Advertisement

Oecologia

, Volume 189, Issue 3, pp 621–636 | Cite as

Inter-individual differences in ontogenetic trophic shifts among three marine predators

  • Philip MatichEmail author
  • Jeremy J. Kiszka
  • Michael R. Heithaus
  • Baptiste Le Bourg
  • Johann Mourier
Behavioral ecology – original research

Abstract

Ontogenetic niche shifts are widespread. However, individual differences in size at birth, morphology, sex, and personalities can cause variability in behavior. As such, inherent inter-individual differences within populations may lead to context-dependent changes in behavior with animal body size, which is of concern for understanding population dynamics and optimizing ecological monitoring. Using stable carbon and nitrogen isotope values from concurrently sampled tissues, we quantified the direction and magnitude of intraspecific variation in trophic shifts among three shark species, and how these changed with body size: spurdogs (Squalus spp.) in deep-sea habitats off La Réunion, bull sharks (Carcharhinus leucas) in estuarine habitats of the Florida Everglades, and blacktip reef sharks (Carcharhinus melanopterus) in coral reef ecosystems of Moorea, French Polynesia. Intraspecific variation in trophic shifts was limited among spurdogs, and decreased with body size, while bull sharks exhibited greater individual differences in trophic shifts, but also decreased in variability through ontogeny. In contrast, blacktip reef sharks exhibited increased intraspecific variation in trophic interactions with body size. Variability in trophic interactions and ontogenetic shifts are known to be associated with changes in energetic requirements, but can vary with ecological context. Our results suggest that environmental stability may affect variability within populations, and ecosystems with greater spatial and/or temporal variability in environmental conditions, and those with more diverse food webs may facilitate greater individual differences in trophic interactions, and thus ontogenetic trophic shifts. In light of concerns over environmental disturbance, elucidating the contexts that promote or dampen phenotypic variability is invaluable for predicting population- and community-level responses to environmental changes.

Keywords

Dietary shifts Elasmobranchs Foraging development Juveniles Nursery 

Notes

Acknowledgements

Data collection and sample analysis were funded by the National Science Foundation through the Florida Coastal Everglades LTER Program (DEB1237517, DBI0620409, DEB9910514), Florida International University’s Marine Sciences Program, the PADI Foundation, and National Geographic. J Mourier was supported by funding from the Ministère de l’Environnement, du Développement Durable et de l’Energie (MEDDE) together with Agence Nationale des Aires Marines Protégées (AAMP). We thank the many volunteers who assisted with shark fishing in both Moorea and the Florida Everglades, and sample preparation and processing. We thank IFREMER La Réunion and ARVAM (especially JP Quod) for providing sharks in La Réunion. We thank the Texas Research Institute for Environmental Studies for providing logistical support in preparation for the manuscript. Research was approved by and conducted under the protocols of Florida International University’s Institutional Animal Care and Use Committee, and in accordance to sampling permits EVER-2013-SCI-0020, EVER-2011-SCI-0031, EVER-2009-SCI-0024, and EVER-2007-SCI-0025 granted by Everglades National Park. This is the sixth publication for the Coastal Marine Ecology Program, and contribution #121 from the Center for Coastal Oceans Research within the Institute of Water and Environment at Florida International University. Data are made available through the Florida Coastal Everglades LTER program (http://fce.lternet.edu).

Author contribution statement

PM, JJK, MRH, BLB, and JM conceived and designed the sampling protocols. PM, JJK, and JM conducted the fieldwork and collected the data. PM analyzed the data. PM, JJK, MRH, BLB, and JM developed the questions investigated within the manuscript. PM, JJK, MRH, BLB, and JM wrote the manuscript.

Supplementary material

442_2019_4357_MOESM1_ESM.docx (172 kb)
Supplementary material 1 (DOCX 171 kb)

