1. Manire C, Hueter R, Hull E, et al. serological changes associated with gill-net capture and restraint in three species of sharks. Trans Am Fish Soc 2001; 130:1038–1048.
2. Wise G, Mulvey JM, Renshaw GM. Hypoxia tolerance in the epaulette shark (Hemiscyllium ocellatum). J Exp Zool 1998; 281:1–5.
3. Hamlett WC. Sharks, skates, and rays. In: Hamlett WE, ed. The biology of elasmobranch fishes. Baltimore: The Johns Hopkins University Press, 1999.
4. Dickson KA, Gregorio MO, Gruber SJ, et al. Biochemical indices of aerobic and anaerobic capacity in muscle tissues of California elasmobranch fishes differing in typical activity level. Marine Biol 1993; 117:185–193.
5. Mandelmann JW, Skomel GB. Differential sensitivity to capture stress assessed by blood acid-base status in five carcharinid sharks. J Comp Physiol B 2009; 179:267–277.
6. Skomal G. The physiological effects of capture and post-release survivorship in large pelagic fishes. Fish Manage Ecol 2007; 14:81–89.
7. Wells RM, Dunphy BJ. Potential impact of metabolic acidosis on the fixed-acid Bohr effect in snapper (Pagrus auratus) following angling stress. Comp Biochem Physiol A Mol Integr Physiol 2009; 154:56–60.
8. Cooke SJ, Suski CD, Danylchuk SE, et al. Effects of different capture techniques on the physiological condition of bonefish Albula vulpes evaluated using field diagnostic tools. J Fish Biol 2008; 73:1351–1375.
9. Hoffmayer ER, Parsons GR. The physiological response to capture and handling stress in the Atlantic sharpnose shark, Rhizoprionodon terraenovae. Fish Physiol Biochem 2001; 25:277–285.
10. Suski CD, Cooke SJ, Danylchuk AJ, et al. Physiological disturbances and recovery dynamics of bonefish (Albula vulpes), a tropical marine fish, in response to variable exercise and exposure to air. Comp Biochem Physiol Part A 2007; 148:664–673.
11. Mandelmann JW, Farrington MA. The physiological stats and mortality associated with otter-trawl capture, transport, and captivity of an exploited elasmobranch, Squalus acanthias. ICES J Marine Sci 2007; 64:122–130.
12. Frick LH, Reina RD. The physiological response of Port Jackson sharks and Australian swellsharks to sedation, gill-net capture, and repeated sampling in captivity. North Am J Fisheries Manag 2009; 29:127–139.
13. Kieffer JD. Limits to exhaustive exercise in fish. Comp Biochem Physiol A Mol Integr Physiol 2000; 126:161–179.
14. Lee G, Farrell AP, Lotto A, et al. Excess post-exercise oxygen consumption in adult sockeye (Oncorhynchus nerka) and coho (O. kisutch) salmon following critical speed swimming. J Exp Biol 2003; 206:3253–3260.
15. Richards JG, Heigenhauser GJF, Wood CM. Exercise and recovery metabolism in the pacific spiny dogfish (Squalus acanthias). J Comp Physiol B 2003; 173:463–474.
16. Cliff G, Thurman GD. Pathological and physiological effects of stress during capture and transport in the juvenile dusky shark, Carcharhinus obscurus. Comp Biochem Physiol 1984;78A:167–173.
17. Spargo AL, Kohler N, Skomel G, et al. The physiological effects of angling on post-release survivorship in juvenile sandbar sharks (Carcharhinus plumbeus), in Proceedings. Am Elasmobranch Soc Annu Meet 2001. Available at: www.flmnh.ufl.edu/fish/organizations/aes/abst2001d.htm. Accessed Oct 1, 2010.
18. Wells RM, McIntyre RH, Morgan AK, et al. Physiological stress responses in big gamefish after capture: observations on plasma chemistry and blood factors. Comp Biochem Physiol A 1986; 84:565–571.
19. Arlinghaus R, Klefoth T, Cooke SJ, et al. Physioloical and behavioral consequences of catch-and-release angling on northern pike (Esox lucius L.) Fisheries Res 2009; 97:223–233.
