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The effects of rearing-temperature on body conformation and organ size in young pigs
Camp.Biochem.Physiol.Vol. 77B,No. I, pp. 63-72, 1984 Printedin Great Britain
03050491/84
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80 1984PergamonPressLtd
THE EFFECTS OF REARING-TEMPERATURE ON BODY CONFORMATION AND ORGAN SIZE IN YOUNG PIGS MARTHA E. HEATH A.R.C. Institute of Animal Physiology, Babraham, Cambridge CB2 4AT, England (Received7 June 1983)
Abstract- 1. Piglets were weanedat 14days ofage and subsequentlyreared for 23,35,42 or 59 days in a cold (10°C) or a warm (35°C) environment. They were fed to grow at the same rate by feeding cold-reared pigs more than warm-reared pigs. 2. The external surfacearea, the surfacearea of the nasal cavity and the length of extremities were greater in warm- than in cold-reared pigs. Likewise, the massof the skin with subcutaneousfat was greater in warmreared pigs. 3. The mass of the heart, liver, kidneys, stomach and small intestines was greater in cold- than in warmreared pigs. There was no difference in the massof the muscle,spleen,lungs, and large intestine between the two groups.
INTRODUCTION
Prolonged exposure of mammals to a cold environment has long been known to affect their body composition and organ size.Although most studies
have used rodents as subjects,Weaver and Ingram (1969)exposedpigletsto warm (35°C)and cold (5°C) environmentsto determinethe effectof climateon the morphology of a larger mammal. Pigs rearedin the cold had a shortertotal body lengthas well as shorter legs,tail and snoutand smallerearsthan warm-reared littermates.In a secondstudy Ingram and Weaver (1969)showedthat the vascularityof the skin wasless in cold-rearedthan in warm-rearedpigs. The purpose of the present study was to make further observationson the anatomical differences betweenwarm-rearedand cold-rearedpigs, to determine the time courseof the developmentof these differences,and wherepossible,to determinewhether the differencesweredue to a direct effectof temperatureor to someindirecteffect.Includedaremeasures of total surfacearea,the surfaceareaof the nasalcavity and the weightof the varioustissuesand organs.
RESULTS AND METHODS
Experimental animals Twenty-six piglets (males and females)of the Large White breed were used. Litters of eight piglets were taken from the
sowat 14daysof age.Subsequently, halfof thepigletswere
The piglets were given small quantities of their new diet initially. This was necessary to avoid the stimulation of diarrhea which occurs if piglets are given too much of a new diet. Piglets from both environments were fed to gain weight at the same rate, thus those in the cold ate more food than their warm-reared littermates. Both groups were fed at less than the ad libitum level. The piglets were terminated at different ages (37,49, 56 and 73 days old) and consequently had different final weights. Measurementsmadeon carcasses The surface area of the whole body and of the nasal cavity were measured. Measurements of length were made of the total body, extremities, and individual leg bones.The weight of skeletal muscle, fat, skin with attached subcutaneous fat, bone, heart, lungs, spleen, liver, kidneys, stomach, small intestine and large intestine were measured. To estimate the total surface area of a piglet numerous measurements of the girth and of the distance between consecutive girth measurementswere made along the body and extremities (Fig. 1).The surfacearea betweenconsecutive girth measurementswere calculated using the formula for the frustrum of a cone. The area of the end of the snout and rump were assumedto be flat and estimated from the formula of a circle. The surface area of the ears was calculated by tracing around them, finding the area inside the tracing with a planimeter and multiplying by two to allow for both sides of the ear. The total surfacearea of the piglet was taken to be the sum of these measurements. The accuracyofthis measureof surfacearea has beentested in two ways. Firstly, in four pigs the measure was repeated three times to determine consistency.Consecutive measurements were not significantly different (P > 0.1). Secondly, in
reared in a cold environment while their littermates were reared in a warm environment. All piglets were reared individually in cages so that their diet could be controlled. The temp, both in the cold-room and the warm-room, was initially 30°C and was altered by 2°C per day until T,s of 10 and 35”C, respectively,were attained.
Table1.Compositionof the dry pelleted food fed to Ha&r Ltd., Manufacturers) Ingredient
Quantity
Oil
Diet
Protein Fibre VitaminA
Immediately after being separatedfrom the sow the piglets were introduced to a dry pelleted pig food (Kwik creep: Brooks Hasler Ltd.: Table 1) which thev were fed for the duration of the experiment. The piglets were fed twice daily, at 09:OOand 17:OOhr and weighed before the morning feeding.
Vitamin
D
VitaminE Selenium
63
piglets. (Brooks
3.0:): 18.57, 4.07;
15000i.u./kg 1500 h/kg
15i.u./kg 0.1 mg/kg
64
MARTHA E. HEATH
weighed separately and its total mass estimated by assuming that the proportion of tissueper halfcarcass was equal in both halves. The length of the leg bones were taken as the distance of the two points furthest apart. RESL’L TS
Surface areas and extremity lengths are reported first followed by the presentation of the organ weights. Many of the results are presented as a function of body
Fig. I. The location of girth measurementsused in estimating the surface area of pigs are indicated with dotted lines.
six other pigs the body was wrapped with masking tape. This was then cut away and its surface area determined. The value obtained by this method was compared with the values obtained from girth measurements on the same pigs, The values obtained from the girth measurement technique was consistently 2-Y,, lower than those obtained from the tape technique. The effect of cold on ear growth was assessedin some coldreared pigs by putting an insulating e‘ ar-muff’ over one ear while leaving the second ear unmuffed. The muffed ear was taped against the neck and thus warmed by the body as well as being insulated against the cold. The dimensions of the nasal passageof warm- and coldreared pigs were measured becausethe length of the snout was markedly larger in the warm-reared pigs, A difference in the size of the respiratory surface is of interest since it could enhance their ability to tolerate a hot environment. particularly since pigs do not sweat and the respiratory passageis the only area of evaporative heat loss when a wallow is not available. The heads of five cold- and five warm-reared pigs were frozen and subsequentlycut into a seriesof sliceswith a band saw to obtain approximately IO mm thick cross-sectionsof the nasal passage.The thickness ofeach section was measured and the thickness of the saw blade (1.27 mm) was added to it. The surface area of each cross-section was determined by measuring the perimeter of the nasal passageat the anterior and posterior end of each section with an Image Analyzer and using the formula :
SA = hhJ, +[(Pz-P,)Jl)1
weight. When looking at these graphs it should be remembered that the smaller pigs had been exposed to the experimental conditions for relatively less time than the larger animals. This may account for many of the observed differences being greater in the larger animals than in the smaller ones. Paired t-tests (pairing littermates) were used to determine whether observed differences were significant. The total surface area was greater (P < 0.05) in warm-reared than in cold-reared pigs of the same weight (Fig. 2, top). This difference appears to have occurred entirely in the extremities (Fig. 2, middle)
(1)
where SA = surface area, 11= thickness of the section. p, z smaller perimeter and pz = larger perimeter. The surface areas of consecutive sections were summed to find the total surface area of the passage.The vol of the nasal passagewas similarly calculated for each cross-section by measuring the area inside the perimeter using the Image Analyzer and the equation : c’ = hjrr, +[(uz-lr,).‘2 ]] (2) where V = vol, /I = thickness of the section, (1, = smaller area and aZ = larger area. The total volume was taken as the sum of the vol of the cross-sections. The carcassdissection proceededas follows. The length of the total body and of the tail and limbs were measured.After the whole carcass of each piglet was weighed the head was removed at the junction of the occipital condyle and weighed. The viceral organs were removed and weighed individually after the excessblood and fluid was removed with a sponge. The entire digestive tract was weighed with its contents and subsequently the stomach, small intestine and large intestine were each weighed after their contents had been removed. The length of the large and small intestine were measuredby holding them alongside a meter rule. Care was taken to not stretch the intestine. Next the carcass was halved, each half weighed, and one half separated into bone, skeletal muscle and skin with attached subcutaneous fat. Each tissue was
EXTREMITY SURFACE
ro %’
AREA
TRUNK 8 HEAD SURFACE
.‘I”’ 5
“’
10
AREA
I‘ 15
BODY WEIGHT (KG)
Fig. 2. Surface areas plotted against body weight for warm ( n ) and cold-reared (0) pigs.
