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Photoperiodicity and the thermoregulatory response to noradrenaline in the pigeon
.I. Thermal Bi.h,~l~ Vol, 4, pp. 167 to 171 ,( Pergamon Prcs~. Lid 197tL Printed in Grcal Britain
0306-4565 79 (11(14 0167502.(X) 0
PHOTOPERIODICITY A N D THE THERMOREGULATORY RESPONSE TO NORADRENALINE IN THE PIGEON A. HAIM,* S. SAARELA a n d R. HISSA Department of Zoology, Zoophysiological Laboratory, University of Ouhl, 90100 Oulu 10, Finland
(Received 23 October 1978; accepted in revised form 7 December 1978) Abstract--1. Pigeons acclimated to darkness (241), T, = 22°C) or long scotophase (4L:20D, T, = 22'~C) responded to noradrenaline at 7", = 6°C as if cold-acclimated. Shivering was inhibited, and 15"o2consumption and body temperature were decreased significantly (P <0.001 <0.02). 2. The response of pigeons acclimated to light (24L, To = 22°C) was high but not significantly different from the control group (12L: 12D, To = 22°C). 3, In pigeons acclimated to 4L:20D (To ---- 32°C) shivering was not completely inhibited, even for a short period. 4. A linear relationship was found between decreasing 12o2 and Tb as a response to noradrenaline, which appeared to effect heat production rather than heat dissipation.
Group 1--12L:I2D at Ta --- 22'C---control. Group 2--24D at To = 22C--simulating winter photoperiod, but not temperature, north of the arctic circle. Group 3--4L:20D at T, = 22'C--simulating winter photoperiod, but not temperature, in Oulu, Finland (lights were on between 1000 h and 1400 h). Group 4--24L at T, = 22 C--simulating summer photoperiod, but not temperature, north of the arctic circle. Group 5--4L:20D at T, = 32 C, warm-acclimated (WA) group (lights were on between 1000 h and 1400 h). Group 6 ~ 2 4 L at T, = 6 C, cold-acclimated (CA) group.
INTRODUCTION COLD-ACCLIMATED pigeons, Columba liria, (ambient temperature To = 2°C) and warm-acclimated (T, = 32°C) pigeons, showed significant hypothermia following a peripheral injection of N A at To = 6°C, when c o m p a r e d to the control group, acclimated at To = 22°C (Hissa et al., 1975a). All pigeons in these experiments were kept under a photoperiod of 12 h light (12L) and 12 h dark (12D). The role of the pineal gland, and its m a i n metabolic product melatonin, in t h e r m o r e g u l a t i o n of chickens was emphasized by C o g b u r n et al. (1976}. They assumed that changes of induced illumination could be a m a j o r factor in physiological adjustments to change in ambient temperature. The pigeons, being diurnal birds in n o r t h e r n European cities, d o not migrate in winter, in spite of the extreme cold and short daylength. Therefore the influence of different photoperiods o n the response to NA was investigated, in order to determine whether a short daylength had the same effect o n the pigeon as cold acclimation, and a long daylength had the same effect as a high ambient temperature. An attempt was also m a d e to determine whether temperature or p h o t o p e r i o d had the stronger influence on the response to NA. MATERIALS AND METHODS Thirty-eight pigeons of both sexes, captured in Helsinki in August 1977, and weighing 290--370g were used in the experiments. Prior to the experiments they were individually caged with a photoperiod of 12L: 12D at T, = 22"C, and were supplied with food and water ad lib. After two to four weeks the pigeons were divided into groups, each consisting of six individuals (except in the control group which was eight), and exposed to the following experimental conditions for at least twenty days.
