How dolphins use their blubber to avoid heat
stress during encounters with warm water
M. E. HEATH1 AND S. H. RIDGWAY2
Research and Application Association, San Diego 92192-2683; and 2Bioscience
Division, Naval Command Control and Oceans Surveillance Center, San Diego, California 92152
1Biodiversity
Tursiops truncatus; bottlenose dolphin; core temperature;
heat flow; heat storage
SEVERAL ANATOMIC and physiological adaptations with
probable thermoregulatory function have been described in dolphins. These include a streamlined body
with a highly reduced total surface area for their total
mass and a thick blubber layer that provides insulation
(17, 23). In addition, bottlenose dolphins have a metabolic rate that is 1.6 to ⬎2 times greater than that of
terrestrial mammals of the same body mass (17, 24).
Descriptions have been published of highly specialized
vasculature in the appendages that likely functions in
temperature regulation. Included are multiple veins
surrounding arteries in all of the appendages (3, 14, 21,
23), suggested by Scholander and Schevill (21) to
facilitate heat retention in the body, with countercurrent heat exchange from the warmer arterial blood to
the cooler venous blood, because the latter flows back to
the core. Also, the high degree of vascularization in the
dorsal fin, pectoral flippers, and flukes (3, 14, 23)
implies the importance of these appendages for heat
loss. Another vascular countercurrent heat exchanger
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R1188
is suggested to cool selectively the dolphins’ internalized testes and thereby protect spermatozoa (18).
Although these many reports have focused on describing individual adaptations, there have been no studies
demonstrating how dolphins manage to function in,
and often move between, the wide range of water
temperatures (Tw ) they encounter on a daily or seasonal basis. Dolphins have been observed in a wide
range of ambient Tw, from 1.1 to 31.1°C (7, 8) and even
36–38°C in shallow tropical waters (Ridgway, personal
observation). The latter observation is remarkable because these temperatures are at or above core temperatures reported for dolphins, and, because they are
submerged in water, dolphins cannot, as terrestrial
mammals can, use evaporation to lose heat. This
observation was the stimulus for the present investigation.
Our study used a simple protocol of steadily warming
ambient water under highly controlled conditions to
simulate the thermal conditions encountered by a
dolphin moving from cool pelagic water to warm inshore or estuarine water. The dolphins responded to
warmer water with a massive redistribution of heat
within their bodies from the body core to peripheral
tissues. This was demonstrated by significant reductions in core temperature instead of the pronounced
increase that should have occurred due to metabolic
heat production in conditions in which they could not
lose heat to the environment. This unique thermoregulatory response acts to delay the onset of hyperthermia
or heat stress for an hour or longer even during
encounters with 36°C water. Clearly it is this mechanism that allows dolphins to explore and forage safely
in the very warm summertime water that exists inshore in shallow tropical gulfs, bays, and estuaries.
METHODS
We studied six bottlenose dolphins (Tursiops truncatus,
139- to 238-kg body mass, see Table 1). The animals used in
these studies were maintained under Federal Regulations
promulgated under the Animal Welfare Act and in accordance
to the National Research Council Guide. Protocols were
approved by appropriate Institutional Animal Care and Use
Committees. The dolphins were selected for their ability to
rest quietly on a fleece-lined sling of a transport chamber
(0.76 m deep ⫻ 0.8 m wide ⫻ 3.3 m long) while submerged in
water to ⬃3–4 in. below the base of the dorsal fin (Fig. 1). A
1 -horsepower pump (Hayward Pool Pump, Fairmont, CA)
⁄2
was used to continuously circulate the water in the chamber
and through a Jacuzzi heating system (One series; Teledyne
Laars, Moorpark, CA) that was turned on and off as needed to
carry out the protocol. The 1- to 2-h-long experiments included ⬃30 min of baseline when the dolphins were in San
Diego Bay-temperature water (15–22°C) and a 30- to 60-min
Downloaded from http://ajpregu.physiology.org/ by 10.220.33.5 on June 16, 2017
Heath, M. E., and S. H. Ridgway. How dolphins use their
blubber to avoid heat stress during encounters with warm
water. Am. J. Physiol. 276 (Regulatory Integrative Comp.
