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, 211 (6), 687-97

The Structural Design of the Bat Wing Web and Its Possible Role in Gas Exchange

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The Structural Design of the Bat Wing Web and Its Possible Role in Gas Exchange

Andrew N Makanya et al. J Anat.

Abstract

The structure of the skin in the epauletted fruit bat (Epomophorus wahlbergi) wing and body trunk was studied with a view to understanding possible adaptations for gas metabolism and thermoregulation. In addition, gas exchange measurements were performed using a respirometer designed for the purpose. The body skin had an epidermis, a dermis with hair follicles and sweat glands and a fat-laden hypodermis. In contrast, the wing web skin was made up of a thin bilayered epidermis separated by a connective tissue core with collagen and elastic fibres and was devoid of hair follicles and sweat glands. The wings spanned 18-24 cm each, with about 753 cm2 of surface exposed to air. The body skin epidermis was thick (61 +/- 3 microm, SEM), the stratum corneum alone taking a third of it (21 +/- 3 microm). In contrast, the wing web skin epidermis was thinner at 9.8 +/- 0.7 microm, with a stratum corneum measuring 4.1 +/- 0.3 microm (41%). The wing capillaries in the wing web skin ran in the middle of the connective tissue core, with a resultant surface-capillary diffusion distance of 26.8 +/- 3.2 microm. The rate of oxygen consumption (VO2) of the wings alone and of the whole animal measured under light anaesthesia at ambient temperatures of 24 masculineC and 33 masculineC, averaged 6% and 10% of the total, respectively. Rate of carbon dioxide production had similar values. The membrane diffusing capacity for the wing web was estimated to be 0.019 ml O2 min(-1) mmHg(-1). We conclude that in Epomophorus wahlbergi, the wing web has structural modifications that permit a substantial contribution to the total gas exchange.

Figures

Fig. 1
Fig. 1
Schematic diagram showing the set-up of the equipment used for the measurements of rates of oxygen consumption and carbon dioxide production in the bat. A thin polyethylene separator was fitted around the animal's neck, dividing the respirometer into a lower compartment (A) which housed the head and an upper compartment (B), which housed the rest of the body of the animal. The gases flowing out of the chambers were dried and channeled by a pump through a carbon dioxide analyser and an oxygen analyser for measurements of the concentration of the respective gases. The outputs of the analysers, with the pump flow and the respirometer temperature, were conveyed to an Analog Digital Data Conversion Board for on-line display, acquisition and data analysis by a mini-computer (PC). Analysis of the gases from either of the compartments could be accomplished by opening the respective valves. Further details are provided under Materials and methods.
Fig. 2
Fig. 2
Distribution of blood vessels in the bat wing web. (a) The whole wing, showing the distribution of the finger bones and large vessels (arrowhead) in the boneless wing membrane. Scale bar = 5 cm. (b) A higher magnification of the wing web membrane stretched between the fourth and fifth fingers with prominent large blood vessels. Scale bar = 5 cm. Notice the rich supply of blood vessels in the wing web.
Fig. 3
Fig. 3
Semithin sections comparing the structural characteristics of the wing web skin (left panels) and body skin (right panels) in the bat. (a,b) Low magnification (scale bars = 500 µm). Note the enormous folding of the wing web skin compared to the body skin. Hair follicles (encircled) are evident in the body skin. (c,d) Intermediate magnification (scale bars = 100 µm). The wing web is highly folded, with a double layer of epidermis (rectangles in c). The demarcation between the epidermis and dermis is not evident and the two epidermal layers are separated by a central core of connective tissue (asterisks). Unlike the wing web skin, the body skin has a relatively thick epidermis (E), a conspicuous dermis (D) with prominent sweat glands (S) and hair follicles (arrowhead). Note also the hypodermis (H). (e,f) High magnification (scale bars = 10 µm). In the wing web, the thin epidermis (rectangle) is only a few cells thick, and the connective tissue core (asterisks) presents a central capillary network (arrowheads). At the same magnification, in the body skin only the epidermis (E) with a thick stratum corneum (asterisk) and part of the epidermis (D) with sweat glands (S) have been captured.
Fig. 4
Fig. 4
Scanning electron micrographs of the wing web skin (a) and the body skin (b) showing the remarkable topographical differences. The wing web is virtually devoid of hairs. Its rough surface presents keratinized layers in the process of peeling off (see also Figs 3 and 5). In contrast, the body skin is virtually covered by a thick coat of tall hairs, fully masking the skin surface. Scale bars: a = 10 µm; b = 500 µm.
Fig. 5
Fig. 5
Transmission electron micrographs of the wing web, showing the layers and the position of the core capillaries. All scale bars = 3 µm. (a,b) The capillaries (Ca) are placed within the core tissue (CT), approximately equidistant from both surfaces. Notice a melanocyte (arrowhead in b) with melanin granules and a fibroblast (asterisk) close to the capillary. (c,d) The non-keratinized part of the epidermis is one to two cells thick (asterisks) and is covered by the stratum corneum with about 10 layers of flattened keratinocytes (dark arrowheads in c; white arrowheads in d). Both the keratinocytes and the other epidermal cells may contain melanin granules (white arrowheads in c).
Fig. 6
Fig. 6
Graphs showing V˙O2 (left panel) and V˙CO2 (right panel) of the total body and of the wings, each measured at two temperatures. Unfilled symbols (thin lines) refer to different bats. Filled symbols (thick lines) refer to the mean values of the group, with bars indicating 1 SEM. Note that for clarity, the Y-axis has a different scale below and above the break. At the higher temperature, in most cases total V˙O2and V˙CO2 decreased, whereas the gas exchange attributed to wings, on average remained almost constant.
Fig. 7
Fig. 7
Gas exchanged through the wings, expressed as percent of the total, during cold and warm conditions. Clear columns refer to measurements of rate of oxygen consumption and filled columns refer to measurements of rate of carbon dioxide production. Columns represent group averages; bars indicate standard errors. Symbols refer to the values of the individual bats.

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