Download Responses to Rapid Temperature Change in Vertebrate Ectotherms

AMER. ZOOL.,19:225-237 (1979).
Responses to Rapid Temperature Change in Vertebrate Ectotherms
LARRY I. CRAWSHAW
Departments of Rehabilitation Medicine and Pharmacology, College of Physicians and
Surgeons, Columbia University, New York, Netu York 10032
SYNOPSIS Vertebrate ectotherms often encounter rapid, large scale changes in body temperature. In this paper, I discuss the direct effects of changing body temperature on physiological parameters, as well as corrective responses initiated by the animal. For many
biological functions, mean body temperature provides a useful measure of the thermal
effects produced by an altered environmental temperature. Under most conditions, the
fins and body surface of fish are more important avenues of heat exchange than the gills.
The local thermal sensitivity of peripheral blood vessels results in vasomotor adjustments
which can alter thermal conductivity. Acid-base balance is challenged by changes in body
temperature. Shifts in body temperature also alter metabolic demands, enzyme conformation, ionic and osmotic relationships, spontaneous activity levels and nervous system function. Compensatory mechanisms include behavioral thermoregulation, by which animals
seek to avoid stressful thermal environments, and autonomic restorative responses such as
high temperature panting in reptiles. Water breathers may initiate anticipatory responses
to minimize arterial oxygen fluctuations during termperature change. The organization of
the central neuronal network underlying the above regulatory responses is unclear. Both
air and water breathers are able to initiate compensatory acid-base responses, but the
strategies utilized by the two groups are quite different. Altered body temperature initiates
long-term acclimation responses, and if rapid, can also trigger stress responses.
INTRODUCTION
In this paper, I will explore some of the
events that ensue when the thermal environment of a vertebrate ectotherm is
rapidly altered. This paper is not intended
as a comprehensive review; rather, it is intended to provide insights into some important aspects of the myriad changes that
take place following body temperature
changes in these animals. The topics
treated have been placed in two broad
categories: 1) the direct effects that an altered environmental temperature has
upon the various tissues of the animal, and
2) homeostatic mechanisms, which the
I thank Drs. E. R. Nadel, S. S. Hillman, W. W.
Reynolds, E. N. Smith, G. L. Florant and Mr. D. E.
Lemons for providing helpful criticism and discussion of this paper. During preparation of this article,
the author was supported by NSF Grant PCM 7609658 and N1H Grant 1-R01 NS15318-01 and the
general fund of the Department of Rehabilitation
Medicine. The supportive and stimulating atmosphere created by Drs. J. A. Downey and L. J. Cote is
most appreciated. This publication and the symposium were made possible by NSF Grant PCM 7805691 to W. W. Reynolds.
animal actively initiates to minimize or
eliminate the deleterious effects of rapid
thermal change. In the first category, I will
cover the effect of changing environmental
temperature on heat balance, acid-base
balance, metabolic rate, peripheral blood
flow, locomotor activity, ion and water
flux, enzyme systems and the nervous system. In the second category, I will evaluate
some of the active adjustments made by
ectotherms in the face of changing temperature: behavioral thermoregulation, autonomic thermoregulation, feed-forward
(anticipatory) autonomic adjustments,
neuronal mechanisms underlying the three
preceding adjustments, acid-base adjustments, hormonal responses and long-term
acclimation.
DIRECT EFFECTS OF ALTERED ENVIRONMENTAL
TEMPERATURE
Heat exchange
The predominant modes of head transfer depend upon the nature of the surrounding environment. For aquatic ani-
225
226
LARRY I. CRAWSHAW
mals, conduction (and its facilitation by that most of the heat exchange in fish occonvection) is of primary importance. In curred at the gills, but recent measureterrestrial animals, radiation and evapora- ments on sea ravens (Hemitripterus amerition are also substantial factors. Because of canus) indicate that 70-90% of the metathe high thermal conductance and heat bolic heat is lost through the body wall and
capacity of water, thermal shifts in aquatic fins (Stevens and Sutterlin, 1976). Slightly
organisms are typically more rapid. With lower estimates (40-70%) were arrived at
the exception of thermally stable environ- (Sorenson and Fromm, 1976) by measurments, the temperatures found in various ing heat transfer at isolated-perfused gill
portions of the body of an ectotherm are arches of rainbow trout, and by utilizing a
determined by a complex weighting of tubular heat exchange model. Crawshaw
thermal environments encountered in the (1976) demonstrated that different body
sites were differentially affected by temrecent past.
Experiments designed to investigate peratures at the gills and body surface of
rapid temperature changes in ectotherms carp. When the mouth, buccal cavity and
often involve a step change from one con- gills (inspiratory temperature) were mainstant temperature to another. A deep body tained at one temperature and the retemperature (such as that in the esoph- maining body surface at another, internal
agus, stomach, rectum, heart or brain) is temperatures attained stable values. The
monitored to assess the rapidity with which relative influence of inspiratory temperathe animal's body temperature is altered by ture was as follows: brain temperature,
the new environment. Although such point 68%; deep dorsal muscle temperature,
measurements appear easy to characterize 50%; intestinal temperature, 30%.
in terms of Newton's law of excess temperWhen water temperature changes
ature (Bartholomew and Tucker, 1963; rapidly, the body surface and fins account
Stevens and Fry, 1970, 1974), they belie for a particularly large proportion of the
the speed with which the whole animal's heat transfer. Consider the heat loss by the
tissue temperatures change. Generalized carp illustrated in Figure 1. Fifty percent
effects of changing temperature on such of the change in mean body temperature
parameters as metabolic rate or acid-base occurred in about 1.25 min, with a loss in
balance are well indicated by the mean tis- body heat content of:
sue temperature of an animal. Such de(558g) (0.83 cal-g--1 "C"1) (4.2°C)
terminations have been made by placing
= 1945cal(8138J)
ectotherms in a calorimeter at a temperature different from that of the constant Where: 558g = mass of 1carp
0.83 cal-g--' "C"
temperature holding tank. Results from
= specific heat of whole animal
such experiments on a carp, (Cyprinus car4.2°C = change in T b
pio), a lamprey (Lampetra tridentata) and a
turtle {Pseudemys scripta) show the rapidjty The heat loss through the gills during
with which mean body temperature (Tb) this period can be estimated by assuming a
changes as compared to changes in core cardiac output of 0.020 ml-g-~'min~' for
temperature (Fig. 1).