References

  1. Arias-Gonzalez JE, Delesalle B, Salvat B et al (1997) Trophic functioning of the Tiahura reef sector, Moorea Island, French Polynesia. Coral Reefs 16:231–246CrossRefGoogle Scholar
  2. Barton BT (2010) Climate warming and predation risk during herbivore ontogeny. Ecology 91:2811–2818CrossRefPubMedGoogle Scholar
  3. Bascompte J, Melian C, Sala E (2005) Interaction strength combinations and the voerfishing of a marine food web. PNAS 102:5443–5447CrossRefPubMedGoogle Scholar
  4. Baskett ML, Fabina NS, Gross K (2014) Response diversity can increase ecological resilience to disturbance in coral reefs. Am Nat 184:E16–E31CrossRefPubMedGoogle Scholar
  5. Bearhop S, Adams CE, Waldron S et al (2004) Determining trophic niche width: a novel approach using stable isotope analysis. J An Ecol 73:1007–1012CrossRefGoogle Scholar
  6. Beckerman AP, Petchey OL, Warren PH (2006) Foraging biology predicts food web complexity. PNAS 103:13745–13749CrossRefPubMedGoogle Scholar
  7. 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 455:245–256CrossRefGoogle Scholar
  8. Bird CS, Veríssimo A, Magozzi S et al (2018) A global perspective on the trophic geography of sharks. Nature Ecol Evol 2:305–399Google Scholar
  9. Bolnick DI, Yang LH, Fordyce JA et al (2002) Measuring individual-level resource specialization. Ecology 83:2936–2941CrossRefGoogle Scholar
  10. Bolnick DI, Svanbäck R, Fordyce JA et al (2003) The ecology of individuals: incidence and implications of individual specialization. Am Nat 161:1–28CrossRefPubMedGoogle Scholar
  11. Bolnick DI, Amarasekare P, Araújo MS et al (2011) Why intraspecific trait variation matters in community ecology. Trend Ecol Evol 26:183–192CrossRefGoogle Scholar
  12. Boucek RE, Rehage JS (2013) No free lunch: displaced marsh consumers regulate a prey subsidy to an estuarine consumer. Oikos 122:1453–1464Google Scholar
  13. Branstetter S, Stiles R (1987) Age and growth estimates of the bull shark, Carcharhinus leucas, from the northern Gulf of Mexico. Environ Biol Fish 20:169–181CrossRefGoogle Scholar
  14. 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 538:273–283CrossRefGoogle Scholar
  15. 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 492:185–198CrossRefGoogle Scholar
  16. Chapin FS III, Walker BH, Hobbs RJ et al (1997) Biotic control over the functioning of ecosystems. Science 277:500–504CrossRefGoogle Scholar
  17. Chouvelon T, Spitz J, Cherel Y et al (2011) Inter-specific and ontogenic differences in δ13C and δ15N values and Hg and Cd concentrations of cephalopods. Mar Ecol Prog Ser 433:107–120CrossRefGoogle Scholar
  18. Churchill DA, Heithaus MR, Grubbs RD (2015) Effects of lipid and urea extraction on δ15N values of deep-sea sharks and hagfish: Can mathematical correction factors be generated? Deep Sea Res Part II 115:103–108CrossRefGoogle Scholar
  19. 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 25:562–573CrossRefGoogle Scholar
  20. Colles A, Liow LH, Prinzing A (2009) Are specialists at risk under environmental change? Neoecological, paleoecological and phylogenetic approaches. Ecol Lett 12:849–863CrossRefPubMedPubMedCentralGoogle Scholar
  21. Davis S, Ogden JC (1994) Everglades: the ecosystem and its restoration. CRC Press, LondonCrossRefGoogle Scholar
  22. de Roos AM, Persson (2013) Population and community ecology of ontogentic development. Princeton Univ Press, PrincetonCrossRefGoogle Scholar
  23. 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 54:1956–1968CrossRefPubMedGoogle Scholar
  24. 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 26:309–323CrossRefGoogle Scholar
  25. Duffy JE (2009) Why biodiversity is important to the functioning of real-world ecosystems. Front Ecol Environ 7:437–444CrossRefGoogle Scholar
  26. Ebert DA, Fowler S, Compagno L (2013) Sharks of the world. Wild Nature Press, PlymouthGoogle Scholar
  27. Edmunds PJ, Leichter JJ, Adjeroud M (2010) Landscape-scale variation in coral recruitment in Moorea, French Polynesia. Mar Ecol Prog Ser 414:75–89CrossRefGoogle Scholar
  28. 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 54:640–645CrossRefGoogle Scholar
