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In absolute terms, flight is a highly energetically expensive form of locomotion. However, with respect to its cost per unit distance covered, powered flight is a very efficient mode of transport. Birds and bats are the only extant vertebrate taxa that have achieved flight. Phylogenetically different, they independently accomplished this elite mode of locomotion by employing diverse adaptive schemes and strategies. Integration of functional and structural parameters, a transaction that resulted in certain trade-offs and compromises, was used to overcome exacting constraints. Unique morphological, physiological and biochemical properties were initiated and refined to enhance the uptake, transfer and utilization of oxygen for high aerobic capacities. In bats, exquisite pulmonary structural parameters were combined with optimal haematological ones: a thin blood-gas barrier, a large pulmonary capillary blood volume and a remarkably extensive alveolar surface area in certain species developed in a remarkably large lung. These factors were augmented by, for example, exceptionally high venous haematocrits and haemoglobin concentrations. In birds, a particularly large respiratory surface area and a remarkably thin blood-gas (tissue) barrier developed in a small, rigid lung; a highly efficient cross-current system was fabricated within the parabronchi. The development of flight in only four animal taxa (among all the animal groups that have ever evolved; i.e. insects, the now-extinct pterosaurs, birds and bats) provides evidence for the enormous biophysical and energetic constraints that have stymied volancy. Bats improved a fundamentally mammalian lung to procure the large amounts of oxygen needed for flight. The lung/air sac system of birds is not therefore a prescriptive morphology for flight: the essence of its design can be found in the evolution of the reptilian lung, the immediate progenitor stock from which birds arose. The attainment of flight is a classic paradigm of the remarkable adaptability inherent in organismal and organic biology for countering selective pressures by initiating elegant morphologies and physiologies.

The extents of functional surfaces (villi, microvilli) have been estimated at different longitudinal sites, and in the entire small intestine, for three species of bats belonging to two feeding groups: insect- and fruit-eaters. In all species, surface areas and other structural quantities tended to be greatest at more cranial sites and to decline caudally. The entomophagous bat (Miniopterus inflatus) had a mean body mass (coefficient of variation) of 8.9 g (5%) and a mean intestinal length of 20 cm (6%). The surface area of the basic intestinal tube (primary mucosa) was 9.1 cm2 (10%) but this was amplified to 48 cm2 (13%) by villi and to 0.13 m2 (20%) by microvilli. The total number of microvilli per intestine was 4 x 10(11) (20%). The average microvillus had a diameter of 8 nm (10%), a length of 1.1 microns (22%) and a membrane surface area of 0.32 micron 2 (31%). In two species of fruit bats (Epomophorus wahlbergi and Lisonycteris angolensis), body masses were greater and intestines longer, the values being 76.0 g (18%) and 76.9 g (4%), and 73 cm (16%) and 72 cm (7%), respectively. Surface areas were also greater, amounting to 76 cm2 (26%) and 45 cm2 (8%) for the primary mucosa, 547 cm2 (29%) and 314 cm2 (16%) for villi and 2.7 m2 (23%) and 1.5 m2 (18%) for microvilli. An increase in the number of microvilli, 33 x 10(11) (19%) and 15 x 10(11) (24%) per intestine, contributed to the more extensive surface area but there were concomitant changes in the dimensions of microvilli. Mean diameters were 94 nm (8%) and 111 nm (4%), and mean lengths were 2.8 microns (12%) and 2.9 microns (10%), respectively. Thus, an increase in the surface area of the average microvillus to 0.83 micron 2 (12%) and 1.02 microns 2 (11%) also contributed to the greater total surface area of microvilli. The lifestyle-related differences in total microvillous surface areas persisted when structural quantities were normalised for the differences in body masses. The values for total microvillous surface area were 148 cm2g-1 (20%) in the entomophagous bat, 355 cm2g-1 (20%) in E. wahlbergi and 192 cm2g-1 (17%) in L. angolensis. This was true despite the fact that the insecteater possessed a greater length of intestine per unit of body mass: 22 mm g-1 (8%) versus 9-10 mm g-1 (9-10%) for the fruit-eaters.

A tissue sampling protocol has been devised for studying the functional surfaces of chiropteran small intestine and drawing comparisons within and between species. The goal was to obtain minimally biased stereological estimates of villous and microvillous surface areas and the numbers of microvilli. The approach is illustrated using the intestines of 3 bats (from frugivorous and entomophagous groups) and is based on the use of vertical sections and cycloid test arcs. A sampling scheme with 3 levels was employed. At level 1 (macroscopy), primary mucosal area was estimated from intestinal length and perimeter. Amplification factors due to villi were estimated at level 2 (light microscopy, LM) whilst microvillous amplifications were estimated at level 3 (transmission electron microscopy, TEM). The absolute surfaces, lengths and diameters of microvilli were used to calculate packing densities and absolute numbers. Estimated villous surface areas of the entire small intestine were 44.4 cm2 (Miniopterus inflatus, entomophagous), 410 cm2 (Epomophorus wahlbergi, frugivorous) and 237 cm2 (Lisonycteris angolensis, frugivorous). Corresponding microvillous surface areas were 0.11, 1.69 and 1.01 m2 whilst the numbers of microvilli per intestine were 4.5, 23.4 and 8.8 x 10(11). When normalised for body weights, microvillous surfaces were 122, 246 and 133 cm2/g respectively. The functional surfaces of the fruit bat appear to be more extensive than those of the entomophagous bat.

