Metabolic Routing of Dietary Nutrients in Birds: Effects of Diet Quality and Macronutrient Composition Revealed Using Stable Isotopes

During fall migration many songbirds switch from consuming primarily insects to consuming mostly fruit. Fruits with more carbohydrates and less protein may be sufficient to rebuild expended fat stores, but such fruits may be inadequate to replace catabolized protein. We manipulated the concentrations and isotopic signatures of macronutrients in diets fed to birds to study the effects of diet quality on metabolic routing of dietary nutrients. We estimated that approximately 45% and 75%, respectively, of the carbon in proteinaceous tissue of birds switched to high‐ or low‐protein diets came from nonprotein dietary sources. In contrast, we estimated that approximately 100% and 20%–80%, respectively, of the nitrogen in proteinaceous tissues of birds switched to high‐ or low‐protein diets was attributable to dietary protein. Thus, the routing and assimilation of dietary carbon and nitrogen differed depending on diet composition. As a result, δ15N of tissues collected from wild animals that consume high‐quality diets may reliably indicate the dietary protein source, whereas δ13C of these same tissues is likely the product of metabolic routing of carbon from several macronutrients. These results have implications for how isotopic discrimination is best estimated and how we can study macronutrient routing in wild animals.

[1]  D. Levey,et al.  Effects of elemental composition on the incorporation of dietary nitrogen and carbon isotopic signatures in an omnivorous songbird , 2003, Oecologia.

[2]  J. Parrish Behavioral, energetic, and conservation implications of foraging plasticity during migration , 2000 .

[3]  H. Mizutani,et al.  ^(13)C and ^(15)N Enrichment Factors of Feathers of 11 Species of Adult Birds , 1992 .

[4]  J. Parrish Patterns of frugivory and energetic condition in Nearctic landbirds during Autumn migration , 1997 .

[5]  Stuart Bearhop,et al.  Factors That Influence Assimilation Rates and Fractionation of Nitrogen and Carbon Stable Isotopes in Avian Blood and Feathers , 2002, Physiological and Biochemical Zoology.

[6]  J. M. Starck,et al.  Physiological and Ecological Adaptations to Feeding in Vertebrates , 2005 .

[7]  D. Post USING STABLE ISOTOPES TO ESTIMATE TROPHIC POSITION: MODELS, METHODS, AND ASSUMPTIONS , 2002 .

[8]  S. McWilliams,et al.  A Test for Passive Absorption of Glucose in Yellow-Rumped Warblers and Its Ecological Implications , 1997, Physiological Zoology.

[9]  W. Tonn,et al.  TROPHIC RELATIONS OF THE RED-NECKED GREBE ON LAKES IN THE WESTERN BOREAL FOREST: A STABLE-ISOTOPE ANALYSIS , 2004 .

[10]  M. J. Deniro,et al.  Influence of Diet On the Distribtion of Nitrogen Isotopes in Animals , 1978 .

[11]  L. Tieszen,et al.  Fractionation and turnover of stable carbon isotopes in animal tissues: Implications for δ13C analysis of diet , 1983, Oecologia.

[12]  F. Bairlein Fruit-eating in brids and its nutritional consequences☆ , 1996 .

[13]  S. McWilliams,et al.  DETERMINANTS OF DIETARY PREFERENCE IN YELLOW-RUMPED WARBLERS , 2002 .

[14]  F. Spina,et al.  Protein loss during long-distance migratory flight in passerine birds: adaptation and constraint. , 2002, The Journal of experimental biology.

[15]  M. J. Deniro,et al.  Mechanism of carbon isotope fractionation associated with lipid synthesis. , 1977, Science.

[16]  M. Ben‐David,et al.  Annual and seasonal changes in diets of martens: evidence from stable isotope analysis , 1997, Oecologia.

[17]  R. Furness,et al.  Influence of Lipid and Uric Acid on δ13C and δ15N Values of Avian Blood: Implications for Trophic Studies , 2000 .

[18]  U. Safriel,et al.  Why are there so few exclusively frugivorous birds? Experiments on fruit digestibility , 1989 .

[19]  K. Hobson,et al.  Assessing Avian Diets Using Stable Isotopes I: Turnover of 13C in Tissues , 1992 .

[20]  D. O'Brien,et al.  STABLE ISOTOPES IN ANIMAL ECOLOGY: ASSUMPTIONS, CAVEATS, AND A CALL FOR MORE LABORATORY EXPERIMENTS , 1997 .

[21]  K. Hobson,et al.  Isotopic fractionation and turnover in captive Garden Warblers (Sylvia borin): implications for delineating dietary and migratory associations in wild passerines , 2003 .

[22]  K. Hobson,et al.  BLOOD ISOTOPIC (δ13C AND δ15N) TURNOVER AND DIET-TISSUE FRACTIONATION FACTORS IN CAPTIVE DUNLIN (CALIDRIS ALPINA PACIFICA) , 2004 .

[23]  Robert G. Clark,et al.  Assessing Avian Diets Using Stable Isotopes II: Factors Influencing Diet-Tissue Fractionation , 1992 .

[24]  H. Biebach,et al.  The role of protein during migration in passerine birds , 1998 .

[25]  D. Levey,et al.  Digestive Responses of Temperate Birds Switched to Fruit or Insect Diets , 1989 .

[26]  B. Pinshow,et al.  Changes in Lean Mass and in Organs of Nutrient Assimilation in a Long‐Distance Passerine Migrant at a Springtime Stopover Site , 1998, Physiological Zoology.

[27]  S. Macko,et al.  STABLE-ISOTOPE ANALYSIS OF CANVASBACK WINTER DIET IN UPPER CHESAPEAKE BAY , 2001 .

[28]  J. Kelly Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology , 2000 .

[29]  K. Hobson,et al.  Using stable carbon (δ13C) and nitrogen (δ15N) isotopes to infer trophic relationships among black and grizzly bears in the upper Columbia River basin, British Columbia , 2000 .

[30]  F. Bairlein Nutritional requirements for maintenance of body weight and fat deposition in the long-distance migratory garden warbler, Sylvia borin (Boddaert). , 1987, Comparative biochemistry and physiology. A, Comparative physiology.

[31]  C. T. Robbins,et al.  USE OF STABLE ISOTOPES TO DETERMINE DIETS OF LIVING AND EXTINCT BEARS , 1996 .

[32]  L. Gannes,et al.  Natural Abundance Variations in Stable Isotopes and Their Potential Uses in Animal Physiological Ecology , 2022 .

[33]  S. McWilliams,et al.  Stable isotopes in breath, blood, feces and feathers can indicate intra-individual changes in the diet of migratory songbirds , 2005, Oecologia.

[34]  J. Hayes,et al.  Biosynthetic control of the natural abundance of carbon 13 at specific positions within fatty acids in Escherichia coli. Evidence regarding the coupling of fatty acid and phospholipid synthesis. , 1980, The Journal of biological chemistry.

[35]  M. Witmer Ecological and Evolutionary Implications of Energy and Protein Requirements of Avian Frugivores Eating Sugary Diets , 1998, Physiological Zoology.

[36]  D. Phillips Mixing models in analyses of diet using multiple stable isotopes: a critique , 2001, Oecologia.