AMER. ZOOL., 13:505-512 (1973).
The Effects of Temperature on Respiration in the Amphibia
WALTER G. WHITFORD
Department of Biology, New Mexico Stale University, Las Cruces, New Mexico
88003
SYNOPSIS. The effects of temporal me on respiration in amphibians are primarily effects on gas exchange patterns and rate of oxygen consumption (Qo2) in major
groups of amphibians. In temperate zone amphibians except plethodontid salamanders, pulmonary oxygen uptake increases with temperature. In plethodontid salamanders cutaneous gas exchange predominates and increases at higher temperatures. Aquatic salamanders are characterized by a lower Q o than temperate amphibians at all temperatures. Tropical anurans have a Q o equivalent to temperate
amphibians at a tempcrarure 10 C greater. The ability of amphibians to supply their
tissues with oxygen and the effects of temperature on amphibian respiratory parameters are suggested as probable factors causing these relationships.
Recent evidence for temperature independent reduction in Q o in fossorial amphibians and species differences in metabolic scope is discussed.
An analysis of the effects of temperature
on respiration in the Amphibia is complicated by the combinations of respiratory
surfaces involved in amphibian gas exchange. Aquatic forms may use combinations of gills, skin, lungs, and buccopharyngeal surfaces in gas exchange (Guimond
and Hutchison, 1972). Terrestrial amphibians exchange respiratory gases via the skin,
lungs, and buccopharynx, but in some
forms (family Plethodontidae and representatives in two other families: Salamandridae and Ambystomatidae) lungs
have been lost and nearly all respiratory
exchange is cutaneous (Whitford and
Hutchison, 1965). Therefore, some of the
most interesting and important effects of
temperature on amphibians are on gas exchange patterns.
The relative roles of skin and lung-buccopharyngeal respiration have been examined in 14 species of salamanders representing three families and in 21 species of
anurans representing eight families. Two
patterns of gas exchange emerged when
these data were examined. The gas exchange patterns in lungless salamanders,
family Plethodontidae, at different temperatures are shown in Figure 1 (data from
I thank Robert Guimond, Victor Hutchison, and
Roger Seymour for providing me with manuscripts
and unpublished data. Fenton Kay assisted with
computer analysis of data. Victor Hutchison and
my graduate students critically reviewed the manuscript.
Whitford and Hutchison, 1965). Salamanders of the family Plethodontidae apparently lost their lungs as an adaptation to
life in or adjacent to rapidly flowing mountain streams (Dunn, 1926). In Plethodontid
salamanders between 82% and 95% of the
carbon dioxide elimination is through the
skin, and from 83% to 93% of the oxygen
uptake is through the skin. Figure 1 includes data from only one completely terrestrial plethodontid, Plethodon glutinosus.
Whitford and Hutchison (1965) found that
this species obtained significantly more
oxygen via the buccopharyngeal surfaces
than the other species. Based on data for
P. glutinosus at one temperature, 15 C, it
is probable that variation with temperature
in the gas exchange pattern of terrestrial
plethodontids would not be dissimilar to
that shown in Figure 1 except that the
buccopharyngeal surfaces might account
for a slightly greater percentage of the
total oxygen consumption.
In salamanders with lungs and in anurans (exclusive of tropical forms), the
variances in gas exchange values due to
body size partly account for the differences
in responses of the gas exchange patterns
to different temperatures. While the other
factors causing slight differences in gas exchange patterns between species may be
of interest, the general pattern of gas exchange response to temperature (see Fig.
2) is most instructive. Most of the carbon
dioxide exchange is cutaneous at all tem-
505
506
WALTER G. WHITFORD
•
O
A
A
Pul
Cut
Pul
Cut
O,
O,
CO,
CO,
E
5
10
15
20
26
30
TEMPERATUREt
FIG. 1. The effect of temperature on cutaneous and
buccopharyngeal gas exchange in plethodontid salamanders. The 15 C points are means for four species. At 5 C and 25 C data were available only for
Desmognothus quadramaculalus (Whitford and
Hutchison, 1965).
