AMER. ZOOL., 34:178-183 (1994)
Environmental Factors as Determinants in Bimodal Breathing:
An Introductory Overview1
PIERRE DEJOURS
Centre d'Ecologie et Physiologie Energeliques, Centre National de la Recherche Scientifique,
23, rue Becquerel, 67087 Strasbourg, France
SYNOPSIS. The physicochemical properties of the environment, water,
air, and more or less humid soils, are extremely different and impose
anatomical and physiological adaptations. Generally water breathers
exchange through gills and skin; in the air breathers cutaneous respiration
is generally small or negligible, and gas exchanges take place in lungs or
in tracheae. The main difference between water and air as to O2 and CO2
is that O2 is much less soluble in water than CO2, whereas O2 and CO2
capacitances in air are identical and the CO2 capacitances in water and
in air are similar. This results in very different CO2 tensions in waterand in air-breathers. Since air is rich in O2 compared to water, air breathers
breathe much less than the water breathers, and so their Pco2's are much
higher. However, at the same temperature, water- and air-breathers have
about the same pH, thanks to proper adjustment of the bicarbonates. In
amphibious animals, those having gill-skin exchanges with water and
pulmonary exchanges with air, the proportion of O2 and CO2 exchanges
are not evenly distributed among the several exchangers: the aquatic gas
exchanger is the main route for the CO2 output, whereas the gas-phase
exchanger is the main route for O2 uptake.
An increase of temperature has several consequences: 1) decrease of
the O2 and CO2 capacitances in water and, to a lesser extent, in air; 2)
increase of the energy metabolism, O2 consumption, CO2 production, etc.;
3) changes of the pH of the ambient water and of the body fluids. These
effects of the changes of temperature are seen in all living beings; in the
amphibious animals, the increase of temperature augments the O2 uptake
by the lung and the CO2 output by the branchial and/or cutaneous routes.
That is to say that the temperature variations change the intensity of the
gas exchanges and the distribution of O2 uptake and CO2 output between
the gill-skin exchanger and the lung exchanger.
It is classical to oppose terrestrial life to aquatic life; the amphibious,
often bimodal animals represent intermediate forms which presumably
play an essential role in the evolution and transition from an aquatic to
a terrestrial abode.
which lists mainly the properties which affect
respiratory functions: gas exchanges,
mechanics of breathing. The differences are
sizeable; however, the CO 2 solubility
( p a c i t a ' n c e ) coefficients in water and in air
P
a r e s i m i l a r F u r t h e rmore, the O2 and CO2
capacitances are decreased by increases of
1
From the Symposium Current Perspectives on the salinity and, On the Other hand, the CO2
Evolution, Ecology, and Comparative Physiology of capacitance may be increased several times
INTRODUCTION
Nature of the environment and routes for
gas exchanges
_ , , . . . ,
c
The physicochemical properties of water
and air are different, as shown by Table 1
Bimodal Breathing organized by R. P. Henry and N.
ifthewatpr a<; wawatpr mntains hiifFpr(V»
*s et tel ( ^ W a t e f ' *?**f water - Contains DUtter(S)
J. Smatresk and presented at the Annual Meeting of
the American Society of Zoologists, 27-30 December, (
^ejours, 198 1).
1991 at Atlanta, Georgia.
In many phyla, O 2 and CO 2 exchanges
178
179
AMBIENT FACTORS AND AMPHIBIOUS BREATHING
TABLE 1. Some differences between water and air: physiological consequences.
