temperature regulation in the california sea lion (zalophus californianus)

Temperature Regulation in the California Sea Lion (Zalophus californianus)Author(s): G. C. Whittow, D. T. Matsuura and Y. C. LinSource: Physiological Zoology, Vol. 45, No. 1 (Jan., 1972), pp. 68-77Published by: The University of Chicago PressStable URL: http://www.jstor.org/stable/30155928 .

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TEMPERATURE REGULATION IN THE CALIFORNIA SEA LION (ZALOPHUS CALIFORNIANUS)1

G. C. WHITTOW, D. T. MATSUURA, AND Y. C. LIN

Department of Physiology, School of Medicine, University of Hawaii, Honolulu, Hawaii 96822

INTRODUCTION

Under natural conditions, California Sea Lions are found as far south as Mexico, with a subspecies on the Gala- pagos Islands (Scheffer 1958). When they are on land, they may therefore encounter high air temperatures and high levels of solar radiation. It is un- certain whether they respond to these conditions by behavioral thermoregulation, as the field observations of Peter- son and Bartholomew (1967) would suggest, or by physiological means. The experiments reported in this paper were designed to investigate the latter pos- sibility-that these animals are physiologically equipped to deal with a hot environment, as some other species of pinnipeds appear to be (Bartholomew and Wilke 1956).

MATERIAL AND METHODS

Experiments were performed on three California sea lions approximately 1 year old, their body weight ranging from 38 to 45 kg. The animals were kept in pens out of doors and in the shade. Each pen was provided with a tub (6 ft long X 3 ft wide X 1 ft deep) of fresh running water, and each sea lion was fed 8% of its body weight a day, of frozen smelt, supplemented with vitamin and mineral capsules. As

the animals were always fed after an experiment and at the end of the day, they had fasted for approximately 16 hr before the experiment began.

Each animal was exposed, on a separate occasion, to each of four different air temperatures, approximately 36, 30, 18, and 10 C, in a temperature- controlled room. The relative humidity of the air could not be controlled, and in different experiments it varied within the range 46%-58%. However, in any one experiment, the humidity did not change by more than -L2 %. The air movement was approximately 50 ft/ minute. Throughout the exposure, which lasted for at least 3 hr, measurements were made at 20-min intervals of rectal temperature, skin temperature, hair surface temperature, heart rate, and respiratory rate. In addition, measurements of heat flow from the skin and tests for sweating were made after the animals had been in the climatic room for approximately 2! hr. Skin temperature measurements were made on a small area of shaved skin on the back, approximately 35 cm rostral to the tail, on an area of bare skin on one of the front flippers and on a similar area on one of the hind flippers. Measurements of heat flow and tests for the presence of sweating were also made on the area of shaved skin on the back of the animal. The data for heat flow (H) were used in conjunction with the values for rectal temperature (Tr) and skin tempera-

1 This work was supported by grant GB 8393 from the National Science Foundation and by the U.S. Naval Undersea Research and Development Center, Hawaii.

68



THERMOREGULATION IN SEA LIONS 69

ture (Ts) to compute the tissue insulation (I), in degrees Celsius, square meter, hour, per kilocalorie of heat flow, in accordance with the following relationship:

(Tr - Ts) oC I--

H (kcal/m2 hr)

The "thermal circulation index" (TCI) for the front flipper was computed as follows:

Ts - Ta TCI =TsTa

Tr - Ts'

where Tr, Ts, and Ta are the rectal temperature, skin temperature of the flipper, and air temperature, respec- tively (Burton and Edholm 1955). Hair surface temperatures were made contralaterally to the shaved area of skin on the back.

During the experiments, the animals wore a lightweight harness which was tethered to the sides of a specially designed pen. Although the animals could make small postural movements, they could not turn completely around within the pen. The head and neck of the animal were free. If the animal was wet before the experiment, suffi- cient time was allowed for it to dry before it entered the temperature-controlled room.