this fish (Randall, 1970), and that 85% of
General aspects of heat exchange in ec- the excess heat in the blood is lost during
totherms can be found in a number of passage through the gills (Stevens a>nd
sources (Bakken and Gates, 1975; Stevens Sutterlin, 1976).
and Sutterlin, 1976; Erskine and Spotila,
(0.85) (558g) (0.02 ml-g-^mirr 1 )
1977). One area of recent interest involves
(1.25 min) (9.2°C)
the amount of heat transfer occurring at
(0.92 cal-g--|OC-')
the gills in fish. It was previously thought (1.06 g-ml-1) = 106 cal (443.5J)
FIG. 1. Changes in mean body temperature (Tb),
brain temperature (Tbr). dorsal muscle temperature
(Tdm). intestine temperature (Tln), heart temperature
(T,,e) and heart rate (HR) following placement of (a) a
lamprey, (b) a carp and (c) a turtle at one temperature
into a calorimeter of another temperature. (From
Lemons and Crawshaw, 1978; Crawshaw, 1976; and
Crawshaw et al., 1978)
227
ECTOTHERM RESPONSES TO TEMPERATURE CHANGE
m
•
0
*'
( a ) . 2 0 6 kg Lamprey
I 2 3 4 5 6 7 8 9 10 II 12 13 14 15 16
25
( b ) 0.556 kg CARP
500
r
k^OO
I
300 -S; 20
200
8
i
100
0L
|
I5L
35
30
25
25
l 5
20
( c ) . 8 4 7 kg TURTLE
* HR
15
10
5
0
2
4
6
8
MINUTES
10 12
228
LARRY I. CRAWSHAW
Where: 9.2°C = mean temperature dif- ature, although effective in altering beference between gills and envi- havioral thermoregulation (Myhre and
ronment
Hammel, 1969), does not affect heating
0.92 cal-g-- lo C-' = specific heat and cooling rates in this animal. Also unafof blood (Stevens and Sutterlin, fected is the rate at which marginal vessels
1976)
refill after the blood is expressed by appli1.06 g-ml~' = density of blood
cation of gentle pressure (Hammel, per0.85 = proportion of excess heat sonal communication). Spray and May
lost during passage through gills
(1972), however, provide suggestive eviThus, when this carp was placed in cooler dence for the involvement of a regulatory
water, about 5%, (106 cal/1945 cal) of the system: thermal hysteresis was abolished in
heat exchange that occurred during the the turtle (Chrysemys picta belli) following
first 1.25 min took place at the gill surface.
section of the dorsal roots innervating its
In reptiles and amphibians, evaporation carapace. Unless the sectioning in some
and radiation are also important modes of way interfered with the sympathetic innerheat transfer. In these animals, as well as in vation of the peripheral vessels, their data
the aquatic vertebrates, skin blood flow is suggest the necessity of sensory input for
critical in determining the rate at which the thermal hysteresis.
heat is delivered to the body surface and
dissipated to the environment. These pe- Cardiovascular system
ripheral blood vessels dilate when the skin
is heated and constrict when the skin is
The heart-rate hysteresis, typically seen
cooled. These characteristic responses when vertebrate ectotherms are heated
have been documented visually (Cowles, and cooled (Reynolds, 1977) — heart rates
1958; Heath etal., 1968; Voigt, 1975), and are typically higher at a given body temwith i:i:!Xe clearance (Morgareidge and perature during heating—is largely due to
White, 1969; Weathers and White, 1971) two factors. First, heart temperature
in several species of reptiles.
changes more rapidly than body temperMost vertebrate ectotherms heat faster ature (see Fig. lc), producing a direct
than they cool (Bartholomew and Tucker, thermal effect (underestimated by mea1963; Fry and Hochachka, 1970; Spray surements of cloacal or intestinal temperand May, 1972; Spigarelli et al., 1977; see ature) on the tissue of the heart (Spray and
Smith, 1979 [this series] for a discussion of Belkin, 1972). Second, cutaneous blood
thermal relationships in crocodilians), al- How increases in response to heating prothough the opposite effect is sometimes duce an augmented cardiovascular deseen (Spray and May, 1972; Reynolds, mand, which is met by increasing heart
1977). This thermal hysteresis is occasion- rate (Weathers and White, 1971). Voigt
ally referred to as physiological control or (1975) found that the desert tortoise
thermoregulation, implying active control (Gopherus agassizii) is chronically vasodiby the animal (Bartholomew et al., 1965; lated, and therefore heats and cools at the
Smith, 1976; Reynolds and Casterlin, same rate in the laboratory. Nevertheless,
1978), but little evidence exists to implicate heating rates in the field were up to ten
the involvement of a thermally sensitive times faster than cooling rates, leading
regulatory system (which entails sensors, Voigt to suggest that in the case of terrescomparators and effectors). Rather, local trial ectotherms, behavioral postures and
vasomotor effects alter thermal conductiv- activities can be more important than
ity at the body surface. The Australian physiological adjustments in the determiskink (Tiliqufi scincoides) heats faster than it nation of thermal exchange rates.
cools (Bartholomewetal., 1965). When the
Specialized anatomical arrangement of
skin of these animals is warm, the vessels the vasculature can also beneficially alter
on the margin of the ventral scales dilate, heat exchange in ectotherms. The most
producing a visibly reddened belly. Ma- familiar example is the vascular counternipulation of anterior brainstem temper- current heat exchanger present in tuna
ECTOTHERM RESPONSES TO TEMPERATURE CHANGE
and lamnid sharks. The exchanger allows
the maintenance of temperatures well
above ambient in deep muscles (Carey,
1973; Dizon and Brill, this symposium).
The heat exchanger also functions very effectively as a barrier to environmentally
induced thermal fluctuation; this is likely
its primary function in small tuna. Skipjack
tuna {Katsuwonus pelamis) exchange heat
with the environment at only half the rate
of typical fish (Stevens et at., 1974).
