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Marine Biology

, 166:39 | Cite as

From ecologically equivalent individuals to contrasting colonies: quantifying isotopic niche and individual foraging specialization in an endangered oceanic seabird

  • Anne E. WileyEmail author
  • Sam Rossman
  • Peggy H. Ostrom
  • Christine A. M. France
  • Jay Penniman
  • Cathleen Bailey
  • Fern Duvall
  • Elise F. Zipkin
  • Helen F. James
Original paper

Abstract

Quantifying individual specialization and other forms of intraspecific ecological diversity can reveal variation that is critical for evolutionary or behavioral adaption of a species to changing environments. Here, the isotopic niche and degree of individual foraging specialization were quantified for an endangered seabird, the Hawaiian petrel (Pterodroma sandwichensis), nesting on Lānaʻi (20°48′N, 156°52′W) and 72 km away on Haleakalā, Maui (20°42′N, 156°15′W; 20° 43′N, 156°14′W) between 2006 and 2011. Stable isotope values (δ13C and δ15N) from sequentially grown flight feathers provided time-series data that reflect the foraging habitat (relative latitude, nutrient regime of foraging location) and diet (trophic level) of individual birds across the period of molt. The two colonies differed in mean δ15N and δ13C throughout the period of molt, total nitrogen isotopic niche width, and extent of individual specialization with regard to δ15N. It is likely that petrels from Lānaʻi and Haleakalā use different feeding locations during the non-breeding season, when they are no longer tied to closely spaced breeding colonies. The loss of either colony could result in a substantial, long-term reduction in ecological diversity of the species (and perhaps, in adaptability). In contrast, comparisons of measured versus null specialization indices strongly suggest that both Lānaʻi and Haleakalā populations consist of individual generalists. Individual generalization with regard to foraging habitat and diet is here predicted to be common among tropical and subtropical oceanic seabirds. Such generalization could facilitate rapid, population-level responses of seabird species to marine environmental change via individual plasticity.

Notes

Acknowledgements

We thank the Bird Division, National Museum of Natural History, for access to and assistance with specimens. We also thank Haleakalā National Park and the Hawaii Department of Land and Natural Resources (Division of Forestry and Wildlife) for facilitating sampling of salvaged Hawaiian petrels. Funding was provided through Peter Buck and Stable Isotope Postdoctoral Fellowships from the Smithsonian Institution.

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.

Ethical approval

All applicable international, national, and institutional guidelines for the care and use of animals were followed. Salvaged seabird carcasses were collected under the Endangered Species Act permit TE-145562 and the cooperative agreement between the Hawaii Department of Land and Natural Resources and the US Fish and Wildlife Service. Funding was provided by National Museum of Natural History, Smithsonian Institution.

Supplementary material

227_2019_3483_MOESM1_ESM.pdf (257 kb)
Electronic Supplementary Material 1. Stable isotope data, information regarding the date of death for Hawaiian petrels in this study, and graphical depiction of stable nitrogen isotope data by year
227_2019_3483_MOESM2_ESM.r (31 kb)
Electronic Supplementary Material 2. Data, statistical modeling and processing file. The R script contains all data, model files, and code to run our model for the LANAI AND HALA. colonies provided JAGS and the appropriate R packages are installed