The methods used in our experiments have been described in detail by Saarela & Hissa (1977). Oxygen consumption (~2) was measured in an open system (airflow rate of 1.5 litre/hour) using a paramagnetic 02 analyzer (Beckman E2), and recorded at T~ = 26'C and T, = 6'C. Recording was started after 2 h of equilibrium at each temperature. Simultaneously bare wingpit body temperature (T,), and bare foot temperature (TIt were measured with thermocouples, and recorded (Ellab Z94-B). Pectoral muscle shivering at To = 6 C was recorded with electrodes connected to a Varioscript V822 physiopolygraph (Schwartzerk and the total frequency content was measured using a FA-790 Frequency Integrator (Schwartzer). All experiments started at 0830 h. L-arterenol bitartrate (Sigma) was injected i.m. (2 mg/kg as a base) at T, = 6~C after stabilization of ~ r Th, TI and shivering. in order to minimize disturbance to the birds, an injection needle was inserted into the breast muscle, and :connected to a disposable syringe of 1 ml outside the metabolic chamber by a polyethylene tube. ¢o2, Tb, TI and shivering were recorded for a minimum of one hour following NA administration. Student's t-test was used to test for significant differences in the responses to different treatments. RESU LTS Oxygen c o n s u m p t i o n at To = 6°C was significantly' elevated (P < 0.05) in birds from group 3 (4L:20D
* Present address--University of Haifa, Oranim, P.O. Kiryat Tivon, Israel. 167
168
A. HAIM, S. SAARELAand R. HISSA Table 1. Mean (+ S.E.) oxygen consumption (6~)~) body temperature (Th) and foot temperature (Ty) measured in pigeons from all experimental groups at ambient temperature T~ = 6'C Test groups
I/o~ + S.E. ml/100g min
(n)
Control 24D 4L:20D 24L 4L:20D WA 24L CA
8 6 6 6 6 4
2.57 2.52 3.05 2.64 3.03 2.95
Tb + S.E. '~C
_ 0.168 + 0.109 + 0.134" + 0.134 + 0.158 +_ 0.135
40.2 39.5 40.3 39.3 40.6 39.9
7"/+ S.E. ~C
_+ 0.18 + 0.51 + 0.37 + 0.64 + 0.25 + 0.36
28.2 26.3 27.5 26.9 31.2 33.0
+ + + _ + +
1.79 1.47 2.61 2.47 1.62 0.97*
* Significantly different (P < 0.05) from the control group.
acclimated at To = 22°C) compared to pigeons from the control group. A non-significant elevation in oxygen consumption was also observed in pigeons from groups 5 and 6 (Table 1). Body temperature at To = 6°C did not differ significantly in any of the studied groups. Foot temperature was significantly higher (P < 0.05) at T= = 2°C in birds acclimated at 24L (Table 1), compared to the control group. In all experimental groups, except the WA group (4L:20D at T= = 32°C), shivering at T= = 6°C was inhibited for a certain period due to the injection of NA. (Fig. 1). Pigeons acclimated to 24D and 4L:20D at To = 22°C showed a strong response to NA at
Ta = 6°C. Shivering in these birds was inhibited (Fig. 1), this was accompanied by a significant fall in oxygen consumption (P < 0.001), body temperature (P < 0.001 and P < 0.02) and a decrease in foot temperature (Fig. 2). An elevation in foot temperature was however observed, immediately after the NA injection, (first phase, Fig. 2), while with the decrease in I)o~ and Tb a decrease in foot temperature was observed in all groups (second phase, Fig. 2). The mean maximum decrease in oxygen consumption and body temperature in pigeons acclimated to 24L at To = 22°C, although high compared to the control group, did not differ significantly from it (Fig. 2).
group
'I 'I 'I 'I 'I ,]
2
n
1
12:12
LD
control 7
2
0:24
LO
5
3
4:20
LD
6
LD
6
LD
.320C 5
LO
-2 °C
0
a o i ¢
g u
2
0
2
0
4
2
24:0
0
5
2
4:20
0
6
2
24:0
4
0 !
!
1
i
0
2O
40
i
60
rain
Fig. 1. Effect of noradrenaline (2 mg/kg bw, i.m.) on shivering in pigeons from all experimental groups at ambient temperature To = 6°C. t = O--time of NA injection. Shaded areas represent shivering.
Photoperiodicity in the pigeon group
o!
5
1234
6
A9o21 -0.2' -0.4. !
i
-0.6. -0.8"
+8= "T+
~
+4
-
T
1
O 0
-
| ~ 1l ¢ 0
-4
-
group
1
23
7 6 6 5
,~
5 6 6 4
Fig. 2. Mean maximum (+ S.E.) decrease in oxygen consumption (Al?o2), body temperature (zlTb) and foot temperature (ATs) in pigeons at ambient temperature 6°C as a response to an injection of noradrenaline (2 mg/kg bw, i.m.). T~-rises.immediately(lst phaseJ and then follows the decrease of Vo2 and Tb, (2nd phase). *---significantlydifferent (P <0.05) from control group; **--significantly different (P < 0.02) from control group; ***---significantlydifferent P <0.001) from control group.
