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Influence of thermal and nutritional acclimatization on body temperatures and metabolic rate
0300-9629~x3;030511)-05s03.00’I~ 0 19X3 Pergkamon Press Ltd
INFLUENCE OF THERMAL AND NUTRITIONAL ACCLIMATIZATION ON BODY TEMPERATURES AND METABOLIC RATE M. MACARI*, D. L. Department
of Applied
and M. J. DAUNCEY
INGRAM
Biology, ARC Institute of Animal Cambridge CB2 4AT, UK (Received
12 July
Physiology,
Babraham,
1982)
Abstract-l. An investigation of the influence of previous thermal and nutritional experience on body temperatures and metabolic rate has been carried out with growing piglets, Littermates were kept. from shortly after birth, at either 10 or 35’C and fed either a high (H) or a low (L) energy intake. At 8 weeks of age the animals were exposed to a series of environmental temperatures of 10, 20, 27 and 35°C for 1.5 hr and their rates of oxygen consumption were determined over the last 45 min. At the end of the session body temperatures were measured, 2. Rectal temperatures measured 24 hr after the start of the last meal were higher at each test temperature in piglets which had been living at 35°C than in those at 10°C. Also, rectal temperatures were higher in those on the H intake for animals which had been living in either the hot or the cold environment. 3. Skin temperature on the back was similar in all groups at any given test temperature although there was a tendency for those on an H intake to have the higher temperatures. Skin temperatures of the legs and ears were higher in the IOH and 1OL groups than in the 35H or 35L groups at all the test environmental temperatures; energy intake had little effect. 4. Metabolic rate was greater for the animals on the H than the L intake, for those which had been living at either 10 or 35°C at all the test environmental temperatures. The analysis did not reveal any significant difference related to the overall effect of living temperature. which was independent of energy intake. 5. At thermal neutrality (27’C) there was a significant interaction, between energy intake and normal living temperature, on metabolic rate. Living temperature was found to modify the effect of intake: the difference between the two intakes was greater in those from the cold environment than from the hot.
INTRODUCTION Studies of acclimatization ture have been made
to environmental
tempera-
in many species (Chaffee & Roberts, 1971) but in few investigations has the energy intake of the animals been controlled. If homeotherms live in either a hot or a cold environment, then for those in the cold energy intake increases to meet the demand for thermoregulatory thermogenesis, while in the hot environment food intake declines (Hamilton, 1976). A change in energy intake even in the absence of a change in ambient temperature affects several physiological systems. Animals on a high energy intake have an elevated resting metabolic rate and this improves the tolerance to cold and so lowers the critical temperature (Graham et al., 1959. in sheep; Close et (I/., 1971, in pigs; Dauncey, 1980, in man). An increase in energy intake also affects the metabolism of thyroid hormones (Ingram & Kaciuba-Uscilko, 1977, in pigs) and thermoregulatory behaviour (Weiss, 1957, in mice; Baldwin & Ingram, 1968, in pigs). Some of the changes in physiological parameters which occur after acclimatization may therefore be related to the concomitant increase in energy intake rather than to environmental temperature per se.
The growing pig provides a useful subject in which to study problems on the interaction between temperature and nutrition because the animal’s ad /ihitum food intake is large even at high ambient temperatures, and therefore two markedly different intakes can be eaten in both a hot and a cold environment. In the present investigation body temperatures and metabolic rates have been measured at a series of test ambient temperatures, in piglets living from shortly after birth in an environment which was either hot or cold and on either a high or a low energy intake. The objectives of the study were two-fold. First, to determine what changes in body temperatures and metabolic rate occur after prolonged exposure to different combinations of environmental temperature and energy intake. Second, to determine if environ-, mental temperature exerts an effect which is independent of that due to energy intake. MATERIALS AND METHODS
Thirty-six piglets from eight litters of the Large breed kept at the Institute farm were used. Acclimatimtior~ All animals
* On leave from UNESP
aud eneryy
White
intuke
were removed from the sow at 12-14 days of age and housed in individual pens. Half the animals in
Brazil. 549
M. MACARI et al.
550
each htter were placed in a room where the temperature was reduced from 28 to 10°C over a 14 day period; the rest were kept in a room where the temperature was increased from 28 to 35°C over the same period. The animals in each room were divided into one set which received a high (H) energy intake of standard feed and another which received a low intake (L), in a single meal once per day. The actual amount of food given was increased as the animals grew, but the ratio of H to L was always 2: 1 and by the age of 6 weeks it was fixed at 600 or 300 g. All piglets were weighed daily. E\-perimental
ofoxygen
this way the significance of the separate contributions of individual factors to the total variance could be tested. In particular, attention was paid to the effects of: (1) the temperature at which the animals had been living, (2) the level of energy intake and (3) the interaction between temperature and energy Intake. A significant interaction could for example mean that the effect of energy intake was different at 35 compared with 10°C.
