AMERICAN JOURNAL OF PrrYsroLoGY

Vol. 215, No. 2, August J 968. Prinied in U.S.A.

Cutaneous gas exchange in bats

CLYDE F. HERREID II, WILLIAM L. BRETZ,

AND KNUT SCHMIDT-NIELSEN
Ds;barfmant of Zoology, Duke University, Durham, North Carolina
A?

HERREID$LYDE F.11, WILLIAM L. BRETZ,ANDKNI..ITSCHMIDT- pears, grapes, and bananas. A multivitamin supplement
NIELSEN. Cutaneous gas exchange in bats. Am. J+ Physiol. 215(2) : (Pervinal) was given to both species. The average weight
506-508. 1968.-Carbon dioxide and oxygen exchange of Eptesicus was 20.2 g (range 15.8-23.8 g) and that of
through the skin were measured in two species of bats (Eptesicus Pteropus was 583 g (508-636 g).
fuscus and Pteropus pokiocephalus). No significant cutaneous up- To measure cutaneous gas exchange a bat was en-
take of oxygen was noted. The cutaneous CO2 loss increased
closed in a Plexiglas chamber with the head outside and
with temperature. On a body weight basis the cutaneous out-
put of CO2 was higher than in pigeon, man, or turtle, but much the rest of the body and wings inside the chamber.
lower than in a frog or salamander. When CO2 loss is calcu- Changes in the chamber air were determined by analysis
lated on the basis of surface area (wings included), bats are not of withdrawn samples. The top was sealed with a rubber
exceptional. The cutaneous CO2 loss in bats is a higher fraction gasket and secured to the chamber with bolts. The bat’s
of the total CO2 output than in other terrestrial vertebrates, head passed through a wide-bore rubber stopper in one
reaching 11.5 y0 of the total in Eptesicus at 37,5 C. This is modest side of the chamber with a rubber diaphragm as a seal
compared to the 274% for amphibians. around the neck of the animal. To monitor air, wing, and
rectal temperatures, thermocouples were passed through
carbon dioxide; oxygen; skin; respiration; metabolism; another stopper which also had a tube for ventilation of
temperature the body chamber between experiments. To permit gas
samples to be withdrawn without changes in pressure in
the chamber, a heavy balloon was placed inside and
connected via a tube to the outside. Preliminary experi-
S TUDIES of cutaneous gas exchange in homeotherms ments showed the need for mixing of the chamber
which was achieved with a small propeller driven from
air,
have been confined mostly to man where an estimated
l-Z% of the total respiratory exchange occurs through the outside by a magnetic stirring unit. Tests with known
the skin (2). It is not known what proportion of the CO2 gas mixtures placed in the chamber and analyzed at
output and 02 uptake via the skin is due to metabolism intervals showed that the gas composition in the empty
of the skin tissue itself and what proportion is due to dif- chamber did not detectably change during periods of
fusion from the vascular bed. Usually, both processes are several hours.
considered under the heading of cutaneous respiration. In setting up an experiment, a bat, which had been fed
Bats have exceptionally large skin areas. The ratio of 12-18 hr before, was immobilized with outstretched
flight membrane surface to furred body surface is re- wings on a hardware cloth frame by passing string or cord
ported to range from 4: 1 to 8 : 1 (9). Furthermore, the over the neck and wings with small pieces of tape at the
flight membranes are very thin and well vascularized, wing tips. (In most experiments with Pterupus the wings
suggesting that higher rates of cutaneous gas exchange were not outstretched.) The bat was placed in the cham-
might occur in bats than in other homeotherms. ber within a temperature-controlled room and thermo-
To examine this possibility we measured the cutaneous couples were inserted. After the top was secured, air was
gas exchange of two species of bats. They differ greatly in passed through the chamber for an equilibration time of
size and are from different suborders of the Chiroptera. l-2 hr after which the air flow was clamped off. A gas
The big brown bat (Eptesicus fuscus, suborder Micro- sample was quickly withdrawn from the chamber via a
chiroptera) is widely distributed in North America. The small stoppered port and analyzed for CO2 and 02 with
Australian flying fox (Pter@us ~oliocefdalus, a fruit-eating a Scholander &~-CC gas analyzer (10). All values are
bat of the suborder Megachiroptera) is among the largest given as STPD.
bats in the world with a wing spread often over 1 m. Gas samples were withdrawn from the chamber at lo-
or 15-min intervals for 1 hr. The buildup of CO 2 (and
decrease in 02) was linear with time. Runs of many
METHODS
hours were conducted without observable departure
Eptesicus fuscus was captured in North Carolina and from linearity. Although the diffusion head for the gases
maintained on a diet of meal worms, whereas Pter@us was changing, this was minor in contrast to the total
poliocephalus was shipped from Australia and fed on apples, pressure head and no departure from linearity was ex-
506

