Enrique Caviedes-Vidal

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.

The digestive adaptation of flying vertebrates: High intestinal paracellular absorption compensates for smaller guts

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.

Dietary modulation of intestinal enzymes of the house sparrow (Passer domesticus): testing an adaptive hypothesis

Insectivorous/frugivorous passerine species studied so far lack the ability to modulate intestinal maltase activity, in contrast to galliformes. We tested for dietary modulation of small intestine (SI) enzymes including maltase in house sparrows to understand whether the difference between the galliformes on the one hand, and the passerines on the other, reflects a phylogenetic pattern (maltase modulated in galliformes but not passerines), a dietary pattern (maltase modulated in granivores but not insectivore/frugivores), some other pattern, or chance. We also tested the prediction that intestinal peptidase activity would be increased on a high protein (HP) diet. Birds were fed three diets high in starch, protein, or lipid for 10 days. For birds on the HP diet (60.3% protein) we observed the predicted upward modulation of aminopeptidase-N activity, as compared with the lower-protein, high starch (HS) (12.8% protein) diet. In contrast, birds eating the HS diet had similar maltase and sucrase activities, and only slightly higher isomaltase activity, compared with birds eating the high protein (HP), starch-free diet. Birds eating high lipid (HL) diet had low activities of both carbohydrases and peptidase. Considering that the statistical power of our tests was adequate, we conclude that house sparrows show little or no increase in carbohydrases in response to elevated dietary carbohydrate. We cannot reject the hypothesis that maltase lability among avian species has a phylogenetic component, or that high dietary fat has a depressing effect on both carbohydrase and peptidase activities.

Paracellular Absorption: A Bat Breaks the Mammal Paradigm

Bats tend to have less intestinal tissue than comparably sized nonflying mammals. The corresponding reduction in intestinal volume and hence mass of digesta carried is advantageous because the costs of flight increase with load carried and because take-off and maneuverability are diminished at heavier masses. Water soluble compounds, such as glucose and amino acids, are absorbed in the small intestine mainly via two pathways, the transporter-mediated transcellular and the passive, paracellular pathways. Using the microchiropteran bat Artibeus literatus (mean mass 80.6±3.7 g), we tested the predictions that absorption of water-soluble compounds that are not actively transported would be extensive as a compensatory mechanism for relatively less intestinal tissue, and would decline with increasing molecular mass in accord with sieve-like paracellular absorption. Using a standard pharmacokinetic technique, we fed, or injected intraperitonealy the metabolically inert carbohydrates L-rhamnose (molecular mass = 164 Da) and cellobiose (molecular mass = 342 Da) which are absorbed only by paracellular transport, and 3-O-methyl-D-glucose (3OMD-glucose) which is absorbed via both mediated (active) and paracellular transport. As predicted, the bioavailability of paracellular probes declined with increasing molecular mass (rhamnose, 90±11%; cellobiose, 10±3%, n = 8) and was significantly higher in bats than has been reported for laboratory rats and other mammals. In addition, absorption of 3OMD-glucose was high (96±11%). We estimated that the bats rely on passive, paracellular absorption for more than 70% of their total glucose absorption, much more than in non-flying mammals. Although possibly compensating for less intestinal tissue, a high intestinal permeability that permits passive absorption might be less selective than a carrier-mediated system for nutrient absorption and might permit toxins to be absorbed from plant and animal material in the intestinal lumen.

Kidney Mass and Relative Medullary Thickness of Rodents in Relation to Habitat, Body Size, and Phylogeny

We tested the hypotheses that relative medullary thickness (RMT) and kidney mass are positively related to habitat aridity in rodents, after controlling for correlations with body mass. Body mass, mass‐corrected kidney mass, mass‐corrected RMT, mass‐corrected maximum urine concentration, and habitat (scored on a semiquantitative scale of 1–4 to indicate increasing aridity) all showed statistically significant phylogenetic signal. Body mass varied significantly among habitats, with the main difference being that aquatic species are larger than those from other habitats. Mass‐corrected RMT and urine concentration showed a significant positive correlation (N = 38; conventional r = 0.649, phylogenetically independent contrasts [IC] r = 0.685), thus validating RMT as a comparative index of urine concentrating ability. RMT scaled with body mass to an exponent significantly less than 0 (N = 141 species; conventional allometric slope = −0.145 [95% confidence interval (CI) = −0.172, −0.117], IC allometric slope = −0.132 [95% CI = −0.180, −0.083]). Kidney mass scaled to an exponent significantly less than unity (N = 104 species; conventional slope = 0.809 [95% CI = 0.751, 0.868], IC slope = 0.773 [95% CI = 0.676, 0.871]). Both conventional and phylogenetic analysis indicated that RMT varied among habitats, with rodents from arid areas having the largest values of RMT. A phylogenetic analysis indicated that mass‐corrected kidney mass was positively related to habitat aridity.