20. Robin ED, Murdaugh HV, Millen JE. Acid-base, fluid and electrolyte metabolism in the elasmobranch. 3. Oxygen, CO-2, bicarbonate and lactate exchange across the gill. J Cell Physiol 1966; 67:93–100.
21. Ferguson RA, Tufts BL. Physiological effects of brief air exposure in exhaustively exercised rainbow trout (Oncorhynchus mykiss): implications for ‘catch and release’ fisheries. Can J Fish Aquat Sci 1992; 49:1157–1162.
22. Hanley CS, Clyde VL, Wallace RS, et al. Effects of anesthesia and surgery on serial blood gas values and lactate concentrations in yellow perch (Perca flavescens), walleye pike (Sander vitreus), and koi (Cyprinus caprio). J Am Vet Med Assoc 2010; 236:1104–1108.
23. Wood CM, Turner JD, Graham MS. Why do fish die after severe exercise? J Fish Biol 1983; 22:189–201.
24. Cooper AR, Morris S. The blood respiratory, haematological, acid-base and ionic status of the Port Jackson shark, Heterodontus portusjacksoni, during recovery from anaesthesia and surgery—a comparison with sampling by direct caudal puncture. Comp Biochem Physiol 1998;119A:895–903.
25. Carlson JK, Parsons GR. Respiratory and hematological responses of the bonnethead shark, Sphyrna tiburo, to acute changes of dissolved oxygen. J Exp Marine Biol Ecol 2003; 294:15–26.
26. Piiper J, Baumgarten, D. Blood lactate and acid-base balance in the elasmobranch Scyliorhinus stellaris after exhausting activity Pubbl Staz Zool Napoli 1969; 37:84–94.
27. Skov PV, Bennett MB. The secondary vascular system of Actinopterygii: interspecific variation in origins and investmen. Zoomorphology 2003; 122:181–190.
28. Olson KR. Secondary circulation in fish: anatomical organization and physiological significance. J Exp Zool 1996; 275:172–185.
29. Chopin LK, Amey AP, Bennett MB. A systemic secondary vessel system is present in the teleost fish Tandanus tandanus and absent in the elasmobranchs Carcharhinus melanopterus and Rhinobatos typus and in the dipnoan Neoceratodus forsteri. J Zool 1998; 246:105–110.
30. Steffensen JF, Lomholt JP. The secondary vascular system. In: Hoar WS, Randall DJ, Farrell AP, eds. Fish physiology. Vol 12A. San Diego: Academic Press, 1992;185–217.
31. Vogel WOP. Systemic vascular anastomoses, primary and secondary vessels in fish, and the phylogeny of lymphatics. In: Cardiovascular shunts: phylogenetic, ontogenetic and clinical aspects. Vol 22. Copenhagen: Muskegaard, 1985; 21:143–159.
32. Berzins IK, Whitaker MS, March G, et al. Delineation of the vasculature associated with the cranial dorsal fin in the smooth dogfish shark (Mustelus canis) and the brown shark (Carcharinus plumbeus) (abstr), in Proceedings. Annu Meet Int Assoc Aquatic Anim Med 1998;131.
33. Satchell GH. Circulatory system: distinctive attributes of the circulation of elasmobranch fish. In: Hamlett WC, ed. Sharks, skates, and rays: the biology of elasmobranch fishes. Baltimore: The Johns Hopkins University Press, 1999;218–237.
34. Mylniczenko ND, Curtis EW, Wilborn RE, et al. Differences in hematocrit of blood samples obtained from two venipuncture sites in sharks. Am J Vet Res 2006; 67:1861–1864.
35. Alistair DM, Dove, Arnold J, et al. Blood cells and serum chemistry in the world's largest fish: the whale shark Rhincodon typus. Aquatic Biol 2010; 9:177–183.
36. Harrenstein LA, Tornquist SJ, Miller-Morgan TJ, et al. Evaluation of a point-of-care blood analyzer and determination of reference ranges for blood parameters in rockfish. J Am Vet Med Assoc 2005; 226:255–265.
37. Gallagher AJ, Frick LH, Bushnell PG, et al. Blood gas, oxygen saturation, pH, and lactate values in elasmobranch blood measured with a commercially available portable clinical analyzer and standard laboratory instruments. J Aquatic Anim Health 2010; 22:229–234.