Physiol. 45): R1188–R1194, 1999.—Dolphins have been observed swimming in inshore tropical waters as warm as
36–38°C. A simple protocol that mimicked the thermal conditions encountered by a dolphin moving from cool pelagic to
warm inshore water was used to determine how dolphins
avoid hyperthermia in water temperatures (Tw ) at and above
their normal core temperature (Tc ). Tw (2 sites), rectal temperature (Tre; 3 depths), and skin temperature (Tsk; 7 sites)
and rate of heat flow (4–5 sites) between the skin and the
environment were measured while the dolphin rested in a
chamber during a 30-min baseline and 40–60 min while
water was warmed at ⬃0.43°C/min until temperatures of
34–36°C were attained. Instead of the expected increase, Tre
consistently showed declines during the warming ramp,
sometimes by amounts that were remarkable both in their
magnitude (1.35°C) and rapidity (8–15 min). The reduction in
Tre occurred even while heat loss to the environment was
prevented by continued controlled warming of the water that
kept Tw slightly above Tsk and while metabolic heat production alone should have added 1.6–2°C/h to the Tc. This
reduction in Tc could only be due to a massive redistribution
of heat from the core to the blubber layer.
TEMPERATURE REGULATION IN DOLPHINS
Table 1. Physical characteristics of dolphins studied
Dolphin
Weight, kg
Length, cm
Sex
Age, yr
BEN
DAS
BUS
BUG
MOD
YOG
238.14
207.75
161.93
142.88
139.25
165.56
262
264
242
233
247
250
M
F
M
M
M
M
35
27
16
15
14
16
RESULTS
Figure 2 provides graphs of a representative experiment on one dolphin. Table 2 provides a summary of
results from all 10 experiments, including air temperature, baseline Tw, the depth of the rectal probe, Tre
measures from all three thermocouples during the 5
min of baseline before initiation of the warming ramp,
the minimum Tre observed at each site that occurred
during the warming ramp or plateau, and mean respiratory frequency during baseline and during the warming ramp and plateau. The mean difference in Tre
between the baseline values and the minimum values
is also given. It was calculated as the mean of the three
site means given for baseline minus the mean of the
minima at the same three sites that occurred when the
water was warmed. A summary of heat flow data is
provided in Table 3. Included are the calculated mean
heat flow during the baseline and the calculated mean
of data collected from the onset of the warming ramp to
the initiation of the plateau.
Figure 2 illustrates the result of the experiment in
which the most pronounced reduction in Tre occurred
(experiment 1 in Table 2), and the following describes
the events in detail. During the baseline, Tw was
⬃15.5°C, Tre (Fig. 2A) were between 36.6 and 36.7, Tsk
(Fig. 2B) of submerged regions were 15.5–17°C, and
heat was flowing out of the dolphin (Fig. 2C) at a
steady, low rate (10–80 W/m2, depending on the site).
Warming of the water began at 22 min. During the
initial 15–19 min of the warming ramp (time ⫽ 22 to
⬃37–41 min), Tre (Fig. 2A) did not change noticeably.
Tsk (Fig. 2B) rose but lagged slightly behind the rise in
Tw, and the direction of heat flow (Fig. 2C) was reversed, flowing from the water to the dolphin as shown
for the pectoral flipper, flukes, and body wall. The
dorsal fin was out of water, so its temperature and heat
flow continued at near baseline levels. However, a
change occurred beginning at ⬃15 min into the warming ramp (time ⫽ 37 min) and at a Tw of ⬃21°C, when
Tre began to decline. The decline was initially slow. As
Fig. 1. Setup for warming ramp experiments in dolphins, including location of thermocouples, heat flow
disks, and electrocardiogram (ECG) electrodes. During
1- to 2-h-long experiments, water in chamber was
initially at San Diego Bay temperature and was subsequently warmed to 34–36°C (see Fig. 2).
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period when the Tw was warmed at a rate of ⬃0.43°C/min.
The water was warmed to 34–36°C and maintained at this
plateau level for another 20–60 min, specifically to observe
the effects of exposure to warm water on core temperature,
before return to baseline level.
Tw was measured at both ends of the chamber in wellcirculated water. Skin temperatures (Tsk ) were measured,
with thermocouples insulated from the water on the fluke,
dorsal fin, pectoral flippers, and up to four locations along the
trunk. Rectal temperatures (Tre ) were measured with a probe
that incorporated three thermocouples positioned at 8-cm
intervals from the tip. This type of probe was used because of
the report by Rommel et al. (18) of a vascular countercurrent
heat exchanger 15–20 cm long adjacent to the colon in a
region 15–35 cm past the anus, which could significantly
affect measurements of Tre at depths ⬍40 cm. Rectal probe
depth was measured at the end of each experiment and
ranged from 34 to 56 cm past the anus. It was ⱖ40 cm deep in
8 of the 10 experiments. Heat flow through the skin was
measured with heat flow disks (Concept Engineering, Old
Saybrook, CT) applied to the fluke, dorsal fin, pectoral
flippers, tail stock, and lateral trunk regions. The heat flow
disks were held in place continuously at a standard constant
pressure; a heat-conductive paste applied between the heat
flow disk and the skin ensured complete thermal contact with
the skin. The signal in millivolts collected from each heat flow
disk was converted to Watts per square meter using the
calibration coefficient unique to each disk and supplied by the
manufacturer. Data were collected at 1-min intervals throughout the experiment using a Fluke data logger (model 2625A)
and portable computer. Respiratory frequency was monitored
by recording the number of breaths taken during 5-min
periods. An electrocardiogram was monitored throughout the
experiments for safety reasons.
