Todd J. McWhorter

Does Gut Function Limit Hummingbird Food Intake

Many nectar‐feeding bird species decrease food intake when sugar concentration in food is increased. This feeding response can be explained by two alternative hypotheses: compensatory feeding and physiological constraint. The compensatory feeding hypothesis predicts that if birds vary intake to maintain a constant energy intake to match energy expenditures, then they should increase intake when expenditures are increased. Broad‐tailed hummingbirds were presented with sucrose solutions at four concentrations (292, 584, 876, and 1,168 mmol L−1) and exposed to two environmental temperatures (10° and 22°C). Birds decreased volumetric food intake in response to sugar concentration. However, when they were exposed to a relatively sudden drop in environmental temperature and, hence, to an acute increase in thermoregulatory energy expenditures, they did not increase their rate of energy consumption and lost mass. These results support the existence of a physiological constraint on feeding intake. A simple chemical reactor model based on intestinal morphology and in vitro measurements of sucrose hydrolysis predicted observed intake rates closely. This model suggests that intestinal sucrose hydrolysis rates were near maximal and, thus, may have imposed limits to sugar assimilation. Although sugar assimilation was high (95%), the proportions of excreted sucrose, glucose, and fructose found in excreta differed significantly. The monosaccharides glucose and fructose were about eight and three times more abundant than sucrose, respectively. Broad‐tailed hummingbirds are small high‐altitude endotherms that face unpredictable weather and the energetic expense of premigratory fattening. Digestive processes have the potential to impose severe challenges to their energy budgets.

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.

Integrating landscape ecology and conservation physiology

The need to understand how anthropogenic landscape alteration affects fauna populations has never been more pressing. The importance of developing an understanding of the processes behind local extinction is widely acknowledged, but inference from spatial patterns of fauna distribution continues to dominate. However, this approach is limited in its ability to generate strong predictions about future distributions and local extinctions, especially when population-level responses to landscape alteration are subject to long time lags. We review the potential for indices of physiological stress and condition to contribute to understanding of how landscape pattern affects species persistence. Such measures can indicate habitat quality from the perspective of the individual animal, and can reveal environmental stressors before their negative consequences begin to manifest at a population level. Spatial patterns of chronic stress may therefore yield valuable insight into how landscape alteration influences species. We propose that the emerging disciplines of conservation physiology and macrophysiology have much to offer spatial ecology, and have great potential to reveal the physiological pathways through which habitat alteration affects fauna populations and their persistence in fragmented landscapes.

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.

Hummingbirds rely on both paracellular and carrier-mediated intestinal glucose absorption to fuel high metabolism

Twenty years ago, the highest active glucose transport rate and lowest passive glucose permeability in vertebrates were reported in Rufous and Annas hummingbirds (Selasphorus rufus, Calypte anna). These first measurements of intestinal nutrient absorption in nectarivores provided an unprecedented physiological foundation for understanding their foraging ecology. They showed that physiological processes are determinants of feeding behaviour. The conclusion that active, mediated transport accounts for essentially all glucose absorption in hummingbirds influenced two decades of subsequent research on the digestive physiology and nutritional ecology of nectarivores. Here, we report new findings demonstrating that the passive permeability of hummingbird intestines to glucose is much higher than previously reported, suggesting that not all sugar uptake is mediated. Even while possessing the highest active glucose transport rates measured in vertebrates, hummingbirds must rely partially on passive non-mediated intestinal nutrient absorption to meet their high mass-specific metabolic demands.

Absorption of sugars in the Egyptian fruit bat (Rousettus aegyptiacus): a paradox explained

SUMMARY Two decades ago D. J. Keegan reported results on Egyptian fruit bats (Rousettus aegyptiacus, Megachiroptera) that were strangely at odds with the prevailing understanding of how glucose is absorbed in the mammalian intestine. Keegans in vitro tests for glucose transport against a concentration gradient and with phloridzin inhibition in fruit bat intestine were all negative, although he used several different tissue preparations and had positive control results with laboratory rats. Because glucose absorption by fruit bats is nonetheless efficient, Keegan postulated that the rapid glucose absorption from the fruit bat intestine is not through the enterocytes, but must occur via spaces between the cells. Thus, we hypothesized that absorption of water-soluble compounds that are not actively transported would be extensive in these bats, and would decline with increasing molecular mass in accord with sieve-like paracellular absorption. We did not presume from Keegans studies that there is no Na+-coupled, mediated sugar transport in these bats, and our study was not designed to rule it out, but rather to quantify the level of possible non-mediated 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 by paracellular uptake, and 3-O-methyl-d-glucose (3OMd-glucose), a d-glucose analog that is absorbed via both mediated (active) and paracellular uptake. As predicted, the bioavailability of paracellular probes declined with increasing molecular mass (rhamnose, 62±4%; cellobiose, 22±4%) and was significantly higher in bats than has been reported for rats and other mammals. In addition, fractional absorption of 3OMd-glucose was high (91±2%). We estimated that Egyptian fruit bats rely on passive, paracellular absorption for the majority of their glucose absorption (at least 55% of 3OMd-glucose absorption), much more than in non-flying mammals.