65
Effects of temperature on organ size in pigs
was due to differencesin circulation, and therefore nutrient supply,or wasdue to tissuetemp per se. The lengthof the snoutwaslonger(P < 0.05) in the muffed q 10°C 01 m warm-rearedpigs(Fig. 4).The dimensionsof the nasal 3 unmuffed n passage weremeasuredto determineif the surfacearea J from which respiratoryevaporativeheat loss occurs differedin the two groupsof pigs.Table2 providesthe data on the dimensionsof the nasal passagesof five pairs of littermates.The Iength (P < 0.025) surface area (P < 0.025),and vol (P < 0.035)of the nasal passage waslargerin warm-rearedthan in cold-reared pigs. But there was no significant differencein the 0 surfacearea to vol ratio (P > 0.1). Thus, although Fig. 3. An illustration of the direct effect of temp on tissue warm-rearedpigshavea largersurfacefor evaporative growth. The ear of a cold-reared pig which had a “muff” heat loss, they do not show an adaptiveincreasein covering it (hatched) was larger than the normally exposed surfacearea to vol ratio which would maximizethe ear (black). The ear of a warm-reared littermate was the heat lost from a given volume of air passingthrough largest of all (white). the nose.
q
35’C
1
1 I
Length of body and extremities
sinceno difference(P > 0.1)in the surfaceareaof the headand trunk regionswasfound (Fig. 2, bottom). To get an impressionof how tempeffectsthe surface areaof extremities,oneear of someof the cold-reared pigswascoveredwith an insulatingear muff while the other ear remainedexposedto the environment.In Fig. 3 the outline of the muffedand unmuffedearsof a pig are illustrated along with that of a warm-reared littermate.The smallestear wasthe uninsulatedear of the cold-rearedpig. The intermediatesizedearwasthe insulated one and the largest ear belongedto the warm-rearedpig. This is a good demonstrationof ambienttemp directly affectingthe growth of a tissue. Insulating the ear merely kept it warmer than the unprotectedear.If therewereno direct effectof temp, then the muffedand unmuffedears would not have differedin size. What was impossibleto determine, however,waswhetherthe effectof tempon eargrowth
0-5 BODY
WEIGHT
(KG)
The lengthof the body and of someof its parts were measuredasa reflectionof skeletalgrowth.Total body length was greater(P < 0.05)in warm- than in coldrearedpigs of the samebody weightas wasthe length of the snout,the tail and leg bones(P < 0.05. Fig. 4). All of thesedifferencesindicate a differencein bone growth betweenthe two groups.That is, bonegrowth is reducedin cold-rearedpigs.Most of thesedifferences weregreaterin the larger (older)animalsthan in the smaller(younger)individuals. The differencesin skeletallength appearnot to be the result of differencesin tissuetemperature.This is deducedfrom the observation(Fig. 5) that the relation betweenthe lengthsof proximal (femur) and distal (tibia) bonesof the legwerethe samein both groupsof pigs. If tissue temp were playing a role in bone development,then the more distal bones of coldrearedpigs would be colder and thereforegrow less
:v
15 BODY
WEIGHT
(KG)
Fig. 4. Length of the total body, femur, tail and snout related to total body weight for warm-(W) and coldreared (0) pigs.
66
MAKTHA
E. HEATH
a linear fashion. Secondly, the tirsucs could be separated into three distinct groups: (a) those tissues which were larger in cold-reared than in warm-reared pigs.(b) those tissues which were larger in warm-reared than in cold-reared pigs. and (c) those which shoucd no signs of being affected by rearing temp. The mass of the heart. liver. kidneys. stomach and small intestine were larger (P < 0.05) in cold-reared LL than in warm-reared pigs of the same body wei+t I Fig. s 6). In addition, the length of the small intestine \+as : greater (P < 0.05) in cold-reared than in warm-reared G& .lO pigs. Only the skin with attached subcutaneous fat and skeletal mass and bone length were greater (I’ c (0.05) TIBIA LENGTH (Ml in warm-reared than cold-reared pigs (Fig. 7). Organs and tissues which were unaffected (P > 0. I ) by cold exposure were the skeletal muscle. spleen. lungs. and large intestine. It should be noted that the relation between the mass of these tissues and total body mass is also unaffected by diffcrcncca in ICLCIof food intake. Although the relation of muscle mass to total body mass was the same (P > 0.1) in both groups of pigs. it can be seen from Fig. 8 that there is an increase in the slope of this relationship from 0.39 in pigs less than 6 kg to 0.53 in pigs greater than 6 kg. This is attributable to an increased amount of fat in the muscle tissue of k .O% ti $0 70 ab larger (older) pigs. since the relation of fat-free muscle TOTAL LENGTH (M) mass to total body weight is linear over the entire range Fig. 5. The relation betweenfemur length and tibia length of body weights. (top) and between femur length and total body length (bottom)is the samein warm-(m) andcold-reared(0) reared pigs.
(because of a Qlo effect) than their more proximal bones.This would not be expected in warm-reared pigs where tissue temperature would be uniformly high throughout the body. Furthermore. it appears that the differences in bone growth are present throughout the body since the relation of femur length to total body length is the same in both groups of piglets (Fig. 5). These results indicate an indirect affect of T, on skeletal growth in relation to body weight. This indirect effect of T, is also affecting surface area since the diminished length of the legs and tail results in their having a reduced surface area. When organ or tissue weight was plotted against body weight two observations could be made. Firstly, most of the tissues varied with body weight in roughly
Pair I Pair ?
The results of this study show that total external surface area and the surface area of the nasal cavity. total body length and the length of individual bones. and the mass of the skeleton and skin with attached subcutaneousfat are all greater in warm-reared than in cold-reared pigs of the same body weight. In contrast. the mass of the kidneys. heart, liver. stomach and small intestine and the length of the small intestine arc greater in cold-reared than in warm-reared pigs. These observed differences may be due either to direct or indirect effects of temp, or to the differences in level of food intake between the two groups. Few actual measurements of surface area have been made on animals reared in widely differing ambient temps. Sundstroem (1922) found that mice exposed to tropical heat had larger surface areas than controls exposed to neutral conditions. Relatively more studies
Psir 4 Pair 5
1 I? 7.32 7.52 x.09 X.h3
x.14 9.55 9.44 9.59 8 74
98.00 88.80 92.25 96.99 103.12
I I627 I I7.W 94.17 110.79 I I X.29
13.5 12.34 13.X0 I?.84 14.8X
MeLin S.D.