R1189
R1190
TEMPERATURE REGULATION IN DOLPHINS
Tw reached 27–28°C (time ⫽ 48 min), Tre began a more
conspicuous decline that continued for 14 min. Tre
reached a minimum of 35–35.8°C (top), which was
0.9–1.3°C lower than their baseline levels. Within 4–8
DISCUSSION
Although observations of wild dolphins swimming in
very warm water had shown us that these animals
have some mechanism for short-term heat tolerance,
the nature of the mechanism discovered in these experiments was completely unexpected. The dolphins consistently showed declines in Tre during encounters with
warm water in each of 10 experiments (Fig. 2A and
Table 2). During warming ramps and plateaus of
70–140 min combined duration, Tre increased by no
more than 0.2°C above baseline levels and only after an
initial decline in Tre. This is surprising because core
temperature should have increased by 1.6 to ⬎2.0°C/h
from resting metabolic heat production alone in such
conditions in which the dolphins cannot lose their
Fig. 2. Results of experiment (experiment 1 in Table 2) in which most
pronounced change in rectal temperature occurred. Water temperature (Twater ), which clearly depicts baseline, warming ramp, and
plateau periods during protocol, is shown in A, B, and C as a thick
solid black line. A, B, and C show response in rectal temperature (A),
skin temperature and respiratory frequency (resp freq; B), and heat
flow (C) from dolphin. Also depicted in A is increase in core temperature (Tc ) expected from resting metabolic heat production during
warming ramp and plateau calculated from values reported by
Ridgway and Patton (17) and Williams et al. (24). Bodyt-stock and
bodylateral, measures made on the tail stock and lateral surfaces of the
dolphin, respectively.
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min, Tre began to rise again, at a rate of ⬃0.03°C/min,
while the warming ramp continued. Also occurring
within the period when Tre decline were plateaus and
then declines in the rate of heat gain from the water for
all submerged surfaces. Because this occurred while
the warming ramp was continuing, the only possible
explanation is a rise in temperature of peripheral
tissues that was greater than the rise in Tw. Finally, the
rate at which Tre should increase during the experiment, based on previously measured resting metabolic
rates in bottlenose dolphins (15, 23) is shown in Fig. 2.
Given the metabolic heat production of dolphins, it
would have been just as remarkable an observation if
there had been no change in core temperature (rather
than a reduction) during the exposure to warm water.
However, it was the observed decline in core temperature that revealed the mechanism dolphins are using to
tolerate very warm water.
The summary of Tre, respiratory frequency, and heat
flow data provided in Tables 2 and 3 reveals the
consistency among all the experiments. Tre declined in
all 10 of the experiments (mean ⫾ SD, 0.5 ⫾ 0.27; range
of mean difference, 0.33–1.07°C) during either the
warming ramp or beginning of the plateau. Because the
timing of the decline in Tre differed between experiments, averaging Tre for all experiments would obscure
rather than reveal the response. As is shown in Fig. 2B,
the Tsk in all experiments followed, but some measures
lagged slightly behind, Tw. Trends in heat flow (Table 3)
were also similar in all experiments. Baseline respiratory frequency was between 1.4 and 4.1 breaths/min
and either decreased or increased by ⬍1 breath/min
during warming.
R1191
TEMPERATURE REGULATION IN DOLPHINS
Table 2. Changes in Tre of dolphins during encounters with warm water
Dolphin
BEN
DAS
BUS
BUG
MOD
YOG
Expt.
No.
