Scott R. McWilliams

Phenotypic flexibility in digestive system structure and function in migratory birds and its ecological significance

Birds during migration must satisfy the high energy and nutrient demands associated with repeated, intensive flight while often experiencing unpredictable variation in food supply and food quality. Solutions to such different challenges may often be physiologically incompatible. For example, increased food intake and gut size are primarily responsible for satisfying the high energy and nutrient demands associated with migration in birds. However, short-term fasting or food restriction during flight may cause partial atrophy of the gut that may limit utilization of ingested food energy and nutrients. We review the evidence available on the effects of long- and short-term changes in food quality and quantity on digestive performance in migratory birds, and the importance of digestive constraints in limiting the tempo of migration in birds. Another important physiological consequence of feeding in birds is the effect of diet on body composition dynamics during migration. Recent evidence suggests that birds utilize and replenish both protein and fat reserves during migration, and diet quality influences the rate of replenishment of both these reserves. We conclude that diet and phenotypic flexibility in both body composition and the digestive system of migratory birds are important in allowing birds to successfully overcome the often-conflicting physiological challenges of migration.

Physiological regulatory networks: ecological roles and evolutionary constraints

Ecological and evolutionary physiology has traditionally focused on one aspect of physiology at a time. Here, we discuss the implications of considering physiological regulatory networks (PRNs) as integrated wholes, a perspective that reveals novel roles for physiology in organismal ecology and evolution. For example, evolutionary response to changes in resource abundance might be constrained by the role of dietary micronutrients in immune response regulation, given a particular pathogen environment. Because many physiological components impact more than one process, organismal homeostasis is maintained, individual fitness is determined and evolutionary change is constrained (or facilitated) by interactions within PRNs. We discuss how PRN structure and its system-level properties could determine both individual performance and patterns of physiological evolution.

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.

Effect of dietary fatty acid composition on depot fat and exercise performance in a migrating songbird, the red-eyed vireo

SUMMARY Most migrating birds accumulate lipid stores as their primary source of energy for fueling long distance flights. Lipid stores of birds during migration are composed of mostly unsaturated fatty acids; whether such a fatty acid composition enhances exercise performance of birds is unknown. We tested this hypothesis by measuring metabolic rate at rest and during intense exercise in two groups of red-eyed vireos, a long-distance migratory passerine, fed either a diet containing 82% unsaturated fat (82%U), or one containing 58% unsaturated fat (58%U). Vireos fed the 82%U diet had fat stores containing (77%) unsaturated fatty acids, whereas vireos fed the 58% U diet had fat stores containing less (66%) unsaturated fatty acids. Blood metabolites measured prior to and immediately following exercise confirmed that vireos were metabolizing endogenous fat during intense exercise. Mass-specific resting metabolic rate (RMR) was similar for vireos fed the 58%U diet (2.75±0.32 ml O2 g–1 h–1) and for vireos fed the 82%U diet (2.30±0.30 ml O2 g–1 h–1). However, mass-specific peak metabolic rate (MRpeak) was 25% higher in vireos fed the 58%U diet (28.55±1.47 ml O2 g–1 h–1) than in vireos fed the 82%U diet (21.50±1.76 ml O2 g–1 h–1). Such whole-animal energetic effects of fatty acid composition of birds suggest that the energetic cost of migration in birds may be affected by the fatty acid composition of the diet.

Carbon Turnover in Tissues of a Passerine Bird: Allometry, Isotopic Clocks, and Phenotypic Flexibility in Organ Size

Stable isotopes are an important tool for physiological and behavioral ecologists, although their usefulness depends on a thorough understanding of the dynamics of isotope incorporation into tissue(s) over time. In contrast to hair, claws, and feathers, most animal tissues continuously incorporate carbon (and other elements), and so carbon isotope values may change over time, depending on resource use and tissue‐specific metabolic rates. Here we report the carbon turnover rate for 12 tissues from a passerine bird, the zebra finch (Taeniopygia guttata). We measured average carbon retention time (τ) for 8 d for small intestine; 10–13 d for gizzard, kidney, liver, pancreas, and proventriculus; 17–21 d for heart, brain, blood, and flight muscle; and 26–28 d for leg muscle and skin. We used these data, along with the few other published estimates, to confirm that the fractional rate of isotopic turnover for red blood cells, whole blood, liver, and leg muscle scales with body mass to approximately the −1/4 power. Our data also support several key assumptions of the “isotopic‐clock” model, which uses differences in isotope value between tissues, along with estimates of turnover rate of these tissues, to predict time elapsed since a diet shift. Finally, we show that between‐tissues differences in turnover rate largely, but not entirely, explain the extent of phenotypic flexibility in organs of garden warblers during their long‐distance flight across the Sahara Desert during spring. More studies that measure tissue‐specific protein synthesis, metabolic rate, and elemental turnover in many tissues from a variety of animals are needed.

