ACTA THERIOLOGICA Vol. 22, 9: 159—180, 1977

Changes in Thermogenesis and its Hormonal Regulators during the Postnatal Development of Rabbits and Guinea Pigs

Alina Barbara PIEKARZEWSKA P i e k a r z e w s k a A. B„ 1977: C h a n g e s in t h e r m o g e n e s i s a n d its h o r m o n a l r e g u l a t o r s d u r i n g t h e p o s t n a t a l d e v e l o p m e n t of r a b b i t s a n d g u i n e a pigs. Acta theriol., 22, 9: 159—180 [With 5 Tables, 2 Figs & P l a t e s VI— IX]. T h e s t u d i e s c a r r i e d out on 48 r a b b i t s and 87 g u i n e a pigs, d u r i n g f i r s t w e e k s of t h e i r p o s t e m b r y o n i c life, w e r e a i m e d to f i n d t h e c a u s e s of t h e c o n s i d e r a b l e d i f f e r e n c e s in t h e c a p a c i t y of t h e n e w b o r n s of t h e s e t w o species to m a i n t a i n t h e r m a l homeostasis. T h e p o o r e r capacity of n e w b o r n r a b b i t s to m a i n t a i n t h e r m a l h o m e o s t a s i s is p a r t l y due to t h e lack of t h e r m a l insulation in t h e f o r m of f u r . N e w b o r n r a b b i t s a r e also c h a r a c t e r i z e d by lower h e a t p r o d u c t i o n , w h i c h d u r i n g t h e f i r s t w e e k of life is 127.5 k c a l / k g 24 h or 65.5 kcal/kgO-75 24 h. w h e r e a s in t h e case of g u i n e a pigs t h e s e v a l u e s a r e 137.6 k c a l / k g 24 h or 73.3 kcal/kg 0 75 . H e a t p r o d u c t i o n r a t e d u r i n g t h e initial period of y o u n g r a b b i t s ' life i n c r e a s e s q u i t e r a p i d l y a n d in i n d i v i d u a l s 14-day-old is on an a v e r a g e 128.2 kcal/kg 0 -"^, t h a t is, a b o u t t w i c e as m u c h as in t h e n e w b o r n r a b b i t s a n d t h e a d u l t i n d i v i d u a l s of this species. In g u i n e a pigs the c h a n g e s in h e a t p r o d u c t i o n r a t e d u r i n g p o s t e m b r y o n i c d e v e l o p m e n t a r e f a r s m a l l e r . In both species o n t o g e n i c c h a n g e s in h e a t p r o d u c t i o n r a t e t a k e place p a r a l l e l to c h a n g e s in t h y r o i d activity. T h e d i f f e r e n c e s f o u n d in m o r p h o l o g i c a l m a t u r i t y a n d r e l a t i v e w e i g h t of t h e a d r e n a l g l a n d s of these a n i m a l s p e r m i t to a s s u m e t h a t t h e a d r e n e r g i c s y s t e m p l a y s a m o r e i m p o r t a n t r o l e in h e a t p r o d u c t i o n in t h e n e w b o r n g u i n e a pigs t h a n in t h e n e w b o r n r a b b i t s . [Inst. A n i m . Physiol. Nutr., Polish Acad. Sci., 05-110 J a b ł o n n a n e a r Warsaw], I. I N T R O D U C T I O N

Newborn mammals or newly-hatched birds usually possess a far weaker capacity for maintaining a constant body temperature than adult individuals of the same species. Physiology textbooks give the immaturity of thermoregulation mechanisms in newborn animals as the cause of this deficiency. Such immaturity, from the theoretical point of view, can be fully understandable, particularly in mammals, since throughout embryonic life the animals remain under thermostatic conditions ensured by the mother's organism, and do not, therefore, need their own thermoregulation mechanism. The moment of a mammal's birth, however, constitutes an abrupt change in environment f r o m warm and wet to far colder and dryer. Rapid heat losses through radiation and convection 1159]

