  Google Scholar 

  • Walsh PJ, Kajimura M, Mommsen TP, Wood CM (2006) Metabolic organization and effects of feeding on enzyme activities of the dogfish shark (Squalus acanthias) rectal gland. J Exp Biol 209:2929–2938. doi:10.1242/jeb.02329

    Article  CAS  PubMed  Google Scholar 

  • Wells RMG, McIntyre RH, Morgan AK, Davie PS (1986) Physiological stress responses in big gamefish after capture: observations on plasma chemistry and blood factors. Comp Biochem Physiol (A) 84:565–571. doi:10.1016/0300-9629(86)90366-X

    Article  CAS  Google Scholar 

  • Whitney NM, White CF, Gleiss AC, Schwieterman GD, Anderson P, Hueter RE, Skomal GB (2016) A novel method for determining post-release mortality, behavior, and recovery period using acceleration data loggers. Fish Res 183:210–221. doi:10.1016/j.fishres.2016.06.003

    Article  Google Scholar 

  • Wingfield JC, Romero LM (2001) Adrenocortical responses to stress and their modulation in free-living vertebrates. Compr Physiol. doi:10.1002/cphy.cp070411

    Google Scholar 

  • Wood CM, Turner JD, Graham MS (1983) Why do fish die after severe exercise? J Fish Biol 22:189–201. doi:10.1111/j.1095-8649.1983.tb04739.x

    Article  CAS  Google Scholar 

  • Wright PA, Wood CM (2015) Regulation of ions, acid-base, and nitrogenous wastes in Elasmobranchs. In: Farrel AP, Brauner CJ (eds) Physiology of elasmobranch fishes: internal processes, vol 34. Academic Press, London, p 279

    Chapter  Google Scholar 

  • Wright AJ, Deak T, Parsons ECM (2011) Size matters: management of stress responses and chronic stress in beaked whales and other marine mammals may require larger exclusion zones. Mar Pol Bull 63(1):5–9. doi:10.1016/j.marpolbul.2009.11.024

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We would like to thank Chris Fisher and OCEARCH crew for sponsorship, access to the vessel, tools, sharks and professional fishing experience, CAPES for the fellowship grant to NW (99999.006477/2015-01) and ASA (BJT-A049/2013), FAPESP for the fellowship grant to HB (2013/25930-0), Fernando Ferradosa for reviewing the English and both anonymous reviewers for their significant and valuable contributions to the final version of this manuscript.

Author information

Authors and Affiliations

  1. Departamento de Fisiologia, Setor de Ciências Biológicas, Universidade Federal do Paraná (UFPR) – Centro Politécnico, Curitiba, PR, CEP 81531-990, Brazil

    Natascha Wosnick & Carolina Arruda Freire

  2. Centro de Estudos do Mar, Universidade Federal do Paraná, Pontal do Paraná, PR, CEP 83255976, Brazil

    Hugo Bornatowski

  3. Laboratório de Tecnologia Pesqueira, Departamento de Pesca e Aquicultura, Universidade Federal Rural de Pernambuco, Av. Dom Manoel de Medeiros s/n, Dois Irmãos, Recife, CEP 52171900, Brazil

    Carolina Ferraz, André Afonso & Fábio Hissa Vieira Hazin

  4. Laboratório de Metabolismo e Reprodução de Organismos Aquáticos, Departamento de Fisiologia, Instituto de Biociências, Universidade de São Paulo, Rua do Matão, travessa 14, 321, Cidade Universitária, São Paulo, SP, Brazil

    Bianca Sousa Rangel

Authors
  1. Natascha Wosnick
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hugo Bornatowski
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Carolina Ferraz
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. André Afonso
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Bianca Sousa Rangel
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Fábio Hissa Vieira Hazin
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Carolina Arruda Freire
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Natascha Wosnick.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wosnick, N., Bornatowski, H., Ferraz, C. et al. Talking to the dead: using Post-mortem data in the assessment of stress in tiger sharks (Galeocerdo cuvier) (Péron and Lesueur, 1822). Fish Physiol Biochem 43, 165–178 (2017). https://doi.org/10.1007/s10695-016-0276-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-016-0276-5

Keywords

Search

Navigation