peratures, varying from 81% at 5 C to
76% at 25 C. The lungs supply from 32%
of the oxygen consumed at 5 C to 68% at
25 C. The increases in pulmonary oxygen
uptake and CO2 release are directly related to changes in breathing rates and
tidal volumes. Amphibians exhibit two
distinct types of breathing or pulsations of
the buccal floor: buccal oscillations which
move air back and forth across the buccopharyngeal mucosa, but do not result in
lung ventilation; and large buccal pulsations accompanied by opening and closing
of nares and glottis which result in lung
ventilation (Whitford and Hutchison, 1963,
1965; Hutchison et al., 1968; Gans and
Dejongh, 1969). The linear increase in pulmonary oxygen uptake (Fig. 2) is the result of increases in tidal volumes and
breathing rates. The rate and volume of
lung ventilation increase linearly with temperature (Hutchison et al., 1968), but
changes in rate of buccopharyngeal oscillations between species are variable. The
contribution of buccal oscillations to gas
exchange in amphibians in problematical.
This air exchange is the only means of air
movement available to plethodontids and
accounts for a small per cent of the total
gas exchange (between 15% and 25%)
(Whitford and Hutchison, 1965); however,
in amphibians with lungs, the contribution
of this movement of air to respiratory exchange has not been objectively assessed.
The rate of buccopharyngeal movements
in salamanders and frogs increases as a
function of temperature which suggests
that this mode of ventilation contributes
to the increased pulmonary gas exchange.
Das and Srivastava (1957) proposed that
the ratio between lung ventilatory movements and buccopharyngeal oscillations
was a constant (K) in various species of
amphibians. However, K varies considerably in the same species at different temperatures (Hutchison et al., 1968; Guimond
and Hutchison, 1968). If buccopharyngeal
oscillations serve primarily an olfactory
function as suggested by Matthes (1927),
Vos (1936), and Elkan (1955), it is not like-
•
O
k
A
Pul Oj
Cul O,
Pul CO,
Cul CO,
E
-a
„•*
5
W
15
TEMPERATURE
20
25
30
t
FIG. 2. The effect of temperatuie on gas exchange
patterns of salamanders with lungs and anurans.
Each point represents the average of published gas
exchange values (Whitford and Hutchison, 1963,
1965; 1966; Hutchison et al., 1968; Vinegar and
Hutchison, 1965; Guimond and Hutchison, 1968) .
TABLE 1. Pulmonary efficiencies in a variety of amphibian species at different temperatures.*
Species
Ambysioma maculatum
Tarica granulosa
Desmognathus quadramaculatus
Bufo americanus
Bufo ooreas
Bufo cognatus
Bttfo marinus
Bufo terrestris
Hyla versicolor
Rana catesbeiana
Jtana sylvatica
Xenopus laevis
Ceratophrys calcurntta
Kana pipiens
10
15
1.43
.81
0.93
0.79
0.731
0.31
1.20
1.00
1.00
0.21
Beference
Whitford and Hutchison (1963)
Whitford and Hutchison (1965)
Whitford and Hutchison (1965)
Hutchison et al. (1968)
2.241
0.14
0.92
0.36
0.38
0.10
1.00
0.21
Guimond and Hutchison (1968)
20
0.97
0.311
0.86
0.72
0.52
0.38
1.00
0.75
1.27
1.60
25
1.07
* Pulmonary efficiency is the volume of oxygen removed by the pulmonary surfaces divided by the
volume of oxygen inspired by both lung and buceopharyngeal ventilation. Volume of oxygen inspired
is calculated from ventilatory rates and tidal volumes.
1
Data on buccopharyngeal ventilation only.
ly that the rate of these movements would
respond to temperature in a linear fashion.
Although ventilatory rates and tidal volumes increase at higher temperatures in
amphibians with lungs, the per cent oxygen removed from inspired air by the pulmonary and buccopharyngeal surface does
not increase (Table 1). In some species pulmonary efficiency decreases gradually at
higher temperatures, but in some frogs the
efficiency at 15 C is higher than at 5 C.
The low efficiencies at all temperatures
strongly support the contention that the
forced pump ventilatory system in amphibians results in poor mixing in the
lungs (Gans, 1970). The variances in efficiencies could be due to a combination of
measurement technique and/or the varying
role of the buccopharynx in respiration in
different species.
