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Metabolic adaptation to local climate in birds
Camp. Biochem. Physiol., 1974,Vol. 48A, pp. 175to 187.Pergnmon Press. Printed in Great Britain
METABOLIC
ADAPTATION TO LOCAL BIRDS*
S. CHARLES
and
KENDEIGHl
CHARLES
CLIMATE
IN
R. BLEM2
‘Department of Zoology, University of Illinois, Champaign, Illinois 61820, and 2Department of Biology, Virginia Commonwealth University, Richmond, Virginia 23220, U.S.A. (Received
1 June
1973)
Abstract-l. Existence metabolism in house sparrows, Passer domesticus, collected at nine North American localities, varies inversely with mean midwinter and mid-summer temperatures of collection sites at rates of 0.0036 and 0.0041 kcal g-l day-’ ‘C-l, respectively. 2. Behavioral responses and improved insulation during the winter provide further adaptation to cold climates at rates of 0.0019 and 0.00012 kcal g-l day-’ ‘C-l, respectively. 3. Within the range of collection sites, ultimate minimal existence metabolism decreases southward, while upper critical temperatures predicted from these values increase. 4. Ultimate maximum existence metabolism and lower limits of temperature tolerance increase northward with drop in winter temperature and constitute the critical metabolic characteristics that enable the species to be permanent residents at the collection sites. 5. Maximum and minimum existence energy values and ultimate lower limits of temperature tolerance are used to construct a graphic physiological model for the distribution of house sparrows in North America.
INTRODUCTION THE WIDE distribution
logical
and other
moderate Arctic
adaptations
climates.
with
its
house
sparrow,
Churchill,
for surviving
to the tropics
and reproducing
If the class Aves originated
great
resources and other tions in physiology, the adjustments
of birds from the Arctic
seasonal
fluctuations
presupposes in extreme
in the tropics,
in temperature,
factors must have required progressive behavior and even morphology. Even
physioas well as
dispersal
into the
photoperiod,
food
evolutionary adaptamore remarkable are
that must have been made to enable a single species, such as the all the way from Passer domesticus, to occur and reproduce
in northern
Manitoba
on the
Hudson
Bay,
to southern
Mexico
and
Guatemala. This is particularly striking considering that the species was introduced into North America from Europe within only the last 125 years. * The research for this paper was supported in part by grants from the National Science Foundation. 17.5 7
176
S. CHARLESKENDEIGH AND CHARLESR. BLEM
It is well known that cold-blooded forms compensate for lower ambient temperatures by maintaining a higher rate of metabolism than their relatives in warmer climates (Bartholomew, 1972). Warm-blooded birds and mammals, however, are supposed to adapt to cold by improving their body insulation rather than adjusting their rate of metabolism (Scholander et al., 1950). Doubt that this was entirely true is raised by Hudson & Kimzey’s (1966) finding that house sparrows from three northern localities in the United States had a higher rate of standard metabolism than did birds from Texas, by Trost’s (1972) study of the horned lark, Eremophila alpestris, which showed that a hot desert subspecies maintained a lower metabolic rate than did another subspecies from a milder climate, and by Dawson & Bennett’s (1973) finding that desert species of pigeons and doves have lower metabolism than species from cooler regions. The present study with the house sparrow is to investigate this problem on a wider scale. The manner in which adaptation occurs within this species may reflect also the manner in which other species have become adapted to different climates, especially to temperature, at different latitudes in the northern hemisphere. ANALYSIS
Existence metabolism The rate of existence metabolism was measured in samples of live house sparrows obtained from nine localities in the United States and Canada (Blem, 1973). Existence metabolism is the amount of energy required by caged birds to maintain constant weight over a period of days. It is measured by the amount of food actually metabolized (caloric content of food ingested minus calories in excreta). Included as components of existence metabolism are basal metabolism, suprabasal tissue metabolism for body temperature regulation, the heat increment of feeding and the energy requirements for the minimal locomotor activity permitted by the small cages. Existence metabolism was measured over the whole range of ambient temperatures tolerated by the birds, and regression line equations were obtained for each locality (Table 1). Existence metabolism determined in this manner does not include energy requirements for free existence, reproduction, molt or other activities of free-living birds but is comparable from one locality to another. The “measured” existence metabolism (M = kcal g-l day-l) for mid-summer (average for June, July and August) and for mid-winter (average for December, January and February) were calculated from the equations (Table 1) using the monthly normal mean temperatures (t = “C) at each locality (Tables 2 and 3). For those localities where regression lines were obtained for one season only, values for the missing season were calculated, allowing for seasonal acclimatization. Seasonal acclimatization in terms of the whole bird (kcal/bird-day) was obtained using a correction factor of - 1*0+0*05t for the winter, and + l-O-0*05t for the summer (Kendeigh, 1973). All equations in this paper, however, are given in terms of specific weight (g) since Blem (1973) found that individual weight of birds varied positively with latitude (temperature).
