Abstract
Quantifying the physiological stress response of chondrichthyans to capture has assisted the development of fishing practices conducive to their survival. However, currently used indicators of stress show significant interspecific and intraspecific variation in species’ physiological responses and tolerances to capture. To improve our understanding of chondrichthyan stress physiology and potentially reduce variation when quantifying the stress response, we investigated the use of the adenylate energy charge (AEC); a measure of available metabolic energy. To determine tissues sensitive to metabolic stress, we extracted samples of the brain, heart, liver, white muscle and blood from gummy sharks (Mustelus antarcticus) immediately following gillnet capture and after 3 h recovery under laboratory conditions. Capture caused significant declines in liver, white muscle and blood AEC, whereas no decline was detected in the heart and brain AEC. Following 3 h of recovery from capture, the AEC of the liver and blood returned to “unstressed” levels (control values) whereas white muscle AEC was not significantly different to that immediately after capture. Our results show that the liver is most sensitive to metabolic stress and white muscle offers a practical method to sample animals non-lethally for determination of the AEC. The AEC is a highly informative indicator of stress and unlike current indicators, it can directly measure the change in available energy and thus the metabolic stress experienced by a given tissue. Cellular metabolism is highly conserved across organisms and, therefore, we think the AEC can also provide a standardised form of measuring capture stress in many chondrichthyan species.
Similar content being viewed by others
References
Afonso AS, Hazin FHV (2014) Post-release survival and behavior and exposure to fisheries in juvenile tiger sharks, Galeocerdo cuvier, from the South Atlantic. J Exp Mar Biol Ecol 454:55–62
Atkinson DE (1968) Energy charge of adenylate pool as a regulatory parameter. Interaction with feedback modifiers. Biochemistry 7:4030–4034
Benoît HP, Hurlbut T, Chassé J, Jonsen ID (2012) Estimating fishery-scale rates of discard mortality using conditional reasoning. Fish Res 125:318–330
Braccini, M, Rijn, JV, Frick, L (2012) High post-capture survival for sharks, rays and chimaeras discarded in the main shark fishery of Australia? PLoS One 7:e32547
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 Mol Integr Physiol 162:94–100
Butler PJ, Taylor EW (1971) Response of the dogfish (Scyliorhinus canicula L.) to slowly induced and rapidly induced hypoxia. Comp Biochem Physiol A Physiol 39:307–323
Butler P, Taylor E (1975) The effect of progressive hypoxia on respiration in the dogfish (Scyliorhinus canicula) at different seasonal temperatures. J Exp Biol 63:117–130
Caldwell CA, Hinshaw JM (1994) Nucleotides and the adenylate energy charge as indicators of stress in rainbow trout (Oncorhyncus mykiss) subjected to a range of dissolved oxygen concentrations. Comp Biochem Physiol B Biochem Mol Biol 109:313–323
Cartamil DP, Sepulveda CA, Wegner NC, Aalbers SA, Baquero A, Graham JB (2011) Archival tagging of subadult and adult common thresher sharks (Alopias vulpinus) off the coast of southern California. Mar Biol 158:935–944
Cliff G, Thurman G (1984) Pathological and physiological effects of stress during capture and transport in the juvenile dusky shark, Carcharhinus obscurus. Comp Biochem Physiol A Physiol 78:167–173