Baseline
Twater ,
°C
1
2
3
4
5
6
7
8
9
10
15.5
18.5
16
19
19
17.5
19.5
18.5
21.5
20.5
Tair ,
°C
Depth
of Tre
Probe,
cm
1
17
21
16
22
19
19
22
22
20
22
49
40
46
37
50
41
50
56
34
46
36.6
36.6
36.8
37.05
37.3
37.1
37.2
37.2
37
36.2
36.6
36.6
36.8
37.1
37.3
37.1
37
37.2
36.9
36.1
36.7
36.6
36.8
37.1
37.3
37
36.8
37.3
36.9
36.2
35.6
36
36.5
36.3
37
36.8
36.9
36.7
36.5
35.9
35.8
36
36.3
36.2
37
36.7
36.6
36.9
36.4
36
36.91
0.35
36.88
0.35
36.87
0.34
36.42
0.46
36.39
0.40
Mean
SD
Baseline
Tre , °C
Mean
Change
in Tre ,
°C
Baseline
Warm
Change
35.4
36
36
36.6
36.8
36.5
36.4
36.8
36.4
35.6
1.07
0.6
0.53
0.73
0.37
0.4
0.37
0.43
0.5
0.33
1.53
1.4
1.5
1.9
4.08
2.7
4.1
2.7
3
1.8
1.92
1.63
1.96
1.48
3.47
2.54
3.34
2.48
2.63
2.13
0.39
0.23
0.46
⫺0.42
⫺0.61
⫺0.16
⫺0.76
⫺0.22
⫺0.37
0.33
36.25
0.48
0.50
0.27
2.47
1.02
2.36
0.67
⫺0.11
0.44
Minimum
Tre , °C
2
3
1
2
3
Respiratory Frequency,
breaths/min
metabolic heat to the environment. Note that the
metabolic rate of bottlenose dolphins is 1.6 to ⬎2 times
higher (15, 23) than in most mammals of similar mass
(9).
Although the reduction in Tre was unexpected in this
situation, the Tre recorded in this study (35.4–37.3°C)
were always within the range of values reported previously for bottlenose dolphins (33.4–38.8°C) (4, 10, 11,
13, 15, 19). Also, even the largest decline in Tre observed, 1.3°C, is less than one-half the 3°C decline in
core temperature observed in a dolphin returned to its
pool after it had been removed on a padded stretcher for
25 min (10). Heat flow levels recorded during baseline
were within the range previously reported (4).
We reject, for the following several reasons, the
possibility that the observed reductions in Tre represent
only a transient shift in local tissue temperature in that
region of the colon where a countercurrent heat exchanger occurs (18). 1) In 8 of the 10 experiments, the
deepest measure of Tre was made at depths of 40–56
cm, well beyond the location (15–35 cm past the anus)
of the heat exchanger (18) and, therefore, representative of true core temperature. 2) Tre did not rebound
Table 3. Heat loss and gain by dolphins during
baseline period and warming ramp
Baseline
Expt.
No. Pectoral Dorsal Flukes
1
2
3
4
5
6
7
8
9
10
⫺54.5
⫺97.4
⫺23.1
⫺70.6
⫺89.7
⫺26.2
⫺7.2
⫺19.8
⫺47.3
⫺30.1
Body
⫺31.2 ⫺5.9 ⫺80.1
⫺18.6
2.4 ⫺85.8
⫺7.8
0.9 ⫺25.6
⫺93.7
0.2 ⫺82.6
⫺88.6
8.9 ⫺97.9
7.6 13.5 ⫺88.7
⫺27.2 ⫺21.7 ⫺65
1.8 ⫺1.1
61.7
⫺30.8
2.3 ⫺74.9
⫺52.5 ⫺17 ⫺111.1
Mean ⫺46.6 ⫺34.1
SD
30.9
35.8
⫺, Heat loss.