As mentioned above, in individuals from the WA group shivering was decreased as a response to NA but was not completely inhibited even for a short period (Fig. 1). Oxygen consumption and body temperature decreased slightly but less than in the control group (Fig. 2). In pigeons from the CA group oxygen consumption and body temperature showed a decrease similar to the control group (Fig. 2), although shivering occurred to a greater degree than in the control group and they recovered quicker (Fig. 1). The decrease in body temperature and oxygen consumption following a NA injection were found to be linearly correlated (Fig. 3) (y = 4.99 + 0.77, r = 0.998). T.B, 4 / 2 - - t
169 DISCUSSION
The results from this study showed that pigeons acclimated to long or complete darkness (4L:20D or 24D) at 7", = 22°C reacted to NA as if they were cold-acclimated. At To = 6°C, NA inhibited shivering in these birds and caused a significant (P < 0.001) decrease in oxygen consumption, accompanied by hypothermia (Figs 1 and 2). The hypothermic effect. of NA at To = 6°C is in agreement with the report on cold acclimated pigeons (Hissa et al. 1975a) and on pigeons treated with thyroxine (Saarela & Hissa 1977). Birds from the 24L group acclimated at T, = 22°C responded similarly to pigeons acclimated to To = 32°C 12L:12D (Hissa et al. 1975a). On the basis of these results, it may be assumed that changes in photoperiod have an effect similar to changes in ambient temperature. If acclimation to a long scotophase has the same effect as acclimation to low ambient temperature, it may be assumed that pigeons acclimated at 4L:20D at To = 32°C would have a very high response to NA, as they are acclimated to a "cold" and a "hot" environment. However, our results (Fig. 2) showed that a long scotophase abolishes the effect of acclimation to temperatures above the thermoneutral zone. Birds acclimated to 24L at T, = 2°C showed a stronger response than those of 4L:20D at To = 32°C (Fig. 2). This may be due to cold acclimation or to the fact that they were exposed to continuous light. However, the response to NA of these pigeons was smaller compared to group 4 (Fig. 2). The high levels of Vo, in these groups (5, 6) at T° = 6°C before the injection of NA, could be mediated through the thyroid gland (Saarela & Hissa 1977). Marley & Stephenson (1975) studied the thermoregulatory effects of NA infused into the hypothalamus of the chick. One of the effects induced by NA was hypothermia while leg temperature was increased immediately after the infusion. In their opinion NA had inhibitory and facilitatory effects on some mechanisms of heat production and heat dissipation. Earlier Allen & Marley (1967) suggested that peripherally injected monoamines in avian species may have a direct central effect at thermoregulatory centers. An increase in leg temperature after the NA injection was noted in pigeons from the different groups. The linear relationship between the fall of Tb and I?o2 as a response to NA injection, although the pigeons were accli: mated to different conditions (Fig. 3), may indicate that heat production mechanisms in birds from our experiments were vulnerable to NA, rather than mechanisms of heat dissipation. The role of the cardiovascular system and the importance of the bare legs in heat dissipation by birds was emphasized by Steen & Steen (1965) and Purves (1975). In their opinion the main avenue for heat dissipation at high ambient temperatures is the bare part of the legs. The high foot temperature at 7", = 6°C in both groups (5 and 6) that were oppositely treated with temperature and illumination (Table 1) resulted from a high heat dissipation. It may be assumed that the high rate of heat dissipation is caused either by an increase in heat production due to acclimation to low ambient temperature Ta = 2°C (group 6), or to + long scotophase (group 5), this having the same effect
170
A. HAIM.S. SAARFLAand R. HISSA 5
0 0
E t
~ 2
I
I
!
!
I
0.1
0.3
0.5
0.7
maximal
I
AVo~I mln~lllOOg.mln
Fig. 3. Relation between maximum decrease in oxygen consumption iAl?o:) and body temperature (ATb) due to an injection of noradrenaline (2 mg/kg bw, i.m.) to pigeons from all experimental groups at ambient temperature T, = CC.