Acid-base balance
As animals heat or cool, important
changes occur in their acid-base status.
The effect of this changed status is quite
different for animals that breathe air or
water. These effects have been the subject
of several recent, excellent reviews (Randall, 1974; Rahn, 1976; Reeves, 1977),
which should be consulted for a more detailed exposition.
If the temperature of vertebrate blood is
increased in vitro (with a constant CO2
content), pH decreases and PCo2 increases.
The pH change is due mainly to a temperature induced increase in the dissociation
of histidine imidazole groups of proteins.
The altered pH, and the change in CO2
solubility predict changes observed in Pco-2These temperature related changes are
such that protein charge states remain constant (Reeves, 1976). These acid-base alterations are actively defended by ectotherms, and are referred to as the maintenance of a constant relative alkalinity
(Rahn, 1976) oralphastat regulation (Reeves,
1972, 1977). Enzyme optima follow a
similar temperature dependence (Hazel et
al., 1978), and apparent Michaelis-Menten
constants (Km values) of different vertebrate M4-lactate dehydrogenases are conserved only if the pH of the assay medium
is varied in a manner consistent with the
changes described above (Yancey and
Somero, 1978). These changes occur automatically, because of the effects of temperature on chemical equilibria. Their
maintenance requires adjustment of the
animal's acid-base metabolism, and will be
discussed under the category of active adjustments.
229
Metabolic rate
Many studies document the increased
metabolic rate that vertebrate ectotherms
maintain at higher body temperatures
(Whittow, 1970). Much evidence is based
on acclimated animals; less well-appreciated is the fact that rapid, but relatively
small thermal alterations can produce large
metabolic changes. Thus, Meuwis and Heuts
(1957) observed that the respiratory frequency of carp (Cyprinus carpio) doubled
following a temperature increase from
32°C to 36°C. As thermal acclimation occurred, the ventilation rate decreased.
Forty-eight hours after the temperature
increase, the ventilation rate was only elevated by 15 percent.
Instantaneous temperature compensation
Large metabolic changes following shifts
in body temperature are minimized in
some animals by mechanisms of instantaneous temperature compensation. Such
mechanisms are most highly developed in
intertidal invertebrates (Newell, 1969), but
are probably present to some extent in vertebrate ectotherms. Postulated modes of
operation of "instantaneous" thermal
compensation include thermal effects on
enzyme-substrate interaction and thermally induced alterations in enzyme structure (Hazel and Prosser, 1974). These
changes operate to counteract the usual
accelerant effect of increased temperature
on chemical reactions.
Osmotic and ionic balance
Water breathers may encounter disruptions of osmotic and ionic balance following moderate or large temperature shifts.
These disruptions are most pronounced
when temperatures near the upper or
lower survival limit are encountered anddepend upon both the rate and amplitude
of temperature change. In fish, gills are a
major site for both active and passive ionic
exchange with the environment, and the
large scale respiratory changes that occur
during alterations in body temperature in-
230
LARRY I. CRAWSHAW
duce problems in electrolyte balance
(Houston, 1973).
In the eel {Anguilla anguilla), Motais and
Isaia (1973) found that water flux increased with increasing acclimation temperature. Rapid increases in temperature
produced fluxes greater than those present in animals acclimated to the increased
temperature, while decreases in temperature produced exactly the opposite effect.
These effects would be predicted from the
changes in respiratory activity induced by
thermal changes. Diffusion and transport
processes at the membrane sites are also
temperature-dependent. In goldfish (Carassius auratus) and salt water adapted flounders (Platichthysjiesus) passive Na+ flux exhibited a much smaller temperature dependence (Qm=2) than active Na + /K + exchange mechanisms (Qi<>=3 — 6) (Maetz,
1.972; Maetz and Evans, 1972). At low
temperatures then, active exchange mechanisms may have insufficient capacity in
relation to passive ion movements, while at
high temperatures, survival problems may
be related to high absolute levels of ion
flux. Ion transport mechanisms are also affected by hormone secretions, which will
be discussed subsequently.
Activity
via the hypothalamic thermoregulatory
centers, since cooling of the anterior brainstem in brown bullheads (Ictalurus nebulosus) led to decreased activity (Crawshaw
and Hammel, 1974).
Nervous system function
In addition to effects on the motor centers, temperature changes involving the
whole organism affect all aspects of nervous system function. Most sensitive are
highly organized systems involving many
synapses. Conditioned reflexes are more
sensitive than direct reflexes, which are in
turn more sensitive than peripheral nerve
conduction (Prosser, 1973; Lagerspetz,
1974). Since physiological regulatory systems involve intricate neural networks, the
complexity of the homeostatic responses to
thermal change in ectotherms can be readily appreciated.
HOMEOSTATIC MECHANISMS
Behavioral thermoregulation
Vertebrate ectotherms possess a number of interacting homeostatic systems
which serve to minimize the deleterious effects of rapid temperature change. Thermal stresses can often be abated by appropriate selection of a microclimate, and such
behavioral thermoregulation is often a
major determinant of the overall activity
pattern of ectotherms (Whittow, 1970).
The ability to sense peripheral temperature change is well-developed in ectotherms (liardach, 1956; Dizon etal., 1974;
Dizon et al., 1976), and has been implicated
in the regulation o( body temperature in
these animals (Myhre and Hammel, 1969;
Crawshaw and Hammel, 1971, 1974). The
temperature of the anterior brainstem
(Myhre and Hammel, 1969; Crawshaw
and Hammel, 1971, 1973, 1974) and spinal
cord (Duclaux etal., 1973) is also important
in this regard.
Temperature change by itself raises the
level of spontaneous activity in fish (Peterson and Anderson, 1969; Olla and Studholm, 1971; Stevens, 1972), thus increasing the metabolic rate. Friedlander et al.
