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Factors affecting individual foraging specialization and temporal diet stability across the range of a large “generalist” apex predator

Abstract

Individual niche specialization (INS) is increasingly recognized as an important component of ecological and evolutionary dynamics. However, most studies that have investigated INS have focused on the effects of niche width and inter- and intraspecific competition on INS in small-bodied species for short time periods, with less attention paid to INS in large-bodied reptilian predators and the effects of available prey types on INS. We investigated the prevalence, causes, and consequences of INS in foraging behaviors across different populations of American alligators (Alligator mississippiensis), the dominant aquatic apex predator across the southeast US, using stomach contents and stable isotopes. Gut contents revealed that, over the short term, although alligator populations occupied wide ranges of the INS spectrum, general patterns were apparent. Alligator populations inhabiting lakes exhibited lower INS than coastal populations, likely driven by variation in habitat type and available prey types. Stable isotopes revealed that over longer time spans alligators exhibited remarkably consistent use of variable mixtures of carbon pools (e.g., marine and freshwater food webs). We conclude that INS in large-bodied reptilian predator populations is likely affected by variation in available prey types and habitat heterogeneity, and that INS should be incorporated into management strategies to efficiently meet intended goals. Also, ecological models, which typically do not consider behavioral variability, should include INS to increase model realism and applicability.

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References

  1. Adams D, Paperno R (2012) Stable isotopes and mercury in a model estuarine fish: multibasin comparisons with water quality, community structure, and available prey base. Sci Total Environ 414:445–455

  2. Araujo M, Bolnick DI, Machado G, Giaretta AA, dos Reis SF (2007) Using δ13C stable isotopes to quantify individual-level diet variation. Oecologia 152:643–654

  3. Araujo M, Bolnick DI, Martinelli LA, Giaretta AA, dos Reis SF (2009) Individual-level diet variation in four species of Brazilian frogs. J Anim Ecol 78:848–856

  4. Araujo M, Bolnick DI, Layman CA (2011) The ecological causes of individual specialisation. Ecol Lett 14:948–958

  5. Bachmann R, Hoyer MV, Canfield DE (1999) The restoration of Lake Apopka in relation to alternative stable states. Hydrobiologia 394:219–232

  6. Baird RW, Abrams PA, Dill LM (1992) Possible indirect inter- actions between transient and resident killer whales: implications for the evolution of foraging specializations in the genus Orcinus. Oecologia 89:125–132

  7. Bolnick D, Yang LH, Fordyce JA, Davis JM, Svanback R (2002) Measuring individual-level resource specialization. Ecology 83:2936–2941

  8. Bolnick D, Svanback R, Fordyce JA, Yang LH, Davis JM, Husley CD, Forister ML (2003) The ecology of individuals: incidence and implications of individual specialization. Am Nat 161:1–28

  9. Bolnick D, Svanback R, Araujo MS, Persson L (2007) Comparative support for the niche variation hypothesis that more generalized populations also are more heterogeneous. Proc Natl Acad Sci USA 104:10075–10079

  10. Bolnick D, Ingram T, Stutz WE, Snowberg LK, Lau OL, Paull JS (2010) Ecological release from interspecific competition leads to decoupled changes in population and individual niche width. Proc R Soc Lond B 277:1789–1797

  11. Dalerum F, Angerbjorn A (2005) Resolving temporal variation in vertebrate diets using naturally occurring stable isotopes. Oecologia 144:647–658

  12. Dall S, Bell AM, Bolnick DI, Ratnieks FLW (2012) An evolutionary ecology of individual differences. Ecol Lett 15:1189–1198

  13. Darby P, Bennetts RE, Karunaratne LB (2006) Apple snail densities in habitats used by foraging snail kites. Fla Field Nat 34:37–47

  14. Darimont C, Paquet PC, Reimchen TE (2009) Landscape heterogeneity and marine subsidy generate extensive intrapopulation niche diversity in a large terrestrial vertebrate. J Anim Ecol 78:126–133

  15. Delany M (1990) Late summer diet of juvenile American alligators. J Herpetol 24:418–421

  16. Delany M, Abercrombie CL (1986) American alligator food-habits in north-central Florida. J Wildl Manag 50:348–353

  17. Delany M, Woodward AR, Kochel IH (1988) Nuisance alligator food habits in Florida. Fla Field Nat 16:90–96

  18. Delany M, Linda SB, Moore CT (1999) Diet and condition of American alligators in 4 Florida lakes. Proc Annu Conf Southeast Assoc Fish Wildl Agencies 53:375–389