Coles, JA, Sigg, DC, Iaizzo, PA (2009) Reversible and irreversible damage of the myocardium: new ischemic syndromes, ischemia/reperfusion injury, and cardioprotection. In: Iaizzo PA (ed) Handbook of cardiac anatomy, physiology, and devices (2nd edn), pp 219–229. (Springer Science + Business Media, LLC)
Cosgrove R, Arregui I, Arrizabalaga H, Goni N, Neilson JD (2015) Predation of pop-up satellite archival tagged albacore (Thunnus alalunga). Fish Res 162:48–52
Dalla Via J, van den Thillart G, Cattani O, Dezwaan A (1994) Influence of long-term hypoxia exposure on the energy metabolism of Solea solea. II. Intermediary metabolism in blood, liver and muscle. Mar Ecol Prog Ser 111:17–27
Dapp DR, Walker TI, Huveneers C, Reina RD (2015) Respiratory mode and gear type are important determinants of elasmobranch immediate and post-release mortality. Fish Fish. doi:10.1111/faf.12124
Davie PS, Farrell AP (1991) Cardiac performance of an isolated heart preparation from the dogfish (Squalus acanthias)—the effects of hypoxia and coronary-artery perfusion. Can J Zool Revue Canadienne de Zoologie 69:1822–1828
Development Core Team R (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Divers SJ, Boone SS, Berliner A, Kurimo EA, Boysen KA, Johnson DR, Killgore KJ, George SG, Hoover JJ (2013) Nonlethal acquisition of large liver samples from free-ranging river sturgeon (Scaphirynchus) using single-entry endoscopic biopsy forceps. J Wildl Dis 49:321–331
Driedzic WR, Hochachka PW (1976) Control of energy metabolism in fish white muscle. Am J Physiol 230:579–582
Dulvy NK, Fowler SL, Musick JA, Cavanagh RD, Kyne PM, Harrison LR, Carlson JK, Davidson LNK, Fordham SV, Francis MP, Pollock CM, Simpfendorfer CA, Burgess GH, Carpenter KE, Compagno LJV, Ebert DA, Gibson C, Heupel MR, Livingstone SR, Sanciangco JC, Stevens JD, Valenti S, White WT (2014) Extinction risk and conservation of the world’s sharks and rays. Elife 3:1–34
Eltzschig HK, Collard CD (2004) Vascular ischaemia and reperfusion injury. Br Med Bull 70:71–86
Frick LH, Reina RD, Walker TI (2009) The physiological response of Port Jackson sharks and Australian swellsharks to sedation, gill-net capture, and repeated sampling in captivity. North Am J Fish Manag 29:127–139
Frick LH, Reina RD, Walker TI (2010a) Stress related physiological changes and post-release survival of Port Jackson sharks (Heterodontus portusjacksoni) and gummy sharks (Mustelus antarcticus) following gill-net and longline capture in captivity. J Exp Mar Biol Ecol 385:29–37
Frick LH, Walker TI, Reina RD (2010b) Trawl capture of Port Jackson sharks, Heterodontus portusjacksoni, and gummy sharks, Mustelus antarcticus, in a controlled setting: effects of tow duration, air exposure and crowding. Fish Res 106:344–350
Frick LH, Walker TI, Reina RD (2012) Immediate and delayed effects of gill-net capture on acid-base balance and intramuscular lactate concentration of gummy sharks, Mustelus antarcticus. Comp Biochem Physiol A Mol Integr Physiol 162:88–93
Gallagher AJ, Serafy JE, Cooke SJ, 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
Gamperl, AK, Driedzic, WR (2009) Cardiovascular function and cardiac metabolism. In: Richards JG, Farrell AP, Brauner CJ (eds) Hypoxia, vol 27. Elsevier Academic Press, USA, pp 301–360
Giesy JP (1988) Phosphoadenylate concentrations and adenylate energy-charge of largemouth bass (Micropterus salmoides): relationship with condition factor and blood cortisol. Comp Biochem Physiol A Physiol 90:367–377
Haya K, Waiwood BA, Vaneeckhaute L (1985) Disruption of energy metabolism and smoltification during exposure of juvenile Atlantic salmon (Salmo salar) to low pH. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 82:323–329
Heath AG (1984) Changes in tissue adenylates and water content of bluegill, Lepomis macrochirus, exposed to copper. J Fish Biol 24:299–309