Since respiratory surface area and effective volume of the buccopharyngeal cavity
used in pumping air into the lungs vary
as a function of body size expressed by
KWh, where b has a value less than 1, much
of the variation in gas exchange values may
be explained by variation in body size
(Whitford and Hutchison, 1967; Hutchison
et al., 1968). When body size is eliminated
as a variable, several generalizations concerning the effect of temperature on respiration in amphibians are apparent (Figs.
3, 4). Relationships of plethodontids and
tropical anurans at other temperatures are
missing because of insufficient data. Summarized, these generalizations are: (1) Tem-
perate zone anurans and salamanders with
lungs have higher rates of oxygen consumption (Qoo) than lungless salamanders
(Plethodontidae) at the same temperature.
(2) The oxygen consumption of tropical
anurans is equivalent to that of temperate
anurans at a temperature 10 C less than
—
—
TEMPERATE ZONE ANUHANS AND SALAMANDERS
PLETHODONTIDAE
SALAMANDERS AT 1S°C
TROPICAL ANURANS AT 25*C
40
«0 SO
GRAMS
FIG. 3. A comparison of the effects of temperature
on oxygen consumption in several groups of amphibians. The lines represent the best fit linear regression lines computed by least squares. Data are
from Dunlap (1971), Fitzpatrick et al. (1971, 1972),
Guimond and Hutchison (1968, 1972), Hutchison
et al. (1968), Jameson et al. (1970), Morris et al.
(1963), Packard (1971), Tashian and Ray (1957),
Vinegar and Hutchison (1965) , Whitford and
Hutchison
(1963, 1965, 1967), Whitford and
Sherman (1968), Whitford (1968), Wood and
Orr (1969), and Wood (1972).
508
WALTER G. WHITFORD
O2 = oxygen consumption in cc per hr and
W = weight in grams, are:
E
O
temperate amphibians
5C:logO 2 = —.97 + .65 log W.
15C:logO 2 = —.81 + .78 log W.
25C:log0 2 = —.45 + .67 log W.
tropical anuraiis
25C:logO. = — .714 + .71 log W.
Plothodontidae
15C:logO 2 = —1.36 + 1.17 log W.
aquatic salamanders
5C: —1.72+ .761ogTF.
15 C: —1.69 + .93 1ogTF.
25 C: —1.65 + 1.00 log W.
80
FIG. 4. The effects of temperature and body size
on several groups of amphibians. Data from sources
cited in Figure 3.
the temperature of the tropical frogs. (3)
The oxygen consumption of aquatic salamanders is significantly lower that that of
terrestrial salamanders at all temperatures.
(4) There is no significant difference in
oxygen consumption between temperate
zone frogs and salamanders with lungs.
The effect of temperature on these groups
of amphibians is predicted by the following equations where O2 is oxygen consumption in microliters per gram per hour and
T is temperature in degrees Celsius:
aquatic salamanders
Plethodontidae
Os = 1.8 + 1.05 T
O2 = 14.6 + 2.5 T
temperate lunged amphibians
O2 = 8.9 + 5.3 T
tropical anurans
O2 = —20.4 + 5.2 T
The variance in these data is largely due
to variations in body size that are not eliminated when oxygen consumption is
expressed on a unit weight basis. Therefore, the same data were used to compute
regression equations of log10 oxygen consumption and log]0 body weight which are
plotted in Figure 3. These equations, where
This analysis demonstrated that for the
groups with sufficiently large sample sizes
(all except aquatic salamanders) most of
the variance in oxygen consumption at a
given temperature was due to body size
(r2 values between .84 and .97).
The lack of difference in Q 02 in temperate zone frogs and salamanders at different temperatures reflects similarities in
gas exchange parameters in these species
and does not support the contention
(Salthe, 1965) that frogs generally have
higher respiratory rates than salamanders.