FRUIT QUALITY AND CONSUMPTION BY SONGBIRDS DURING AUTUMN MIGRATION

Abstract Seasonal fruits are an important food resource for small songbirds during autumn migration in southern New England. Therefore, conservation and management of important stopover sites used by migrating birds requires knowledge about nutritional requirements of songbirds and nutritional composition of commonly consumed fruits. We measured nutrient composition and energy density of nine common fruits on Block Island, Rhode Island, and conducted a field experiment to estimate consumption rates of three of these fruits by birds during autumn migration. Most common fruits on Block Island contained primarily carbohydrates (41.3–91.2% dry weight), and little protein (2.6–8.6%) and fat (0.9–3.7%), although three contained more fat: Myrica pennsylvanica (50.3%), Viburnum dentatum (41.3%), and Parthenocissus quinquefolia (23.6%). Bird consumption of high-fat, high-energy V. dentatum fruit and high-carbohydrate, low-energy Phytolacca americana fruit was greater than consumption of Aronia melanocarpa, a high-carbohydrate, low-energy fruit. We estimated that migratory birds on Block Island must eat up to four times their body mass in fruit wet weight each day to satisfy their energy requirements when eating low-energy fruits such as P. americana, and they cannot satisfy their protein requirements when eating only certain high-energy fruits such as V. dentatum. Our results suggest that many migratory birds must eat both fruits and insects to meet their dietary needs. Thus, shrubland habitat at important migratory stopover sites such as Block Island should be managed so that it contains a variety of preferred fruit-bearing shrubs and an adequate abundance of insects.

Patterns of Fuel use and Storage in Migrating Passerines in Relation to Fruit Resources at Autumn Stopover Sites

ABSTRACT. Fuel deposition rates of migrating birds may indicate the quality of habitat at stopover sites, yet little is known about how diet habits and food availability affect fat and protein metabolism in free-living songbirds at stopover sites. We compared plasma indicators of fat deposition (triglyceride), fat catabolism (B-hydroxybutyrate), and protein catabolism (uric acid) among passerine species that are frugivorous to a variable degree during autumn stopover on Block Island, Rhode Island. We also compared plasma lipid metabolites from 3 of these species that were captured at 2 stopover sites with different fruit abundance. The more frugivorous Hermit Thrushes (Catharus guttatus) had the highest plasma triglyceride, and uric acid was highest in the least frugivorous species sampled on Block Island, but other differences among species were not clearly related to diet. B-hydroxybutyrate was more variable among the species sampled on Block Island. Plasma triglyceride was significantly higher in Hermit Thrushes captured on Block Island, where fruit resources were abundant, than in Hermit Thrushes captured at a mainland site in southern Rhode Island, where less fruit was available. Our results suggest that diet habits may influence fat and protein metabolism in migrating passerines, but careful study design and statistical analyses are necessary to control for or minimize the effects of the many influential factors that affect plasma metabolites so they can be used to assess fuel deposition in free-living birds and to compare the quality of migration stopover sites.

