Spatial and seasonal variation in δ15N and δ13C values in a mesopredator shark, Squalus suckleyi, revealed through multitissue analyses

Marine Biology

Volumn 160, Issue 2, 2013, Pages 399-411

  Reum, Jonathan C P ^a,b   Essington, Timothy E ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b NORTHWEST FISHERIES SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BODY SIZE; CARBON ISOTOPE; DIET; FEEDING; INTRAPOPULATION VARIATION; ISOTOPIC COMPOSITION; NITROGEN ISOTOPE; PREDATOR; SEASONAL VARIATION; SHARK; SPATIAL VARIATION; TURNOVER;

PUGET SOUND; STRAIT OF GEORGIA; UNITED STATES; WASHINGTON [UNITED STATES];

CHONDRICHTHYES; SQUALIDAE; SQUALUS; SQUALUS ACANTHIAS;

EID: 84872497626     PISSN: 00253162     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00227-012-2096-1     Document Type: Article

References (68)

1. Anderson MJ, Gribble NA (1998) Partitioning the variation among spatial, temporal and environmental components in a multivariate data set. Aust J Ecol 23: 158-167.
2. Andrews KS, Harvey C (in press) Ecosystem-level consequences of movement: seasonal variation in the trophic impact of a top predator. Mar Ecol Progr Ser.
3. Andrews KS, Levin PS, Katz SL, Farrer D, Gallucci VF, Bargmann G (2007) Acoustic monitoring of sixgill shark movements in Puget Sound: evidence for localized movement. Can J Zool 85: 1136-1142.
4. Barnes C, Jennings S, Polunin NVC, Lancaster JE (2008) The importance of quantifying inherent variability when interpreting stable isotope field data. Oecologia 155: 227-235.
5. Beamish RJ, Sweeting RM (2009) Spiny dogfish in the Pelagic waters of the Strait of Georgia and Puget Sound. In: Gallucci VF, McFarlane GA, Bargmann G (eds) Biology and management of dogfish sharks. American Fishery Society, Bethesda, pp 101-118.
6. Bolnick DI, Svanback R, Fordyce JA, Yang LH, Davis JM, Hulsey CD, Forister ML (2003) The ecology of individuals: incidence and implications of individual specialization. Am Nat 161: 1-28.
7. Bolnick DI, Svanback R, Araújo MS, Persson L (2007) Comparative support for the niche variation hypothesis that more generalized populations also are more heterogeneous. Proc Natl Acad Sci USA 104: 10075-10079.
8. Borcard D, Gillet F, Legendre P (2011) Numerical Ecology with R. Springer, New York.
9. Borrell A, Cardona L, Kumarran RP, Aguilar A (2011) Trophic ecology of elasmobranchs caught off Gujarat, India, as inferred from stable isotopes. ICES J Mar Sci 68: 547-554.
10. 15N incorporation in house sparrows (Passer domesticus). Oecologia 144: 226-232.
11. DeNiro MJ, Epstein S (1977) Mechanism of carbon isotope fractionation associated with lipid-synthesis. Science 197: 261-263.
12. Duffy EJ, Beauchamp DA, Sweeting RM, Beamish RJ, Brennan JS (2010) Ontogenetic diet shifts of juvenile chinook salmon in nearshore and offshore habitats of Puget Sound. T Am Fish Soc 139: 803-823.
13. Dulvy NK, Baum JK, Clarke S, Compagno LJV, Cortes E, Domingo A, Fordham S, Fowler S, Francis MP, Gibson C, Martinez J, Musick JA, Soldo A, Stevens JD, Valenti S (2008) You can swim but you can't hide: the global status and conservation of oceanic pelagic sharks and rays. Aquat Conserv 18: 459-482.
14. Ebert DA, White WT, Goldman KJ, Compagno LJV, Daly-Engle T, Ward R (2010) Resurrection and redescription of Squalus suckleyi (Girard, 1854) from the North Pacific, with comments on the Squalus acanthias subgroup (Squaliformes: Squalidae). Zootaxa 2612: 22-40.
15. Essington TE, Paulsen CE (2010) Quantifying hypoxia impacts on an estuarine demersal community using a hierarchical ensemble approach. Ecosystems 13: 1035-1048.
16. Ferretti F, Myers RA, Serena F, Lotze HK (2008) Loss of large predatory sharks from the Mediterranean Sea. Conserv Biol 22: 952-964.
17. Ferretti F, Worm B, Britten GL, Heithaus MR, Lotze HK (2010) Patterns and ecosystem consequences of shark declines in the ocean. Ecol Lett 13: 1055-1071.
18. Grubbs RD (2010) Ontogenetic shifts in movement and habitat use. In: Carrier JC, Musick JA, Heithaus MR (eds) Sharks and their relatives II: biodiversity, adaptive physiology, and conservation. CRC Press, Boca Raton, pp 319-350.
19. Hart JL (1973) Pacific fishes of Canada. Bull Fish Res Board Can 180: 740.
