Abstract
When using stable isotopes as dietary tracers it is essential to consider effects of nutritional state on isotopic fractionation. While starvation is known to induce enrichment of 15N in body tissues, effects of moderate food restriction on isotope signatures have rarely been tested. We conducted two experiments to investigate effects of a 50–55% reduction in food intake on δ15N and δ13C values in blood cells and whole blood of tufted puffin chicks, a species that exhibits a variety of adaptive responses to nutritional deficits. We found that blood from puffin chicks fed ad libitum became enriched in 15N and 13C compared to food-restricted chicks. Our results show that 15N enrichment is not always associated with food deprivation and argue effects of growth on diet–tissue fractionation of nitrogen stable isotopes (Δ15N) need to be considered in stable isotope studies. The decrease in δ13C of whole blood and blood cells in restricted birds is likely due to incorporation of carbon from 13C-depleted lipids into proteins. Effects of nutritional restriction on δ15N and δ13C values were relatively small in both experiments (δ15N: 0.77 and 0.41‰, δ13C: 0.20 and 0.25‰) compared to effects of ecological processes, indicating physiological effects do not preclude the use of carbon and nitrogen stable isotopes in studies of seabird ecology. Nevertheless, our results demonstrate that physiological processes affect nitrogen and carbon stable isotopes in growing birds and we caution isotope ecologists to consider these effects to avoid drawing spurious conclusions.
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Alonso-Alvarez C, Ferrer M (2001) A biochemical study of fasting, subfeeding, and recovery processes in yellow-legged gulls. Physiol Biochem Zool 74:703–713
Ambrose SH, Norr L (1993) Carbon isotopic evidence for routing of dietary protein to bone collagen, and whole diet to bone apatite carbonate: purified diet growth experiments. In: Lambert J, Grupe G (eds) Molecular archeology of prehistoric human bone. Springer, Berlin, pp 1–37
Ben-David M, McColl CJ, Boonstra R, Karels TJ (1999) 15N signatures do not reflect body condition in arctic ground squirrels. Can J Zool 77:1373–1378
Cherel Y, Hobson KA, Bailleul F, Groscolas R (2005a) Nutrition, physiology, and stable isotopes: new information from fasting and molting penguins. Ecology 86:2881–2888
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. Physiol Biochem Zool 78:106–115
Cherel Y, Phillips RA, Hobson KA, McGill R (2006) Stable isotope evidence of diverse species-specific and individual wintering strategies in seabirds. Biol Lett 2:301–303
DeNiro MJ, Epstein S (1977) Mechanism of carbon isotope fractionation associated with lipid synthesis. Science 197:182–191
Forero MG, Bortolotti GR, Hobson KA, Donazar JA, Bertelloti M, Guillermo B (2004) High trophic overlap within the seabird community of Argentinean Patagonia: a multiscale approach. J Anim Ecol 73:789–801
Frazer TK, Ross RM, Quetin LB, Montoya JP (1997) Turnover of carbon and nitrogen during growth of larval krill, Euphausia suberba Dana: a stable isotope approach. J Exp Mar Biol Ecol 212:259–275
Gannes LZ, O’Brien DM, Martinez del Rio C (1997) Stable isotopes in animal ecology: assumptions, caveats, and a call for more laboratory experiments. Ecology 78:1271–1276
Gannes LZ, Martinez del Rio C, Koch P (1998) Natural abundance variations in stable isotopes and their potential uses in animal physiological ecology. Comp Biochem Physiol 119:725–737
Gjerdrum C (2001) Nestling growth and parental provisioning of tufted puffins (Fratercula cirrhata) on triangle island, British Columbia. M.Sc. Thesis. Simon Fraser University, Burnaby
Gjerdrum C, Vallee AMJ, Cassady St. Clair C, Bertram DF, Ryder JL, Blackburn GS (2003) Tufted puffin reproduction reveals ocean climate variability. Proc Natl Acad Sci 100:9377–9382
Hatch KA, Sacksteder KA, Treichel IW, Cook MA, Porter WP (1995) Early detection of catabolic state via change in 13C/12C ratios of blood proteins. Biochem Biophys Res Commun 212:719–726
Hobson KA (1999) Tracing origins and migration of wildlife using stable isotopes: a review. Oecologia 120:314–326
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 95:388–394
Hobson KA, Clark RG (1993) Turnover of d13C in cellular and plasma fractions of blood: implications for non-destructive sampling in avian dietary studies. Auk 110:638–641
Hobson KA, Piatt JF, Pitocchelli J (1994) Using stable isotopes to determine seabird trophic relationships. J Anim Ecol 63:786–798
Hobson KA, Welch HE (1992) Determination of trophic relationships within a high arctic marine food web using δ13C and δ15N analysis. Mar Ecol Prog Ser 84:9–18
