Marine Biology

, Volume 159, Issue 4, pp 873–880 | Cite as

Stable isotope ratios of a tropical marine predator: confounding effects of nutritional status during growth

  • Larisa Lee CruzEmail author
  • Rona A. R. McGill
  • Simon J. Goodman
  • Keith C. Hamer
Original Paper


Stable isotope analysis of carbon and nitrogen is frequently used to study the diets and foraging ecology of marine predators. However, isotopic values may also be affected by an individual’s nutritional status and associated physiological processes. Here, we use C and N stable isotopes in blood and feathers of blue-footed booby chicks at the Galápagos Islands to examine how isotopic values are related to body condition and growth rate, and to assess the consistency in the isotope ratios of individuals during growth. Size dimorphism in blue-footed boobies provided an additional opportunity to examine how isotope ratios differ between sexes in relation to body size and growth rate. There was no significant difference between sexes but both C and N stable isotopes were significantly negatively related to the body condition of chicks. These data were consistent with individual variation in physiological processes affecting fractionation, although we cannot rule out the possibility that they were also influenced to some extent by population-level variation in the stable isotope ratios of prey fed to chicks, for instance related to prey size, depth or lipid content. Our results highlight the need for methods that take proper account of confounding physiological factors in isotopic studies of foraging ecology and diet.


Stable Isotope Body Condition Stable Isotope Analysis Stable Isotope Ratio Sexual Size Dimorphism 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We thank Marilyn Cruz, Pamela Martínez, Sarah-L. Smith, Alberto Vélez and Pablo Mejía for their help in the field, and Virna Cedeño, Washington Tapia, David Vizuete, Miton Mora, Efraín García and Nelson García for logistical support and advice. We thank Natalia Tirado from the Charles Darwin Research Station for help identifying prey species. Stable isotope analyses were carried out at SUERC, UK, and we particularly thank Jason Newton for his help. We also thank two anonymous reviewers for their comments on previous versions of this manuscript. This study was funded by Consejo Nacional de Ciencia y Tecnología, Mexico, and carried out in collaboration with the Galápagos National Park Service and the Galápagos Genetics, Epidemiology and Pathology Laboratory with support from the UK government (DEFRA Darwin Initiative Grants 162-12-17 and EDIPO 15).