METABOLIC ADAPTATION TO LOCALCLIMATEIN BIRDS
177
TABLE I-EXISTENCE METABOLISM EQUATIONS FOR SAMPLESOF HOUSE SPARROWS COLLECTED DURING MID-SUMMER (S) OR MID-WINTER (W) AT NINENORTH AMERICANLOCALITIES Regression equation Location
(t = “C)
____
kcal g-l day-i =
Churchill, Manitoba (S) Winnipeg, Manitoba (W) Winnipeg, Manitoba (S) Duluth, Minnesota (S) St. James, Minnesota (W) Monticello, Illinois (W) Monticello, Illinois (S) Amarillo, Texas (W) Amarillo, Texas (S) Flagstaff, Arizona (S) Tucson, Arizona (W) Vero Beach, Florida (W) Vero Beach, Florida (S)
1~05-O~Ol5t 0~98-O~Ol3t 0~92-0~005t 1~10-0~018t 0~98-OOll t 0~95-0~012t 1~00-0~013t 0.97-0.014t 1~02-0~014t 1~13-0~018t 0.92-0.012t 0~95-0~014t 0~95-0012t
TABLE ~-STATISTICAL DATAFOR FOR MID-WINTERENERGETIC~ OF THE HOUSESPARROWAT
NINE NORTH AMERICAN LOCALITIES
Ultimate limit of tolerance (“C)
Ultimate maximum potential (kcal g-’ day-‘)
Measured
Expected
- 25.3
- 31.4
1445*
1.360*
I.274
+0.086
- 15.9
- 30.8
1.380
I.187
I.161
+0.026
-11.6
- 25.9
1.488*
I.251 *
I.109
$0.142
- 26.3
I.269
I.072
I.071
+O.OOl
-2.6
-
-
1.129*
I.012
+0.117
-18
- 27.3
1.278
0.972
0,992
-0*020
4.0
- 26.7
1.344
0.914
0.922
- 0.008
IO.8
- 25.2
1.222
0.790
0.840
- o*oso
18.7
- 23.5
I.279
0.688
0.746
- 0.058
Average winter temTz;ture
Churchill, Manitoba Winnipeg, Manitoba Duluth, Minnesota St. James, Minnesota Flagstaff, Arizona Monticello, Illinois Amarillo, Texas Tucson, Arizona Vero Beach, Florida
- a.4
Winter existence metabolism (kcal g-l day-‘) Difference
* Corrected for acclimatization to the winter season, using the equation obtained only on summer birds.
S. CHARLESKJZNDEIGHAND CHARLESR. BLEM
178
TABLE 3-STATISTICAL DATA FOR MID-SUMMERENERGETICS OF THE HOUSESPARROWAT NINE NORTH AMERICAN LOCALITIES Summer existence metabolism (kcal g-l day-i)
Average summer temperature
Churchill, Manitoba Winnipeg, Manitoba Duluth, Minnesota St. James, Minnesota Flagstaff, Arizona Monticello, Illinois Amarillo, Texas Tucson, Arizona Vero Beach, Florida
PC)
Measured
9.8 18.3 17.0 22.1 17.2 23.0 26.1 28.9 27.3
0.903 0.829 0.794 0.756* 0.820 0.701 0.655 0.583 * 0.622
* Corrected for acclimatization obtained only on winter birds.
The expected rates obtained at Champaign, (Kendeigh, 1970) :
to the
Expected 0.883 0.772 0.789 0.723 0.786 0.711 0.671 0.634 0.655
summer
season,
using
of existence metabolism were calculated Illinois, based on studies over a long Winter Summer:
Difference
: M = 0.9%0.011
t,
M = l-02-0.013t.
+ 0.020 + 0.057 + 0.005 +0.033 + 0.034 - 0.010 -0.016 - 0.051 - 0.033 the
equation
from equations period of years
(1) (2)
This locality is approximately midway in latitude and near the center of the range of the species. The several introductions at various times of the species from Europe were mostly at these middle latitudes and from these latitudes the species has dispersed both northward and southward. The “difference” between the measured and expected rates represents the direction and extent to which the species has become metabolically adapted to the temperature of each locality. It is obvious (Tables 2 and 3) that at far northern localities, existence metabolism, as measured, is higher than expected, at far southern localities it is lower, although there is an appreciable irregularity in the change from one extreme to the other. When these “differences” are plotted (Fig. 1) against average ambient temperatures, two linear regression lines are obtained having the following equations and standard errors of estimate: Winter: Summer
:
M = 0.013-0.0036t + 0.057,
(3)
M = 0*090-0.0041 t _I O-026.
(4)
There is no significant difference in the slope existence metabolism becomes adapted inversely
of the two lines, with temperature
meaning that at the average
METABOLIC
ADAPTATION
TO
LOCAL
CLIMATE
IN
BIRDS
179
FIG. 1. Metabolic adaptation related to temperature, or the difference between measured and expected rates of existence metabolism during winter and summer. The letters represent the different localities listed in Table 1. See equations (3) and (4) for the regressions of the two lines.
rate of 0.00385 kcal g-l day-l ‘C-l. The range of adaptation in summer birds between northern and southern localities ( + 0.050 to - 0.028 kcal g-r day-l “C-r) is considerably shorter than in winter birds (+ 0.104 to -0.054) and is displaced These differences are the result of seasonal about 18” to higher temperatures. acclimatization. Adaptation mechanism Although the above study of metabolic adaptation to local climates has been based on analysis of existence metabolism, the physiological adaptation shown is most likely in the components of basal metabolism and suprabasal tissue metabolism (standard metabolism), rather than any adjustment in heat increment of feeding or locomotor cage activity. When the average rates of oxygen consumption measured by Hudson & Kimzey (1966) for house sparrows at 35°C during the daytime and in the zone of thermal neutrality at night are converted to kcal g-r day-l (1 cm3 0, = 4.8 g-Cal), the differences in standard metabolic rates between Houston, Texas, and the three northern localities divided by the differences in normal mean annual temperatures between the localities average 0.0059 kcal g-l day-l “C-l (Boulder, Colorado, 0.0074; Syracuse, New York, 0.0062; Ann Arbor, Michigan, 0.0042). This rate of change in metabolism per degree of ambient temperature is higher than that given above (0.00385). This difference in rate may be due in part to the different circumstances under which the measurements were made but more likely involves something more fundamental. The fact that Hudson & Kimzey obtained the latitudinal variation in metabolic rate even after all the birds had been kept at the same temperature for several months indicates that the geographic differences are not temporary adjustments, comparable to seasonal acclimatization, but are genetic
180
S. CHARLESKENDEIGHANDCHARLESR. BLEM
adaptations that are inherited. However, further investigation is required to establish this point. The higher regression coefficients for the birds at Houston where the birds were confined in flight cages all equally exposed to the same temperatures for a long period of time suggests that a masking factor was involved in our measurements that alleviated the need for the full potential of physiological adaptation. This masking factor could well be differences in behavior of birds from different localities. Local observers at Churchill in northern Manitoba report that the birds there spend most of their time in and around the large grain elevators where abundant food and artificial heat provide a microhabitat much more favorable than the prevailing macrohabitat. Even birds at middle latitudes are well known to roost in dense thickets, vines on buildings, or inside barns or sheds where they The extent of use of artificial shelters doubtless varies obtain some protection. inversely with latitude, although quantitative information on this point is lacking. In Fig. 1, the data for Churchill, Winnipeg, St. James and Monticello fall well below the regression line for winter birds, although, surprisingly, Duluth and Flagstaff lie well above the line. For the summer months, only Churchill falls appreciably below the line. In order to eliminate the “grain elevator effect”, at least in part, the regression line for the winter season has been recalculated omitting Churchill and Winnipeg and the regression line for the summer omitting Churchill, to give the following equations: Winter:
M = 0.025-0.0055t + 0.0593,
(5)
Summer:
M = 0*150-0.0066t + 0.0220.