References

  1. Adams J, Flora S (2009) Correlating seabird movements with ocean winds: linking satellite telemetry with ocean scatterometry. Mar Biol 157:915–929CrossRefGoogle Scholar
  2. Altabet M, Francois R (1994) Sedimentary nitrogen isotopic ratio as a recorder for surface ocean nitrate utilization. Glob Biogeochem Cycles 8:103–116CrossRefGoogle Scholar
  3. Araújo MS, Bolnick DI, Layman CA (2011) The ecological causes of individual specialisation. Ecol Lett 14:948–958CrossRefGoogle Scholar
  4. Bolnick DI, Yang LH, Fordyce JA, Davis JM, Svanbäck R (2002) Measuring individual-level resource specialization. Ecol 83:2936–2941CrossRefGoogle Scholar
  5. Bolnick DI, Svanbäck R, Fordyce JA, Yang LH, Davis JM, Hulsey CD, Forister ML (2003) The ecology of individuals: incidence and implications of individual specialization. Am Nat 161:1–28CrossRefGoogle Scholar
  6. Bolnick DI, Amarasekare P, Levine JM, Novak M, Rudolf VHW, Schreiber SJ, Urban MC, Vasseur DA (2011) Why intraspecific trait variation matters in community ecology. Trends Ecol Evol 26:183–192CrossRefGoogle Scholar
  7. Bond AL, Jardine TD, Hobson KA (2016) Multi-tissue stable-isotope analyses can identify dietary specialization. Methods Ecol Evol 7:1428–1437CrossRefGoogle Scholar
  8. Bonnet-Lebrun AS, Phillips RA, Manica A, Rodrigues ASL (2018) Quantifying individual specialization using tracking data: a case study on two species of albatrosses. Mar Biol 165:152CrossRefGoogle Scholar
  9. Ceia FR, Ramos JA (2015) Individual specialization in the foraging and feeding strategies of seabirds: a review. Mar Biol 162:1923–1938CrossRefGoogle Scholar
  10. Cherel Y, Quillfeldt P, Delord K, Weimerskirch H (2016) Combination of at-sea activity, geolocation and feather stable isotopes documents where and when seabirds molt. Front Ecol Evol 4:3CrossRefGoogle Scholar
  11. Crandall KA, Bininda-emonds ORP, Mace GM, Wayne RK (2000) Considering evolutionary processes in conservation biology. Trends Ecol Evol 15:290–295CrossRefGoogle Scholar
  12. Croxall JP, Butchart SHM, Lascelles B, Stattersfield AJ, Sullivan B, Symes A, Taylor P (2012) Seabird conservation status, threats and priority actions: a global assessment. Bird Conserv Int 22:1–34CrossRefGoogle Scholar
  13. Cunningham GB, Nevitt GA (2011) Evidence for olfactory learning in procellariiform seabird chicks. J Avian Biol 42:85–88CrossRefGoogle Scholar
  14. Darimont CT, Paquet PC, Reimchen TE (2009) Landscape heterogeneity and marine subsidy generate extensive intrapopulation niche diversity in a large terrestrial vertebrate. J Anim Ecol 78:126–133CrossRefGoogle Scholar
  15. Development Core Team R (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  16. Farrell JW, Pedersen TF, Calvert SE, Nielsen B (1995) Glacial-interglacial changes in nutrient utilization in the equatorial Pacific Ocean. Nature 3:514–517CrossRefGoogle Scholar
  17. Gagne TO, Hyrenbach KD, Hagemann ME, Van Houtan KS (2018) Trophic signatures of seabirds suggest shifts in oceanic ecosystems. Sci Adv 4:eaao3946CrossRefGoogle Scholar
  18. Gelman A, Hill J (2007) Data analysis using regression and multilevel/hierarchical models. Cambridge University Press, New YorkGoogle Scholar
  19. Goericke R, Fry B (1994) Variation of marine plankton δ13C with latitude, temperature, and dissolved CO2 in the world ocean. Glob Biogeochem Cycles 8:85–90CrossRefGoogle Scholar