Kelly JF (2000) Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology. Can J Zool 78:1–27
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 151:365–371
King JR, Murphy ME (1985) Periods of nutritional stress in the annual cycle of endotherms: fact or fiction? Am Zool 25:955–964
Kitaysky AS (1999) Metabolic and developmental responses of alcid chicks to experimental variation in food intake. Physiol Biochem Zool 72:462–473
Kitaysky AS, Kitaiskaia EV, Wingfield JC, Piatt JF (2001) Dietary restriction causes chronic elevation of corticosterone and enhances stress response in red-legged kittiwake chicks. J Comp Physiol B 171:701–709
Kitaysky AS, Romano MD, Piatt JF, Wingfield JC, Kikuchi M (2005) The adrenocortical response of tufted puffin chicks to nutritional deficits. Horm Behav 47:606–619
Klasing KC (1998) Comparative avian nutrition. CAB International, Wallingford, UK
Littell RC, Henry PR, Ammerman CB (1998) Statistical analysis of repeated measures data using SAS procedures. J Anim Sci 76:1216–1231
Macko SA, Fogel Estep ML, Engel MH, Hare PE (1986) Kinetic fractionation of stable nitrogen isotopes during amino acid transamination. Geochim Cosmochim Acta 50:2143–2146
Martinez del Rio C, Wolf BO (2005) Mass-balance models for animal isotopic ecology. In: Starck JM, Wang T (eds) Physiological and ecological adaptations to feeding in vertebrates. Science Publishers, Enfield, NH, pp 141–174
Minigawa M, Wada E (1984) Stepwise enrichment of δ15N along food chains: further evidence and the relationship between δ15N and animal age. Geochim Cosmochim Acta 48:1135–1140
Niizuma Y, Araki Y, Mori H, Takahashi A, Watanuki Y (2002) Responses of body components to changes in the energetic demand throughout the breeding stages of rhinoceros auklets. Can J Zool 80:1549–1555
Nunez-de la Mora A, Drummond H, Wingfield JC (1996) Hormonal correlates of dominance and starvation-induced aggression in chicks of the blue-footed booby. Ethology 102:748–761
Oelbermann K, Scheu S (2002) Stable isotope enrichment (δ15N and δ13C) in a generalist predator (Pardosa lugubris, Aranea: Lycosidae): effects of prey quality. Oecologia 130:337–344
Pearson SF, Levey DJ, Greenberg CH, Martinez del Rio C (2003) Effects of elemental composition on the incorporation of dietary nitrogen and carbon isotopic signatures in an omnivorous songbird. Oecologia 135:516–523
Piatt JF, Kitaysky AS (2002) Tufted Puffin (Fratercula cirrhata). In: Poole A, Gill F (eds) The birds of North America, vol 708. The Birds of North America Inc., Philadelphia, PA, pp 1–31
Podlesack DW, McWilliams SR (2006) Metabolic routing of dietary nutrients in birds: effects of diet quality and macronutrient composition revealed using stable isotopes. Physiol Biochem Zool 79:534–549
Schmidt O, Scrimgeour CM, Curry JP (1999) Carbon and nitrogen stable isotope ratios in body tissue and mucus of feeding and fasting earthworms (Lumbricus festivus). Oecologia 118:9–15
Thompson DR, Phillips RA, Stewart FM, Waldron S (2000) Low δ13C signatures in pelagic seabirds: lipid ingestion as a potential source of 13C-depleted carbon in the Procellariiforms. Mar Ecol Prog Ser 208:265–271
Voigt CC, Matt F (2004) Nitrogen stress causes unpredictable enrichments of 15N in two nectar-feeding bat species. J Exp Biol 207:1741–1748
Votier SC, Bearhop S, MacCormick A, Ratcliffe N, Furness RW (2003) Assesing the diet of great skuas, Catharacta skua, using five different techniques. Polar Biol 26:20–26
Wilson RP, La Cock GD, Wilson MP, Mollagee F (1985) Differential digestion of fish and squid in jackass penguins, Spheniscus demersus. Ornis Scand 16:77–79
Acknowledgments
Funding was provided by NOAA/NMFS (NA16FX1270) to CLB, by NPRB to CLB and CTW, by EVOS Trustees Council and NPRB to ASK, and by fellowships from AK EPSCoR to CTW and JS. We thank Rachael Orben, Travis Cooper, John Brewer, and Erin Whidden for assistance with feeding experiments and lab work and two anonymous reviewers for helpful comments. All procedures were approved by Institutional Animal Care and Use Committees at the University of Washington (IACUC #2212-26) and University of Alaska Fairbanks (#05-43) and authorized under state and federal permits.
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Communicated by Carlos Martinez del Rio.
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Williams, C.T., Buck, C.L., Sears, J. et al. Effects of nutritional restriction on nitrogen and carbon stable isotopes in growing seabirds. Oecologia 153, 11–18 (2007). https://doi.org/10.1007/s00442-007-0717-z
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DOI: https://doi.org/10.1007/s00442-007-0717-z