38. Innis CJ, Tlusty M, Merigo C, et al. Metabolic and respiratory status of cold-stunned Kemp's ridley sea turtles (Lepidochelys kempii). J Comp Physiol B 2007; 177:623–630.
39. Jensen AL, Kjelgaard-Hansen M. Method comparison in the clinical laboratory. Vet Clin Pathol 2006; 35:276–286.
40. Bland JM, Altman DG. Statistical methods for assessing agreement between two methods of clinical measurement. Lancet 1986; 1:307–310.
41. Zady MF. Z-12: correlation and simple least squares regression. Available at: www.westgard.com/lessons-5.htm. Accessed May 23, 2010.
42. Chapman CA, Renshaw GM. Hematological responses of the grey carpet shark (Chiloscyllium punctattum) and epaulette shark (Hemiscyllium ocellatum) to anoxia and re-oxygenation. J Exp Zool A Ecol Genet Physiol 2009; 311:422–438.
43. Lowe TE, Wells RMG, Baldwin J. Absence of regulated blood-oxygen transport in response to strenuous exercise by the Shovel-nosed Ray, Rhinobatos typus. Mar Freshw Res 1995; 46:441–446.
44. Quesenberry KE, Rosenthal KL. Endocrine diseases. In: Quesenberry KE, Carpenter JW, eds. Ferrets, rabbits, and rodents clinical medicine and surgery. 2nd ed. Philadelphia: WB Saunders Co, 2004;79–90.
45. Torres Filho IP, Martuchelli Filho V, et al. In vivo observations on the microcirculation of the catfish (Hypostomus of punctatus) fin. Comp Biochem Physiol 1994; 107:43–47.
Advertisement
Objective—To establish reference ranges for critical care blood values measured in wild and aquarium-housed elasmobranchs by use of a point-of-care (POC) blood analyzer and to compare values on the basis of species category (pelagic, benthic, or intermediate) and phlebotomy site.
Design—Cross-sectional study.
Animals—66 wild and 89 aquarium-housed elasmobranchs (sharks and rays).
Procedures—Aquarium-housed elasmobranchs were anesthetized for sample collection; wild elasmobranchs were caught via hook and line fishing, manually restrained for sample collection, and released. Blood was collected from 2 sites/fish (dorsal sinus region and tail vasculature) and analyzed with the POC analyzer. Reference values of critical care blood analytes were calculated for species most represented in each population. Values were compared on the basis of species categorization (pelagic, intermediate, or benthic) and collection site.
Results—Oxygen saturation and circulating concentrations of lactate and glucose were significantly different among aquarium-housed pelagic, intermediate, and benthic species. Lactate concentration was significantly different among these categories in wild elasmobranchs. Significant differences were detected between samples from the 2 collection sites for all blood analytes. In both study populations, pH and lactate values were infrequently < 7.2 or > 5 mmol/L, respectively.
Conclusions and Clinical Relevance—Brevity of handling or chemical restraint may have reduced secondary stress responses in fish because extreme variations in blood analyte values were infrequent. Sample collection site, species categorization, acclimation to handling, and restraint technique should be considered when assessing values obtained with the POC analyzer used in this study for blood analytes and immediate metabolic status in elasmobranchs.
Dr. Mylniczenko's present address is Disney's Animals, Science & Environment, PO Box 10,000, Lake Buena Vista, FL 32830.
Dr. Zachariah's present address is Brevard Zoo, 8225 N Wickham Rd, Melbourne, FL 32940.
Ms. Wilborn's present address is Cooperative Institute for Marine and Atmospheric Studies, Rosenstiel School for Marine and Atmospheric Science, University of Miami, Miami, FL 33149.
Supported by the John G. Shedd Aquarium and Chicago Zoological Society. The point-of-care blood analyzer products used in this study were provided by Dr. Nancy Wisnewski at Heska Corp.
The authors thank Dr. Dawn Zimmerman, George Parsons, Stacy Schultz, and Dr. Michelle Davis for technical support and the John G. Shedd Aquarium and Chicago Zoological Society for provision of equipment.