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 intraperitoneally 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.     

Morphological bases for intestinal paracellular absorption in bats and rodents

Flying mammals present unique intestinal adaptations, such as lower intestinal surface area than nonflying mammals, and they compensate for this with higher paracellular absorption of glucose. There is no consensus about the mechanistic bases for this physiological phenomenon. The surface area of the small intestine is a key determinant of the absorptive capacity by both the transcellular and the paracellular pathways; thus, information about intestinal surface area and micro-anatomical structure can help explain differences among species in absorptive capacity. In order to elucidate a possible mechanism for the high paracellular nutrient absorption in bats, we performed a comparative analysis of intestinal villi architecture and enterocyte size and number in microchiropterans and rodents. We collected data from intestines of six bat species and five rodent species using hematoxylin and eosin staining and histological measurements. For the analysis we added measurements from published studies employing similar methodology, making in total a comparison of nine species each of rodents and bats. Bats presented shorter intestines than rodents. After correction for body size differences, bats had ~41% less nominal surface area (NSA) than rodents. Villous enhancement of surface area (SEF) was ~64% greater in bats than in rodents, mainly because of longer villi and a greater density of villi in bat intestines. Both taxa exhibited similar enterocyte diameter. Bats exceeded rodents by ~103% in enterocyte density per cm² NSA, but they do not significantly differ in total number of enterocytes per whole animal. In addition, there is a correlation between SEF and clearance per cm² NSA of L-arabinose, a nonactively transported paracellular probe. We infer that an increased enterocyte density per cm² NSA corresponds to increased density of tight junctions per cm² NSA, which provides a partial mechanistic explanation for understanding the high paracellular absorption observed in bats compared to nonflying mammals.     

Paracellular Absorption Is Relatively Low in the Herbivorous Egyptian Spiny-Tailed Lizard,Uromastyx aegyptia

Absorption of small water-soluble nutrients in vertebrate intestines occurs both by specific, mediated transport and by non-specific, passive, paracellular transport. Although it is apparent that paracellular absorption represents a significant route for nutrient absorption in many birds and mammals, especially small, flying species, its importance in ectothermic vertebrates has not previously been explored. Therefore, we measured fractional absorption (ƒ) and absorption rate of three paracellular probes (arabinose, l-rhamnose, cellobiose) and of 3-O-methyl d-glucose (absorbed by both mediated and paracellular pathways) by the large herbivorous lizard, Uromastyx aegyptia, to explore the relative importance of paracellular and mediated transport in an ectothermic, terrestrial vertebrate. Fractional absorption of 3-O-methyl d-glucose was high (ƒ = 0.73±0.04) and similar to other vertebrates; ƒ of the paracellular probes was relatively low (arabinose ƒ = 0.31±0.03, l-rhamnose ƒ = 0.19±0.02, and cellobiose ƒ = 0.14±0.02), and decreased with molecular mass, a pattern consistent with other vertebrates. Paracellular absorption accounted for approximately 24% of total 3-O-methyl d-glucose uptake, indicating low reliance on this pathway for these herbivorous lizards, a pattern similar to that found in other terrestrial vertebrates, and different from small flying endotherms (both birds and bats).     

A Comparison of mucosal surface area and villous histology in small intestines of the Brazilian free‐tailed bat (Tadarida brasiliensis) and the mouse (Mus musculus)

Studies on birds have led to the hypothesis that increased intestinal absorption between enterocytes (paracellular) evolved as a compensation for smaller intestinal size in fliers, which was perhaps selected to minimize the mass of digesta carried. This hypothesis predicts that bats will also exhibit relatively reduced intestinal size and high paracellular absorption, compared with nonflying mammals. Published studies on three bat species indicate relatively high paracellular absorption. One mechanism for increasing paracellular absorption per cm² small intestine (SI) is increased number of tight junctions (TJs) across which paracellular absorption occurs. To our knowledge, we provide the first comparative analysis of enterocyte size and number in flying and nonflying mammals. Intestines of insectivorous bats Tadarida brasiliensis were compared with Mus musculus using hematoxylin and eosin staining method. Bats had shorter and narrower SIs than mice, and after correction for body size difference by normalizing to mass^3/4, the bats had 40% less nominal surface area than the mouse, as predicted. Villous enhancement of surface area was 90% greater in the bat than in the mouse, mainly because of longer villi and a greater density of villi in bat intestines. Bat and mouse were similar in enterocyte diameter. Bats exceeded mice by 54.4% in villous area per cm length SI and by 95% in number of enterocytes per cm² of the nominal surface area of the SI. Therefore, an increased density of TJs per cm² SI may be a mechanistic explanation that helps to understand the high paracellular absorption observed in bats compared to nonflying mammals. J. Morphol. 276:102–108, 2015. © 2014 Wiley Periodicals, Inc.     

