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Oecologia

, Volume 189, Issue 2, pp 395–406 | Cite as

Trophic declines and decadal-scale foraging segregation in three pelagic seabirds

  • Kaycee E. MorraEmail author
  • Yoshito Chikaraishi
  • Hasand Gandhi
  • Helen F. James
  • Sam Rossman
  • Anne E. Wiley
  • Andre F. Raine
  • Jessie Beck
  • Peggy H. Ostrom
Behavioral ecology –original research

Abstract

We investigated how foraging habits vary among three ecologically distinct wide-ranging seabirds. Using amino acid δ15N proxies for nutrient regime (δ15NPhe) and trophic position (Δδ15NGlu-Phe), we compared Newell’s shearwater (Puffinus newelli) and Laysan albatross (Phoebastria immutabilis) foraging habits over the past 50–100 years, respectively, to published records for the Hawaiian petrel (Pterodroma sandwichensis). Standard ellipses constructed from the isotope proxies show that inter-population and interspecific foraging segregation have persisted for several decades. We found no evidence of a shift in nutrient regime at the base of the food web for the three species. However, our data identify a trophic decline during the past century for Newell’s shearwater and Laysan albatross (probability ≥ 0.97), echoing a similar decline observed in the Hawaiian petrel. During this time, Newell’s shearwaters and Hawaiian petrels have experienced population declines and Laysan albatross has experienced range extension and apparent population stability. Counting other recent studies, a pattern of trophic decline over the past century has now been identified in eight species of pelagic seabirds that breed in the Hawaiian Islands. Because our study species forage broadly across the North Pacific Ocean and differ in morphological and behavioral traits and feeding methods, the identified trophic declines suggest a pervasive shift in food web architecture within the past century.

Keywords

Stable isotope Amino acid Trophic decline Foraging ecology Seabird 

Notes

Acknowledgements

We thank the Bird Division, National Museum of Natural History, the Bernice Bishop Museum, and the California Academy of Sciences for the loan of specimens and permission to sample them. We are grateful to the National Marine Fisheries Service, Alaska Fisheries Science Center, Pacific Islands Regional Office—Fisheries Observer Program staff and observers, the vessels and crew of the Hawaii longline fisheries that supported the observers, Oikonos and Shannon Fitzgerald, Bill Walker, and Hannah Nevins, in particular, for facilitating sampling of salvaged Laysan albatross. We acknowledge the Hawaii Department of Land and Natural Resources (Division of Forestry and Wildlife) and the Kaua`i Endangered Seabird Recovery Project for facilitating sampling of salvaged Newell’s shearwaters. Funding was generously provided by the National Science Foundation DEB 0,745,604, Michigan State University, and the Wetmore Fund of the Bird Division, Smithsonian Institution.

Author contribution statement

KEM, PHO, HFJ, and AEW formulated the idea. KEM, PHO, and SR wrote the manuscript. All authors engaged in intellectual exchange and manuscript editing. KEM, PHO, YC, and HG developed methodology and performed laboratory analyses. SR and KEM performed statistical analyses. AR and JB facilitated access to salvaged birds. KEM, AEW, HFJ, AR, and PHO collected samples.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

442_2018_4330_MOESM1_ESM.docx (32 kb)
Supplementary material 1 (DOCX 31 kb)

