Seasonal changes in temperature acclimatization of the house sparrow, passer domesticus

Comp. Biochem. Physiol., 1970, Vol. 33, pp. 559 to 578. PergamonPress. Printed in Great Britain

SEASONAL CHANGES IN TEMPERATURE ACCLIMATIZATION OF THE HOUSE SPARROW, PASSER DOMESTICUS* L. B R U C E B A R N E T T ~ Department of Zoology, University of Illinois, Champaign (Received 10 May 1969)

A b s t r a c t - - 1 . Lower limits of temperature tolerance in acclimatized house sparrows was greatest in January (-25°C) and least in August (0°C). The loss of tolerance was gradual in the spring (3°C/month), but the gain in tolerance was rapid in the autumn (6°C/month). 2. The weight of body feathers increased 70 per cent following molt which coincided with a gain in cold tolerance of 12°C, 3. The birds were significantly fatter and the fatty acids more unsaturated in the winter than in the summer. 4. Oxygen consumption of brain and muscle tissue in vitro increased in the winter while that of liver tissue declined. INTRODUCTION BIRDS and m a m m a l s that are p e r m a n e n t residents in t e m p e r a t e climates prepare for the stress of winter by making a n u m b e r of physiological and morphological changes referred to as acclimatization (Hart, 1957; West, 1962; Helms, 1968). T h i s study of the house sparrow was undertaken in order to concentrate on some of the m o n t h - b y - m o n t h changes in acclimatization to cold t h r o u g h o u t an entire year. T h e principle objective was to correlate m o n t h l y changes in the lower limit of t e m p e r a t u r e tolerance with changes in insulation, fat reserves, and tissue metabolism. LOWER L I M I T S OF TEMPERATURE TOLERANCE T h e house sparrow has been found to be able to extend its limit of tolerance f r o m 0°C in the s u m m e r to - 3 5 ° C in the winter (Kendeigh, 1949; Davis, 1955). Starlings (Sturnus vulgaris), pigeons and evening grosbeaks (Hesperiphona vespertina) also have a greater cold resistance during the winter (Hart, 1962). * This work is based on a thesis submitted in partial fulfilment of the requirements for the Doctor of Philosophy degree in Zoology at the University of Illinois. The project was supported with funds from the National Science Foundation through grants awarded to Dr. S. Charles Kendeigh. t Present address: Biology Department, Waynesburg College, Waynesburg, Pennsylvania 15370. 559

560

L. BRUCE BARNETT

Procedure House sparrows were captured at night during the first week of each month at a duck farm near Champaign, Illinois. T h e y were kept in a large outdoor aviary (2 × 2'3 x 2.2 m) until they were used in the experiments. These birds experienced an initial weight loss of 1-2 g but regained this weight within a week. Groups of 10-20 birds were taken from the aviary, weighed and placed in individual cages (31 × 16 × 30 cm) out-of-doors for 4-8 days. There was a permanent weight loss of 1-1 g (range = 0"2-1"7 g) in becoming habituated to these experimental cages. T h e y were supplied with food (University of Illinois chick starter mash No. 521) and water or snow ad lib. Birds which did not maintain their weight were not used in the experiments. For each experimental temperature, a group of 4-10 birds was transferred directly from out-of-doors into the cold cabinet. T h e y were placed in cages equipped with microswitches (Martin, 1967) which were connected to a 20-point Esterline Angus strip chart recorder in order to record daily activity and the time of death. T h e time clock was set for the mean photoperiod of the month plus a 40-rain total "twilight" of very reduced illumination ( < 1 fc, 7½ W). T h e cabinet temperature was set at near the suspected tolerance limit of the birds for that month. T h e birds were weighed in the morning at the start of the experiment and on every third day thereafter, with the experiment ending on the sixth day. Lack of tolerance was evidenced by death or failure to maintain constant weight ( _+0'5 g) between weighings. Two, three and sometimes four different groups of birds were used each month over a range of temperatures in order to bracket the 50 per cent level of mortality (LO~0). The LD~0 was determined by plotting the per cent mortality vs. temperature and observing where the plotted line crossed 50 per cent. During the late summer when juveniles became abundant in the collection, they were tested simultaneously but separately from the adults. The sex ratio of both juveniles and adults was maintained as close as possible to 50 : 50. A chi-square test showed no difference in lethality between the sexes. T h e level of significance was set at 0"05 for all statistical tests unless indicated otherwise. Results and Discussion A d u l t b i r d s h a d least t o l e r a n c e to c o l d d u r i n g A u g u s t a n d S e p t e m b e r (0°C) a n d g r e a t e s t t o l e r a n c e d u r i n g J a n u a r y ( - 2 5 ° C ) (Fig. 1). J u v e n i l e s w e r e less t o l e r a n t t h a n a d u l t s d u r i n g A u g u s t a n d S e p t e m b e r . T h e loss o f t o l e r a n c e b e t w e e n J a n u a r y a n d S e p t e m b e r was m o r e g r a d u a l ( 3 ° C / m o n t h ) t h a n t h e gain of t o l e r a n c e f r o m S e p t e m b e r to J a n u a r y ( 6 ° C / m o n t h ) . T h e g r e a t e s t i n c r e a s e in t o l e r a n c e (12°C) c a m e w i t h t h e t e r m i n a t i o n of m o l t . T h e LOs0 for O c t o b e r is o n l y an a p p r o x i m a t i o n b e c a u s e of t h e v a r i a b i l i t y in t h e a m o u n t o f m o l t b e t w e e n i n d i v i d u a l s a n d also b e c a u s e o f t h e falling t e m p e r a t u r e d u r i n g t h e m o n t h w h i c h r e s u l t e d in rapid acclimatization of the birds. T h e y e a r 1967 in t h e locality of t h i s s p a r r o w p o p u l a t i o n was t h e t h i r d c o l d e s t in t h e p a s t 40 years. T h e s u m m e r m e a n t e m p e r a t u r e (21.9°C) was 1.1 ° b e l o w n o r m a l ( I l l i n o i s S t a t e W a t e r S u r v e y W e a t h e r S u m m a r y for C h a m p a i g n - U r b a n a ) . T h e l o w e s t t e m p e r a t u r e r e c o r d e d was - 2 5 ° C on 1 J a n u a r y 1968, w h i c h was t h e s a m e as t h e l o w e r l i m i t of t o l e r a n c e for t h a t m o n t h . T h e c o l d w e a t h e r l a s t e d several d a y s a n d d e a d w i l d b i r d s w e r e n o t i c e d a r o u n d t h e U n i v e r s i t y , b u t n o n e of t h e b i r d s in t h e a v i a r y died. T h e b a r n s w h e r e t h e s p a r r o w s r o o s t e d w e r e o p e n a n d u n h e a t e d in t h e w i n t e r t h u s t h e t e m p e r a t u r e i n s i d e was a b o u t t h e s a m e as outside. H o w e v e r , t h e b i r d s h a d an a m p l e s u p p l y o f d u c k feed, t h e y w e r e p r o t e c t e d f r o m