Digestive Efficiency Mediated by Serum Calcium Predicts Bone Mineral Density in the Common Marmoset (Callithrix jacchus)

Two health problems have plagued captive common marmoset (Callithrix jacchus) colonies for nearly as long as those colonies have existed: marmoset wasting syndrome and metabolic bone disease. While marmoset wasting syndrome is explicitly linked to nutrient malabsorption, we propose metabolic bone disease is also linked to nutrient malabsorption, although indirectly. If animals experience negative nutrient balance chronically, critical nutrients may be taken from mineral stores such as the skeleton, thus leaving those stores depleted. We indirectly tested this prediction through an initial investigation of digestive efficiency, as measured by apparent energy digestibility, and serum parameters known to play a part in metabolic bone mineral density of captive common marmoset monkeys. In our initial study on 12 clinically healthy animals, we found a wide range of digestive efficiencies, and subjects with lower digestive efficiency had lower serum vitamin D despite having higher food intakes. A second experiment on 23 subjects including several with suspected bone disease was undertaken to measure digestive and serum parameters, with the addition of a measure of bone mineral density by dual‐energy X‐ray absorptiometry (DEXA). Bone mineral density was positively associated with apparent digestibility of energy, vitamin D, and serum calcium. Further, digestive efficiency was found to predict bone mineral density when mediated by serum calcium. These data indicate that a poor ability to digest and absorb nutrients leads to calcium and vitamin D insufficiency. Vitamin D absorption may be particularly critical for indoor‐housed animals, as opposed to animals in a more natural setting, because vitamin D that would otherwise be synthesized via exposure to sunlight must be absorbed from their diet. If malabsorption persists, metabolic bone disease is a possible consequence in common marmosets. These findings support our hypothesis that both wasting syndrome and metabolic bone disease in captive common marmosets are consequences of inefficient nutrient absorption. Am. J. Primatol. 75:153‐160, 2013. © 2012 Wiley Periodicals, Inc.     

L-glucose absorption in house sparrows (<Emphasis Type="Italic">Passer domesticus</Emphasis>) is nonmediated

We previously demonstrated in intact house sparrows substantial absorption in vivo of L-glucose, the stereoisomer of D-glucose that is assumed not to interact with the intestines D-glucose transporter. Results of some studies challenge this assumption for other species. Therefore, we tested it in vitro and in vivo, based on the principle that if absorption of a compound (L-glucose) is mediated, then absorption of its tracer will be competitively inhibited by high concentrations of either the compound itself or other compounds (e.g., D-glucose) whose absorption is mediated by the same mechanism. An alternative hypothesis that L-glucose absorption is primarily paracellular predicts that its absorption in vivo will be increased (not decreased) in the presence of D-glucose, because the permeability of this pathway is supposedly enhanced when Na⁺-coupled glucose absorption occurs. First, using intact tissue in vitro, we found that uptake of tracer-radiolabeled L-glucose was not significantly inhibited by high concentrations (100 mM) of either L-glucose or 3-O-methyl-D-glucose, a non-metabolizable but actively transported D-glucose analogue. Second, using intact house sparrows, we found that fractional absorption of the L-glucose tracer was significantly increased, not reduced, when gavaged along with 200 mM 3-O-methyl-D-glucose. This result was confirmed in another experiment where L-glucose fractional absorption was significantly higher in the presence vs. absence of food in the gut. The greater absorption was apparently not due simply to longer retention time of digesta, because no significant difference was found among retention times. Our results are consistent with the idea that L-glucose is absorbed in a non-mediated fashion, largely via the paracellular pathway in vivo.Abbreviations AUC area under the curve - 3OMD-glucose 3-O-methyl-D-glucose Communicated by I.D. Hume     

Allometry of paracellular absorption in birds

Water-soluble nutrients can be absorbed across the intestinal epithelium by transcellular and paracellular processes. Recent studies suggest that small birds (<180 g) have more extensive paracellular absorption of glucose than nonflying mammals. This may be a feature that compensates for a reduced small intestine size because small birds have smaller mass-corrected intestinal length than do nonflying mammals, but the difference diminishes in larger birds. We hypothesized that if this explanation were correct, there would be a negative correlation between paracellular absorption and body mass in birds and that larger birds would have paracellular absorption comparable to that of nonflying mammals. We tested this hypothesis, using consistent methodology, by measuring the extent of absorption of a series of inert carbohydrate probes in heavier bird species (>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.     