(1976), studying goldfish, found the cerebellum to be an important mediator of activity level. The behavioral sequence of
events which followed whole animal heating or cooling (hyperexcitability, motor incoordination, disequilibrium and areflexia)
was also induced by heating or cooling the
cerebellum. In cerebellectomized fish, less
heating or cooling was needed to elicit
hyperexcitability and the subsequent lack
of coordination. Further, electrical activity
of inhibitory cerebellar interneurons and
Purkinje neurons was disturbed by the
same alteration in body temperature as the Autonomk thermoregiihition
behavioral events. Thermal effects on sponCertain reptiles and amphibians appaitaneous activity are probably not mediated ently utilize the sensing and integrating
231
ECTOTHERM RESPONSES TO TEMPERATURE CHANGE
portions of the above thermoregulatory were immobilized with gallamine triethionetwork to modulate evaporative heat loss dide, indicating that the observed effects
in warm environments. These reptiles in- were not secondary to induced changes in
crease evaporative heat loss by panting and activity. Very rapid changes in ambient
frothing when very high temperatures are water temperature (3°C in 15 seconds)
encountered (Schmidt-Nielsen and Daw- produce alterations in ventilatory minute
son, 1964; Cloudsley-Thompson, 1968, volume in carp (Cyprinus carpio) which are
1970). Autonomic thermoregulatory re- rate sensitive (Crawshaw, 1976) and altersponses, like behavioral thermoregulatory ations in ventilation and cardiac frequenresponses, are influenced by ambient, cies in lampreys (Lampetra tridentata) which
brainstem and core temperatures (Craw- occur too rapidly to be due to changes in
ford and Barber, 1974; Morgareidge and brain temperature or mean body temperHammel, 1975). Panting thresholds in the ature (Lemons and Crawshaw, 1978).
lizard {Amphibolurus muricatus) are elevated Similar changes do not occur in the turtle
by increased acclimation temperatures and (Pseudemys scripta) (Fig. 2).
longer photoperiods (Heatwole et al.,
1975). The cutaneous mucous glands of
the bullfrog (Rana catesbeiana) function
during basking to keep the animal's integument moist. It appears that these
8!
glands are influenced by thermoregulatory
IK)
neuronal networks, since mucous dis0.206 kg
charge rates are increased by heating of
LAMPREY
the head and decreased by brain transection below the level of the anterior
1 ^
90
hypothalamus (Lillywhite, 1971).
I
Feed-forward autonomic adjustments in water
breathers
As compared to air, water has a low oxygen content, low diffusion rate and a high
viscosity. In water breathing ectotherms
the maintenance of an adequate oxygen
supply is of paramount importance, and
the maintenance of blood oxygen levels
takes precedence over CO2 elimination
(which occurs readily because of its high
solubility) (Randall, 1974). There is some
evidence that the thermoregulatory system
is involved in maintaining oxygen supplies
during conditions of rapid thermal
change. Increasing and decreasing the
anterior brainstem temperature of the
California scorpionfish (Scorpaena guttata)
caused proportional increases and decreases in the ventilatory minute volume.
These changes were related to the absolute
temperature, and not the rate of change
(Crawshaw et al., 1973). The temperature
of the spinal cord has been shown to affect
heart rate (Iriki et al., 1976; Nagai and
Iriki, 1977). In some experiments the fish
SB 80
280k
I 23°
,. 180
0.821kg
TURTLE
u
>
^20
0
1
2
3
4
TIME (MIN)
FIG. 2. Changes in ventilatory and circulatory
parameters when ectotherms encounter rapid decreases in water temperature. Temperature change
was initiated at t=0, and took about 20 sec to complete. The decrease was 3°C for the lamprey and
carp and 10°C for the turtle.
232
LARRY I. CRAWSHAW
Behavioral and autonomic responses to
temperature change in fish and mammals
have many similarities. Both response systems are similarly controlled in that
peripheral and anterior brainstem temperatures are transduced and integrated to
produce a restorative response of the appropriate direction and magnitude. In
both classes, the absolute peripheral temperature and the rate of peripheral temperature change are important inputs to
the thermoregulatory centers (Cabanac,
1975). In the anterior brainstem only the
absolute temperature appears important
in the determination of the regulatory response (Hammel, 1968). Fish and mammals both utilize behavioral responses to
avoid noxious temperatures; failing this,
autonomic responses are activated. In
mammals, these responses (such as shivering or panting) serve to maintain internal temperature. Although most fish cannot maintain a constant internal temperature, they could utilize the thermoregulatory network to anticipate the physiological
changes which inevitably accompany thermal change. This feed-forward system
would allow water breathers to initiate restorative responses in important regulated
variables without the necessity of incurring
a deficit to furnish the appropriate error
signal. Water breathing vertebrates may
have evolved such a control system, subsequently modified by air breathers in the
development of endothermy.
The rapid increases in ventilation and
heart rate which occur following increases
in surface, anterior brainstem and spinal
cord temperatures could serve to maintain
arterial PO2 levels during the inevitable increases in metabolism. Prompt decreases in
cardiovascular and respiratory activity
following the detection of decreased temperatures could minimize the expenditure
of energy necessary for gill ventilation and
active ion transport during periods of
rapidly falling metabolic requirements.
Neurons involved in temperature regulation
The characteristics of peripheral temperature sensitive neurons in amphibians
(Spray, 1974) appear very similar to the
well-studied corresponding neurons in
mammals (Hensel, 1973a). The identification of central neurons involved in temperature regulation has been difficult. Although both warm and cold sensitive neurons have been located in the anterior brainstem of fish (Greer and Gardner, 1970,
1974; Nelson, 1978), reptiles (Cabanac et
al., 1967) and mammals (Hensel, 19736), it
is unclear whether these neurons are actually involved in thermoregulation. Pekin
ducks do not respond to anterior brainstem heating or cooling with thermoregulatory responses, yet a normal population
of warm and cold sensitive neurons was
found when the hypothalamus of a conscious duck was probed with microelectrodes (Simon et al., 1977).
Feed-forward autonomic adjustment in air
breathers
It has been suggested that reptiles also
utilize the thermoregulatory network to
anticipate metabolic deficits, since alterations of the anterior brainstem temperature produce changes in blood pressure
(Rodbard et al., 1950; Heath et al., 1968)
and oxygen uptake (Siegel and Privitera,
1976) in turtles. Although the metabolic
requirements of reptiles do indeed increase with temperature, it seems unlikely
that active regulation is involved in anticipating oxygen requirements. Rather, in
these air breathing ectotherms acid-base
regulation is more primary. The effects
that anterior brainstem temperature manipulations have on blood pressure and O2
uptake in reptiles is difficult to interpret,
but non-specific excitation of systems involving behavioral arousal or vascular resistance could be involved.
