Matich, P.; Marine Sciences Program, Florida International University, 3000 NE 151st, North Miami, FL 33181, United States, Texas Research Institute for Environmental Studies, Sam Houston State University, 2424 Sam Houston Avenue, Huntsville, TX 77341, United States
Kiszka, J. J.; Marine Sciences Program, Florida International University, 3000 NE 151st, North Miami, FL 33181, United States
Heithaus, M. R.; Marine Sciences Program, Florida International University, 3000 NE 151st, North Miami, FL 33181, United States
Le Bourg, Baptiste ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Océanographie biologique
Mourier, J.; PSL Research University: EPHE-UPVD-CNRS, USR 3278 CRIOBE, Perpignan, 66860, France, Laboratoire d’excellence ‘CORAIL’, EPHE, PSL Research University, UPVD, CNRS, USR 3278 CRIOBE, Papetoai, Moorea, French Polynesia, UMR MARBEC (IRD, Ifremer, Univ. Montpellier, CNRS), Sète, 34203, France
Language :
English
Title :
Inter-individual differences in ontogenetic trophic shifts among three marine predators
Arias-Gonzalez JE, Delesalle B, Salvat B et al (1997) Trophic functioning of the Tiahura reef sector, Moorea Island, French Polynesia. Coral Reefs 16:231–246
Barton BT (2010) Climate warming and predation risk during herbivore ontogeny. Ecology 91:2811–2818
Bascompte J, Melian C, Sala E (2005) Interaction strength combinations and the voerfishing of a marine food web. PNAS 102:5443–5447
Baskett ML, Fabina NS, Gross K (2014) Response diversity can increase ecological resilience to disturbance in coral reefs. Am Nat 184:E16–E31
Bearhop S, Adams CE, Waldron S et al (2004) Determining trophic niche width: a novel approach using stable isotope analysis. J An Ecol 73:1007–1012
Belicka LL, Matich P, Jaffé R et al (2012) Fatty acids and stable isotopes as indicators of early-life feeding and potential maternal resource dependency in the bull shark Carcharhinus leucas. Mar Ecol Prog Ser 455:245–256
Bird CS, Veríssimo A, Magozzi S et al (2018) A global perspective on the trophic geography of sharks. Nature Ecol Evol 2:305–399
Bolnick DI, Yang LH, Fordyce JA et al (2002) Measuring individual-level resource specialization. Ecology 83:2936–2941
Bolnick DI, Svanbäck R, Fordyce JA et al (2003) The ecology of individuals: incidence and implications of individual specialization. Am Nat 161:1–28
Bolnick DI, Amarasekare P, Araújo MS et al (2011) Why intraspecific trait variation matters in community ecology. Trend Ecol Evol 26:183–192
Boucek RE, Rehage JS (2013) No free lunch: displaced marsh consumers regulate a prey subsidy to an estuarine consumer. Oikos 122:1453–1464
Branstetter S, Stiles R (1987) Age and growth estimates of the bull shark, Carcharhinus leucas, from the northern Gulf of Mexico. Environ Biol Fish 20:169–181
Brena PF, Mourier J, Planes S et al (2015) Shark and ray provisioning: functional insights into behavioral, ecological and physiological responses across multiple scales. Mar Ecol Prog Ser 538:273–283
Caut S, Jowers MJ, Michel L et al (2013) Diet- and tissue-specific incorporation of isotopes in the shark Scyliorhinus stellaris, a North Sea mesopredator. Mar Ecol Prog Ser 492:185–198
Chapin FS III, Walker BH, Hobbs RJ et al (1997) Biotic control over the functioning of ecosystems. Science 277:500–504
Chouvelon T, Spitz J, Cherel Y et al (2011) Inter-specific and ontogenic differences in δ 13 C and δ 15 N values and Hg and Cd concentrations of cephalopods. Mar Ecol Prog Ser 433:107–120
Churchill DA, Heithaus MR, Grubbs RD (2015) Effects of lipid and urea extraction on δ 15 N values of deep-sea sharks and hagfish: Can mathematical correction factors be generated? Deep Sea Res Part II 115:103–108
Clutton-Brock T, Sheldon BC (2010) Individuals and populations: the role of long-term, individual-based studies of animals in ecology and evolutionary biology. Trend Ecol Evol 25:562–573
Colles A, Liow LH, Prinzing A (2009) Are specialists at risk under environmental change? Neoecological, paleoecological and phylogenetic approaches. Ecol Lett 12:849–863
Davis S, Ogden JC (1994) Everglades: the ecosystem and its restoration. CRC Press, London
de Roos AM, Persson (2013) Population and community ecology of ontogentic development. Princeton Univ Press, Princeton
Donohue K, Messiqua D, Pyle EH et al (2000) Evidence of adaptive divergence in plasticity: density- and site-dependent selection on shade-avoidance responses in Impatiens capensis. Evolution 54:1956–1968