(6)
The two temperature coefficients (average = 0*00605 kcal g-l day-l “C-l) then become similar to the one calculated from the data of Hudson & Kimzey (0.0059). If with the extensive use of artificial shelter the rates of energy use vary with ambient temperature according to equations (3) and (4) and with less extensive use of artificial shelter it varies as equations (5) and (6), then the difference between the two sets of equations approximates the way behavioral adjustments affect the metabolic rate at different temperatures (Fig. 2). For the winter season, this is:
M = 0.012-0.0019t
(7)
M = 0.060-0.0025t.
(8)
and for the summer:
Were it not for this behavioral adjustment, physiological acclimatization to live in northern localities during the winter would be according to equation (5). HOWever, this physiological acclimatization could well include changes in rate of heat Blem (1974) found that carcasses of northern loss as well as in heat production. populations of the house sparrow with the feathers smoothed around the body had a 3-18 per cent lower rate of heat conductance per unit surface area than did southern populations, which he related to increased insulation provided by fat.
METABOLIC
ADAPTATION
TO LOCAL CLIMATE
181
IN BIRDS
+0.20
+0.15
:
-
(June-August)
+o. IO -
_
3 P ‘b, +0.05 2
-
2 O-
(December-February) -0.05
‘\
t
-0.101 8 -30
-25
’
-20
a
-15
’
-10
-5
1
’
0
Temperature
8
+5
+10
1
+I5
0
+20
0
~25
1
+30
eC)
FIG. 2. Partition of total adaptation (equation 11) between insulation (equation lo), behavior (equations 7 and 8) and metabolism (equations 3 and 4) related to temperature. There
to be no significant differences line identified by the equation:
appeared
regression
in plumage.
M = 0.0234+ 0.00012t f 0.00083.
His data fall on a
(9)
The temperature (t) used was the normal mean for January, the coldest month, and data were available for eight localities with temperatures ranging from - 27.4 to + 16.9”C. The difference in rate of heat conductance between that at the lowest temperature (Churchill) and at higher temperatures (extreme at Vero Beach) represents the savings or conservation of heat obtained by the increase in insulation at the lower temperatures. Since this varies linearly, it is represented, when translated in terms of the mean winter instead of January temperatures, by the equation:
M = 0*0022-0.00012t.
(10)
The saving of heat production by the better insulation is relatively small. There is no certainty, however, that the rate of heat conductance on dead carcasses is quantitatively transferable to the living bird. Blood circulation in the living bird would increase the rate of heat flow from the core through the shell to the skin, giving greater importance to the fat layer under the skin. On the other hand, the living bird could fluff its feathers to various degrees as the need arises, thereby increasing their effectiveness in providing insulation. Total adaptation of birds in the winter to cold, including that of metabolism, behavior and increased insulation, follows the equation :
M = 0*0272-0.00562t.
(11)
182
S. CHARLES KENDEICH AND CHARLES R. BLEM
At Churchill, using equations (3), (7) and (9), metabolic adaptation accounts for 61 per cent of the total, behavior adjustment for 36 per cent and better body insulation for 3 per cent. At Monticello, the proportions are 52, 41 and 6 per cent respectively, indicating that the relative importance of metabolic adaptation increases at lower ambient temperatures. Warm-blooded animals have an advantage over most cold-blooded ones in that a necessity for full expression of metabolic adjustment (0.00562 kcal g-l day-l “C-l) is alleviated by reducing the rate of heat loss by better insulation and behavior adjustments. There still remains, however, a substantial amount of metabolic adjustment required-in the house sparrow, approximately O-00385 kcal g-l day-l “C-l. The higher intensity of metabolism per unit mass of tissue in cold climates may require similar adaptation of enzyme and hormone action as in cold-blooded forms, but this needs to be investigated. At high ambient temperatures, for instance at Vero Beach (Fig. l), use of artificial shelter, similar to the behavior adjustment at low ambient temperature, would depress the metabolic rate perhaps excessively. At any rate, such behavior is reduced to a minimum, since apparently does not occur. Likewise, insulation such insulation becomes a liability when a high rate of heat loss becomes advantageous. Lower limit of temperature tolerance The higher rate of metabolism of birds adapted to low temperature should enable them to tolerate lower extreme temperatures, since this lower limit of temperature tolerance is determined by the maximum amount of energy that the bird can mobilize. The incipient lower limit of temperature tolerance is determined by sudden exposure of freshly caught birds to extreme temperature without The incipient lower limit of temperature tolerance allowing time for acclimation. increases during the winter (Barnett, 1970) and at higher latitudes geographically (Blem, 1973). The ultimate limit of temperature tolerance is, however, of more concern here. It is determined by gradual or stepwise exposure of birds to progressively lower temperatures allowing acclimation to occur. These are the values given in Table 2. The “ultimate maximum potential” for energy mobilization was calculated using these temperatures. It is fairly obvious from the data that the ultimate limit of temperature tolerance (T) varies inversely with average winter temperature (t). The significant linear equation is :
T = - 26.4 + 0.178t _t 0.54. With
this equation
the “expected” Churchill Winnipeg Duluth St. James
ultimate
- 30.9”C - 29.2 - 28.5 -27.9
limits
(12)
of temperature
Monticello Amarillo Tucson Vero Beach
-
26.7 25.7 24.5 23.1
tolerance
are :
METABOLIC
ADAPTATION
TO LOCAL CLIMATE IN BIRDS
183
Maximum metabolism There is also evidence in Table 2 for the ultimate maximum metabolic to be higher at low ambient temperatures. The significant linear equation Churchill) is : M = 1.321-0.00%
+ 0.036.