Acid-base regulation in air breathers
In air breathers, appropriate acid-base
balance is maintained in the face of thermal change (while maintaining a constant
total CO2 concentration) by altering the
ratio of pulmonary ventilation to metabolic
CO2 production. The turtle (Pseudemys
scripta) has been shown to make such adjustments promptly after shifts in body
233
ECTOTHERM RESPONSES TO TEMPERATURE CHANGE
temperature Jackson and Kagen, 1976).
These adjustments allow reptiles not only
to tolerate, but actively to initiate large
changes in body temperature. Thus Pearson and Bradford (1976) report that the
Active gill ion exchange mechanisms are
utilized by fish for ionic regulation: C1~V
H C ( V exchange, and Na+/NH4+ or H +
exchange (Evans, 1975; Maetz, 1976). It
has been suggested that these exchange
iguanid lizard (Liolaemus multiformis) basks mechanisms are involved in the pH adin early morning sunlight and raises its justments induced by thermal shifts (Ranbody temperature from 5°C to 30°C in dall and Cameron, 1973). There is a large
about 30 minutes, and Crawshaw et al. body of suggestive data, but this hypothesis
(1978) found that turtles (Pseudemys scripta) has not been clearly demonstrated to date.
acclimated to 3°C for three weeks, selected It is of interest, however, that the trout
water above 30°C in less than one hour. (Salmo gairdneri), which has a rather poor
Other factors favoring adjustment to rapid ability to tolerate alterations in body temthermal change in reptiles include oxygen perature, also has a relatively weak Cl~/
availability and a greatly decreased ex- HCO:i~ exchange process (Janssen and
change of ions and water between the Randall, 1975). The eurythermal killifish
animal and the environment.
(Fundulus heteroclitus) has a very active
Amphibians occupy an intermediate po- C1 ~/HCO:i~ exchange, present not only on
sition between reptiles and fish, since the the gill surface, but also on the opercular
skin and the lungs are both important res- epithelium (Karnaky and Kinter, 1977;
piratory organs. Mackenzie and Jackson Deghan et al., 1977). However, pH imbal(1978) determined that acid-base regulation during temperature change in the
20
30
40
50
bullfrog (Rana catesbeiana) was accom1
>-10°C
plished by ventilatory adjustments. Skin
30
40
50
CO2 conductance (skin CO2 loss/transt7°C
cutaneous Pco2) w a s n ° t significantly affected by temperature.
Acid-base regulation in water breathers
Water breathers face a difficult problem
in making acid-base adjustments to altered
body temperature. Since water has a relatively low O2 content and a high CO2 solubility, fish closely regulate arterial PO2
levels, with arterial PC02 remaining at fixed
levels slightly ( 2 - 5 mm Hg) above the PC02
of the breathing medium (Randall and
Cameron, 1973; Janssen and Randall,
1975). Changes in ventilation cannot be
utilized to maintain blood pH at appropriate levels, and following a rapid shift in
body temperature water breathers experience an acid-base imbalance. This imbalance is corrected by alterations in bicarbonate excretion (Randall and Cameron,
1973; Cameron, 1976; Romanenko and
Kotsar, 1976), which may take hours or
days to complete. In Figure 3 a Davenport
diagram (Cameron, 1976) depicts the
acid-base events in a salmonid following a
change from 10°C to 17°C water.
8
.2 4 ° 22
1 I I |/|
7-9
I I I /I
10 C
,2
I
I -I
80
PH
I I I I I I I I
X I
FIG. 3 . D a v e n p o r t d i a g r a m showing acid-base
events caused by a temperature increase in a salmonid. T h e normal animal acclimated to 10°C has
values corresponding to point A, with an O H " / H +
ratio of about 33. T h e passive pH change caused by
pK temperature-dependence causes a shift to B, with
dpH/°C=0.003. Subsequent reduction of HCO,* by
exchange lor Cl~ leads to a new steady state at C,
which yields the same O H " / H + ratio of 33. Broken
lines with numbers show P c ( h isolines. Figure and
adapted caption from Cameron (1976).
234
LARRY I. CRAWSHAW
ances considerably greater than those produced by rapid alterations of body temperature are tolerated during exercise or
manipulation of pH or PC02 within the arteries or in the inspired water (Janssen and
Randall, 1975; Daye and Garside, 1975;
Wood etal., 1977).
The central nervous system sites and
modes of sensitivity involved in ectotherm
acid-base regulation are unclear, although
the theoretical requirements of such a system have been discussed (Reeves, 1976).
Stress responses
Large, rapid shifts in ambient temperature elicit generalized stress responses.
Chowers et al. (1964), found that rapid
lowering of the ambient temperature to
0°C elicited cortisol secretion in dogs, as
did acute lowering of the preoptic/anterior
hypothalamic temperature. Gradual cooling (over 45 minutes) produced no elevation in plasma cortisol. The corticoid stress
response in fish is also affected by increasing or elevated temperatures (Strange et
al., 1977). Such responses are particularly
important in fish and amphibians, since
adrenal and pituitary hormones produce
alterations in ion permeability and ion
transport (Evans, 1975; 1978; Sawyer et al.,
1978), as well as generalized effects on
metabolism.
Long-term acclimation
As the acute physiological responses are
mobilized to meet the demands of altered
body temperature, long-term adjustments
are initiated which enable the animal to
operate more efficiently at the new body
temperature (Hazel and Prosser, 1974).
The overall acclimation response involves
a complex interaction between physiological, hormonal and cellular processes, and
takes place over a period of hours and
days. The central nervous system is important in the response (Lagerspetz, 1974),
but its exact role remains unclear, as does
the nature of the primary inducing stimulus at the cellular level. It is clear that
many changes involve "feedback to the
genetic material. . ., and subsequently to
the protein synthetic system" (Hazel and
Prosser, 1974).
