, Volume 178, Issue 2, pp 347–359 | Cite as

Individual variation in ontogenetic niche shifts in habitat use and movement patterns of a large estuarine predator (Carcharhinus leucas)

  • Philip Matich
  • Michael R. Heithaus
Behavioral ecology - Original research


Ontogenetic niche shifts are common among animals, yet most studies only investigate niche shifts at the population level, which may overlook considerable differences among individuals in the timing and dynamics of these shifts. Such divergent behaviors within size-/age-classes have important implications for the roles a population—and specific age-classes—play in their respective ecosystem(s). Using acoustic telemetry, we tracked the movements of juvenile bull sharks in the Shark River Estuary of Everglades National Park, Florida, and found that sharks increased their use of marine microhabitats with age to take advantage of more abundant resources, but continued to use freshwater and estuarine microhabitats as refuges from marine predators. Within this population-level ontogenetic niche shift, however, movement patterns varied among individual sharks, with 47 % of sharks exhibiting condition-dependent habitat use and 53 % appearing risk-averse regardless of body condition. Among sharks older than age 0, fifty percent made regular movements between adjacent regions of the estuary, while the other half made less predictable movements that often featured long-term residence in specific regions. Individual differences were apparently shaped by both intrinsic and extrinsic factors, including individual responses to food-risk trade-offs and body condition. These differences appear to develop early in the lives of bull sharks, and persist throughout their residencies in nursery habitats. The widespread occurrence of intraspecific variation in behavior among mobile taxa suggests it is important in shaping population dynamics of at least some species, and elucidating the contexts and timing in which it develops and persists is important for understanding its role within communities.


Acoustic telemetry Fast fourier transform Niche-width expansion Shark nursery State-dependent behavior 



Funding for this project was provided by the National Science Foundation to the Florida Coastal Everglades LTER Program (DBI0620409, DEB9910514, DRL0959026) and Florida International University’s Marine Sciences Program. We thank the many volunteers who assisted with shark fishing. Special thanks to Adam Rosenblatt for establishing the array of acoustic receivers and helping with downloading data, and providing analytical support. Thanks to Andrew Fritz for developing software for managing movement data and providing analytical support. Thanks also to Joel Trexler for providing logistical and analytical support for this project. Thanks to Philip Stoddard for providing comments on earlier versions of 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 with sampling permits EVER-2011-SCI-0031, EVER-2009-SCI-0024, and EVER-2007-SCI-0025 granted by Everglades National Park.