Drago M, Cardona L, Aguilar A et al (2010) Diet of lactating South American sea lions, as inferred from stable isotopes, influences pup growth. Mar Mamm Sci 26:309–323
Duffy JE (2009) Why biodiversity is important to the functioning of real-world ecosystems. Front Ecol Environ 7:437–444
Ebert DA, Fowler S, Compagno L (2013) Sharks of the world. Wild Nature Press, Plymouth
Edmunds PJ, Leichter JJ, Adjeroud M (2010) Landscape-scale variation in coral recruitment in Moorea, French Polynesia. Mar Ecol Prog Ser 414:75–89
Elliot M, Quintino V (2007) The Estuarine Quality Paradox, Environmental Homeostastis and the difficulty of detecting anthropogenic stress in naturally stressed areas. Mar Pollut Bull 54:640–645
Estrada JA, Rice AN, Natanson LJ et al (2006) Use of isotopic analysis of vertebrae in reconstructing ontogenetic feeding ecology in white sharks. Ecology 87:829–834
Field IC, Bradshaw CJA, van der Hoff J et al (2007) Age-related shifts in the diet composition of southern elephant seals expand overall foraging niche. Mar Biol 150:1441–1452
Gross MR, Charnov EL (1980) Alternative male life histories in bluegill sunfish. Proc Nat Acad Sci 77:6937–6940
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, London, pp 319–350
Heithaus MR, Delius BK, Wirsing AJ et al (2009) Physical factors influencing the distribution of a top predator in a subtropical oligotrophic estuary. Limnol Oceanogr 54:472–482
Hooper DU, Chapin FS, Ewel JJ et al (2005) Effects of biodiversity on ecosystems functioning: a consensus of current knowledge. Ecol Mono 75:3–35
Hooper DU, Adair EC, Cardinale BJ et al (2012) A global synthesis reveals biodiversity loss as a major driver of ecosystem change. Nature 486:105–108
Hückstadt LA, Koch PL, McDonald BI et al (2012) Stable isotope analyses reveal individual variability in the trophic ecology of a top predator, the southern elephant seal. Oecologia 169:395–406
Hussey NE, MacNeil MA, Olin JA et al (2012) Stable isotopes and elasmobranchs: tissue types, methods, applications and assumptions. J Fish Biol 80:1449–1484
Hyndes GA, Nagelkerken I, McLeod RJ et al (2014) Mechanisms and ecological roles of carbon transfer within coastal seascapes. Biol Rev 89:232–254
Kim SL, Koch PL (2012) Methods to collect, preserve, and prepare elasmobranch tissues for stable isotope analysis. Environ Biol Fish 95:53–63
Kim SL, del Rio CM, Casper D et al (2012) Isotopic incorporation rates for shark tissues from a long-term captive feeding study. J Exper Biol 215:2495–2500
Knoff A, Hohn A, Macko S (2008) Ontogenetic diet changes in bottlenose dolphins (Tursiops truncatus) reflected through stable isotopes. Mar Mamm Sci 24:128–137
Kyne PM, Simpfendorfer CA (2010) Deepwater chondrichthyans. In: Carrier JC et al (eds) Sharks and their relatives II: biodiversity, adaptive physiology, and conservation. CRC Press, London, pp 37–113
Lamy T, Legendre P, Chancerelle Y et al (2015) Understanding the spatio-temporal response of coral reef fish communities to natural disturbances: insights from beta-diversity decomposition. PLoS One 10:e0138696
Layman CA, Araujo MS, Boucek R et al (2012) Applying stable isotopes to examine food web structure: an overview of analytical tools. Biol Rev 87:542–562
Leichter JJ, Stokes MD, Hench JL et al (2012) The island-scale internal wave climate of Moorea, French Polynesia. J Geophys Res Oceans 117:C06008
Leu M, Hanser SE, Knick ST (2008) The human footprint in the west: a large-scale analysis of anthropogenic impacts. Ecol App 18:1119–1139
Lindenmayer DB, Likens GE, Andersen A et al (2012) Value of long-term ecological studies. Austral Ecol 37:745–757
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
Martinez del Rio C, Wolf N, Carelton SA et al (2009) Isotopic ecology ten years after a call for more laboratory experiments. Biol Rev 84:91–111
Matich P, Heithaus MR (2014) Multi-tissue stable isotope analysis and acoustic telemetry reveal seasonal variability in the trophic interactions of juvenile bull sharks in a coastal estuary. J An Ecol 83:199–213
Matich P, Heithaus MR (2015) Individual variation in ontogenetic niche shifts in habitat use and movement patterns of a large estuarine predator (Carcharhinus leucas). Oecologia 178:347–359