160

A. B. Piekarzewska

begin immediately, and during the first hours after birth also, through intensive evaporation of water from the moist body surface. Such losses usually lead to a quick drop in the body temperature of the newborn animals, this having been described in detail in piglets (N e w 1 a n d et al., 1952) and young rabbits (P o c z o p k o, 1969). The various species differ, however, from each other very considerably in respect of their capacity for maintaining thermal homeostasis during the first few days after birth. For instance newborn calves (O b r ac e v i c, 1954; R o y et al., 1971) or lambs ( A l e x a n d e r & B r o o k . 1960; S i m m s, 1971) are capable of maintaining thermal homeostasis in only a slightly narrower range of variations in ambient temperature than adult cows and sheep, whereas newborn mice ( C a s s i n & O t i s , 1960; L a g e r s p e t z , 1962) or the rat (G u 1 i c k, 1937; B u c h a n a n & H i l l , 1947; P o c z o p k o , 1961) differ only slightly from poikilothermic animals. When comparing the capacity for maintaining thermal homeostasis in newborn rats and calves it is, however, difficult to understand clearly the causes of these differences, since they may to a considerable extent be due to t h e less favourable body surface to body mass ratio in the rat, and not only to the immaturity of thermoregulation mechanisms. H u l l (1973) considers that even very limited capacity for maintaining a constant body temperature by newborn rabbits should be explained by the unfavourable body surface to body mass ratio and insufficient insulation, and not the immaturity of heat production mechanisms. The purpose of the present studies was to trace the maturing process of the thermogenesis mechanism. They were carried out on animals with very similar relative body surface, but which even so differed considerably in their capacity for maintaining thermal homeostasis, i.e. rabbits and guinea pigs. Attention was paid to whether the animals chosen for the experiments differ in early stages of development in respect of rate of heat production in a way which would explain differences in capacity fcr thermoregulation. Examination was also made of thyroid gland activity and the weight and structure of the adrenal glands, since the hormones of these glands play an important part in regulation of thermogenesis and stimulation of heat production under the effect of cold. II. MATERIAL AND M E T H O D S 2.1. Experimental Animals The s t u d i e s w e r e c a r r i e d out on 48 r a b b i t s and 87 guinea pigs varying in age f r o m several hours to about 4 weeks a f t e r brith, a n d also for purposes of comparison on adult individuals. Both rabbits and guinea pigs w e r e unidentified

Postnatal development of rabbits and guinea pigs

161

h y b r i d s which were bred in the animal sheds of the I n s t i t u t e . The young a n i m a l s r e m a i n e d with their m o t h e r s for 4 weeks a f t e r birth, except for the short i n t e r v a l s needed for m e a s u r e m e n t s . 2.2. Heat Production H e a t production was evaluated on the basis of results of d e t e r m i n a t i o n s of 0 2 and C 0 2 exchange m a d e by m e a n s of a d i a f e r o m e t e r (Kipp and Zonen, Delft, Holland). D u r i n g m e a s u r e m e n t s the animals w e r e kept u n d e r resting metabolism conditions, t h a t is, in a state of complete physical rest and at t h e r m o n e u t r a l i t y b u t w e r e not fasted before measuring. Choice of n e u t r a l a m b i e n t t e m p e r a t u r e for young r a b b i t s of d i f f e r e n t age was m a d e on the basis of the s t u d y by H u l l (1965) and P o c z o p k o (1969) and for guinea pigs on t h e s t u d y by B r ü c k & W ü n n e n b e r g (1965a). The accepted t e m p e r a t u r e s w e r e as follows: Age, days Rabbits Guinea pigs