561

SEASONAL ACCLIMATIZATION I N THE HOUSE SPARROW

the wind and most of them roosted in insulated cavities where they probably lost less body heat (Kendeigh, 1961). The maximum tolerance limit of the experimental birds in the winter ( - 25°C) was not as low as has been reported before ( - 3 5 ° C , Kendeigh, 1949). Kendeigh lowered the temperature stepwise over a period of several days, thus acclimating the birds and increasing their tolerance limits about IO°C. 25

15 I0 (.,.) o

5 0 -5

E I--

-I0 -15 -20

~'°~

-25 ~-

-30

F

_

I

M

]

A

l

M

[

d

'~

d

Molt

I

A

I

S

[

0

i

N

D

d

FIG. 1. Lower limits of temperature tolerance (LDs0) for the house sparrow in central Illinois (O adults; • juveniles), mean monthly temperature (A), and lowest minimum temperature (©). At temperatures near the lower limit of tolerance many of the birds had short periods of activity during the night, and all of the birds were active 1-3 hr before the lights came on in the morning. Weighing of the food containers showed that they were consuming 1-2 g or 10-20 per cent of their daily food intake during the night. Nocturnal feeding and activity was not observed in birds at moderate temperatures, and diminished in those cold-stressed birds which maintained their weight. A similar feeding pattern has been observed in wild house sparrows during the winter (Beer, 1961). At average daily temperatures below - 20°C birds arrived at an outdoor feeding station well before sunrise or as soon as it was light enough to see, and some birds did not leave until after sunset. This activity decreased as temperature ameliorated. Thus it appears that house sparrows alter their feeding patterns in order to survive cold stressful conditions. The extent to which they feed at night apparently depends on how well they can see or are familiar with their surroundings.

562

L. BRUCEBAaNETT

T h e cumulative per cent mortality of the experimental birds was plotted against log time to death each month. It was found that two different curves or responses were occurring (e.g. Fig. 2). At extreme temperatures the curve was broken into two linear segments. Such lines reflect two conjoining log-normal distributions, thus two separate causes of death could be operating (Tyler, 1966). T h e rapid death on the first day at extreme low temperatures may be due to the direct effects of cold shock causing a failure of the respiratory center (Randall, 1943). Death occurring Day I 98

2

I

3

4

5

G

1 / 1 1

95--

7

90-8070--

.~ 60-~ 50~ 40 n

50

U /

! /

10

5

2 I 5O0

l l l I000 l Time to

r

~ ~ i'

death,

',J

I0,000

rain

FIG. 2. Cumultative per cent mortality plotted against log time to death for November birds at 70 per cent ( - 20°C) and 100 per cent ( - 25°C) lethal temperatures. One day = 1440 min. The lines are fitted by eye and show the two different slopes which occurred at more extreme temperatures. on subsequent days was preceded by a steady loss of weight (4-6 g) indicating a progressively severe negative energy balance and starvation. T h e break in the mortality line was not evident at less extreme but still intolerable temperatures suggesting that most of the deaths were due not to shock but to an inability to maintain an energy balance. F r o m the mortality records kept for the duration of the study, it was observed that winter birds were able to withstand the initial shock of the cold better than summer birds since only 19 per cent of the winter birds died on the first day compared to 49 per cent of the summer birds.

SEASONAL ACCLIMATIZATION I N THE HOUSE SPARROW

MORPHOLOGICAL

563

ASPECTS OF ACCLIMATIZATION

F e a t h e r s p l a y an i m p o r t a n t role in s e a s o n a l a c c l i m a t i z a t i o n . K e n d e i g h (1934) n o t e d a 29 p e r c e n t i n c r e a s e o f w i n t e r o v e r s u m m e r f e a t h e r w e i g h t s in t h e h o u s e s p a r r o w , a n d W e s t (1960) f o u n d a 25 p e r c e n t i n c r e a s e in t h o s e o f t h e t r e e s p a r r o w (Spizella arborea). V e g h t e (1964) c a l c u l a t e d t h e p l u m a g e a n d t i s s u e i n s u l a t i o n o f t h e g r a y j a y (Perisorez~ canadensis) a n d f o u n d t h a t b o t h c o m p o n e n t s i n c r e a s e d in t h e w i n t e r season. Many small birds have conspicuous winter augmentation of their body weight a n d fat r e s e r v e s ( K i n g & F a r n e r , 1966; H e l m s , 1968). I t h a s also b e e n p o s t u l a t e d t h a t a m o r e u n s a t u r a t e d fat, w h i c h h a s a l o w e r m e l t i n g p o i n t , m a y b e a v a i l a b l e in c o l d w e a t h e r ( P r e c h t et al., 1955).

Procedure T h e house sparrows used for carcass analysis were weighed and banded the evening they were captured, approximately 3 hr after sunset. T h e y were kept overnight indoors in a loose bag to curtail activity and then reweighed in the morning before sacrificing. This was done to assure that the alimentary canal was empty. T h e birds were plucked and the feathers separated into flight feathers (remiges and rectrices) and body feathers. T h e feathers were dried under a vacuum for at least 18 hr at 40°C and then weighed in tightly covered plastic cups. T h e carcasses were frozen, cut up and freeze-dried at least 24 hr at room temperature. After determining the dry weight, the specimens were homogenized in a Waxing blendor with methanol. T h e homogenate was filtered twice and then submitted to extraction with refluxing petroleum ether for 24 hr (Salee, 1958). T h e amount of body fat was determined as the loss of weight of the carcass homogenate. T h e per cent nitrogen (% N) of the carcasses was determined by the standard Kjeldahl method. Seasonal differences in fatty acid composition of the lipids were investigated for August and January. T h e methanol and ether extracts were combined and transesterified by refluxing for 3 hr with anhydrous methanol containing 1 per cent (v/v) sulfuric acid (American Oil Chemists' Society, 1966). Gas-liquid chromatography was performed with a Varian Aerograph 600D chromatograph equipped with a 7{-9 ft (2"3-2-7 m ) x ~ in. (3"175 mm) o.d. copper column packed with 15 % diethylene glycol succinate ( D E G S ) on acid-washed chromosorb W. T h e column was kept at 180°C and the nitrogen flow rate was held at 80-100 ml/min. Qualitative identification of fatty acid esters was achieved by comparison of relative retention times with a series of standards (James, 1960).