potential (omitting
(13)
Using equation (13) and the mean winter temperature (Table 2), the “expected” ultimate maximum potential for various localities would be as follows: Churchill Winnipeg Duluth St. James
1.448 kcal g-i day-l 1.401 1.379 l-363
Monticello Amarillo Tucson Vero Beach
1.330 1.301 1.267 l-227
Minimal metabolism A high rate of metabolism is disadvantageous at high ambient temperatures since the excess heat production must be dissipated to prevent rise in body temperature. Standard metabolism becomes minimal (basal metabolism) in the zone of thermal neutrality, or if a zone is not present, then at the upper critical ambient temperature, or approximately 37°C in the house sparrow. Existence metabolism also decreases linearly to this temperature (Kendeigh, 1969a) where it is only O-529 kcal g-l day-l in summer-acclimatized birds at Champaign, Illinois. Using this value as a reference, the ultimate minimal existence metabolism at each locality at the upper critical temperature may be calculated with equation (4): Churchill Winnipeg Duluth St. James Monticello
0.579 kcal g-l day-r 0.545 0.550 0.530 O-526
Flagstaff Amarillo Tucson Vero Beach
0.549 0.5 14 0.502 O-509
Upper critical temperature No study has been made of relative resistance to high temperature in birds from different localities. Northern birds with their higher metabolism and other adaptations would be expected to have lower tolerance than do birds from southern localities, and this would be expressed in their having lower upper critical temperatures. These can be approximated by substituting for M in equation (2) the metabolic values for the upper critical temperature given above and solving for t. This gives the following upper critical temperatures: Churchill Winnipeg Duluth Flagstaff St. James
33*2”C 35.8 35.4 35.5 36.9
Monticello Amarillo Tucson Vero Beach
37.2 38.2 39.1 38.5
184
S. CHARLES I&WEIGH
AND CHARLES R. BLEM
If the summer equations obtained by Blem (1973) for local populations are used instead of equation (2), Duluth birds have an upper critical ambient temperature of 30*6”C and Vero Beach birds have 36*8”C with other localities falling in between, except for Winnipeg which gives an entirely anomalous value. DISCUSSION
An evaluation A higher rate of metabolism at low ambient temperatures in cold-blooded animals has the obvious advantage of enabling the individuals to maintain greater activity-more nearly equal to that of animals in warmer climates than would otherwise be possible. In warm-blooded animals, activity is not so closely affected by ambient temperatures, and when temperature is not extreme, the surplus heat produced must be dissipated or wasted. There is a further disadvantage in that the higher rate of metabolism requires a higher rate of feeding, and, at times, food is often difficult to find in adequate quantity. The adaptive feature of the higher metabolic rate is that it enables the birds to mobilize energy so that they can tolerate and be active at more extreme low temperatures. This permits the species to maintain permanent residency rather than becoming a migrant and to disperse farther into higher latitudes. The wastage of energy at moderate to high ambient temperatures, where it is not required, is not an excessive penalty to pay for the obvious advantage received. As Packard (1968) points out for northern microtine voles, where an increase in standard metabolism is also joined with a higher “summit” metabolism, this greater cold resistance is the character being subjected to natural selection. A lower rate of metabolism at high ambient temperatures is adaptive in a different way. Maintaining body temperature control at high ambient temperatures requires evaporative cooling which leads to panting and inactivity as temperatures become extreme. This is alleviated by acquiring a lower rate of heat production, and this lightening of requirements for heat loss permits tolerance and activity at higher temperatures. Thus occupancy of warmer lower latitudes or tropical regions becomes possible. A physiological model Using the data for the calculated maximum and minimum potential energy mobilization and ultimate lower limits of temperature tolerance and upper critical temperatures, a physiological model in graph form has been constructed (Fig. 3). The upper line connects the highest ultimate maximum potential at the lowest limit of temperature tolerance with the highest minimum potential at the lowest upper critical temperature, as would be experienced by birds at Churchill. The lower line connects the lowest ultimate maximum potential as might well be shown by birds at Veracruz with the lowest minimum potential as shown by birds in the desert region of Tucson. Regression lines for all localities where the species now occurs fall within these boundaries.
METABOLIC
ADAPTATION
TO LOCAL CLIMATE
185
IN BIRDS
T
3
-Q T 6
IO-
3
s
0.5 I
-40
I
-30
I
-20
I
I
I
-0
0
l10
Temperature
I
tm
I
t30
I
+40
PC)
FIG. 3. Physiological model of inclusive metabolic adjustment to local climates. Balboa Heights (BH) in the Panama Canal Zone and presently outside the distributional limits of the species is represented by a dot at the lower end of the line showing ultimate maximum potential. Heavy lines represent ultimate maximum (U. Max.) and ultimate minimal (U. Min.) potentials.