as low ambient temperature, although the pigeons were exposed to Ta = 32°C. The existence of non-shivering thermogenesis (NST) in birds is a matter still under discussion. Dawson & Hudson (1970) stated that shivering was the main source for chemical heat production. On the basis of studies by Hart (1962) and West (1965), it may be concluded that shivering in an adult bird is not complemented by NST. On the other hand, Freeman (1970) found, on the basis of the calorigenic effect of thyroxine and triiodothyronine, that NST occurred in chickens. However, in our experiments, shivering in birds acclimated to 24L at To = 2°C was eliminated as a response to NA, but not to the same degree as in the control group (Fig. 1). Yet, in such :pigeons, oxygen consumption and body temperature were decreased to the same degree as in the control group (Fig. 2). These results suggest that another heat production mechanism, responsive to NA, is involved in thermoregulation of the pigeon, apart from the shivering. The role of the pineal gland and its main hormone melatonin in thermoregulation of mammals was discussed by Heldmaier & Hoffmann (1974), and Lynch & Epstein.(1976), and in body temperature and thermoregulation of birds by Binkley et al. (1971), Binkley (1974) and Cogburn et al. (1976). Recently John et al. (1978), showed that body temperature in pinealectomized pigeons at To = 25°C or 3°C was higher compared to the control group, during photophase and scotophase. In their study it was also shown that melatonin could reverse the hypothermic effect of pinealectomy. Axeirod & Wurtman (1964) found that
in chickens acclimated to continuous light, there was a high increase in melatonin production. The thyroid seems to be one of the endocrine glands that could be affected by melatonin, and this would have a direct effect on heat production in the pigeon (other endocrine glands are not ruled out). It is therefore possible that a significant increase in heat production at To = 6°C of individuals from the 4L:20D group acclimated at To = 22°C (Table 1) may be due to a decrease in melatonin synthesis. In the group of pigeons acclimated to 24L at To = 22°C there was no significant change in heat production at To = 6°C, compared to the control group. In spite of this result, it is difficult to draw any conclusions since in this group there was no light and dark cycle. It is tempting to speculate whether the pineal gland' is a mediator in increasing or decreasing heat production in the pigeon, in the long term, as it is stimulated by changes of dark/light cycles, which are constant and repetitive each year. Acknowledgements--We thank Professor A. Berman for his helpful discussion. We thank Dr P. R. Condy for his editing remarks. This research was supported by a scholarship from the Finnish Ministry of Education and the National Science Council of Finland. REFERENCES
ALLEND. J. & MARLEYE. (1967) Effect of sympathomimetic and allied amines on temperature and oxygen consumption in chickens. Br. J. Pharmac. Chemother. 31, 290-312.
Photoperiodicity in the pigeon AXELROD J. & WURTMAN R. J. (1964) Melatonin synthesis in the hen pineal gland and its control by light. Nature, Lorul. 201, 1134. BINKLEY S. A. (1974) Pineal and melatonin: circadian rhythms and body temperature of sparrows, in Chronobiology (Edited by SCHEVING, HALBERG and PAUL¥), pp. 582-585. lgaku-Shion, Tokyo. BINKLEY S., KLUTH E. & MENAKER M. {1971) Pineal function in sparrows: Circadian rhythms and body temperature. Science, New York 174, 311-314. COGBURN L. A., HARRISON P. C. & BROWN D. E. (1976) Scotophase-dependent thermoregulatory dysfunction in pinealectomized chickens. Proe, Soc. exp. Biol. Med. 153, 197-201. DAWSON W. R. & HUDSON J. W. (1970) Birds. In Comparatit'e physiolo.qy of thermorequlation, Vol. 1, (Edited by WmTTOW G. C.), pp. 223-310. Academic Press, New York. FREEMAN B. M. (1970) Thermoregulatory mechanisms of the neonate fowl. Comp. Biochera. Physiol. 33, 219-230. HARt J. S. (1962) Seasonal acclimatization in four species of small wild birds. Physiol. Zo~l. 35, 224-236. HI~LOMAtER G. & HOFFM^NN K. (1974} Melatonin stimu-lares growth of brown adipose tissue. Nature. Lond. 247, 224-225. ItlSSA R., PYiSRNIL~ A. & SAARELAS. 11975a) Effect of peripheral noradrenaline on the thermoregulation in temperature-acclimated pigeon. Comp. Biochem. Physiol. 51C, 243-247.
171
HISSA R., SAARELAS. • PYORNILA A. (1975h) Thermoregulatory effects of peripheral injections of monoamines in the pigeon. Comp. Biochem. Physiol. 51C, 235-241. JOHN T. M., 1TOH S. & GEORGE J. C. (1978) On the role of the pineal in thermoregulation in the pigeon. Hormone Res. 9, 41-56. LYNCH G. R. & EPSTEIN A. L. (19761 Melatonin induced changes in gonads, pelage and thermogenic characters in the white-footed mouse, Peromyscus leucopus. Comp. Biochem. Physiol. 53t2, 67-68. MARLE¥ E. & STEPHENSON J. D. (1975) Effect of noradrenaline infused into the chick hypothalamus on thermoregulation below thermoneutrality. J. Physiol. 245, 28~ 303. PURVES M. J. (1975) Cardiovascular control. In Avian physioloqy. Symposia (Edited by PEAKER M.), pp. 13-32. Academic Press, New York. SAARELA S. & HlSSA R. (1977) Thermoregulatory effects of peripheral catecholamines on the pigeon after treatment with thyroxine or thiouracil. Comp. Biochem. Physiol. 56C, 25--30. STEEN I. & STEEN J. B. (1965) The importance of the legs in the thermoregulation of birds. Aeta physiol, scand. 63, 285-291. WEST G. C. (1965) Shivering and heat production in wild birds. Physiol. Zoid. 38, I 11-120.