  29. Estrada JA, Rice AN, Natanson LJ et al (2006) Use of isotopic analysis of vertebrae in reconstructing ontogenetic feeding ecology in white sharks. Ecology 87:829–834CrossRefPubMedGoogle Scholar
  30. 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 150:1441–1452CrossRefGoogle Scholar
  31. Gross MR, Charnov EL (1980) Alternative male life histories in bluegill sunfish. Proc Nat Acad Sci 77:6937–6940CrossRefPubMedGoogle Scholar
  32. 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 319–350Google Scholar
  33. 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 54:472–482CrossRefGoogle Scholar
  34. Hooper DU, Chapin FS, Ewel JJ et al (2005) Effects of biodiversity on ecosystems functioning: a consensus of current knowledge. Ecol Mono 75:3–35CrossRefGoogle Scholar
  35. Hooper DU, Adair EC, Cardinale BJ et al (2012) A global synthesis reveals biodiversity loss as a major driver of ecosystem change. Nature 486:105–108CrossRefPubMedGoogle Scholar
  36. 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 169:395–406CrossRefPubMedGoogle Scholar
  37. Hussey NE, MacNeil MA, Olin JA et al (2012) Stable isotopes and elasmobranchs: tissue types, methods, applications and assumptions. J Fish Biol 80:1449–1484CrossRefPubMedGoogle Scholar
  38. Hyndes GA, Nagelkerken I, McLeod RJ et al (2014) Mechanisms and ecological roles of carbon transfer within coastal seascapes. Biol Rev 89:232–254CrossRefPubMedGoogle Scholar
  39. Kim SL, Koch PL (2012) Methods to collect, preserve, and prepare elasmobranch tissues for stable isotope analysis. Environ Biol Fish 95:53–63CrossRefGoogle Scholar
  40. 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 215:2495–2500CrossRefGoogle Scholar
  41. Knoff A, Hohn A, Macko S (2008) Ontogenetic diet changes in bottlenose dolphins (Tursiops truncatus) reflected through stable isotopes. Mar Mamm Sci 24:128–137CrossRefGoogle Scholar
  42. 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 37–113Google Scholar
  43. 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:e0138696CrossRefPubMedPubMedCentralGoogle Scholar
  44. Layman CA, Araujo MS, Boucek R et al (2012) Applying stable isotopes to examine food web structure: an overview of analytical tools. Biol Rev 87:542–562CrossRefGoogle Scholar
  45. Leichter JJ, Stokes MD, Hench JL et al (2012) The island-scale internal wave climate of Moorea, French Polynesia. J Geophys Res Oceans 117:C06008CrossRefGoogle Scholar
  46. Leu M, Hanser SE, Knick ST (2008) The human footprint in the west: a large-scale analysis of anthropogenic impacts. Ecol App 18:1119–1139CrossRefGoogle Scholar
  47. Lindenmayer DB, Likens GE, Andersen A et al (2012) Value of long-term ecological studies. Austral Ecol 37:745–757CrossRefGoogle Scholar
  48. MacNeil MA, Drouillard KG, Fisk AT (2006) Variable uptake and elimination of stable nitrogen isotopes between tissues in fish. Can J Fish Aquat Sci 63:345–353CrossRefGoogle Scholar
  49. Martinez del Rio C, Wolf N, Carelton SA et al (2009) Isotopic ecology ten years after a call for more laboratory experiments. Biol Rev 84:91–111CrossRefGoogle Scholar
  50. 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 83:199–213CrossRefGoogle Scholar
  51. 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 178:347–359CrossRefPubMedGoogle Scholar
  52. 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 67:877–885CrossRefGoogle Scholar
  53. Matich P, Heithaus MR, Layman CA (2011) Contrasting patterns of individual specialization and trophic coupling in two marine apex predators. J An Ecol 80:295–304CrossRefGoogle Scholar
  54. Matich P, Kiszka JJ, Heithaus MR et al (2015) Short-term shifts of stable isotope (δ13C, δ15N) values in juvenile sharks within nursery areas suggest rapid shifts in trophic interactions. J Exper Mar Biol Ecol 465:83–91CrossRefGoogle Scholar
  55. Matich P, Ault JS, Boucek RE et al (2017) Ecological niche partitioning within a large predator guild in a nutrient-limited estuary. Limnol Oceanog 62:934–953CrossRefGoogle Scholar
  56. McCauley DJ, Young HS, Dunbar RB et al (2012) Assessing the effects of large mobile predators on ecosystem connectivity. Ecol App 22:1711–1717CrossRefGoogle Scholar
