Tissue-specific isotope trophic discrimination factors and turnover rates in a marine elasmobranch: Empirical and modeling results

Canadian Journal of Fisheries and Aquatic Sciences

Volumn 69, Issue 3, 2012, Pages 551-564

  Malpica Cruz, Luis ^a   Herzka, Sharon Z ^a,b   Sosa Nishizaki, Oscar ^a   Lazo, Juan Pablo ^a  

^a Center for Scientific Research and Higher Education of Ensenada (CICESE)   (United States)

^b CENTRO DE INVESTIGACIÓN CIENTÍFICA Y DE EDUCACIÓN SUPERIOR DE ENSENADA   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMASS; BLOOD; BODY SIZE; CARBON ISOTOPE; DIET; GROWTH RATE; ISOTOPIC ANALYSIS; LABORATORY METHOD; MARINE ECOSYSTEM; MUSCLE; NITROGEN ISOTOPE; SHARK; TURNOVER; WILD POPULATION;

CHONDRICHTHYES; ELASMOBRANCHII; FELIDAE; TELEOSTEI; TRIAKIS; TRIAKIS SEMIFASCIATA;

EID: 84857826940     PISSN: 0706652X     EISSN: 12057533     Source Type: Journal    
DOI: 10.1139/F2011-172     Document Type: Article

References (51)