Measurements of rectal temperature were made by a Yellow Springs Instru- ment (YSI) thermistor probe (no. 401) inserted into the rectum to a depth of 12 cm. Skin and hair surface temperatures were measured by a YSI surface probe (no. 402). The probes were connected to a YSI Telethermometer (no. 46). Respiratory rates and heart rates were recorded by needle electrodes connected to a Physiograph impedance pneumograph and Hi-Gain preamplifier. Heat-flow determinations were made

with a Hatfield heat-flow disk (Hatfield 1950) connected to a Turner micro- voltmeter. Two methods were used to detect the presence of sweating: the starch iodide technique (Randall 1946) and by the application of quinizarin 2-6-disulfonic acid to the skin (Gutt- man 1942). Surface areas were esti- mated from linear measurements made on the animal; the trunk was treated as two cones and the flippers as tri- angles. The results of the experiments were examined statistically by the stu- dent t-test for two small samples (Bailey 1959).

RESULTS

FIELD OBSERVATIONS

When the animals were exposed to direct sunlight on land, they remained reasonably quiet until their coats had dried. Following this, their activity increased and small areas of shade or moisture were sought. Shallow burrows were excavated in the sand and the animals frequently lay on their backs and waved their front flippers. Each animal urinated under these conditions, and it was able, in this way, to keep the ventral surface of its abdomen and thorax moist. The respiratory rate did not appear to increase during exposure to solar radiation, but the three sea lions adopted an open-mouthed, gasp- ing type of breathing when they were clearly heat stressed.

LABORATORY STUDIES

Rectal temperature.-At air temperatures of approximately 36 and 30 C, the animals were unable to achieve thermal equilibrium and their rectal temperatures increased throughout the exposure (fig. 1). At the higher of these two environmental temperatures (36 C), the animals were in fact removed



70 G. C. WHITTOW, D. T. MATSUURA, AND Y. C. LIN

37-0 c o 55'6

x 30-4

0 6o0

37-0 - - o x o a - o 17-9

I I I I I I AI

O 30 60 90 120 150 180

TIME OF EXPOSURE (min) FIG. 1.-Rectal temperatures (Tr) of three California sea lions during exposure to the air tempera-

tures indicated to the right of the figure. Each point represents the mean value for the three animals, with the exception of the points connected by a broken line, which include data for two animals only.

from the climatic room when their rectal temperatures had reached 40 C, after 100-140 min. At air temperatures of 18 and 10 C, rectal temperatures were well maintained.

Skin temperatures and tissue insulation.-The skin temperature on the back of the animal increased in the two hotter environments (36 and 30 C). At air temperatures of 18 and 10 C, the skin temperatures tended to decrease with time, but periods of activity on the part of the animal resulted in increases in skin temperature (fig. 2). Comparison of the skin temperatures at the different air temperatures suggested that a decrease in the blood flow to the skin occurred between air temperatures of 18 and 10 C. Some support for this suggestion is provided

by the data presented in figure 3, which shows the tissue insulation at different air temperatures. The data are rather fragmentary, but they do indicate that at air temperatures above approximately 15 C the tissue insulation is low but that at temperatures below 15 C the insulation increases rather abruptly.

Flipper skin temperatures.-The skin temperature of the flippers also increased in the two hotter environments and tended to decrease at air temperatures of 18 and 10 C (fig. 4). The behavior of the flipper skin temperature was similar to that of the trunk in that the temperature increased when the animal became active. An additional source of variation in the skin temperature of the flipper was provided




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-o 179

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I I I I I I I1 0 30 60 90 120 150 180

TIME OF EXPOSURE (min) FIG. 2.-Skin temperature (Ts) on the back of three California sea lions during exposure to differ-

ent air temperatures. Notations as in fig. 1.

by the animal tucking its flipper under its body. When this occurred, the flipper temperature increased. It was dif- ficult to decide from the data for flipper temperatures whether there was an underlying change in blood flow at the different air temperatures. In order to provide more information on this point, the thermal circulation index (TCI) was computed for the front flipper after the animals had been exposed to each of the four air temperatures for 100 min. The results are shown in figure 5. The main point illustrated by figure 5 is that the TCI was signifi- cantly lower (t = 89.7; .02 > P > .01) at an air temperature of 18 C than at 30 C.

The surface area of the flippers represented 31% (30%-33 % ) of the total surface area of the animals.

Hair temperature.-In general, the surface temperature of the coat varied in a manner similar to that of the skin temperature of the shaved area on the back. At the lowest air temperatures used, however, it was observed that the temperature of the hair was higher than that of the shaved skin, which suggested that the skin temperature under the hair was even higher.