Warming Ramp
⫺1.8
10.7
⫺77.3
23.3
Pectoral Dorsal Flukes Body
14.5
49.6
28.3
15.4
48
147.6
⫺5.6
60.1
36.9
68.4
46.3
42.2
⫺29.9
⫺37.3
⫺69.8
⫺92.1
⫺82.8
⫺9.2
⫺5.7
⫺27.8
⫺45.2
⫺56.8
141.4
99.3
104.4
142.2
150.3
141.2
58.9
113.6
83.6
63.3
99.2
51.1
62.5
59
64.2
59.7
60.9
80.4
27.3
⫺45.7 109.8 62.7
29.5 33.8 19.6
sharply after reaching its lowest level, as would be
expected if it were due only to local shifts in tissue
temperature that are not representative of core temperature. 3) Tre increases slowly during the remainder
of the warming ramp and plateau in Tw and at a rate
(0.026–0.033°C/min) to be expected from metabolic
heat production in bottlenose dolphins (16, 24). 4) The
heat exchanger depends on the heat loss from the
flukes and dorsal fin region (18). In preliminary experiments, declines in Tre of 0.8–0.9°C were recorded in
dolphins submerged in warm water and gaining heat
from both of these regions. 5) In the experiment shown
in Fig. 2, the flukes are gaining heat and only the dorsal
fin region is losing heat. If this area is, generously,
estimated as ⬃0.50 m2 at the mean rate of heat flow of
33.64 W/m2, no more than 16.82 W were lost from this
skin-air interface. This amount of heat loss can cool, by
the requisite 2°C (sum of metabolic heat and reduced
Tre ), only 2.1 kg of tissue in this 238-kg dolphin. 6) It is
impossible for the blood from the dorsal fin region to
mix with blood from the flukes (which are gaining heat)
and traverse ⬎40 cm of warmer tissues before reaching
the rectal region and not gain any heat en route. 7)
Even if a 2.1-kg region of tissue could have been cooled
by 2°C, it is impossible for it to cause, by tissue
conduction, a similar reduction in tissue temperature
at the 49-cm depth of the deepest thermocouple, located
9–14 cm beyond the described heat exchanger. 8) Heat
is lost from the dorsal fin region throughout the experiment at a constant rate. Thus its effect on Tre should be
constant, and not confined to only 15 min in the middle
of the experiment. It is concluded, therefore, that the
declines in Tre in response to warm water represent a
true reduction in the temperature of the body core.
It is also clear that these reductions in core temperature were not due to heat loss to either the water or the
air. During the warming ramp in particular, the changes
in Tsk lagged slightly behind the changes in Tw (Fig.
2B). This is as expected because the water was being
warmed externally and circulated through the tank.
Because of this, heat flowed from the water to the
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Baseline water temperature varied because experiments were conducted at different times of year. Rectal probe contained 3 thermocouples,
1 at the full depth of the probe (given in centimeters past anus), and the others at 8-cm intervals. Tre , rectal temperature; Twater , water
temperature; Tair , air temperature.
R1192
TEMPERATURE REGULATION IN DOLPHINS
volume increased from 5.5 to 10 liters. It is clear from
these calculations that the decline in body core temperature cannot be due to heat loss via evaporation from the
respiratory tract.
In comparison, a 1°C reduction in core temperature
over a 15-min period represents ⬎675 W. This estimate
assumes a specific heat of the tissues of 3.47 J/g (12)
and that the core represents 75% (e.g., 178.5 kg) of the
total body mass. The latter assumption is based on the
report that total fat content in bottlenose dolphins is
18.5% total body mass (15), that all fat is located in the
insulative subcutaneous layer (15), and that core extends to near the blubber layer (5). It is concluded that
the marked reduction in Tre, which represents a true
decline in core temperature, cannot be attributed to
heat loss from the body and must be due to a massive
redistribution of heat within the body from the core to
the periphery. The redistribution of heat likely occurs
both by conduction and by large increases in blood flow
to the periphery, which rapidly transports heat to those
tissues.
How reasonable is the suggestion that the reduction
in core temperature is due to the redistribution of heat?
Because the blubber layer acts as insulation in the cool
pelagic water, when the dolphin moves into warm
water, the blubber is cooler than both the ambient
water and the body core. It is therefore a heat sink to
both. Because almost all the temperature gradient
between the initial 15.5°C water and the 36.6°C core
temperature occurs in the blubber layer (5), we can
assume an initial mean blubber temperature of ⬃26°C.
If the blubber and appendages represent 25% of total
body mass (59.5 kg), then a 2°C reduction in core
temperature would require a 6°C rise in mean blubber
and appendage temperature to 32°C. The net heat gain
from the water via the appendages and body surfaces at
the measured rates would add another 2.2°C to the
peripheral tissues over the entire span of the experiment, bringing their temperature to ⬎34°C. This correlates well with the observation that, whereas the
flippers and flukes reach equilibrium with the water at
70–80 min (as demonstrated by reaching zero heat
flow), heat continues to be gained via the body wall
until the very end, when Tw is lowered to between 34
and 35°C. Finally, if a redistribution of heat within the
body did not occur, then the reduction in heat gain from
the environment by the submerged surfaces cannot be
explained. This is because a 2.2°C increase in peripheral tissue temperature gained from the warm water is
inadequate to bring the appendages and blubber to
equilibrium with the water.
Importance of this thermoregulatory mechanism.
These observations suggest that a common response of
dolphins to encountering warm water is a redistribution of heat such that core temperature is reduced and
blubber and appendage temperatures are increased.