  20. González-Suárez M, Revilla Eloy (2013) Variability in life-history and ecological traits is a buffer against extinction in mammals. Ecol Lett 16:242–251CrossRefGoogle Scholar
  21. Graham BS, Koch PL, Newsome SD, McMahon KW, Aurioles D (2010) Using isoscapes to trace the movements and foraging behavior of top predators in oceanic ecosystems. In: West JB, Bowen GJ, Dawson TE, Tu KP (eds) Isoscapes: understanding movement, pattern, and process on earth through isotope mapping. Springer, Dordrecht, Heidelberg, London, New York, pp 299–318CrossRefGoogle Scholar
  22. Hobson KA, Bairlein F (2003) Isotopic fractionation and turnover in captive Garden Warblers (Sylvia borin): implications for delineating dietary and migratory associations in wild passerines. Can J Zool 81:1630–1635CrossRefGoogle Scholar
  23. Hobson KA, Clark RG (1992) Assessing avian diets using stable isotopes I: turnover of 13C in tissues. Condor 1:181–188CrossRefGoogle Scholar
  24. Hückstädt LA, Koch PL, McDonald BI, Goebel ME, Crocker DE, Costa DP (2012) Stable isotope analyses reveal individual variability in the trophic ecology of a top marine predator, the southern elephant seal. Oecologia 169:395–406CrossRefGoogle Scholar
  25. Jaeger A, Connan M, Richard P, Cherel Y (2010) Use of stable isotopes to quantify seasonal changes of trophic niche and levels of population and individual specialisation in seabirds. Mar Ecol Prog Ser 401:269–277CrossRefGoogle Scholar
  26. Kelly JF (2000) Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology. Can J Zool 78:1–27CrossRefGoogle Scholar
  27. Langston NE, Rohwer S (1996) Molt-breeding tradeoffs in albatrosses: life history implications for big birds. Oikos 76:498–510CrossRefGoogle Scholar
  28. Morra KE, Wiley AE, James HF, Dutcher A, Ostrom PH (2018) Influence of feather selection and sampling protocol on interpretations of Hawaiian Petrel (Pterodroma sandwichensis) nonbreeding season foraging habits from stable isotope analysis. Waterbirds 41:93–100CrossRefGoogle Scholar
  29. Morra KE, Chikaraishi Y, Gandhi H, James HF, Rossman S, Wiley AE, Raine AF, Beck J, Ostrom PH (2019) Trophic declines and decadal-scale foraging segregation in three pelagic seabirds. Oecologia.  https://doi.org/10.1007/s00442018043308 CrossRefPubMedGoogle Scholar
  30. Nevitt GA (2008) Sensory ecology on the high seas: the odor world of the procellariiform seabirds. J Exp Biol 211:1706–1713CrossRefGoogle Scholar
  31. Newsome SD, Tinker MT, Monson DH, Oftedal OT, Ralls K, Staedler MM, Fogel ML, Estes JA (2009) Using stable isotopes to investigate individual diet specialization in California sea otters (Enhydra lutris nereis). Ecology 90:961–974CrossRefGoogle Scholar
  32. Newsome SD, Tinker MT, Gill VA, Hoyt ZN, Doroff A, Nichol L, Bodkin JL (2015) The interaction of intraspecific competition and habitat on individual diet specialization: a near range-wide examination of sea otters. Oecologia 178:45–59CrossRefGoogle Scholar
  33. Ohkouchi N, Chikaraishi Y, Close HG, Fry B, Larsen T, Madigan DJ, McCarthy MD, McMahon KW, Nagata T, Naito YI, Ogawa NO, Popp BN, Steffan S, Takano Y, Tayasu I, Wyatt ASJ, Yamaguchi YT, Yokoyama Y (2017) Advances in the application of amino acid nitrogen isotopic analysis in ecological and biogeochemical studies. Org Geochem 113:150–174CrossRefGoogle Scholar
  34. Ostrom PH, Wiley AE, Rossman S, Stricker CA, James HF (2014) Unexpected hydrogen isotope variation in oceanic pelagic seabirds. Oecologia 175:1227–1235CrossRefGoogle Scholar
