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).
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.
In vertebrates and invertebrates, morphological and functional features of gastrointestinal (GI) tracts generally reflect food chemistry, such as content of carbohydrates, proteins, fats, and material(s) refractory to rapid digestion (e.g., cellulose). The expression of digestive enzymes and nutrient transporters approximately matches the dietary load of their respective substrates, with relatively modest excess capacity. Mechanisms explaining differences in hydrolase activity between populations and species include gene copy number variations and single-nucleotide polymorphisms. Transcriptional and posttranscriptional adjustments mediate phenotypic changes in the expression of hydrolases and transporters in response to dietary signals. Many species respond to higher food intake by flexibly increasing digestive compartment size. Fermentative processes by symbiotic microorganisms are important for cellulose degradation but are relatively slow, so animals that rely on those processes typically possess special enlarged compartment(s) to maintain a microbiota and other GI structures that slow digesta flow. The taxon richness of the gut microbiota, usually identified by 16S rRNA gene sequencing, is typically an order of magnitude greater in vertebrates than invertebrates, and the interspecific variation in microbial composition is strongly influenced by diet. Many of the nutrient transporters are orthologous across different animal phyla, though functional details may vary (e.g., glucose and amino acid transport with K+ rather than Na+ as a counter ion). Paracellular absorption is important in many birds. Natural toxins are ubiquitous in foods and may influence key features such as digesta transit, enzymatic breakdown, microbial fermentation, and absorption
Daily energy metabolism and water flux were measured with doubly labeled water in the free-living insectivorous lizards Cnemidophorus tigris (mean body mass 15.7 g) and Callisaurus draconoides (8.6 g) in June 1979 in the Colorado Desert of California. C. tigris was an active forager; it spent 91% of its 5-h daily activity period in movement. C. draconoides was a sit-and-wait predator; it spent less than 2% of its 10-h activity period in movement. C. tigris had significantly higher rates of field energy metabolism and water influx (210 Jg day, 36.8 ul HO g day, N=19) than C. draconoides (136, 17.1, N=18). There were no significant differences between the sexes within either species.The extra costs of free existence were calculated from differences between field metabolic rates and maintenance costs estimated from laboratory respirometry. Rates of energy metabolism during the field activity period were about 1.5x resting levels at 40° C (∼field active body temperature) for C. draconoides and 3.3 x resting levels at 40° C (∼field active body temperature) for the more active C. tigris. Feeding rates calculated from water influx data were 13.3 mg g day for C. tigris and 5.8 mg g day for C. draconoides. Though C. tigris had a high rate of energy expenditure, its foraging efficiency [Formula: see text] was higher than C. draconoides'.
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