  57. McClellan CM, Read AJ (2007) Complexity and variation in loggerhead sea turtle life history. Biol Lett 3:592–594CrossRefPubMedPubMedCentralGoogle Scholar
  58. McMeans BC, Olin JA, Benz GW (2009) Stable-isotope comparisons between embryos and mothers of a placentatrophic shark species. J Fish Biol 75:2464–2474CrossRefPubMedGoogle Scholar
  59. Mittelbach GG, Ballew NG, Kjevik MK (2014) Fish behavioral types and their ecological consequences. Can J Fish Aquat Sci 71:1–18CrossRefGoogle Scholar
  60. Moran NA (1992) The evolutionary maintenance of alternative phenotypes. Am Nat 139:971–989CrossRefGoogle Scholar
  61. Mourier J, Vercelloni J, Planes S (2012) Evidence of social communities in a spatially structured network of a free-ranging shark species. Annu Behav 83:389–401CrossRefGoogle Scholar
  62. Mourier J, Mills SC, Planes S (2013) Population structure, spatial distribution and life-history traits of blacktip reef sharks Carcharhinus melanopterus. J Fish Biol 82:979–993CrossRefPubMedGoogle Scholar
  63. Moya-Laraño J (2011) Genetic variation, predator-prey interactions and food web structure. Philos Trans R Soc Lond B 366:1425–1437CrossRefGoogle Scholar
  64. Naeem S, Bunker DE, Hector A et al (2009) Biodiversity, ecosystem-functioning, and human wellbeing. Oxford University Press, New YorkCrossRefGoogle Scholar
  65. 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 143:732–743CrossRefGoogle Scholar
  66. Newman SP, Handy RD, Gruber SH (2010) Diet and prey preference of juvenile lemon sharks Negaprion brevirostris. Mar Ecol Prog Ser 398:221–234CrossRefGoogle Scholar
  67. Newsome SD, Martinze del Rio C, Bearhop S et al (2007) A niche for isotopic ecology. Front Ecol Environ 5:429–436CrossRefGoogle Scholar
  68. Newsome SD, Etnier MA, Monson DH et al (2009a) Retrospective characterization of ontogenetic shifts in killer whale diets via δ13C and δ15N analysis of teeth. Mar Ecol Prog Ser 374:229–242CrossRefGoogle Scholar
  69. 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 90:961–974CrossRefPubMedGoogle Scholar
  70. 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 3:457–464CrossRefPubMedGoogle Scholar
  71. Nilsson KA, McCann KS, Caskenette AL (2018) Interaction strength and stability in stage-structured food web modules. Oikos 5:5.  https://doi.org/10.1111/oik.05029 CrossRefGoogle Scholar
  72. 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 25:1008–1016CrossRefGoogle Scholar
  73. Oliver TH, Heard MS, Isaac NJB et al (2015) Biodiversity and resilience of ecosystem functions. Trends Ecolo Evol 30:673–684CrossRefGoogle Scholar
  74. Persson L, de Roos AM (2013) Symmetry breaking in ecological systems through different energy efficiencies of juveniles and adults. Ecology 94:1487–1498CrossRefPubMedGoogle Scholar
  75. Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718CrossRefGoogle Scholar
  76. Post DM (2003) Individual variation in the timing of ontogenetic niche shifts in largemouth bass. Ecology 84:1298–1310CrossRefGoogle Scholar
  77. 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 152:179–189CrossRefPubMedGoogle Scholar
  78. 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 83Google Scholar
  79. Riede JO, Rall BC, Banasek-Richter C et al (2010) Scaling of food-web properties with diversity and complexity across ecosystems. Adv Ecol Res 42:139–170CrossRefGoogle Scholar
  80. Rigby C, Simpfendorfer CA (2015) Patterns in life history traits of deep-water chondrichthyans. Deep-Sea Res II 115:30–40CrossRefGoogle Scholar
  81. Rivest EB, Gouhier TC (2015) Complex environmental forcing across the biogeographical range of coral populations. PLoS One 10:e0121742CrossRefPubMedPubMedCentralGoogle Scholar
  82. 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 26:156–167CrossRefGoogle Scholar
  83. 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 178:5–16CrossRefPubMedGoogle Scholar
  84. Sala E, Knowlton N (2006) Global marine biodiversity trends. Annu Rev Environ Res 31:93–122CrossRefGoogle Scholar