7 74 O.h?
9 09 0.64
95.83 551
I I I.32 IO.01
I?.3X lhX9 099 1.7x P < 0 ox
Rur 3
Paired
,-test
P < 0.025
P < 0.025
17.X7 IX.35 I.382 Ih.9 17.27
7.51 7.’
h 50 h 3x
Effects of
temperature on organsizein pigs
67
L
5
60.
w 3
40.
L 5 I
. 20.
“I’ 5
4,
“I
; P 100. s
“-I
10
15
?;..:g .
/' Ii‘
PJ
0. G B
,O:
z
20-
.
,F
4,..
a --““-‘L
5
QA .5 BODY WEIGHT
10
15
lb"
15
(KG)
5,
OO
5
10
15
BODY WEIGHT (KG)
Fig. 6. The weight of the kidneys, liver, stomach, heart, and small intestine in relation to total body weight in warm- (m) and cold-reared (0) pigs. Also the length of the small intestine in relation to total body weight.
(Sumner,1915;Ogle,1934;MichieandMcLaren1956, Weaver and Ingram, 1969)have reported larger or longerextremitiesin animalsexposedto hot environments and smaller or shorter extremitiesin animals exposedto cold environments.These findings also indicatea differencein surfacearea. The presentstudy showedthat the differencesin surfaceareaof warm- and cold-rearedpigs are attributablewholly to differences in theextremitiesand not to any differenceoccurring in the surfacearea of the trunk or head.The differencein ear size and surface areaappearsto be dueto a direct effectof temperature on tissuegrowth. That is, the result of a Qr,, effectin which growth proceedsmore slowly in colder tissues, or, the resultof cold inducedvasoconstrictionrestricting the nutrient supply which in turn reducesthe rate of growth. In contrast to the ear, the smallersurface areasof the limbs and tail of cold-rearedpigsis at least in part attributableto an indirecteffectoftemp.That is the indirect effect of rearing-tempon bone growth which resultsin theseappendages being shorter and havinglesssurfaceareain cold-rearedpigs. Weaverand Ingram (1969)also observedthis effect of rearing-tempon bonegrowth whenthey measured
the length of individual long bonesof pigs rearedin cold (SC), neutral (25°C)and warm (35°C)environments.They too found that the long bonesof coldrearedpigs were shorter than those of warm-reared pigs. But they also showedevidencethat boneswere shorterin warm-rearedpigs than in pigs rearedin the neutralenvironment,althoughthis differencewasless pronounced.This is furtherevidencethat thedifference in bonegrowth is not due to a Q,,, effect. The nature of the indirect effect of T, on bone growth, can only be speculatedupon. It could be hormonal,geneticor nutritional. Pochneeand Heaton (1976)foundthat femurmasswasgreaterin rats which ate their food in a singlemealrather than nibbling.In the presentstudy cold-rearedpigs tendedto eat most of their food as a meal after feeding time whereas warm-rearedpigs nibbled throughout the day but femur masswas lessrather than greaterin the coldrearedmeal-eaters(Fig. 7).Deprivationof protein has alsobeenshownto reducelong bonegrowth(Platt and Stewart, 1962)but again, in the present study the short-bonedcold-rearedpigs ate more and retained more nitrogen than their warm-rearedlittermatesof the sameweight (Heath,in press).It is possiblethat
MARTHAr “-
68
20 1.8 I
I
OO
..I.....
10 5 BODY WEIGHT (KG)
..I
I
15
Fig. 7. The weightof the skin with subcutaneous fat (top)and bone(bottom)in relation to the total body weightof warm( n ) and cold-reared(0) pigs.
cold-exposure may have affected skeletal growth by affecting the secretion of growth hormone, which is known to affect bone growth (Williams, 1974).
-
and grew more slowly. This indicates that the mass of these organs can be affected by level of food intake alone. Although Widdowson and McCance (1960) found no difference in the weight of the kidneys in overfed and control rats, Kennedy( 1957)reported that the size of the kidneys was correlated to nitrogen intake. The larger kidney mass of cold-reared pigs of the present study may be due to their having a higher rate of nitrogen intake due to their higher level of food intake. Schmidt and Widdowson (1967)attributed the hypertrophy of the liver, kidneys and the gastrointestinal tract of cold-reared rats to their higher level of food intake. Also, Koong rl (11.(1982) have recently shown that elevation of food intake contributes to the hypertrophy of the stomach, small intestine, liver and kidneys of pigs, but they did not find the elevated food intake to have any effect on the mass of the heart or spleen. Pocknee and Heaton (1976) found that the mass 01 the liver, kidneys, small intestine, and stomach were greater in m ‘ eal-eater’ rats than in continuously fed controls (nibblers). Therefore, frequency of food intake may also have contributed the difference in the size of digestive organs. It is clear, from the present study, that even after as little as 3 weeks of exposure to the different environments, the mass of most tissueswere already affected. While the magnitude of the differences in warm- and cold-reared pigs were the same (parallel) over the entire range of exposure periods for some measurements (tail length, snout length, total surface area, extremity surface area) most often the differences increased with length of exposure. This may indicate that the tail and snout are at a particularly dynamic stagein their growth during the early part of the study.
Organ size and tissue muss The mass of the various organs and tissues have been measuredin warm- and cold-exposed (or reared) animals of several species(Tables 3 and 4). The results are remarkably similar even though the studies differ in the size and age of animals used, and the temp and length of exposure. That is, the heart, liver, kidneys thyroid and adrenals were larger in cold-exposed and smaller in warm-exposed animals than in controls. Barnett and Widdowson (1965) also showed that the weight of the stomach, small intestine and large intestine were larger in cold-exposed mice, and Baker and Ashworth (1958)showed the pancreasto be larger in cold exposed rats. In contrast, total body fat, nitrogen and skeletal muscle mass were less in coldexposedthan in control animals. The effect of environmental temp on spleen mass was variable. Lung mass was found to be unaffected by temp (Heroux and Gridgeman, 1958). Besides the effect of cold-exposure per se, the differences in organ weights could be due to the differences in the level or frequency of food intake. Certainly, all of these organs are involved in the processing of the food eaten. That is, in digestion, transport of nutrients and wastes, or elimination of wastes. Widdowson and McCance (1960) found that the heart, liver, stomach and small intestine were larger in rats which were overfed than in rats which were terminated at the same weight but which were fed less
0
/
FAT FREE
MUSCLE
/ I....I... OO
5
)....A 10
15
BODY WEIGHT (KG)
Fig. 8. The relation of total musclemass(top) and fat-free musclemass(bottom)to total body massin warm- (m) and cold-reared(0) pigs.
