William H. Karasov

Morphometrics of the Avian Small Intestine Compared with That of Nonflying Mammals: A Phylogenetic Approach

Flying animals may experience a selective constraint on gut volume because the energetic cost of flight increases and maneuverability decreases with greater digesta load. The small intestine is the primary site of absorption of most nutrients (e.g., carbohydrates, proteins, fat) in both birds and mammals. Therefore, we used a phylogenetically informed approach to compare small intestine morphometric measurements of birds with those of nonflying mammals and to test for effects of diet within each clade. We also compared the fit of nonphylogenetic and phylogenetic models to test for phylogenetic signal after accounting for effects of body mass, clade, and/or diet. We provide a new MATLAB program (Regressionv2.m) that facilitates a flexible model‐fitting approach in comparative studies. As compared with nonflying mammals, birds had 51% less nominal small intestine surface area (area of a smooth bore tube) and 32% less volume. For animals <365 g in body mass, birds also had significantly shorter small intestines (20%–33% shorter, depending on body mass). Diet was also a significant factor explaining variation in small intestine nominal surface area of both birds and nonflying mammals, small intestine mass of mammals, and small intestine volume of both birds and nonflying mammals. On the basis of the phylogenetic trees used in our analyses, small intestine length and nominal surface area exhibited statistically significant phylogenetic signal in birds but not in mammals. Thus, for birds, related species tended to be similar in small intestine length and nominal surface area, even after accounting for relations with body mass and diet. A reduced small intestine in birds may decrease the capacity for breakdown and active absorption of nutrients. Birds do not seem to compensate for reduced digestive and absorptive capacity via a longer gut retention time of food, but we found some evidence that birds have an increased mucosal surface area via a greater villus area, although not enough to compensate for reduced nominal surface area. We predict that without increased rate of enzyme hydrolysis and/or mediated transport and without increased passive absorption of water‐soluble nutrients, birds may operate with a reduced digestive capacity, compared with that of nonflying mammals, to meet an increase in metabolic needs (i.e., a reduced spare capacity).

A simple method for measuring intestinal solute uptake in vitro

SummaryWe describe a method of measuring intestinal solute uptake that combines the virtues of simplicity, good tissue viability as reflected in high uptake rates, and reduction of unstirred layers comparable to the best reported for chambers. An everted sleeve of intestine is mounted on a grooved rod stationed immediately over a stirring bar rotating at 1,200 rpm. The effect of edge damage is negligible. The coefficient of variation of uptake measurements is 7%. For mouse intestine andd-glucose at high concentrations an incubation time of 1 min represents a suitable compromise among several competing criteria.l-glucose is used to correct actived-glucose uptake simultaneously for adherent fluid and for passive uptake. The techniques general utility is illustrated by its application to intestines of four species representing four classes of vertebrates.

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.

The Trade‐Offs Between Digestion Rate and Efficiency in Warblers and Their Ecological Implications

Frugivory in birds is associated with rapid gut passage whereas insectivory is associated with slower gut passage. This is interpreted by some avian ecologists to reflect an inherent digestive constraint on diet selection, but it could also result from dietary acclimation. We predicted that Yellow-rumped Warblers (Dendroica coronata) acclimated to fruit-, insect-, and seed-based diets would exhibit retention times that increase in that rank order, because this is the rank order of retention time across species that eat these types of food. We also predicted a trade-off between rate of processing (the inverse of retention time) and extraction efficiency. This is based on the assumption that digestive enzymes or absorptive capacity occur in the gastrointestinal tract at levels that are not in great excess, and so less contact time between enzymes and digesta reduces the extraction efficiency. To test these predictions, we measured retention time (using aqueous and lipid-phase inert markers) and extraction efficiency of glucose, sucrose, leucine, starch, and the lipid glycerol trioleate (using radio-labeled nutrients and inert markers). Our results were in accordance with predictions. Mouth-to-anus total mean retention time (TMRT) of Yellow-rumped Warblers acclimated to fruit-, insect-, and seed-based diets were, respectively, 46 ± 9, 62 ± 6, and 114 ± 9 min for polyethylene glycol (PEG, an aqueous marker) : results were similar for the lipid phase marker in most cases. But Yellow-rumped Warblers that were switched suddenly to an alternate diet did not readjust TMRT when tested 2 h later or did so incompletely. We found no diet-related morphological changes in the digestive tract, and thus attribute these results to changes in gut motility. Extraction efficiency was uniformly high across all diets for glucose (88 ± 1%), but varied among diet groups according to our prediction for leucine (range 82-94%), sucrose (58-85%), starch (9-48%), and lipid (18-82%). We review how features of the Yellow-rumped Warblers digestive system permit relatively high energy uptake across a wide variety of food types. The most notable constraining feature was a low starch hydrolysis rate, probably restricting them from relying on starchy foods. Thus, digestive strategy (i.e., a combination of retention time of food in the gut and digestive efficiency) somewhat determines diet, but in more respects diet determines strategy.