Dispersal into tropics No work has been done with birds occurring still farther south. Veracruz, Mexico, lies just within the known southernmost limit of the species along the Gulf of Mexico. Mean summer temperatures here average 27*O”C, comparable to Vero Beach and slightly lower than at Tucson. Mean winter temperatures average 22*3”C, which is considerably higher than at these two localities. By equations (12) and (13), the ultimate lower limit of temperature tolerance should be - 22*4”C and the ultimate maximum potential, 1.209 kcal g-l day-l. Balboa Heights in the Panama Canal Zone lies outside the present distributional Its summer temperature of 26+X is within the limits range of the house sparrow. analyzed for other localities. Temperature remains very uniform through the year. The average winter temperature of 26*7”C would imply an ultimate lower limit of temperature tolerance of -21*6”C and an ultimate maximum potential of l-187 kcal g-l day-l. The winter season should present no obstacle for the existence of the species. There is no reason, as far as bioenergetics is concerned, why the house sparrow should not eventually spread through the American subtropics and tropics. Inter-species differences The differences between local populations in metabolic adaptations demonstrated to occur intra-specifically appear also to occur inter-specifically between birds occurring in different climates. Several species of desert birds (Rising, 1969 ; Dawson & Bennett, 1973) have been shown to have rates of metabolism below those predicted from equations based on a large number of species inhabiting a
186
S. CHARLESKENDEIGHAND CHARLESR. BLEM
variety of climates. Likewise northern species adapted to cold climates have been shown with higher than predicted rates of metabolism (West, 1972) and to have greater potentialities for mobilizing energy than southern species (Kendeigh, 1969b). It is suggested that, in predicting the rate of metabolism of a species from its known weight, allowance always be made for higher rates for birds from cold regions and lower rates for birds from warm regions. With further study, perhaps this correction factor can also be quantified for other species. The varying ability of species to adapt metabolically, as well as by modifying their insulative control of heat loss and their behavioral responses, needs to be considered in understanding the differences in their distributional limits, relative population levels and migratory status. CONCLUSIONS
With dispersal from temperate to cold (Arctic) climates, birds (house sparrows) evolve higher rates of metabolism, lower limits of temperature tolerance and greater capacities for mobilizing energy. This is in addition to their better insulation and behavioral responses for avoiding extreme cold. With dispersal from temperate to warm (and tropical) climates, birds (house sparrows) evolve lower rates of metabolism and higher upper critical temperatures. The extreme present northward dispersal of the house sparrow in the western hemisphere is closely correlated with behavioral adjustments (such as use of grain elevators) to avoid full exposure to macroclimates. Further southward dispersal of the house sparrow in the western hemisphere into the tropics is not limited by metabolic factors and may be expected to occur.
REFERENCES BARNETTL. B. (1970) Seasonal changes in temperature acclimatization of the house sparrow, Passer domesticus. Comp. Biochem. Physiol. 33, 559-578. BARTHOLOMEWG. A. (1972) Body temperature and energy transformation. In Animal Physiology: Principles and Adaptations (Edited by GORDONM. S.), 2nd Edn., pp. 298368. Macmillan, New York. BLEM C. R. (1973) Geographic variation in the bioenergetics of the house sparrow. Omith. Monogr. 14, 96-121. BLEM C. R. (1974) Geographic variation in thermal conductance in the house sparrow, Passer domesticus. Comp. Biochem. Physiol. 47A, 101-108. DAWSONW. R. & BENNETTA. F. (1973) Roles of metabolic level and temperature regulation in the adjustment of western plumed pigeons (Lophophapsferruginea) to desert conditions. Comp. Biochem. Physiol. 44A, 249-266. HUDSONJ. W. & KIMZEY S. W. (1966) Temperature regulation and metabolic rhythms in populations of the house sparrow, Passer domesticus. Comp. Biochem. Physiol. 17, 203217. KENDEIGHS. C. (1969a) Energy responses of birds to their thermal environment. Wilson Bull. 81, 441-449. KENDEIGHS. C. (1969b) Resistance to cold and Bergmann’s rule. Auk 86, 13-25. KENDEIGHS. C. (1970) Energy requirements for existence in relation to size of bird. Condor 72, 60-65.
METABOLICADAPTATION TO LOCALCLIMATEIN BIRDS
187
KENDEIGHS. C. (1973) Latitudinal trends in the metabolic adjustments of the house sparrow to its environment in North America. (To be published.) PACKARDG. C. (1968) Oxygen consumption of ik?icrotus montunus in relation to ambient temperature. J. Mammal. 49, 215-220. RISING J. D. (1969) A comparison of metabolism and evaporative water losses of Baltimore and Bullock orioles. Comp. Biochem. Physiol. 31, 915-925. SCHOLANDERP. F., HOCK R., WALTERSV. & IRVING L. (1950) Adaptation to cold in Arctic and tropical mammals and birds in relation to body temperature, insulation, and basal metabolic rate. Biol. Bull., mar. biol Lab., Woods Hole 99, 259-271. TROST C. H. (1972) Adaptations of horned larks (Eremophilu alpestris) to hot environments. Auk 89, 506-527. WEST G. C. (1972) Seasonal differences in resting metabolic rate of Alaskan ptarmigan. Comp. Biochem. Physiol. 42, 867-876. Key Word Index-Birds; house sparrow, Passer domesticus; energy metabolism; logical adaptation; temperature; physiological model.
physio-
METABOLIC
ADAPTATION TO LOCAL BIRDS*
S. CHARLES
and
KENDEIGHl
CHARLES
CLIMATE
IN
R. BLEM2
‘Department of Zoology, University of Illinois, Champaign, Illinois 61820, and 2Department of Biology, Virginia Commonwealth University, Richmond, Virginia 23220, U.S.A. (Received
1 June
1973)
Abstract-l. Existence metabolism in house sparrows, Passer domesticus, collected at nine North American localities, varies inversely with mean midwinter and mid-summer temperatures of collection sites at rates of 0.0036 and 0.0041 kcal g-l day-’ ‘C-l, respectively. 2. Behavioral responses and improved insulation during the winter provide further adaptation to cold climates at rates of 0.0019 and 0.00012 kcal g-l day-’ ‘C-l, respectively. 3. Within the range of collection sites, ultimate minimal existence metabolism decreases southward, while upper critical temperatures predicted from these values increase. 4. Ultimate maximum existence metabolism and lower limits of temperature tolerance increase northward with drop in winter temperature and constitute the critical metabolic characteristics that enable the species to be permanent residents at the collection sites. 5. Maximum and minimum existence energy values and ultimate lower limits of temperature tolerance are used to construct a graphic physiological model for the distribution of house sparrows in North America.