  1. Barton BT (2010) Climate warming and predation risk during herbivore ontogeny. Ecology 91:2811–2818CrossRefPubMedGoogle Scholar
  2. Bell AM, Hankison SJ, Laskowski KL (2009) The repeatability of behavior: a meta-analysis. Anim Behav 77:771–783CrossRefPubMedCentralPubMedGoogle Scholar
  3. 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 161:1–28CrossRefPubMedGoogle Scholar
  4. Bolnick DI, Amarasekare P, Araujo MS, Burger R, Levine JM, Novak M, Rudolf VHW, Schreiber SJ, Urban MC, Vasseur DA (2011) Why intraspecific trait variation matters in community ecology. Trend Ecol Evol 26:183–192CrossRefGoogle Scholar
  5. Bransky JW, Dorn NJ (2013) Prey use of wetland benthivorous sunfishes: ontogenetic, interspecific and seasonal variation. Environ Biol Fish 96:1329–1340CrossRefGoogle Scholar
  6. Brien ML, Webb GJ, Lang JW, McGuinness KA, Christian KA (2013) Born to be bad: agonistic behavior in hatchling saltwater crocodiles (Crocodylus porosus). Behavior 150:737–762Google Scholar
  7. Castro JI (2011) The sharks of North America. Oxford University Press, CaryGoogle Scholar
  8. Childers DL (2006) A synthesis of long-term research by the Florida Coastal Everglades LTER Program. Hydrobiologia 569:531–544CrossRefGoogle Scholar
  9. Clark CW (1994) Antipredator behaviour and the asset protection principle. Behav Ecol 5:159–170CrossRefGoogle Scholar
  10. Clark CW, Mangel M (2000) Dynamic state variable models in ecology. Methods and applications. Oxford University Press, CaryGoogle Scholar
  11. Conrath CL, Musick JA (2010) Residency, space use and movement patterns of juvenile sandbar sharks (Carcharhinus plumbeus) within a Virginia summer nursery area. Mar Freshwater Res 61:223–235CrossRefGoogle Scholar
  12. Curtis TH, Adams DH, Burgess GH (2011) Seasonal distribution and habitat associations of bull sharks in the Indian River Lagoon, Florida: a 30-year synthesis. Trans Am Fish Soc 140:1213–1226CrossRefGoogle Scholar
  13. Davis S, Childers DL, Lorenz JJ, Wanless HR, Hopkins TE (2005) A conceptual model of ecological interactions in the mangrove estuaries of the Florida Everglades. Wetlands 25:832–842CrossRefGoogle Scholar
  14. Day T, Young KA (2004) Competitive and facilitative evolutionary diversification. Bioscience 54:101–109CrossRefGoogle Scholar
  15. de Roos AM, Leonardsson K, Persson L, Mittlebach GG (2002) Ontogenetic niche shifts and flexible behavior in size-structured populations. Ecol Monogr 72:271–292CrossRefGoogle Scholar
  16. Espinoza M, Farrugia TJ, Lowe CG (2011) Habitat use, movements and site fidelity of the gray smooth-hound shark (Mustelus californicus Gill 1863) in a newly restored southern California estuary. J Exp Mar Biol Ecol 401:63–74CrossRefGoogle Scholar
  17. Gross MR (1991) Salmon breeding behavior and life history evolution in changing environments. Ecology 72:1180–1186CrossRefGoogle Scholar
  18. Gross MR, Charnov EL (1980) Alternative male life histories in bluegill sunfish. Proc Natl Acad Sci 77:6937–6940CrossRefPubMedCentralPubMedGoogle Scholar
  19. Gross MR, Repka J (1998) Game theory and inheritance in the conditional strategy. In: Dugatkin LA, Reeve HK (eds) Game theory and animal behavior. Oxford University Press, New York, pp 168–187Google Scholar
  20. Grubbs RD (2010) Ontogenetic shifts in movements and habitat use. In: Carrier JC, Musick JA, Heithaus MR (eds) Sharks and their relatives. II. Biodiversity, adaptive physiology, and conservation. CRC, Boca Raton, pp 319–350CrossRefGoogle Scholar
  21. Guttridge TL, Gruber SH, Franks BR, Kessel ST, Gledhill KS, Uphill J, Krause J, Sims DW (2012) Deep danger: intera-specific predation risk influences habitat use and aggregation formation of juvenile lemon sharks Negaprion brevirostris. Mar Ecol Prog Ser 445:279–291CrossRefGoogle Scholar
  22. Hays GC, Kennedy H, Frost BW (2001) Individual variability in diel vertical migration of a marine copepod: why some individuals remain at depth when others migrate. Limnol Oceanogr 46:2050–2054CrossRefGoogle Scholar
  23. Heithaus MR (2007) Nursery areas as essential shark habitats: a theoretical perspective. Am Fish Soc Symp 50:3–13Google Scholar
  24. Heithaus MR, Frid A, Wirsing AJ, Dill LM, Fourqurean JW, Burkholder D, Thomson J, Bejder L (2007a) State-dependent risk-taking by green sea turtles mediates top-down effects of tiger shark intimidation in a marine ecosystem. J Anim Ecol 76:837–844CrossRefPubMedGoogle Scholar
  25. Heithaus MR, Burkholder D, Hueter RE, Heithaus LI, Pratt HL Jr, Carrier JC (2007b) Spatial and temporal variation in shark communities of the Lower Florida Keys and evidence for historical population declines. Can J Fish Aquat Sci 64:1302–1313CrossRefGoogle Scholar
  26. Heithaus MR, Delius BK, Wirsing AJ, Dunphy-Daly MM (2009) Physical factors influencing the distribution of a top predator in a subtropical oligotrophic estuary. Limnol Oceanogr 54:472–482CrossRefGoogle Scholar
  27. 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. II. Biodiversity, adaptive physiology, and conservation. CRC, Boca Raton, pp 611–637CrossRefGoogle Scholar
  28. Heupel MR, Carlson JK, Simpfendorfer CA (2007) Shark nursery areas: concepts, definition, characterization and assumptions. Mar Ecol Prog Ser 337:287–297CrossRefGoogle Scholar