Ecological Physiology of Diet and Digestive Systems

The morphological and functional design of gastrointestinal tracts of many vertebrates and invertebrates can be explained largely by the interaction between diet chemical constituents and principles of economic design, both of which are embodied in chemical reactor models of gut function. Natural selection seems to have led to the expression of digestive features that approximately match digestive capacities with dietary loads while exhibiting relatively modest excess. Mechanisms explaining differences in hydrolase activity between populations and species include gene copy number variations and single-nucleotide polymorphisms. In many animals, both transcriptional adjustment and posttranscriptional adjustment mediate phenotypic flexibility in the expression of intestinal hydrolases and transporters in response to dietary signals. Digestive performance of animals depends also on their gastrointestinal microbiome. The microbiome seems to be characterized by large beta diversity among hosts and by a common core metagenome and seems to differ flexibly among animals with different diets.

Effect of dietary carbohydrate on monosaccharide uptake by mouse small intestine in vitro.

Using intestinal sleeves in vitro, we studied the effect of dietary carbohydrate on active monosaccharide uptake in mice. Dietary carbohydrate did not affect numerous parameters of intestinal structure, such as length, circumference, weight, protein content, villus dimensions and density, and area at the villus level. Mice on a carbohydrate‐free diet had active D‐glucose uptake relatively independent of position along the small intestine. A carbohydrate‐containing diet reversibly and within 1 day stimulated uptake except in the ileum, restoring the proximal‐to‐distal gradient in glucose uptake normally observed. This stimulation involved a 81‐116% increase in the Michaelis‐ Menton constant Vmax, and also an apparent increase in the Michaelis‐ Menton constant Km, that may however be an artifact arising from unstirred‐layer effects. Active uptake of 3‐O‐methyl‐D‐glucose also increased, permeability to glucose remained unchanged, and proline uptake reversibly decreased (probably due to the lower protein content of the carbohydrate‐containing diets). The effect of fasting on active monosaccharide uptake seemed largely due to withdrawal of dietary carbohydrate, rather than of calories per se. It is concluded that dietary carbohydrate causes induction of monosaccharide carriers in the intestine, along with its more familiar induction of pancreatic amylase and intestinal disaccharidases. Substrate‐dependent carrier induction may be physiologically significant in maintaining the proximal‐to‐distal gradient of glucose transport. An appendix presents measurements of villus area as a function of position along the intestine.

Digestive Plasticity in Avian Energetics and Feeding Ecology

This chapter focuses on changes in gastrointestinal (GI) structure and function and how they influence the supply of energy and nutrients for maintenance and production (growth, storage, and reproduction). There is considerable evidence that digestive features are influenced by factors such as diet quality and quantity in species from many avian orders including the Anseriformes (Ankney 1977; Drobney 1984; Prop and Vulink 1992), Galliformes (Gasaway 1976; Moss 1983), Columbiformes (Kenward and Sibly 1977), and Passeriformes (Davis 1961; Al- Dabbagh et al. 1987; Brugger 1991; Walsberg and Thompson 1990). The likely ecological importance of digestive adjustments is suggested by a number of theoretical arguments and some observations.

Diet breadth of mammalian herbivores: nutrient versus detoxification constraints.