Key Word Index--Noradrenaline; photoperiod: acclimation: thermoregulation: shivering: oxygen-consumption.
0306-4565 79 (11(14 0167502.(X) 0
PHOTOPERIODICITY A N D THE THERMOREGULATORY RESPONSE TO NORADRENALINE IN THE PIGEON A. HAIM,* S. SAARELA a n d R. HISSA Department of Zoology, Zoophysiological Laboratory, University of Ouhl, 90100 Oulu 10, Finland
(Received 23 October 1978; accepted in revised form 7 December 1978) Abstract--1. Pigeons acclimated to darkness (241), T, = 22°C) or long scotophase (4L:20D, T, = 22'~C) responded to noradrenaline at 7", = 6°C as if cold-acclimated. Shivering was inhibited, and 15"o2consumption and body temperature were decreased significantly (P <0.001 <0.02). 2. The response of pigeons acclimated to light (24L, To = 22°C) was high but not significantly different from the control group (12L: 12D, To = 22°C). 3, In pigeons acclimated to 4L:20D (To ---- 32°C) shivering was not completely inhibited, even for a short period. 4. A linear relationship was found between decreasing 12o2 and Tb as a response to noradrenaline, which appeared to effect heat production rather than heat dissipation.
Group 1--12L:I2D at Ta --- 22'C---control. Group 2--24D at To = 22C--simulating winter photoperiod, but not temperature, north of the arctic circle. Group 3--4L:20D at T, = 22'C--simulating winter photoperiod, but not temperature, in Oulu, Finland (lights were on between 1000 h and 1400 h). Group 4--24L at T, = 22 C--simulating summer photoperiod, but not temperature, north of the arctic circle. Group 5--4L:20D at T, = 32 C, warm-acclimated (WA) group (lights were on between 1000 h and 1400 h). Group 6 ~ 2 4 L at T, = 6 C, cold-acclimated (CA) group.
INTRODUCTION COLD-ACCLIMATED pigeons, Columba liria, (ambient temperature To = 2°C) and warm-acclimated (T, = 32°C) pigeons, showed significant hypothermia following a peripheral injection of N A at To = 6°C, when c o m p a r e d to the control group, acclimated at To = 22°C (Hissa et al., 1975a). All pigeons in these experiments were kept under a photoperiod of 12 h light (12L) and 12 h dark (12D). The role of the pineal gland, and its m a i n metabolic product melatonin, in t h e r m o r e g u l a t i o n of chickens was emphasized by C o g b u r n et al. (1976}. They assumed that changes of induced illumination could be a m a j o r factor in physiological adjustments to change in ambient temperature. The pigeons, being diurnal birds in n o r t h e r n European cities, d o not migrate in winter, in spite of the extreme cold and short daylength. Therefore the influence of different photoperiods o n the response to NA was investigated, in order to determine whether a short daylength had the same effect o n the pigeon as cold acclimation, and a long daylength had the same effect as a high ambient temperature. An attempt was also m a d e to determine whether temperature or p h o t o p e r i o d had the stronger influence on the response to NA. MATERIALS AND METHODS Thirty-eight pigeons of both sexes, captured in Helsinki in August 1977, and weighing 290--370g were used in the experiments. Prior to the experiments they were individually caged with a photoperiod of 12L: 12D at T, = 22"C, and were supplied with food and water ad lib. After two to four weeks the pigeons were divided into groups, each consisting of six individuals (except in the control group which was eight), and exposed to the following experimental conditions for at least twenty days.
