Expanded trophic complexity among large sharks

Food Webs

Volumn 4, Issue , 2015, Pages 1-7

  Hussey, Nigel E ^a   MacNeil, M Aaron ^b   Siple, Margaret C ^c   Popp, Brian N ^c   Dudley, Sheldon F J ^d,e   Fisk, Aaron T ^a  

^a UNIVERSITY OF WINDSOR   (Canada)

^b AUSTRALIAN INSTITUTE OF MARINE SCIENCE   (Australia)

^c UNIVERSITY OF HAWAII   (United States)

^d Natal Sharks Board   (South Africa)

^e UNIVERSITY OF KWAZULU NATAL   (South Africa)

Author keywords

CSIA AA; Elasmobranchs; Stable isotopes; Stomach contents; Trophic position

Indexed keywords

CHONDRICHTHYES; ELASMOBRANCHII;

EID: 84930669912     PISSN: None     EISSN: 23522496     Source Type: Journal    
DOI: 10.1016/j.fooweb.2015.04.002     Document Type: Article

References (76)

1. Bonfil R., Meÿer M., Scholl M., Johnson R., O'Brien S., Oosthuzien H., Swanson S., Kotze D., Paterson M. Transoceanic migration, spatial dynamics and population linkages of white sharks. Science 2005, 310:100-103.
2. Branch T.A., Watson R., Fulton E.A., Jennings S., McGilliard C.R., Pablico G.T., Ricard D., Tracey S.R. The trophic fingerprint of marine fisheries. Nature 2010, 468:431-435.
3. Cabana G., Rasmussen J.B. Comparison of aquatic food chains using nitrogen isotopes. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:10844-10847.
4. Caut S., Angulo E., Courchamp F. Variation in discrimination factors (δ15N and δ13C): the effect of diet isotopic values and applications for diet reconstruction. J. Appl. Ecol. 2009, 46:443-453.
5. Caut S., Jowers M.J., Michel L., Lepoint G., Fisk A.T. Diet- and tissue-specific incorporation of isotopes in the shark Scyliorhinus stellaris, a North Sea mesopredator. Mar. Ecol. Prog. Ser. 2013, 492:185-198.
6. Chalcraft D.R., Resetarits W.J. Predator identity and ecological impacts: functional redundancy or functional diversity. Ecology 2003, 84:2407-2418.
7. Chalcraft D.R., Resetarits W.J. Mapping functional similarity on the basis of trait similarity. Am. Nat. 2003, 162:390-402.
8. Chesson P.L. Mechanisms of maintenance of species diversity. Annu. Rev. Ecol. Syst. 2000, 31:343-366.
9. Chikaraishi Y., Ogawa N.O., Kashiyama Y., Takano Y., Suga H., Tomitani A., Miyashita H., Kitazato H., Ohkouchi N. Determination of aquatic food-web structure based on compound specific nitrogen isotope composition of amino acids. Limnol. Oceanogr. Methods 2009, 7:740-750.
10. Christensen V., Pauly D. ECOPATH II - a software for balancing steady-state ecosystem models and calculating network characteristics. Ecol. Model. 1992, 61:169-185.
11. Christensen V., Guenette S., Heymans J., Walters C.J., Watson R., Zeller D., Pauly D. Hundred-year decline of North Atlantic predatory fishes. Fish Fish. 2003, 4:1-24.
12. Cliff G., Dudley S.F.J. Sharks caught in the protective gill nets off Natal, South Africa. 4. The bull shark Carcharhinus leucas Valenciennes. S. Afr. J. Mar. Sci. 1991, 10:253-270.
13. Cliff G., Dudley S.F.J. Sharks caught in the protective gill nets off Natal, South Africa. 5. The Java shark Carcharhinus amboinensis (Müller and Henle). S. Afr. J. Mar. Sci. 1991, 11:443-453.
14. Cliff G., Dudley S.F.J., Davis B. Sharks caught in the protective gill nets off Natal, South Africa. 3. The shortfin mako shark Isurus oxyrinchus (Rafinesque). S. Afr. J. Mar. Sci. 1990, 9:115-126.
15. Cortés E. Standardised diet compositions and trophic levels of sharks. ICES J. Mar. Sci. 1999, 56:707-717.
16. Cortés E. Life history patterns and correlations in sharks. Rev. Fish. Sci. 2000, 4:299-344.
17. Crooks K.R., Soule M.E. Mesopredator release and avifaunal extinctions in a fragmented system. Nature 1999, 400:563-566.