The rate of oxygen consumption in amphibians may be primarily a function of
the ability of the animal to obtain oxygen
from its environment. The allometry of
body surface and buccopharyngeal volume
have been shown to be probable determinants of rates of oxygen consumption
(Whitford and Hutchison, 1967; Hutchison
et al., 1968). The loss of lungs in the plethodontidae, as an adaptation to rapid
flowing stream habitats, eliminated a mode
of varying the oxygen supply at higher
temperatures by lung ventilation, thus relegating these amphibians to environments
characterized by temperatures below 30 C
(Brattstrom, 1963). Although over 100 species of plethodontid salamanders occur in
the neotropical region in a variety of forest
habitats, from lowlands to high paramo
(Brame and Wake, 1963), no physiological
data are available for any of these forms,
and consequently, generalizations concerning plethodontids must await data on neotropical plethodontids. In frogs as well as
in salamanders, the positive pressure ventilation system results in ineffective respira-
TEMPERATURE AND RESPIRATION IN AMPHIBIA
tory exchange (Gans, 1970). The rate of cutaneous oxygen exchange is a function of
the PO2 difference between skin capillaries
and the air. With changes in heart rate
and cardiac output as the only means available for establishing a more favorable
gradient, changes in the rate of cutaneous
oxygen uptake at higher temperatures decrease at higher temperatures. Thus, the
ability to supply oxygen to the tissues appears to be limited in lunged forms as well
as in plethodontids.
Reduced oxygen consumption in tropical
anurans when compared with temperate
forms reflects shifts in temperature optima
of enzyme systems. The Q 02 response
curves are similar to those of temperate
forms indicating that the similar gas exchange parameters are involved, but that
these have been adjusted in the evolution
of tropical species to respond to a higher
and more constant thermal environment.
Aquatic salamanders have lower rates
of oxygen consumption at all temperatures than any other group of amphibians
(Fig. 3). This relationship holds for very
small (Norris et al., 1963), intermediate
(Whitford and Sherman, 1968), and large
salamanders (Guimond and Hutchison,
1972). In arid environments metamorphosed salamanders are forced to spend
extended periods of time in an aquatic
environment. Under these circumstances,
Qo2 is reduced below that in air, but the
rate of surfacing and pulmonary gas exchange increases with temperature (Whitford and Sherman, 1968). Wood (1972) also
showed that the oxygen consumption of
transformed Dicamptodon ensatus measured in a water-air system, while significantly higher than in larval animals of the
same size, was lower than predicted for a
land dwelling salamander. This suggests
that the metabolic rates of aquatic amphibians have been evolutionally adjusted
to accommodate the lower availability of
oxygen in their environment. These data
also support the contention of Norris et
al. (1963) that amphibians are partial metabolic conformers with respect to oxygen
tension. At lower temperatures (15 C and
below) gas exchange in aquatic salamanders
509
appears to be primarily cutaneous (Whitford. and Sherman, 1968; Guimond and
Hutchison, 1972). Guimond and Hutchison
(1972) reported that, in Necturus maculosus
at higher temperatures or when excited,
the branchial surface assume the dominant
role in gas exchange. Wood (1972) reported
that in Dicamptodon ensatus larvae, gill
ventilation rate increased from 9 per min
at 10 C to 48 per min at 20 C, and at 20 C
the larvae surfaced to gulp air. Thus, higher environmental temperatures appear to
require active participation of respiratory
surfaces other than the skin in aquatic salamanders as well as in terrestrial amphibians.
Submerged frogs also exhibit reductions
in oxygen consumption (Jones, 1967, 1972)
which accommodate bradycardia. However,
this reduction in Q 02 appears to be dependent on oxygen tension because Jones
(1967) showed that R. pipiens submerged
in 100% oxygenated water showed no reduction in Q 02 and only slight bradycardia. Data on oxygen consumption in water
in aquatic frogs such as Pipa pipa, Xenopus
laevis, or Ascaphus truei would be of value
in determining if all groups of aquatic amphibians exhibit reduced Q02.
Variables other than differences in gas
exchange surfaces influence the interpretation of the effects of temperature on respiration in the amphibia. Season of the
year, photoperiod, and time of day have
been shown to affect gas exchange patterns
(Bohr, 1900; Krogh, 1904; Dolk and Postma, 1927; Long and Johnson, 1952; Vernberg, 1952; Fromm and Johnson, 1955;
Whitford and Hutchison, 1965; Vinegar
and Hutchison, 1965; Guimond and
Hutchison, 1968, 1972). In temperate zone
frogs, oxygen consumption peaked in the
spring, had a slight rise in the fall, and fell
to low levels in the winter. Photoperiod
effects on amphibian gas exchange patterns
are difficult to evaluate. Whitford and
Hutchison (1965) reported that at 15 C
Ambystoma maculatum had a significantly higher Q o , when acclimated to a 16-hr
photoperiod than at an 8-hr light period.
