Re~pirutio~ Physiology (1970) 9, 151-161; N~rt~-Ho~~a~d~~~iish~g Company, Amsterdum

GAS EXC~NGE BETWEEN AIR AND WATER AND THE VENTILATION

PATTERN IIN THE ELECTRIC EEL

J. FARBERIANDII. RAHN

department of Physiology, School of Medicine, State University of New York at B~~a~o~~u~a~o,

New York 14214, U.S.A.

Abstract. The electric eel is an obligate air breather that rises periodically to the surface to exchange
gas. By barring access to the surface of an aquarium except for a breathing hole the expired and
inspired volumes can be measured in a free swimming animal by placing over the hole a funnel for
the collection and analyses of gases or for recording of the breathing pattern. At 26 “C the total
oxygen uptake was 0.5 ml/min/kg of which 78 ‘A was absorbed from the air and the remainder from
the water. In contrast 81% of the CO2 was eliminated into the water by the skin, the rest into the
air. As a result the gas exchange ratio in the air was 0.25 and in the water 3.65 with an overall ratio
of 1.0, Expired and inspired volumes were 31 and 35 ml, respectively, in a 2.76 kg animal, and the
buccai cavity empties almost completely with each breath. The total respiratory cycle is completed
in 0.4 set with maximal inspiratory and expiratory flow velocities of 250 and 330 ml/set, respectively.

Air-breathing fish Oxygen consumption

Breathing pattern Respiratory quotient
Control of breathing Skin respiration

It is well established that the electric eel, Elect~5ph~~u~ elec~~i~~s,is an obligate air
breather that rises to the surface every few minutes to exchange the air volume in
the buccal cavity. As JOHANSEN et al. (1968) have recently shown by direct sampling
of the buccal gas volume the 0, is rapidly diminished after inspiration but the CO2
tension plateaus off around 30 torr. These observations as well as those of GAREY
and RAHN (1970) suggest that in this scaleless animal much of the CO2 is excreted
through the skin into the water while presumably a very sig~~cant 0, uptake takes
place in the highly perfused buccal cavity.
It was therefore of interest to establish quantitatively the partition of the 0,
uptake and CO2 elimination between air and water in the normal, free swimming
Received for publicatforz 14 October 1969.
1 These studies were aided in part by Contract N~Ol4-68-A-0216, (NR 101”722), between the
O&e of Naval Research, Department of the Navy, and the State University of New York at Buffalo.
Present address: Department of Physiology, Dartmouth Medical College, Hanover, N.H.

151
152 J. FARBERANDH. RAHN

electric eel and to measure the tidal volme, the buccal “lung volume” as well as
airflow characteristics of a single breath. While our observations were limited to a
single animal it is well to point out that all the measurements were performed without
any physical contact between the free swimming animal and various measuring
devices.

Methods
A 2.76 kg electric eel obtained from the Amazon area was kept in a filtered and
aerated 90 L tank at a temperature between 25 and 27 “C. The animal was fed regularly
and remained in good condition over a period of 3 months. A wire mesh was per-
manently placed 1 cm below the tank water level. A single opening (7 x 18 cm) in
the mesh provided a sufficiently large breathing hole for the animal. Since all recording
and gas collecting devices were placed above this breathing hole, the animal was not
constrained. The arrangement is quite ideal since contrary to the findings of SOHANSEN
et al. (1968) the entire expired gas volume is normally always eliminated through the
mouth and not through the opercular openings.

GGSEXCHANGE
IN AIR
Oxygen and CQz exchange in air was measured from individual breaths by placing
a known volume of the inert gas argon into a stoppered funnel inverted over the
breathing hole in the wire mesh. The animal expired into the funnel, thereby dihning
the Ar with Q2, CO, and N,, and a portion of this mixture was then reinspired. The
contents of the funnel was next withdrawn, the volume measured, and the fraction
of Q,, CO, and Ar measured by an MS-4 multichannel mass spectrometer (AEI
Ltd.). The interval that the animal had remained submerged since the previous
breath was known, so the average Veo2~sTPD~ and Vol(sTPDjcould be calculated. The
volume of expiration, VE(BTPS),volume of inspiration, VI(BTPS),partial pressure of
expired oxygen, PEG,, and of expired carbon dioxide, PEAR,,as well as the gas exchange
ratio, R, were also determined from this analysis. Buccal cavity volume, VM{BTP~),
at the time of expiration was obtained by calculating the dilution of argon which
occurred after the animal rebreathed the Ar in the funnel 3 to 4 times.