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Copyright © 1968 American Physiological Society. All rights reserved.
CUTANEOUS GAS EXCHANGE IN BATS 507

petted. Often a second test was made after the 1st hr tion by assuming an RQ of 0.8. In the few instances
experiment with an intervening period of 15 min to where we succeeded in making both measurements, total
flush the air from the chamber. The bats did not urinate metabolism was similar to published values.
during the experiment so that all CO2 presumably was As noted above the percent CO2 leaving the skin of
exchanged through the skin. Eptesicus increased with temperature. This increase is due
Air temperature in the chamber remained within to the increase in absolute skin output (Table 1) and to
H.5 C of the desired level. Body temperatures indicated changes in the total metabolism of the bat with tempera-
that both species were acting like true homeotherms ture. Episesicus has a thermoneutral point near 35 C.
during the experiment, and torpor did not occur. On a Below this temperature the total metabolism rises rapidly.
few occasions it was possible to measure simultaneously Thus at low air temperatures, e.g., 18 C, not only is the
the 02 consumption from the head region using a Beck- skin CO2 loss low but the total metabolic rate is high,
man G-Z gas analyzer. resulting in a small proportion of the total CO2 leaving
The surface area of the furred body, less the flight via the skin. At high temperatures the lowering of the
membranes, was estimated from Meeh’s equation metabolic rate as well as the simultaneous increase in
S(cm2) = 10 Wbm>l o.67. The surface area of the cutaneous CO2 output contribute to the increasing frac-
flight membranes was obtained by tracing the shape of tion of total CO2 lost via the skin. Data for Pteropus were
the animal with extended wings on paper and deter- similar (Table 1).
mining the area of the flight membranes with a planime- Whereas CO2 diffused out of the skin of the bats there
ter. The flight membrane area obtained in this way was was only limited evidence to suggest that 0 2 passed into
doubled and added to the estimated furred body area to the skin. The oxygen content of the bat chamber de-
obtain the surface area of the entire animal. creased slightly, but not significantly, during the course
of an hour’s experiment.
RESULTS

Cutaneous output of CO2 was a function of tempera- DISCUSSION

ture; at high air temperatures CO2 loss was increased The cutaneous CO2 output of bats increased with
(Table 1). Both species of bats showed this trend whether temperature. A similar pattern has been found for man
CO 2 output was calculated on a basis of weight or surface (2). This could be explained by increased skin metabo-
area, or as percent of the total metabolic CO2 loss. The lism or by peripheral vascular dilation at high tempera-
greatest change in CO2 loss in Eptesicus occurred above ture. In bats, wing temperature was similar to air tem-
35 C where vasomoter changes were also observed+ While perature, and the skin probably had higher CO2
the blood vessels of the flight membranes were relatively production at the higher temperatures. It is doubtful,
constricted at 35 C they were engorged at 37.5 C. Marked however, that increased skin metabolism alone would
vasodilation in flight membranes at high temperatures
has been noted previously in bats (9). It was not possible
to extend the experiments to higher temperatures be- TABLE 2. Cutaneous carbon dioxide loss in vartebrates
cause the animals died at 40 C. I
What proportion of the CO2 exchange of the whole bat Cutaneous CO2 Loss+
-- -
occurs through the skin. 7 For this calculation we used Aw T~;P,
Reference
w g mZ CO2 ml CO2
previous results for the total metabolism of the bats (1, (kg
hr)-1 1 to21
2,s hr)-1Cm2
3), because simultaneous determinations of total and skin -- ,_
metabolism were very difficult. Oxygen consumption Frog (Rana), 37.5 20 129 74.3 427 6
data from the literature were converted to CO2 produc- N = 10
Salamander 25 95 84.0 11
(Am bystoma),
TABLE 1 l Carbon dioxide oufout from the skin of bats N=?
I Turtle (Emys), 50 23 1.35 0.3t 4.93 7
Cutaneous CO2 Loss N=l
Species Temp, “C Pigeon, N = 1 300 24-29 8.8 1l 2t 57 7
ml co2 % msotal ml CO2 (m2 Man, N = 6 70,000 20-3 I 2.12 1 l 4t 84 2
(kg hr)-1 hr)-1 Big brown 20 25 53 1.8 25.7 Present
I