RESULTS The body weights of the animals at the time that the measurements were made are given in Table 1. As
expected, the heaviest piglets were the 35H group and the lightest the 1OL. The absence of any demand for thermoregulatory heat production at 35°C combined with a low intake, on the one hand and the high thermoregulatory demand combined with a high energy intake at lO”C, on the other, resulted in intermediate weights for the 35L and 10H groups. Body
consumption
Rates of oxygen consumption were determined in an open circuit respiration chamber using a paramagnetic analyser (Type OA 184, Taylor Servomex Ltd). The chamber was of a similar size and construction to the animal’s own living pen and was housed in a temperature controlled room. A closed circuit television system enabled an observer to monitor the animal and only those values of oxygen consumption which corresponded to a period when it was inactive were used. Each session lasted 1.5 hr and was started 24 hr after the last meal, which had usually been eaten within 2 hr. Values for oxygen consumption were corrected to STP and expressed as ml Oz/kgo.75 per min. The 0.75 exponent was used to correct for differences in body weight and was of particular importance since the animals on different treatments grew at different rates. Measurement
analysis
The results were subjected to the analysis of variance. In
procedure
When the animals were seven weeks of age each was placed in the respiration chamber at its normal living temperature for 1.5 hr every day, to accustom it to the procedure. At eight weeks of age the rate of oxygen consumption was measured at the animal’s normal living temperature and in the subsequent week at a series of other environmental temperatures of 10, 20 and 27°C. In preliminary studies, it had been found that piglets which had been living in the cold developed hyperthermia at 35”C, particularly if they had been on a high energy intake and therefore determinations were not made at 35°C for piglets which had been living in the cold. Rate
Statistical
of body temperatures
Rectal temperature was measured at the end of 1.5 hr in the respiration chamber, by inserting a probe 50 mm deep into the rectum. Skin temperatures were measured at the same time by attaching probes to the skin with surgical tape. The temperature of the skin was recorded on the tip of the ear, over the carpels and on the back to one side of
the mid line between the scapulae.
Table
temperatures
Rectal
(Fig. la). A separate analysis temperatures was made for each of the test temperatures and it was found that in each case the effect of the living temperature was significant, with those from 35°C having the higher deep body temperature (P < 0.001). In addition, there was also a significant effect of energy intake, with those on the H intake having the higher deep body temperature (P < 0.001 at 27 and 20°C; P < 0.05 at 10°C). The interactions for each analysis of variance were also significant (P < 0.01) suggesting that the effect of energy intake on the deep body temperature was more striking for those living in the cold than in the hot. Skin temperatures on the back (Fig. lb). There were no significant differences in the temperatures recorded on the backs of the animals on different treatments, Skin temperutures on the extremities (Figs lc und Id). The temperatures recorded on the pina of the ear and over the carpels were significantly higher in those animals which had been living at 10 than at 35°C at each of the test temperatures (P < 0.01). By contrast, the level of energy intake had little effect, although there was a tendency for the temperatures on the leg
1. Body weights of piglets living at 10 or 35°C on a high (H) or low (L) energy intake
Treatment
Body
weight (kg)
SEM Number animals
Group
10H
1OL
35H
35L
14.0
7.4
16.9
10.7
0.21
0.12
0.81
0.42
9
8
8
9
of
Values were recorded on the day that oxygen body temperatures were first determined.
consumption
and
Acclimatization
551
Fig. 1. Mean values of deep body and peripheral temperature, measured at various test ambient temperatures, in piglets which had been living at 10 or 35°C on a high (H) or low (L) energy intake: 0 lOH, ??lOL, A 35H, A 35L.
to be greater on the H than on the L intake lowest test temperature (Fig. id, P < 0.05).