  1. Anderson DJ (1989) Differential responses of boobies and other seabirds in the Galápagos to the 1986–87 El Niño southern oscillation event. Mar Ecol Prog Ser 52:209–216CrossRefGoogle Scholar
  2. Au DWK, Pitman RL (1986) Seabird interactions with dolphins and tuna in the Eastern Tropical Pacific. Condor 88:304–317CrossRefGoogle Scholar
  3. Aurioles-Gamboa D, Newsome SD, Salazar-Pico S, Koch PL (2009) Stable isotope differences between sea lions (Zalophus) from the Gulf of California and Galápagos Islands. J Mammal 90:1410–1420CrossRefGoogle Scholar
  4. Bearhop S, Teece MA, Waldron S, Furness RW (2000) Influence of Lipid and Uric Acid on δ13C and δ15N values of avian blood: implications for trophic studies. Auk 117:504–507CrossRefGoogle Scholar
  5. Bearhop S, Waldron S, Votier SC, Furness RW (2002) Factors that influence assimilation rates and fractionation of nitrogen and carbon stable isotopes in avian blood and feathers. Physiol Biochem Zool 75:451–458CrossRefGoogle Scholar
  6. Bearhop S, Phillips RA, McGill RAR, Cherel Y, Dawson DA, Croxall JP (2006) Stable isotopes indicate sex-specific and long-term individual foraging specialisation in diving seabirds. Mar Ecol Prog Ser 311:157–164. doi: 10.3354/meps311157 CrossRefGoogle Scholar
  7. Bermúdez-Humarán LG, García-García A, Leal-Garza CH, Riojas-Valdes VM, Jaramillo-Rangel G, Montes-de-Oca-Luna R (2002) Molecular sexing of monomorphic endangered Ara birds. J Exp Zool 292:677–680CrossRefGoogle Scholar
  8. Bihn JH, Gebauer G, Brandl R (2010) Loss of functional diversity of ant assemblages in secondary tropical forests. Ecology 91:782–792. doi: 10.1890/08-1276.1 CrossRefGoogle Scholar
  9. Blüthgen N, Gebauer G, Fiedler K (2003) Disentangling a rainforest food web using stable isotopes: dietary diversity in a species-rich ant community. Oecologia 137:426–435CrossRefGoogle Scholar
  10. Bode A, Carrera P, Lens S (2003) The pelagic foodweb in the upwelling ecosystem of Galicia (NW Spain) during spring: natural abundance of stable carbon and nitrogen isotopes. ICES J Mar Sci 60:11–22CrossRefGoogle Scholar
  11. Burger AE, Shaffer SA (2008) Application of tracking and data-logging technology in research and conservation of seabirds. Auk 125:253–264CrossRefGoogle Scholar
  12. Catry T, Ramos JA, Le Corre M, Kojadinovic J, Bustamante P (2008) The role of stable isotopes and mercury concentrations to describe seabird foraging ecology in tropical environments. Mar Biol 155:637–647CrossRefGoogle Scholar
  13. Cherel Y, Hobson KA, Bailleul F, Groscolas R (2005a) Nutrition, physiology, and stable isotopes: new information from fasting and moulting penguins. Ecology 86:2881–2888CrossRefGoogle Scholar
  14. Cherel Y, Hobson KA, Hassani S (2005b) Isotopic discrimination between food and blood and feathers of captive penguins: implications for dietary studies in the wild. Phys Biochem Zool 78:106–115CrossRefGoogle Scholar
  15. Cherel Y, Kernaleguen L, Richard P, Guinet C (2009) Whisker isotopic signature depicts migration patterns and multi-year intra- and inter-individual foraging strategies in fur seals. Biol Lett 5:830–832CrossRefGoogle Scholar
  16. Drummond H, Osorno JL, Torres R, García-Chavelas C, Merchant Larios H (1991) Sexual size dimorphism and sibling competition: implications for avian sex ratios. Am Nat 138:623–641CrossRefGoogle Scholar
  17. Ehrich D, Tarroux A, Stien J, Lecompte N, Killengreen S, Berteaux D, Yoccoz NG (2010) Stable isotope analysis: modelling lipid normalization for muscle and eggs from arctic mammals and birds. Methods Ecol Evol 2:66–76CrossRefGoogle Scholar
  18. Forero MG, Hobson KA (2003) Using stable isotopes of nitrogen and carbon to study seabird ecology: applications in the Mediterranean seabird community. Sci Marina 67(Suppl 2):23–32Google Scholar
  19. Forero MG, Tella K (2002) Conspecific food competition explains variability in colony size: a test in Magellanic penguins. Ecology 83:3466–3475CrossRefGoogle Scholar
  20. Forero MG, Hobson KA, Bortolotti GR, Donázar JA, Bertellotti M, Blanco G (2002) Food resource utilisation by the Magellanic penguin evaluated through stable-isotope analysis: segregation by sex and age and influence on offspring quality. Mar Ecol Prog Ser 234:289–299CrossRefGoogle Scholar