Calculations T h e wet weight (WW) used in calculating the body percentages was the live weight taken in the morning following capture. T h e total amount of body water (TW) was determined b y subtracting the weight of the dried carcass plus dried feathers from the morning wet weight. T h e weight following fat extraction is referred to as the lean dry weight (LDW), and the loss in carcass weight after extraction constitutes the total body fat (TF). T h e protein content was calculated by % N x 6"25 x L D W , and the residue was considered to be carbohydrate and ash. T h e percentages of the various components were calculated on a wet weight basis, and the lipid index values were calculated as L I = T F / L D W . Differences between months, ages and sexes were analyzed with one-way and two-way analyses of variance, and Duncan's new multiple range test with Kramer's modification was used to determine between which months the differences occurred (Steel & Torrie, 1960). Regression and correlation analyses were used for comparing changes in body components. T h e iodine value as an index of unsaturation was calculated from the per cent of the various fatty acids present (Zar, 1967).

564

L. BRUCEBARNETT

Results and Discussion The total body wet weights were highest in the spring months (Table 1), but not significantly higher than during the winter months. The birds were significantly lower in weight during the late summer months. Davis (1955) also found a peak weight in April and a low in September for the house sparrow. Body weight increased in the fall at a rate of about 0.5 g/month until the high winter weight was reached in January. All of the body components had significant differences between months but not between sexes except during the breeding period of late March and April when females were fatter (0.4 g). Juveniles were significantly lighter in June through August and consequently were excluded from the data presented. In the months of September through December juvenile weights were pooled with those of adults.

Nonfat body components Since the house sparrows' bodies were 63-66 per cent water, the correlation between wet weight (WW) and water content (TW) was very high (r = 0.91), and the regression of water on body weight was linear (TW = - 0.93 + 0-66 W W + 0.52). However, the percentage of water in the body did not change with body weight. The percentage of lean-dry weight was significantly correlated with body weight (r = 0.87) and with body water (r = 0.73). Therefore, even though the basic size of the birds varied from month to month, the nonfat components were stable in relation to each other.

Body fat The total amount of fat on the birds was significantly greater in the winter months (1.8 g, L I = 0.28) than in September and October (1-3 g, L I = 0.22). These values are lower than have been reported for similar-sized species (King & Farner, 1966; Helms et al., 1967) because the sparrows were killed after fasting through the night while the other species were killed during the mid-afternoon, which is the time of highest body weight and fat deposition (Helms & Drury, 1960; Kontogiannis, 1967). Carcass analysis of some house sparrows killed in the evening as compared to morning-killed birds indicated that about 1 g of fat was lost during the night under confined conditions. If this amount is added to that shown in Table 1, the amount of fat on house sparrows in the evening (2.3-2.8 g, L I = 0.39-0.44) is comparable to some species (e.g. Zonotrichia leucophrys and Acanthis sp.), but low compared to others (Z. albicollis and Dendroica coronata) (King & Farner, 1966). The magnitude of fat deposition may depend on the feeding habits of the birds and the availability of food as well as the temperature and season. The increase in fat that the house sparrows experienced in the winter was negatively correlated (r = - 0 . 4 , T F = 1-95-0.01T_+0-27, P < 0 . 0 5 ) with the mean ambient temperature for the week prior to their collection. The negative correlation of total body weight with temperature (r = - 0.2, WW = 2 7 . 9 - 0-03T _+1"51) was not significant (0-05 < P < 0-1), however, which indicates that changes

9

10

10

8

7

9

7

16

15

9

10

10

8 February

28 March

18 April

3 May

30 May

1 July

2 August

31 August

2 October

3 November

1 December

3 January

29-7-+0.5

29"1+0"6

28"9-+0"5

28"6-+0.5

27.8+0.4

29.0_+0.5

28.1 +0"7

30"4_+0.7

29"5 +0"6

30"7+0-5

29"7+0"6

29"3+0"5

29"0+0"6

27"7+0'5

27"1_+0'6

27-2_+0-4

26"3_+0"4

25.1+0.3

26.4+0.5

26.1 +0.7

27.8+0.7

27"4+0"6

28"2+0.4

27"3+0"6

27"1+0"4

26"7+0"6

Morning 16"8_+0"4 (62.8) 17"1_+0"3 (63"1) 17"4+0"4 (63"5) 18"3 +0"4 (64"9) 18"1 -+0-5 (65"9) 17.9_+0.4 (64.6) 17.2-+0.5 (65 "6) 17.4+0.3 (65.6) 16-5+0.3 (65.8) 17"0+0"3 (64.6) 17"4+0"3 (63-8) 17.2+0.4 (63 "4) 17"7+0"3 (63-8)

Water

* Mean + S.E.

Figures in parentheses are the per cent of the morning wet wt.

10

5 January

Evening

Wet wt.

1"78_+0.08 (6"7) 1"78_+0.07 (6"6) 1-57+0-10 (5"7) 1"61 +0"09 (5"6) 1"59+0.06 (5"8) 1.68+0.21 (6-0) 1.53 +0.06 (5.9) 1"46-+0.09 (5"5) 1"30-+0.05 (5-2) 1"32+0.06 (5"0) 1"56_+0"05 (5"7) 1"66_+0.13 (6"2) 1"57-+0.07 (5 "6)

Lipids

0"24

0"26

0"25

0.22

0.22

0.24

0.26

0.25

0"26

0"24

0"24

0-28

0"28

Lipid index 6.27+0.15 (23.5) 6"32_+0.09 (23.3) 6"56+0-15 (24"0) 6"61 +0"11 (23-4) 6"03 +0"16 (22.0) 6.57+0.18 (23.6) 5.96-+0.17 (22.8) 6.18+0.11 (23-4) 5.85+0.08 (23-3) 6'03+0"10 (22"9) 6-28_+0"10 (23.1) 6"33_+0"13 (23 "4) 6'57-+0"13 (23 "7)

Lean-dry wt.