Rat Peromyscus Rat Rat Mouse Rat Rat Ground squirrel Pig Hamster Pig Pig Peromyscus
Mouse Mouse Mouse Mouse MO”%
Species 28-32 28-32 28-32 28-32 31-33 35 30 35 32 34-35 33 28 30 35 35 33 35
13-23 13-23 13-23 13-23 21-27
28
15 24 25 24-26 22 18 25 23 20 23 24
Exoosure Temp”C A A A A A
140 140 140 140 140 210 A Natural population 5748 A A 3@36 45 A 150 A 18 A A 56 A 60 A 72 GSR 41 A 60 A
Food
Duration (days)
-
-
:
35y76 variable -
3-59 young 100 g
48:60 Y-a a Y
O-210 -
&140 Cl40 O-140 Cl40 a -
-
+ + + + +
+
+ +
+
+ + + +
-
A, ad libitum; GSR, grown at same rate; RT, room temp; a, adults; y, young; +. larger; 0, no difference; -, smaller
Sundstroem (1922a) Sunstroem (1922b) Sunstroem (1922~) Sundstroem (1930) Ogle (1934) Herrington and Nelbach (1942) Sealander(1951) Heroux and Hart (1954) Young and Cook (1955) Michie and McLaren (1956) Hale et al. (1959) Vacek et al. (1961) Pohl and Hart (1965) Fuller (1965) Cassuto and Chaffee(1966) Weaver and Ingram (1969) Sugahara et 01.(1970) Roberts and ChaiTee(1976)
References
+
0
+
+ +
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+
-
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Table 3. The effects ofexposing animals to hot as compared to thermally neutral environments on the size of their organs and tissues
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MARTHA I?. HEATH
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Effectsof temperature on organ size in pigs Other organs, which increase in size at a rate correlated with the increase in body weight, showed greater differences in the larger pigs which had been exposed to the respective environments for longer. The length of the small intestine showed the greatest increase in length during the early stages ofexposure as if there is a shorter period of time when intestinal growth is most influenced by rearing-temp or level of food intake.
71
Heroux 0. and Schonbaum E. (1959) Comparison between seasonaland thermal acclimation in white rats. III. Studies of the adrenal cortex. Can. J. Biochem.Physiol. 37, 12551261. Herrington L. P. and Nelbach J. H. (1947) Relation of gland weights to growth and aging processesin rats exposed to certain environmental conditons. Endocrinology 30, 375386.
Holeckova E., Baudysova M. and Michl J. (1974) Effect of acclimation to cold on rat kidney growth in uiuo and in vitro. Physiol. Biochem.23, 97-100. Hosslin H. V. (1888) Ueber die ursache der scheinbaren Acknowledyements~I thank Mr Frank Pluck for assistance abhangigkeit des umsatzesvon der grosseder korperoberin the dissection of the pigs, Dr Hector Dott for use of his flache. Archs Physiol. 11,323-379. Image Analyzer and MS Kein Wan for typing the manuscript. Huestis R. R. (1931) Seasonal pelage differences in PerI am also indebted to my Ph.D. Supervisor, Dr D. L. Ingram, omyscus.J. Mammal. 12, 372-375. for his advice during this study. Ingram D. L. and Weaver M. E. (I 969) A quantitative study of the blood vesselsof the pig’s skin and the influence of environmental temperature. Anat. Rec. 163, 517-524. Kennedy G. C. (1957) The effect of gas on the somatic and REFERENCES visceral responseto overnutrition in the rat. J. Endocr. 15, Baker D. Cl. and Ashworth M. A. 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A., PekasJ. C. and Yen J. (I 982) Effects Chaffee R. R. J., Atzet J. E. and Kelly K. H. (1962) Effect of of plane of nutrition on organ size and fasting heat multiple vs single caging on body and organ growth during production in pigs. J. Nutr. 112, 1638-1642. cold acclimation. Am. Zoo/. 2, 511. Chevillard L., Cade M. and Portet R. (1962) Somatic and Laurie E. M. 0. (1946)The reproduction of the house mouse (Mus musculus)living in different environments. Proc. R metabolic variations in the rat living at different temperaSot. B. 133,248-281. tures. J. Physiol., Paris. 54, 314315. Dugal L. P. and Therier M. (1949) The influence of ascorbic Michie D. and McLaren A. (1956)The effect of raising mice at a low and high temperature on growth and variability. In acid on the adrenal weight during cold exposure. Problemsof Physiology of’ the Pre-weaning Period in Man Endocrinology 44,42&426. and Mammals. Summary of papers pp. 5&5 I. Fuller M. F. (1965) The effect of environmental temperature Mills C. A. (1945) Influence of environment temperatures on on nitrogen metabolism and growth of young pigs. Br. J. warm-blooded animals. Ann. N.Y Acad. Sci. 46,97-98. Nutr.19, 531-546. Gilson S. B. (1950) Studies on adaptation to cold in the rat. Ogle C. A. (1934) Climatic influence on the male albino mouse. Am. J. Physiol. 107, 635-640. Am.J. Physiol. 161, 87-91. Page E. and Babineau L. (1950) The effect of cold environHale H. B., Mefferd R. D., Vawter G., Foester G. E. and ment on the hibernating gland of the rat. Rec. Can. Biol. 9, Griscuolo A. (1959) Influence of long term exposure to 202-205. adverseenvironments on organ weights and histology. Am. Platt B. S. and Stewart R. J. C. (1962)Transverse trabeculae .I. Physiol. 196, 520-524. and osteoporosis in bones in experimental protein-caloric Harrison G. A., Morton R. J. and Weiner J. S. (1959) The deficiency. Br. J. Nutr. 16, 483-496. growth in weight and tail length of inbred and hybrid mice Pochnee R. C. and Heaton F. W. (1976)The effect of feeding reared at two different temperatures. Phil. Trans. R. Sot. frequency on the growth and composition of individual 242,479-516. organs in the rat. Br. J. Nutr. 35,977104. Hart J. S. (I 956) Seasonalchanges in insulation of the fur. Pohl H. and Hart J. S. (1965) Thermoregulation and cold Can. J. Zool. 34, 53-57. acclimation in a hibernator, Cirellus tridrcvmlineatus. J. Heath M. E. (1983) The effects of rearing temperature on appl. Physiol. 20, 398404. body composition in young pigs. Comp. Biochem.Physiol. Prizibram V. (1925) Arch. EntwMech Organ. 104, 548-559. (in press). Rand C. G., Riggs D. S. and Talbot N. B. (1952)The influence Heroux 0. (1958) Weights and composition of muscles of of environmental temperature on the metabolism of the warm and cold-acclimated rats. Can. J. Biochem.Physiol. thyroid hormone in the rat. Endoc.rino/ogy51, 562-569. 36,281-293. Heroux 0. and Campbell J. S. (1959) Comparison between Roberts J. C. and Chaffee R. R. J. (1976) Metabolic and seasonal and thermal acclimation in white rats. IV. biochemical aspectsof heat acclimation in the deer mouse. Camp. Biochem.Physiol. 53A, 367-373. Morphological and pathological changes.Can. J. Biochem. Physiol. 37, 1263-1269. Schmidt P. and Widdowson E. M. (1967)The effect of a low protein diet and a cold environment on calorie intake and Heroux 0. and Gridgeman N. T. (1958) The effect of cold acclimation on the size of organs and bones of rats with body compositon in the rat. Br. J. Nutr. 21,457-465. special referenceto modes of expressionof results, Can. J. SealanderJ. A. (1951) Survival of Peromyscusin relation to Biochem.Physioi. 35, 209-2 16. environmental temperature and acclimation at high and Heroux 0. and Hart J. S.(1954)Comparison of four indices of low temperatures.Am. Nat. 46, 2577311. adrenal activity in rats acclimated to 30, 15, I C ‘ . Am. J. SellersE. A. (1957)Adaptative and related phenomenain rats Physiol. 178, 4455448. exposed to cold. A review. Rw. Can. Biol. 16, 1755188.