The integration of digestion and osmoregulation in the avian gut.

We review digestion and osmoregulation in the avian gut, with an emphasis on the ways these different functions might interact to support or constrain each other and the ways they support the functioning of the whole animal in its natural environment. Differences between birds and other vertebrates are highlighted because these differences may make birds excellent models for study and may suggest interesting directions for future research. At a given body size birds, compared with mammals, tend to eat more food but have less small intestine and retain food in their gastrointestinal tract (GIT) for shorter periods of time, despite generally higher mass‐specific energy demands. On most foods, however, they are not less efficient at digestion, which begs the question how they compensate. Intestinal tissue‐specific rates of enzymatic breakdown of substrates and rates of active transport do not appear higher in birds than in mammals, nor is there a demonstrated difference in the extent to which those rates can be modulated during acclimation to different feeding regimes (e.g. diet, relative intake level). One compensation appears to be more extensive reliance on passive nutrient absorption by the paracellular pathway, because the avian species studied so far exceed the mammalian species by a factor of at least two‐ to threefold in this regard. Undigested residues reach the hindgut, but there is little evidence that most wild birds recover microbial metabolites of nutritional significance (essential amino acids and vitamins) by re‐ingestion of faeces, in contrast to many hindgut fermenting mammals and possibly poultry. In birds, there is some evidence for hindgut capacity to breakdown either microbial protein or protein that escapes the small intestine intact, freeing up essential amino acids, and there is considerable evidence for an amino acid absorptive capacity in the hindgut of both avian and mammalian hindgut fermenters. Birds, unlike mammals, do not excrete hyperosmotic urine (i.e. more than five times plasma osmotic concentration). Urine is mixed with digesta rather than directly eliminated, and so the avian gut plays a relatively more important role in water and salt regulation than in mammals. Responses to dehydration and high‐ and low‐salt loads are reviewed. Intestinal absorption of ingested water is modulated to help achieve water balance in one species studied (a nectar‐feeding sunbird), the first demonstration of this in any terrestrial vertebrate. In many wild avian species the size and digestive capacity of the GIT is increased or decreased by as much as 50% in response to nutritional challenges such as hyperphagia, food restriction or fasting. The coincident impacts of these changes on osmoregulatory or immune function of the gut are poorly understood.

Developmental Changes in Digestive Physiology of Nestling House Sparrows, Passer domesticus

Six decades of studies have speculated that digestive capacity might limit avian growth rate or that developmental changes in the gut might determine developmental changes in digestive efficiency. However, there are no studies on digestive enzymes during avian development, except for studies on mainly domestic birds that exhibit the precocial mode of development. We studied alimentary organ masses, intestinal enzyme activities (sucrase, maltase, isomaltase, aminopeptidase‐N), and pancreatic enzyme activities (amylase, trypsin, chymotrypsin) during development of a wild passerine bird exhibiting the altricial mode of development. Wild nestling house sparrows were studied immediately after removal from the nest (days 0, 3, 6 of age; day \documentclass{aastex} \usepackage{amsbsy} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{bm} \usepackage{mathrsfs} \usepackage{pifont} \usepackage{stmaryrd} \usepackage{textcomp} \usepackage{portland,xspace} \usepackage{amsmath,amsxtra} \usepackage[OT2,OT1]{fontenc} \newcommand\cyr{ \renewcommand\rmdefault{wncyr} \renewcommand\sfdefault{wncyss} \renewcommand\encodingdefault{OT2} \normalfont \selectfont} \DeclareTextFontCommand{\textcyr}{\cyr} \pagestyle{empty} \DeclareMathSizes{10}{9}{7}{6} \begin{document} \landscape

Developmental adjustments of house sparrow (Passer domesticus) nestlings to diet composition.

0=\mathrm{hatch}\,