The methods used in our experiments have been described in detail by Saarela & Hissa (1977). Oxygen consumption (~2) was measured in an open system (airflow rate of 1.5 litre/hour) using a paramagnetic 02 analyzer (Beckman E2), and recorded at T~ = 26'C and T, = 6'C. Recording was started after 2 h of equilibrium at each temperature. Simultaneously bare wingpit body temperature (T,), and bare foot temperature (TIt were measured with thermocouples, and recorded (Ellab Z94-B). Pectoral muscle shivering at To = 6 C was recorded with electrodes connected to a Varioscript V822 physiopolygraph (Schwartzerk and the total frequency content was measured using a FA-790 Frequency Integrator (Schwartzer). All experiments started at 0830 h. L-arterenol bitartrate (Sigma) was injected i.m. (2 mg/kg as a base) at T, = 6~C after stabilization of ~ r Th, TI and shivering. in order to minimize disturbance to the birds, an injection needle was inserted into the breast muscle, and :connected to a disposable syringe of 1 ml outside the metabolic chamber by a polyethylene tube. ¢o2, Tb, TI and shivering were recorded for a minimum of one hour following NA administration. Student's t-test was used to test for significant differences in the responses to different treatments. RESU LTS Oxygen c o n s u m p t i o n at To = 6°C was significantly' elevated (P < 0.05) in birds from group 3 (4L:20D
* Present address--University of Haifa, Oranim, P.O. Kiryat Tivon, Israel. 167
168
A. HAIM, S. SAARELAand R. HISSA Table 1. Mean (+ S.E.) oxygen consumption (6~)~) body temperature (Th) and foot temperature (Ty) measured in pigeons from all experimental groups at ambient temperature T~ = 6'C Test groups
I/o~ + S.E. ml/100g min
(n)
Control 24D 4L:20D 24L 4L:20D WA 24L CA
8 6 6 6 6 4
2.57 2.52 3.05 2.64 3.03 2.95
Tb + S.E. '~C
_ 0.168 + 0.109 + 0.134" + 0.134 + 0.158 +_ 0.135
40.2 39.5 40.3 39.3 40.6 39.9
7"/+ S.E. ~C
_+ 0.18 + 0.51 + 0.37 + 0.64 + 0.25 + 0.36
28.2 26.3 27.5 26.9 31.2 33.0
+ + + _ + +
1.79 1.47 2.61 2.47 1.62 0.97*
* Significantly different (P < 0.05) from the control group.
acclimated at To = 22°C) compared to pigeons from the control group. A non-significant elevation in oxygen consumption was also observed in pigeons from groups 5 and 6 (Table 1). Body temperature at To = 6°C did not differ significantly in any of the studied groups. Foot temperature was significantly higher (P < 0.05) at T= = 2°C in birds acclimated at 24L (Table 1), compared to the control group. In all experimental groups, except the WA group (4L:20D at T= = 32°C), shivering at T= = 6°C was inhibited for a certain period due to the injection of NA. (Fig. 1). Pigeons acclimated to 24D and 4L:20D at To = 22°C showed a strong response to NA at
Ta = 6°C. Shivering in these birds was inhibited (Fig. 1), this was accompanied by a significant fall in oxygen consumption (P < 0.001), body temperature (P < 0.001 and P < 0.02) and a decrease in foot temperature (Fig. 2). An elevation in foot temperature was however observed, immediately after the NA injection, (first phase, Fig. 2), while with the decrease in I)o~ and Tb a decrease in foot temperature was observed in all groups (second phase, Fig. 2). The mean maximum decrease in oxygen consumption and body temperature in pigeons acclimated to 24L at To = 22°C, although high compared to the control group, did not differ significantly from it (Fig. 2).
group
'I 'I 'I 'I 'I ,]
2
n
1
12:12
LD
control 7
2
0:24
LO
5
3
4:20
LD
6
LD
6
LD
.320C 5
LO
-2 °C
0
a o i ¢
g u
2
0
2
0
4
2
24:0
0
5
2
4:20
0
6
2
24:0
4
0 !
!
1
i
0
2O
40
i
60
rain
Fig. 1. Effect of noradrenaline (2 mg/kg bw, i.m.) on shivering in pigeons from all experimental groups at ambient temperature To = 6°C. t = O--time of NA injection. Shaded areas represent shivering.
Photoperiodicity in the pigeon group
o!
5
1234
6
A9o21 -0.2' -0.4. !
i
-0.6. -0.8"
+8= "T+
~
+4
-
T
1
O 0
-
| ~ 1l ¢ 0
-4
-
group
1
23
7 6 6 5
,~
5 6 6 4
Fig. 2. Mean maximum (+ S.E.) decrease in oxygen consumption (Al?o2), body temperature (zlTb) and foot temperature (ATs) in pigeons at ambient temperature 6°C as a response to an injection of noradrenaline (2 mg/kg bw, i.m.). T~-rises.immediately(lst phaseJ and then follows the decrease of Vo2 and Tb, (2nd phase). *---significantlydifferent (P <0.05) from control group; **--significantly different (P < 0.02) from control group; ***---significantlydifferent P <0.001) from control group.