Differences among captive callitrichids in the digestive responses to dietary gum

Although many members of the Callitrichidae, a monophyletic family of small, New World monkeys, have been observed to feed on plant exudates, available field data support the generalization that pygmy and common marmosets (Cebuella pygmaea and Callithrix jacchus) feed on gums to a greater extent than most other callitrichids. Because microbial fermentation is required for vertebrates to digest gums, gum-feeding primates may react differently to dietary gum from their relatives that eat little gum. To test this hypothesis, digestion trials were conducted on animals from the two marmoset species, two tamarin species (Saguinus fuscicollis and S. oedipus), and a species of lion tamarin (Leontopithecus rosalia). These species span the range of body sizes within the Callitrichidae. All animals were fed two variations of a homogeneous diet, which differed only in that gum arabic was added to one. Transit time of digesta (TFA) and digestive efficiency (as measured by the coefficients of apparent digestibility of dry matter and energy [ADDM and ADE, respectively]) were compared between diets for each individual. As predicted, the digestive responses of marmosets differed from the responses of the other study species. In marmosets, TFA tended to be longer when gum was added to the diet, while TFA did not change in the other three species. Digestive efficiency decreased in tamarins and lion tamarins with the addition of gum to the diet; marmoset digestive efficiency was unaffected by diet. The results of this research are consistent with the hypothesis that marmosets have digestive adaptations that aid in the digestion of gum that other callitrichids lack. © 1996 Wiley-Liss, Inc.     

Capacity for absorption of water-soluble secondary metabolites greater in birds than in rodents

Plant secondary metabolites (SMs) are pervasive in animal foods and potentially influence feeding behavior, interspecies interactions, and the distribution and abundance of animals. Some of the major classes of naturally occurring SMs in plants include many water-soluble compounds in the molecular size range that could cross the intestinal epithelium via the paracellular space by diffusion or solvent drag. There are differences among species in paracellular permeability. Using Middle Eastern rodent and avian consumers of fruits containing SMs, we tested the hypothesis that avian species would have significantly higher paracellular permeability than rodent species. Permeability in intact animals was assessed using standard pharmacological methodology to measure absorption of two radiolabeled, inert, neutral water-soluble probes that do not interact with intestinal nutrient transporters, L-arabinose (M_r = 150.1 Da) and lactulose (M_r = 342.3 Da). We also measured absorption of labeled 3-O-methyl-D-glucose (3OMD-glucose; M_r = 194.2 Da), which is a nonmetabolized analogue of D-glucose that is passively absorbed through the paracellular space but also transported across the enterocyte membranes. Most glucose was absorbed by all species, but arabinose fractional absorption (f) was nearly three times higher in birds (1.03±0.17, n = 15 in two species) compared to rodents (0.37±0.06, n = 10 in two species) (P<0.001). Surprisingly, the apparent rates of absorption in birds of arabinose exceeded those of 3OMD-glucose. Our findings are in agreement with previous work showing that the paracellular pathway is more prominent in birds relative to nonflying mammals, and suggests that birds may be challenged by greater absorption of water-soluble, dietary SMs. The increased expression of the paracellular pathway in birds hints at a tradeoff: the free energy birds gain by absorbing water-soluble nutrients passively may be offset by the metabolic demands placed on them to eliminate concomitantly absorbed SMs.     

How do food passage rate and assimilation differ between herbivorous lizards and nonruminant mammals?

Summary What digestive adaptations permit herbivorous nonruminant mammals to sustain much higher metabolic rates than herbivorous lizards, despite gross similarity in digestive anatomy and physiology? We approached this question by comparing four herbivorous species eating the same diet of alfalfa pellets: two lizards (chuckwalla and desert iugana) and two mammals (desert woodrat and laboratory mouse). The mammals had longer small and large intestines, greater intestinal surface area, much higher (by an order of magnitude) food intake normalized to metabolic live mass, and much faster food passage times (a few hours instead of a few days). Among both reptiles and mammals, passage times increase with body size and are longer for herbivores than for carnivores. The herbivorous lizards, despite these much slower passage times, had slightly lower apparent digestive efficiencies than the mammals. At least for chuckwallas, this difference from mammals was not due to differences in body temperature regime. Comparisons of chuckwallas and woodrats in their assimilation of various dietary components showed that the woodrat's main advantage lay in greater assimilation of the dietary fiber fraction. Woodrats achieved greater fiber digestion despite shorter residence time, but possibly because of a larger fermentation chamber, coprophagy, and/or different conditions for microbial fermentation. We conclude with a comparative overview of digestive function in herbivorous lizards and mammals, and with a list of four major unsolved questions.     