CONCLUDING REMARKS
Dynamic situations, such as rapidly changing temperatures, are difficult to investigate and are therefore studied less than
steady state conditions. Most animals, however, regularly experience changing environmental conditions to which they must
sense and respond appropriately. The rate
of thermal change provides an important
input in the elicitation of regulatory responses and is critical in the determination
of stressful and lethal conditions. Changing temperatures produce effects which
are fundamentally different depending on
whether vertebrate ectotherms breathe air
or water.
REFERENCES
Bardach, J. E. 1956. The sensitivity of the goldfish
Carassius auratus L. to point heat stimulation. Amer.
Nat. 90:309-317.
Bakken, G. S. and D. M. Gates. 1975. Heat-transfer
analysis of animals: Some implications for field
ecology, physiology and evolution. In D. M. Gates
and R. B. Schmerl (eds.), Perspectives in biophysical
ecology, pp. 255-290. Springer, Berlin.
Bartholomew, G. A. and V. A. Tucker. 1963. Control
of changes in body temperature, metabolism and
circulation by the agamid lizard Amphibolurus barbatus. Physiol. Zool. 36:199-218.
Bartholomew, G. A., V. A. Tucker, and A. K. Lee.
1965. Oxygen consumption, thermal conductance
and heart rate in the Australian skink Tiliqua scincoides. Copeia 1965:169-173.
Cabanac, M. 1975. Temperature regulation. Ann.
Rev. Physiol. 37:415-439.
Cabanac, M., H. T. Hammel, and J. D. Hardy. 1967.
Tiliqua scincoides: Temperature sensitive units in
lizard brain. Science. 158:1050-1051.
Cameron, J. N. 1976. Branchial ion uptake in arctic
grayling: Resting values and effects of acid-base
disturbance. J. Exp. Biol. 64:711-725.
Carey, F. G. 1973. Fishes with warm bodies. Sci.
Amer. 228:36-44.
Chowers, I., H. T. Hammel, S. B. Stromme, and S. M.
McCann. 1964. Comparison of environmental and
preoptic cooling on plasma cortisol levels. Amer. J.
Physiol. 207:577-582.
Cloudsley-Thompson, J. L. 1968. Thermoregulation
in tortoises. Nature (London) 217:575.
Cloudsley-Thompson, J. L. 1970. On the biology of
the desert tortoise Testudo sulcata Miller in Sudan. J.
Zool. (London) 160:17-33.
Cowles, R. B. 1958. Evolution of dermal temperature
regulation. Evolution 12:347-357.
Crawford, E. C, Jr., and B.J. Barber. 1974. Effects of
ECTOTHERM RESPONSES TO TEMPERATURE CHANGE
core, skin and brain temperature on panting in the
lizard Sauromalus obesus. Amer. Physiol 226:569573.
Crawshaw, L. I. 1976. Effect of rapid temperature
change on mean body temperature and gill ventilation in carp. Am. J. Physiol. 231:837-841.
Crawshaw, L. I. 1977. Physiological and behavioral
reactions of fishes to temperature change. J.
Fish. Res. Board Can. 34:730-734.
Crawshaw, L. I. and H. T. Hammel. 1971. Behavioral
thermoregulation in two species of antarctic fish.
LifeSci. 10:1009-1020.
Crawshaw, L. 1. and H. T. Hammel. 1973. Behavioral
temperature regulation in the California horn
Shark Heterodontus francisci. Brain Behav. Evol.
7:447-452.
Crawshaw, L. I. and H. T. Hammel. 1974. Behavioral
regulation of internal temperature in the brown
bullhead Ictalurus nebulosus. Comp. Biochem.
Physiol. 47A:51-60.
Crawshaw, L. I., H. T. Hammel, and W. L. Carey.
1973. Brainstem temperature affects gill ventilation
in the California scorpionfish. Science 181:579-581.
Crawshaw, L. 1., M. H. Johnson, and D. E. Lemons.
1978. Temperature selection and responses to
rapid temperature change in the turtle Pseudemys
scripta. Fed. Proc. 37:622.
Daye, P. G. and E. T. Garside. 1975. Lethal levels of
pH for brook trout Salvehnus fontmalis (Mitchill)
Can. J. Zool. 53:639-641.
Degham, K. J., J. K. J. Karnaky, andj. A. Zodunaisky.
1977. Active chloride transport in the in vitro operculor skin of a teleost, a gill-like epithelium rich in
chloride cells. J. Physiol 271:155-192.
Dizon, A. E. and R. W. Brill. 1979. Thermoregulation
in tunas. Amer. Zool. 19:249-265.
Dizon, A. E., T. C. Byles, and E. D. Stevens. 1976.
Short communication; perception of abrupt temperature decrease by restrained skipjack tuna
Katsuwonus pelamis.]. Thermal Biol. 1:185-187.
Dizon, A. E., E. D. Stevens, W. H. Neill, and J. J.
Magnuson. 1974. Sensitivity of restrained skipjack
tuna Katsuwonus pelamis to abrupt increases in temperature. Comp. Biochem. Physiol. 49A:291-299.
Dudaux, R., M. Fantino, and M. Cabanac. 1973.
Comportement thermoregulateur chez Rana esculenta. Influence du rechauffement spinal. Pfluegers Arch. 342:347-358.
Erskine, D. J. and J. R. Spotila. 1977. Heat energy
budget analysis and heat transfer in the largemouth
blackbass. Physiol. Zool. 50:157-169.
Evans, D. H. 1975. Ionic exchange mechanisms in fish
gills. Comp. Biochem. Physiol. 51A:491-495.
Evans, D. H. 1978. Hormonal control of sodium
transport by the gills of teleost fish. In I. Assenmacher and D. S. Farner (eds.), Environmental endocrinology, pp. 204-209. Springer-Verlag, New
York.
Friedlander, M. J., N. Kotchabhakdi, and C. L.
Prosser. 1976. Effects of cold and heat on behavior
and cerebellar function in goldfish. J. Comp.
Physiol. 112:19-45.
Fry, F. E. J. and P. W. Hochachka. 1970. Fish./n G. C.
Whittow (ed.), Comparative physiology of thermoregulation, Vol. 1, Invertebrates and non-mammalian verte-
235
brates, pp. 79-134. Academic Press, Inc., New York.