Respiratory rates.-The mean respiratory rates of the three animals at the four air temperatures are presented in figure 6. The pattern of breathing was irregular and the respiratory rates were low. There was no evidence of thermal polypnea at the higher air temperatures, but the three animals did adopt open-mouthed breathing when they were hyperthermic and they salivated profusely.




0-180-F

- 0-030

E x

G 0.020

10 20 30

AIR TEMP. (0C) FIG. 3.-Tissue insulation (I) on the back of the California sea lion at different air temperatures.

Each point represents a single measurement on one of the animals. The different symbols identify the three animals.

Cutaneous moisture loss.-Neither of the techniques used indicated that sweating occurred when the animals were hyperthermic.

Heart rates.-The heart rates were irregular, varying with each respira- tion and with the activity of the animals. These variations tended to ob- scure any effect of temperature on the heart rate. In the few instances in which the animals did not struggle un- duly, the heart rate increased by 10- 15 beats/minute when the animals became hyperthermic.

Shivering.-One animal shivered at an air temperature of 9 C, when its rectal temperature was 36.7 C, the temperature of the shaved skin was 19.9 C, and the temperature on the surface of the coat was 23.3 C.

Other responses.-When the animals became hyperthermic, at air temperatures of 30 and 36 C, they urinated at a deep body temperature of approximately 38.5 C. When the rectal temperature exceeded 39 C, the animals defecated frequently.

DISCUSSION

Under the conditions prevailing in these experiments, the sea lions were unable to attain thermal equilibrium at air temperatures of 30 or 36 C. An air temperature of 30 C is not unlikely in the Galapagos Islands or off the Mexican coast. With an added heat load from solar radiation, sea lions would not be able to endure such conditions continuously for more than a




.-- 35-6

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r 30-0 . 0---- 17-9

c_

250

20.0

10.1

15-00 15 30 I I I I I 180 0 30 60 90 120 150 180

TIME OF EXPOSURE (min)

FIG. 4.-Skin temperature on the front flippers of three California sea lions at various air temperatures. Notations as in fig. 1.

few hours. This conclusion conforms with the field observations on the Cali- fornia sea lion made by Peterson and Bartholomew (1967).

The diminution in the skin temperature of the back and the increase in tissue insulation between air temperatures of 18 and 10 C suggest that a decrease in the blood flow to the skin occurred between these temperatures. In this respect, the sea lion differs from terrestrial haired mammals such as the ox (Whittow 1962), in which the skin temperature of the trunk decreases uni- formly with environmental temperature. On the other hand, it resembles relatively hairless animals such as the pig (Ingram 1964) and another marine mammal, the walrus (Ray and Fay 1968). There is evidence of a similar phenomenon in the Weddell seal (Ray and Smith 1968) and also in the harbor seal (Hart and Irving 1959). The air temperature at which a large diminution in skin temperature occurs

varies, however, in different species. This conclusion has to be qualified, in the case of the sea lions, in the light of the relatively high hair temperature at low air temperatures. This may mean that the blood flow through the skin under the coat does not diminish until air temperatures lower than those used in the present investigation are reached. It would be interesting to know whether the skin blood flow of a species such as the northern fur seal, which has a thick waterproof coat, be- haves in a manner similar to that of species with a short wettable coat.

Evidence that the blood flow through the flippers diminishes between air temperatures of 30 and 18 C, that is, at a higher level of air temperature than that of the skin of the back, is to be expected. The flippers have a higher ratio of surface area to volume than does the trunk of the animal, and they should lose heat more rapidly. A thermoregulatory function for the




12-OT-

50 x 5-0-

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2-0-

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I-I

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AIR TEMP. (0C) FIG. 5.-Thermal circulation index (TCI) of the front flippers of three California sea lions at various

air temperatures. Notations as in fig. 3. The highest point (X) is not connected to its fellows be- cause in this instance the flipper was tucked under the body of the animal.

flippers has been claimed in the harbor seal (Irving and Hart 1957; Hart and Irving 1959), the northern fur seal (Irving et al. 1962), the walrus (Ray and Fay 1968), and the Weddell seal (Ray and Smith 1968).

