Diet reconstruction and resource partitioning of a Caribbean marine mesopredator using stable isotope Bayesian modelling

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Tilley, Alexander ^a,b   López Angarita, Juliana ^b,c   Turner, John R ^a  

^a BANGOR UNIVERSITY   (United Kingdom)

^b Talking Oceans Foundation   (Colombia)

^c UNIVERSITY OF YORK   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON 13; NITROGEN 15;

ANIMAL TISSUE; ANNELID; ARTICLE; BAYES THEOREM; BELIZE; BIVALVE; CARCHARHINUS PEREZI; CONTROLLED STUDY; CRUSTACEA; DASYATIS AMERICANA; ECOLOGICAL NICHE; FISH; FOOD COMPOSITION; GINGLYMOSTOMA CIRRATUM; ISOTOPE ANALYSIS; NONHUMAN; PREY SELECTION; RESOURCE PARTITIONING; SHARK; SYMPATRY; TELEOST; TROPHIC LEVEL; WILD SPECIES;

ANIMALS; BAYES THEOREM; BELIZE; FOOD CHAIN; FOOD HABITS; ISOTOPES; MASS SPECTROMETRY; MODELS, THEORETICAL; SHARKS;

EID: 84893356078     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0079560     Document Type: Article

References (62)

1. Baum JK, Worm B (2009) Cascading top-down effects of changing oceanic predator abundances. J Anim Ecol 78: 699-714. doi:10.1111/j.1365-2656.2009. 01531.x.
2. Newsome SD, Martinez del Rio C, Bearhop S, Phillips D (2007) A niche for isotopic ecology. Front Ecol Environ 5: 429-436. doi:10.1890/060150.1. (Pubitemid 47557322)
3. Fagan W (1997) Omnivory as a stabilizing feature of natural communities. Am Nat 150: 554-567.
4. O'Gorman E, Tompkins E (2009) Perturbations to trophic interactions and the stability of complex food webs. PNAS 106: 13393-13398.
5. Bascompte J, Melián C, Sala E (2005) Interaction strength combinations and the overfishing of a marine food web. PNAS 102: 5443-5447. (Pubitemid 40530277)
6. Bowman R, Stillwell C, Michaels W, Grosslein M (2000) Food of northwest Atlantic fishes and two common species of squid. NOAA Technical Memorandum NMFS-NE-155.
7. Vaudo J, Heithaus M (2011) Dietary niche overlap in a nearshore elasmobranch mesopredator community. MEPS 425: 247-260. doi:10.3354/meps08988.
8. Thrush SF (1999) Complex role of predators in structuring soft-sediment macrobenthic communities: Implications of changes in spatial scale for experimental studies. Aust J Ecol 24: 344-354.
9. O'Shea OR, Thums M, van Keulen M, Meekan MG (2011) Bioturbation by stingrays at Ningaloo Reef, Western Australia. Mar Freshwater Res 63: 189-197.
10. Randall J (1967) Food Habits of Reef Fishes of the West Indies. Stud Trop Oceanogr 5: 665-847.
11. Gilliam D, Sullivan KM (1993) Diet and Feeding Habits of the Southern Stingray Dasyatis americana in the Central Bahamas. Bull Mar Sci 52: 1007-1013. (Pubitemid 24429894)
12. Wetherbee BM, Cortés E (2004) Food consumption and feeding habits. In: Musick JA, Heithaus M, Carrier JC, editors. Sharks and their relatives I. Boca Raton, Florida: CRC Press, Vol. 1. pp. 225-246.
13. Michener R, Kaufman L (2007) Stable isotope ratios as tracers in marine food webs: An update. In: Michener R, Lajtha K, editors. Stable Isotopes in Ecology and Environmental Science. Blackwell Publishing. pp. 238-270.
14. Peterson B, Fry B (1987) Stable isotopes in ecosystem studies. Annu Rev Ecol Syst 18: 293-320.
15. Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83: 703-718.
16. Bearhop S, Adams C, Waldron S, Fuller R, Macleod H (2004) Determining trophic niche width: a novel approach using stable isotope analysis. J Anim Ecol 73: 1007-1012. (Pubitemid 39123240)
17. Jackson A, Inger R, Parnell A, Bearhop S (2011) Comparing isotopic niche widths among and within communities: SIBER - Stable Isotope Bayesian Ellipses in R. J Anim Ecol 80: 595-602.
18. Arthur K, Boyle M, Limpus C (2008) Ontogenetic changes in diet and habitat use in green sea turtle (Chelonia mydas) life history. MEPS 362: 303-311. doi:10.3354/meps07440. (Pubitemid 352045332)
19. Caut S, Angulo E, Courchamp F (2009) Variation in discrimination factors (Δ 15N and Δ 13C): the effect of diet isotopic values and applications for diet reconstruction. J Appl Ecol 46: 443-453. doi:10.1111/j.1365-2664.2009.01620.x.
20. MacNeil M, 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. doi:10.1139/f05-219.