Greer, G. L. and D. R. Gardner. 1970. Temperature
sensitive neurons in the brain of brook trout. Science 169:1220-1222.
Greer, G. L. and D. R. Gardner. 1974. Characterization of responses from temperature-sensitive units
in trout brain. Comp. Biochem. Physiol. 48A:189203.
Hammel, H. T. 1968. Regulation of internal body
temperature. Ann. Rev. Physiol. 30:641-710.
Hazel, J. R., W. S. Garlick, and P. A. Sellner. 1978.
Effects of assay temperature upon pH optima of
enzymes from poikilotherms test of imidazole alphastat hypotheses. J. Comp. Physiol. 123B:97104.
Hazel, J. R. and C. L. Prosser. 1974. Molecular mechanisms of temperature compensation in poikilotherms. Physiol. Rev. 54:620-677.
Heath, J. E., E. Gasdorf, and R. G. Northcuu. 1968.
The effect of thermal stimulation of anterior
hypothalamus on blood pressure in the turtle.
Comp. Biochem. Physiol. 26:509-518.
Heatwole, H., B. T. Firth, and H. Stoddart. 1975.
Influence of season, photoperiod and thermal acclimation on the panting threshold of Amphibolurus muricatus. J. Exp. Zool. 191:183-192.
Hensel, H., Marburg/Lahn. 1973a. Handbook of sensory physiology, Vol. 2, Somato-Sensory system, /n
A. Iggo (ed.), Cutaneous thermoreceptors, pp. 79-110.
Springer-Verlag, Berlin/Heidelberg, New York.
Hensel, H. 19736. Neural processes in thermoregulation. Physiol. Rev. 53:948-1017.
Houston, A. H. 1973. Environmental temperature
and the body fluid system of the teleost. In W. Chavin (ed.), Responses of fish to environmental changes.
Charles C. Thomas, Springfield, Illinois.
Iriki, M., S. Murata, M. Nagai, and K. Tsuchiya. 1976.
Effects of thermal stimulation to the spinal cord on
heart rate in cyprinid fishes. Comp. Biochem.
Physiol. 53A:61-63.
Jackson, D. C. and R. D. Kagen. 1976. Effects of temperature transients on gas exchange and acid-base
status of turtles. Amer. J. Physiol. 230:1389-1393.
Janssen, R. G. and D. J. Randall. 1975. The effects of
changes in pH and PCOj in blood and water on
breathing in rainbow trout Salmo gatrdneri. Respir.
Physiol. 25:235-245.
Karnaky, K. J.,Jr., and W. B. Kinter. 1977. Killifish
opercular skin: A flat epithelium with a high density of chloride cells. J. Exp. Zool. 199:355-364.
Lagerspetz, K. Y. H. 1974. Temperature acclimation
and the nervous system. Biol. Rev. 49:477-514.
Lemons, D. E. and L. I. Crawshaw. 1978. Temperature regulation in the Pacific lamprey. Fed. Proc.
37:929.
Lillywhite, H. B. 1971. Thermal modulation of
cutaneous mucus discharge as a determinant of
evaporative water loss in the frog, Rana catesbeiana.
2. Vergl. Physiologic 73:84-104.
Mackenzie, J. A. and D. C. Jackson. 1978. The effect
of temperature on cutaneous CO2 loss and conductance in the bullfrog. Respir. Physiol.
32:313-324.
Maetz, J. 1972. Branchial sodium exchange and ammonia excretion in the goldfish Carassius auratus;
236
LARRY I. CRAWSHAW
Effects of ammonia-loading and temperature
changes. J. Exp. Biol. 56:601-620.
Maetz.J. 1976. Transport of ions and water across the
epithelium of fish gills. Ciba Found. Symp.
38:133-159.
Maetz, J. and D. H. Evans. 1972. Effects of temperature on branchial sodium-exchange and extrusion
mechanisms in the seawater-adapted flounder
Platichthysflesus L. J. Exp. Biol. 56:565-585.
Meuwis, A. L. and M. J. Heuts. 1957 Temperature
dependence of breathing rate in carp. Biol. Bull.
112:97-107.
Mbrgareidge, K. R. and H. T. Hammel. 1975.
Evaporative water loss in box turtles: Effects of
rostral brainstem and other temperatures. Science.
187:366-368.
Morgareidge, K. R. and F. N. White. 1969. Cutaneous
vascular changes during heating and cooling in the
Galapagos marine iguana. Nature. 223:587-591.
Motais, R. and J. Isaia. 1973. Temperature-dependence of permeability to water and to sodium of the
gill epithelium of the eel Anguilla anguilla. J. Exp.
Biol. 56:587-600.
Myhre, K. and H. T. Hammel. 1969. Behavioral regulation of internal temperature in the lizard Tiliqua
scincoides. Amer. J. Physiol. 217:1490-1495.
Nagai, M. and M. Iriki. 1977. Characteristics of heart
rate responses elicited by thermal stimulation of the
spinal cord of the carp Cyprinus carpio. Comp.
Biochem. Physiol. 57:417-421.
Nelson, D. O. 1978. Temperature sensitive neurons
in the preoptic region of sunfish. Physiol. 21:84.
Newell, R. C. 1969. Effects of fluctuations in temperature on the metabolism of intertidal invertebrates.
Amer. Zool. 9:293-307.
Olla, B. and A. L. Studholme. 1971. The effect of
temperature on the activity of bluefish, Pomatomus
saltatrix L. Biol. Bull. 141:337-349.
Pearson, O. P. and D. F. Bradford. 1976. Thermoregulation of lizards and toads at high altitudes
in Peru. Copeia 1976:155-170.
Peterson, R. H. and J. M. Anderson. 1969. Influence
of temperature change on spontaneous locomotor
activity and oxygen consumption of Atlantic salmon, Salmo salar, acclimated to two temperatures. J.
Fish. Res. Board Can. 26:93-109.
dioxide content and body temperature in bullfrogs.
Respir. Physiol. 14:219-236.
Reeves, R. B. 1976. Temperature-induced changes in
blood acid-base status: Donnan r a and red cell volume. J. Appl. Physiol. 40:762-767.