Holts DB, Bedford DW (1993) Horizontal and vertical movements of the shortfin mako shark, Isurus oxyrhincus, in the Southern California Bight. Aust J Mar Freshw Res 44:901–909
Hyatt MW, Anderson PA, O’Donnell PM, Berzins IK (2012) Assessment of acid-base derangements among bonnethead (Sphyrna tiburo), bull (Carcharhinus leucas), and lemon (Negaprion brevirostris) sharks from gillnet and longline capture and handling methods. Comp Biochem Physiol A Mol Integr Physiol 162:113–120
Ip YK, Chew SF (2010) Ammonia production, excretion, toxicity, and defense in fish: a review. Frontiers in Physiology 1:134
Jibb LA, Richards JG (2008) AMP-activated protein kinase activity during metabolic rate depression in the hypoxic goldfish, Carassius auratus. J Exp Biol 211:3111–3122
Jorgensen JB, Mustafa T (1980) The effect of hypoxia on carbohydrate metabolism in flounder (Platichthys flesus L.)—II. High energy phosphate compounds and the role of glycolytic and gluconeogenetic enzymes. Comp Biochem Physiol B Biochem Mol Biol 67:249–256
Konietschke F, Placzek M, Schaarschmidt F, Hothorn LA (2014) nparcomp: an R software package for nonparametric multiple comparisons and simultaneous confidence intervals. J Stat Softw 61:1–17
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
Marshall H, Field L, Afiadata A, Sepulveda C, Skomal G, Bernal D (2011) Hematological indicators of stress in longline-captured sharks. Comp Biochem Physiol A Mol Integr Physiol 162:121–129
Moyes C, Fragoso N, Musyll M, Brill R (2006) Predicting postrelease survival in large pelagic fish. Trans Am Fish Soc 135:1389–1397
Noguchi K, Gel YR, Brunner E, Konietschke F (2012) nparLD: an R software package for the nonparametric analysis of longitudinal data in factorial experiments. J Stat Softw 50:1–23
Piiper J, Baumgarten D, Meyer M (1970) Effects of hypoxia upon respiration and circulation in the dogfish Scyliorhinus stellaris. Comp Biochem Physiol 36:513–520
Renshaw GMC, Kerrisk CB, Nilsson GE (2002) The role of adenosine in the anoxic survival of the epaulette shark, Hemiscyllium ocellatum. Comp Biochem Physiol B Biochem Mol Biol 131:133–141
Renshaw GMC, Wise G, Dodd PR (2010) Ecophysiology of neuronal metabolism in transiently oxygen-depleted environments: evidence that GABA is accumulated pre-synaptically in the cerebellum. Comp Biochem Physiol A Mol Integr Physiol 155:486–492
Renshaw GMC, Kutek AK, Grant GD, Anoopkumar-Dukie S (2012) Forecasting elasmobranch survival following exposure to severe stressors. Comp Biochem Physiol A Mol Integr Physiol 162:101–112
Richards JG (2009) Metabolic and molecular responses of fish to hypoxia. In: Richards JG, Farrell AP, Brauner CJ (eds) Hypoxia, vol 27. Elsevier Academic Press, USA, pp 443–485
Richards JG, Heigenhauser GJF, Wood CM (2003) Exercise and recovery metabolism in the pacific spiny dogfish (Squalus acanthias). J Comp Physiol B 173:463–474
Robbins WD (2006) Evaluation of two underwater biopsy probes for in situ collection of shark tissue samples. Mar Ecol Prog Ser 310:213–217
Singer M (1998) Management of multiple organ failure: guidelines but no hard-and-fast rules. J Antimicrob Chemother 41:103–112
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 Mol Integr Physiol 162:146–155
Soengas JL, Aldegunde M (2002) Energy metabolism of fish brain. Comp Biochem Physiol B Biochem Mol Biol 131:271–296
Speers-Roesch B, Treberg JR (2010) The unusual energy metabolism of elasmobranch fishes. Comp Biochem Physiol A Mol Integr Physiol 155:417–434