21. Hussey NE, Chapman DD, Donnelly E, Abercrombie DL, Fisk AT (2011) Finicky samples: an assessment of shark fin as a source material for stable isotope analysis. Limnol Oceanogr-Meth 9: 524-532. doi:10.4319/lom.2011.9.524.
22. Hussey NE, MacNeil MA, Olin JA, McMeans BC, Kinney MJ, et al. (2012) Stable isotopes and elasmobranchs: tissue types, methods, applications and assumptions. J Fish Biology 80: 1449-1484.
23. Kim SL, Casper DR, Galván-Magaña F, Ochoa-Díaz R, Hernández-Aguilar SB, et al. (2012) Carbon and nitrogen discrimination factors for elasmobranch soft tissues based on a long-term controlled feeding study. Environ Biol Fish 95: 37-52.
24. Hussey NE, Brush J, McCarthy ID, Fisk AT (2009) d15N and d13C diet-tissue discrimination factors for large sharks under semi-controlled conditions. Comparative Biochemistry and Physiology, Part A 155: 1-9. doi:10.1016/j.cbpa. 2009.09.023.
25. Hussey NE, Wintner S, Dudley SFJ, Cliff G, Cocks DT, et al. (2010) Maternal investment and size-specific reproductive output in carcharhinid sharks. J Anim Ecol 79: 184-193. doi:10.1111/j.1365-2656.2009.01623.x.
26. Bigelow H, Schroeder W (1953) Fishes of the Western North Atlantic. Memoir Sears Foundation for Marine Research. 1 pp.
27. CONAPESCA-INP (2004) Plan de Acción Nacional para el Manejo y Conservación de Tiburones, Rayas y Especies Afines en México. MazatlánMéxico: Comisión Nacional de Acuacultura y Pesca e Instituto Nacional de la Pesca, Secretaría de Agricultura, Ganadería, Desarrollo Rural, Pesca y Alimentación. 1 p.
28. Grijalba-Bendeck M, Polo-Silva C, Acero A (2007) Una aproximación a la abundancia de los Batoideos capturados artesanalmente en Santa Marta (Colombia). Bol Invest Mar Cost 36: 251-268.
29. Aguiar A, Valentin J, Rosa RS (2009) Habitat use by Dasyatis americana in a south-western Atlantic oceanic island. J Mar Biol Ass 89: 1147-1152. doi:10.1017/S0025315409000058.
30. Garro A, Vargas R, Zanella I, Le Foulgo L (2009) Análisis de las capturas de tiburones y rayas en las pesquerías artesanales de tárcoles, pacífico central de Costa Rica. Rev Mar y Cost 1: 145-157.
31. Tilley A, Strindberg S (2013) Population density estimation of southern stingrays Dasyatis americana on a Caribbean atoll using distance sampling. Aquatic Conserv 23: 202-209. doi:10.1002/aqc.2317.
32. Tilley A, López-Angarita J, Turner JR (2013) Effects of scale and habitat distribution on the movement of the southern stingray Dasyatis americana on a Caribbean atoll. MEPS 482: 169-179. doi:10.3354/meps10285.
33. Snelson F Jr, Williams S (1981) Notes on the occurrence, distribution, and biology of elasmobranch fishes in the Indian River Lagoon system, Florida. Estuaries 4: 110-120.
34. Smith K, Herrnkind W (1992) Predation on early juvenile spiny lobsters Panulirus argus (Latreille): influence of size and shelter. J Exp Mar Bio Ecol 157: 3-18.
35. Howarth LM, Roberts CM, Thurstan RH, Stewart BD (2013) The unintended consequences of simplifying the sea: making the case for complexity. Fish and Fisheries. doi:10.1111/faf.12041.
36. Baum JK, Myers RA, Kehler DG, Worm B, Harley SJ, et al. (2003) Collapse and conservation of shark populations in the Northwest Atlantic. Science 299: 389-392. (Pubitemid 36120041)
37. Cortés E (1999) Standardized diet compositions and trophic levels of sharks. ICES J Mar Sci 56: 707-717.
38. Preston T, Owens NJP (1983) Interfacing an automatic elemental analyser with an isotope ratio mass spectrometer: the potential for fully automated total nitrogen and nitrogen-15 analysis. Analyst 108: 971-977. doi:10.1039/ an9830800971.
39. Post DM, Layman CA, Albrey Arrington D, Takimoto G, Quattrochi J, et al. (2007) Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152: 179-189. (Pubitemid 46640011)
40. Layman CA, Arrington DA, Montaña CG, Post DM (2007) Can Stable Isotope Ratios Provide for Community-Wide Measures of Trophic Structure? Ecology 88: 42-48. (Pubitemid 46596820)
41. Robbins C, Felicetti LA, Florin S (2010) The impact of protein quality on stable nitrogen isotope ratio discrimination and assimilated diet estimation. Oecologia 162: 571-571579.