GASEXCHANGE
IN WATIER
To obtain the O2 and COz exchange in water via the skin, the volume of water in
the tank was reduced to approximately 40 L while a lucite plate covered the water
surface except for a small breathing hole. The water was continuously stirred by an
electric pump. To further minimize the transfer of gas between water and air, the
water surface of the breathing hole was covered with mineral oil. Oxygen uptake
was determined by periodic sampling of the water and measurement of Po, with an
IL Q2 electrode. Knowing the solubility, ct, of O2 in water at the temperature of 25 “C
and volume of water in the tank, Vtank, the To2 was calculated from the decrease
in Po, with time, t.
 GASEXCHANGE
BETWEEN
AIRANDWATER 153

APo, - cc* Vtank.

Thus VozSTPD= dt

In separate experiments, the output of COz was measured by periodic sampling of

tank water and analysis of total COz content, GoI, with the manometric Van Slyke
(5 ml samples). Carbon dioxide output was calculated from the increase in COz
content with time.

AC
Thus Vcoz = c~;sTpD - Vtank.

MEASUREMENT
OF AIRFLOW
Measurement of individual respiratory cycles were done with a pneumotachograph
made from a 21 mm i.d. plastic tube into which a wide mesh screen was inserted
(mesh= 1.5 mm”) to provide minimal resistance to flow (R< .5 mm H,O/lOOO ml/set).
Inspired and expired flow rates were measured, as well as the period of the respiratory
cycle. Inspiratory volume was calculated by graphically integrating the flow curve.

Results

GASEXCHANGE
IN AIR
Gas exchange in air was obtained from the analysis of 18 random breaths using the
Ar dilution technique and is shown in figs. 1A and 1B. Average Vo2 and Vcoz decreased
as the interval between breaths increased (fig. 1A). The gas exchange ratio, R, was
low, usually less than .3, and tended to decrease with increased breath-holding, thereby
diminishing the already small CO, output from the lung. This phenomenon is also
seen in the expired partial pressure of O2 and CO2 (fig. IB) where we observe that
PEARtends to decrease with increased breathholding, while PEAKSshows no apparent
increase. Data from JOHANSENet al. (1968) of O2 and CO2 pressure in the mouth,
PM, sampled during a breath-holding interval has been included in fig. 1, and shows
the time course of partial pressure changes before an expiration. Note that Philcozis
close to a plateau value after about 1 min of breath holding. Also, the AP,, in the
mouth is highest in the ftrst minute, indicating a maximum Vo, during this time. The
weighted mean value for Vo2, Vco2 and R from all data points is indicated in fig. 1A
and represents a total of 13 hr of air breathing.

GASEXCHANGE
IN WATER
The uptake of oxygen from the water was measured in three determinations on
different days, where P,, decrease in the sealed tank was determined over 45-300 min
(fig. 2). The decrease in Po, appeared generally linear, even at partial pressures as
low as 30 mm Hg. Elimination of CO, into the tank water was measured by direct
determination of COz content increase in the sealed tank. The results of four ex-
periments of 90-180 min duration are presented in fig. 3.
154 J. FARBER AND H. RAHN

0.4

0.3

0.2

I
l

2.0

1.5 - l

1.0 -

0.5 -
o

C%
*A0 ,AA

1 I I 1
1 2 3 4 5 6 7 8 9
Minutes before Breath

Fig. 1A. Gas exchange in air showing vo,, %J, and R, for 18 ~div~dual random breaths. *oz,
i’co, and R represent average values where total gas exchange is divided by the time interval before
the breath. Trends in the data are drawn by eye. Inset shows the weighted mean values of *o,, ir,oz
and R for all breaths.

mm Hg

140

120
1968)

100 -

60-

e
1 2 3 4 5 6 7 8 9
Minutes before Breath

Fig. 1B. Expired 02 and COZ tensions obtained after 18 individual random breaths. Data for the
first 2 min are analyses of buccal cavity gases reported by JOHANSBN et al. (1968).
 GAS EXCHANGE BETWEEN AIR AND WATER 155

“02mllmin
,
\ 0.20

\L 0.34

PO2

60 t

I overage = 0.3 1 ml/min

Fig, 2. The decrease in tank water PO, with time in 3 separate determinations. The slope was deter-
mined by least squares analysis and vo2 is noted for each run.