  35. Ostrom PH, Wiley AE, James HF, Rossman S, Walker WA, Zipkin EF, Chikaraishi Y (2017) Broad-scale trophic shift in the pelagic North Pacific revealed by an oceanic seabird. Proc R Soc B Biol Sci 284:20162436CrossRefGoogle Scholar
  36. Paleczny M, Hammill E, Karpouzi V, Pauly D (2015) Population trend of the world’s monitored seabirds, 1950–2010. PLoS One 10:e0129342CrossRefGoogle Scholar
  37. Phillips RA, Lewis S, González-solís J, Daunt F (2017) Causes and consequences of individual variability and specialization in foraging and migration strategies of seabirds. Mar Ecol Prog Ser 578:117–150CrossRefGoogle Scholar
  38. Pitman RL (1982) Distribution and foraging habits of the Dark-rumped Petrel (Pterodroma phaeopygia) in the eastern tropical Pacific. Bull Pac Seab Gr 9:72Google Scholar
  39. Plummer M (2003) JAGS: a program for analysis of Bayesian graphical models using Gibbs Sampling. In: Proceedings of the third international workshop on distributed statistical computing. R Project for Statistical Computing, Vienna, AustriaGoogle Scholar
  40. Pontón-Cevallos J, Dwyer RG, Franklin CE, Bunce A, Dwyer RG, Franklin CE, Bunce A (2017) Understanding resource partitioning in sympatric seabirds living in tropical marine environments. Austral Ornithol 117:31–39Google Scholar
  41. Provencher JF, Elliott KH, Gaston AJ, Braune BM (2013) Networks of prey specialization in an Arctic monomorphic seabird. J Avian Biol 44:551–560CrossRefGoogle Scholar
  42. Pyle P (2008) Molt and age determination in Procellariiformes. Identification guide to North American Birds, part 2. Slate Creek Press, Point Reyes Station, pp 248–260Google Scholar
  43. Pyle P, Webster DL, Baird RW (2011) Notes on petrels of the Dark-rumped Petrel complex (Pterodroma phaeopygia/sandwichensis) in Hawaiian waters. North Am Birds 65:364–367Google Scholar
  44. Quillfeldt P, Voigt CC, Masello JF (2010) Plasticity versus repeatability in seabird migratory behaviour. Behav Ecol Sociobiol 64:1157–1164CrossRefGoogle Scholar
  45. Rossman S, Ostrom PH, Stolen M, Barros NB, Gandhi H, Stricker CA, Wells RS (2015) Individual specialization in the foraging habits of female bottlenose dolphins living in a trophically diverse and habitat rich estuary. Oecologia 178:415–425CrossRefGoogle Scholar
  46. Roughgarden J (1972) Evolution of Niche Width. Am Nat 106:683–718CrossRefGoogle Scholar
  47. Semmens BX, Ward EJ, Moore JW, Darimont CT (2009) Quantifying inter-and intra-population niche variability using hierarchical bayesian stable isotope mixing models. PLoS One 4:e6187CrossRefGoogle Scholar
  48. Simons TR (1984) A population model of the endangered Hawaiian Dark-rumped Petrel. J Wildl Manag 48:1065–1076CrossRefGoogle Scholar
  49. Simons TR (1985) Biology and behavior of the endangered Hawaiian Dark-rumped Petrel. Condor 87:229–245CrossRefGoogle Scholar
  50. Simons TR, Hodges CN (1998) Dark-rumped Petrel (Pterodroma phaeopygia). Birds N Am 345:24Google Scholar
  51. Spear LB, Ainley DG, Nur N, Howell SNG, Condor T, Aug N, Howell NG, Reyes P, Observatory B, Beach S (1995) population size and factors affecting at-sea distributions of four endangered procellariids in the tropical Pacific. Condor 97:613–638CrossRefGoogle Scholar
  52. Svanbäck R, Bolnick DI (2005) Intraspecific competition affects the strength of individual specialization: an optimal diet theory method. Evol Ecol Res 7:993–1012Google Scholar
  53. Vander Zanden HB, Bjorndal KA, Reich KJ, Bolten AB (2010) Individual specialists in a generalist population: results from a long-term stable isotope series. Biol Lett 6:711–714CrossRefGoogle Scholar