72
MAKTHA E. HEATH
Straw J. A. and Fregiey M. J. (1967) Evaluation of thyroid function during cold acclimation. J. nppl. Pkysiol. 23, 825830. Sugahara M., Baker H., Harmon B. G. and Jensen A. H. (1970) Effect of ambient temperature on performance and carcassdevelopment in young swine. J. Anim. Sci. 31, 5962. Sumner F. B. (1909) Some effects of external conditions on the white mouse. J. e.up. Zoo/. 7, 97-155. Sumner F. B. (1913) The effects of atmospheric temperature upon body temperature of mice. /. up. 2001.15, 3 155377. Sumner F. B. (1915)Some studies ofenvironmental influence, heredity correlations and growth in the white mouse. J. esp. Zoo/. 18, 325-432. Sundstroem E. S. (1922a)Studieson the adaptattons of albino mice to an artificially produced tropical climate. I. Effect of the various factors composing a tropical climate on growth and fertility of mice. Am. J. Phl;siol. 60, 397-415. Sundstroem E. S. (1922b) Studieson the adaptation of albino mice to an artificially produced tropical climate. II. Relations of body form and especially the surface area to the reactions released by and the resistance to a tropical climate. Am. J. PhWol. 60, 416-424.
Sundstroem E. S. (1922~)Studieson the adaptations ofalbino mice to an artificially produced tropical climate. III. Effect of the tropical climate on growth and pigmentation of hair and the dependenceof theseintegumental functions on the temperature coefficient law. Am. J. Physiol. 60, 425-432. Vacek Z., Hahn P. and Koldovsky 0. (1961) The effect of rearing infant rats at three environmental temperatures on the structure of some of their organs. .I. Anat. 95,21&219. Weaver M. E. and Ingram D. L. (1969) Morphological changesin swine associatedwith environmental temperature. EcoloqJ,50, 71&713. Widdowson E. M. and McCance R. A. (1960) Some effectsof acceleratinggrowth. I. Generalsomaticdevelopment. Pro<~. R. Sot. B. 152, 188m 206. Williams R. H. (1974) 7e\-rhor>kof’ t‘n docrinolol~. W. B. Saunders Co., Philadelphia. Woods R. and Carlson L. D. (1956) Thyroxine secretion in rats exposed to cold. Edoc~rinoloyy 59, 323 330. You R. W. and Sellers E. A. (1951) Increased oxygen consumption and succinoxidaseactivity of liver tissueafter exposure of rats to cold. Endocrinoloq~ 49, 374-378. Young D. B. and Cook S. F. (1955) Body lipids in small mammals following prolonged exposure to high and low temperature. Am. .J. PIlysiol. 181, 72-74.
03050491/84
$3.00 + 0.00
80 1984PergamonPressLtd
THE EFFECTS OF REARING-TEMPERATURE ON BODY CONFORMATION AND ORGAN SIZE IN YOUNG PIGS MARTHA E. HEATH A.R.C. Institute of Animal Physiology, Babraham, Cambridge CB2 4AT, England (Received7 June 1983)
Abstract- 1. Piglets were weanedat 14days ofage and subsequentlyreared for 23,35,42 or 59 days in a cold (10°C) or a warm (35°C) environment. They were fed to grow at the same rate by feeding cold-reared pigs more than warm-reared pigs. 2. The external surfacearea, the surfacearea of the nasal cavity and the length of extremities were greater in warm- than in cold-reared pigs. Likewise, the massof the skin with subcutaneousfat was greater in warmreared pigs. 3. The mass of the heart, liver, kidneys, stomach and small intestines was greater in cold- than in warmreared pigs. There was no difference in the massof the muscle,spleen,lungs, and large intestine between the two groups.
INTRODUCTION
Prolonged exposure of mammals to a cold environment has long been known to affect their body composition and organ size.Although most studies
have used rodents as subjects,Weaver and Ingram (1969)exposedpigletsto warm (35°C)and cold (5°C) environmentsto determinethe effectof climateon the morphology of a larger mammal. Pigs rearedin the cold had a shortertotal body lengthas well as shorter legs,tail and snoutand smallerearsthan warm-reared littermates.In a secondstudy Ingram and Weaver (1969)showedthat the vascularityof the skin wasless in cold-rearedthan in warm-rearedpigs. The purpose of the present study was to make further observationson the anatomical differences betweenwarm-rearedand cold-rearedpigs, to determine the time courseof the developmentof these differences,and wherepossible,to determinewhether the differencesweredue to a direct effectof temperatureor to someindirecteffect.Includedaremeasures of total surfacearea,the surfaceareaof the nasalcavity and the weightof the varioustissuesand organs.
RESULTS AND METHODS
Experimental animals Twenty-six piglets (males and females)of the Large White breed were used. Litters of eight piglets were taken from the
sowat 14daysof age.Subsequently, halfof thepigletswere
The piglets were given small quantities of their new diet initially. This was necessary to avoid the stimulation of diarrhea which occurs if piglets are given too much of a new diet. Piglets from both environments were fed to gain weight at the same rate, thus those in the cold ate more food than their warm-reared littermates. Both groups were fed at less than the ad libitum level. The piglets were terminated at different ages (37,49, 56 and 73 days old) and consequently had different final weights. Measurementsmadeon carcasses The surface area of the whole body and of the nasal cavity were measured. Measurements of length were made of the total body, extremities, and individual leg bones.The weight of skeletal muscle, fat, skin with attached subcutaneous fat, bone, heart, lungs, spleen, liver, kidneys, stomach, small intestine and large intestine were measured. To estimate the total surface area of a piglet numerous measurements of the girth and of the distance between consecutive girth measurementswere made along the body and extremities (Fig. 1).The surfacearea betweenconsecutive girth measurementswere calculated using the formula for the frustrum of a cone. The area of the end of the snout and rump were assumedto be flat and estimated from the formula of a circle. The surface area of the ears was calculated by tracing around them, finding the area inside the tracing with a planimeter and multiplying by two to allow for both sides of the ear. The total surfacearea of the piglet was taken to be the sum of these measurements. The accuracyofthis measureof surfacearea has beentested in two ways. Firstly, in four pigs the measure was repeated three times to determine consistency.Consecutive measurements were not significantly different (P > 0.1). Secondly, in
reared in a cold environment while their littermates were reared in a warm environment. All piglets were reared individually in cages so that their diet could be controlled. The temp, both in the cold-room and the warm-room, was initially 30°C and was altered by 2°C per day until T,s of 10 and 35”C, respectively,were attained.