.
vol % co, “CO,
5.01 cl ,I 1.27 ml/mi.n

4.0 - I
id
. average = 1. I 3 ml/min
.

p .
3~5~~--____
I I I I
1 2 3 hrs

Fig. 3. The increase in Cco, in tank water with time during 4 determinations. Slopes were determined
by the least squares analysis and ~CO, for each run is noted.
156 J. FARBER AND H. RAHN

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250

S T

B TT
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ml/
set
o I--. 1 -

1ooL
I
T
s
‘2
2001

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Fig. 4. Pneumotachometer recordings of the respiratory cycle. The 4 upper records represent con-
secutive breaths. In the lower record one cycle is enlarged indicating the airtlow rates. For the
analysis of time and volume calculation it was necessary to differentiate between airflow produced
by water displacement as the animal surfaces under the funnel which preceeds the airflow from the
buccal cavity. We believe that the first part of the expiration record represents the former while
the true expired volume follows the dotted curve. A similar consideration must be given for the end
of inspiration.

VENTILATION, TIDAL AND BUCCAL CAVITY VOLUMES

The respiratory cycle of the electric eel shows a rather uniform pattern. Pneumo-
tachograph tracings of four consecutive breaths along with an enlarged composite
are shown in fig. 4. The time of inspiration, expiration, and maximum inspiratory
and expiratory flow is tabulated for each breath in table 1.
Inspiratory and expiratory volume, as determined by Ar dilution are shown in
fig. 5. Twenty-four random breaths have been presented, eighteen of them from the
gas exchange experiments discussed above. Increasing time beneath the surface
seems to have had little effect on inspired and expired volume. A mean inspired volume
of 35 ml +.7 ml SE. and an expired volume 31.2 ml +.6 ml S.E. was calculated.
The difference between these volumes is significant and is probably due to the low
gas exchange ratio in the buccal cavity. Using the mean inspired volume and the

total gas exchange of the data points in fig. 1, a theoretical curve for inspiratory-
expiratory volume difference with increased breath-holding intervals was calculated
and shown in fig. 5 as solid lines. Inspired volumes were also calculated from the
 GAS EXCHANGEBETWEENAIR AND WATER 157

I I I I I I I 1 I 1 1
1 2 3 4 5 6 7 8 9
Minutes before Breath

Fig. 5. Inspired tidal volumes, VI, and expired volumes, VE, calculated from the gas dilution ex-
periments. The inspired volumes average 35 ml and appear to be independent of breathing cycle.
The lower continuous line represents the calculated expired volume based upon the changes in gas
exchange ratio values of fig. 1. The buccal volume values, VM, determined by Ar rebreathing are
similar to the expired volume values.

TABLE 1
Analysis of 4 random breaths.

Breath Interval %ax Expir Inspir Respir VI

No. before mljsec time time cycle* ml
breath Expir Inspir set set set

1 5.17 250 330 .20 .16 .41 38.5

2 1.75 250 315 .20 .16 .42 35.0
3 2.00 147 325 .12 .16 .33 39.5
4 5.33 250 325 .20 .15 .39 42.0

* Includes pause between expiration and inspiration.

Vr: total volume inspired computed from integration of inspiratory flow record.

integrated flow curves, table 1, and are shown in fig. 5 as open circles, VI. The buccal
cavity volumes were calculated from the Ar rebreathing experiments. The results of
six trials are shown as open squares, VM, in fig. 5. These values are similar to the
expired volume determined from the gas exchange experiments, VE, and suggest that
most of the buccal cavity volume is replaced with each breath.