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.     

The sweet life: diet sugar concentration influences paracellular glucose absorption

Small birds and bats face strong selection pressure to digest food rapidly in order to reduce digesta mass carried during flight. One mechanism is rapid absorption of a high proportion of glucose via the paracellular pathway (transfer between epithelial cells, not mediated by transporter proteins). Intestinal paracellular permeability to glucose was assessed for two nectarivorous passerines, the Australian New Holland honeyeater (Phylidonyris novaehollandiae) and African white-bellied sunbird (Cinnyris talatala) by measuring the bioavailability of radiolabelled, passively absorbed l -glucose. Bioavailability was high in both species and increased with diet sugar concentration (honeyeaters, 37 and 81% and sunbirds, 53 and 71% for 250 and 1000mmoll-1 sucrose diets, respectively). We conclude that the relative contribution of paracellular to total glucose absorption increases with greater digesta retention time in the intestine, and paracellular absorption may also be modulated by factors such as intestinal lumen osmolality and interaction with mediated glucose uptake. The dynamic state of paracellular absorption should be taken into account in future studies.     

Hooks for mammal pollination?

Summary Two species of Banksia (family Proteaceae) studied in Australia were shown to be pollinated by small, non-flying mammals rather than by birds as previously thought, and to possess several adaptations appropriate for mammal-rather than bird-pollination: odor, troughs that channel excess nectar to the ground for attraction, open inflorescence structure for nectar accessibility, hooked wiry styles for effective pollen transfer, crepuscular and nocturnal nectar and pollen presentation, and copious nectar. This apparently is the first documentation with quantified data of pollination by non-flying mammals, although many other probable examples exist.     

Intestinal passive absorption of water-soluble compounds by sparrows: effect of molecular size and luminal nutrients

We tested predictions that: (1) absorption of water-soluble probes decreases with increasing molecular size, consistent with movement through effective pores in epithelia, and (2) absorption of probes is enhanced when measured in the presence of luminal nutrients, as predicted for paracellular solvent drag. Probes (L-arabinose, L-rhamnose, perseitol, lactulose; MW 150.1-342.3 Da) were gavaged in nonanesthetized House sparrows ( Passer domesticus), or injected into the pectoralis, and serially measured in plasma. Bioavailability was calculated as F=AUC by gavage/AUC by injection, where AUC is the area under the curve of plasma probe concentration vs. time. Consistent with predictions, F declined with probe size by 75% from the smallest to the largest probe, and absorption of probes increased by 40% in the presence of luminal glucose or food compared to a mannitol control. Absorption of water-soluble probes by sparrows is much higher than in humans, which is much higher than in rats. These differences seem mainly attributable to differences in paracellular solvent flux and less to differences in effective paracellular pore size.     

Paracellular absorption in laboratory mice: Molecule size-dependent but low capacity

Water-soluble nutrients are absorbed by the small intestine via transcellular and paracellular processes. The capacity for paracellular absorption seems lower in nonfliers than in fliers, although that conclusion rests largely on a comparison of relatively larger nonflying mammals (> 155 g) and relatively smaller flying birds (< 155 g). We report on paracellular absorption in laboratory mice, the smallest nonflying mammal species studied to date. Using a standard pharmacokinetic technique, we measured the extent of absorption (fractional absorption = f) of inert carbohydrate probes: l-arabinose (M_r = 150.13 Da) and cellobiose (342.3) that are absorbed exclusively by the paracellular route, and 3-O-methyl d-glucose (3OMD-glucose) (M_r = 194) absorbed both paracellularly and transcellularly. f was measured accurately in urine collection trials of 5–10 h duration. Absorption of 3OMD-glucose by mice was essentially complete (f = 0.95 ± 0.07) and much higher than that for l-arabinose (f = 0.21 ± 0.02), indicating that in mice, like other nonflying mammals, > 80% of glucose is absorbed by mediated process(es) rather than the passive, paracellular route. As in all other vertebrates, absorption of cellobiose (f = 0.13 ± 0.02) was even lower than that for l-arabinose, suggesting an equivalent molecular size cut-off for flying and nonflying animals and thus a comparable effective TJ aperture. An important ecological implication is that smaller water-soluble plant secondary metabolites that have been shown to be absorbed by the paracellular path in cell culture, such as phenolics and alkaloids, might be absorbed in substantial amounts by bats and small birds relative to nonflying mammals such as mice.     

