Contrasting digestive strategies of fruit-eating birds

1. Sugary fruits dominate the annual diet of Cedar Waxwings (Bombycilla cedrorum), whereas lipid-rich foods dominate the diets of frugivorous thrushes. Nutrient utilization and preferences of Cedar Waxwings and thrushes fed sugary and lipid-rich natural fruits were assessed to ascertain the potential for nutrient-based specializations that could explain diet selection in nature. 2. Compared allometrically, Cedar Waxwings showed higher rates of sugar assimilation from sugary fruits than did thrushes, by virtue of higher intake rates, and achieved the highest energy assimilation rates when eating a sugary fruit. A trade-off to this digestive strategy appears to be less efficient utilization of lipids when eating exclusively lipid-rich fruits. 3. Thrushes digested lipids more efficiently than Cedar Waxwings as a function of intake rate or estimated retention time, and thrushes achieved the highest energy assimilation rates when eating a lipid-rich fruit. Specialization to a diet rich in lipids appears to limit the rate at which sugary fruits can be processed. 4. Within each bird species, sugar digestive efficiencies were high and were not reduced at higher intake rates. Lipids were consumed at lower rates than sugars, and lipid digestive efficiencies declined with increasing intake rates. Frugivorous birds modulated digestive processing of fruits according to the time needed for efficient digestion and/or absorption of sugars and lipids, respectively. 5. Rate of nitrogen intake, not sugar assimilation, positively influenced body mass changes of birds. Sugary fruits appear nutritionally rich in energy, but limited in protein for avian frugivores. Relatively high intake rates and low protein requirements of Cedar Waxwings suggest that specialization to sugary, low-protein diets involves traits that facilitate acquisition and conservation of protein/amino acids. 6. Cedar Waxwings and thrushes show digestive specialization to the utilization of sugars and lipids, respectively, as dominant dietary nutrients. These traits explain patterns of food selection by these birds in the laboratory and in nature. Variation in the value of particular fruit nutrients to different birds renders the dietary descriptor of ‘frugivore’ ambiguous in a nutritional context.

[1]  M. Witmer Do avian frugivores absorb fruit sugars inefficiently? How dietary nutrient concentration can affect coefficients of digestive efficiency , 1999 .

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

[3]  M. Witmer DO SEEDS HINDER DIGESTIVE PROCESSING OF FRUIT PULP? IMPLICATIONS FOR PLANT/FRUGIVORE MUTUALISMS , 1998 .

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

[5]  T. Givnish,et al.  Nutritional determinants of diet in three Turacos in a tropical montane forest , 1997 .

[6]  M. Witmer Consequences of an alien shrub on the plumage coloration and ecology of Cedar Waxwings , 1996 .

[7]  M. Witmer Annual diet of Cedar Waxwings based on U.S. Biological Survey records (1885-1950) compared to diet of American Robins : Contrasts in dietary patterns and natural history , 1996 .

[8]  Is most glucose absorbed passively in northern bobwhite , 1996 .

[9]  W. Karasov,et al.  The Trade‐Offs Between Digestion Rate and Efficiency in Warblers and Their Ecological Implications , 1995 .

[10]  P. V. Soest Nutritional Ecology of the Ruminant , 1994 .

[11]  C. Conway,et al.  Seasonal Changes in Fatty Acid Composition of the Wood Thrush , 1994 .

[12]  S. Cork,et al.  Glucose absorption by a nectarivorous bird: the passive pathway is paramount. , 1994, The American journal of physiology.

[13]  M. Willson Fruit choices by captive American Robins , 1994 .

[14]  D. Levey,et al.  Gut passage of insects by european starlings and comparison with other species , 1994 .

[15]  F. Bairlein,et al.  Nutritional mechanisms and temporal control of migratory energy accumulation in birds. , 1994, Annual review of nutrition.

[16]  D. Levey,et al.  How do Frugivores Process Fruit? Gastrointestinal Transit and Glucose Absorption in Cedar Waxwings (Bombycilla Cedrorum) , 1992 .

[17]  A. Place Comparative aspects of lipid digestion and absorption: physiological correlates of wax ester digestion. , 1992, The American journal of physiology.