  19. Doren R, Trexler JC, Gottlieb AD, Harwell MC (2009) Ecological indicators for system-wide assessment of the greater Everglades ecosystem restoration program. Ecol Indic 9S:S2–S16

  20. Elsey R, McNease L, Joanen T, Kinler N (1992) Food habits of native wild and farm-released juvenile alligators. Proc Annu Conf Southeast Assoc Fish Wildl Agencies 46:57–66

  21. Estes J, Riedman ML, Staedler MM, Tinker MT, Lyon BE (2003) Individual variation in prey selection by sea otters: patterns, causes and implications. J Anim Ecol 72:144–155

  22. Fitzgerald L (1989) An evaluation of stomach flushing techniques for crocodilians. J Herpetol 23:170–172

  23. Ford J, Ellis GM, Barrett-Lennard LG, Morton AB, Palm RS, Balcomb KC (1998) Dietary specialization in two sympatric populations of killer whales (Orcinus orca) in coastal British Columbia and adjacent waters. Can J Zool 76:1456–1471

  24. Fry B (2006) Stable isotope ecology. Springer, New York

  25. Gabrey S (2010) Demographic and geographic variation in food habits of American alligators (Alligator mississippiensis) in Louisiana. Herpetol Conserv Biol 5:241–250

  26. Garnett S (1985) The consequences of slow chitin digestion on crocodilian diet analyses. J Herpetol 19:303–304

  27. Goodwin T, Marion WR (1979) Seasonal activity and habitat preferences of adult alligators in a north-central Florida lake. J Herpetol 13:157–164

  28. Gu B, Schelske CL, Hoyer MV (1997) Intrapopulation feeding diversity in blue tilapia: evidence from stable-isotope analyses. Ecology 78:2263–2266

  29. Heithaus M (2013) Predators, prey, and the ecological roles of sea turtles. In: Wyneken J, Lohmann KJ, Musick JA (eds) The biology of sea turtles, vol III. CRC, Boca Raton, pp 249–284

  30. Holling C (1959) Some characteristics of simple types of predation and parasitism. Can Entomol 91:385–398

  31. Janes D, Gutzke WHN (2002) Factors affecting retention time of turtle scutes in stomachs of American alligators, Alligator mississippiensis. Am Midl Nat 148:115–119

  32. Kislalioglu M, Gibson RN (1976) Prey “handling-time” and its importance in food selection by the 15-spined stickleback, Spinachi spinachia (L.). J Exp Mar Biol Ecol 25:151–158

  33. Knudsen R, Primicerio R, Amundsen P, Klemetsen A (2010) Temporal stability of individual feeding specialization may promote speciation. J Anim Ecol 79:161–168

  34. Layman C, Quattrochi JP, Peyer CM, Allgeier JE (2007) Niche width collapse in a resilient top predator following ecosystem fragmentation. Ecol Lett 10:937–944

  35. Matich P, Heithaus MR, Layman CA (2011) Contrasting patterns of individual specialization and trophic coupling in two marine apex predators. J Anim Ecol 80:294–305

  36. Mazzotti F, Brandt LA (1994) Ecology of the American alligator in a seasonally fluctuating environment. In: Davis D, Ogden J (eds) Everglades: the ecosystem and its restoration. St. Lucie Press, Delray Beach, pp 485–505

  37. Nifong J, Rosenblatt AE, Johnson NA, Barichivich W, Silliman BR, Heithaus MR (2012) American alligator digestion rate of blue crabs and its implications for stomach contents analysis. Copeia 2012:419–423

  38. Peterson B, Howarth RW (1987) Sulfur, carbon, and nitrogen isotopes used to trace organic matter flow in the salt-marsh estuaries of Sapelo Island, Georgia. Limnol Oceanogr 32:1195–1213

  39. Polidori C, Santoro D, Blüthgen N (2013) Does prey mobility affect niche width and individual specialization in hunting wasps? A network-based analysis. Oikos 122:385–394

  40. Polis G (1984) Age structure component of niche width and intraspecific resource partitioning: can age groups function as ecological species? Am Nat 123:541–564

  41. Quevedo M, Svanback R, Eklov P (2009) Intrapopulation niche partitioning in a generalist predator limits food web connectivity. Ecology 90:2263–2274

  42. Rice A, Ross JP, Finger AG, Owen R (2005) Application and evaluation of a stomach flushing technique for alligators. Herpetol Rev 36:400–401

  43. Rice A, Ross JP, Woodward AR, Carbonneau DA, Percival HF (2007) Alligator diet in relation to alligator mortality on Lake Griffin, FL. Southeast Nat 6:97–110