18. Dale J.J., Wallsgrove N.J., Popp B.N., Holland K.N. Nursery habitat use and foraging ecology of the brown stingray Dasyatis lata determined from stomach contents, bulk and amino acid stable isotopes. Mar. Ecol. Prog. Ser. 2011, 433:221-236.
19. Dicken M.L., Booth A.J., Smale M.J., Cliff G. Spatial and seasonal distribution patterns of juvenile and adult raggedtooth sharks (Carcharias taurus) tagged off the east coast of South Africa. Mar. Freshw. Res. 2007, 58:127-134.
20. Diemer K.M., Mann B.Q., Hussey N.E. Distribution and movement of scalloped hammerhead Sphyrna lewini and smooth hammerhead Sphyrna zygaena along the east coast of southern Africa. Afr. J. Mar. Sci. 2011, 33:229-238.
21. Dudley S.F.J., Cliff G. Sharks caught in the protective gill nets off Natal, South Africa. 7. The blacktip shark Carcharhinus limbatus (Valenciennes). S. Afr. J. Mar. Sci. 1993, 13:237-254.
22. Dudley S.F.J., Cliff G., Zungu M.P., Smale M.J. Sharks caught in the protective gill nets off KwaZulu-Natal, South Africa. 10. The dusky shark, Carcharhinus obscurus (LeSueur 1818). Afr. J. Mar. Sci. 2005, 27:107-127.
23. Estes J.A., Terborgh J., Brashares J.S., Power M.E., Berger J., Bond W.J., Carpenter S.R., Essington T.E., Holt R.D., Jackson J.B.C., et al. Trophic downgrading of planet earth. Science 2011, 333:301-306.
24. Estrada J.A., Rice A.N., Natanson L.J., Skomal G.B. Use of isotopic analysis in reconstructing ontogenetic feeding ecology in white sharks. Ecology 2006, 87:829-834.
25. Ferretti F., Worm B., Britten G.L., Heithaus M.R., Lotze H.K. Patterns and ecosystem consequences of shark declines in the ocean. Ecol. Lett. 2010, 13:1055-1071.
26. Fry B. Food web structure on Georges Bank from stable C, N and S isotopic composition. Limnol. Oceanogr. 1988, 33:1182-1190.
27. Garcia V.B., Lucifora L.O., Myers R.A. The importance of habitat and life history extinction risk in sharks, skates, rays and chimaeras. Proc. R. Soc. Lond. B 2008, 275:83-89.
28. Germain L.R., Koch P.L., Harvey J., McCarthy M.D. Nitrogen isotope fractionation in amino acids from harbour seals: implications for compound-specific trophic position calculations. Mar. Ecol. Prog. Ser. 2013, 482:265-277.
29. Heithaus M.R., Vaudo J.J., Kreicker S., Layman C.A., Krutzen M., Burkholder D.A., Bessey C., Sarabia R., Cameron K., Wirsing A., Thomson J.A., Dunphy-Daly M.M. Apparent resource partitioning and trophic structure of large-bodied marine predators in a relatively pristine seagrass ecosystem. Mar. Ecol. Prog. Ser. 2013, 481:225-237.
30. Heithaus M.R., Frid A., Wirsing A.J., Worm B. Predicting the ecological consequences of marine top predator declines. Trends Ecol. Evol. 2008, 23:202-210.
31. Hoen D.K., Kim S.L., Hussey N.E., Wallsgrove N.J., Drazen J.C., Popp B.N. Amino acid 15N trophic enrichment factors of four large carnivorous fishes. J. Exp. Mar. Biol. Ecol. 2014, 453:76-83.
32. Huckstadt L.A., Rojas C.P., Antezana T. Stable isotope analysis reveals pelagic foraging by the Southern sea lion in central Chile. J. Exp. Mar. Biol. Ecol. 2007, 347:123-133.
33. Hussey N.E., McCarthy I.D., Dudley S.F.J., Mann B.Q. Nursery grounds, movement patterns and growth rates of dusky sharks, Carcharhinus obscurus: a long-term tag and release study in South Africa. Mar. Freshw. Res. 2009, 60:571-583.
34. Hussey N.E., Brush J., McCarthy I.D., Fisk A.T. δ15N and δ13C diet–tissue discrimination factors for large sharks under semi-controlled conditions. Comp. Biochem. Phys. A 2010, 155:445-453. 10.1016/j.cbpa.2009.09.023.
35. Hussey N.E., McCann H., Cliff G., Dudley S.F.J., Wintner S.P., Fisk A.T. Size-based analysis of the diet and trophic position of the white shark (Carcharodon carcharias) in South African waters. Global Perspectives on the Biology and Life History of the Great White Shark 2011, CRC Press, Boca Raton, Flo., USA. M.L. Domeier (Ed.).