References

  1. Adams J, Flora S (2010) Correlating seabird movements with ocean winds: linking satellite telemetry with ocean scatterometry. Mar Biol 157:915–929CrossRefGoogle Scholar
  2. Ainley DG, Telfer TC, Reynolds MH (1997) Newell’s Shearwater (Puffinus newelli), version 2.0. In: Rodewald PG (ed) The Birds of North America. Cornell Lab of Ornithology, Ithaca, New YorkGoogle Scholar
  3. Ainley DG, Walker WA, Spencer GC, Holmes ND (2014) The prey of Newell’s shearwater Puffinus newelli in Hawaiian waters. Mar Ornithol 44:69–72Google Scholar
  4. Altabet M, Francois R (1994) Sedimentary nitrogen isotopic ratio as a recorder for surface ocean nitrate utilization. Glob Biogeochem Cycles 8:103–116CrossRefGoogle Scholar
  5. Arata JA, Sievert PR, Naughton MB (2009) Status assessment of Laysan and black-footed albatrosses, North Pacific Ocean, 1923–2005. US Geological Survey, Reston, Virginia, pp 2009–5131Google Scholar
  6. Awkerman JA, Anderson DJ, Whittow GC (2009) Laysan Albatross (Phoebastria immutabilis), version 2.0. In: Rodewald PG (ed) The birds of North America. Cornell Lab of Ornithology, Ithaca, New YorkGoogle Scholar
  7. Ballance LT, Ainley DG, Hunt GL Jr (2001) Seabird foraging ecology. In: Steele JH, Thorpe SA, Turekian KK (eds) Encyclopedia of ocean sciences, vol 5. Academic Press, London, pp 2636–2644CrossRefGoogle Scholar
  8. Bearhop S, Phillips RA, McGill R, Cherel Y, Dawson DA, Croxall JP (2006) Stable isotopes indicate sex-specific and long-term individual foraging specialization in diving seabirds. Mar Ecol Prog Ser 311:157–164CrossRefGoogle Scholar
  9. Bisson JR (2008) Diet dynamics and trophic relations of Laysan and black-footed albatrosses associated with pelagic longline fishing. MS thesis, University of Hawaii at Manoa, Hawaii, USAGoogle Scholar
  10. Block BA, Jonsen ID, Jorgensen SJ, Winship AJ, Shaffer SA, Bograd SJ, Hazen EL, Foley DG, Breed GA, Harrison AL, Ganong JE, Swithenbank A, Castleton M, Dewar H, Mate BR, Shillinger GL, Schaefer KM, Benson SR, Weise MJ, Henry RW, Costa DP (2011) Tracking apex marine predator movements in a dynamic ocean. Nature 475:86–90CrossRefPubMedGoogle Scholar
  11. Broughton JM (1994) Size of the bursa of Fabricius in relation to gonad size and age in Laysan and Black-footed Albatrosses. Condor 96:203–207CrossRefGoogle Scholar
  12. Casciotti KL, Trull TW, Glover DM, Davies D (2008) Constraints on nitrogen cycling at the subtropical North Pacific Station ALOHA from isotopic measurements of nitrate and particulate nitrogen. Deep Res Part II 55:1661–1672CrossRefGoogle Scholar
  13. Cheung WW, Meeuwig JJ, Feng M, Harvey E, Lam VW, Langlois T, Slawinski D, Sun C, Pauly D (2012) Climate-change induced tropicalisation of marine communities in Western Australia. Mar Freshw Res 63:415–427CrossRefGoogle Scholar
  14. Chikaraishi Y, Kashiyama Y, Ogawa NO, Kitazato H, Ohkouchi N (2007) Metabolic control of nitrogen isotope composition of amino acids in macroalgae and gastropods: implications for aquatic food web studies. Mar Ecol Prog Ser 342:85–90CrossRefGoogle Scholar
  15. Chikaraishi Y, Ogawa NO, Kashiyama Y, Takano Y, Suga H, Tomitani A, Miyashita H, Kitazato H, Ohkouchi N (2009) Determination of aquatic food- web structure based on compound-specific nitrogen isotopic composition of amino acids. Limnol Oceanogr 7:740–750CrossRefGoogle Scholar
  16. Choy CA (2013) Pelagic food web connectivity in the north Pacific subtropical gyre: a combined perspective from multiple biochemical tracers and diet. PhD dissertation, University of Hawaii at Manoa, Hawaii, USAGoogle Scholar
  17. Coe R (2002) It’s the effect size, stupid: What effect size is and why it is important. A paper presented at the Annual Conference of the British Educational Research Association, University of Exeter, Exeter, Devon, EnglandGoogle Scholar
  18. Conners MG, Goetsch C, Budge SM, Walker WA, Mitani Y, Costa DP, Shaffer SA (2018) Fisheries exploitation by albatross quantified with lipid analysis. Front Mar Sci. 5:113CrossRefGoogle Scholar