Guimond and Hutchison (1963) found that
in Rana pipiens photoperiod resulted in
510
WALTER G. WHITFORD
elevated Q 02 at 15 C, and Vinegar and
Hutchinson (1965) reported that photoperiod affected QO2 in Rana clamitans only
at 5 C. Guimond and Hutchison (1972) reported that photoperiod had no effect on
oxygen consumption or gas exchange patterns in the aquatic salamander, Nee turns
maculosus. In addition, there was no evidence in these studies that photoperiod affected the role of skin and lungs in respiration at different temperatures. Based on
the limited data in these studies, it appears
that photoperiod is a minor variable in
comparison with temperature as a factor
affecting respiration in amphibians. The
seasonal changes are more difficult to evaluate because of complications of temperature acclimatization, photoperiod, and the
time of day at which measurements were
made. In the only report dealing with
daily cycles and photoperiod acclimation
in amphibians, Guimond and Hutchison
(1968) found that QO2 was elevated at the
beginning of the dark cycle and that differences in photoperiod altered the onset of
maximum and minimum Qo.,.
Standard or resting measurements of a
physiological process in response to an environmental parameter provides only a
partial picture of the effects of an environmental variable. There are scant data on
respiration in ectotherms during activity,
and data on respiration during activity in
amphibia are limited to a single report by
Seymour (1973«). He found that the metabolic scopes (active oxygen consumption
minus resting oxygen consumption) in
Scaphiopus hammondi and Biifo cognatus
increased greatly at successively higher
temperatures and were considerably greater
than those for two species of Rana studied
(Fig. 5). The greater metabolic scope in
toads is apparently related to their fossorial habits. Seymour (1973a) calculated
that spadefoot toads have an elevated oxygen consumption during digging and shortly thereafter to repay an oxygen debt and
pointed out that burrowing activity and
movement in the soil is characteristic of
these animals. Thus, a high metabolic scope
is advantageous in an ectotherm that engages in digging. He also calculated that
—
Scaphiopus
hammondii
' — Birfo cognatus
Rana caiesbeiana
- * — Rana ptptens
8
oe
y
2
TEMPERATURE
X
FIG. 5. The metabolic scope in four species of
anurans at different temperatures. Metabolic scope
is the active oxygen consumption minus the resting oxygen consumption. (Redrawn from Seymour,
1973a.)
the metabolic rate of active spadefoot toads
is 95% of the predicted basal metabolic
rate of a mammal. These studies demonstrate that both the response to temperature and the magnitude of metabolic scope
differ in species of amphibians having the
same resting gas exchange pattern and
resting respiratory rate. Since the species
studied occupy different habitats and have
different habits, generalizations concerning
the significance of these differences must
await further studies.
It is evident from the preceding discussion that respiration in amphibians is primarily a temperature-dependent process.
However, there are species of amphibians
in which there are temperature-independent changes in respiration. There is a
large body of literature dealing with temperature acclimation in amphibians which
results in some degree of temperature compensation and, thus, temperature independence depending on acclimation status
and temperatures at which Qo.2 was measured. (See Fitzpatrick et al., 1971, 1972,
and Dunlap, 1971 for a review of the litera-
TEMPERATURE AND RESPIRATION IN AMPHIBIA
511
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Dolk, H. E., and N. Postma. 1927. t)ber die Haut
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Dunlap, D. G. 1971. Acutely measured metabolic
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Dunn, E. R. 1926. The salamanders of the family
Plethodontidae. Smith College, Northampton,
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Elkan, E. 1955. The buccal and pharyngeal mucous
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Fitzpatrick, L. C, J. R. Bristol, and R. M. Stokes.
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Fitzpatrick, L. C , J. R. Bristol, and R. M. Stokes.
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TEMPERATURE °C
Cans, C. 1970. Respiration in early tetrapods—the
frog is a red herring. Evolution 24:723-734.
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sumption of spadefoot toads resting on the surface
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in oxygen consumption in dormant spade- Guimond, R. W., and V. H. Hutchison. 1968. The
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gen consumption between 75% and 85% Cuimond, R. W., and V. H. Hutchison. 1972. Pulmonary, branchial and cutaneous gas exchange
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Metabolic and morphological adaptation to heterogenous environments by the Pacific tree toad,
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