INTRODUCTION THE WIDE distribution
logical
and other
moderate Arctic
adaptations
climates.
with
its
house
sparrow,
Churchill,
for surviving
to the tropics
and reproducing
If the class Aves originated
great
resources and other tions in physiology, the adjustments
of birds from the Arctic
seasonal
fluctuations
presupposes in extreme
in the tropics,
in temperature,
factors must have required progressive behavior and even morphology. Even
physioas well as
dispersal
into the
photoperiod,
food
evolutionary adaptamore remarkable are
that must have been made to enable a single species, such as the all the way from Passer domesticus, to occur and reproduce
in northern
Manitoba
on the
Hudson
Bay,
to southern
Mexico
and
Guatemala. This is particularly striking considering that the species was introduced into North America from Europe within only the last 125 years. * The research for this paper was supported in part by grants from the National Science Foundation. 17.5 7
176
S. CHARLESKENDEIGH AND CHARLESR. BLEM
It is well known that cold-blooded forms compensate for lower ambient temperatures by maintaining a higher rate of metabolism than their relatives in warmer climates (Bartholomew, 1972). Warm-blooded birds and mammals, however, are supposed to adapt to cold by improving their body insulation rather than adjusting their rate of metabolism (Scholander et al., 1950). Doubt that this was entirely true is raised by Hudson & Kimzey’s (1966) finding that house sparrows from three northern localities in the United States had a higher rate of standard metabolism than did birds from Texas, by Trost’s (1972) study of the horned lark, Eremophila alpestris, which showed that a hot desert subspecies maintained a lower metabolic rate than did another subspecies from a milder climate, and by Dawson & Bennett’s (1973) finding that desert species of pigeons and doves have lower metabolism than species from cooler regions. The present study with the house sparrow is to investigate this problem on a wider scale. The manner in which adaptation occurs within this species may reflect also the manner in which other species have become adapted to different climates, especially to temperature, at different latitudes in the northern hemisphere. ANALYSIS
Existence metabolism The rate of existence metabolism was measured in samples of live house sparrows obtained from nine localities in the United States and Canada (Blem, 1973). Existence metabolism is the amount of energy required by caged birds to maintain constant weight over a period of days. It is measured by the amount of food actually metabolized (caloric content of food ingested minus calories in excreta). Included as components of existence metabolism are basal metabolism, suprabasal tissue metabolism for body temperature regulation, the heat increment of feeding and the energy requirements for the minimal locomotor activity permitted by the small cages. Existence metabolism was measured over the whole range of ambient temperatures tolerated by the birds, and regression line equations were obtained for each locality (Table 1). Existence metabolism determined in this manner does not include energy requirements for free existence, reproduction, molt or other activities of free-living birds but is comparable from one locality to another. The “measured” existence metabolism (M = kcal g-l day-l) for mid-summer (average for June, July and August) and for mid-winter (average for December, January and February) were calculated from the equations (Table 1) using the monthly normal mean temperatures (t = “C) at each locality (Tables 2 and 3). For those localities where regression lines were obtained for one season only, values for the missing season were calculated, allowing for seasonal acclimatization. Seasonal acclimatization in terms of the whole bird (kcal/bird-day) was obtained using a correction factor of - 1*0+0*05t for the winter, and + l-O-0*05t for the summer (Kendeigh, 1973). All equations in this paper, however, are given in terms of specific weight (g) since Blem (1973) found that individual weight of birds varied positively with latitude (temperature).
METABOLIC ADAPTATION TO LOCALCLIMATEIN BIRDS
177
TABLE I-EXISTENCE METABOLISM EQUATIONS FOR SAMPLESOF HOUSE SPARROWS COLLECTED DURING MID-SUMMER (S) OR MID-WINTER (W) AT NINENORTH AMERICANLOCALITIES Regression equation Location
(t = “C)
____
kcal g-l day-i =
Churchill, Manitoba (S) Winnipeg, Manitoba (W) Winnipeg, Manitoba (S) Duluth, Minnesota (S) St. James, Minnesota (W) Monticello, Illinois (W) Monticello, Illinois (S) Amarillo, Texas (W) Amarillo, Texas (S) Flagstaff, Arizona (S) Tucson, Arizona (W) Vero Beach, Florida (W) Vero Beach, Florida (S)
1~05-O~Ol5t 0~98-O~Ol3t 0~92-0~005t 1~10-0~018t 0~98-OOll t 0~95-0~012t 1~00-0~013t 0.97-0.014t 1~02-0~014t 1~13-0~018t 0.92-0.012t 0~95-0~014t 0~95-0012t
TABLE ~-STATISTICAL DATAFOR FOR MID-WINTERENERGETIC~ OF THE HOUSESPARROWAT
NINE NORTH AMERICAN LOCALITIES
Ultimate limit of tolerance (“C)
Ultimate maximum potential (kcal g-’ day-‘)
Measured
Expected
- 25.3
- 31.4
1445*
1.360*
I.274
+0.086
- 15.9
- 30.8
1.380
I.187
I.161
+0.026
-11.6
- 25.9
1.488*
I.251 *
I.109
$0.142
- 26.3
I.269
I.072
I.071
+O.OOl
-2.6
-
-
1.129*
I.012
+0.117
-18
- 27.3
1.278
0.972
0,992
-0*020
4.0
- 26.7
1.344
0.914
0.922
- 0.008
IO.8
- 25.2
1.222
0.790
0.840
- o*oso
18.7
- 23.5
I.279
0.688
0.746
- 0.058
Average winter temTz;ture
Churchill, Manitoba Winnipeg, Manitoba Duluth, Minnesota St. James, Minnesota Flagstaff, Arizona Monticello, Illinois Amarillo, Texas Tucson, Arizona Vero Beach, Florida
- a.4
Winter existence metabolism (kcal g-l day-‘) Difference
* Corrected for acclimatization to the winter season, using the equation obtained only on summer birds.