[18]  C. Bosque,et al.  Digestive efficiency and rate of food passage in oilbird nestlings , 1992 .

[19]  A. Place,et al.  LIVING OFF THE WAX OF THE LAND: BAYBERRIES AND YELLOW-RUMPED WARBLERS , 1992 .

[20]  D. Levey,et al.  Digestive modulation in a seasonal frugivore, the American robin (Turdus migratorius). , 1992, The American journal of physiology.

[21]  D. Levey,et al.  Evolutionary Implications of Fruit-Processing Limitations in Cedar Waxwings , 1991, The American Naturalist.

[22]  D. Levey,et al.  Digestive System Trade-offs and Adaptations of Frugivorous Passerine Birds , 1990, Physiological Zoology.

[23]  W. Karasov,et al.  Digestion Strategies in Nectar- and Fruit-Eating Birds and the Sugar Composition of Plant Rewards , 1990, The American Naturalist.

[24]  J. Pappenheimer Paracellular intestinal absorption of glucose, creatinine, and mannitol in normal animals: relation to body size. , 1990, The American journal of physiology.

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

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

[27]  D. Levey Physiological Basis and Ecological Consequences of Sugar Preferences in Cedar Waxwings , 1989 .

[28]  C. Herrera VERTEBRATE-DISPERSED PLANTS OF THE IBERIAN PENINSULA: A STUDY OF FRUIT CHARACTERISTICS' , 1987 .

[29]  J. Denslow,et al.  A synthetic diet for fruit-eating birds , 1987 .

[30]  Duong Phan,et al.  Food Passage and Intestinal Nutrient Absorption in Hummingbirds , 1986 .

[31]  Robert A. Johnson,et al.  Nutritional Values of Wild Fruits and Consumption by Migrant Frugivorous Birds , 1985 .

[32]  Montague W. Demment,et al.  A Nutritional Explanation for Body-Size Patterns of Ruminant and Nonruminant Herbivores , 1985, The American Naturalist.

[33]  J. Denslow,et al.  Neotropical Avian Frugivores: Patterns of Behavior, Morphology, and Nutrition, with Consequences for Fruit Selection , 1985 .

[34]  C. Herrera ADAPTATION TO FRUGIVORY OF MEDITERRANEAN AVIAN SEED DISPERSERS , 1984 .

[35]  A. E. Sorensen Nutrition, energy and passage time: experiments with fruit preference in European blackbirds (Turdus merula) , 1984 .

[36]  D. Small,et al.  Lipid digestion and absorption. , 1983, Annual review of physiology.

[37]  D. W. White,et al.  Additional Information on Temperate Bird-Disseminated Fruits: Response to Herrera's Comments , 1982, The American Naturalist.

[38]  P. V. Soest,et al.  Utilization of bamboo by the giant panda. , 1982, The Journal of nutrition.

[39]  C. Herrera Are Tropical Fruits More Rewarding to Dispersers Than Temperature Ones? , 1981, The American Naturalist.

[40]  J. Sell,et al.  Influence of Fat and Carbohydrate Source on Rate of Food Passage of Semipurified Diets for Laying Hens , 1981 .

[41]  Richard M. Sibly,et al.  Strategies of digestion and defecation , 1981 .

[42]  E. Stiles Patterns of Fruit Presentation and Seed Dispersal in Bird-Disseminated Woody Plants in the Eastern Deciduous Forest , 1980, The American Naturalist.

[43]  P. Berthold The control and significance of animal and vegetable nutrition in omnivorous songbirds , 1976 .

[44]  A. Willis,et al.  The estimation of carbohydrates in plant extracts by anthrone. , 1954, The Biochemical journal.

[45]  H. Zim,et al.  American Wildlife and Plants: A Guide To Wildlife Food Habits , 1951 .

[46]  R. Mccance,et al.  The available carbohydrate of fruits: Determination of glucose, fructose, sucrose and starch. , 1935, The Biochemical journal.

[47]  E. Huntington Geography of American Notables , 1931 .

[48]  R. Ridgway On Fisher's Petrel (Æstrelata fisheri) , 1895 .