Discussion
The combined O2 consumption and CO, elimination for the buccal cavity and skin
is presented in table 2. For comparison to other primitive air breathers, the division
of gas exchange of two frogs (Bufo americanus, Rana pipiens) (HUTCHISON, WHITFORD
158 J. FARBERAND H. RAHN

TABLE 2
Gas exchange partition between air and water in the electric eel.

vc, vco, R

Air 1.06 0.26 0.25

Water 0.31 1.13 3.65
Total 1.37 1.39 1.01

TABLE 3
Gas exchange partition between lung and skin in various amphibians and fish.

% voz %&co, R Reference

lung skin lung skin lung skin overall

in air
25 “C Bufo 66 34 17 83 0.37 2.18 0.95 HUXHISON,
americanus WHITFORDand
KOHL, 1968
25 “C Rana 68 32 43 57 0.45 1.47 0.72 HUTCHISON,
pipiens WHITFORDand
KOHL, 1968
25 “C Ambystoma 69 31 29 71 0.31 1.65 0.72 WHITFO~~ and
tigrinum HUXHISON, 1965
25 “C Taricha 68 32 32 68 0.30 2.07 0.86 WHITFORDand
granulosa HUTCHISON,1965

in water Air Water Air Water Air Water overall

20 ‘C Protopterus 89 11 30 70 0.26 4.9 0.77 LENFANTand

aethiopicus JOHANSEN,1968
25-27 ‘C Electro- 78 22 19 81 0.25 3.65 1.01 -
phorus electricus

and KOHL, 1968), two salamanders (Taricha granulosa, Ambystoma tigrinum)

(WHITFORD and HUTCHISON, 1965), and the African lungfish (Protopterus aethiopicus)
(LENFANT and JOHANSEN, 1968) is shown in relation to the electric eel (table 3). The
same trend is apparent in all species shown, namely dependence on the air ventilating
apparatus for 0, demand, while other routes serve for the bulk of CO, excretion.
An especially interesting comparison is that of the lungfish to the electric eel, in that
both are free swimming in the water environment.
The comparative independence of CO, output upon ventilation is emphasized in
our studies by the consistency of PcoZ in the expired gas with different breath-holding
intervals. As no anatomical dead space is likely in an animal which exchanges gas
in its buccal cavity, it seems safe to assume that the pressures of gas measured in the
expirate are the same as those existing in the mouth and that a lack of Pco2 change
 GAS EXCHANGEBETWEENAIR AND WATER 159

with increased breath holding indicates that this gas is in equilibrium with the blood
leaving the mouth. JOHANSEN et al. (1968) have obtained values for mixed arterial
blood Pcol in the eel. Under conditions where the breath-holding intervals of their
animals were similar to ours, the arterial values obtained were comparable to the
mean PcoZ in the mouth found in our experiments (35 torr).
Much of the ability of the eel to remain apnoeic for several minutes and still retain
an adequate 0, consumption rests on the low pressures of 0, necessary to saturate
the blood hemoglobin. The O2 dissociation curve for the electric eel obtained by
JOHANSENet al. (1968) shows that hemoglobin is 90 % saturated at a pressure of about
31 torr. Our data shows, however, that To, tends to decrease with increased breath-
holding time. Explanation of this phenomenon may lie partly with JOHANSEN’S(1968)
finding that blood flow to the mouth tends to decrease during the breath-holding
interval, but it is also clear that the pressure of 0, in the mouth at the time of ex-
piration is well below that necessary for hemoglobin saturation in many breaths
(fig. 1).
To investigate this point, we recorded the number of breaths the animal took
over the course of a day or more in three determinations, by pneumotachometer. The
average interval between breaths was analyzed on an hour to hour basis. We deter-
mined that the undisturbed animal might breathe at a rhythm consistent with our
data for several hours, although smaller or larger average intervals were also seen.
Since these animals die after 15-20 min of air deprivation (GAREY and RAHN, 1970),
it is unlikely that they can accumulate a substantial oxygen debt over several hours
of inadequate ventilation. As a further check on the 0, uptake of the animal, 50 ml
of oxygen was placed in a funnel inverted over the air hole. After each breath, the
contents of the funnel were withdrawn, the CO, absorbed and the decrease in volume
determined. In this way, the 0, consumption over many consecutive breaths could
be determined. The \joZ values found are shown in fig. 6 and are comparable to the
1.06 ml/min mean from random breaths. Note that the first breath the animal took
from the funnel would contain -60 % 0, (50 ml 0, + N 30 ml N, from the expired
gas). By the time funnel volume decreased to 10 ml, 0, would still make up 25 %
of the inspired gas. All this would result in the maintenance of mouth P,, above the
saturation pressure of hemoglobin for longer periods of breath holding and thereby
help maintain boz.
The total vo2 of the electric eel at ambient temperatures between 25-27 “C averages
0.50 ml/min/kg. These data compare well with another sedentary air breather, the
lungfish (Protopterus), whose 302 at 20 “C was found to be 0.25 ml/min/kg (LENFANT
and JOHANSEN, 1968).
The question of whether the skin could be made to account for more of the total
0, consumption was qualitatively investigated by increasing the 0, pressure in the
water to over 600 mm Hg while the animal breathed air. Under these conditions some
intervals between breaths were over 20 min. A breath-holding time this long would
kill the animal under field conditions. In normal tank water P,, loo-130 torr, the
maximum interval between breaths was about 10 min. These data suggest that blood
160 J. FARBER AND H. RAHN