at the
Resting metabolic rute The rates of oxygen consumption obtained at each of the test temperatures are given in Table 2a. The results for each environmental temperature at which the animals were tested were analysed separately to test the hypothesis that the rate of oxygen consumption at any given temperature depended partly on the animal’s energy intake and partly on the temperature at which the animal normally lived. Table 2b presents the values from the analysis of variance which are related to the separate effects of living temperature and energy intake. In this table, for example, the value for the H intake was been averaged over temperature, i.e. the mean of IOH and 35H; similarly the values of, e.g. 1OC have been averaged over energy intake, i.e. IOH and 1OL. For all the treatment groups, 27’C represented a thermally neutral environment at which there was neither shivering nor hyperthermia. At this temperature the analysis revealed that the differences in metabolic rate related to energy intake were statistically significant (P < 0.001) whereas those related to the temperature at which the animals had been living were not (Table 2b). Moreover the interaction term between the effects due to the living temperature and to energy intake was also significant (P < 0.001). This indicated that the difference in oxygen consumption related to energy intake was greater for the animals which had been living in the cold environment than for those which had been living in the hot. Analysis of the values for oxygen consumption determined at 20 and 10°C also showed a statistically significant effect related to energy intake (P < 0.001) but not to the animal’s normal living temperature. At these environmental temperatures the interaction term was not statistically significant, suggesting that the effect of energy intake on oxygen consumption
was similar for animals and 35°C.
which had been living at 10
DISCUSSION
The present results show that 24 hr after presentation of the last meal, which was usually eaten within 2 hr, piglets which had been living at 10°C had lower rectal temperatures than those which had been living at 35°C. A low rectal temperature has been reported in people living in the cold, and groups such as the Australian aborigines and the Kalahari bushmen who have been exposed to cold for long periods tolerate this fall in deep body temperature without shivering (Wyndham & Morrison, 1958. Hammel et al., 1959). A decline in core temperature in the cold could be regarded as advantageous since less energy would be required to regulate the body at a lower temperature. The level of energy intake was also found to influence rectal temperature, particularly in those which had been living at 10°C with those on the H intake having the higher core temperature. If those living at 10°C had been allowed to eat cld lib. they would have taken more food than the amount provided as the H intake and would then have been subjected to two opposing influences on their core temperatures The particular body temperature achieved by an animal will thus depend on the balance between the relative influences of ambient temperature and energy intake. For example, Hamilton & Brobeck (1964) reported that rats which had been exposed to the cold for 3 weeks and allowed to eat ud lib. had higher deep body temperatures than did controls. The higher rectal temperature associated with an ambient temperature of 35°C does not appear to confer any obvious advantage on the animal. It is true that a high core temperature increases the gradient over which heat can be lost, but the Arrhenius-Vant Hoff effect increases metabolic rate and thus increases the heat load. However, it is clear that the animals in
552
M. MACARI et ul. Table Za. Resting temperatures
oxygen consumption (ml 02/kgo~” per min) measured at various environmental for piglets normally living at 10 or 35’C on a high (H) or a low (L) energy intake (mean values k SEM) Temperature
Treatment
Group
n
at
measurements
8
15.5
+ 1.22
10.4
35L
9
12.4
i
1.15
10H
9
17.8
f
1OL
8
11.0
t
made
(OC) 35
27
0.69
8.2
? 0.53
9.2
? 0.79
8.1
i 0.65
6.5
? 0.50
6.5
? 0.40
1.15
11.5
t 0.65
11.2
? 0.50
1.31
7.0
0.83
5.3
? 0.64
Table 2b. Mean values for oxygen consumption normal living temperature and energy intake
i
i
(ml OJkg”.‘”
Temperature
factor
per min) related
at
which
to the separate
measurements
effects of
were
made
(OC)
27
20
10
Living temperature energy intake) .:, qver
were
20
10
35H
Environmental
which
(averaged
:
Energy intake* (averaged over living temperature):
35Oc
13.9
? 0.84
9.3
? 0.48
7.4
+ 0.37
10°C
14.4
f 0.87
9.2
? 0.53
8.2
f
High
16.6
? 0.84
10.9
i
0.48
9.7
+ 0.37
Low
11.7
t
5 0.53
5.9
+ 0.41
0.87
Values taken from the analysis of variance (means f SEM). * Differences related to energy intake were all statistically significant, lo hving temperature were not