The capacity for paracellular absorption in the insectivorous bat Tadarida brasiliensis

Water-soluble nutrients are absorbed by the small intestine via transcellular and paracellular processes. The capacity for paracellular absorption seems greater in fliers than in nonfliers, although that conclusion rests mainly on a comparison of flying birds and nonflying mammals because only two frugivorous bat species have been studied. Furthermore, the bats studied so far were relatively large (>85 g, compared with most bat species which are <20 g) and were not insectivores (like about 70 % of bat species). We studied the small (11 g) insectivorous bat Tadarida brasiliensis and tested the prediction that the capacity for paracellular absorption would be as high as in the other bat and avian species studied so far, well above that in terrestrial, nonflying mammals. Using standard pharmacokinetic technique, we measured the extent of absorption (fractional absorption = f) of inert carbohydrate probes: L-arabinose (MM = 150.13) absorbed exclusively by paracellular route and 3OMD-glucose (MM = 194) absorbed both paracellularly and transcellularly. As predicted, the capacity of paracellular absorption in this insectivorous bat was high (L-arabinose f = 1.03 ± 0.14) as in other frugivorous bats and small birds. Absorption of 3OMD-glucose was also complete (f = 1.09 ± 0.17), but >80 % was accounted for by paracellular absorption. We conclude that passive paracellular absorption of molecules of the size of amino acids and glucose is extensive in this bat and, generally in bats, significantly higher than that in nonflying mammals, although the exact extent can be somewhat lower or higher depending on molecule size, polarity and charge.     

The impact of a run-of-the-river hydroelectric dam on a non-volant small-mammal assemblage in Brazilian Amazonia

There are few scientific studies evaluating the impact of the loss of wetlands on the banks of tropical rivers on assemblages of small non-flying mammals. To understand the possible deleterious effects of hydroelectric construction in tropical forests on this group of mammals, we used data from 2 years of monitoring carried out during the period before the filling of a hydroelectric plant reservoir in the Brazilian Amazon, and related them to vegetation, soil and topography. We captured 659 individuals of 20 small-mammal species. The species assemblage composition in the flooded areas was a subset of species that occurred in both floodable and non-floodable areas, and only one species was captured exclusively in the flooded area. Species composition was influenced by the proportion of sand, by soil nutrient concentration and distance from water bodies. We conclude that there is no evidence that the flooding of low-lying areas along the Madeira River would negatively affect the assemblage of non-flying small mammals in the short term because the remaining areas have similar assemblages of small mammals as those destined for flooding. Whether the area lost will be important for population dynamics will depend on the conservation of the remaining areas.     

The proximal airway of the bat Tadarida brasiliensis: a minimum entropy production design

The bronchial tree of most mammalian lungs is a good example of an efficient distribution system whose geometry and dimensions of branched structures are important factors in determining the efficiency of respiration. Small and flying endothermic animals have high-energy requirements, requiring morphological and physiological adaptations to reduce energy loss. Here we show that Tadarida brasiliensis, a nocturnal small bat whose energy requirements are exacerbated by this small size and by their frequent exposure to high altitude, has a different morphology in the proximal airway, sustained by a wider trachea and better scaling factors, than other non-flying mammals. This design allows a great decrease of the volume specific resistance of the proximal airway and in consequence a very low entropy production during breathing, approximately 1/18 of that expected for a non-flying mammals of similar body size.     

Experimental evidence for pollination of Banksia spp. by non-flying mammals

Summary The importance of non-flying mammals as pollinators of Banksia integrifolia and B. spinulosa was analysed by examining the effect of pollinator exclusions on fruit-set. Visitation by potential pollinators was also measured by observation and by indirect methods. Nonflying mammals were frequent visitors to inflorescences of both Banksia species. The aluminium sleeves used to exclude non-flying mammals from B. integrifolia trees were associated with a reduction in both the number of infructescences produced and the number of fruit per infructescence, indicating that non-flying mammals were important pollinators. Bird-nets over trees also significantly reduced the number of fruit per infructescence, but had no significant effect on the number of infructescences produced. The results of exclusion experiments using single inflorescences were inconclusive due to low fruitset. No conclusions could be drawn from these experiments with B. spinulosa. However, results for B. integrifolia support the conclusions of whole-tree experiments. Analysis of the genotype frequencies in seed from B. integrifolia provided no support for the hypothesis that the relatively limited mobility of non-flying mammal pollinators would cause inbreeding.     

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 Anna's 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.