SEASONAL CHANGES IN COMPOSITION OF LIPID STORES IN MIGRATORY BIRDS: CAUSES AND CONSEQUENCES

Abstract It is well established that birds use fat stores to primarily fuel migration; however, few studies have focused on the causes and consequences of observed seasonal changes in fatty acid composition of fat stores in birds. We propose and test two hypotheses that address the causes of these seasonal changes in composition of fat stores: (1) diet composition determines fatty acid composition of fat stores, and (2) birds selectively metabolize and store certain fatty acids during migration in lieu of changing their diet. When we offered Red-eyed Vireos (Vireo olivaceous) choices between diets that differed only in fatty acid composition, vireos preferred diets with more triolein over diets with more tristearin and tripalmitin, and these preferences were similar between seasons. We also collected fat samples six times throughout the year from captive Red-eyed Vireos fed one of two diets differing in fatty acid composition, and found that fatty acid composition of stored fat differed by diet and changed over time, although these changes were not season-specific or consistent with the selective-metabolism hypothesis. Thus, fatty acid composition of stored fat was primarily a product of diet composition; selective metabolism possibly played a minor, but important, role. Given recent evidence that fatty acid composition of birds affects their energy expenditure during intense exercise, the implication is that birds at stopover sites can influence the fatty acid composition of their body fat by selective feeding, and this can significantly affect the energetic cost of migration. Cambios Estacionales en la Composición de las Reservas Lipídicas en Aves Migratorias: Causas y Consecuencias Resumen. Se sabe que las aves utilizan reservas de grasa principalmente como fuente de energía durante la migración; sin embargo, pocos estudios han analizado las causas y consecuencias de los cambios estacionales en la composición de ácidos grasos de las reservas de grasa de las aves. Aquí proponemos y probamos dos hipótesis que se relacionan con las causas de los cambios estacionales en la composición de las reservas de grasa: (1) la composición de la dieta determina la composición de ácidos grasos de las reservas de grasa, y (2) las aves metabolizan y almacenan de manera selectiva ciertos ácidos grasos durante la migración, en lugar de cambiar sus dietas. Ofrecimos a individuos de la especie Vireo olivaceous para que elijan entre dietas que sólo diferían en la composición de ácidos grasos, los cuáles prefirieron dietas con más trioleina que dietas con más tristearina y tripalmitina, y estas preferencias fueron similares entre estaciones. Colectamos además muestras de grasa, en seis oportunidades a lo largo del año, de individuos en cautiverio alimentados con una de las dos dietas disponibles, las que difirieron en la composición de ácidos grasos. Encontramos que la composición de ácidos grasos de las reservas de grasa difirió en relación a las dietas y varió a lo largo del tiempo, aunque estos cambios no fueron estacionalmente específicos ni coherentes con la hipótesis de metabolismo selectivo. Por lo tanto, la composición de ácidos grasos de las reservas de grasa fue principalmente el producto de la composición de la dieta; el metabolismo selectivo probablemente jugó un papel menor, aunque importante. Existe evidencia reciente que sugiere que la composición de ácidos grasos en las aves afecta el gasto energético que tienen durante períodos de ejercicios intensos, lo que implica que las aves pueden influir sobre la composición de los ácidos grasos en sus reservas de grasa al alimentarse de manera selectiva en los sitios de parada migratoria, lo que puede afectar significativamente el costo energético de la migración.

A Test for Passive Absorption of Glucose in Yellow-Rumped Warblers and Its Ecological Implications

In an earlier study, we found that yellow-rumped warblers had in vitro active uptake rates of D-glucose that were only a few percent of the glucose absorption rate achieved at the wholeanimal level. Here we used a pharmacokinetic technique to test whether a substantial amount of sugar can be absorbed passively. We used yellow-rumped warblers (Dendroica coronata), known for their seasonal frugivory, freely feeding on a synthetic mash formulated with naturally occurring concentrations of D-glucose. Birds absorbed 89.8% ± 1.0% (SE) of the D-glucose in the mash. When fed the same mash with trace-labeled ³H L-glucose, the stereoisomer that does not interact with the intestinal Na⁺-glucose cotransporter, ³H appeared in plasma, an indication that this stereoisomer of glucose was absorbed. We used ³H levels in plasma and excreta in a pharmacokinetic model to calculate L-glucose extraction efficiency (i.e., the percent absorbed). Calculated mean extraction efficiency for the passively absorbed L-glucose averaged 91% ± 23%. Our finding of considerable passive absorption reconciles the in vitro and in vivo results for D-glucose absorption and is in concert with results from five other avian species. The passive pathway appears to provide birds with an absorptive process that can respond quickly to changing luminal concentration and that is energetically inexpensive to maintain and modulate in real time but that may bear a cost. Less discriminate passive absorption might increase vulnerability to toxins and thus constrain foraging behavior and limit the breadth of the dietary niche.

Digestive adjustments in cedar waxwings to high feeding rate

Birds may dramatically increase their food intake during migratory periods or during winter. We tested the hypotheses that when birds are hyperphagic, (a) their digesta retention time and extraction efficiency will not change compared with that of birds feeding at reduced rates, (b) their total capacity for breakdown and absorption of nutrients will increase, and (c) the mechanism responsible for the increase in total capacity will be an increase in amount of intestine rather than an increase in intestinal tissue-specific enzyme activity or nutrient transporter activity. We measured gut anatomy, retention time of digesta, enzyme hydrolysis rates, nutrient absorption rates, and digestive efficiency in individual cedar waxwings (Bombycilla cedrorum) acclimated to –20°C or +21°C. Compared with cedar waxwings held at +21°C, waxwings acclimated to –20°C more than tripled their daily food intake. Mass of digestive organs increased by 22–53%, but rates of enzyme activity and nutrient uptake per unit of small intestine did not change significantly. Retention time of digesta declined slightly, and there was a small decrease in digestive efficiency. As predicted, the main adjustment to increased energy requirements and food intake was an increase in gut length, mass, and volume which largely compensated for increased digesta flow at high intake rates. However, we detected a small reduction in retention time and digestive efficiency in waxwings with high intakes which suggests that these waxwings may be unable to further increase their gut size (i.e., that the increase in gut size was maximal). If adjustments involving gut size require weeks of acclimation time, migration patterns and the pace of migration in birds could be influenced by time required for preparation of the gut. J. Exp. Zool. 283:394–407, 1999.