20. Heithaus MR, Frid A, Vaudo JJ, Worm B, Wirsing AJ (2010) Unraveling the ecological importance of elasmobranchs. In: Carrier JC, Musick JA, Heithaus MR (eds) Sharks and their relatives: biodiversity, adaptation physiology, and conservation. CRC Press, Boca Raton, pp 611-638.
21. Hobson KA, Piatt JF, Pitocchelli J (1994) Using stable isotopes to determine seabird trophic relationships. J Anim Ecol 63: 786-798.
22. Hoffman JC, Sutton TT (2010) Lipid correction for carbon stable isotope analysis of deep-sea fishes. Deep Sea Res 57: 956-964.
23. Hyslop EJ (1980) Stomach contents analysis: a review of methods and their application. J Fish Biol 17: 411-429.
24. Janssen MH, Arcese P, Kyser T, Bertram D, Norris RD (2011) Stable isotopes reveal strategic allocation of resources during juvenile development in a cryptic and threatened seabird, the Marbled Murrelet (Brachyramus marmoratus). Can J Fish Aquat 89: 859-868.
25. Jennings S, Pinnegar JK, Polunin NVC, Warr KJ (2002) Linking size-based and trophic analyses of benthic community structure. Mar Ecol Prog Ser 226: 77-85.
26. Jones BC, Green GH (1977) Food and feeding of spiny dogfish (Squalus acanthias) in British Columbia waters. J Fish Res Board Can 34: 2067-2078.
27. Ketchen KS (1986) The spiny dogfish (Squalus acanthias) in the northeast Pacific and a history of its utilization. Can Spec Pub Fish Aquat Sci 88: 78.
28. 13 values from aquatic organisms, with implications for isotope mixing models. J Appl Ecol 43: 1213-1222.
29. Kim SL, Martínez del Rio C, Casper D, Koch PL (2012) Isotopic incorporation rates for shark tissues from a long-term captive feeding study. J Exp Biol 215: 2495-2500.
30. 14N in pelagic biota of Prince William Sound, Alaska. Can J Fish Aquat Sci 56: 94-117.
31. Larson S, Christiansen J, Griffing D, Ashe J, Lowry D, Andrews K (2011) Relatedness and polyandry of sixgill sharks, Hexanchus griseus, in an urban estuary. Conserv Genet 12: 679-690.
32. Layman CA, Arrington DA, Montana CG, Post DM (2007) Can stable isotope ratios provide for community-wide measures of trophic structure? Ecology 88: 42-48.
33. Legendre P, Legendre L (1998) Numerical ecology. Elsevier Science, Amsterdam.
34. Lesage V, Hammill MO, Kovacs KM (2001) Marine mammals and community structure of the Estuary and Gulf of St Lawrence, Canada: evidence from stable isotope analysis. Mar Ecol Prog Ser 210: 203-221.
35. Logan JM, Lutcavage ME (2010) Stable isotope dynamics in elasmobranch fishes. Hydrobiologia 644: 231-244.
36. Logan JM, Jardine TD, Miller TJ, Bunn SE, Cunjak RA, Lutcavage ME (2008) Lipid corrections in carbon and nitrogen stable isotope analyses: comparison of chemical extraction and modelling methods. J Anim Ecol 77: 838-846.
37. MacNeil MA, Skomal GB, Fisk AT (2005) Stable isotopes from multiple tissues reveal diet switching in sharks. Mar Ecol Prog Ser 302: 199-206.
38. MacNeil MA, Drouillard KG, Fisk AT (2006) Variable uptake and elimination of stable nitrogen isotopes between tissues in fish. Can J Fish Aquat Sci 63: 345-353.
39. Manly BFJ (2006) Randomization, Bootstrap and Monte Carlo methods in biology, 2nd edn. CRC Press, Boca Raton.
40. Matich P, Heithaus MR, Layman CA (2010) Contrasting patterns of individual specialization and trophic coupling in two marine apex predators. J Anim Ecol 80: 294-305.
41. McConnaughey T, McRoy CP (1979) Food-web structure and the fractionation of carbon isotopes in the Bering Sea. Mar Biol 53: 257-262.
42. Ménard F, Lorrain A, Potier M, Marsac F (2007) Isotopic evidence of distinct feeding ecologies and movement patterns in two migratory predators (yellowfin tuna and swordfish) of the western Indian Ocean. Mar Biol 153: 141-152.
43. Newsome SD, del Rio CM, Bearhop S, Phillips DL (2007) A niche for isotopic ecology. Front Ecol Environ 5: 429-436.
44. Olson RJ, Popp BN, Graham BS, López-Ibarra GA, Galván-Magaña F, Lennert-Cody CE, Bocanegra-Castillo N, Wallsgrove NJ, Gier E b, Alatorre-Ramírez V, Balance LT, Fry B (2010) Food-web inferences of stable isotope spatial patterns in copepods and yellowfin tuna in the pelagic eastern Pacific Ocean. Prog Oceanog 86: 124-138.