1"43+0"03

1"43+0'04

1.50+0.02

1.53-+0.04

1.02-+0.09

0.90+0.07

0.98-+0.05

1.20+0.06

1"22_+0"05

1"22_+0'01

1"41+0"04

1.39+0"02

1"40+0'04

Body

Flight

0"46+0.01

0"46_+0.01

0"46_+0.01

0"44-+0"01

0"39+0.01

0"44-+0.02

0.47_+0.01

0"47+0.01

0"47_+0"01

0"46+0"01

0"47+0"01

0"48+0"01

0"48+0"01

Feathers

CONSTITUENTS OF WILD HOUSE SPARROWS I N GRAMS.* A L L COMPONENTS WERE SIGNIFICANTLY DIFFERENT ( P < 0 " 0 5 ) BETWEEN MONTHS

No.

1--BODY

Date

TABLE

0

>

o

z

> ,q

N

> ¢)

z

>

566

L. BRUCEBARNETT

in fat content are so small as not to affect morning weight appreciably. These data indicate that house sparrows are not exceptionally fat in the winter which may be a result of their close association with man and the ease with which they can obtain food. Chromatographs of the lipid methyl esters from the body fat revealed that there was a significant seasonal decrease in stearic (18 : 0) and linoleic (18 : 2), and an increase in oleic (18 : 1) and docosahexanoic (22 : 6) (Table 2). More importantly, the total amount of unsaturation as expressed by the iodine value was significantly greater in January than in August. This means that during the colder winter months some if not all of the body fat has a lower melting point and thus is more easily mobilized in cold weather. Some mammals have been found to have more unsaturated fat in their extremities and surface layers where their temperature T A B L E 2 - - R E L A T I V E AMOUNTS AND THE MEAN IODINE VALUE OF THE COMMON ( < 1 PER CENT) FATTY ACIDS OF HOUSE SPARROWS CAPTURED IN A U G U S T AND JANUARY

% in mixture ( + S.E.) c : d*

Fatty acid

August

January

16 : 0 16 : 1 18 : 0 18 : 1 18 : 2 20 : 4 22 : 6

Palmitic Palmitoleic Stearic Oleic Linoleic Arachidonic Docosahexaenoic

27.80 + 0"46 7"08 + 0"35 13'83 + 0"99 29.88 + 1"04 15.78+0-36 3"78 + 0"29 1-83 + 0.22

26"32 + 0"50 6.97 +0.40 10"95 + 0"38 t 35"08 + 1"39t 11-47+0"79t 4'88 + 0"58 4'32 + 0'41t

Mean iodine value

80"55 + 0"80

92"81 + 2"45t

d = Number of carbon atoms : number of double bonds. t Significant difference (P< 0"05) : between months. * c :

is not as high as the core temperature of the body (Dean & Hilditch, 1933 ; Irving et al., 1957; K o d a m a & Pace, 1963, 1964), but similar changes in the tissues of birds have not been reported. Zar (1967, and personal communication) investigated the fatty acids from the brain, liver, breast muscle, heart, feet and adipose tissue of cold-acclimated house sparrows but found no change in saturation in response to relatively short-term cold treatment. Bower & Helms (1969) found a shift to a more unsaturated condition from November to April in the slate-colored junco (Junco hyemalis), but they attributed it to changes in diet and not to changes in temperature.

Feathers T h e weight of the feathers was lowest in August at the start of molt and highest in October as molt was ending. T h i s 70 per cent increase may account for m u c h of the increased cold tolerance observed in the birds. T h e gradual loss and wear

567

SEASONAL ACCLIMATIZATION I N THE HOUSE SPARROW

of feathers in the spring may also explain why cold tolerance was not lost as rapidly as the rise in environmental temperature.

Effects of cold stress In order to assess the effects of cold stress on body composition, a sample of 8 wild birds killed in the morning and 8 cold-stressed birds which had died in the cold cabinets was analyzed during July and October (Table 3). There was no significant difference between months, but the cold-stressed birds were significantly lower in water (12.8 per cent), fat (52.8 per cent), protein (16.9 per cent) TABLE 3 - - C A R C A S S

Treatment Wild(g) Cold stressed (g) Difference (g) Probability

COMPOSITION OF 8 W I L D AND 8 COLD-STRESSED HOUSE SPARROWS

Wet wt. 26.3+0.5

Water

17.2+0.4 (65"5) 22"6_+0'8 15"0+0"6 (66"4) - 3"7 - 2"2 < 0"01 < 0'05

Lipids

Protein

Carbohydrates, ash

1.42+0.12 4.68_+0.11 1.26_+0.05 (5'4) (17"8) (4"8) 0"67-+0"03 3"89+_0"19 1"32+_0"13 (3"0) (17"2) (5"8) - 0.75 - 0"79 + 0"06 < 0'01 < 0'01 > 0"05

Mean + S.E. ; per cent of wet wt. are in parentheses. and total wet wt. (14.0 per cent) indicating a starved condition. Only ash and carbohydrate levels were similar. It is interesting to note that not all of the fat was utilized before death occurred. Cold lethal experiments on the field sparrow (Spizella pusilla) (Olson, 1965), dickcissel (Spiza americana) (Zimmerman, 1965) and white-throated sparrow (Z. albicollis) (Kontogiannis, 1968) have also shown some fat remaining on the birds at death (0.26 g TF/11.17 g WW, 0.37 g TF/22.4 g W W and 0.67 g TF/22.0 g WW, respectively). Some of the fat includes the phospholipids which are associated with the membrane structures of the cell. These lipids cannot be utilized for energy without a breakdown in the integrity of the cell (Masoro, 1967). Some of the depot fats may remain in the cells because the neutral fatty acids are mobilized and utilized at different rates in times of stress (Hollenberg & Angel, 1963 ; Kodama & Pace, 1963). This unusable portion of the total extractable fat may amount to 20-30 per cent of the body fat of a bird with 2-3 g of fat depending on the species and the time and method of extraction, and it should not be included when computing the fat available for energy utilization. A house sparrow in the winter with an average of 2.8 g of fat would have about 2 g available during the night for thermogenesis. This amount would yield 19 kcal of energy and would enable the bird to survive 16-17 hr at temperatures of - 2 to - 4 ° C (January existence metabolism = 26 kcal/bird per day; Davis, 1955). The amount of fat needed to survive overnight (12 hr) at room temperature (22°C) can be calculated (19.7 kcal/bird per day; Davis, 1955), and the result (1 g)