0—7 35°C 32—34°C

8—14 30—31°C 30—31°C

over 14

adult

27—29°C 25—28°C

24—26°C 24—25°C

The a n i m a l s w e r e taken out f r o m their m o t h e r s and placed in a respiration c h a m b e r . A f t e r equilibrium had been established (20—30 m i n u t e s ) m e a s u r e m e n t s of O, i n t a k e a n d C 0 2 emission w e r e begun, which lasted about 40 minutes. The t h e r m o m e t e r (Ellab, Copenhagen, D e n m a r k ) m a d e it possible f r e q u e n t t e m p e r a t u r e r e a d i n g inside the respiration c h a m b e r . H e a t production was calculated f r o m the a m o u n t of oxygen consumed on the basis of t h e c u r r e n t l y d e t e r m i n e d respiration q u o t i e n t . The time b e t w e e n determination of t h e metabolic r a t e in the same i n d i viduals was not less than one day. 2.3. Development of Thyroid and its Activity R a d i o a c t i v e iodine u p t a k e was determined according to t h e method described by B a r r i n g t o n (1963). Before beginning the test the a n i m a l s w e r e weighed, then a p p r o x i m a t e l y 1 n Ci Na 131 J produced by t h e Nuclear R e s e a r c h I n s t i t u t e at Ś w i e r k was injected subcutaneously and t h e animals placed in cages (without t h e mother), ensuring n e u t r a l t h e r m a l conditions. A f t e r 3 h o u r s t h e animals w e r e killed w i t h excess of ether, the thyroid dissected and i m m e d i a t e l y weighed on a torsion balance. The radioactivity of 1 3 1 J dose given and radioactivity of t h e t h y r o i d w e r e measured in plastic test tubes in a w e l l - t y p e scintilation counter (type LL 2 — BUTJ, Poland). U p t a k e of l 3 1 J by t h e whole gland was e x p r e s s e d in percentages of the dose a d m i n i s t e r e d and a f t e r recalculation of the v a l u e p e r 1 m g of tissue. I m m e d i a t e l y a f t e r m e a s u r i n g radioactivity the thyroids w e r e fixed in Bouin f i x a t i v e , then embedded in p a r a f f i n , sectioned to 7 u and stained w i t h h e m a t o x y l i n and eosine a n d by the PAS method. 2.4. Changes in Weight and Histological Picture of the Adrenals The a d r e n a l s dissected from animal killed w h e n investigating thyroid activity w e r e weighed on a torsion balance, f i x e d in Bouin f i x a t i v e , t h e n embedded in p a r a f f i n , sectioned to 7 li and stained with h e m a t o x y l i n a n d eosine. During histological e x a m i n a t i o n p a r t i c u l a r attention w a s paid to the blood s u p p l y to the gland a n d degree of f o r m a t i o n of the m e d u l l a r part.

162

A. B. Piekarzewska

III. RESULTS

3.1. Changes in Resting Metabolic Rate

Comparison was made of the resting metabolic rate of animals of different age. This rate is expressed in two ways, namely as daily heat production per 1 kilogram of body weight and per metabolic unit of body weight (kg0-75). Resting metabolic rate expressed per kilogram of body weight (Table 1) in newborn rabbits was about 127 kcal, and about 138 kcal/24 h in guinea pigs. In young rabbits significant reduction was observed in this rate on the second day, and later a gradual increase up to a maximum oin the 14th day after birth. A certain increase in resting metabolic rate was also found in guinea pigs but the maximum was reached earlier, that is, as early as the 5th day after birth. On reaching the maximum metabolism rate in both species fell to the values characteristic of adult individuals. Maximum value of metabolic rate in rabbits was aboutt 156, and in guinea pigs 116°/o of the rate observed on the first day after birth. Changes in resting metabolic rate expressed per kg0-75 take a slightly different form to the rate calculated per kilogram of body weight. The results given in table 1 show that metabolic rate on the first day after birth, which is approximately 65 kcal/kg0-75 2 4 h in rabbits and approx. 73 kcal/kg 0 - 75 2 4 h in guinea pigs, did not differ from the metabolic rate found in adult individuals of these species. During ontogenic development there were, however, fairly considerable changes. In young rabbits, after the initial decrease leading on the second day after birth to a value of about 46 kcal/kg 0 - 75 2 4 h, there was a fairly rapid increase, so that at the age of 14 days rate was about 128 kcal/kg0-75 2 4 h. This high metabolic rate was maintained for about the 8th week of life, after which it gradually decreased to become equal at the age of 2.5 months in the case of rabbits with the level characteristic of adult individuals. The metabolic rate of guinea pigs also rose constantly during the initial period of postnatal development and reached a maximum of about 92 kcal/kg0-75 24 h at the age of 17 days. This increase was not as great as in the case of rabbits, but is highly significant statistically (P ' -