  19. Cooper BA, Day RH (1998) Summer behavior and mortality of dark-rumped Petrels and Newell’s Shearwaters at power lines on Kaua`i. Colon Waterbirds 21:11–19CrossRefGoogle Scholar
  20. Cousins KL, Dalzell P, Gilman E (2000) Managing pelagic longline-albatross interactions in the North Pacific Ocean. Marine Ornithol 28:159–174Google Scholar
  21. Deutsch C, Gruber N, Key RM, Sarmiento JL, Ganachaud A (2001) Denitrification and N2 fixation in the pacific ocean. Glob Biogeochem Cycles 15:483–506CrossRefGoogle Scholar
  22. Development Core Team R (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  23. Edwards AE, Rohwer S (2005) Large-scale patterns of molt activation in the flight feathers of two albatross species. Condor 107:835–848CrossRefGoogle Scholar
  24. Ellis G (2012) Compound-specific stable isotopic analysis of protein amino acids: ecological implications in modern and ancient systems. PhD dissertation, University of South Florida, Florida, USAGoogle Scholar
  25. Fernández P, Anderson DJ, Sievert PR, Huyvaert KP (2001) Foraging destinations of three low-latitude albatross (Phoebastria) species. J Zool 254:391–404CrossRefGoogle Scholar
  26. Gaebler OH, Choitz HC, Vitti TG, Vukmirovich R (1963) Significance of N15 excess in nitrogenous compounds of biological origin. Can J Biochem Physiol 41:1089–1097CrossRefPubMedGoogle Scholar
  27. Gagne TO, Hyrenbach KD, Hagemann ME, Van Houtan KS (2018) Trophic signatures of seabirds suggest shifts in oceanic ecosystems. Sci Adv 4:eaao3946CrossRefPubMedPubMedCentralGoogle Scholar
  28. Gelman A, Hill J (2007) Data analysis using regression and multilevel/hierarchical models. Cambridge University Press, New YorkGoogle Scholar
  29. Gelman A, Carlin JB, Stern HS, Rubin DB (2004) Bayesian data analysis: second edition. Texts in statistical science. CRC Press, Boca Raton. ISBN 1-58488-388-XGoogle Scholar
  30. Gould P, Ostrom P, Walker W (1997) Trophic relationships of albatrosses associated with squid and large-mesh drift-net fisheries in the North Pacific ocean. Can J Zool 75:549–562CrossRefGoogle Scholar
  31. 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 Science, Dordrecht, pp 299–318CrossRefGoogle Scholar
  32. Gruber N, Sarmiento JL (1997) Global patterns of marine nitrogen fixation and denitrification. Glob Biogeochem Cycles 11:235–266CrossRefGoogle Scholar
  33. Harrison CS, Hida TS, Seki MP (1983) Hawaiian seabird feeding ecology. Wildl Monogr 85:1–71Google Scholar
  34. Hinke JT, Polito MJ, Goebel ME, Jarvis S, Reiss CS, Thorrold SR, Trivelpiece WZ, Watters GM (2015) Spatial and isotopic niche partitioning during winter in chinstrap and Adélie penguins from the South Shetland Islands. Ecosphere 6:125CrossRefGoogle Scholar
  35. Hobson KA, Clark RG (1992) Assessing avian diets using stable isotopes I: turnover of 13C in tissues. Condor 94:181–188CrossRefGoogle Scholar
  36. Jackson JB (2008) Ecological extinction and evolution in the brave new ocean. Proc Natl Acad Sci 105:11458–11465CrossRefPubMedGoogle Scholar
  37. Jackson AL, Inger R, Parnell AC, Bearhop S (2011) Comparing isotopic niche widths among and within communities: SIBER—stable isotope bayesian ellipses in R. J Anim Ecol 80:595–602CrossRefPubMedGoogle Scholar
  38. Judge SW, Hu D, Bailey CN (2014) Comparative analyses of Hawaiian Petrel Pterodroma sandwichensis morphometrics. Marine Ornithol 42:81–84Google Scholar
  39. Karl D, Letelier R, Tupas L, Dore J, Christian J, Hebel D (1997) The role of nitrogen fixation in biogeochemical cycling in the subtropical North Pacific Ocean. Nature 388:533–538CrossRefGoogle Scholar
  40. Kays R, Crofoot MC, Jetz W, Wikelski M (2015) Terrestrial animal tracking as an eye on life and planet. Science 348:aaa2478CrossRefPubMedGoogle Scholar
  41. Kelleher K (2005) Discards in the world’s marine fisheries: an update. FAO Fisheries Technical Paper No. 470Google Scholar
  42. Kim IN, Lee K, Gruber N, Karl DM, Bullister JL, Yang S, Kim TW (2014) Increasing anthropogenic nitrogen in the North Pacific Ocean. Science 346:1102–1106CrossRefPubMedGoogle Scholar