S. CHARLESKJZNDEIGHAND CHARLESR. BLEM
178
TABLE 3-STATISTICAL DATA FOR MID-SUMMERENERGETICS OF THE HOUSESPARROWAT NINE NORTH AMERICAN LOCALITIES Summer existence metabolism (kcal g-l day-i)
Average summer temperature
Churchill, Manitoba Winnipeg, Manitoba Duluth, Minnesota St. James, Minnesota Flagstaff, Arizona Monticello, Illinois Amarillo, Texas Tucson, Arizona Vero Beach, Florida
PC)
Measured
9.8 18.3 17.0 22.1 17.2 23.0 26.1 28.9 27.3
0.903 0.829 0.794 0.756* 0.820 0.701 0.655 0.583 * 0.622
* Corrected for acclimatization obtained only on winter birds.
The expected rates obtained at Champaign, (Kendeigh, 1970) :
to the
Expected 0.883 0.772 0.789 0.723 0.786 0.711 0.671 0.634 0.655
summer
season,
using
of existence metabolism were calculated Illinois, based on studies over a long Winter Summer:
Difference
: M = 0.9%0.011
t,
M = l-02-0.013t.
+ 0.020 + 0.057 + 0.005 +0.033 + 0.034 - 0.010 -0.016 - 0.051 - 0.033 the
equation
from equations period of years
(1) (2)
This locality is approximately midway in latitude and near the center of the range of the species. The several introductions at various times of the species from Europe were mostly at these middle latitudes and from these latitudes the species has dispersed both northward and southward. The “difference” between the measured and expected rates represents the direction and extent to which the species has become metabolically adapted to the temperature of each locality. It is obvious (Tables 2 and 3) that at far northern localities, existence metabolism, as measured, is higher than expected, at far southern localities it is lower, although there is an appreciable irregularity in the change from one extreme to the other. When these “differences” are plotted (Fig. 1) against average ambient temperatures, two linear regression lines are obtained having the following equations and standard errors of estimate: Winter: Summer
:
M = 0.013-0.0036t + 0.057,
(3)
M = 0*090-0.0041 t _I O-026.
(4)
There is no significant difference in the slope existence metabolism becomes adapted inversely
of the two lines, with temperature
meaning that at the average
METABOLIC
ADAPTATION
TO
LOCAL
CLIMATE
IN
BIRDS
179
FIG. 1. Metabolic adaptation related to temperature, or the difference between measured and expected rates of existence metabolism during winter and summer. The letters represent the different localities listed in Table 1. See equations (3) and (4) for the regressions of the two lines.
rate of 0.00385 kcal g-l day-l ‘C-l. The range of adaptation in summer birds between northern and southern localities ( + 0.050 to - 0.028 kcal g-r day-l “C-r) is considerably shorter than in winter birds (+ 0.104 to -0.054) and is displaced These differences are the result of seasonal about 18” to higher temperatures. acclimatization. Adaptation mechanism Although the above study of metabolic adaptation to local climates has been based on analysis of existence metabolism, the physiological adaptation shown is most likely in the components of basal metabolism and suprabasal tissue metabolism (standard metabolism), rather than any adjustment in heat increment of feeding or locomotor cage activity. When the average rates of oxygen consumption measured by Hudson & Kimzey (1966) for house sparrows at 35°C during the daytime and in the zone of thermal neutrality at night are converted to kcal g-r day-l (1 cm3 0, = 4.8 g-Cal), the differences in standard metabolic rates between Houston, Texas, and the three northern localities divided by the differences in normal mean annual temperatures between the localities average 0.0059 kcal g-l day-l “C-l (Boulder, Colorado, 0.0074; Syracuse, New York, 0.0062; Ann Arbor, Michigan, 0.0042). This rate of change in metabolism per degree of ambient temperature is higher than that given above (0.00385). This difference in rate may be due in part to the different circumstances under which the measurements were made but more likely involves something more fundamental. The fact that Hudson & Kimzey obtained the latitudinal variation in metabolic rate even after all the birds had been kept at the same temperature for several months indicates that the geographic differences are not temporary adjustments, comparable to seasonal acclimatization, but are genetic
180
S. CHARLESKENDEIGHANDCHARLESR. BLEM
adaptations that are inherited. However, further investigation is required to establish this point. The higher regression coefficients for the birds at Houston where the birds were confined in flight cages all equally exposed to the same temperatures for a long period of time suggests that a masking factor was involved in our measurements that alleviated the need for the full potential of physiological adaptation. This masking factor could well be differences in behavior of birds from different localities. Local observers at Churchill in northern Manitoba report that the birds there spend most of their time in and around the large grain elevators where abundant food and artificial heat provide a microhabitat much more favorable than the prevailing macrohabitat. Even birds at middle latitudes are well known to roost in dense thickets, vines on buildings, or inside barns or sheds where they The extent of use of artificial shelters doubtless varies obtain some protection. inversely with latitude, although quantitative information on this point is lacking. In Fig. 1, the data for Churchill, Winnipeg, St. James and Monticello fall well below the regression line for winter birds, although, surprisingly, Duluth and Flagstaff lie well above the line. For the summer months, only Churchill falls appreciably below the line. In order to eliminate the “grain elevator effect”, at least in part, the regression line for the winter season has been recalculated omitting Churchill and Winnipeg and the regression line for the summer omitting Churchill, to give the following equations: Winter:
M = 0.025-0.0055t + 0.0593,
(5)
Summer:
M = 0*150-0.0066t + 0.0220.
(6)
The two temperature coefficients (average = 0*00605 kcal g-l day-l “C-l) then become similar to the one calculated from the data of Hudson & Kimzey (0.0059). If with the extensive use of artificial shelter the rates of energy use vary with ambient temperature according to equations (3) and (4) and with less extensive use of artificial shelter it varies as equations (5) and (6), then the difference between the two sets of equations approximates the way behavioral adjustments affect the metabolic rate at different temperatures (Fig. 2). For the winter season, this is:
M = 0.012-0.0019t
(7)
M = 0.060-0.0025t.