36. Hussey N.E., Dudley S.F.J., McCarthy I.D., Cliff G., Fisk A.T. Stable isotope profiles of large marine predators: viable indicators of trophic position, diet and movement in sharks. Can. J. Fish. Aquat. Sci. 2012, 68:2029-2045.
37. Hussey N.E., MacNeil M.A., Olin J.A., McMeans B.C., Kinney M.J., Chapman D.D., Fisk A.T. Stable isotopes in elasmobranchs: tissue types, methods, applications and assumptions. J. Fish Biol. 2012, 80:1449-1484.
38. Hussey N.E., MacNeil M.A., McMeans B.C., Olin J.A., Dudley S.F.J., Cliff G., Wintner S.P., Fennessy S.T., Fisk A.T. Rescaling the trophic structure of marine food webs. Ecol. Lett. 2014, 17:239-250.
39. Hussey N.E., MacNeil M.A., McMeans B.C., Olin J.A., Dudley S.F.J., Cliff G., Wintner S.P., Fennessy S.T., Fisk A.T. Corrigendum to Hussey et al. (2014). Ecol. Lett. 2014, 17:239-250.
40. Jennings S., Greenstreet S.P.R., Hill L., Piet G.J., Pinnegar J.K., Warr K.J. Long-term trends in the trophic structure of the North Sea fish community: evidence from stable isotope analysis, size spectra and community metrics. Mar. Biol. 2002, 141:1085-1097.
41. Kim S.L., del Rio C.M., Casper D., Koch P.L. Isotopic incorporation rates for shark tissues from a long-term captive feeding study. J. Exp. Biol. 2012, 15:2495-2500.
42. Kitchell J.F., Essington C.H., Boggs D.E., Schindler D.E., Walters C.J. The role of sharks and longline fisheries in a pelagic ecosystem of the central Pacific. Ecosystems 2002, 5:202-216.
43. Leonard D. Estimating a bivariate linear relationship. Bayesian Anal. 2011, 6:727-754.
44. Loreau M. Does functional redundancy exist?. Oikos 2004, 104:606-611.
45. Madigan D.J., Carlisle A.B., Snodgrass O.E., Litvin S.Y., Mitcheli F., Block B.A. Stable isotope analysis challenges wasp-waist food web assumptions in an upwelling pelagic ecosystem. Sci. Rep. 2012, 2:654.
46. Matich P., Heithaus M.R., Layman C.A. Contrasting patterns of individual specialization and trophic coupling in two marine apex predators. J. Anim. Ecol. 2011, 80:294-305.
47. McCarthy M.D., Benner R., Lee C., Fogel M.L. Amino acid nitrogen isotopic fractionation patterns as indicators of heterotrophy in plankton, particulate, and dissolved organic matter. Geochim. Cosmochim. Acta 2007, 71:4727-4744.
48. McClelland J.W., Montoya J.P. Trophic relationships and the nitrogen isotopic composition of amino acids in plankton. Ecology 2002, 83:2173-2180.
49. McClelland J.W., Holl C.M., Montoya J.P. Relating low delta N-15 values of zooplankton to N-2-fixation in the tropical North Atlantic: insights provided by stable isotope ratios of amino acids. Deep-Sea Res. I 2003, 50:849-861.
50. McLaren B.E., Peterson R.O. Wolves, moose and tree rings on Isle Royal. Science 1994, 266:1555-1558.
51. Motta P.J., Huber D.R. Prey capture behavior and feeding mechanics of elasmobranchs. Biology of Sharks and Their Relatives 2012, Taylor and Francis Group, LLC, Boca Raton. Second ed. J.C. Carrier, J.A. Musick JA, M.R. Heithaus (Eds.).
52. Myers R.A., Worm B. Rapid worldwide depletion of predatory fish communities. Nature 2003, 423:280-283.
53. Myers R.A., Baum J.K., Shepherd T.D., Powers S.P., Peterson C.H. Cascading effects of the loss of apex predatory sharks from a costal ocean. Science 2007, 315:1846-1850.
54. Naem S. Species redundancy and ecosystem reliability. Conserv. Biol. 1998, 12:39-45.
55. Olin J.A., Hussey N.E., Grgicak-Mannion A., Fritts M.W., Fisk A.T. Intra-taxa variability in δ15N diet-tissue discrimination factors of top predators. PLoS One 2013, 8(10):e77567. 10.1371/journal.pone.0077567.
56. Paine R.T. Species complexity and species diversity. Am. Nat. 1966, 100:65-75.