This is advantageous in two ways. First, it reduces the
amount and rate of heat gained by the dolphin from the
warm ambient water through a ‘‘preemptive strike’’ of
actively warming its blubber layer and appendages
rather than allowing these cool tissues, which normally
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dolphin as documented by the heat flow measurements
(Fig. 2C) and in accordance with the laws of heat flow
and thermodynamics. The only exception occurred in
Fig. 2, for the pectoral flipper over a 14-min period
during the warming ramp (time ⫽ 46–60 min) when
this dolphin raised the flipper Tsk slightly (ⱕ0.5°C)
above Tw and heat flow was temporarily from the
flipper to the water at ⬍30 W/m2. Because the surface
area of the flippers is ⬃0.15 m2, this amounts to ⬃4.5 W
(or 4.5 J/s) leaving the dolphin. This was the only
experiment in which this was observed, and it cannot
account for the large decrease in Tre. Likewise, the
16.82 W of heat loss from the region of the dorsal fin
exposed to air cannot account for the amount of heat
lost from the dolphin’s core. In contrast, during this
same 15-min period when Tre declines, an estimated
150.4 W was being gained from the environment via the
flukes and body surface.
Finally, there is no indication that dolphins increase
evaporative heat loss from their respiratory tract by
panting during exposure to warm water. Baseline
respiratory frequency ranged from 1.4 to 4.1 breaths/
min for all experiments (Table 2). During the warming
ramp and plateau, respiratory frequency sometimes
increased and sometimes decreased, but by ⬍1 breath/
min. The breaths taken did not seem to increase in
volume when the water was warmed, although tidal
volume was not measured directly. Also, dolphins are
breathing moist air from the layer immediately above
the water surface, such that the inhaled air is already
largely saturated with water. Thus the amount of
evaporation that can occur from respiratory surfaces is
limited to the difference in the amount of water in
inhaled air of 17–22°C (15 mg/l to 19.8 mg/l in saturated air) for the different experiments, and the amount
of water in saturated air being exhaled. Although it
seems that exhaled air would be near core temperature
(saturated 36°C contains 41.9 mg/l of water), measurements in experiments on six bottlenose dolphins by
Coulombe et al. (2) revealed otherwise. They found the
mean temperature and water content of inhaled air
was 19.4°C and 14 mg/l, respectively, and for exhaled
air, 22.9°C and 16.7 mg/l, respectively, with both being
75% saturated. This provides for only 2.7 mg/l water
loss rather than the 26.9 mg/l if exhaled air was 36°C
and 100% saturated. Irving et al. (6) measured tidal
volumes from bottlenose dolphins of 5.5–10 liters. For
the experiment shown in Fig. 2, the heat loss by
evaporation from the respiratory tract during the time
when core temperature declined is estimated as 0.1856
W. This is calculated from the change in respiratory
frequency (0.17 breaths/min), assuming the greatest
tidal volume of 10 liters, a 2.7 mg/l rate of water loss,
and there being 580 cal/s (or 2426.7 W) heat loss per
gram of water loss. Even if tidal volume had increased
from the lower 5.5 liters during baseline to a full 10
liters during the warming ramp, only 0.835 W could
have been lost from the respiratory tract via evaporation. The highest estimate of respiratory evaporative
heat loss in all ten experiments was 0.83 W if tidal
volume was unchanged at 10 liters or 3.73 W if tidal
TEMPERATURE REGULATION IN DOLPHINS
environment as in terrestrial mammals, but rather to
delay hyperthermia by both reducing core temperature
and limiting heat gain from the water.
Remarkable thermoregulatory responses have been
reported in some terrestrial mammals, including the
camel (20) and oryx (22) that inhabit hot, arid environments. Their response to heat stress involves a combination of evaporative heat loss and heat storage; the
latter increases in camels when they are dehydrated
(20). A large increase in core temperature during the
day earmarks heat storage. The heat is lost back to the
environment at night. Schmidt-Nielsen et al. (20) point
out that heat storage is valuable to terrestrial mammals both in limiting the amount of heat that is gained
from the hot environment and in conserving body
water. This is true because the increase in body temperature diminishes the temperature gradient between the
environment and the animal. As heat gain is reduced,
the need for evaporative heat loss is also diminished. In
dolphins, the redistribution of heat from the core to the
peripheral tissues is another adaptation that provides
this same advantage of reducing total heat gain from
the environment. Because core temperature never increased ⬎0.2°C above baseline levels during these
highly controlled short-term studies with dolphins, the
degree to which dolphins use heat storage as a thermoregulatory strategy remains unclear.