  43. Kirch PV (1990) The evolution of sociopolitical complexity in prehistoric Hawaii: an assessment of the archaeological evidence. J World Prehist 4:311–345CrossRefGoogle Scholar
  44. Larsen T, Ventura M, Anderson N, O’Brien DM, Piatkowski U, McCarthy M (2013) Tracing carbon sources through aquatic and terrestrial food webs using amino acid stable isotope fingerprinting. PLoS One 8:e73441CrossRefPubMedPubMedCentralGoogle Scholar
  45. Lorrain A, Graham B, Ménard F, Popp B, Bouillon S, Van Breugel P, Cherel Y (2009) Nitrogen and carbon isotope values of individual amino acids: a tool to study foraging ecology of penguins in the Southern Ocean. Mar Ecol Prog Ser 391:293–306CrossRefGoogle Scholar
  46. McClelland JW, Montoya JP (2002) Trophic relationships and the nitrogen isotopic composition of amino acids in plankton. Ecology 83:2173–2180CrossRefGoogle Scholar
  47. McMahon KW, McCarthy MD (2016) Embracing variability in amino acid δ15N fractionation: mechanisms, implications, and applications for trophic ecology. Ecosphere 7:e01511CrossRefGoogle Scholar
  48. Mitchell C, Ogura C, Meadows DW, Kane A, Strommer L, Fretz S, Leonard D, McClung A (2005) Hawaii’s comprehensive wildlife conservation strategy. Department of Land and Natural Resources, HonoluluGoogle Scholar
  49. Myers RA, Worm B (2003) Rapid worldwide depletion of predatory fish communities. Nature 423:280–283CrossRefPubMedGoogle Scholar
  50. Myers RA, Baum JK, Shepherd TD, Powers SP, Peterson CH (2007) Cascading effects of the loss of apex predatory sharks from a coastal ocean. Science 315:1846–1850CrossRefPubMedGoogle Scholar
  51. Naughton MB, Romano MD, Zimmerman TS (2007) A conservation action plan for Black-footed Albatross (Phoebastria nigripes) and Laysan Albatross (P. immutabilis). Ver. 1.0Google Scholar
  52. Niethammer KR, Patrick LB (1998) White tern (Gygis alba), version 2.0. In: Poole AF, Gill FB (eds) The birds of North America. Cornell Lab of Ornithology, Ithaca, New YorkGoogle Scholar
  53. 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
  54. 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 284:20162436–20162442CrossRefPubMedGoogle Scholar
  55. Paleczny M, Hammill E, Karpouzi V, Pauly D (2015) Population trend of the world’s monitored seabirds, 1950–2010. PLoS One 10:e0129342CrossRefPubMedPubMedCentralGoogle Scholar
  56. Pitman RL, Walker WA, Everett WT, Gallo-Reynoso JP (2004) Population status, foods and foraging of Laysan albatrosses Phoebastria immutabilis nesting on Guadalupe Island, Mexico. Marine Ornithol 32:159–165Google Scholar
  57. Plummer M (2003) JAGS: a program for analysis of Bayesian graphical models using Gibbs Sampling. In: Hornik K, Leisch F, Zeileis A (eds) Proceedings of the third international workshop on distributed statistical computing. R Project for Statistical Computing, Technische Universität Wien, ViennaGoogle Scholar
  58. Polovina JJ, Woodworth-Jefcoats PA (2013) Fishery-induced changes in the subtropical Pacific pelagic ecosystem size structure: observations and theory. PLoS One 8:e62341CrossRefPubMedPubMedCentralGoogle Scholar
  59. 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
  60. Raine AF, Holmes ND, Travers M, Cooper BA, Day RH (2017) Declining population trends of Hawaiian petrel and Newell’s Shearwater on the island of Kaua`i, Hawaii, USA. Condor 119:405–415CrossRefGoogle Scholar
  61. 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 178:415–425CrossRefPubMedGoogle Scholar
  62. Rossman S, Ostrom PH, Gordon F, Zipkin EF (2016) Beyond carbon and nitrogen: guidelines for estimating three-dimensional isotopic niche space. Ecol and Evol 6:2405–2413CrossRefGoogle Scholar
  63. Rucklidge GJ, Milne G, McGaw BA, Milne E, Robins SP (1992) Turnover rates of different collagen types measured by isotope ratio mass spectrometry. Biochim Biophys Acta 1156:57–61CrossRefPubMedGoogle Scholar
  64. Schreiber RW (1984) Tropical seabird biology. Cooper Ornithological Society, KansasGoogle Scholar
  65. Schreiber EA, Burger J (2001) Biology of marine birds. CRC Press, FloridaCrossRefGoogle Scholar