Water
Air
Air/water
O 2 capacitance
CO2 capacitance
O2 and CO2 coeff.
of diffusion
= 30
O2 and CO2 tensions
=8,000
acid-base balance
Viscosity
= 1/60
cost of breathing, circulation, skeleton, locomotion, gravity
H2O turnover
osmoregulation
ionoregulation
nitrogen catabolism
heat dissipation
Density
Water availability
Salt concentration
NH3 capacitance
Heat capacity
Heat conductivity
Heat of evaporation
variable
=1/800
low
variable
=2,450 kj-liter-1
take place through the integuments which
eventually may be folded to increase the
surface area exposed to the milieu. But in
several groups of water breathers, the surface for gas exchange is increased by the
development of gills, which result from
evaginations of the endoderm. In air breathers, cutaneous respiration may be important
and the integument is the only route for gas
exchange in some groups as earthworms and
collemboles; but generally air breathers possess special devices for gas exchanges: tracheae (insects), bookgills (scorpions and
some spiders), mantle cavities (snails) or
lungs, all arising from invaginations of the
ectoderm. The development of these special
anatomical structures in air breathers is
made necessary to avoid desiccation of animals living in open land.
Dual breathers (also called amphibious
breathers) i.e., animals who may exchange
O2 and CO2 with air and with water either
simultaneously, alternatively, or intermittently, are generally bimodal, with gills for
water breathing and lungs for air breathing.
Consequently these words "dual" and
"bimodal" are often used interchangeably.
However, it should be remembered that
there is almost always some cutaneous gas
exchange, and that some dual breathers are
trimodal (skin, gills and lungs), e.g., the salamander Siren lacertina (Guimond and
Hutchinson, 1973) and the reedfish Calamoichthys calabaricus (Sacca and Burggren,
= 1/700
= 1/3,500
= 1/24
body temperature
1982). A special case of amphibiousness is
offered by animals such as arthropods (crabs,
barnacles), some molluscs (bivalves), and
fishes (blennies), which live in the intertidal
zone and are exposed alternately to water
and to air (Bridges, 1988; McMahon, 1988;
Truchot, 1987a). These animals generally
use the same structures for their gas exchange
with water or with air.
THE O2 AND CO2 TENSIONS IN WATER
BREATHERS, AIR BREATHERS AND
AMPHIBIOUS BREATHERS
To understand the respiratory traits of
amphibious breathers, it is first necessary to
compare an obligate and exclusive air
breather with an obligate and exclusive water
breather.
Figure 1 is a PCO2 vs. PO2 diagram. The
lower curve concerns a water breather, a
trout, living in unbuffered fresh water; it
shows that API,EQ2 is much greater than
APE,I CO2 . This is a ready consequence of the
fact that O2 is much less soluble in water
than in air. Even if the water breather were
able to extract all of the dissolved O2 in
water, that is if APi,Eo2 was 156 Torr (which
is an impossible assumption), its expired
Pco2 would reach only a few Torr because
of the very high solubility of CO2 in water
relative to O2 (Rahn, 1966). However, in an
air breather, a turtle in the case of Figure 1,
an animal which breathes much less than
the trout since air as compared to water is
180
PIERRE DEJOURS
FIG. 1. PCQJ vs. POi diagram. The two straight lines
originating at point I (156 Torr) representing POl and
Pco2 of the inspired milieu, are respiratory quotient
lines in non-carbonated water and air at sea level (R
= 1; temperature = 20°C). Point B at 55 Torr corresponds to expired POj and Pco, for a given water ventilation Vw and may be the expired water of a trout
living in uncarbonated fresh water. Point C is hypothetical; it indicates the expired POj and PCO; an air
breather would have if its ventilation, Vair, were identical to that of the aquatic animal B. Air breathers
breathe much less than water breathers and their expired
points D move along the R lines; their exact positions
depend on the extraction coefficient (from Rahn, 1967;
Dejours, 1978).
ilar because their PCO2 values are exactly balanced by proportional [HCO^] (Fig. 2).