There are other reasons why it is difficult, and
perhaps inappropriate, to compare the thermoregulatory ability of marine mammals with that of terrestrial
mammals. The terrestrial and marine environments
are different and mandate different responses. For
example, evaporation is an essential mechanism in
mammals for heat loss in hot terrestrial environments.
However, this powerful heat loss mechanism, which
requires an air-water interface, is essentially unavailable in dolphins, which spend their lives submerged in
water, do not pant, and are inhaling air that is already
saturated with water. Also, dolphins must contend with
a higher rate of metabolic heat production than terrestrial mammals (17, 24). Finally, most terrestrial mammals lack the subcutaneous blubber needed for the
redistribution of heat that occurs in dolphins. The
exceptions, pigs and hippopotamuses, are unlikely to
encounter in their habitat the rapid transition from
cool to warm temperatures that make this response
useful.
Despite the limitations imposed by their aquatic
environment, dolphins have evolved a unique thermoregulatory response to safely extend their range into
the warmest marine water environments. The keystone of their response is an impressive redistribution
of heat in the body from the core to the peripheral
tissues. The sudden shift from using the blubber layer
and appendages as insulation in cool water to exploiting them as a heat sink in response to heat stress was
unexpected and is the most remarkable aspect of the
dolphins’ thermoregulatory response.
We thank Dr. W. G. Miller and the marine mammal trainers at
Bioscience Division, Naval Command Control and Oceans Surveillance Center for their technical assistance.
Downloaded from http://ajpregu.physiology.org/ by 10.220.33.5 on June 16, 2017
act as insulation, to act as an enormous heat sink to the
warm ambient water. Second, it provides a safety
margin in core temperature for the dolphin that has
entered an environment that may pose a ‘‘heat stress.’’
In the experiment illustrated in Figure 2, instead of the
dolphin becoming hyperthermic within a few minutes
(as would occur if Tre increased at onset of warming
ramp due to addition of metabolic heat that cannot be
lost to environment in these conditions), the decline in
Tre provides a remarkable hour-long delay to any
increase in core temperature. This mechanism probably allows the animal to safely enter a very warm,
shallow bay to forage briefly before returning to deeper
and cooler waters offshore. For example, dolphins have
been observed foraging in shallow, high-salinity bays of
the Arabian Gulf in summer in Tw as high as 36–38°C
(Ridgway, personal observation). The results of the
present study suggest that these dolphins would probably be active in deeper, cooler water of the gulf before
and after such foraging excursions.
It is important to note that the reduction in Tre did
not begin immediately as the warming ramp was
initiated but rather occurred several minutes (15–20
min) into the warming ramp. This suggests that this
thermoregulatory response is neither a passive nor an
immediate response to all encounters with warmer
water, but rather that it is a controlled response that is
probably orchestrated by the nervous system and likely
stimulated and driven by Tsk and/or rate of change in
Tsk.
There are several factors that can influence the
effectiveness of this thermoregulatory mechanism, including 1) the temperature of the blubber and skin
layers before the dolphin encounters warm water, 2)
the magnitude of the difference in temperature of the
core and peripheral tissues, and 3) the mass of the core
and peripheral tissues. These variables contribute to
the variations in the magnitude of the drop in core
temperature observed in experiments. Also note that
this mechanism can be used only one time during each
encounter with warm water because the peripheral
tissues can be warmed only once. Finally, it is important that this mechanism be used only when there is a
real threat of heat stress, because once the heat from
the core moves to peripheral tissues, it cannot be
gathered back to the core.
There are characteristics of this response in dolphins
that identify it as a true thermoregulatory adaptation
and distinguish it from responses observed in other
mammals. Humans and other homeotherms increase
blood flow to the skin specifically to enhance heat loss to
the environment. A small reduction in core temperature of short duration sometimes occurs as a by-product
of this response in humans moving quickly from a cold
to a hot environment (1). This temporary reduction in
core temperature provides no advantage to human
survival. In sharp contrast, the described thermoregulatory response by dolphins unequivocally provides an
advantage to their survival during encounters with
very warm water. Furthermore, blood flow to peripheral tissues is increased, not to increase heat loss to the
R1193
R1194
TEMPERATURE REGULATION IN DOLPHINS
This research was funded by the Office of Naval Research.
Address for reprint requests: M. E. Heath, Biodiversity Research
and Application Association, PO Box 22683, San Diego, CA 921922683 (E-mail: [email protected]).
Received 18 August 1998; accepted in final form 24 November 1998.
REFERENCES
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1. Ashoff, J., and R. Weaver. Kern und schale im waermehaushalt des menschen. Naturwissenschaften 45: 477–485, 1958.