568

L. BRUCEBARNETT

agrees with the amount actually found to be used (1 g) thus confirming the accuracy of these estimates. U n d e r extreme cold stress birds can also obtain energy f r o m protein catabolism. T h e cold-stressed house sparrows were about 0.79 g lower in protein than the wild birds, which m a y have been due partly to muscular atrophy incident to caging. However, Kontogiannis (1968) compared caged white-throated sparrows dying f r o m cold stress with caged control birds and found that cold-stressed birds lost about 0.9 g. Therefore, proteins might add another 4 kcal of energy (protein = 4"8 kcal/g) (Kleiber, 1961; p. 125), or roughly 4 hr of survival time. However, this m e c h a n i s m of survival has the danger of weakening the bird so that it cannot fly to feed or escape predators. T h e a m o u n t of protein that wild birds can afford to lose m a y be m u c h less than that of a caged bird. T I S S U E METABOLISM Seasonal metabolic responses of whole birds are well known and, in general, it has been found that their standard metabolic rate is lower in the winter than in the s u m m e r (King & Farner, 1961; West, 1962; Kendeigh, 1969). However, the metabolic contributions m a d e by the various tissues are not understood as well. Liver and kidney tissue metabolism has been studied in growing chickens (Crandall & Smith, 1952) and enzymatic assays of the liver and pectoral muscle have been m a d e on the house sparrow and the white-crowned sparrow under the effects of cold acclimation (Chaffee et al., 1963 ; Chaffee & Mayhew, 1964). Tissue metabolism is understood somewhat better in mammals, especially rats (Weiss, 1954, 1957; H e r o u x & Willmer, 1960, 1962) and hibernators (see Burlington & Wiebers, 1967, for recent literature). T h e oxygen consumption of the brain, liver and pectoral muscle tissues of wild house sparrows was measured throughout the year in order to determine the metabolic responses of these tissues to seasonal fluctuations in t e m p e r a t u r e out-ofdoors. M e a s u r e m e n t s were also made on birds which had been cold-acclimated in order to compare the effects of acclimation with acclimatization. Procedure

Wild house sparrows from which tissues were taken were captured monthly and left in the outdoor aviary until the time of the experiment. The tissue respiration measurements were made during the latter half of each month and one bird per day was used. The measurements were always made in the afternoon to avoid diurnal changes in metabolism. In order to measure the tissue response to cold acclimation, birds were selected which had maintained constant weight in the cold-tolerance tests. Since these tests were conducted over a number of months, the acclimation temperature ranged from - 3 ° C in August to 24°C in December, and the period of acclimation lasted from 1 to 2 weeks. The procedure for measuring the oxygen consumption of the tissues was the same for both out-of-door and cold-acclimated birds. The birds were killed by decapitation, and the cerebral hemispheres, the liver and the right pectoral muscle were quickly excised and placed into ice-cold Krebs-Ringer phosphate solution (Umbreit et al., 1964; p. 132). The brain and liver tissues were sliced with a Stadie-Riggs hand microtome and the muscle fibers were stripped from the inside belly of the pectoralis major (Field, 1948). Enough tissue was obtained for duplicate and sometimes -

569

SEASONAL A C C L I M A T I Z A T I O N I N T H E H O U S E S P A R R O W

triplicate samples. T h e wet weight of the tissue slices was between 50 and 100 rag. T h e y were placed directly into standard Warburg reaction vessels which contained 2 ml of the incubation medium and 0"2 ml of 10% K O H in the center well. T h e incubation medium was a modified Krebs-Ringer phosphate solution with a glucose substrate (Weiss, 1954). T h e gas phase consisted of pure oxygen which was introduced by the evacuation method (Umbreit et al., 1964; p. 68). Blanks containing the above components minus the tissues were also run. Oxygen consumption was measured on a Gilson differential respirometer using an allglass system. T h e temperature at which the determinations were made was 41°C. Following a 10-min equilibration period, readings were taken every 10 rain for 1 hr. T h e tissues were weighed at the end of the run, dried in a vacuum oven at 50°C for 18 hr and then reweighed. T h e respirometry results were expressed in microliters of oxygen consumed per mg dry wt. of tissue per hr (Qo,) and corrected for standard temperature and pressure and the blank. Since there were usually two to three tissue samples per organ, the results were analyzed with a one-way analysis of variance for treatments with subsamples (Steel & Torrie, 1960).

Results The metabolic responses of the tissues were different between outdoor acclimatized and indoor acclimated birds and hence they will be discussed separately. Acclimatization Oxygen consumption was higher in the brain than in the other tissues and increased significantly in the autumn and winter (Fig. 3). The increase was linear

12Brain J~ ~"

IC--

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FIC. 3. Oxygen consumption in vitro of brain, liver and pectoral muscle tissues from outdoor-acclimatized house sparrows. Mean Qo~ values of each tissue are connected together for each month. T h e vertical lines represent + 2 S.E.

570

L. BRUCEBARNETT

with decreasing temperatures at a rate of 1 F1 O2/mg per hr for every 2.3°C drop in m o n t h l y mean temperature (Fig. 4). Liver tissue respiration was significantly higher in the s u m m e r and lower in the winter, but there was considerable variation between months. T h e metabolic 17•

16-

M = I & 8 4 - O . 15T + 1.60 ( r = - 0 . 6 4 )

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FIG. 4. Brain tissue metabolism (M) as a function of mean monthly temperature (T) ( _ S.E. of estimate of M).

tJ-

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as a f u n c t i o n o f a m b i e n t t e m p e r a t u r e to the

experiment.

3 days prior

571

SEASONAL ACCLIMATIZATION IN THE HOUSE SPARROW

rates of the liver tissues were analyzed by a polynomial regression analysis to compare them with mean daily temperatures 3 days prior to the experiment (Fig. 5). The results indicate that, in general, metabolism increases as the environmental temperature increases. This agrees with studies of acclimatized white rats and wild Norway rats which also had higher rates of liver respiration in the summer than in the winter (Heroux & Willmer, 1960, 1962). Endogenous resting metabolism was lowest in the muscles, but the rates for muscle metabolism require cautious interpretation since the error of the respirometer is relatively great (10-20 per cent) at low levels of respiration. There was a significant increase in muscle metabolism in December, and the best-fit regression line of metabolism was for the mean temperature 1 day prior to the experiment (Fig. 6). As the ambient temperature decreased from 20 to 0°C, the respiration of the muscle increased significantly and thus produced more heat for thermoregulation. No physiological explanation can be offered for the marked decline in respiration below zero degrees. However, since the sample size was small, it may have been due to experimental error. 9--

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FIG. 6. M u s c l e tissue m e t a b o l i s m as a f u n c t i o n o f a m b i e n t t e m p e r a t u r e for the day p r i o r to the e x p e r i m e n t .