  85. Salisbury CL, Seddon N, Cooney CR et al (2012) The latitudinal gradient in dispersal constraints: ecological specialisation drives diversification in tropical birds. Ecol Lett 15:847–855CrossRefPubMedGoogle Scholar
  86. Sánchez-Hernández J, Eloranta AP, Finstad AG et al (2017) Community structure affects trophic ontogeny in a predatory fish. Ecol Evol 7:358–367CrossRefPubMedGoogle Scholar
  87. 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:e103132CrossRefPubMedPubMedCentralGoogle Scholar
  88. 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 37:957–969CrossRefGoogle Scholar
  89. 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 27:481–497CrossRefGoogle Scholar
  90. 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 579:233–238CrossRefGoogle Scholar
  91. Sih A, Bell A, Johnson JC (2004) Behavioral syndromes: an ecological and evolutionary overview. Trend Ecol Evol 19:372–378CrossRefGoogle Scholar
  92. Skulason S, Smith TB (1995) Resource polymorphisms in vertebrates. Trend Ecol Evol 10:366–370CrossRefGoogle Scholar
  93. Snover ML (2008) Ontogenetic habitat shifts in marine organisms: Influencing factors and the impact of climate variability. Bull Mar Sci 83:53–67Google Scholar
  94. Subalusky AL, Fitzgerald LA, Smith LL (2009) Ontogenetic niche shifts in the American Alligator establish functional connectivity between aquatic systems. Biol Conserv 142:1507–1514CrossRefGoogle Scholar
  95. Taylor SM, Bennett MB (2008) Cephalopod dietary specialization and ontogenetic partitioning of the Australian weasel shark Hemigaleus australiensis White, Last & Compagno. J Fish Biol 72:917–936CrossRefGoogle Scholar
  96. Tilman D, Reich PB, Knops JMH (2006) Biodiversity and ecosystem stability in a decade-long grassland experiment. Nature 441:629–632CrossRefPubMedGoogle Scholar
  97. 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 44:301–308CrossRefGoogle Scholar
  98. Tyler PA (2003) Ecosystems of the deep oceans. Elsevier, USAGoogle Scholar
  99. 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: 28-41Google Scholar
  100. 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:e0116182CrossRefPubMedPubMedCentralGoogle Scholar
  101. Werner EE, Gilliam JF (1984) The ontogenetic niche and species interactions in size-structured populations. Annu Rev Ecol System 15:393–425CrossRefGoogle Scholar
  102. Wilbur HM (1980) Complex life cycles. Annu Rev Ecol Syst 11:67–93CrossRefGoogle Scholar
  103. Wiley TR, Simpfendorfer CA (2007) The ecology of elasmobranches occurring in the Everglades National Park, Florida: implications for conservation and management. Bull Mar Sci 80:171–189Google Scholar
  104. Wolf N, Carleton SA, Martínez del Rio C (2009) Ten years of experimental animal isotopic ecology. Func Ecol 23:17–26CrossRefGoogle Scholar
  105. Woodward G, Hildrew AG (2002) Body-size determinants of niche overlap and intraguild predation within a complex food web. J Annu Ecol 71:1063–1074CrossRefGoogle Scholar
  106. Wright AJ, Kyhn LA (2015) Practical management of cumulative anthropogenic impacts with working marine examples. Conserv Biol 29:333–340CrossRefPubMedGoogle Scholar
  107. Yang LH, Rudolf VHW (2010) Phenology, ontogeny and the effects of climate change on the timing of species interactions. Ecol Lett 13:1–10CrossRefPubMedGoogle Scholar
  108. 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 13:20170433CrossRefPubMedPubMedCentralGoogle Scholar
  109. 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 4:4649–4657CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Marine Sciences ProgramFlorida International UniversityNorth MiamiUSA
  2. 2.Texas Research Institute for Environmental StudiesSam Houston State UniversityHuntsvilleUSA
  3. 3.LIttoral ENvironnement et Sociétés (LIENSs)UMR 7266 CNRS-Université de la RochelleLa RochelleFrance
  4. 4.Laboratory of Oceanology, MARE CentreUniversité de LiègeLiègeBelgium
  5. 5.PSL Research University: EPHE-UPVD-CNRS, USR 3278 CRIOBEPerpignanFrance
  6. 6.Laboratoire d’excellence ‘CORAIL’, EPHEPSL Research University, UPVD, CNRS, USR 3278 CRIOBEMooreaFrench Polynesia
  7. 7.UMR MARBEC (IRD, Ifremer, Univ. Montpellier, CNRS)SèteFrance

Personalised recommendations