  21. Forero MG, González-Solís J, Hobson KA, Donázar JA, Bertellotti M, Blanco G, Bortolotti GR (2005) Stable isotopes reveal trophic segregation by sex and age in the southern giant petrel in two different food webs. Mar Ecol Prog Ser 296:107–113CrossRefGoogle Scholar
  22. Fridolfsson AK, Ellegren H (1999) A simple and universal method for molecular sexing of non-ratite birds. J Avian Biol 30:116–121CrossRefGoogle Scholar
  23. Gannes LZ, O’Brien DM, Martínez del Rio C (1997) Stable isotopes in animal ecology: assumptions, caveats, and a call for more laboratory experiments. Ecology 78:1271–1276. doi: 10.1890/0012-9658 CrossRefGoogle Scholar
  24. Hamer KC, Furness RW, Caldow RWG (1991) The effects of changes in food availability on the breeding ecology of Great Skuas Catharacta skua in Shetland. J Zool 223:175–188CrossRefGoogle Scholar
  25. Hobson KA, Clark RG (1992) Assessing avian diets using stable isotopes I: turnover of 13 C in tissues. Condor 94:181–188CrossRefGoogle Scholar
  26. Hobson KA, Alisauskas RT, Clark RG (1993) Stable-nitrogen isotope enrichment in avian tissues due to fasting and nutritional stress: implications for isotopic analyses of diet. Condor 95:388–394CrossRefGoogle Scholar
  27. Hobson KA, Piatt JF, Pitocchelli J (1994) Using stable isotopes to determine seabird trophic relationships. J Anim Ecol 63:786–798CrossRefGoogle Scholar
  28. Inger R, Bearhop S (2008) Applications of stable isotope analyses to avian ecology. Ibis 150:447–461CrossRefGoogle Scholar
  29. Kempster B, Zanette L, Longstaffe FJ, MacDougall-Shackleton SA, Wingfield JC, Clinchy M (2007) Do stable isotopes reflect nutritional stress? Results from a laboratory experiment on song sparrows. Oecologia 151:365–371CrossRefGoogle Scholar
  30. Layman CA, Winemiller KO, Arrington DA, Jepsen DB (2005) Body size and trophic position in a diverse tropical food web. Ecology 86:2530–2535CrossRefGoogle Scholar
  31. Magrath MJL, Van Lieshout E, Pen I, Visser GH, Komdeur J (2007) Estimating expenditure on male and female offspring in a sexually size-dimorphic bird: a comparison of different methods. J Anim Ecol 76:1169–1180CrossRefGoogle Scholar
  32. Martínez del Rio C, Wolf N, Carleton SA, Gannes LZ (2009) Isotopic ecology ten years after a call for more laboratory experiments. Biol Rev 84:91–111CrossRefGoogle Scholar
  33. Nelson JB (1978) The Sulidae: gannets and boobies. Oxford University Press, OxfordGoogle Scholar
  34. Owen JC, Sogge MK, Kern MD (2005) Habitat and sex differences in physiological condition of breeding Southwestern willow flycatchers (Empidonax trailli extimus). Auk 122:1261–1270CrossRefGoogle Scholar
  35. Papastamatiou YP, Friedlander AM, Caselle JE, Lowe CG (2010) Long-term movement patterns and trophic ecology of blacktip reef sharks (Carcharhinus melanopterus) at Palmyra Atoll. J Exp Mar Biol Ecol 386:94–102CrossRefGoogle Scholar
  36. Pearson SF, Levey DJ, Greenberg CH, Martínez del Rio C (2003) Effects of elemental composition on the incorporation of dietary nitrogen and carbon isotopic signatures in an omnivorous songbird. Oecologia 135:516–523Google Scholar
  37. Pecquerie L, Nisbet RM, Fablet R, Lorrain A, Kooijman SALM (2010) The impact of metabolism on stable isotope dynamics: a theoretical framework. Phil Trans R Soc B 365:3455–3468CrossRefGoogle Scholar
  38. Phillips D, Eldridge P (2006) Estimating the timing of diet shifts using stable isotopes. Oecologia 147:195–203CrossRefGoogle Scholar
  39. Phillips RA, Catry P, Silk JRD, Bearhop S, McGill RAR, Afanasyev V, Strange IJ (2007) Movements, winter distribution and activity patterns of Falkland and brown skuas: insights from loggers and isotopes. Mar Ecol Prog Ser 345:281–291. doi: 10.3354/meps06991 CrossRefGoogle Scholar
  40. Ponsard S, Averbuch P (1999) Should growing and adult animals fed on the same diet show different δ15N values? Rapid Commun Mass Spectrom 13:1305–1310CrossRefGoogle Scholar
  41. Post DM, Layman CA, Arrington DA, Takimoto G, Quattrochi J, Montaña CG (2007) Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analysis. Oecologia 152:179–189CrossRefGoogle Scholar