42. Parnell AC, Inger R, Bearhop S, Jackson AL (2010) Source Partitioning Using Stable Isotopes: Coping with Too Much Variation. PLoS ONE 5: e9672. doi:10.1371/journal.pone.0009672.
43. Froese R, Pauly D (2000) FishBase 2000, concepts, design and data sources. Froese R, Pauly D, editors Los Banos, Laguna, Philippines, ICLARM. 1 p.
44. Dale J, Wallsgrove N, Popp B, Holland KN (2011) Nursery habitat use and foraging ecology of the brown stingray Dasyatis lata determined from stomach contents, bulk and amino acid stable isotopes. MEPS 433: 221-236. doi:10.3354/meps09171.
45. Ward-Campbell BMS, Beamish FWH (2005) Ontogenetic changes in morphology and diet in the snakehead, Channa limbata, a predatory fish in western Thailand. Environ Biol Fish 72: 251-257. doi:10.1007/s10641-004-1744-9. (Pubitemid 40572893)
46. Cummings D, Booth D, Lee R, Simpson S, Pile A (2010) Ontogenetic diet shifts in the reef fish Pseudanthias rubrizonatus from isolated populations on the North-West Shelf of Australia. MEPS 419: 211-222. doi:10.3354/meps08827.
47. Werner EE (1984) The Ontogenetic Niche and Species Interactions in Size-Structured Populations. Annu Rev Ecol Syst 15: 393-425. doi:10.1146/annurev.ecolsys.15.1.393.
48. Lin HG, Banks T, Sternberg L (1991) Variations in 13C values for the seagrass Thalassia testudinum and its relations to mangrove carbon. Aquat Bot 40: 333-341.
49. Saglam H, Ak O, Kutlu S, Aydin I (2010) Diet and feeding strategy of the common stingray Dasyatis pastinaca (Linnaeus, 1758) on the Turkish coast of southeastern Black Sea. Cah Biol Mar 51: 37-44.
50. Smith J, Merriner J (1985) Food habits and feeding behavior of the cownose ray, Rhinoptera bonasus, in lower Chesapeake Bay. Estuaries 8: 305-310. (Pubitemid 17247016)
51. Stokes M, Holland N (1992) Southern Stingray (Dasyatis americana) Feeding on Lancelets (Branchiostoma floridae). J Fish Biology 41: 1043-1044.
52. Vanderklift M, Ponsard S (2003) Sources of variation in consumer-diet d 15 N enrichment: a meta-analysis. Oecologia 136: 169-182. (Pubitemid 36933250)
53. Robbins C, Felicetti LA, Sponheimer M (2005) The effect of dietary protein quality on nitrogen isotope discrimination in mammals and birds. Oecologia 144: 534-540. doi:10.1007/s00442-005-0021-8. (Pubitemid 41218804)
54. Hussey NE, Olin JA, Kinney MJ, McMeans BC, Fisk AT (2012) Lipid extraction effects on stable isotope values (d13C and d15N) of elasmobranch muscle tissue. J Exp Mar Bio Ecol 434-5: 7-15.
55. Matich P, Heithaus M, Layman CA (2010) Contrasting patterns of individual specialization and trophic coupling in two marine apex predators. J Anim Ecol 80: 294-305. doi:10.1111/j.1365-2656.2010.01753.x.
56. Cortés E, Gruber SH (1990) Diet, feeding habits and estimates of daily ration of young lemon sharks, Negaprion brevirostris (Poey). Copeia: 204-218.
57. Peterson C, Fodrie FJ, Summerson HC, Powers S (2001) Site-Specific and Density-Dependent Extinction of Prey by Schooling Rays: Generation of a Population Sink in Top-Quality Habitat for Bay Scallops. Oecologia 129: 349-356. (Pubitemid 33066001)
58. Valentine J, Heck K Jr, Harper P (1994) Effects of bioturbation in controlling turtlegrass (Thalassia testudinum Banks ex König) abundance: evidence from field enclosures and observations in the Northern Gulf of Mexico. J Exp Mar Bio Ecol 178: 182-192.
59. Henningsen A (2000) Notes on reproduction in the Southern Stingray, Dasyatis americana (Chondrichthyes : Dasyatidae), in a captive environment. Copeia 3: 826-828.
60. O'Gorman E, Enright RA, Tompkins E (2008) Predator diversity enhances secondary production and decreases the likelihood of trophic cascades. Oecologia 158: 557-567. doi:10.1007/s00442-008-1165-0.
61. Smith WD, Cailliet GM, Cortés E (2008) Demography and elasticity of the diamond stingray, Dasyatis dipterura : parameter uncertainty and resilience to fishing pressure. Mar Freshwater Res 59: 575. doi:10.1071/MF07020.
62. Vander Zanden M, Rasmussen JB (2001) Variation in d15N and d13C trophic fractionation: implications for aquatic food web studies. Limnol Oceanogr 46: 2061-2066. (Pubitemid 34009955)