the present study had very different tolerances of heat, since those living at 10°C could not be tested at 35°C without risk of severe hyperthermia. This difference in tolerance was probably related to some physiological property or properties acquired by the animals living at 35”C, rather than to the effects of living at IO”C, * since differences in tolerance have been demonstrated previously between piglets living at thermal neutrality (26°C) or in a hot environment (35°C) (Ingram, 1977). By contrast with rectal temperature, the skin temperatures on the extremities were higher as a result of living in the cold than in the hot, whereas the level of energy intake had virtually no effect. A similar situation has again been described in adult man. Studies on the GaspC fishermen have shown that these people, who habitually have to immerse their hands in cold water while working, have a higher blood flow in their hands and tolerate the cold conditions better than do controls (LeBlanc et al., 1960). As a consequence of this higher blood flow and hence much greater rate of heat loss, the Gasp& fishermen have an exaggerated response to cooling of the whole body and shiver more than do controls under such conditions. Similarly, peripheral temperatures and hence blood flow have been found to be higher in Eskimo people than in Europeans (Brown et CL/.,1954). This protection against tissue cooling which is given by the high blood flow is possible only by the use of more energy for heat production, but in spite of this extra requirement there was very little evidence of a reduc-
7.6
P < 0.001, whereas
0.41
those related
tion in extremity temperatures when energy intake was low in those living in the cold in the present study. Consideration of the rates of oxygen consumption in Table 2a suggests that, at any given environmental temperature, metabolic rate is influenced more by energy intake than by the environmental temperature at which the animal normally lives. For example at a test temperature of 10°C there is a large difference in the rate of oxygen consumption between H and L intakes for animals which had been living either in the hot or in the cold. By contrast there is very little difference between 35H and 10H or between 35L and 1OL. Statistical tests aimed at separating the independent effects of energy intake and living temperature revealed that at each of the test temperatures at which the metabolic rate was estimated there was an effect related to energy intake but not to the temperature at which the animals had been living. The results thus indicate that the metabolic response to a given environmental temperature is not influenced by prolonged exposure to heat or cold alone. Under conditions where animals can eat ud lib., differences in metabolic rate which are apparently related to environmental temperature will develop, because in the cold more food will be eaten. The metabolic rate at 27°C is of particular significance because it was thermally neutral for all the animals. At this temperature there was no shivering and no hyperthermia and the rate of oxygen consumption
Acclimatization
therefore provided an estimate of the basal metabolic rate. At this test temperature there was a difference related to the independent effect of energy intake but not to that of living temperature. The analysis, however, revealed that there was a significant interaction between energy intake and living temperature which indicated that the effect of energy intake on metabolic rate was significantly greater in animals normally living in a cold environment than in the hot. The basal metabolic rate at thermal neutrality is therefore influenced indirectly by the temperature at which the animal normally lives because it modifies the effect of energy intake. It is therefore concluded that after acclimatization body temperatures are directly influenced by both living temperature and energy intake. By contrast, the changes in the metabolic response to environmental temperature which occur after prolonged exposure to hot or cold temperatures depend predominantly on the induced changes in energy intake. Thus the overall effects of acclimatization can be assessed only when energy intake is taken into account. Acknu~~(edyrme,lt-The authors ARC Statistics Group, Cambridge sis.
thank Mr D. E. Walters, for the statistical analy-
REFERENCES
BALDWIN B. A. & INGRAM D. L. (1968) The effects of food intake and acclimatization to temperature on behavioral thermoregulation in pigs and mice. P/~ysiol. B&m. 3,
395-400. BROWN G. M., BIRD G. S., BOAG T. J., BOAG L. M., DELAHAYE J. D., GREENJ. E., HATCHER J. D. & PAGE J. (1954) The circulation in cold acclimatization. Circulufian 9, 813-822.