Acclimation House sparrows that were cold acclimated in the summer months had an increase in their muscle and liver tissue metabolism which was usually significantly higher than that of outdoor birds (Table 4). An exception occurred in August when the livers of the cold-acclimated birds had a significantly lower rate of metabolism than those of outdoor birds. This coincided with a threefold increase in muscle metabolism. The brain tissue did not increase in metabolism in response to the relatively short exposure of cold temperature. These same results have been obtained in experiments with tissues from cold-acclimated rats (Weiss, 1954, 1957). 19

Cold Outdoor Cold Outdoor Cold Outdoor Cold Outdoor Cold Outdoor

Treatment (-10) (6) (-5) (13) ( - 3) (21) ( - 3) (18) (-24) (0)

--3 5 8 12 2 11 6 8

n --11"5+0"3 12"4+0"5 12.6 + 0"6 11-0+0"6 10"5 + 0"3 11-8+0"5 15"2+0-3 13"9_+0"6

Brain ( m e a n + S.E.) --0'05 0"09 0"14 0"18 0"04 0"15 0"05 0-12

C.V. 6 9 4 6 10 17 2 11 8 8

n

ACCLIMATIZED BIRDS

8"1 + 0 " 4 6"7 + 0"5 8"4+0"4* 5"8+0"5 6"6 + 0"4* 8"2+0"3 9-6 + 0'6 8"0+0.7 4"8+0"5 5"8+0'5

Liver (mean-+ S.E.) 0"12 0'22 0"10 0"21 0"17 0"15 0"09 0.28 0"27 0"26

C.V.

4 6 4 6 12 17 3 10 8 8

n

2"4+0"1" 1"3 + 0"1 2"5+0.3* 1"4+0"1 6"5 + 0"8* 3"2+0-4 4"8 + 0"2 3"2+0"4 6"0+0"4 6"0_+0"6

Muscle (mean_+ S.E.)

0-08 0"27 0"21 0"22 0"41 0-53 0"06 0"38 0.19 0"26

C.V.

OF TISSUES FROM COLD-ACCLIMATED HOUSE SPARROWS COMPARED TO OUTDOOR-

* Significant difference b e t w e e n t r e a t m e n t s at 0'05 level.

n = sample size, C.V. = S . D . / M e a n .

December

September

August

July

May

Month

O 2 / m g p e r hr)

Ambient temperature (°C)

TABLE 4--~ETABOLIC RATES (~1

o r~

bo

SEASONAL A C C L I M A T I Z A T I O N I N THE HOUSE S P A R R O W

573

In December, however, the cold-acclimated birds had metabolic rates in the tissues which were not significantly different from those of birds out-of-doors. The brain and muscle tissues had very high rates (Qo~ = 3-4/zl above the summer average) which coincided with the seasonal increase in metabolism. Thus cold acclimation appears to elicit a different metabolic response than acclimatization only in the summer months. Discussion The metabolic adjustments a homeotherm makes in response to decreasing temperatures depends upon whether the exposure to cold was under constant conditions in a laboratory or in fluctuating temperatures out-of-doors (Hart, 1957). Short-time cold acclimation causes an elevation in metabolic rate while long-time acclimation, which includes increased insulation, etc., results in a lower metabolic rate in the winter than in the summer. The results of this study of house sparrow tissues indicated that the differences in response may be true only in the summer. During the winter it appears that the tissues are already operating at maximum efficiency for the cold and, therefore, cold acclimation does not increase metabolism any further. Each tissue makes a varying contribution towards the entire heat production of the body. Jansky (1962) reported that in the golden hamster the muscles contributed 76 per cent, the liver 5 per cent and the brain 3 per cent of the theoretical total metabolic capacity as measured by the cytochrome oxidase activity. Chaffee & Mayhew (1964) found in the house sparrow that the succinoxidase activity per mg of protein was twice as high in the pectoral muscle as in the liver and, since the mass of the muscle is six times greater than the liver, the total succinoxidase activity in the muscle is twelve times that of the liver. The oxygen consumption in muscle tissue slices is characteristically low when measured in vitro with glucose as a substrate. Were the muscle tissue to be stimulated, it would have greater calorigenic activity. The rapid rise in muscle metabolism seen in December may have been a similar quick response to the severe weather which occurred at that time as when placed in the cold cabinet. Since the muscle is the major source of heat production in the body it is important that it be able to increase its calorigenesis whenever the bird is cold-stressed. Even though the liver tissue appears to rank second to the muscle in heat production, its seasonal response is more similar to that of the intact animal, i.e. metabolism is higher in the summer than in the winter. The brain, because of its high rate of metabolism, produces an appreciable amount of heat, but since the head may lose large amounts of heat due to its low insulation, the total heat contribution to the body is uncertain. It has been shown in some mammals that over a period of time heat production changes from shivering to nonshivering thermogenesis. However, in birds, most of the evidence indicates that shivering is the primary source of heat production (Hart, 1962; Chaffee et al., 1963; West, 1965). Noradrenalin, which mediates nonshivering thermogenesis in mammals (Hsieh & Carlson, 1957), failed to increase