Matich P, Heithaus MR, Layman CA (2010) Size-based variation in inter-tissue comparisons of stable carbon and nitrogen isotopic signatures of bull sharks (Carcharhinus leucas) and tiger sharks (Galeocerdo cuvier). Can J Fish Aquat Sci 67:877–885
Matich P, Heithaus MR, Layman CA (2011) Contrasting patterns of individual specialization and trophic coupling in two marine apex predators. J An Ecol 80:295–304
Matich P, Kiszka JJ, Heithaus MR et al (2015) Short-term shifts of stable isotope (δ 13 C, δ 15 N) values in juvenile sharks within nursery areas suggest rapid shifts in trophic interactions. J Exper Mar Biol Ecol 465:83–91
Matich P, Ault JS, Boucek RE et al (2017) Ecological niche partitioning within a large predator guild in a nutrient-limited estuary. Limnol Oceanog 62:934–953
McCauley DJ, Young HS, Dunbar RB et al (2012) Assessing the effects of large mobile predators on ecosystem connectivity. Ecol App 22:1711–1717
McClellan CM, Read AJ (2007) Complexity and variation in loggerhead sea turtle life history. Biol Lett 3:592–594
McMeans BC, Olin JA, Benz GW (2009) Stable-isotope comparisons between embryos and mothers of a placentatrophic shark species. J Fish Biol 75:2464–2474
Mittelbach GG, Ballew NG, Kjevik MK (2014) Fish behavioral types and their ecological consequences. Can J Fish Aquat Sci 71:1–18
Moran NA (1992) The evolutionary maintenance of alternative phenotypes. Am Nat 139:971–989
Mourier J, Vercelloni J, Planes S (2012) Evidence of social communities in a spatially structured network of a free-ranging shark species. Annu Behav 83:389–401
Mourier J, Mills SC, Planes S (2013) Population structure, spatial distribution and life-history traits of blacktip reef sharks Carcharhinus melanopterus. J Fish Biol 82:979–993
Moya-Laraño J (2011) Genetic variation, predator-prey interactions and food web structure. Philos Trans R Soc Lond B 366:1425–1437
Naeem S, Bunker DE, Hector A et al (2009) Biodiversity, ecosystem-functioning, and human wellbeing. Oxford University Press, New York
Natanson LJ, Adams DH, Winton MV et al (2014) Age and growth of the bull shark in the western North Atlantic Ocean. Trans Am Fish Soc 143:732–743
Newman SP, Handy RD, Gruber SH (2010) Diet and prey preference of juvenile lemon sharks Negaprion brevirostris. Mar Ecol Prog Ser 398:221–234
Newsome SD, Martinze del Rio C, Bearhop S et al (2007) A niche for isotopic ecology. Front Ecol Environ 5:429–436
Newsome SD, Etnier MA, Monson DH et al (2009a) Retrospective characterization of ontogenetic shifts in killer whale diets via δ 13 C and δ 15 N analysis of teeth. Mar Ecol Prog Ser 374:229–242
Newsome SD, Tinker MT, Monson DH et al (2009b) Using stable isotopes to investigate individual diet specialization in California sea otters (Enhydra lutris nereis). Ecology 90:961–974
Niemelä PT, Vainikka A, Forsman JT et al (2013) How does variation in the environment and individual cognition explain the existence of consistent behavioral differences? Ecol Evol 3:457–464
Nilsson KA, McCann KS, Caskenette AL (2018) Interaction strength and stability in stage-structured food web modules. Oikos 5:5. 10.1111/oik.05029
Olin JA, Hussey NE, Fritts M et al (2011) Maternal meddling in neonatal sharks: implications for interpreting stable isotopes in young animals. Rapid Comm Mass Spect 25:1008–1016
Oliver TH, Heard MS, Isaac NJB et al (2015) Biodiversity and resilience of ecosystem functions. Trends Ecolo Evol 30:673–684
Persson L, de Roos AM (2013) Symmetry breaking in ecological systems through different energy efficiencies of juveniles and adults. Ecology 94:1487–1498
Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718
Post DM (2003) Individual variation in the timing of ontogenetic niche shifts in largemouth bass. Ecology 84:1298–1310
Post DM, Layman CA, Arrington DA 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
Pritchard DW (1967) What is an estuary: physical standpoint. In: Estuaries (ed) Lauf GH, pp 3–5. Washington, DC, USA: American Association for the Advancement of Science, Publication 83
Riede JO, Rall BC, Banasek-Richter C et al (2010) Scaling of food-web properties with diversity and complexity across ecosystems. Adv Ecol Res 42:139–170
Rigby C, Simpfendorfer CA (2015) Patterns in life history traits of deep-water chondrichthyans. Deep-Sea Res II 115:30–40
Rivest EB, Gouhier TC (2015) Complex environmental forcing across the biogeographical range of coral populations. PLoS One 10:e0121742