Table1.Compositionof the dry pelleted food fed to Ha&r Ltd., Manufacturers) Ingredient
Quantity
Oil
Diet
Protein Fibre VitaminA
Immediately after being separatedfrom the sow the piglets were introduced to a dry pelleted pig food (Kwik creep: Brooks Hasler Ltd.: Table 1) which thev were fed for the duration of the experiment. The piglets were fed twice daily, at 09:OOand 17:OOhr and weighed before the morning feeding.
Vitamin
D
VitaminE Selenium
63
piglets. (Brooks
3.0:): 18.57, 4.07;
15000i.u./kg 1500 h/kg
15i.u./kg 0.1 mg/kg
64
MARTHA E. HEATH
weighed separately and its total mass estimated by assuming that the proportion of tissueper halfcarcass was equal in both halves. The length of the leg bones were taken as the distance of the two points furthest apart. RESL’L TS
Surface areas and extremity lengths are reported first followed by the presentation of the organ weights. Many of the results are presented as a function of body
Fig. I. The location of girth measurementsused in estimating the surface area of pigs are indicated with dotted lines.
six other pigs the body was wrapped with masking tape. This was then cut away and its surface area determined. The value obtained by this method was compared with the values obtained from girth measurements on the same pigs, The values obtained from the girth measurement technique was consistently 2-Y,, lower than those obtained from the tape technique. The effect of cold on ear growth was assessedin some coldreared pigs by putting an insulating e‘ ar-muff’ over one ear while leaving the second ear unmuffed. The muffed ear was taped against the neck and thus warmed by the body as well as being insulated against the cold. The dimensions of the nasal passageof warm- and coldreared pigs were measured becausethe length of the snout was markedly larger in the warm-reared pigs, A difference in the size of the respiratory surface is of interest since it could enhance their ability to tolerate a hot environment. particularly since pigs do not sweat and the respiratory passageis the only area of evaporative heat loss when a wallow is not available. The heads of five cold- and five warm-reared pigs were frozen and subsequentlycut into a seriesof sliceswith a band saw to obtain approximately IO mm thick cross-sectionsof the nasal passage.The thickness ofeach section was measured and the thickness of the saw blade (1.27 mm) was added to it. The surface area of each cross-section was determined by measuring the perimeter of the nasal passageat the anterior and posterior end of each section with an Image Analyzer and using the formula :
SA = hhJ, +[(Pz-P,)Jl)1
weight. When looking at these graphs it should be remembered that the smaller pigs had been exposed to the experimental conditions for relatively less time than the larger animals. This may account for many of the observed differences being greater in the larger animals than in the smaller ones. Paired t-tests (pairing littermates) were used to determine whether observed differences were significant. The total surface area was greater (P < 0.05) in warm-reared than in cold-reared pigs of the same weight (Fig. 2, top). This difference appears to have occurred entirely in the extremities (Fig. 2, middle)
(1)
where SA = surface area, 11= thickness of the section. p, z smaller perimeter and pz = larger perimeter. The surface areas of consecutive sections were summed to find the total surface area of the passage.The vol of the nasal passagewas similarly calculated for each cross-section by measuring the area inside the perimeter using the Image Analyzer and the equation : c’ = hjrr, +[(uz-lr,).‘2 ]] (2) where V = vol, /I = thickness of the section, (1, = smaller area and aZ = larger area. The total volume was taken as the sum of the vol of the cross-sections. The carcassdissection proceededas follows. The length of the total body and of the tail and limbs were measured.After the whole carcass of each piglet was weighed the head was removed at the junction of the occipital condyle and weighed. The viceral organs were removed and weighed individually after the excessblood and fluid was removed with a sponge. The entire digestive tract was weighed with its contents and subsequently the stomach, small intestine and large intestine were each weighed after their contents had been removed. The length of the large and small intestine were measuredby holding them alongside a meter rule. Care was taken to not stretch the intestine. Next the carcass was halved, each half weighed, and one half separated into bone, skeletal muscle and skin with attached subcutaneous fat. Each tissue was
EXTREMITY SURFACE
ro %’
AREA
TRUNK 8 HEAD SURFACE
.‘I”’ 5
“’
10
AREA
I‘ 15
BODY WEIGHT (KG)
Fig. 2. Surface areas plotted against body weight for warm ( n ) and cold-reared (0) pigs.
65
Effects of temperature on organ size in pigs
was due to differencesin circulation, and therefore nutrient supply,or wasdue to tissuetemp per se. The lengthof the snoutwaslonger(P < 0.05) in the muffed q 10°C 01 m warm-rearedpigs(Fig. 4).The dimensionsof the nasal 3 unmuffed n passage weremeasuredto determineif the surfacearea J from which respiratoryevaporativeheat loss occurs differedin the two groupsof pigs.Table2 providesthe data on the dimensionsof the nasal passagesof five pairs of littermates.The Iength (P < 0.025) surface area (P < 0.025),and vol (P < 0.035)of the nasal passage waslargerin warm-rearedthan in cold-reared pigs. But there was no significant differencein the 0 surfacearea to vol ratio (P > 0.1). Thus, although Fig. 3. An illustration of the direct effect of temp on tissue warm-rearedpigshavea largersurfacefor evaporative growth. The ear of a cold-reared pig which had a “muff” heat loss, they do not show an adaptiveincreasein covering it (hatched) was larger than the normally exposed surfacearea to vol ratio which would maximizethe ear (black). The ear of a warm-reared littermate was the heat lost from a given volume of air passingthrough largest of all (white). the nose.
q
35’C
1
1 I
Length of body and extremities
sinceno difference(P > 0.1)in the surfaceareaof the headand trunk regionswasfound (Fig. 2, bottom). To get an impressionof how tempeffectsthe surface areaof extremities,oneear of someof the cold-reared pigswascoveredwith an insulatingear muff while the other ear remainedexposedto the environment.In Fig. 3 the outline of the muffedand unmuffedearsof a pig are illustrated along with that of a warm-reared littermate.The smallestear wasthe uninsulatedear of the cold-rearedpig. The intermediatesizedearwasthe insulated one and the largest ear belongedto the warm-rearedpig. This is a good demonstrationof ambienttemp directly affectingthe growth of a tissue. Insulating the ear merely kept it warmer than the unprotectedear.If therewereno direct effectof temp, then the muffedand unmuffedears would not have differedin size. What was impossibleto determine, however,waswhetherthe effectof tempon eargrowth
0-5 BODY
WEIGHT
(KG)
The lengthof the body and of someof its parts were measuredasa reflectionof skeletalgrowth.Total body length was greater(P < 0.05)in warm- than in coldrearedpigs of the samebody weightas wasthe length of the snout,the tail and leg bones(P < 0.05. Fig. 4). All of thesedifferencesindicate a differencein bone growth betweenthe two groups.That is, bonegrowth is reducedin cold-rearedpigs.Most of thesedifferences weregreaterin the larger (older)animalsthan in the smaller(younger)individuals. The differencesin skeletallength appearnot to be the result of differencesin tissuetemperature.This is deducedfrom the observation(Fig. 5) that the relation betweenthe lengthsof proximal (femur) and distal (tibia) bonesof the legwerethe samein both groupsof pigs. If tissue temp were playing a role in bone development,then the more distal bones of coldrearedpigs would be colder and thereforegrow less
:v
15 BODY
WEIGHT
(KG)
Fig. 4. Length of the total body, femur, tail and snout related to total body weight for warm-(W) and coldreared (0) pigs.