Although changes in the insulation, TCI, and skin temperature of the back and flippers have been interpreted in terms of variations in blood flow, they could equally well be explained by a countercurrent heat-exchange mechanism between arterial and venous blood, operating with or without a

change in blood flow (Scholander and Krog 1957). There is no anatomical or histological evidence for this in the California sea lion, but the arrange- ment of the blood vessels in the flippers of the northern fur seal and harbor seal provides the basis for such a mechanism (Tarasoff and Fisher 1970). In view of the high proportion of the total surface area represented by the flippers, they are probably of considerable importance in the regulation of heat loss in sea lions, par- ticularly under cold conditions.




8-0

7-0 A 10-1

35-6 6.0- x . x

30"4

o: 40 - 0-o - p

o o

2-0

30 60 90 120 150 180

TIME OF EXPOSURE (min) FIG. 6.-Respiratory rates of the three sea lions at different air temperatures. Notations as in

fig. 1.

At an air temperature of 36 C, the tissue insulation on the trunk of the animal was higher while the TCI in the flipper tended to be lower, than at an air temperature of 30 C. Although the differences are not statistically significant, they do suggest that at elevated levels of body temperature the blood flow to the skin may ac- tually decrease, possibly associated with a diminution of cardiac output (Whittow, Sturkie, and Stein 1964).

The absence of thermal polypnea in sea lions, even at a rectal temperature higher than 40 C, was surprizing in view of reports that both the northern fur seal (Bartholomew and Wilke 1956) and the harbor seal (Harrison and Kooyman 1968) pant when they are hot. On the other hand, Peterson

and Bartholomew (1967) did not ob- serve panting in the California sea lion rookery on San Nicholas Island, even in bulls engaged in vigorous fighting. Furthermore, panting did not occur in either the Weddell seal (Ray and Smith 1968) or the walrus (Ray and Fay 1968). The absence of thermal polypnea does not necessarily mean that sea lions are not able to increase their respiratory evaporative water loss during exposure to heat. The open- mouthed breathing observed during hyperthermia might result in a signifi- cantly greater moisture loss per breath, in spite of the fact that the respiratory rate did not increase. This could be accomplished by a greater tidal volume or by a diminished cooling of the expired air when the animal breathed




through its mouth (Schmidt-Nielsen, Bretz, and Taylor 1970).

The failure to detect sweating during exposure to heat was unexpected in the light of reports that sweating occurs in the northern fur seal (Bar- tholomew and Wilke 1956), albeit from the flipper. Preliminary histological studies on the skin of the Cali- fornia sea lion indicate that there are sweat glands in the skin. Their ap- parent failure to respond to heat is analogous to the absence of thermal sweating in the pig (Ingram 1964) and the dog (Aoki and Wada 1951).

The sea lion appears to be one of the very few mammals that neither sweats nor pants. The only water available to marine mammals is the water in their food, and seawater. There is little evidence that seals drink seawater or that their kidneys are especially equipped to deal with it (Harrison and Kooyman 1968; Depocas, Hart, and Fisher 1969). It is possible therefore that in marine mammals con- siderations of water economy take precedence over the regulation of body temperature.

Although measurements of heat production were not made in this study, it is of interest that one animal shivered when its skin temperature was close to 20 C. Hart and Irving (1959) noted that the heat production of the harbor seal increased, at a similar skin temperature, when the animals were tested during the summer.

During this investigation, evidence was obtained that the California sea lion has a strongly developed pattern

of thermoregulatory behavior, which is described in more detail in another report (Whittow, Ohata, and Mat- suura 1971). This would accord with the field observations of Peterson and Bartholomew (1967), and with the conclusion which has emerged from the present study, that sea lions are not very well equipped physiologically to deal with a hot environment.

SUMMARY

The physiological responses of three California sea lions to different environmental temperatures were studied, principally in order to determine whether this species is physiologically equipped to deal with a hot environment.

None of the animals was able to achieve thermal equilibrium at an air temperature of 30 or 36 C. At 36 C, the animals were removed from the climatic room when their rectal temperatures had increased to 40 C.

Evidence was obtained that sea lions respond to these conditions by increas- ing the blood flow to the skin both on the trunk and in the extremities.

Neither thermal polypnea nor sweating was observed during exposure to heat, indicating that physiological evaporative cooling mechanisms are relatively unimportant in this species.