553
CHAFFEE R. R. J. & ROBERTS J. C. (1971) Temperature acclimatization in birds and mammals. A~III. Rrr. Physioi. 33, 155-202. CLOSE W. H., MOUNT L. E. & START I. (1971) The influence of environmental temperature and plane of nutrition on heat losses from groups of growing pigs. Atlir,~. Prod. 13, 285-294. DAUNCEY M. J. (1980) Metabolic effects of altering the 24 hour energy intake in man, using direct and indirect calorimetry. Br. J. Nurr. 43, 257-269. GRAHAM N. McC., WAINMAX F. W., BLAXTER K. L. & ARMSTRONG D. G. (1959) Environmental temperature, energy metabolism and heat regulation in sheep 1. Energy metabolism in closely clipped sheep. J. uqric. Sci. 12, 13-24. HAMILTON C. L. (1976) Environmental temperature and feeding behaviour. In Progress in Biornrteorology. Div. B. Vol. 1, Part 1 (Edited by TRUMP S. W.). pp. 174-18.3. Swets & Zeitlinger, Amsterdam. HAMILTON C. L. & BROBECK J. R. (1964) Food intake and temperature regulation in rats with rostra1 hypothalamic lesions. Ain. J. Physiol. 207, 29 I-297. HAMMEL H. T., ELSNER R. W., Lr M~SURIER D. H.. AKIXRSEN H. T. & MILAN F. A. (1959) Thermal and metabolic responses of the Australian aborigine exposed to moderate cold in summer. J. uppl. Physiol. 14, 605 -615. INGRAM D. L. (1977) Adaptation to ambient temperature in growing pigs. efiiicqrrs Arch. qc’s. Physiol. 367, 257-264. INGRAM D. L. & KACIUBA-USCILU H. ( 1977) The influence of food intake and ambient temperature on the rate of thyroxine utilization. J. Physinl. Lmd. 270, 43 I-438. LEBLANC J.. HILDES J. A. & HEROUX0. (1960) Tolerance of Gasp& fishermen to cold water. J. trppi. Pl~~~siol. 15. 1031-1034. WEISS B. (1957) Thermal behaviour of the subnourished and pantothenic acid deprived rat. J. wnp. Phy.siol. Psychol. 50, 481-485. WYNDHAM C. H. & MORRISO> J. F. (19581 Adjustment to cold of Bushmen in the Kalahari Desert. J. upoi. Ph~siol: 13, 219-225.
INFLUENCE OF THERMAL AND NUTRITIONAL ACCLIMATIZATION ON BODY TEMPERATURES AND METABOLIC RATE M. MACARI*, D. L. Department
of Applied
and M. J. DAUNCEY
INGRAM
Biology, ARC Institute of Animal Cambridge CB2 4AT, UK (Received
12 July
Physiology,
Babraham,
1982)
Abstract-l. An investigation of the influence of previous thermal and nutritional experience on body temperatures and metabolic rate has been carried out with growing piglets, Littermates were kept. from shortly after birth, at either 10 or 35’C and fed either a high (H) or a low (L) energy intake. At 8 weeks of age the animals were exposed to a series of environmental temperatures of 10, 20, 27 and 35°C for 1.5 hr and their rates of oxygen consumption were determined over the last 45 min. At the end of the session body temperatures were measured, 2. Rectal temperatures measured 24 hr after the start of the last meal were higher at each test temperature in piglets which had been living at 35°C than in those at 10°C. Also, rectal temperatures were higher in those on the H intake for animals which had been living in either the hot or the cold environment. 3. Skin temperature on the back was similar in all groups at any given test temperature although there was a tendency for those on an H intake to have the higher temperatures. Skin temperatures of the legs and ears were higher in the IOH and 1OL groups than in the 35H or 35L groups at all the test environmental temperatures; energy intake had little effect. 4. Metabolic rate was greater for the animals on the H than the L intake, for those which had been living at either 10 or 35°C at all the test environmental temperatures. The analysis did not reveal any significant difference related to the overall effect of living temperature. which was independent of energy intake. 5. At thermal neutrality (27’C) there was a significant interaction, between energy intake and normal living temperature, on metabolic rate. Living temperature was found to modify the effect of intake: the difference between the two intakes was greater in those from the cold environment than from the hot.
INTRODUCTION Studies of acclimatization ture have been made
to environmental
tempera-
in many species (Chaffee & Roberts, 1971) but in few investigations has the energy intake of the animals been controlled. If homeotherms live in either a hot or a cold environment, then for those in the cold energy intake increases to meet the demand for thermoregulatory thermogenesis, while in the hot environment food intake declines (Hamilton, 1976). A change in energy intake even in the absence of a change in ambient temperature affects several physiological systems. Animals on a high energy intake have an elevated resting metabolic rate and this improves the tolerance to cold and so lowers the critical temperature (Graham et al., 1959. in sheep; Close et (I/., 1971, in pigs; Dauncey, 1980, in man). An increase in energy intake also affects the metabolism of thyroid hormones (Ingram & Kaciuba-Uscilko, 1977, in pigs) and thermoregulatory behaviour (Weiss, 1957, in mice; Baldwin & Ingram, 1968, in pigs). Some of the changes in physiological parameters which occur after acclimatization may therefore be related to the concomitant increase in energy intake rather than to environmental temperature per se.