  42. Quillfeldt P, Bugoni L, McGill RAR, Masello JF, Furness RW (2008a) Differences in stable isotopes in blood and feathers of seabirds are consistent across species, age and latitude: implications for food web studies. Mar Biol 155:593–598CrossRefGoogle Scholar
  43. Quillfeldt P, McGill RAR, Masello JF, Weiss F, Strange IJ, Brickle P, Furness RW (2008b) Stable isotope analysis reveals sexual and environmental variability and individual consistency in foraging of thin-billed prions. Mar Ecol Prog Ser 373:137–148. doi: 10.3354/meps07751 CrossRefGoogle Scholar
  44. Quillfeldt P, Masello JF, McGill RAR, Adams M, Furness RW (2010) Moving polewards in winter: a recent change in the migratory strategy of a pelagic seabird? Front Zool 7:15CrossRefGoogle Scholar
  45. R Development Core Team (2008) R: a language, environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  46. Riou S, Hamer KC (2010) Lipid metabolism, begging behaviour and nestling obesity in a pelagic seabird. Funct Ecol 24:340–346CrossRefGoogle Scholar
  47. Sears J, Hatch SA, O’Brien DM (2009) Disentangling effects of growth and nutritional status on seabird stable isotope ratios. Oecologia 159:41–48CrossRefGoogle Scholar
  48. Sotiropoulos MA, Tonn WM, Wassenaar LI (2004) Effects of lipid extraction on stable carbon and nitrogen isotope analysis of fish tissues: potential consequences for food web studies. Ecol Freshw Fish 13:155–160CrossRefGoogle Scholar
  49. Torres R, Drummond H (1999) Does large size make daughters of the blue-footed booby more expensive than sons? J Anim Ecol 68:1133–1141CrossRefGoogle Scholar
  50. Trueman CN, McGill RAR, Guyard PH (2005) The effect of growth rate on tissue-diet isotopic spacing in rapidly growing animals. An experimental study with Atlantic salmon (Salmo salar). Rapid Commun Mass Spectrom 19:3239–3247CrossRefGoogle Scholar
  51. Velando A (2002) Experimental manipulation of maternal effort produces differential effects in sons and daughters: implications for adaptive sex ratios in the blue-footed booby. Behav Ecol 13:443–449CrossRefGoogle Scholar
  52. Votier SC, Bearhop S, Witt MJ, Inger R, Thompson D, Newton J (2010) Individual responses of seabirds to commercial fisheries revealed using GPS tracking, stable isotopes and vessel monitoring systems. J Appl Ecol 47:487–497CrossRefGoogle Scholar
  53. Weimerskirch H, Shaffer SA, Tremblay Y, Costa DP, Gadenne H, Kato A, Ropert-Coudert Y, Sato K, Aurioles D (2009) Species- and sex-specific differences in foraging behaviour and foraging zones in blue-footed and brown boobies in the Gulf of California. Mar Ecol Prog Ser 391:267–278CrossRefGoogle Scholar
  54. West JB, Bowen GJ, Cerling TE, Ehleringer JR (2006) Stable isotopes as one of nature’s ecological recorders. Trends Ecol Evol 21:408–414CrossRefGoogle Scholar
  55. Williams C, Buck C, Sears J, Kitaysky A (2007) Effects of nutritional restriction on nitrogen and carbon stable isotopes in growing seabirds. Oecologia 153:11–18CrossRefGoogle Scholar
  56. Wolf JBW, Harrod C, Brunner S, Salazar S, Trillmich F, Tautz D (2008) Tracing early stages of species differentiation: ecological, morphological and genetic divergence in Galapagos sea lion populations. BMC Evol Biol 8:150. doi: 10.1186/1471-2148-8-150 CrossRefGoogle Scholar
  57. Wolf N, Carleton SA, Martínez del Rio C (2009) Ten years of experimental animal isotopic ecology. Funct Ecol 23:17–26CrossRefGoogle Scholar
  58. Zavalaga CB, Benvenutti S, Dall’Antonia L, Emslie SD (2007) Diving behavior of the blue-footed boobies Sula nebouxii in northern Peru in relation to sex, body size and prey type. Mar Ecol Prog Ser 336:291–303CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Larisa Lee Cruz
    • 1
    Email author
  • Rona A. R. McGill
    • 2
  • Simon J. Goodman
    • 1
  • Keith C. Hamer
    • 1
  1. 1.Institute of Integrative and Comparative BiologyUniversity of LeedsLeedsUK
  2. 2.NERC Life Science Mass Spectrometry Facility, Scottish Universities Environmental Research CentreEast KilbrideUK

Personalised recommendations