66
MAKTHA
E. HEATH
a linear fashion. Secondly, the tirsucs could be separated into three distinct groups: (a) those tissues which were larger in cold-reared than in warm-reared pigs.(b) those tissues which were larger in warm-reared than in cold-reared pigs. and (c) those which shoucd no signs of being affected by rearing temp. The mass of the heart. liver. kidneys. stomach and small intestine were larger (P < 0.05) in cold-reared LL than in warm-reared pigs of the same body wei+t I Fig. s 6). In addition, the length of the small intestine \+as : greater (P < 0.05) in cold-reared than in warm-reared G& .lO pigs. Only the skin with attached subcutaneous fat and skeletal mass and bone length were greater (I’ c (0.05) TIBIA LENGTH (Ml in warm-reared than cold-reared pigs (Fig. 7). Organs and tissues which were unaffected (P > 0. I ) by cold exposure were the skeletal muscle. spleen. lungs. and large intestine. It should be noted that the relation between the mass of these tissues and total body mass is also unaffected by diffcrcncca in ICLCIof food intake. Although the relation of muscle mass to total body mass was the same (P > 0.1) in both groups of pigs. it can be seen from Fig. 8 that there is an increase in the slope of this relationship from 0.39 in pigs less than 6 kg to 0.53 in pigs greater than 6 kg. This is attributable to an increased amount of fat in the muscle tissue of k .O% ti $0 70 ab larger (older) pigs. since the relation of fat-free muscle TOTAL LENGTH (M) mass to total body weight is linear over the entire range Fig. 5. The relation betweenfemur length and tibia length of body weights. (top) and between femur length and total body length (bottom)is the samein warm-(m) andcold-reared(0) reared pigs.
(because of a Qlo effect) than their more proximal bones.This would not be expected in warm-reared pigs where tissue temperature would be uniformly high throughout the body. Furthermore. it appears that the differences in bone growth are present throughout the body since the relation of femur length to total body length is the same in both groups of piglets (Fig. 5). These results indicate an indirect affect of T, on skeletal growth in relation to body weight. This indirect effect of T, is also affecting surface area since the diminished length of the legs and tail results in their having a reduced surface area. When organ or tissue weight was plotted against body weight two observations could be made. Firstly, most of the tissues varied with body weight in roughly
Pair I Pair ?
The results of this study show that total external surface area and the surface area of the nasal cavity. total body length and the length of individual bones. and the mass of the skeleton and skin with attached subcutaneousfat are all greater in warm-reared than in cold-reared pigs of the same body weight. In contrast. the mass of the kidneys. heart, liver. stomach and small intestine and the length of the small intestine arc greater in cold-reared than in warm-reared pigs. These observed differences may be due either to direct or indirect effects of temp, or to the differences in level of food intake between the two groups. Few actual measurements of surface area have been made on animals reared in widely differing ambient temps. Sundstroem (1922) found that mice exposed to tropical heat had larger surface areas than controls exposed to neutral conditions. Relatively more studies
Psir 4 Pair 5
1 I? 7.32 7.52 x.09 X.h3
x.14 9.55 9.44 9.59 8 74
98.00 88.80 92.25 96.99 103.12
I I627 I I7.W 94.17 110.79 I I X.29
13.5 12.34 13.X0 I?.84 14.8X
MeLin S.D.
7 74 O.h?
9 09 0.64
95.83 551
I I I.32 IO.01
I?.3X lhX9 099 1.7x P < 0 ox
Rur 3
Paired
,-test
P < 0.025
P < 0.025
17.X7 IX.35 I.382 Ih.9 17.27
7.51 7.’
h 50 h 3x
Effects of
temperature on organsizein pigs
67
L
5
60.
w 3
40.
L 5 I
. 20.
“I’ 5
4,
“I
; P 100. s
“-I
10
15
?;..:g .
/' Ii‘
PJ
0. G B
,O:
z
20-
.
,F
4,..
a --““-‘L
5
QA .5 BODY WEIGHT
10
15
lb"
15
(KG)
5,
OO
5
10
15
BODY WEIGHT (KG)
Fig. 6. The weight of the kidneys, liver, stomach, heart, and small intestine in relation to total body weight in warm- (m) and cold-reared (0) pigs. Also the length of the small intestine in relation to total body weight.
(Sumner,1915;Ogle,1934;MichieandMcLaren1956, Weaver and Ingram, 1969)have reported larger or longerextremitiesin animalsexposedto hot environments and smaller or shorter extremitiesin animals exposedto cold environments.These findings also indicatea differencein surfacearea. The presentstudy showedthat the differencesin surfaceareaof warm- and cold-rearedpigs are attributablewholly to differences in theextremitiesand not to any differenceoccurring in the surfacearea of the trunk or head.The differencein ear size and surface areaappearsto be dueto a direct effectof temperature on tissuegrowth. That is, the result of a Qr,, effectin which growth proceedsmore slowly in colder tissues, or, the resultof cold inducedvasoconstrictionrestricting the nutrient supply which in turn reducesthe rate of growth. In contrast to the ear, the smallersurface areasof the limbs and tail of cold-rearedpigsis at least in part attributableto an indirecteffectoftemp.That is the indirect effect of rearing-tempon bone growth which resultsin theseappendages being shorter and havinglesssurfaceareain cold-rearedpigs. Weaverand Ingram (1969)also observedthis effect of rearing-tempon bonegrowth whenthey measured
the length of individual long bonesof pigs rearedin cold (SC), neutral (25°C)and warm (35°C)environments.They too found that the long bonesof coldrearedpigs were shorter than those of warm-reared pigs. But they also showedevidencethat boneswere shorterin warm-rearedpigs than in pigs rearedin the neutralenvironment,althoughthis differencewasless pronounced.This is furtherevidencethat thedifference in bonegrowth is not due to a Q,,, effect. The nature of the indirect effect of T, on bone growth, can only be speculatedupon. It could be hormonal,geneticor nutritional. Pochneeand Heaton (1976)foundthat femurmasswasgreaterin rats which ate their food in a singlemealrather than nibbling.In the presentstudy cold-rearedpigs tendedto eat most of their food as a meal after feeding time whereas warm-rearedpigs nibbled throughout the day but femur masswas lessrather than greaterin the coldrearedmeal-eaters(Fig. 7).Deprivationof protein has alsobeenshownto reducelong bonegrowth(Platt and Stewart, 1962)but again, in the present study the short-bonedcold-rearedpigs ate more and retained more nitrogen than their warm-rearedlittermatesof the sameweight (Heath,in press).It is possiblethat
MARTHAr “-
68
20 1.8 I
I
OO
..I.....