Rosenblatt AE, Heithaus MR, Mather ME et al (2013) The roles of large top predators in coastal ecosystems: new insights from Long-Term Ecological Research. Oceanography 26:156–167
Rosenblatt AE, Nifong JC, Heithaus MR et al (2015) Factors affecting individual foraging specialization and temporal diet stability across the range of a large “generalist” apex predator. Oecologia 178:5–16
Sala E, Knowlton N (2006) Global marine biodiversity trends. Annu Rev Environ Res 31:93–122
Salisbury CL, Seddon N, Cooney CR et al (2012) The latitudinal gradient in dispersal constraints: ecological specialisation drives diversification in tropical birds. Ecol Lett 15:847–855
Sánchez-Hernández J, Eloranta AP, Finstad AG et al (2017) Community structure affects trophic ontogeny in a predatory fish. Ecol Evol 7:358–367
Saporiti F, Bearhop S, Silva L et al (2014) Longer and less overlapping food webs in anthropogenically disturbed marine ecosystems: confirmations from the past. PLoS One 9:e103132
Saporiti F, Bearhop S, Vales DG et al (2016) Resource partitioning among air-breathing marine predators: are body size and mouth diameter the major determinants? Mar Ecol 37:957–969
Shipley ON, Brooks EJ, Madigan DJ et al (2017a) Stable isotope analysis in deep-sea chondrichthyans: recent challenges, ecological insights, and future directions. Rev Fish Biol Fish 27:481–497
Shipley ON, Murchie KJ, Frisk MG et al (2017b) Low lipid and urea effects and inter-tissue comparisons of stable isotope signatures in three nearshore elasmobranchs. Mar Ecol Prog Ser 579:233–238
Sih A, Bell A, Johnson JC (2004) Behavioral syndromes: an ecological and evolutionary overview. Trend Ecol Evol 19:372–378
Skulason S, Smith TB (1995) Resource polymorphisms in vertebrates. Trend Ecol Evol 10:366–370
Snover ML (2008) Ontogenetic habitat shifts in marine organisms: Influencing factors and the impact of climate variability. Bull Mar Sci 83:53–67
Subalusky AL, Fitzgerald LA, Smith LL (2009) Ontogenetic niche shifts in the American Alligator establish functional connectivity between aquatic systems. Biol Conserv 142:1507–1514
Taylor SM, Bennett MB (2008) Cephalopod dietary specialization and ontogenetic partitioning of the Australian weasel shark Hemigaleus australiensis White, Last & Compagno. J Fish Biol 72:917–936
Tilman D, Reich PB, Knops JMH (2006) Biodiversity and ecosystem stability in a decade-long grassland experiment. Nature 441:629–632
Torres-Rojas YE, Hernandez-Herrera A, Galván-Magaña F et al (2010) Stomach content analysis of juvenile, scalloped hammerhead shark Sphyrna lewini captured off the coast of Mazatlan, Mexico. Aquat Ecol 44:301–308
Tyler PA (2003) Ecosystems of the deep oceans. Elsevier, USA
Valls M, Rueda L, Quetglas A (2017) Feeding strategies and resource partitioning among elasmobranchs and cephalopods in Mediterranean deep-sea ecosystems. Deep-Sea Res Part I: 28-41
Vander Zanden JM, Clayton MK, Moody EK et al (2015) Stable isotope turnover and half-life in animal tissues: a literature synthesis. PLoS One 10:e0116182
Werner EE, Gilliam JF (1984) The ontogenetic niche and species interactions in size-structured populations. Annu Rev Ecol System 15:393–425
Wilbur HM (1980) Complex life cycles. Annu Rev Ecol Syst 11:67–93
Wiley TR, Simpfendorfer CA (2007) The ecology of elasmobranches occurring in the Everglades National Park, Florida: implications for conservation and management. Bull Mar Sci 80:171–189
Wolf N, Carleton SA, Martínez del Rio C (2009) Ten years of experimental animal isotopic ecology. Func Ecol 23:17–26
Woodward G, Hildrew AG (2002) Body-size determinants of niche overlap and intraguild predation within a complex food web. J Annu Ecol 71:1063–1074
Wright AJ, Kyhn LA (2015) Practical management of cumulative anthropogenic impacts with working marine examples. Conserv Biol 29:333–340
Yang LH, Rudolf VHW (2010) Phenology, ontogeny and the effects of climate change on the timing of species interactions. Ecol Lett 13:1–10
Yurkowski DJ, Hussey NE, Fisk AT et al (2017) Temporal shifts in intraguild predation pressure between beluga whales and Greenland halibut in a changing Arctic. Biol Lett 13:20170433
Zhao T, Villéger S, Lek S et al (2014) High intraspecific variability in the functional niche of a predator is associated with ontogenetic shift and individual specialization. Ecol Evol 4:4649–4657