  44. Ripple W, Estes JA, Beschta RL, Wilmers CC, Ritchie EG, Hebblewhite M, Berger J, Elmhagen B, Letnic M, Nelson MP, Schmitz OJ, Smith DW, Wallach AD, Wirsing AJ (2014) Status and ecological effects of the world’s largest carnivores. Science 343:1241484

  45. Rooney N, McCann K, Gellner G, Moore JC (2006) Structural asymmetry and the stability of diverse food webs. Nature 442:265–269

  46. Rosenblatt A, Heithaus MR (2011) Does variation in movement tactics and trophic interactions among American alligators create habitat linkages? J Anim Ecol 80:786–798

  47. Rosenblatt A, Heithaus MR (2013) Slow isotope turnover rates and low discrimination values in the American alligator: implications for interpretation of ectotherm stable isotope data. Physiol Biochem Zool 86:137–148

  48. Rosenblatt A, Heithaus MR, Mazzotti FJ, Cherkiss M, Jeffery B (2013) Intra-population variation in activity ranges, diel patterns, movement rates, and habitat use of American alligators in a subtropical estuary. Estuar Coast Shelf Sci 135:182–190

  49. Roughgarden J (1972) Evolution of niche width. Am Nat 106:683–718

  50. Roughgarden J (1979) Theory of population genetics and evolutionary ecology: an introduction. Macmillan, New York

  51. Skulason S, Smith TB (1995) Resource polymorphisms in vertebrates. Trends Ecol Evol 10:366–370

  52. Temeles E, Pan IL, Brennan JL, Horwitt JN (2000) Evidence for ecological causation of sexual dimorphism in a hummingbird. Science 289:441–443

  53. Thiemann G, Iverson SJ, Stirling I, Obbard ME (2011) Individual patterns of prey selection and dietary specialization in an Arctic marine carnivore. Oikos 120:1469–1478

  54. Tinker M, Bentall G, Estes JA (2008) Food limitation leads to behavioral diversification and dietary specialization in sea otters. Proc Natl Acad Sci USA 105:560–565

  55. Woo K, Elliott KH, Davidson M, Gaston AJ, Davoren GK (2008) Individual specialization in diet by a generalist marine predator reflects specialization in foraging behaviour. J Anim Ecol 77:1082–1091

  56. Woodroffe R, Lindsey PA, Romanach SS, Ranah SMKO (2007) African wild dogs (Lycaon pictus) can subsist on small prey: implications for conservation. J Mammal 88:181–193

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Acknowledgments

We thank Michael Delany, Steven Gabrey, and Amanda Rice for generously allowing us to use their alligator stomach contents data. This research was made possible by funding from the National Science Foundation through the Florida Coastal Everglades Long-Term Ecological Research program under Grant No. DBI-0620409 and from the National Oceanic and Atmospheric Administration under Award No. NA10NOS4200022 (09102903). Additional funding was provided by Florida International University (FIU) and the University of Florida (UF). A.E.R. was supported by an FIU Dissertation Year Fellowship during manuscript preparation. All animal care and use was performed in accordance with the UF Institutional Animal Care and Use Committee (IACUC) under Protocol No. 201005071, the FIU IACUC under Protocol No. 09-015 and 09-013, and the Kennedy Space Center IACUC under Protocol No. GRD-06-044. All field collections were performed under FFWCC Scientific Collecting Permit No. SPGS-10-44R and SPGS-10-43, Georgia Department of Natural Resources Scientific Collecting Permit No. 29-WBH-10-33, and Everglades National Park Permit No. 0024, 0025, and 0031. We thank all the volunteers who assisted with field work and data collection, especially Phil Matich, Kirk Gastrich, Katy Cameron, Greg Mineau, and Derek Burkholder. Use of trade, product, or firm names does not imply endorsement by the U.S. Government or the authors. All work carried out in this study comply with the current laws of the USA.

Conflict of interest

We declare that we have no conflict of interest.

Author information

Correspondence to Adam E. Rosenblatt.

Additional information

Communicated by Craig A. Layman.

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Rosenblatt, A.E., Nifong, J.C., Heithaus, M.R. et al. Factors affecting individual foraging specialization and temporal diet stability across the range of a large “generalist” apex predator. Oecologia 178, 5–16 (2015). https://doi.org/10.1007/s00442-014-3201-6

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Keywords

  • American alligator
  • Alligator mississippiensis
  • Stomach content analysis
  • Stable isotope analysis
  • Food web