The growing pig provides a useful subject in which to study problems on the interaction between temperature and nutrition because the animal’s ad /ihitum food intake is large even at high ambient temperatures, and therefore two markedly different intakes can be eaten in both a hot and a cold environment. In the present investigation body temperatures and metabolic rates have been measured at a series of test ambient temperatures, in piglets living from shortly after birth in an environment which was either hot or cold and on either a high or a low energy intake. The objectives of the study were two-fold. First, to determine what changes in body temperatures and metabolic rate occur after prolonged exposure to different combinations of environmental temperature and energy intake. Second, to determine if environ-, mental temperature exerts an effect which is independent of that due to energy intake. MATERIALS AND METHODS
Thirty-six piglets from eight litters of the Large breed kept at the Institute farm were used. Acclimatimtior~ All animals
* On leave from UNESP
aud eneryy
White
intuke
were removed from the sow at 12-14 days of age and housed in individual pens. Half the animals in
Brazil. 549
M. MACARI et al.
550
each htter were placed in a room where the temperature was reduced from 28 to 10°C over a 14 day period; the rest were kept in a room where the temperature was increased from 28 to 35°C over the same period. The animals in each room were divided into one set which received a high (H) energy intake of standard feed and another which received a low intake (L), in a single meal once per day. The actual amount of food given was increased as the animals grew, but the ratio of H to L was always 2: 1 and by the age of 6 weeks it was fixed at 600 or 300 g. All piglets were weighed daily. E\-perimental
ofoxygen
this way the significance of the separate contributions of individual factors to the total variance could be tested. In particular, attention was paid to the effects of: (1) the temperature at which the animals had been living, (2) the level of energy intake and (3) the interaction between temperature and energy Intake. A significant interaction could for example mean that the effect of energy intake was different at 35 compared with 10°C.
RESULTS The body weights of the animals at the time that the measurements were made are given in Table 1. As
expected, the heaviest piglets were the 35H group and the lightest the 1OL. The absence of any demand for thermoregulatory heat production at 35°C combined with a low intake, on the one hand and the high thermoregulatory demand combined with a high energy intake at lO”C, on the other, resulted in intermediate weights for the 35L and 10H groups. Body
consumption
Rates of oxygen consumption were determined in an open circuit respiration chamber using a paramagnetic analyser (Type OA 184, Taylor Servomex Ltd). The chamber was of a similar size and construction to the animal’s own living pen and was housed in a temperature controlled room. A closed circuit television system enabled an observer to monitor the animal and only those values of oxygen consumption which corresponded to a period when it was inactive were used. Each session lasted 1.5 hr and was started 24 hr after the last meal, which had usually been eaten within 2 hr. Values for oxygen consumption were corrected to STP and expressed as ml Oz/kgo.75 per min. The 0.75 exponent was used to correct for differences in body weight and was of particular importance since the animals on different treatments grew at different rates. Measurement
analysis
The results were subjected to the analysis of variance. In
procedure
When the animals were seven weeks of age each was placed in the respiration chamber at its normal living temperature for 1.5 hr every day, to accustom it to the procedure. At eight weeks of age the rate of oxygen consumption was measured at the animal’s normal living temperature and in the subsequent week at a series of other environmental temperatures of 10, 20 and 27°C. In preliminary studies, it had been found that piglets which had been living in the cold developed hyperthermia at 35”C, particularly if they had been on a high energy intake and therefore determinations were not made at 35°C for piglets which had been living in the cold. Rate
Statistical
of body temperatures
Rectal temperature was measured at the end of 1.5 hr in the respiration chamber, by inserting a probe 50 mm deep into the rectum. Skin temperatures were measured at the same time by attaching probes to the skin with surgical tape. The temperature of the skin was recorded on the tip of the ear, over the carpels and on the back to one side of
the mid line between the scapulae.