These characteristics of respiration in
exclusive water breathers and exclusive air
breathers allow us to consider the respiration of dual breathers. Figure 2 shows that
the acid-base balance, ABB, of a bullfrog
tadpole is analogous to that of a trout, but
that the adult bullfrog, a bimodal amphibious breather, has higher PCO2 and [HCOf ]
than the tadpole, such that their pHs are
very similar. In dual breathers, the relative
importance of the skin-gill route for
exchange in water and of the pulmonary
route for exchange in gas phase varies; the
more an animal is a pulmonary breather,
the higher is its blood CO2 tension and
[HCO3-] (Lenfant and Johansen, 1967).
Since the origin of animal life is aquatic,
dual breathers and air breathers should be
compared to water breathers; consequently
one may say that air and amphibious
breathers, with relatively high PCO2 and
2
very rich in O2, API,EO2 and APE,ICO2 are
similar (they are identical if the respiratory
quotient is unity), because their capacitances in air are identical. These considerations concern external respiration, but it is
obvious that the gas tensions resulting from
external breathing influence the tensions of
all compartments of the body.
What about the acid-base balance of these
animals with such different PCOz values in
their body fluids? Their blood pHs are sim-
are in a state of compensated
hypercapnic acidosis.
PHYSICOCHEMICAL AND PHYSIOLOGICAL
EFFECTS OF TEMPERATURE CHANGES
The effects of ambient temperature
changes are three-fold.
1. The increase of temperature decreases
the capacitances of O2 and CO2 in water and
in air. In water the changes of capacitance
are very important; when the temperature
is raised from 0 to 35°C, O2 concentration
in water decreases by half at constant PO2
(Fig. 3). The relative variation for the same
thermal rise is 50% higher for CO2 than for
O2. On the contrary, in air the capacitances
of both O2 and CO2 are slightly decreased
by an increase of temperature.
2. The increase of temperature raises the
intensity of energy metabolism in poikilotherms (Fig. 3), an effect often expressed by
the Q10 factor (the increase of energy metabolism for an increase of 10°C). Since
thermal increases physically decrease the O2
availability and the CO2 capacitance of the
FIG. 2. Acid-base balance of trout, tadpole and adult water, as seen in the previous paragraph,
bullfrog, and turtle on a [HCOf] vs. pH diagram. Buffer the increase of energy production with temlines are arbitrary. Data from Randall and Cameron perature represents an ecological pressure
(1973) for the trout; from Erasmus et al. (1970) for the
bullfrog; from Howell et al. (1970) for the turtle. The for an aquatic poikilotherm to get access to
ambient air which is relatively very rich in
curvilinear lines are CO2 isobars.
181
AMBIENT FACTORS AND AMPHIBIOUS BREATHING
O2, that is, to become a dual breather or
eventually an air breather.
3. The increase of temperature decreases
the neutral pH of water, with a coefficient
of about -0.017 pH unit/°C (Fig. 3, lower
part). Rahn and Howell (1978) published
an historical sketch about the relation
between acid-base balance and temperature. It has been demonstrated by several
authors (see for review Rahn et al., 1975;
Reeves, 1977; Truchot, 19876) that the
thermal increment has a parallel effect on
the pH values of the "milieu interieur"
which is regularly above the pH vs. temperature curve of the neutral water, a phenomenon named "constant relative alkalinity." This ABB changes of the "milieu
interieur" with temperature are observed in
air-, water- and amphibious breathers, e.g.,
Carcinus maenas (Truchot 1973, 1987a).
10
20
30
temperature "C
FIG. 3. Upper part: a) Solubilities of O2 and CO2 in
distilled water as a function of temperature. The solubilities at 0°C are taken as 100% (from Dejours, 1988).
b) Metabolic rates Mx, e.g., MOi, Klco,, of poikilothermic animals as a function of temperature (right scale;
arbitrary unit, taking the value at 0°C as 1). Q,o is
assumed to be 2.5. Lower part: pH of neutral water as
a function of temperature.