Funnel Volume
ml/min
ib
50 2 A 1.01
ml 0 1.01
40 0 1.00
0 1.15

30

20

10

I I I I I I
10 20 30
Minutes

Fig. 6. The decrease in funnel volume in consecutive breaths when COZ is absorbed. The slope of
each line represents vo2.

flowing to the skin can be made to carry more O,, when sufficient driving pressure
is available. However, the approximately linear decrease of PO, with time in normally
oxygenated water (fig. 2) suggests an independence of vo, upon P,, within wide
normal limits (down to 30 torr). For example, the PO, of the Amazon River, where
this animal is found, is about 50 mm Hg (GAREY and RAHN, 1970).
Our results have indicated that the animal exchanges, essentially, his entire gas
volume each time he breathes. An additional study was performed to determine if
any gas did remain in the buccal cavity after expiration. A volume of Ar equal to the
average inspiratory volume (35 ml) was presented to the animal in a funnel. Expira-
tion into the funnel diluted the Ar by a little less than half, and that concentration
was then inspired. The eel now was allowed to take a single breath of air without
the funnel, but afterwards the funnel was replaced and the next expiration is into 35 ml
of air. This last breath was analyzed for Ar concentration and by serial dilution, the
amount of gas left in the mouth after the free expiration into air was determined.
Six measurements gave a remaining fraction of gas in the mouth of between 5 and
10% or a little over 3 ml at a maximum. These results cannot be separated from a
partial reinspiration of expired gas, a fraction which may not be negligible because
of the rapidity of the animal’s respiratory cycle. In any case, the functional residual
capacity of the electric eel, that is the amount of gas left in the “lung” after a normal
expiration, is relatively small or minimal when compared to the residual volume in
higher vertebrates. This provides one advantage, namely that the maximal volume
of O2 can be inspired with each breath and allows the eel to go for long intervals
between breaths, although at the expense of less stable O2 and COZ tensions.

References
GAREY,W. F. and H. FLUIN(1970). Normal arterial gas tensions and pH and the breathing frequency
of the electric eel. Respir. Physiol. 9: 141-150.
 GAS EXCHANGE BETWEEN AIR AND WATER 161

HUTCHISON, V. H., W. G. WHITFORD and M. KOHL (1968). Relation of body size and surface area
to gas exchange in Anurans. Physiol. Zool. 41: 65-85.
JOHANSEN, K., C. LENFANT, K. SCHMIDT-NIELSEN and J. A. PETERSEN (1968). Gas exchange and
control of breathing in the electric eel, Electrophorus electricus. Z. vergl. Physiol. 61: 137-163.
LENFANT, C. and K. JOHANSEN(1968). Respiration in the African lungfish, Protopterus aethiopicus.
J. Exptl. Biol. 49: 437-452.
WHITFORD, W. G. and V. H. HUTCHISON (1965). Gas exchange in salamanders. Physiol. Zool. 38:
228-242.