45. Perry RI, Thompson PA, Mackas DL, Harrison PJ, Yelland DR (2002) Stable carbon isotopes as pelagic food web tracers in adjacent shelf and slope regions off British Columbia, Canada. Can J Fish Aquat 56: 2477-2486.
46. Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annu Rev Ecol Syst 18: 293-320.
47. Quevedo M, Svanback R, Eklov P (2009) Intrapopulation niche partitioning in a generalist predator limits food web connectivity. Ecology 90: 2263-2274.
48. Reum JCP (2011) Lipid correction model for a cosmopolitan predator, spiny dogfish Squalus acanthias. J Fish Biol 79: 2060-2066.
49. Reum JCP, Essington TE (2008) Seasonal variation in guild structure of the Puget Sound demersal fish community. Estuar Coast 31: 790-801.
50. Reum JCP, Essington TE (2011) Season- and depth-dependent variation in the demersal fish assemblage of a large fjord estuary (Puget Sound, Washington). Fish Bull 109: 186-197.
51. Revill AT, Young JW, Lansdell M (2009) Stable isotopic evidence for trophic groupings and bio-regionalization of predators and their prey in oceanic waters off eastern Australia. Mar Biol 156: 1241-1253.
52. Sampson L, Galvan-Magana F, De Silva-Davila R, Aguiniga-Garcia S, O'Sullivan JB (2010) Diet and trophic position of the devil rays Mobula thurstoni and Mobula japanica as inferred from stable isotope analysis. J Mar Biol Assoc UK 90: 969-976.
53. Schmidt SN, Olden JD, Solomon CT, Vander Zanden MJ (2007) Quantitative approaches to the analysis of stable isotope food web data. Ecology 88: 2793-2802.
54. Semmens BX, Ward EJ, Moore JW, Darimont CT (2009) Quantifying inter- and intra-population niche variability using hierarchical Bayesian stable isotope mixing models. PLoS ONE 4: e6187.
55. Shepherd TD, Myers RA (2005) Direct and indirect fishery effects on small coastal elasmobranchs in the northern Gulf of Mexico. Ecol Lett 8: 1095-1104.
56. Sweeting CJ, Polunin NVC, Jennings S (2006) Effects of chemical lipid extraction and arithmetic lipid correction on stable isotope ratios of fish tissues. Rapid Commun Mass Spectrom 20: 595-601.
57. Tanasichuk RW, Ware DM, Shaw W, McFarlane GA (1991) Variations in diet, daily ration, and feeding periodicity of Pacific Hake (Merluccius productus) and spiny dogfish (Squalus acanthias) off the lower west coast of Vancouver Island. Can J Fish Aquat Sci 48: 2118-2128.
58. Taylor IG, Gallucci VF (2009) Unconfounding the effects of climate and density dependence using 60 years of data on spiny dogfish (Squalus acanthias). Can J Fish Aquat Sci 66: 351-366.
59. Taylor IG, Lippert GR, Gallucci VF, Bargmann G (2009) Movement patterns of spiny dogfish from historical tagging experiments in Washington State. In: Gallucci VF, McFarlane GA, Bargmann G (eds) Biology and management of dogfish sharks. American Fisheries Society, Bethesda, pp 67-76.
60. ter Braak CJF, Verdonschot PFM (1995) Canonical correspondence analysis and related multivariate methods in aquatic ecology. Aquat Sci 57: 255-289.
61. Turner TF, Collyer ML, Krabbenhoft TJ (2010) A general hypothesis-testing framework for stable isotope ratios in ecological studies. Ecology 91: 2227-2233.
62. Vander Zanden MJ, Shuter BJ, Lester NP, Rasmussen JB (2000) Within- and among-population variation in the trophic position of a pelagic predator, lake trout (Salvelinus namaycush). Can J Fish Aquat Sci 57: 725-731.
63. Ward-Paige CA, Mora C, Lotze HK, Pattengill-Semmens C, McClenachan L, Arias-Castro E, Myers RA (2010) Large-scale absence of sharks on reefs in the greater-Caribbean: a footprint of human Pressures. PLoS ONE 5(8): e11968. doi: 10. 1371/journal. pone. 0011968.
64. West JE, Lanksbury J, O'Neill SM (2011) Persistent organic pollutants in marine plankton from Puget Sound. Washington Department of Ecology, Olympia.
65. Wetherbee BM, Cortes E (2004) Food consumption and feeding habits. CRC Press, Boca Raton.
66. Woodland RJ, Secor DH, Wedge ME (2011) Trophic resource overlap between small elasmobranchs and sympatric teleosts in mid-Atlantic Bight nearshore habitats. Estuar Coast 34: 391-404.
67. Zar JH (1999) Biostatistical analysis. Prentice Hall, New Jersey.
68. Zeug S, Peretti D, Winemiller K (2009) Movement into floodplain habitats by gizzard shad (Dorosoma cepedianum) revealed by dietary and stable isotope analyses. Environ Biol Fish 84: 307-314.