THE RELATIVE IMPORTANCE OF O2 AND
CO2 EXCHANGES IN WATER AND AIR
At low temperature the energy metabolism is low, and some amphibious animals
use mainly, sometimes exclusively, their
water exchangers (skin, gill) and little or not
at all their pulmonary exchanger (see Guimond and Hutchinson, 1973). If, when
placed in well aerated water, they still
breathe a little via the pulmonary route the
ventilation may be arrested when some O2
is added to the water.
Let us suppose a potentially amphibious
breather, placed in the cold with a low energy
metabolism; its O2 consumption, MO2, and
its CO2 production, lClCO2, are also low and
may be entirely covered by the branchial
and/or cutaneous exchanges (Vinegar and
Hutchison, 1965; Jackson, 1987). A temperature increase augments KlO2 and ldCO2
(Fig. 3) and the animal may be compelled
to use its pulmonary route to supplement
its O2 and CO2 exchanges with water. As
soon as the pulmonary respiration starts, a
great amount of O2 is taken up by the poorly
oxygenated venous blood which reaches the
lung, because for a given O2 tension air is
much richer in O2 than water (Table 1). Of
course some CO2 is discharged into the fresh
air inhaled in by the animal and raises the
pulmonary PCO2, but its output is limited
because P c o , in venous blood is low (a few
Torr) as a consequence of its low value in
the arterialized blood which leaves the gillskin gas exchanger (see section I). Thus, the
pulmonary KlCO2 is quickly limited and the
pulmonary respiratory quotient, R, is low.
Reciprocally the cutaneous-branchial R, is
high, in such a way that the overallR is the
expression of the overall KtCO2 and td02 (Fig4) (Rahn et al, 1971; Burggren and West,
1982).
DUAL BREATHING AS ONE OF THE
CHARACTERISTICS OF AMPHIBIOUS LIFE,
A NECESSARY STAGE BETWEEN AQUATIC
AND TERRESTRIAL ABODES
Table 1 lists several physicochemical factors of water and air other than those resulting in respiratory adaptations. This long
table is however incomplete, e.g., the properties for light, for sound transmission, etc.,
are not mentioned. Since almost all properties of the milieus are different it is clear
that differences between aquatic, aerial and
amphibious animals are not restricted to
respiratory adaptations.
It is by studying these three categories of
animals that it is possible to figure out how
animal life, and certainly also plant life,
could start in water and colonize the open
land. Then the amphibious life appears to
182
PIERRE DEJOURS
garfish , Lepisosteus
osseus , 22CC
gill-skin
overall
Mco,
20
min- kg
10
lung
min- kg
FIG. 4. Carbon dioxide production, ldCO2, as a function of oxygen consumption, lCto,, in the garfish. The
slopes of the lines correspond to specific respiratory
quotients, R. Points indicate 1) the gill-skin O2-CO2
exchanges with a R value of 2.71 (upper left), 2) the
lung exchanges with a_R value of 0.09 (lower right); 3)
the overall M c o , and IVIQ, with a R value of 0.80 (from
Rahner ai, 1971).
be an intermediary and obligate stage in the
transition from water to land. There is no
paleontological or physiological evidence of
a direct passage from an aquatic to a terrestrial environment.
The most impressive amphibious animals are found among amphibians, particularly the anurans and, to a lesser extent,
the urodeles (Duellman and Trueb, 1986;
Hourdry and Beaumont, 1985). Figure 2
shows that the tadpole is a water breather
and the adult toad is intermediate between
a typical water breather, as the trout, and
an air breather, as the turtle. Between the
two stages, larval and adult, metamorphosis
TRANSPHYLETK
DIVISION
aquatic
occurs, during which the tadpole loses its
gills as lungs develop. It thus becomes a dual
breather, breathing air via the lungs and
exchanging gas through the skin either with
water or air. During metamorphosis, biochemical, anatomical and physiological
characteristics are progressively transformed. For example, most of the anurans
switch from ammoniotelism to dominant
ureotelism. They also pass from swimming
to walking and/or jumping. They economize water and may even live in arid environment, as long as the cutaneous loss is
decreased considerably as it is in the case
of the "water-proof treefrogs who also
switch to the formation of uric acid as a
nitrogen end product, which does not require
water to be disposed of. However, when an
adult air-breathing anuran returns to water
to overwinter or to lay eggs, its terrestrial
characteristics may decrease in intensity or
disappear; its cutaneous respiration becomes
relatively more important and the N-catabolism leads again to ammonia.