As mentioned above, in individuals from the WA group shivering was decreased as a response to NA but was not completely inhibited even for a short period (Fig. 1). Oxygen consumption and body temperature decreased slightly but less than in the control group (Fig. 2). In pigeons from the CA group oxygen consumption and body temperature showed a decrease similar to the control group (Fig. 2), although shivering occurred to a greater degree than in the control group and they recovered quicker (Fig. 1). The decrease in body temperature and oxygen consumption following a NA injection were found to be linearly correlated (Fig. 3) (y = 4.99 + 0.77, r = 0.998). T.B, 4 / 2 - - t
169 DISCUSSION
The results from this study showed that pigeons acclimated to long or complete darkness (4L:20D or 24D) at 7", = 22°C reacted to NA as if they were cold-acclimated. At To = 6°C, NA inhibited shivering in these birds and caused a significant (P < 0.001) decrease in oxygen consumption, accompanied by hypothermia (Figs 1 and 2). The hypothermic effect. of NA at To = 6°C is in agreement with the report on cold acclimated pigeons (Hissa et al. 1975a) and on pigeons treated with thyroxine (Saarela & Hissa 1977). Birds from the 24L group acclimated at T, = 22°C responded similarly to pigeons acclimated to To = 32°C 12L:12D (Hissa et al. 1975a). On the basis of these results, it may be assumed that changes in photoperiod have an effect similar to changes in ambient temperature. If acclimation to a long scotophase has the same effect as acclimation to low ambient temperature, it may be assumed that pigeons acclimated at 4L:20D at To = 32°C would have a very high response to NA, as they are acclimated to a "cold" and a "hot" environment. However, our results (Fig. 2) showed that a long scotophase abolishes the effect of acclimation to temperatures above the thermoneutral zone. Birds acclimated to 24L at T, = 2°C showed a stronger response than those of 4L:20D at To = 32°C (Fig. 2). This may be due to cold acclimation or to the fact that they were exposed to continuous light. However, the response to NA of these pigeons was smaller compared to group 4 (Fig. 2). The high levels of Vo, in these groups (5, 6) at T° = 6°C before the injection of NA, could be mediated through the thyroid gland (Saarela & Hissa 1977). Marley & Stephenson (1975) studied the thermoregulatory effects of NA infused into the hypothalamus of the chick. One of the effects induced by NA was hypothermia while leg temperature was increased immediately after the infusion. In their opinion NA had inhibitory and facilitatory effects on some mechanisms of heat production and heat dissipation. Earlier Allen & Marley (1967) suggested that peripherally injected monoamines in avian species may have a direct central effect at thermoregulatory centers. An increase in leg temperature after the NA injection was noted in pigeons from the different groups. The linear relationship between the fall of Tb and I?o2 as a response to NA injection, although the pigeons were accli: mated to different conditions (Fig. 3), may indicate that heat production mechanisms in birds from our experiments were vulnerable to NA, rather than mechanisms of heat dissipation. The role of the cardiovascular system and the importance of the bare legs in heat dissipation by birds was emphasized by Steen & Steen (1965) and Purves (1975). In their opinion the main avenue for heat dissipation at high ambient temperatures is the bare part of the legs. The high foot temperature at 7", = 6°C in both groups (5 and 6) that were oppositely treated with temperature and illumination (Table 1) resulted from a high heat dissipation. It may be assumed that the high rate of heat dissipation is caused either by an increase in heat production due to acclimation to low ambient temperature Ta = 2°C (group 6), or to + long scotophase (group 5), this having the same effect
170
A. HAIM.S. SAARFLAand R. HISSA 5
0 0
E t
~ 2
I
I
!
!
I
0.1
0.3
0.5
0.7
maximal
I
AVo~I mln~lllOOg.mln
Fig. 3. Relation between maximum decrease in oxygen consumption iAl?o:) and body temperature (ATb) due to an injection of noradrenaline (2 mg/kg bw, i.m.) to pigeons from all experimental groups at ambient temperature T, = CC.