Reeves, R. B. 1977. The interaction of body temperature and acid-base balance in ectothermic vertebrates. Ann. Rev. Physiol. 39:559-586.
Reynolds, W. W. 1977. Thermal equilibration rates in
relation to heartbeat and ventilatory frequencies in
largemouth blackbass Micropterus salmoides. Comp.
Biochem. Physiol. 56A: 195-201.
Reynolds, W. W. and M. E. Casterlin. 1978. Estimation of cardiac output and stroke volume from
thermal equilibration and heartbeat rates in fish.
Hydrobiologia 57:49-52.
Rodbard, S., F. Samson, and D. Ferguson. 1950.
Thermosensitivity of the turtle brain as manifested
by blood pressure changes. Amer. J. Physiol.
160:402-408.
Romamenko, V. P. and M. I. Kotsar. 1976. Regulation of acid-base balance in the blood of fishes
during their adaptation to changes in water temperature. Fiziol. Zh. 22:750-753.
Sawyer, W. H., P. K. T. Pang, and S. M. GalliGallardo. 1978. Environment and osmoregulation
among lungfish and amphibians. In I. Assenmacher
and D. S. Farner (eds.), Environmental endocrinology,
pp. 210-216. Springer-Verlag, New York.
Schmidt-Nielsen, K. and W. R. Dawson. 1964. Terrestrial animals in dry heat: Desert reptiles. In D. B.
Dill (ed.), Handbook of physiology, Section 40, Adapta-
tion to the environment. Amer. Physiol. Soc, Washington, D.C,
Siegel, E. B. and C. A. Privitera. 1976. The effect of
hypothalamic thermal stimulation on respiration in
the turtle. J. Exp. Zool. 196:387-392.
Simon, E., H. T. Hammel, and A. Oksche. 1977.
Thermosensitivity of single units in the hypothalamus ot the conscious Pekin duck. J. Neurobiol.
8:523-535.
Smith, E. N. 1976. Heating and cooling rates of the
American alligator, Alligator mississippiensis. Physiol.
Zool. 49:37-48.
Smith, E. N. 1979. Behavioral and physiological
thermoregulation in crocodihans. Amer. Zool. 19:
Prosser, C. L. 1973. Comparative animal physiology.
239-247.
Saunders, Philadelphia, Pa.
Sorenson, P. R. and P. O. Fromm. 1976. Heat transRahn, H. 1976. Why are pH of 7.4 and pCOs of 40
fer characteristics of isolated-perfused gills of rainnormal values for man? Extrait du Bulletin eurobow trout. J. Comp Physiol. 112:345-357.
peen de Physiopathologie Respiratoire. 12:5-13.
Spigarelli, S. A., M. M. Thommes, and T. L.
Beitinger. 1977. The influence of body weight on
Randall, D. J. 1970. The circulatory system. In W.
Hoar, and D. J. Randall (eds.), Fish physiology, Vol. heating and cooling of selected Lake Michigan
fishes. Comp. Biochem. Physiol. 5:51-57.
4, The nervous system, circulation and respiration, pp.
Spray. D. C. 1974. Characteristics, specificity and ef133-172. Academic Press, New York.
ferent control of frog cutaneous cold receptors. J.
Randall, D. J. 1974. The regulation of H + concentraPhysiol. 237:15-38.
tion in body fluids. Proc. of the Can. Soc. of
Spray, D. C. and D. B. Belkin. 1972. Heart rateZool. Ann. Meeting, pp. 89-94.
cloacal temperature hysteresis in iguana is a result
Randall, D. J. and J. N. Cameron. 1973. Respiratory
of thermal lag. Nature (London) 239:337-338.
control of arterial pH as temperature changes in
rainbow trout Salmo gairdnen. Amer. J. Physiol
Spray, D. C. and M. L. May. 1972. Heating and cool225:997-1002.
ing rates in four species of turtles. Comp. Biochem.
Reeves, R. B. 1972. An imidazole alphastat hypothesis
Physiol. 41A:507-522.
for vertebrate acid-base regulation: Tissue carbon
Stevens, E. D. and F. E. J. Fry. 1970. The rate of
ECTOTHERM RESPONSES TO TEMPERATURE CHANGE
thermal exchange in a teleost Tilapia mossambica.
Can.J. Zool. 48:221-226.
Stevens, E. D. and F. E. J. Fry. 1972. The effect of
changes in ambient temperature on spontaneous
activity in skipjack tuna. Comp. Biochem. Physiol.
42A:803-805.
Stevens, E. D. and F. E. J. Fry. 1974. Heat transfer
and body temperatures in non-thermoregulatory
teleosts. Can.J. Zool. 52:1137-1143.
Stevens, E. D. and A. M. Sutterlin. 1976. Heat transfer between fish and ambient water. J. Exp. Biol.
65:131-145.
Stevens, E. D., H. W. Neill, A. E. Dizon.J. J. Magnuson, and S. Steffel. 1974. Physiology of warmbodied fish. Proc. Int. Union. Physiol. Sci. 9:110.
Strange, R. J., C. B. Schreck, and J. T. Golden. 1977.
Corticoid stress responses to handling and temperature in salmonids. Trans. Am. Fish. Soc.
106:213-218.
237
Voigt, W. G. 1975. Heating and cooling rates and
their effects upon heart rate and subcutaneous
temperatures in the desert tortoise Gopkerus agassizii. Comp. Biochem. Physiol. 52A:527-531.
Weathers, W. W. and F. N. White. 1971. Physiological
thermoregulation in turtles. Amer. J. Physiol.
221:704-710.
Whittow, C. H. 1970. Comparative physiology of ther-
moregulation, Vol. 1. Academic Press, Inc., New
York.
Wood, C. M., B. R. McMahon, and D. G. McDonald.
1977. An analysis of changes in blood pH following
exhausting activity in the starryflounderPlatichthys
stellatus.]. Exp. Biol. 69:173-185.
Yancey, P. H. and G. N. Somers. 1978. Temperature
dependence of intracellular pH: Its role in the conservation of apparent Km values of vertebrate lactate dehydrogenases. J. Comp. Physiol. 125B:129134.