Abstract Two hypotheses, nutrient constraints and detoxification limitation, have been proposed to explain the lack of specialists among mammalian herbivores. The nutrient constraint hypothesis proposes that dietary specialization in mammalian herbivores is rare because no one plant can provide all requisite nutrients. The detoxification limitation hypothesis suggests that the mammalian detoxification system is incapable of detoxifying high doses of similar secondary compounds present in a diet of a single plant species. We experimentally tested these hypotheses by comparing the performance of specialist and generalist woodrats (Neotoma) on a variety of dietary challenges. Neotoma stephensi is a narrow dietary specialist with a single species, one-seeded juniper, Juniperus monosperma, comprising 85–95% of its diet. Compared with other plants available in the habitat, juniper is low in nitrogen and high in fiber, phenolics, and monoterpenes. The generalist woodrat, N. albigula, also consumes one-seeded juniper, but to a lesser degree. The nutrient constraint hypothesis was examined by feeding both species of woodrats a low-nitrogen, high-fiber diet similar to that found in juniper. We found no differences in body mass change, or apparent digestibility of dry matter or nitrogen between the two species of woodrats after 35 days on this diet. Moreover, both species were in positive nitrogen balance. We tested the detoxification limitation hypothesis by comparing the performance of the generalist and specialist on diets with and without juniper leaves, the preferred foliage of the specialist, as well as on diets with and without α-pinene, the predominant monoterpene in juniper. We found that on the juniper diet, compared with the specialist, the generalist consumed less juniper and lost more mass. Urine pH, a general indicator of overall detoxification processes, declined in both groups on the juniper diet. The generalist consumed half the toxin load of the specialist yet its urine pH was slightly lower. Moreover, the generalist consumed significantly less of the treatment with high concentrations of α-pinene compared to the control treatment, while the specialist consumed the same amount of food regardless of α-pinene concentration. For both groups, urine pH declined as levels of α-pinene in the diet increased. The generalist produced a significantly more acidic urine than the specialist on the treatment with the highest α-pinene concentration. Our results suggest that in this system, specialists detoxify plant secondary compounds differently than generalists and plant secondary compounds may be more important than low nutrient levels in maintaining dietary diversity in generalist herbivores.

Digestive System Trade-offs and Adaptations of Frugivorous Passerine Birds

Researchers have historically assumed that short food retention time is a typical trait of frugivorous birds, and our data support this. Because absorptive efficiency is directly related to retention time and absorption rate, we predicted that either rates of nutrient absorption would be higher in frugivores than other birds to compensate for short retention or that absorptive efficiencies would be lower. In the fourpasserine species that we studied, the more frugivorous species had higher intestinal glucose (but notproline) transport activity than the more insectivorous and carnivorous species and higher intestinal sucrase activity. But compared with those of chickens and hummingbirds, small intestines of frugivorous passerines (four species) did not have high rates of glucose and proline uptake in vitro. In accordance with our prediction, in vivo digestive efciency of radiolabeled glucose was 92% in frugivorous cedar waxwings (88% for fructose) and 73% in fruit-eating American robins, less than the expected value near 100%. Digestive effciency for sucrose was even less (62% in cedar waxwings, 0% in American robins). Thus, it appears that the anatomy and physiology of fruit eaters result in less than complete digestion and absorption of sugars. Presumably there is some compensating advantage to short digesta retention thatperhaps increases net rate of energy intake. It may lie in the ability of frugivores to process large amounts of fruitper unit time in spite of the constraint gut volume might place on fruit intake.

Nutritional Costs of a Plant Secondary Metabolite Explain Selective Foraging by Ruffed Grouse

Plant secondary metabolites (PSMs) are commonly thought to deter vertebrate herbivores by being toxic or by reducing nutrient assimilation. An alternative, complementary hypothesis is that PSMs may influence herbivore forage selection at subtoxic levels by imposing high detoxication costs post absorption. Many studies of insect herbivores have been undertaken to measure the metabolic load of detoxication as it relates to host-plant specialization, but results have been equivocal and the subject of much debate. Some recent studies of vertebrate herbivores indicate that metabolism of PSMs can impose a cost by increasing nutrient losses due to conjugation of PSMs to endogenous materials, and by upsetting pH homeostasis. In this study, we demonstrate that detoxication costs in Ruffed Grouse are substantial, and are reduced by selective foraging. In winter, Ruffed Grouse feed preferentially on quaking aspen with relatively low levels of coniferyl benzoate (CB) in staminate flower buds. We collected aspen buds with low- and high-CB levels and conducted feeding trials with captive Ruffed Grouse that had been acclimated to an aspen bud diet. We measured nutrient utilization efficiencies and excretion of detoxication conjugates. Grouse assimilated 24% less energy from high- vs. low-CB buds. Using a nutritional model, we determined that the reduction of energy utilization efficiency was mainly due to dilution of the diet by CB, and not by digestive inhibition. As CB intake increased, grouse excreted more glucuronic acid and ornithine (two major detoxication conjugates), resulting in an energetic cost of 10% to 14% of metabolizable energy intake for low- and high-CB buds, respectively. Conjugation with the amino acid ornithine increased minimum nitrogen requirement by 68% to 90% for low- and high-CB buds, respectively. Ammonium excretion also increased with CB intake, indicating an upset of pH homeostasis. Thus, detoxication costs were relatively high and increased with higher CB intake. Ruffed Grouse preference for low-CB, high-protein aspen buds in nature appears to be related to lower utilization efficiency and higher detoxication costs associated with high CB concentrations. The importance of detoxication cost to herbivores must be more thoroughly evaluated and integrated into existing models of herbivore foraging behavior.