1. Association of Official Analytical Chemists. 1990. 16th ed. Official methods of analysis of AOAC. Vol. 1. Association of Official Analytical Chemists, Arlington, Va., USA.
2. Burnham, K.P., and Anderson, D.R. 2002. Model selection and inference: a practical information-theoretic approach. 2nd ed. Springer-Verlag, New York.
3. Carleton, S.A., and Martínez del Rio, C. 2010. Growth and catabolism in isotopic incorporation: a new formulation and experimental data. Funct. Ecol. 24(4): 805-812. doi:10.1111/j.1365-2435.2010.01700.x.
4. DeNiro, M.J., and Epstein, S. 1977. Mechanism of carbon isotope fractionation associated with lipid synthesis. Science, 197(4300): 261-263. doi:10.1126/science.327543. PMID:327543.
5. DeNiro, M.J., and Epstein, S. 1978. Influence of diet on the distribution of carbon isotopes in animals. Geochim. Cosmochim. Acta, 42(5): 495-506. doi:10.1016/0016-7037(78)90199-0.
6. Dulvy, N.K., and Reynolds, J.D. 1997. Evolutionary transitions among egg-laying, live-bearing and maternal inputs in sharks and rays. Proc. Biol. Sci. 264(1386): 1309-1315. doi:10.1098/rspb.1997.0181.
7. Estrada, J.A., Rice, A.N., Lutcavage, M.E., and Skomal, G.B. 2003. Predicting trophic position in sharks of the north-west Atlantic Ocean using stable isotope analysis. J. Mar. Biol. Assoc. U.K. 83(6): 1347-1350. doi:10.1017/S0025315403008798.
8. Evans, D.H., Piermarini, P.M., and Choe, K.P. 2004. Homeostasis: osmoregulation, pH regulation, and nitrogen excretion In The biology of sharks and their relatives. Edited by J.C. Carrier, J.A. Musick, and M.R. Heithaus. CRC Press, New York. pp. 247-265.
9. Ferry-Graham, L.A. 1998. Effects of prey size and mobility on preycapture kinematics in leopard sharks Triakis semifasciata. J. Exp. Biol. 201(16): 2433-2444. PMID:9679105.
10. Fisk, A.T., Tittlemier, S.A., Pranschke, J.L., and Norstrom, R.J. 2002. Using anthropogenic contaminants and stable isotopes to assess the feeding ecology of Greenland sharks. Ecology, 83(8): 2162-2172. doi:10.1890/0012-9658(2002)083[2162:UACASI]2.0.CO;2.
11. 12C turnover during growth of brown shrimp (Penaeus aztecus). Oecologia, 54(2): 200-204. doi:10.1007/BF00378393.
12. Gannes, L.Z., O'Brien, D.M., and Martínez del Rio, C. 1997. Stable isotopes in animal ecology: assumptions, caveats, and a call for more laboratory experiments. Ecology, 78(4): 1271-1276. doi:10.1890/0012-9658(1997)078[1271:SIIAEA]2.0.CO;2.
13. 13C values in Nile tilapia, Oreochromis niloticus. Naturwissenschaften, 91(2): 90-93. doi:10.1007/s00114-003-0496-2. PMID:14991147.
14. Graham, J.B., Dewar, H., Lai, N.C., Lowell, W.R., and Arce, S.M. 1990. Aspects of shark swimming performance determined using a large water tunnel. J. Exp. Biol. 151: 175-192.
15. Graham, B.S., Grubbs, D., Holland, K., and Popp, B.N. 2007. A rapid ontogenetic shift in the diet of juvenile yellowfin tuna from Hawaii. Mar. Biol. 150(4): 647-658. doi:10.1007/s00227-006-0360-y.
16. Hammerschlag, N. 2006. Osmoregulation in elasmobranchs: a review for fish biologist, behaviourists and ecologists. Mar. Freshwat. Behav. Physiol. 39(3): 209-228. doi:10.1080/10236240600815820.
17. Herzka, S.Z. 2005. Assessing connectivity of estuarine fishes based on stable isotope ratio analysis. Estuar. Coast. Shelf Sci. 64(1): 58-69. doi:10.1016/j.ecss.2005.02.006.
18. Herzka, S.Z., and Holt, G.J. 2000. Changes in isotopic composition of red drum (Sciaenops ocellatus) larvae in response to dietary shifts: potential applications to settlement studies. Can. J. Fish. Aquat. Sci. 57(1): 137-147. doi:10.1139/f99-174.
19. Herzka, S.Z., Holt, S.A., and Holt, G.J. 2001. Documenting the settlement history of individual fish larvae using stable isotope ratios: model development and validation. J. Exp. Mar. Biol. Ecol. 265(1): 49-74. doi:10.1016/S0022-0981(01)00324-0.
20. 15N. Can. J. Fish. Aquat. Sci. 50(10): 2071-2076. doi:10.1139/f93-230.
21. 13C in tissues. Condor, 94(1): 181-188. doi:10.2307/1368807.
22. 15N analysis. Mar. Ecol. Prog. Ser. 128: 1-10. doi:10.3354/meps128001.
23. Hobson, K.A., Schell, D.M., Renouf, D., and Noseworthy, E. 1996. Stable carbon and nitrogen isotopic fractionation between diet and tissues of captive seals: implications for dietary reconstructions involving marine mammals. Can. J. Fish. Aquat. Sci. 53(3): 528-533. doi:10.1139/f95-209.
24. 13C diet-tissue discrimination factors for large sharks under semi-controlled conditions. Comp. Biochem. Physiol. Part A. 155: 445-453.
25. Karasov, W.H., and Martínez del Rio, C. 2007. Physiological ecology: how animals process energy, nutrients, and toxins. Princeton University Press. Princeton, N.J., USA.
26. Kusher, D.I., Smith, S.E., and Cailliet, G.M. 1992. Validated age and growth of the leopard shark, Triakis semifasciata, with comments on reproduction. Environ. Biol. Fishes, 35(2): 187-203. doi:10.1007/BF00002193.