  29. Holland KN, Wetherbee BM, Peterson JD, Lowe CG (1993) Movements and distribution of hammerhead shark pups on their natal grounds. Copeia 2:495–502CrossRefGoogle Scholar
  30. Houston A, Clark A, McNamara J, Mangel M (1988) Dynamic models in behavioural and evolutionary ecology. Nature 332:29–34CrossRefGoogle Scholar
  31. Lowry D, de Castro ALF, Mara K, Whiteneck LB, Delius B, Burgess GH, Motta P (2009) Determining shark size from forensic analysis of bite damage. Mar Biol 156:2483–2492CrossRefGoogle Scholar
  32. Matich P, Heithaus MR (2012) Effects of an extreme temperature event on the behavior and age structure of an estuarine top predator (Carcharhinus leucas). Mar Ecol Prog Ser 447:165–178CrossRefGoogle Scholar
  33. 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 Anim Ecol 83:199–213CrossRefPubMedGoogle Scholar
  34. Matich P, Heithaus MR, Layman CA (2010) Size-based variation in inter-tissue comparisons of stable carbon and nitrogen isotopic signatures of bull sharks (Carcharhinusn leucas) and tiger sharks (Galeocerdo cuvier). Can J Fish Aquat Sci 67:877–885CrossRefGoogle Scholar
  35. Matich P, Heithaus MR, Layman CA (2011) Contrasting patterns of individual specialization and trophic coupling in two marine apex predators. J Anim Ecol 80:295–304CrossRefGoogle Scholar
  36. Mittelbach GG, Ballew NG, Kjelvik MK (2014) Fish behavioral types and their ecological consequences. Can J Fish Aquat Sci 71:1–18CrossRefGoogle Scholar
  37. Neer JA, Thompson BA, Carlson JK (2005) Age and growth of Carcharhinus leucas in the northern Gulf of Mexico: incorporating variability in size at birth. J Fish Biol 67:370–383CrossRefGoogle Scholar
  38. Newsome SD, Etnier MA, Monson DH, Fogel ML (2009) Retrospective characterization of ontogenetic shifts in killer whale diets via δ13C and δ15N analysis of teeth. Mar Ecol Prog Ser 374:229–242CrossRefGoogle Scholar
  39. Odum EP (1980) The status of the three ecosystem-level hypotheses regarding salt marsh estuaries: tidal subsidy, outwelling and detritus-based food chains. In: Kennedy V (ed) Estuarine perspectives. Academic Press, New York, pp 485–495CrossRefGoogle Scholar
  40. Ogden JC, Davis SM, Jacobs KJ, Barnes T, Fling HE (2005) The use of conceptual ecological models to guide ecosystem restoration in south Florida. Wetlands 25:795–809CrossRefGoogle Scholar
  41. Papastamatiou YP, Lowe CG, Caselle JE, Friedlander AM (2009) Scale-dependent effects of habitat on movements and path structure of reef sharks at a predator-dominated atoll. Ecology 90:996–1008CrossRefPubMedGoogle Scholar
  42. Pfennig DW, Rice AM, Martin RA (2007) Field and experimental evidence for competition’s role in phenotypic divergence. Evolution 61:257–271CrossRefPubMedGoogle Scholar
  43. Post DM (2003) Individual variation in the timing of ontogenetic niche shifts in largemouth bass. Ecology 84:1298–1310CrossRefGoogle Scholar
  44. Regnier T, Labonne J, Gaudin P, Bolliet V (2012) Influence of energetic status on ontogenetic niche shifts: emergence from the redd is linked to metabolic rate in brown trout. Oecologia 168:371–380CrossRefPubMedGoogle Scholar
  45. Rosenblatt AE, Heithaus MR (2011) Does variation in movement tactics and trophic interactions among American alligators create habitat linkage? J Anim Ecol 80:786–798CrossRefPubMedGoogle Scholar
  46. Rosenblatt AE, Heithaus MR, Mather ME, Matich P, Nifong JC, Ripple WJ, Silliman BR (2013) The roles of large top predators in coastal ecosystems: new insights from long-term ecological research. Oceanography 26:156–167CrossRefGoogle Scholar
  47. Sih A, Bell A, Johnson JC (2004) Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol Evol 19:372–378CrossRefPubMedGoogle Scholar
  48. Simard M, Zhang K, Rivera-Monroy VH, Ross MS, Ruiz PL, Castaneda-Moya E, Twilley RR, Rodriguez E (2006) Mapping height and biomass of mangrove forests in Everglades National Park with SRTM elevation data. Photogramm Eng Remote Sens 72:299–311CrossRefGoogle Scholar
  49. Simpfendorfer CA, Freitas GG, Wiley TR, Heupel MR (2005) Distribution and habitat partitioning of immature bull sharks (Carcharhinus leucas) in a southwest Florida estuary. Estuaries 28:78–85CrossRefGoogle Scholar
  50. Sinclair ARE, Arcese P (1995) Population consequences of predation-sensitive foraging: the Serengeti wildebeest. Ecology 76:882–891CrossRefGoogle Scholar
  51. Skulason S, Smith TB (1995) Resource polymorphisms in vertebrates. Trends Ecol Evol 10:366–370CrossRefPubMedGoogle Scholar
  52. Smith TB, Skulason S (1996) Evolutionary significance of resource polymorphisms in fishes, amphibians, and birds. Annu Rev Ecol Syst 27:111–133CrossRefGoogle Scholar
  53. Videler JJ, Wardle CS (1991) Fish swimming stride by stride: speed limits and endurance. Rev Fish Biol Fish 1:23–40CrossRefGoogle Scholar
  54. Werner EE, Gilliam JF (1984) The ontogenetic niche and species interactions in size-structured populations. Annu Rev Ecol Syst 15:393–425CrossRefGoogle Scholar
  55. Wilbur HM (1980) Complex life cycles. Annu Rev Ecol Syst 11:67–93CrossRefGoogle Scholar
  56. 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
  57. 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

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.Marine Sciences ProgramFlorida International UniversityNorth MiamiUSA

Personalised recommendations