bat, N = 9 study
Ep fesicus, 20.2Ig 18 21+3 0.4% 10.2 Flying fox, 583 25 18 3.8 36 2 Present
l

25 53zt6 1+87& 25,7 IN=5 study

35 69+8 10.8a/, 33.5 I
-
37.5 1151t16 11.5% j 56.1 * Surface areas for animals other than bats computed from
the equation : S(cm2) = lOw(gram)] OJ7. In bats, measured
15 7ztO 1.1% 14.1 wing areas were added to the computed area. tValues of
25 18&l 3.8% 36.2 total CO2 loss for computing these percentages were estimated
35* 28+0 6.0% 44.2 assuming RQ = 0.8 and using the foIlowing equations for
metabolic rate: turtle: kcal/day = L78(kg) o-728 (ref. 4; tem-
Values are means+1 SE. * Higher, temperatures] were perature correction made) ; pigeon : kcal/day = 78.3 (kg) 0.T23
lethal to &eropus in these experiments. (ref. 8) ; man: kcal/day = 69(kg) o-75 (ref, 5).

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Copyright © 1968 American Physiological Society. All rights reserved.
508 HERREID, BRETZ, AND SCHMIDT-NIELSEN

account for the sharp increase in CO2 output between surface areas. On a weight basis bats do have very high
35 and 37.5 C in Eptesicus (Table 1). How much of the rates of cutan eous CO2 loss compared to pigeon, man,
skin CO 2 is due to skin metabolism and how much is due and turtle, but much lower than frog and salamander
to diffusion from the blood is unknown, but calculations (Table 2), Somewhat surprisingly, the fraction of the
for man have suggested that it comes from both sources total CO2 output which passes through the skin of bats is
(2) not very great, and the maximum observed (I 1.5 %) is
There was some suggestion that oxygen entered the certainly modest compared to the 74 % and 84 % for frog
skin of bats, although statistically this rate was not signifi- and salamander. On the basis of surface area cutaneous
cantly different from zero uptake. Therefore, if cutaneous CO2 loss from bats is also low compared to man and a
oxygen uptake did occur it was at a much lower rate than pigeon. Values from bats were only 33-66 % as much as
the CO2 passage out. This is similar to previous studies those of these homeotherms. If we consider the fact that
with other terrestrial animals (2). The difference in the the flight membrane is mammalian skin, perhaps it
exchange of the two gases is not surprising. The difference should not be too surprising to find relatively high rates
in oxygen partial pressure (tension) between atmosphere of CO2 loss for bats on a weight basis but relatively low
and blood may be higher than for CO2, perhaps about rates when the loss is expressed in terms of surface area.
100 mm for 02 against probably 40 mm for CO2 How- l

ever, the diffusion of these gases through the skin is This study was supported by National Institutes Grant HE-
essentially a diffusion between gas and liquid, and there- 02228.
MT. L. Bretz received support from National Institutes of Health
fore, the higher solubility for CO2 in water (about 30- Grant 2Tl HE 5219.
fold) results in an apparent higher diffusion rate for CO2 K. Schmidt-Nielsen is the recipient of National Institutes of
of approximately 25-fold. He alth Research Career Award 1 X6-GM-2 1,522.
The amount of gas exchange that occurs through the Present address of C. F. Herreid II: Dept. of Biology, State
skin of a bat might be expected to be higher than most University of New York at Buffalo, Buffalo, N, Y.
terrestrial vertebrates, since they have exceptionally large Received for publication 22 January 1968.

REFERENCES

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Copyright © 1968 American Physiological Society. All rights reserved.