The sea lions appeared to show a strongly developed pattern of thermoregulatory behavior when exposed to heat, which suggests that behavioral mechanisms of temperature regulation may be more important than physiological temperature regulation.

LITERATURE CITED

AoKI, T., and M. WADA. 1951. Functional activity of the sweat glands in the hairy skin of the dog. Science 114:123-124.

BAILEY, N. T. J. 1959. Statistical methods in biology. English University Press, London.

BARTHOLOMEW, G. A., and F. WILKE. 1956. Body




temperature in the northern fur seal, Cal- lorhinus ursinus. J. Mammal. 37:327-337.

BURTON, A. C., and 0. G. EDHOLM. 1955. Man in a cold environment. Arnold, London.

DEPOCAS, F., J. S. HART, and H. D. FISHER. 1969. Sea water drinking and water balance in the harbor seal. Amer. Zo6l. 9:587.

GUTTMAN, L. 1942. A demonstration of the study of sweat secretion by the Quinizarin method. Roy. Soc. Med., Proc. 35:77-78.

HARRISON, R. J., and G. L. KOOYMAN. 1968. General physiology of the pinnipedia. In: The Behavior and Physiology of Pinnipeds. ed. R. J. HARRISON, R. C. HUBBARD, R. S. PETER- SON, C. E. RICE, and R. J. SCHUSTERMAN (ed.), The behavior and physiology of pin- nipids. Appleton-Century-Crofts, New York.

HART, J. S., and L. IRVING. 1959. The energetics of harbor seals in air and in water with special consideration of seasonal changes. Can. J. Zo61l. 37:447-457.

HATFIELD, H. S. 1950. A heat-flow meter. J. Physiol. 111:10-11.

INGRAM, D. L. 1964. The effect of environmental temperature on heat loss and thermal insulation in the young pig. Res. Veterinary Sci. 5:357-364.

IRVING, L., and J. S. HART. 1957. The metabolism and insulation of seals as bare-skinned mammals in cold water. Can. J. Zobl. 35:497-511.

IRVING, L., L. J. PEYTON, C. H. BAHN, and R. S. PETERSON. 1962. Regulation of temperature in fur seals. Physiol. Zo61l. 35:275-284.

PETERSON, R. S., and G. A. BARTHOLOMEW. 1967. The natural history and behavior of the California sea lion. American Society of Mammalogists.

RANDALL, W. C. 1946. Sweat gland activity and changing patterns of sweat secretion on the skin surface. Amer. J. Physiol. 147:391-398.

RAY, C., and F. H. FAY. 1968. Influence of climate on the distribution of walruses, Odo- benus rosmarus (Linnaeus). II. Evidence from physiological characteristics. Zoologica 53:19- 32.

RAY, C., and M. S. R. SMITH. 1968. Thermo- regulation of the pup and adult Weddell seal, Leptonychotes weddelli (Lesson), in Antarc- tica. Zoblogica 53:33-48.

SCHEFFER, V. B. 1958. Seals, sea lions and walruses. Stanford University Press, Stanford, Calif.

SCHMIDT-NIELSEN, K., W. L. BRETZ, and C. R. TAYLOR. 1970. Panting in dogs: unidirectional air flow over evaporative surfaces. Science 169:1102-1104.

SCHOLANDER, P. F., and J. KROG. 1957. Counter- current heat exchange and vascular bundles in sloths. J. Appl. Physiol. 10:405-411.

TARASOFF, F. J., and H. D. FISHER. 1970. An- atomy of the hind flippers of two species of seals with reference to thermoregulation. Can. J. Zodl. 48:821-829.

WHITTOw, G. C. 1962. The significance of the extremities of the ox (Bos taurus) in thermoregulation. J. Agr. Sci. 58:109-120.

WHITTOw, G. C., C. A. OHATA, and D. T. MATSUURA. 1971. Behavioral control of body temperature in the unrestrained California sea lion. Commun. Behav. Biol. 6:87-91.

WHITTOW, G. C., P. D. STURKIE, and G. STEIN, JR. 1964. Cardiovascular changes associated with thermal polypnea in the chicken. Amer. J. Physiol. 207:1349-1353.



temperature regulation in the california sea lion (zalophus californianus)

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