Speers-Roesch B, Brauner CJ, Farrell AP, Hickey AJR, Renshaw GMC, Wang YS, Richards JG (2012a) Hypoxia tolerance in elasmobranchs. II. Cardiovascular function and tissue metabolic responses during progressive and relative hypoxia exposures. J Exp Biol 215:103–114
Speers-Roesch B, Richards JG, Brauner CJ, Farrell AP, Hickey AJ, Wang YS, Renshaw GM (2012b) Hypoxia tolerance in elasmobranchs. I. Critical oxygen tension as a measure of blood oxygen transport during hypoxia exposure. J Exp Biol 215:93–102
Speers-Roesch B, Mandic M, Groom DJE, Richards JG (2013) Critical oxygen tensions as predictors of hypoxia tolerance and tissue metabolic responses during hypoxia exposure in fishes. J Exp Mar Biol Ecol 449:239–249
Stenslokken KO, Sundin L, Renshaw GMC, Nilsson GE (2004) Adenosinergic and cholinergic control mechanisms during hypoxia in the epaulette shark (Hemiscyllium ocellatum), with emphasis on branchial circulation. J Exp Biol 207:4451–4461
Storey KB, Storey JM (2005) Oxygen limitation and metabolic rate depression. In: KB Storey (ed) Functional metabolism. Wiley, USA, pp 415–442
Sugaya M, Yasuda T, Suga T, Okita K, Abe T (2011) Change in intramuscular inorganic phosphate during multiple sets of blood flow-restricted low-intensity exercise. Clin Physiol Funct Imaging 31:411–413
Tresise MM, Mokae MLL, Wagenaar GM, Van Dyk JC (2014) A proposed liver needle core biopsy technique for the sharptooth catfish Clarias gariepinus (Burchell) for use in fish health research. J Fish Dis 37:931–934
van den Thillart G, Kesbeke F, Waarde AV (1980) Anaerobic energy-metabolism of goldfish, Crassius auratus (L.)—influence of hypoxia and anoxia on phosphorylated compounds and gycogen. J Comp Physiol 136:45–52
Van der Boon J, de Jong RL, Van den Thillart G, Addink ADF (1992) Reversed-phase ion-paired HPLC of purine nucleotides from skeletal muscle, heart and brain of the goldfish, Crassius auratus L.-II. Influence of environmental anoxia on metabolite levels. Comp Biochem Physiol B Biochem Mol Biol 101:583–586
Van Rijn JA, Reina RD (2010) Distribution of leukocytes as indicators of stress in the Australian swellshark, Cephaloscyllium laticeps. Fish Shellfish Immunol 29:534–538
Vetter RD, Hodson RE (1982) Use of adenylate concentrations and andenylate energy-charge as indicators of hypoxic stress in estuarine fish. Can J Fish Aquat Sci 39:535–541
Yoshino M, Yamamoto C, Murakami K, Katsumata Y, Mori S (1992) Stabilization of the adenylate energy charge—charge in erythrocytes of rats and humans at high-altitude hypoxia. Comp Biochem Physiol A Physiol 101:65–68
Acknowledgments
We thank Carolina and Thomas Weller, Derek Dapp, Lauren Hall and Ricky Tate for fieldwork and manuscript assistance. We thank Roderick Watson and Elizabeth McGrath from the Victorian Marine Science Consortium (VMSC) and Phillip Holt from Monash University for logistical assistance. Funding for this study was provided by the Australian Research Council (ARC) Linkage Grant LP110200572, the Department of Economic Development, Jobs, Transport and Resources Victoria, Australian Fisheries Management Authority (AFMA) and Melbourne Aquarium. This study was conducted in accordance with Monash University Animal Ethics approval number BSCI/2012/16 and DELWP Fisheries permit number RP1115.
Author information
Authors and Affiliations
Corresponding authors
Additional information
Communicated by G. Heldmaier.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Guida, L., Walker, T.I. & Reina, R.D. The adenylate energy charge as a new and useful indicator of capture stress in chondrichthyans. J Comp Physiol B 186, 193–204 (2016). https://doi.org/10.1007/s00360-015-0948-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00360-015-0948-y