1. The lungs of four species of bats, Phyllostomus hastatus (PH, mean body mass, 98 g), Pteropus lylei (PL, 456 g), Pteropus alecto (PA, 667 g), and Pteropus poliocephalus (PP, 928 g) were analysed by morphometric methods. These data increase fivefold the range of body masses for which bat lung data are available, and allow more representative allometric equations to be formulated for bats. 2. Lung volume ranged from 4.9 cm3 for PH to 39 cm3 for PP. The volume density of the lung parenchyma (i.e. the volume proportion of the parenchyma in the lung) ranged from 94% in PP to 89% in PH. Of the components of the parenchyma, the alveoli composed 89% and the blood capillaries about 5%. 3. The surface area of the alveoli exceeded that of the blood-gas (tissue) barrier and that of the capillary endothelium whereas the surface area of the red blood cells as well as that of the capillary endothelium was greater than that of the tissue barrier. PH had the thinnest tissue barrier (0.1204 microns) and PP had the thickest (0.3033 microns). 4. The body mass specific volume of the lung, that of the volume of pulmonary capillary blood, the surface area of the blood-gas (tissue) barrier, the diffusing capacity of the tissue barrier, and the total morphometric pulmonary diffusing capacity in PH all substantially exceeded the corresponding values of the pteropid species (i.e. PL, PA and PP). This conforms with the smaller body mass and hence higher unit mass oxygen consumption of PH, a feature reflected in the functionally superior gas exchange performance of its lungs. 5. Morphometrically, the lungs of different species of bats exhibit remarkable differences which cannot always be correlated with body mass, mode of flight and phylogeny. Conclusive explanations of these pulmonary structural disparities in different species of bats must await additional physiological and flight biomechanical studies. 6. While the slope, the scaling factor (b), of the allometric equation fitted to bat lung volume data (b = 0.82) exceeds the value for flight VO2max (b = 0.70), those for the surface area of the blood-gas (tissue) barrier (b = 0.74), the pulmonary capillary blood volume (b = 0.74), and the total morphometric lung diffusing capacity for oxygen (b = 0.69) all correspond closely to the VO2max value. 7. Allometric comparisons of the morphometric pulmonary parameters of bats, birds and non-flying mammals reveal that superiority of the bat lung over that of the non-flying mammal.(ABSTRACT TRUNCATED AT 400 WORDS)

The lungs of five species of bat Pipistrellus pipistrellus, Miniopterus minor (Peters), Tadarida mops (De Blainville), Cynopterus brachyotis (Muller) and Cheiromeles torquatus (Horstield) have been analysed by morphometric techniques. The mean body weight (W) ranged from 5 g in Pipistrellus pipistrellus to 173 g in Cheiromeles torquatus; the lung volume (VL) ranged from 0.3 cm3 in Pipistrellus to 10 cm3 in Cheiromeles. The volume densities or the main components of the bat lung, namely the parenchyma [VV(p,L)] (the gas exchange region) and the non-parenchyma [VV(np,L)], were closely similar, the VV(p,L) constituting a mean value of 84.2% and the VV(np,L) 15.8% in the five species. The VL, the surface area of the blood--gas (tissue) barrier (St), the pulmonary capillary blood volume (Vc), and the total morphometric pulmonary diffusing capacity (DLO2) were all strongly correlated with body weight. The harmonic mean thickness of the blood--gas (tissue) barrier (tau ht) and the surface density of the blood--gas (tissue) barrier [SV(t,p)] were poorly correlated with W. The bats had a remarkably higher VL than either birds or terrestrial mammals. The Vc in the bat lung was similar to that in the bird lung but higher than that of the terrestrial mammals. The bats had a more extensive St than either the birds or the terrestrial mammals. In the bats the tau ht was thicker than in the birds but thinner than that of the terrestrial mammals. These pulmonary structural adaptations culminated in a higher DLO2 in the bat than either in the birds or in the terrestrial mammals. The superior morphometric properties of the bat lung coupled with the established physiological adaptations may help to explain how the bat lung is capable of providing the immense amount of oxygen demanded by flight.

The lungs of five adult Epauleted Fruit-bats (Epomophorus wahlbergi) of mean body weight 96 g were analysed morphometrically. The lung volume per unit body weight was 0.043 cm3/g, the surface area of the tissue barrier (i.e., the effective alveolar surface area) component of the blood-gas pathway per unit body weight was 138 cm2/g, and the surface density of the tissue barrier (surface area of the tissue barrier per unit volume of parenchyma) was 121 mm2/mm3. The harmonic mean thickness of the tissue barrier was between 0.267 and 0.349 micron. The morphometric pulmonary diffusing capacity per unit body weight (DLO2/W) was 0.02 ml O2 per min per mm Hg per g. These values are compared with those of shrews and birds. It is suggested that in bats enlargement of the lungs, small subdivisions of the air spaces, and a thin blood-gas barrier, could be linked with previously reported circulatory adaptations to account for the high oxygen consumption during flight.