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The Physiological Response of the Caribbean Reef Shark (Carcharhinus Perezi)To Longline Capture☆

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The Physiological Response of the Caribbean Reef Shark (Carcharhinus Perezi)To Longline Capture☆ Comparative Biochemistry and Physiology, Part A 162 (2012) 94–100 Contents lists available at ScienceDirect Comparative Biochemistry and Physiology, Part A journal homepage: www.elsevier.com/locate/cbpa The physiological response of the Caribbean reef shark (Carcharhinus perezi)to longline capture☆ Edward J. Brooks a,b,⁎, John W. Mandelman c, Katherine A. Sloman d, Stephanie Liss a,e, Andy J. Danylchuk f, Steven J. Cooke g, Gregory B. Skomal h, David P. Philipp e, David W. Sims b,i, Cory D. Suski e a Shark Research and Conservation Program, Cape Eleuthera Institute, Eleuthera, The Bahamas b School of Marine Science and Engineering, University of Plymouth, Plymouth, United Kingdom c Edgerton Research Laboratory, New England Aquarium, Central Wharf, Boston, MA, 02110-3399, USA d School of Science, University of the West of Scotland, Paisley, Scotland, United Kingdom e Department of Natural Resources and Environmental Sciences, University of Illinois, Urbana, IL, 61801, USA f Department of Environmental Conservation, University of Massachusetts, Amherst, MA, USA g Fish Ecology and Conservation Physiology Laboratory, Department of Biology and Institute of Environmental Science, Carleton University, Ottawa, ON, K1S 5B6, Canada h Massachusetts Division of Marine Fisheries, 838 South Rodney French Blvd., New Bedford, MA 02744, USA i Marine Biological Association of the United Kingdom, The Laboratory, Citadel Hill, Plymouth, United Kingdom article info abstract Article history: Longline fishing is the most common elasmobranch capture method around the world, yet the physiological Received 2 March 2011 consequences of this technique are poorly understood. To quantify the sub-lethal effects of longline capture in Received in revised form 21 April 2011 the commonly exploited Caribbean reef shark (Carcharhinus perezi), 37 individuals were captured using Accepted 25 April 2011 standard, mid-water longlines. Hook timers provided hooking duration to the nearest minute. Once sharks Available online 13 May 2011 were landed, blood samples were taken and used to measure a suite of physiological parameters. Control data were obtained by sampling an additional three unrestrained Caribbean reef sharks underwater at an Keywords: – Caribbean reef shark established shark feeding site. The greatest level of physiological disruption occurred after 120 180 min of Carcharhinus perezi hooking, whereas sharks exposed to minimal and maximal hook durations exhibited the least disturbed blood Longline chemistry. Significant relationships were established between hooking duration and blood pH, pCO2, lactate, Survivorship glucose, plasma calcium and plasma potassium. Longline capture appears more benign than other methods Capture stress assessed to date, causing a shift in the stress response from acute at the onset of capture to a sub-acute regime Blood chemistry as the capture event progresses, apparently facilitating a degree of physiological recovery. Continued Non-linear stress response investigation into the physiological response of elasmobranchs to longline capture is vital for the effective Parabolic stress response management of such fisheries. © 2011 Elsevier Inc. All rights reserved. 1. Introduction (Wikelski and Cooke, 2006; Cooke and O'Connor, 2010). Documenting the physiological consequences of longline capture in sharks is a vital Longline fishing is thought to be the predominant method of undertaking for effective fisheries management because it can provide commercial capture for sharks (Beerkircher et al., 2002; Lewison et al., insights into the underlying causes of at-vessel mortality and into the 2004; Gilman et al., 2008). In the majority of longline fisheries all or viability of animals post release (Skomal, 2007). part of the shark is harvested, however, in some areas large numbers The capture and release of a shark induces various degrees of of sharks are released alive, due to low species-specific commercial physical trauma and physiological stress, the magnitude of which is value (Beerkircher et al., 2002) and/or to comply with fisheries thought to be dependent on the capture method, capture duration, regulations (Morgan et al., 2009). The emerging discipline of and the specific metabolic capacity of the species (Skomal, 2006; conservation physiology is focused on using physiological tools Skomal, 2007; Mandelman and Skomal, 2009). If physiological stress, and knowledge to understand and address conservation problems physical trauma, or a combination of the two is excessive, then immediate or delayed (post-release) mortality is possible (Skomal, 2007). In cases where sharks survive the capture event, a suite