57. Patil A., Huard D., Fonnesbeck C.J. PyMC: Bayesian stochastic modelling in Python. J. Stat. Softw. 2000, 35:1-81.
58. Pauly D., Christensen V., Dalsgaard J., Froese R., Torres F. Fishing down marine food webs. Science 1998, 279:860-863.
59. Pauly D., Watson R., Alder J. Global trends in world fisheries: impact on marine ecosystems and food security. Proc. R. Soc. Lond. B 2005, 360:5-12.
60. Petchey O.L., Gaston K.J. Functional diversity: back to basics and looking forward. Ecol. Lett. 2006, 9:741-758.
61. Popp B.N., Graham B.S., Olson R.J., Hannides C.C.S., Lott M.J., López-Ibarra G.A., Galván-Magaña F., Fry B. Insight into the trophic ecology of yellowfin tuna, Thunnus albacares, from compound-specific nitrogen isotope analysis of proteinaceous amino acids. Terrestrial Ecology 2007, 173-190. T. Dawson, R. Siegworf (Eds.).
62. Rabehagasoa N., Lorrain A., Bach P., Potier M., Jaquemet S., Richard P., Menard F. Isotopic niches of the blue shark Prionace glauca and the silky shark Carcharhinus falciformis in the southwestern Indian Ocean. Endanger. Species Res. 2012, 17:83-92.
63. Resetarits W.J., Chalcraft D.R. Functional diversity within a morphologically conservative genus of predators: implications for functional equivalence and redundancy in ecological communities. Funct. Ecol. 2007, 21:793-804.
64. Rizzari J.R., Bergseth B.J., Frisch A.J. Impact of conservation areas on trophic interactions between apex predators and herbivores on coral reefs. Conserv. Biol. 2014, 10.1111/cobi.12385.
65. Rupert J.L.W., Travers M.J., Smith L.L., Fortin M.J., Meekan M. Caught in the middle: combined impacts of shark removal and coral loss on the fish communities of coral reefs. PLoS ONE 2013, 10.1371/journal.pone.0074648.
66. Sherwood O.A., Lehmann M.F., Schubert C.J., Scott D.B., McCarthy M.D. Nutrient regime shift in the western North Atlantic indicated by compound-specific delta N-15 of deep-sea gorgonian corals. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:1011-1015.
67. Shurin J.B., Borer E.T., Seabloom E.W., Anderson K., Blanchette C.A., Broitman B., Cooper S.D., Halpern B.S. A cross-ecosystem comparison of the strength of trophic cascades. Ecol. Lett. 2002, 5:785-791.
68. Stevens J.D., Bonfil R., Dulvy N.K., Walker P.A. The effects of fishing on sharks, rays and chimaeras (chondrichthyans), and the implications for marine ecosystems. ICES J. Mar. Sci. 2000, 57:476-494.
69. Strong D.R. Are trophic cascades all wet? Differentiation and donor control in speciose ecosystems. Ecology 1992, 73:747-754.
70. Terborgh J., Lopez L., Nunez P., Rao M., Shahabuddin G., Orihuela G., Riveros M., Ascanio R., Alder G.H., Lambert T.D., Balbas L. Ecological meltdown in predator-free forest fragments. Science 2001, 294:1923-1926.
71. Tricas T.C., McCosker J.E. Predatory behaviour of the white shark (Carcharodon carcharias), with notes on its biology. Proc. Calif. Acad. Sci. 1984, 43:221-238.
72. Walker B.H. Biodiversity and ecological redundancy. Conserv. Biol. 1991, 6:18-23.
73. Wetherbee B.M., Cortes E. Food consumption and feeding habits. Biology of Sharks and Their Relatives 2004, Taylor and Francis Group, LLC, Boca Raton. J.C. Carrier, J.A. Musick, M.R. Heithaus (Eds.).
74. Williams R.J., Martinez N.D. Limits to trophic levels and omnivory in complex food webs: theory and data. Am. Nat. 2004, 163:458-468.
75. Worm B., Hilborn R., Baum J.K., Branch T.A., Collie J.S., Costello C., Fogarty M.J., Fulton E.A., Hutchings J.A., Jennings S., et al. Rebuilding global fisheries. Science 2009, 325:578-585.
76. Yachi S., Loreau M. Biodiversity and ecosystem productivity in a fluctuating environment: the insurance hypothesis. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:1463-1468.