In amphibians, all the functions, respiration, water conservation, nitrogen end
product, locomotion, reproduction, vision
etc., are affected and pass at the time of
metamorphosis from an aquatic pattern to
a terrestrial pattern. It is also the case of
many amphibious fishes.
But there are also animals which are partially amphibious, in the sense that some of
their characteristics are aquatic while others
are terrestrial. For example cetaceans live
in water and swim, but they breathe with
lungs, are ureo- and uricotelic and reproduce like terrestrial mammals. But cetaceans descend from exclusively terrestrial
animals who reinvaded the aquatic habitat.
Other examples of incomplete amphibiousness exist among some crabs, some snails,
some aquatic insects with a gas gill, in
aquatic reptiles and birds.
CONCLUSIONS
PHYLOGENETIC
DIVISION
FIG. 5. Classical phylogenetic tree on which is superimposed a transphyletic division, based on the nature
of the milieu which entails special designs and functions in the different animal groups (Dejours, 1988).
Thus the problem of amphibious breathing cannot be viewed separately from all the
functions which are influenced by the nature
of the milieu where animals live (Dejours,
1979, 1988, 1989; Little, 1983; Moore,
1990). To succeed in the colonization of
land, it is necessary that all functions are
AMBIENT FACTORS AND AMPHIBIOUS BREATHING
183
vertebrates as a function of body temperature. Am.
J. Physiol. 218:600-606.
Jackson, D. C. 1987. How do amphibians breathe
both water and air. In P. Dejours, L. Bolis, C. R.
Taylor, and E. R. Weibel (eds.), Comparative physiology: Life in water and on land, pp. 49-58.
Springer Verlag, Berlin.
Lenfant, C. and K. Johansen. 1967. Respiratory
adaptations in selected amphibians. Respir. Physiol. 2:247-260.
Little, C. 1983. The colonisation of land. Cambridge
University Press, Cambridge.
McMahon, R. F. 1988. Respiratory response to periodic emergences in intertidal molluscs. Amer. Zool.
28:97-114.
Moore, J. A. 1990. The ability to live on dry land,
rather than in water, required major adjustments
in structure and physiology. Amer. Zool. 30:847849.
Rahn, H. 1966. Aquatic gas exchange: Theory. Respir. Physiol. 1:1-14.
ACKNOWLEDGMENTS
Rahn, H. 1967. Gas transport from the external enviI thank J. Armand, H. Beekenkamp and
ronment to the cell. In A. V.S. Reuck and R. Porter
(eds.), Development of the lung, pp. 3-23. Ciba
M. Schneider for their help in the prepaFoundation Symposium. J. & A. Churchill, Lonration of the paper and Dr. S. Dejours for
don.
reviewing the manuscript.
Rahn, H., K. B. Rahn, B. J. Howell, R. Gans, and S.
M. Tenney. 1971. Air breathing of the garfish
(Lepisosteus osseus). Respir. Physiol. 11:285-307.
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successfully adapted to their milieu. Such
statements are very vague, and raise the
problems of the mechanisms of adaptation
and evolution. But since aquatic life,
amphibious life, and terrestrial life are provided with similar adaptations related to the
milieu (respiration, water economy, ionic
excretion, nitrogen end product, locomotion, reproduction, communication, etc.), it
is obvious that onto the phylogenetic division of the animal kingdom must be superimposed a transphyletic division which
shows clearly the primordial aquatic life, the
transitional amphibious life and the terrestrial life (Fig. 5).