of ☆ This paper stems from a presentation in the Symposium "The Physiological Stress homeostatic disruptions can potentially impact growth, feeding, Response in Elasmobranch Fishes", at the 26th annual meeting of the American swimming behaviour, and the immune system, leading to population- Elasmobranch Society, held on July 11, 2010, in Providence, Rhode Island (USA). level consequences (Cooke et al., 2002; Skomal, 2007). ⁎ Corresponding author at: Shark Research and Conservation Program, Cape Eleuthera Institute, PO Box EL-26029, Eleuthera, The Bahamas. Tel.: +1 242 334 8552. Although the study of elasmobranch stress physiology is very much E-mail address: [email protected] (E.J. Brooks). in its infancy, the physiological effects of capture have been quantified 1095-6433/$ – see front matter © 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.cbpa.2011.04.012 E.J. Brooks et al. / Comparative Biochemistry and Physiology, Part A 162 (2012) 94–100 95 for a number of different species and gear types. The majority of Once a candidate shark was identified, its position on the line was research to date has focused on the physiological effects of recreational marked with a numbered and coloured marker and the time of rod and reel capture (e.g. Heberer et al., 2010), however, the effects of hooking back-calculated from the elapsed time on the hook timer. both gillnet (e.g. Frick et al., 2010)andtrawlcapture(Mandelman and Only animals cleanly hooked in the corner of the jaw were selected for Farrington, 2007) have also been quantified. In those studies that sampling. To quantify the physiological stress response over a broad quantified capture duration, the magnitude of the stress response was time range, the hooking duration of each candidate animal was found to be proportional to the magnitude of the stressor, which in the manipulated to encompass up to four hours on the line. The shark was case of most capture events is determined by capture duration and gear then retrieved from the line, secured alongside the boat, and placed in type (Skomal and Bernal, 2010). Despite being the most common tonic immobility (Henningsen, 1994) for blood sampling by caudal capture method for sharks, the physiological consequences of longline venipuncture. Hook duration was defined as the time between capture have received very little attention, with only four published hooking and phlebotomy. Following blood sampling, the hook was studies to date (Moyes et al., 2006; Hight et al., 2007; Mandelman and removed and the animal released. Skomal, 2009; Frick et al., 2010); none of these studies quantified the magnitude of the stress response relative to capture duration. 2.2. Blood collection and analyses It has been suggested that there is considerable inter-specific variation in the stress response in sharks, likely associated with dif- Blood (~3 mL) was drawn by caudal venipuncture using a 38 mm, ferences in metabolic scope (Mandelman and Skomal, 2009). How- 20 gauge needle and a 3 mL syringe (Becton, Dickinson and Company, ever, the response to capture has yet to be assessed for the majority of Franklin Lakes, NJ, USA). All syringes were washed with the species commonly captured on longlines. This information is vital to anticoagulant sodium heparin prior to drawing blood. Approximately understanding the causative factors of at-vessel-mortality and the 95 μl of whole blood was immediately transferred from the syringe viability of sharks post release, both of which have implications for into an iStat CG4+ cartridge, which was in turn inserted into an iStat elasmobranch fisheries management (Moyes et al., 2006). point of care device (Heska Corporation, Fort Collins, CO, USA) for The Caribbean reef shark (C. perezi) is an abundant, large bodied, immediate analysis of pCO2, pH, and lactate levels (Mandelman and reef-associated, apex predator distributed throughout the tropical Farrington, 2007; Mandelman and Skomal, 2009; Gallagher et al., and sub-tropical western Atlantic and greater Caribbean (Compagno, 2010). The time from blood draw to the insertion of the cartridge into 1984). Although fisheries data pertaining to the Caribbean reef shark the iStat was b30 s. Glucose was measured by adding 10 μL of whole are sparse, there are indications that it is commonly captured by blood directly from the syringe to an Accu-Chek glucose metre longline fisheries throughout its range (Amorim et al., 1998; Arocha (Roche Diagnostics, Basel, Switzerland), which had previously been et al., 2002; Rosa et al., 2006). In the United States, it is a prohibited validated for use on fish (Cooke et al., 2008). To calculate haematocrit, species, which is commonly captured and subsequently released a small volume of whole blood was transferred to a 75 mm micro- in the bottom set longline fishery off the Florida Keys (Morgan haematocrit tube (Drummond Scientific, Broomall, PA, USA), the
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