Table
temperatures
Rectal
(Fig. la). A separate analysis temperatures was made for each of the test temperatures and it was found that in each case the effect of the living temperature was significant, with those from 35°C having the higher deep body temperature (P < 0.001). In addition, there was also a significant effect of energy intake, with those on the H intake having the higher deep body temperature (P < 0.001 at 27 and 20°C; P < 0.05 at 10°C). The interactions for each analysis of variance were also significant (P < 0.01) suggesting that the effect of energy intake on the deep body temperature was more striking for those living in the cold than in the hot. Skin temperatures on the back (Fig. lb). There were no significant differences in the temperatures recorded on the backs of the animals on different treatments, Skin temperutures on the extremities (Figs lc und Id). The temperatures recorded on the pina of the ear and over the carpels were significantly higher in those animals which had been living at 10 than at 35°C at each of the test temperatures (P < 0.01). By contrast, the level of energy intake had little effect, although there was a tendency for the temperatures on the leg
1. Body weights of piglets living at 10 or 35°C on a high (H) or low (L) energy intake
Treatment
Body
weight (kg)
SEM Number animals
Group
10H
1OL
35H
35L
14.0
7.4
16.9
10.7
0.21
0.12
0.81
0.42
9
8
8
9
of
Values were recorded on the day that oxygen body temperatures were first determined.
consumption
and
Acclimatization
551
Fig. 1. Mean values of deep body and peripheral temperature, measured at various test ambient temperatures, in piglets which had been living at 10 or 35°C on a high (H) or low (L) energy intake: 0 lOH, ??lOL, A 35H, A 35L.
to be greater on the H than on the L intake lowest test temperature (Fig. id, P < 0.05).
at the
Resting metabolic rute The rates of oxygen consumption obtained at each of the test temperatures are given in Table 2a. The results for each environmental temperature at which the animals were tested were analysed separately to test the hypothesis that the rate of oxygen consumption at any given temperature depended partly on the animal’s energy intake and partly on the temperature at which the animal normally lived. Table 2b presents the values from the analysis of variance which are related to the separate effects of living temperature and energy intake. In this table, for example, the value for the H intake was been averaged over temperature, i.e. the mean of IOH and 35H; similarly the values of, e.g. 1OC have been averaged over energy intake, i.e. IOH and 1OL. For all the treatment groups, 27’C represented a thermally neutral environment at which there was neither shivering nor hyperthermia. At this temperature the analysis revealed that the differences in metabolic rate related to energy intake were statistically significant (P < 0.001) whereas those related to the temperature at which the animals had been living were not (Table 2b). Moreover the interaction term between the effects due to the living temperature and to energy intake was also significant (P < 0.001). This indicated that the difference in oxygen consumption related to energy intake was greater for the animals which had been living in the cold environment than for those which had been living in the hot. Analysis of the values for oxygen consumption determined at 20 and 10°C also showed a statistically significant effect related to energy intake (P < 0.001) but not to the animal’s normal living temperature. At these environmental temperatures the interaction term was not statistically significant, suggesting that the effect of energy intake on oxygen consumption
was similar for animals and 35°C.
which had been living at 10
DISCUSSION
The present results show that 24 hr after presentation of the last meal, which was usually eaten within 2 hr, piglets which had been living at 10°C had lower rectal temperatures than those which had been living at 35°C. A low rectal temperature has been reported in people living in the cold, and groups such as the Australian aborigines and the Kalahari bushmen who have been exposed to cold for long periods tolerate this fall in deep body temperature without shivering (Wyndham & Morrison, 1958. Hammel et al., 1959). A decline in core temperature in the cold could be regarded as advantageous since less energy would be required to regulate the body at a lower temperature. The level of energy intake was also found to influence rectal temperature, particularly in those which had been living at 10°C with those on the H intake having the higher core temperature. If those living at 10°C had been allowed to eat cld lib. they would have taken more food than the amount provided as the H intake and would then have been subjected to two opposing influences on their core temperatures The particular body temperature achieved by an animal will thus depend on the balance between the relative influences of ambient temperature and energy intake. For example, Hamilton & Brobeck (1964) reported that rats which had been exposed to the cold for 3 weeks and allowed to eat ud lib. had higher deep body temperatures than did controls. The higher rectal temperature associated with an ambient temperature of 35°C does not appear to confer any obvious advantage on the animal. It is true that a high core temperature increases the gradient over which heat can be lost, but the Arrhenius-Vant Hoff effect increases metabolic rate and thus increases the heat load. However, it is clear that the animals in