27. Logan, J.M., and Lutcavage, M.E. 2010. Stable isotope dynamics in elasmobranch fishes. Hydrobiologia, 644(1): 231-244. doi:10.1007/s10750-010-0120-3.
28. Logan, J., Haas, H., Deegan, L., and Gaines, E. 2006. Turnover rates of nitrogen stable isotopes in the salt marsh mummichog, Fundulus heteroclitus, following a laboratory diet switch. Oecologia, 147(3): 391-395. doi:10.1007/s00442-005-0277-z. PMID:16249895.
29. Logan, J.M., Jardine, T.D., Miller, T.J., Bunn, S.E., Cunjak, R.A., and Lutcavage, M.E. 2008. Lipid corrections in carbon and nitrogen stable isotope analyses: comparison of chemical extraction and modelling methods. J. Anim. Ecol. 77(4): 838-846. doi:10.1111/j.1365-2656.2008.01394.x. PMID:18489570.
30. Macko, S.A., and Estep, M.L.F. 1984. Microbial alteration of stable nitrogen and carbon isotopic compositions of organic matter. Org. Geochem. 6: 787-790. doi:10.1016/0146-6380(84)90100-1.
31. MacNeil, M.A., Drouillard, K.G., and Fisk, A.T. 2006. Variable uptake and elimination of stable nitrogen isotopes between tissues in fish. Can. J. Fish. Aquat. Sci. 63(2): 345-353. doi:10.1139/f05-219.
32. McCutchan, J.H., Jr, Lewis, W.M., Kendall, C., and McGrath, C.C. 2003. Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos, 102(2): 378-390. doi:10.1034/j.1600-0706.2003.12098.x.
33. McMahon, K.W., Fogel, M.L., Elsdon, T.S., and Thorrold, S.R. 2010. Carbon Isotope fractionation of amino acids in fish muscle reflects biosynthesis and isotopic routing from dietary protein. J. Anim. Ecol. 79(5): 1132-1141. doi:10.1111/j.1365-2656.2010.01722.x.PMID:20629794.
34. Miklos, P., Katzman, S.M., and Cech, J.J. 2003. Effects of temperature on oxygen consumption of the leopard shark, Triakis semifasciata. Environ. Biol. Fishes, 66(1): 15-18. doi:10.1023/A:1023287123495.
35. 15N in adult Pacific herring (Clupea pallasi) following an isotopic shift in diet. Environ. Biol. Fishes, 76(2-4): 177-189. doi:10.1007/s10641-006-9020-9.
36. 15N and animal age. Geochim. Cosmochim. Acta, 48(5): 1135-1140. doi:10.1016/0016-7037(84)90204-7.
37. Olin, J.A., Hussey, N.E., Fritts, M., Heupel, M.R., Simpfendorfer, C. A., Poulakis, G.R., and Fisk, A.T. 2011. Maternal meddling in neonatal sharks: implication for interpreting stable isotopes in young animals. Rapid Commun. Mass Spectrom. 25(8): 1008-1016. doi:10.1002/rcm.4946. PMID:21452377.
38. Ostrom, P.H., Lien, J., and Macko, S.A. 1993. Evaluation of the diet of Sowerby's beaked whale, Mesoplodon bidens, based on isotopic comparisons among northwest Atlantic cetaceans. Can. J. Zool. 71(4): 858-861. doi:10.1139/z93-110.
39. Phillips, D.L., and Eldridge, P.M. 2006. Estimating the timing of diet shifts using stable isotopes. Oecologia, 147(2): 195-203. doi:10.1007/s00442-005-0292-0. PMID:16341714.
40. 15N among fish tissues: implications for study of trophic interactions. Funct. Ecol. 13(2): 225-231. doi:10.1046/j.1365-2435.1999.00301.x.
41. Post, D.M. 2002. Using stable isotope to estimate trophic position: models methods and assumptions. Ecology, 83(3): 703-718. doi:10.1890/0012-9658(2002)083[0703:USITET]2.0.CO;2.
42. Post, D.M., Layman, C.A., Arrington, D.A., Takimoto, G., Quattrochi, J., and Montaña, C.G. 2007. Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia, 152(1): 179-189. doi:10.1007/s00442-006-0630-x. PMID:17225157.
43. 12C correlates with trophic level in pelagic food webs. Ecology, 64(5): 1314-1318. doi:10.2307/1937843.
44. Remme, J.F., Larseen, W.E., Bruheim, I., Sæbø, P.C., Sæbø, A., and Stoknes, I.S. 2006. Lipid content and fatty acid distribution in tissues from Portuguese dogfish, leafscale gulper shark and black dogfish. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 143(4): 459-464.
45. Sakano, H., Fujiwara, E., Nohara, S., and Ueda, H. 2005. Estimation of nitrogen stable isotope turnover rate of Oncorhynchus nerka. Environ. Biol. Fishes, 72(1): 13-18. doi:10.1007/s10641-004-4187-4.
46. Schoeninger, M.J., and DeNiro, M.J. 1984. Nitrogen and carbon isotopic composition of bone collagen from marine and terrestrial animals. Geochim. Cosmochim. Acta, 48(4): 625-639. doi:10.1016/0016-7037(84)90091-7.
47. Smith, S.E. 1984. Timing of vertebral-band deposition in tetracycline- injected leopard sharks. Trans. Am. Fish. Soc. 113(3): 308-313. doi:10.1577/1548-8659(1984)113308:TOVDIT2.0.CO;2.
48. 13C analysis of diet. Oecologia, 57(1-2): 32-37. doi:10.1007/BF00379558.
49. 15N enrichment: a meta-analysis. Oecologia, 136(2): 169-182. doi:10.1007/s00442-003-1270-z. PMID:12802678.
50. 13C trophic fractionation: implications for aquatic food web studies. Limnol. Oceanogr. 46(8): 2061-2066. doi:10.4319/lo.2001.46.8.2061.
51. Wilga, C.D., and Lauder, G.V. 2000. Three-dimensional kinematics and wake structure of the pectoral fins during locomotion in leopard sharks Triakis semifasciata. J. Exp. Biol. 203(Pt 15): 2261-2278. PMID:10887066.