574

L. BRUCEBARNETT

the standard metabolism of curarized pigeons (Hart, 1962), chickens (Chaffee et al., 1963), evening grosbeaks and common redpolls (Acanthis flammea) (West, 1965). Young chickens seem to be an exception, however, since their metabolism increased in response to adrenalin (Freeman, 1966). Cold-acclimated mammals also show an increase in some of the oxidative enzymes of the muscles, but Chaffee et al. (1963) failed to find a similar increase in the enzymes of the house sparrow or the white-crowned sparrow. The present study on the house sparrow suggests that nonshivering thermogenesis may be occurring in the liver and muscle tissues of cold-acclimated birds and the muscle and brain tissues of winter-acclimatized birds since these tissues had elevated metabolic rates in vitro. However, more conclusive evidence is needed. Since there is no increase in the oxidative enzymes, increased calorigenesis may come as a result of alternate metabolic pathways being used which provide more heat and less stored energy (Hochachka, 1967). Thyroxine has been shown to stimulate metabolism in the liver and muscles but not the brain of the rat (Barker & Klitgaard, 1952). The thyroid gland of the house sparrow shows seasonal activity in cold regions (Kendeigh & Wallin, 1966) that parallels the increase in tissue metabolism. However, calorigenesis in the normal organism is regulated by a balance of hormonal factors, and the role of any one hormone is not completely known. CONCLUSIONS The process of acclimatization as seen in the house sparrow includes a number of physiological and morphological adjustments which prepare the birds for survival through the cold winter weather. The birds' tolerance to cold, which is indicative of the seasonal change in acclimatization, increases in the autumn and winter when it is needed most, but then decreases gradually in the spring and summer when other life processes make their demands on the energy supplies of the birds. The fact that the loss of tolerance is gradual in the spring while the gain in tolerance is more abrupt in the autumn is adaptive since it anticipates and protects against unseasonally cold weather. The decrease in cold tolerance in the spring is associated with a gradual loss in weight of body feathers, a decrease in fat reserves and lower metabolic rates in the muscle and brain tissues. The abrupt gain in tolerance to cold temperature in October coincided with the end of molt and a 70 per cent increase in body feather weight. Following molt, the continued increase in cold-temperature tolerance in the winter months is associated with elevated metabolic rates in the brain and muscle tissues. This suggests that the tissues can increase their endogenous metabolic capacity over summer levels. The biochemical mechanisms involved in this increase are still uncertain but seem to be associated with an increase in thyroid activity (Kendeigh & Wallin, 1966). Fat serves primarily as an energy reserve, supplying the body with the needed energy during the long nights and in inclement weather. Subcutaneous fat also

SEASONAL ACCLIMATIZATION IN THE HOUSE SPARROW

575

appears to have some limited ability as an insulation (Veghte, 1964). The increased amount of unsaturated fat found in the house sparrow in the winter may make it possible for the bird to mobilize peripheral stores of fat or at least permit proper membrane function in the extremities at cold temperatures. As Hart (1961) pointed out, acclimation to constant cold, which nearly doubles heat production, leads to cold resistance through increased capacity to produce heat. The process is calorigenically expensive and the lasting benefits are doubtful. A much greater economy of energy is seen in animals which acclimatize to cold climates by increasing their insulation and thus conserving heat. The acclimatized bird also has greater fat reserves and lipids which are more functional at lower temperatures, it consumes more food in the wintertime and it can extend its metabolic capacity down to lower temperatures (Kendeigh, 1949; Hart, 1962). SUMMARY 1. The lower limit of temperature tolerance in adult house sparrows was greatest in January ( - 2 5 ° C ) and least in August and September (0°C). The loss of tolerance was gradual in the spring (3°C/month), but the gain in tolerance was rapid in the autumn (6°C/month). The greatest increase (12°C) occurred in October following molt when the weight of the body feathers increased 70 per cent. 2. The birds lost an average of 1 g of fat overnight. The amount of fat on the birds in the morning before feeding was highest in the winter (1-8 g) and lowest in the summer (1.3 g), and was negatively correlated with the monthly mean temperature. The body fat also increased in unsaturation in the winter. 3. Body weight was highest in the spring (28.2 g) and lowest in late summer (25.1 g). The percentage of fat on the body increased with body size, but the percentages of water and lean-dry weight were the same in all birds regardless of total body weight. 4. Cold-stressed birds did not use all of their fat reserves before death occurred. They lost significant amounts of protein which may have served as energy for calorigenesis. 5. Winter-acclimatized birds had higher rates of metabolism in the brain and muscle tissues and lower rates in the liver tissue than summer-acclimatized birds. Cold-acclimated birds, on the other hand, had higher rates of tissue metabolism in the liver and muscles, while the brain had no change in rate. The possibility of nonshivering thermogenesis occurring in isolated tissues is suggested by the increase in metabolism following cold stress. Acknowledgements--I wish to thank Dr. Kendeigh and Dr. Jerrold H. Zar for their advice and assistance. The use of the University of Illinois IBM 7094/1401 computer facilities was made possible by PHS funds made available to the Zoology Department by the University Research Board.

REFERENCES AMERICANOIL CHEMISTS' SOCIETY(1966) Preparation of methyl esters of long-chain fatty acids..7. Am. Oil Chem. Soc. 43, 12A.

576

L. BRUCEBARNETT

BARKER S. B. & KLITGAARDH. M. (1952) Metabolism of tissues excised from thyroxineinjected rats. Am.J. Physiol. 170, 81-86. BEER J. R. (1961) Winter feeding patterns in the house sparrow. Auk 78, 63-71. BOWER E. & HELMS C. (1969) Seasonal variation in fatty acids of the slate-colored junco Junco hyemalis. Physiol. Zool. 41, 157-168. BURLINGTON R. F. & WIF.BERSJ. E. (1967) The effect of temperature on glycolysis in brain and skeletal muscle from a hibernator and a non-hibernator. Physiol. Zool. 40, 201-206. CHAFFEER. R. J., MAYHEWW. W., DREBINM. & CASSUTOY. (1963) Studies on thermogenesis in cold-acclimated birds. Can.J. Biochem. Physiol. 41, 2215-2220. CHAFFEE R. R. J. & MAYHEW W. W. (1964) Studies on chemical thermoregulation in the house sparrow (Passer domesticus). Can.J. Physiol. Pharmacol. 42, 863-866. CRANDALL R. R. & SMITH H. (1952) Tissue metabolism in growing birds. Proc. Soc. exp. Med. 79, 345-346. DAVIS E. A. (1955) Seasonal changes in the energy balance of the English sparrow. Auk 72, 385-411. DEAN H. K. & HILDITCH T. P. (1933) The body fats of the p i g - - I I I . The influence of body temperature on the composition of depot fats. Bioehem.J. 27, 1950-1956. FIELD J. (1948) Respiration of tissue slices. In Methods in Medical Research (Edited by POTTERV. R.), Vol. 1, Sect. IV, pp. 289-307. Yearbook Publishing Co., Chicago. FREEMAN B. M. (1966) The effects of cold, noradrenalin and adrenalin upon the oxygen consumption and carbohydrate metabolism of the young fowl (Gallus domesticus). Comp. Biochem. Physiol. 18, 309-382. HART J. S. (1957) Climatic and temperature induced changes in the energetics of homeotherms. Rev. Can. Biol. 16, 133-174. HART J. S. (1961) Physiological effects of continued cold on animals and man. Br. Med. Bull. 17~ 19-24. HART J. S. (1962) Seasonal acclimatization in four species of small wild birds. Physiol. Zool. 35, 224-236. HELMS C. W. (1968) Food, fat, and feathers. Am. Zool. 8, 151-167. HELMS C. W. & DRVRY W. H. JR. (1960) Winter and migratory weight and fat: field studies on some North American buntings. Bird-Banding 31, 1-40. HELMS C. W., AUSSIKERW. H., BOWERE. B. & FRETWELLS. D. (1967) A biometric study of major body components of the slate-colored junco,Junco hyemalis. Condor 69, 560-578. HEROUXO. & WILLMERJ. (1960) Respiratory rate (Qo,) of isolated liver of white rats exposed to summer or winter outdoor environmental conditions. Can. J. Biochem. Physiol. 38, 1215-1216. HEROUX O. & WILLMER J. (1962) Respiratory rate (Qo,) of liver slices from summer- and winter-captured wild rats (Rattus norvegicus). Can. J. Biochem. Physiol. 40, 687-688. HOCHACVlKA P. W. (1967) Organization of metabolism during temperature compensation. In Molecular Mechanisms of Temperature Adaptation (Edited by PROSSERC. L.), pp. 177203. AAAS No. 84, Washington, D.C. HOLLENBERG C. H. & ANCEL A. (1963) Relation of fatty acid structure to release and esterification of free fatty acids. Am.J. Physiol. 205, 909-912. HSIEH A. C. L. & CARLSON L. D. (1957) Role of the thyroid in metabolic response to low temperature. Am.J. Physiol. 188, 40-44. IRVING L., SCHMIDT-NIELSEN K. & ABRAHAMSENN. S. B. (1957) On the melting point of animal fats in cold climates. Physiol. Zool. 30, 93-105. JAMES A. T. (1960) Qualitative and quantitative detection of the fatty acids by gas-liquid chromatography. Methods Biochem. Anal. 8, 1-59. JANSKY L. (1962) Maximal steady state metabolism and organ thermogensis in mammals. In Comparative Physiology of Temperature Regulation (Edited by HANNON J. P. & VIERECK E.), pp. 175-201. Arctic Aeromed. Lab., Ft. Wainwright, Alaska.