552
M. MACARI et ul. Table Za. Resting temperatures
oxygen consumption (ml 02/kgo~” per min) measured at various environmental for piglets normally living at 10 or 35’C on a high (H) or a low (L) energy intake (mean values k SEM) Temperature
Treatment
Group
n
at
measurements
8
15.5
+ 1.22
10.4
35L
9
12.4
i
1.15
10H
9
17.8
f
1OL
8
11.0
t
made
(OC) 35
27
0.69
8.2
? 0.53
9.2
? 0.79
8.1
i 0.65
6.5
? 0.50
6.5
? 0.40
1.15
11.5
t 0.65
11.2
? 0.50
1.31
7.0
0.83
5.3
? 0.64
Table 2b. Mean values for oxygen consumption normal living temperature and energy intake
i
i
(ml OJkg”.‘”
Temperature
factor
per min) related
at
which
to the separate
measurements
effects of
were
made
(OC)
27
20
10
Living temperature energy intake) .:, qver
were
20
10
35H
Environmental
which
(averaged
:
Energy intake* (averaged over living temperature):
35Oc
13.9
? 0.84
9.3
? 0.48
7.4
+ 0.37
10°C
14.4
f 0.87
9.2
? 0.53
8.2
f
High
16.6
? 0.84
10.9
i
0.48
9.7
+ 0.37
Low
11.7
t
5 0.53
5.9
+ 0.41
0.87
Values taken from the analysis of variance (means f SEM). * Differences related to energy intake were all statistically significant, lo hving temperature were not
the present study had very different tolerances of heat, since those living at 10°C could not be tested at 35°C without risk of severe hyperthermia. This difference in tolerance was probably related to some physiological property or properties acquired by the animals living at 35”C, rather than to the effects of living at IO”C, * since differences in tolerance have been demonstrated previously between piglets living at thermal neutrality (26°C) or in a hot environment (35°C) (Ingram, 1977). By contrast with rectal temperature, the skin temperatures on the extremities were higher as a result of living in the cold than in the hot, whereas the level of energy intake had virtually no effect. A similar situation has again been described in adult man. Studies on the GaspC fishermen have shown that these people, who habitually have to immerse their hands in cold water while working, have a higher blood flow in their hands and tolerate the cold conditions better than do controls (LeBlanc et al., 1960). As a consequence of this higher blood flow and hence much greater rate of heat loss, the Gasp& fishermen have an exaggerated response to cooling of the whole body and shiver more than do controls under such conditions. Similarly, peripheral temperatures and hence blood flow have been found to be higher in Eskimo people than in Europeans (Brown et CL/.,1954). This protection against tissue cooling which is given by the high blood flow is possible only by the use of more energy for heat production, but in spite of this extra requirement there was very little evidence of a reduc-
7.6
P < 0.001, whereas
0.41
those related
tion in extremity temperatures when energy intake was low in those living in the cold in the present study. Consideration of the rates of oxygen consumption in Table 2a suggests that, at any given environmental temperature, metabolic rate is influenced more by energy intake than by the environmental temperature at which the animal normally lives. For example at a test temperature of 10°C there is a large difference in the rate of oxygen consumption between H and L intakes for animals which had been living either in the hot or in the cold. By contrast there is very little difference between 35H and 10H or between 35L and 1OL. Statistical tests aimed at separating the independent effects of energy intake and living temperature revealed that at each of the test temperatures at which the metabolic rate was estimated there was an effect related to energy intake but not to the temperature at which the animals had been living. The results thus indicate that the metabolic response to a given environmental temperature is not influenced by prolonged exposure to heat or cold alone. Under conditions where animals can eat ud lib., differences in metabolic rate which are apparently related to environmental temperature will develop, because in the cold more food will be eaten. The metabolic rate at 27°C is of particular significance because it was thermally neutral for all the animals. At this temperature there was no shivering and no hyperthermia and the rate of oxygen consumption
Acclimatization
therefore provided an estimate of the basal metabolic rate. At this test temperature there was a difference related to the independent effect of energy intake but not to that of living temperature. The analysis, however, revealed that there was a significant interaction between energy intake and living temperature which indicated that the effect of energy intake on metabolic rate was significantly greater in animals normally living in a cold environment than in the hot. The basal metabolic rate at thermal neutrality is therefore influenced indirectly by the temperature at which the animal normally lives because it modifies the effect of energy intake. It is therefore concluded that after acclimatization body temperatures are directly influenced by both living temperature and energy intake. By contrast, the changes in the metabolic response to environmental temperature which occur after prolonged exposure to hot or cold temperatures depend predominantly on the induced changes in energy intake. Thus the overall effects of acclimatization can be assessed only when energy intake is taken into account. Acknu~~(edyrme,lt-The authors ARC Statistics Group, Cambridge sis.
thank Mr D. E. Walters, for the statistical analy-
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