as low ambient temperature, although the pigeons were exposed to Ta = 32°C. The existence of non-shivering thermogenesis (NST) in birds is a matter still under discussion. Dawson & Hudson (1970) stated that shivering was the main source for chemical heat production. On the basis of studies by Hart (1962) and West (1965), it may be concluded that shivering in an adult bird is not complemented by NST. On the other hand, Freeman (1970) found, on the basis of the calorigenic effect of thyroxine and triiodothyronine, that NST occurred in chickens. However, in our experiments, shivering in birds acclimated to 24L at To = 2°C was eliminated as a response to NA, but not to the same degree as in the control group (Fig. 1). Yet, in such :pigeons, oxygen consumption and body temperature were decreased to the same degree as in the control group (Fig. 2). These results suggest that another heat production mechanism, responsive to NA, is involved in thermoregulation of the pigeon, apart from the shivering. The role of the pineal gland and its main hormone melatonin in thermoregulation of mammals was discussed by Heldmaier & Hoffmann (1974), and Lynch & Epstein.(1976), and in body temperature and thermoregulation of birds by Binkley et al. (1971), Binkley (1974) and Cogburn et al. (1976). Recently John et al. (1978), showed that body temperature in pinealectomized pigeons at To = 25°C or 3°C was higher compared to the control group, during photophase and scotophase. In their study it was also shown that melatonin could reverse the hypothermic effect of pinealectomy. Axeirod & Wurtman (1964) found that
in chickens acclimated to continuous light, there was a high increase in melatonin production. The thyroid seems to be one of the endocrine glands that could be affected by melatonin, and this would have a direct effect on heat production in the pigeon (other endocrine glands are not ruled out). It is therefore possible that a significant increase in heat production at To = 6°C of individuals from the 4L:20D group acclimated at To = 22°C (Table 1) may be due to a decrease in melatonin synthesis. In the group of pigeons acclimated to 24L at To = 22°C there was no significant change in heat production at To = 6°C, compared to the control group. In spite of this result, it is difficult to draw any conclusions since in this group there was no light and dark cycle. It is tempting to speculate whether the pineal gland' is a mediator in increasing or decreasing heat production in the pigeon, in the long term, as it is stimulated by changes of dark/light cycles, which are constant and repetitive each year. Acknowledgements--We thank Professor A. Berman for his helpful discussion. We thank Dr P. R. Condy for his editing remarks. This research was supported by a scholarship from the Finnish Ministry of Education and the National Science Council of Finland. REFERENCES
ALLEND. J. & MARLEYE. (1967) Effect of sympathomimetic and allied amines on temperature and oxygen consumption in chickens. Br. J. Pharmac. Chemother. 31, 290-312.
Photoperiodicity in the pigeon AXELROD J. & WURTMAN R. J. (1964) Melatonin synthesis in the hen pineal gland and its control by light. Nature, Lorul. 201, 1134. BINKLEY S. A. (1974) Pineal and melatonin: circadian rhythms and body temperature of sparrows, in Chronobiology (Edited by SCHEVING, HALBERG and PAUL¥), pp. 582-585. lgaku-Shion, Tokyo. BINKLEY S., KLUTH E. & MENAKER M. {1971) Pineal function in sparrows: Circadian rhythms and body temperature. Science, New York 174, 311-314. COGBURN L. A., HARRISON P. C. & BROWN D. E. (1976) Scotophase-dependent thermoregulatory dysfunction in pinealectomized chickens. Proe, Soc. exp. Biol. Med. 153, 197-201. DAWSON W. R. & HUDSON J. W. (1970) Birds. In Comparatit'e physiolo.qy of thermorequlation, Vol. 1, (Edited by WmTTOW G. C.), pp. 223-310. Academic Press, New York. FREEMAN B. M. (1970) Thermoregulatory mechanisms of the neonate fowl. Comp. Biochera. Physiol. 33, 219-230. HARt J. S. (1962) Seasonal acclimatization in four species of small wild birds. Physiol. Zo~l. 35, 224-236. HI~LOMAtER G. & HOFFM^NN K. (1974} Melatonin stimu-lares growth of brown adipose tissue. Nature. Lond. 247, 224-225. ItlSSA R., PYiSRNIL~ A. & SAARELAS. 11975a) Effect of peripheral noradrenaline on the thermoregulation in temperature-acclimated pigeon. Comp. Biochem. Physiol. 51C, 243-247.
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HISSA R., SAARELAS. • PYORNILA A. (1975h) Thermoregulatory effects of peripheral injections of monoamines in the pigeon. Comp. Biochem. Physiol. 51C, 235-241. JOHN T. M., 1TOH S. & GEORGE J. C. (1978) On the role of the pineal in thermoregulation in the pigeon. Hormone Res. 9, 41-56. LYNCH G. R. & EPSTEIN A. L. (19761 Melatonin induced changes in gonads, pelage and thermogenic characters in the white-footed mouse, Peromyscus leucopus. Comp. Biochem. Physiol. 53t2, 67-68. MARLE¥ E. & STEPHENSON J. D. (1975) Effect of noradrenaline infused into the chick hypothalamus on thermoregulation below thermoneutrality. J. Physiol. 245, 28~ 303. PURVES M. J. (1975) Cardiovascular control. In Avian physioloqy. Symposia (Edited by PEAKER M.), pp. 13-32. Academic Press, New York. SAARELA S. & HlSSA R. (1977) Thermoregulatory effects of peripheral catecholamines on the pigeon after treatment with thyroxine or thiouracil. Comp. Biochem. Physiol. 56C, 25--30. STEEN I. & STEEN J. B. (1965) The importance of the legs in the thermoregulation of birds. Aeta physiol, scand. 63, 285-291. WEST G. C. (1965) Shivering and heat production in wild birds. Physiol. Zoid. 38, I 11-120.
Key Word Index--Noradrenaline; photoperiod: acclimation: thermoregulation: shivering: oxygen-consumption.