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).

Anecdotal evidence suggests that birds have smaller intestines than mammals. In the present analysis, we show that small birds and bats have significantly shorter small intestines and less small intestine nominal (smooth bore tube) surface area than similarly sized nonflying mammals. The corresponding >50% reduction in intestinal volume and hence mass of digesta carried is advantageous because the energetic costs of flight increase with load carried. But, a central dilemma is how birds and bats satisfy relatively high energy needs with less absorptive surface area. Here, we further show that an enhanced paracellular pathway for intestinal absorption of water-soluble nutrients such as glucose and amino acids may compensate for reduced small intestines in volant vertebrates. The evidence is that l -rhamnose and other similarly sized, metabolically inert, nonactively transported monosaccharides are absorbed significantly more in small birds and bats than in nonflying mammals. To broaden our comparison and test the veracity of our finding we surveyed the literature for other similar studies of paracellular absorption. The patterns found in our focal species held up when we included other species surveyed in our analysis. Significantly greater amplification of digestive surface area by villi in small birds, also uncovered by our analysis, may provide one mechanistic explanation for the observation of higher paracellular absorption relative to nonflying mammals. It appears that reduced intestinal size and relatively enhanced intestinal paracellular absorption can be added to the suite of adaptations that have evolved in actively flying vertebrates.

SUMMARY: Increasing evidence indicates that small birds have more extensive non-mediated, paracellular intestinal absorption of hydrosoluble compounds than do mammals, although studies have not employed uniform methodologies or demonstrated differences at the tissue level. The mechanistic bases behind apparent species differences are poorly understood. We show using uniform methodology at the whole-animal level that intact, unanesthetized pigeons had significantly higher absorption of l-arabinose and l-rhamnose, two water-soluble compounds used to measure paracellular absorption, than similarly sized laboratory rats. The species differences were also evident using perfused isolated loops of duodenum,showing that the difference in paracellular absorption occurred at the tissue level, even when d-glucose absorption rates(transcellular+paracellular) were similar between the two species. The greater absorption of these probes in pigeons could not be explained by mediated uptake of the putative paracellular probes, or by increased nominal surface area, increased villus area or increased number of tight junctions. Rats and pigeons had comparable absorption of larger probes, which is consistent with similar effective pore size of the tight junction between enterocytes. The elimination of these mechanistic explanations might suggest that pigeon intestine has relatively higher paracellular solvent drag, but pigeon duodenal segments did not have higher net water absorption than rat duodenal segments. Whatever the exact mechanism(s), the paracellular pathway of both species limits substantial (>5%) fractional absorption to molecules smaller than about 4.8 Å (Mr ca. 350), and permeability to smaller molecules at the tissue level is higher in pigeons than in rats.

Decline of red fox (Vulpes vulpes) populations in Illinois has been attributed to altered geographic landscapes and the eastward expansion of the coyote. To investigate effects of habitat use and competition with coyotes on diets of foxes in intensively farmed landscapes of Illinois, we analyzed carbon and nitrogen isotope ratios (δ¹³C and δ¹⁵N) of foxes, coyotes (Canis latrans), and other local species. Foxes were categorized as rural (agricultural habitat, coyotes present), urban (urban habitat, coyotes absent), or from an agricultural research facility at the University of Illinois (South Farms, agricultural habitat, coyotes absent). Rural foxes had higher fur isotopic values (δ¹³C and δ¹⁵N) than rural coyotes, indicating that coyotes caused foxes to consume prey items from higher trophic levels and eat more C₄plants. Urban foxes had lower isotopic values (δ¹³C and δ¹⁵N) than South Farms foxes, suggesting that habitat use partly determined fox diets; foxes in urbanized habitats consumed prey at lower trophic levels within a largely C₃plant based food web. Models of competitive exclusion by coyotes were better predictors of fox long-term diets, including pup rearing, while habitat use models predicted fox diets on a narrower timescale. Competitive exclusion by coyotes might be an important factor explaining the decline of foxes in the intense farming areas of Illinois.

Water-soluble nutrients can be absorbed across the intestinal epithelium by transcellular and paracellular processes. Recent studies suggest that small birds (300 g) selected from diverse taxa: American coots, mallards, pheasants, and pigeons. Absorption of carbohydrate probes was inversely related to body mass in birds, and absorption of these probes in large birds (>500 g) was comparable to absorption measurements in nonflying mammals. Higher paracellular uptake in the smaller avian species may offer a physiologically inexpensive means of nutrient absorption to compensate for a reduced small intestine size but may make those species more vulnerable to toxicant absorption.