SEASONAL ACCLIMATIZATIONIN THE HOUSE SPARROW

577

KENDEIGH S. C. (1934) The role of environment in the life of birds. Ecol. Monog. 4, 299-417. KENDEIGH S. C. (1949) Effect of temperature and season on energy resources of the English sparrow. Auk 66, 113-127. KENDEIGH S. C. (1961) Energy of birds conserved by roosting in cavities. Wilson Bull. 73, 140-147. KENDEIGH S. C. (1969) Energy response of birds to their thermal environment. Wilson Bull. In press. KENDEIGH S. C. & WALLIN H. E. (1966) Seasonal and taxonomic differences in the size and activity of the thyroid glands in birds. OhiodT. Sci. 66, 369-379. KING J. R. • FARNER D. S. (1961) Energy metabolism, thermal regulation, a n d body temperature. In Biology and Comparative Physiology of Birds (Edited by MARSHALLA. J.), Vol. 2, pp. 215-288. Academic Press, New York. KING J. W. & FARNER D. S. (1966) The adaptive role of winter fattening in the whitecrowned sparrow with comments on its regulation. Am. Nat. 100, 403-418. KLEIBER M. (1961) The Fire of Life. John Wiley, New York. KODAMAA. PACE N. (1963) Cold-dependent changes in tissue fat composition. Fedn Proc. 22, 761-765. KODAMA A. ~¢ PACE N. (1964) Effect of environmental temperature on hamster body fat composition..~, appl. Physiol. 19, 863-867. KONTOGIANNIS J. E. (1967) Day and night changes in body weight of the white-throated sparrow, Zonotrichia albicollis. Auk 84, 390-395. KONTOGIANNIS J. E. (1968) Effect of temperature and exercise on energy intake and body weight of the white-throated sparrow, Zonotrichia albicollis. Physiol. Zool. 41, 54-64. MARTIN E. W. (1967) An improved cage design for experimentation with passeriform birds. Wilson Bull. 79, 335-338. MASORO E. J. (1967) Skeletal muscle l i p i s - - I I I . Analysis of the functioning of skeletal muscle lipids during fasting. ~. biol. Chem. 242, 1111-1114. OLSON J. B. (1965) Effect of temperature and season on the bioenergetics of the eastern field sparrow, SpizellapusillapusiUa. Ph.D. thesis, University of Illinois. PRECHT H., CHRISTOPHERSON J. & HENSEL H. (1955) Temperatur und Leben. Springer, Berlin. RANDALL W. C. (1943) Factors influencing the temperature regulation of birds. Am. ~. Physiol. 139, 56-63. SALEE E. M. (Editor) (1958) Official and Tentative Methods of the American Oil Chemists' Society, 3rd edition. Am. Oil Chem. Soc., Chicago (looseleaf). STEEL R. G. D. ~¢ TORRIE J. H. (1960) Principles and Procedures of Statistics. McGraw-Hill, New York. TYLER A. V. (1966) Some lethal temperature relations of two minnows of the genus Chrosomus. Can. jT. Zool. 44, 349-364. UMBREIT W. W., BURRIS R. H. & STAUFFERJ. F. (1964) Manometric Techniques. Burgess Publ. Co., Minneapolis. VEGHTE J. H. (1964) Thermal and metabolic responses of the gray jay to a cold stress. Physiol. Zool. 37, 316-328. WEISS A. K. (1954) Adaptation of rats to cold air and effects on tissue oxygen consumptions. Am.jT. Physiol. 177, 201-206. WEISS A. K. (1957) Tissue responses in the cold-exposed rat. Am.~. Physiol. 188, 430-434. WEST G. C. (1960) Seasonal variation in the energy balance of the tree sparrow in relation to migration. Auk 77, 306-329. WEST G. C. (1962) Responses and adaptations of wild birds to environmental temperature. In Comparative Physiology of Temperature Regulation (Edited by HANNON J. P. & VIERECK E.), pp. 291-333. Arctic Aeromed. Lab., Ft. Wainwright, Alaska. WEST G. C. (1965) Shivering and heat production in wild birds. Physiol. Zool. 38, 111-120.

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ZAR J. H. (1967) Temperature-induced changes in the fatty-acid composition of the brain and muscle of the house sparrow, Passer domesticus. Ph.D. thesis, University of Illinois. ZIMlVmmVIANJ. L. (1965) Carcass analysis of wild and thermal-stressed dickcissels. Wilson Bull. 77, 55-70. Key Word Index--Acclimatization; house sparrow; cold tolerance; insulation; fat deposition and changes in saturation; tissue metabolism.