  54. Vander Zanden HB, Bjorndal KA, Bolten AB (2013) Temporal consistency and individual specialization in resource use by green turtles in successive life stages. Oecologia 173:767–777CrossRefGoogle Scholar
  55. VanZandt MLA (2012) Distribution and habitat selection of the endangered Hawaiian Petrel (Pterodroma sandwichensis), from the Island of Lana’i. Dissertation, University of Hawai’i at HiloGoogle Scholar
  56. Warham J (1996) The behaviour, population biology and physiology of the petrels. Academic Press, LondonGoogle Scholar
  57. Weimerskirch H (2007) Are seabirds foraging for unpredictable resources? Deep Sea Res Part II Top Stud Oceanogr 54:211–223CrossRefGoogle Scholar
  58. Weimerskirch H, Le Corre M, Jaquemet S, Marsac F (2005) Foraging strategy of a tropical seabird, the red-footed booby, in a dynamic marine environment. Marine Ecol Prog Ser 288:251–261CrossRefGoogle Scholar
  59. Welch AJ, Fleischer RC, James HF, Wiley AE, Ostrom PH, Adams J, Duvall F, Holmes N, Hu D, Penniman J, Swindle KA (2012) Population divergence and gene flow in an endangered and highly mobile seabird. Heredity (Edinb) 109:19–28CrossRefGoogle Scholar
  60. Wiley AE, Ostrom PH, Stricker CA, James HF, Gandhi H (2010) Isotopic characterization of flight feathers in two pelagic seabirds: sampling strategies for ecological studies. Condor 112:337–346CrossRefGoogle Scholar
  61. Wiley AE, Welch AJ, Ostrom PH, James HF, Stricker CA, Fleischer RC, Gandhi H, Adams J, Ainley DG, Duvall F, Holmes N, Hu D, Judge S, Penniman J, Swindle KA (2012) Foraging segregation and genetic divergence between geographically proximate colonies of a highly mobile seabird. Oecologia 168:119–130CrossRefGoogle Scholar
  62. Wiley AE, Ostrom PH, Welch AJ, Fleischer RC, Gandhi H, Southon JR, Stafford TW, Penniman JF, Hu D, Duvall FP, James HF (2013) Millennial-scale isotope records from a wide-ranging predator show evidence of recent human impact to oceanic food webs. Proc Natl Acad Sci USA 110:8972–8977CrossRefGoogle Scholar
  63. Wiley AE, James HF, Ostrom PH (2017) Emerging techniques for isotope studies of avian ecology: emerging frontiers in collections-based ornithological research. Studies in avian biology (no. 50). In: Webster MS (ed) The extended specimen. CRC Press, Boca Raton, pp 89–109Google Scholar
  64. Woo KJ, 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 77:1082–1091CrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  • Anne E. Wiley
    • 1
    • 8
    Email author
  • Sam Rossman
    • 2
    • 3
  • Peggy H. Ostrom
    • 3
  • Christine A. M. France
    • 4
  • Jay Penniman
    • 5
  • Cathleen Bailey
    • 6
  • Fern Duvall
    • 7
  • Elise F. Zipkin
    • 3
  • Helen F. James
    • 8
  1. 1.Department of BiologyUniversity of Akron, Auburn Science CenterAkronUSA
  2. 2.Hubbs-Sea World Research InstituteMelbourne BeachUSA
  3. 3.Department of Integrative BiologyMichigan State UniversityEast LansingUSA
  4. 4.Museum Conservation Institute, Smithsonian InstitutionSuitlandUSA
  5. 5.Pacific Cooperative Studies Unit, Maui Nui Seabird Recovery ProjectUniversity of HawaiiHaikuUSA
  6. 6.MakawaoUSA
  7. 7.Division of Forestry and Wildlife, Department of Land and Natural ResourcesWailukuUSA
  8. 8.Department of Vertebrate Zoology, National Museum of Natural HistorySmithsonian InstitutionWashingtonUSA

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