10 5 BODY WEIGHT (KG)
..I
I
15
Fig. 7. The weightof the skin with subcutaneous fat (top)and bone(bottom)in relation to the total body weightof warm( n ) and cold-reared(0) pigs.
cold-exposure may have affected skeletal growth by affecting the secretion of growth hormone, which is known to affect bone growth (Williams, 1974).
-
and grew more slowly. This indicates that the mass of these organs can be affected by level of food intake alone. Although Widdowson and McCance (1960) found no difference in the weight of the kidneys in overfed and control rats, Kennedy( 1957)reported that the size of the kidneys was correlated to nitrogen intake. The larger kidney mass of cold-reared pigs of the present study may be due to their having a higher rate of nitrogen intake due to their higher level of food intake. Schmidt and Widdowson (1967)attributed the hypertrophy of the liver, kidneys and the gastrointestinal tract of cold-reared rats to their higher level of food intake. Also, Koong rl (11.(1982) have recently shown that elevation of food intake contributes to the hypertrophy of the stomach, small intestine, liver and kidneys of pigs, but they did not find the elevated food intake to have any effect on the mass of the heart or spleen. Pocknee and Heaton (1976) found that the mass 01 the liver, kidneys, small intestine, and stomach were greater in m ‘ eal-eater’ rats than in continuously fed controls (nibblers). Therefore, frequency of food intake may also have contributed the difference in the size of digestive organs. It is clear, from the present study, that even after as little as 3 weeks of exposure to the different environments, the mass of most tissueswere already affected. While the magnitude of the differences in warm- and cold-reared pigs were the same (parallel) over the entire range of exposure periods for some measurements (tail length, snout length, total surface area, extremity surface area) most often the differences increased with length of exposure. This may indicate that the tail and snout are at a particularly dynamic stagein their growth during the early part of the study.
Organ size and tissue muss The mass of the various organs and tissues have been measuredin warm- and cold-exposed (or reared) animals of several species(Tables 3 and 4). The results are remarkably similar even though the studies differ in the size and age of animals used, and the temp and length of exposure. That is, the heart, liver, kidneys thyroid and adrenals were larger in cold-exposed and smaller in warm-exposed animals than in controls. Barnett and Widdowson (1965) also showed that the weight of the stomach, small intestine and large intestine were larger in cold-exposed mice, and Baker and Ashworth (1958)showed the pancreasto be larger in cold exposed rats. In contrast, total body fat, nitrogen and skeletal muscle mass were less in coldexposedthan in control animals. The effect of environmental temp on spleen mass was variable. Lung mass was found to be unaffected by temp (Heroux and Gridgeman, 1958). Besides the effect of cold-exposure per se, the differences in organ weights could be due to the differences in the level or frequency of food intake. Certainly, all of these organs are involved in the processing of the food eaten. That is, in digestion, transport of nutrients and wastes, or elimination of wastes. Widdowson and McCance (1960) found that the heart, liver, stomach and small intestine were larger in rats which were overfed than in rats which were terminated at the same weight but which were fed less
0
/
FAT FREE
MUSCLE
/ I....I... OO
5
)....A 10
15
BODY WEIGHT (KG)
Fig. 8. The relation of total musclemass(top) and fat-free musclemass(bottom)to total body massin warm- (m) and cold-reared(0) pigs.
Rat Peromyscus Rat Rat Mouse Rat Rat Ground squirrel Pig Hamster Pig Pig Peromyscus
Mouse Mouse Mouse Mouse MO”%
Species 28-32 28-32 28-32 28-32 31-33 35 30 35 32 34-35 33 28 30 35 35 33 35
13-23 13-23 13-23 13-23 21-27
28
15 24 25 24-26 22 18 25 23 20 23 24
Exoosure Temp”C A A A A A
140 140 140 140 140 210 A Natural population 5748 A A 3@36 45 A 150 A 18 A A 56 A 60 A 72 GSR 41 A 60 A
Food
Duration (days)
-
-
:
35y76 variable -
3-59 young 100 g
48:60 Y-a a Y
O-210 -
&140 Cl40 O-140 Cl40 a -
-
+ + + + +
+
+ +
+
+ + + +
-
A, ad libitum; GSR, grown at same rate; RT, room temp; a, adults; y, young; +. larger; 0, no difference; -, smaller
Sundstroem (1922a) Sunstroem (1922b) Sunstroem (1922~) Sundstroem (1930) Ogle (1934) Herrington and Nelbach (1942) Sealander(1951) Heroux and Hart (1954) Young and Cook (1955) Michie and McLaren (1956) Hale et al. (1959) Vacek et al. (1961) Pohl and Hart (1965) Fuller (1965) Cassuto and Chaffee(1966) Weaver and Ingram (1969) Sugahara et 01.(1970) Roberts and ChaiTee(1976)
References
+
0
+
+ +
-
+
-
A00
Table 3. The effects ofexposing animals to hot as compared to thermally neutral environments on the size of their organs and tissues
-
0
-
-
-
-
-
-
+
+
+
-
+
% 6 3 C ‘ I 3 2 5 s 0 3 E E. R 5’ -a e. B
MARTHA I?. HEATH
70 +
+ +
+
++
+ I
0 +
0 +
+-I-
i-
L., -t
0
0
I
0
+
+
+
++
-t
+++c
+0
++
0
+
f-i-
+
-I-
++
+
+
+
++
+
+
+ +
+
+
0
Effectsof temperature on organ size in pigs Other organs, which increase in size at a rate correlated with the increase in body weight, showed greater differences in the larger pigs which had been exposed to the respective environments for longer. The length of the small intestine showed the greatest increase in length during the early stages ofexposure as if there is a shorter period of time when intestinal growth is most influenced by rearing-temp or level of food intake.
71
Heroux 0. and Schonbaum E. (1959) Comparison between seasonaland thermal acclimation in white rats. III. Studies of the adrenal cortex. Can. J. Biochem.Physiol. 37, 12551261. Herrington L. P. and Nelbach J. H. (1947) Relation of gland weights to growth and aging processesin rats exposed to certain environmental conditons. Endocrinology 30, 375386.
Holeckova E., Baudysova M. and Michl J. (1974) Effect of acclimation to cold on rat kidney growth in uiuo and in vitro. Physiol. Biochem.23, 97-100. Hosslin H. V. (1888) Ueber die ursache der scheinbaren Acknowledyements~I thank Mr Frank Pluck for assistance abhangigkeit des umsatzesvon der grosseder korperoberin the dissection of the pigs, Dr Hector Dott for use of his flache. Archs Physiol. 11,323-379. Image Analyzer and MS Kein Wan for typing the manuscript. Huestis R. R. (1931) Seasonal pelage differences in PerI am also indebted to my Ph.D. Supervisor, Dr D. L. Ingram, omyscus.J. Mammal. 12, 372-375. for his advice during this study. Ingram D. L. and Weaver M. E. (I 969) A quantitative study of the blood vesselsof the pig’s skin and the influence of environmental temperature. Anat. Rec. 163, 517-524. Kennedy G. C. (1957) The effect of gas on the somatic and REFERENCES visceral responseto overnutrition in the rat. J. Endocr. 15, Baker D. Cl. and Ashworth M. A. 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MAKTHA E. HEATH
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