  66. Schreiber EA, Norton RL (2002) Brown Booby (Sula leucogaster), version 2.0. In: Poole AF, Gill FB (eds) The birds of North America. Cornell Lab of Ornithology, Ithaca, New YorkGoogle Scholar
  67. Schreiber EA, Feare CJ, Harrington BA, Murray BA Jr., Robertson WB Jr., Robertson MJ, Woolfenden GE (2002) Sooty tern (Onychoprion fuscatus), version 2.0. In: Poole AF, Gill FB (eds) The birds of North America. Cornell Lab of Ornithology, Ithaca, New YorkGoogle Scholar
  68. Sherwood OA, Guilderson TP, Batista FC, Schiff JT, McCarthy MD (2014) Increasing subtropical North Pacific Ocean nitrogen fixation since the Little Ice Age. Nature 505:78–81CrossRefPubMedGoogle Scholar
  69. Sigman DM, Mccorkle DC, Francois R, Fischer G (2000) The δ15N of nitrate in the Southern Ocean: nitrogen cycling and circulation in the ocean interior. J Geophys Res 105:19599–19614CrossRefGoogle Scholar
  70. Simons TR (1985) Biology and behavior of the endangered Hawaiian dark-rumped petrel. Condor 87:229–245CrossRefGoogle Scholar
  71. Simons TR, Hodges CN (1998) Hawaiian Petrel (Pterodroma sandwichensis), version 2.0. In: Rodewald PG (ed) The birds of North America. Cornell Lab of Ornithology, Ithaca, New YorkGoogle Scholar
  72. Spear LB, Ainley DG, Nur N, Howell SNG (1995) Population size and factors affecting at-sea distributions of four endangered Procellariids in the tropical pacific. Condor 97:613–638CrossRefGoogle Scholar
  73. Stafford TW, Brendel K, Duhamel RC (1988) Radiocarbon, 13C and 15N analysis of fossil bone: removal of humates with XAD-2 resin. Geochim Chosmochim Acta 52:2257–2267CrossRefGoogle Scholar
  74. VanZandt ML (2012) Distribution and habitat selection of the endangered Hawaiian Petrel (Pterodroma sandwichensis), from the island of Lāna’i. PhD dissertation, University of Hawaii at Hilo, Hawaii, USAGoogle Scholar
  75. Ward P, Myers RA (2005) Shifts in open-ocean fish communities coinciding with the commencement of commercial fishing. Ecology 86:835–847CrossRefGoogle Scholar
  76. Warham J (1996) The behavior, population biology and physiology of the petrels. Academic Press, University of Canterbury, ChristchurchGoogle Scholar
  77. Whittow GC (1997) Wedge-tailed Shearwater (Ardenna pacifica), version 2.0. In: Poole AF, Gill FB (eds) The birds of North America Editors. Cornell Lab of Ornithology, Ithaca, New YorkGoogle Scholar
  78. Wiley AE, Welch AJ, Ostrom PH, James HF, Stricker CA, Fleischer RC, Gandhi H, Adams J, Ainley DG, Duvall F, Holmes N (2012) Foraging segregation and genetic divergence between geographically proximate colonies of a highly mobile seabird. Oecologia 168:119–130CrossRefPubMedGoogle Scholar
  79. Wiley AE, Ostrom PH, Welch AJ, Fleischer RC, Gandhi H, Southon JR, Stafford TR Jr, Penniman JR, 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 110:8972–8977CrossRefPubMedGoogle Scholar
  80. Woodworth-Jefcoats PA, Polovina JJ, Dunne JP, Blanchard JL (2013) Ecosystem size structure response to 21st century climate projection: large fish abundance decreases in the central North Pacific and increases in the California Current. Glob Chang Biol 19:724–733CrossRefPubMedGoogle Scholar
  81. Worm B, Lenihan HS (2013) Threats to marine ecosystems: overfishing and habitat degradation. In: Bertness MR, Silliman BJ, Stachowicz J (eds) Marine Community Ecology and Conservation, Chapter 20. Sinauer Press, Sunderlands, Massachusetts, pp 449–476Google Scholar

Copyright information

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

Authors and Affiliations

  1. 1.Department of Integrative BiologyMichigan State UniversityEast LansingUSA
  2. 2.Institute of Low Temperature ScienceHokkaido UniversitySapporoJapan
  3. 3.Japan Agency for Marine-Earth Science and TechnologyYokosukaJapan
  4. 4.Department of Vertebrate Zoology, National Museum of Natural HistorySmithsonian InstitutionWashingtonUSA
  5. 5.Hubbs-SeaWorld Research InstituteMelbourne BeachUSA
  6. 6.Department of BiologyUniversity of AkronAkronUSA
  7. 7.Kaua`i Endangered Seabird Recovery ProjectKauaiUSA
  8. 8.Oikonos Ecosystem KnowledgeSanta CruzUSA

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