2. Coulombe, H. N., S. H. Ridgway, and W. E. Evans. Respiratory water exchange in two species of porpoise. Science 149:
86–88, 1965.
3. Elsner, R., J. Pirie, D. D. Kenney, and S. Schemmer.
Functional circulatory anatomy of cetacean appendages. In:
Functional Anatomy of Marine Mammals, edited by R. J. Harrison. London: Academic, 1974, p. 143–159.
4. Hampton, I. F. G., G. C. Whittow, J. Szeierczes, and S.
Rutherford. Heat transfer and body temperature in the Atlantic bottlenose dolphin, Tursiops truncatus. Int. J. Biometeorol.
15: 247–253, 1971.
5. Hokkanen, J. E. I. Temperature regulation in marine mammals. J. Theor. Biol. 145: 465–485, 1990.
6. Irving, L., P. F. Scholander, and S. W. Grinnel. The respiration of the porpoise, Tursiops truncatus. J. Cell. Comp. Physiol.
17: 145–168, 1941.
7. Kanwisher, J., and G. Sundnes. Thermal regulation in cetaceans. In: Whales, Dolphins and Porpoises, edited by K. S. Norris.
Berkeley, CA: University of California, 1966, p. 1–397.
8. Kenney, R. D. Bottlenose dolphins off the northeastern United
States. In: The Bottlenose Dolphin, edited by S. Leatherwood and
R. R. Reeves. San Diego, CA: Academic, 1990, p. 369–386.
9. Kleiber, M. The Fire of Life. Huntington, NY: Kreiger, 1975, p.
1–453.
10. MacKay, R. S. Deep body temperature of untethered dolphin
recorded by ingested radio transmitter. Science 144: 864–866,
1964.
11. McGinnis, S. M., G. C. Whittow, C. A. Ohata, and H. Huber.
Body heat dissipation and conservation in two species of dolphins. Comp. Biochem. Physiol. A Physiol. 43A: 417–423, 1972.
12. McLean, J. A., and G. Tobin. Animal and Human Calorimetry.
Cambridge, UK: Cambridge University, 1987.
13. Pabst, D. A., S. A. Rommel, W. A. McLellan, T. M. Williams,
and T. K. Rowles. Thermoregulation of the intra-abdominal
testes of the bottlenose dolphin (Tursiops truncatus) during
exercise. J. Exp. Biol. 198: 221–226, 1995.
14. Parry, D. A. The structure of whale blubber, and a discussion of
its thermal properties. Q. J. Microsc. Sci. 90: 13–26, 1949.
15. Ridgway, S. H. Medical care of marine mammals. J. Am. Vet.
Med. Assoc. 147: 1077–1085, 1965.
16. Ridgway, S. H. Homeostasis in the aquatic environment. In:
Mammals of the Sea, edited by S. H. Ridgway. Springfield, IL:
Thomas, 1972, p. 590–747.
17. Ridgway, S. H., and G. S. Patton. Dolphin thyroid: some
anatomical and physiological findings. Z. vergl. Physiologie 71:
129–141, 1971.
18. Rommel, S. A., D. A. Pabst, W. A. McLellan, J. G. Mead, and
C. W. Potter. Anatomical evidence for a countercurrent heat
exchanger associated with dolphin testes. Anat. Rec. 232: 150–
156, 1992.
19. Rommel, S. A., D. A. Pabst, W. A. McLellan, T. M. Williams,
and W. A. Friedl. Temperature regulation of the testes of
bottlenose dolphin (Tursiops truncatus): evidence from colonic
temperatures. J. Comp. Physiol. [B] 164: 130–134, 1994.
20. Schmidt-Nielsen, K., B. Schmidt-Nielsen, S. A. Jarnum,
and T. R. Houpt. Body temperature of the camel and its relation
to water economy. Am. J. Physiol. 188: 103–112, 1957.
21. Scholander, P. F., and W. E. Schevill. Counter-current vascular heat exchange in the fins of whales. J. Appl. Physiol. 8:
279–282, 1955.
22. Taylor, C. R. The eland and the oryx. Sci. Am. 220: 88–97, 1969.
23. Tomlin, A. G. On the thermal regulation in cetaceans. Priroda
(Mosc.) 6: 55–58, 1951.
24. Williams, T. M., W. A. Freidl, and J. I. Haun. The physiology of
bottlenose dolphins (Tursiops truncatus): heart rate, metabolic
rate and plasma lactate concentration during exercise. J. Exp.
Biol. 179: 31–46, 1993.