Modulation of ingested water absorption by Palestine sunbirds: evidence for adaptive regulation

SUMMARY Nectarivorous birds feed on dilute sugar solutions containing trace amounts of amino acids and electrolytes. To meet their high mass-specific energy demands they must often deal with exceptionally high proportionate water fluxes. Despite nectar intake rates that may reach more than five times body mass per day, hummingbirds appear to absorb all ingested water. Here, we report the results of experiments designed to examine the relationship between nectar intake and water turnover in nectar-feeding Palestine sunbirds (Nectarinia osea). Like hummingbirds, sunbirds ingested large amounts of water. At the lowest sucrose concentration (292 mmol l-1), food intake rates reached 2.2 times body mass. Fractional and total water turnover increased linearly with water ingestion, but the fraction of ingested water absorbed by sunbirds decreased from 100% to 36% with increasing water intake rate. Palestine sunbirds may therefore avoid absorbing, and thus having to eliminate, up to 64% of their ingested water load when feeding on dilute nectars. To our knowledge, this is the first documentation of regulation of water flux across the gastrointestinal tract to the body. Our data suggest that sunbirds regulate transepithelial water flux independently of sugar absorption. These intriguing results open the door to many questions about how water transport is regulated in the vertebrate gastrointestinal tract. We suggest that intestinal water and body water form two separate but interacting pools in nectar-feeding birds. Convergence in diet has led to the evolution of many similar traits in hummingbirds and sunbirds. The physiological traits of these two groups that allow the processing of a water and sugar diet, however, may be very different.

Mechanistic bases for differences in passive absorption

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.

Renal function in Palestine sunbirds: elimination of excess water does not constrain energy intake.

SUMMARY Although the renal responses of birds to dehydration have received significant attention, the consequences of ingesting and processing large quantities of water have been less studied. Nectar-feeding birds must often deal with exceptionally high water intake rates in order to meet their high mass-specific energy demands. Birds that ingest large volumes of water may either eliminate excess water in the kidney or regulate the volume of water absorbed in the gastrointestinal tract. Because water absorption in the gastrointestinal tract of Palestine sunbirds (Nectarinia osea) decreases with increasing water ingestion rate, we predicted that glomerular filtration rate (GFR) in these birds would not be unusually high in spite of large ingested water loads. When feeding on dilute sucrose solutions, sunbirds ingested between 4 and 6 times their body mass in nectar per day, yet they were able to compensate for varying nectar energy density and increased thermoregulatory energy demands with no apparent difficulty. GFR was lower than predicted (1976.22±91.95 μl h-1), and was not exceptionally sensitive to water loading. Plasma glucose concentrations were high, and varied 1.8-fold between fasted (16.08± 0.75 mmol l-1) and fed (28.18±0.68 mmol l-1) sunbirds, but because GFR was low, glucose filtered load also remained relatively low. Essentially the entire glucose filtered load (98%) was recovered by the kidney. Renal fractional water reabsorption (FWR) decreased from 0.98 to 0.64 with increasing water intake. The ability of Palestine sunbirds to reduce the absorption of ingested water in the gastrointestinal tract may resolve the potential conflict between filtering a large excess of absorbed water in the kidney and simultaneously retaining filtered metabolites.

The integration of diet, physiology, and ecology of nectar-feeding birds

El balance entre la adquisicion y el uso de energia es critico para la reproduccion y sobrevivencia. Los presupuestos energeticos de los organismos pueden estar limitados tanto por factores ambientales como por su fisiologia. Estas restricciones pueden ser especialmente importantes para pequenos endotermos como los colibries (picaflores) que tienen costos energeticos altos por unidad de masa. Muchas especies de aves nectarivoras reducen el consumo de alimento cuando la concentracion de azucar aumenta. Esta respuesta puede ser explicada por dos hipotesis alternativas: compensacion alimenticia y restricciones fisiologicas. La primera hipotesis predice que las aves varian el consumo para mantener la ingesta de alimento ajustada a sus gastos energeticos. Por ende, cuando los gastos energeticos aumentan, el consumo debe aumentar. Colibries vibradores (Selasphorus platycercus) y picaflores (Sephanoides sephaniodes) fueron alimentados con dietas de contenido energetico variable y expuestos a varias temperaturas ambientales. Las aves redujeron el volumen consumido en respuesta a un incremento en la concentracion de azucar. Sin embargo, cuando fueron expuestos a bajas temperaturas, y por lo tanto a mayores demandas de termoregulacion, no aumentaron su consumo de energia y perdieron masa corporal. Estos resultados indican la existencia de una limitante fisiologia que restringe a los presupuestos energeticos de los colibries. Limitaciones funcionales (digestivas o perifericas) pueden imponer serios dilemas para los presupuestos de energia de estos pequenos endotermos y por lo tanto jugar un papel significativo en su distribucion, ecologia, e historia natural.