(8)
and for the summer:
Were it not for this behavioral adjustment, physiological acclimatization to live in northern localities during the winter would be according to equation (5). HOWever, this physiological acclimatization could well include changes in rate of heat Blem (1974) found that carcasses of northern loss as well as in heat production. populations of the house sparrow with the feathers smoothed around the body had a 3-18 per cent lower rate of heat conductance per unit surface area than did southern populations, which he related to increased insulation provided by fat.
METABOLIC
ADAPTATION
TO LOCAL CLIMATE
181
IN BIRDS
+0.20
+0.15
:
-
(June-August)
+o. IO -
_
3 P ‘b, +0.05 2
-
2 O-
(December-February) -0.05
‘\
t
-0.101 8 -30
-25
’
-20
a
-15
’
-10
-5
1
’
0
Temperature
8
+5
+10
1
+I5
0
+20
0
~25
1
+30
eC)
FIG. 2. Partition of total adaptation (equation 11) between insulation (equation lo), behavior (equations 7 and 8) and metabolism (equations 3 and 4) related to temperature. There
to be no significant differences line identified by the equation:
appeared
regression
in plumage.
M = 0.0234+ 0.00012t f 0.00083.
His data fall on a
(9)
The temperature (t) used was the normal mean for January, the coldest month, and data were available for eight localities with temperatures ranging from - 27.4 to + 16.9”C. The difference in rate of heat conductance between that at the lowest temperature (Churchill) and at higher temperatures (extreme at Vero Beach) represents the savings or conservation of heat obtained by the increase in insulation at the lower temperatures. Since this varies linearly, it is represented, when translated in terms of the mean winter instead of January temperatures, by the equation:
M = 0*0022-0.00012t.
(10)
The saving of heat production by the better insulation is relatively small. There is no certainty, however, that the rate of heat conductance on dead carcasses is quantitatively transferable to the living bird. Blood circulation in the living bird would increase the rate of heat flow from the core through the shell to the skin, giving greater importance to the fat layer under the skin. On the other hand, the living bird could fluff its feathers to various degrees as the need arises, thereby increasing their effectiveness in providing insulation. Total adaptation of birds in the winter to cold, including that of metabolism, behavior and increased insulation, follows the equation :
M = 0*0272-0.00562t.
(11)
182
S. CHARLES KENDEICH AND CHARLES R. BLEM
At Churchill, using equations (3), (7) and (9), metabolic adaptation accounts for 61 per cent of the total, behavior adjustment for 36 per cent and better body insulation for 3 per cent. At Monticello, the proportions are 52, 41 and 6 per cent respectively, indicating that the relative importance of metabolic adaptation increases at lower ambient temperatures. Warm-blooded animals have an advantage over most cold-blooded ones in that a necessity for full expression of metabolic adjustment (0.00562 kcal g-l day-l “C-l) is alleviated by reducing the rate of heat loss by better insulation and behavior adjustments. There still remains, however, a substantial amount of metabolic adjustment required-in the house sparrow, approximately O-00385 kcal g-l day-l “C-l. The higher intensity of metabolism per unit mass of tissue in cold climates may require similar adaptation of enzyme and hormone action as in cold-blooded forms, but this needs to be investigated. At high ambient temperatures, for instance at Vero Beach (Fig. l), use of artificial shelter, similar to the behavior adjustment at low ambient temperature, would depress the metabolic rate perhaps excessively. At any rate, such behavior is reduced to a minimum, since apparently does not occur. Likewise, insulation such insulation becomes a liability when a high rate of heat loss becomes advantageous. Lower limit of temperature tolerance The higher rate of metabolism of birds adapted to low temperature should enable them to tolerate lower extreme temperatures, since this lower limit of temperature tolerance is determined by the maximum amount of energy that the bird can mobilize. The incipient lower limit of temperature tolerance is determined by sudden exposure of freshly caught birds to extreme temperature without The incipient lower limit of temperature tolerance allowing time for acclimation. increases during the winter (Barnett, 1970) and at higher latitudes geographically (Blem, 1973). The ultimate limit of temperature tolerance is, however, of more concern here. It is determined by gradual or stepwise exposure of birds to progressively lower temperatures allowing acclimation to occur. These are the values given in Table 2. The “ultimate maximum potential” for energy mobilization was calculated using these temperatures. It is fairly obvious from the data that the ultimate limit of temperature tolerance (T) varies inversely with average winter temperature (t). The significant linear equation is :
T = - 26.4 + 0.178t _t 0.54. With
this equation
the “expected” Churchill Winnipeg Duluth St. James
ultimate
- 30.9”C - 29.2 - 28.5 -27.9
limits
(12)
of temperature
Monticello Amarillo Tucson Vero Beach
-
26.7 25.7 24.5 23.1
tolerance
are :
METABOLIC
ADAPTATION
TO LOCAL CLIMATE IN BIRDS
183
Maximum metabolism There is also evidence in Table 2 for the ultimate maximum metabolic to be higher at low ambient temperatures. The significant linear equation Churchill) is : M = 1.321-0.00%
+ 0.036.
potential (omitting
(13)
Using equation (13) and the mean winter temperature (Table 2), the “expected” ultimate maximum potential for various localities would be as follows: Churchill Winnipeg Duluth St. James
1.448 kcal g-i day-l 1.401 1.379 l-363
Monticello Amarillo Tucson Vero Beach
1.330 1.301 1.267 l-227
Minimal metabolism A high rate of metabolism is disadvantageous at high ambient temperatures since the excess heat production must be dissipated to prevent rise in body temperature. Standard metabolism becomes minimal (basal metabolism) in the zone of thermal neutrality, or if a zone is not present, then at the upper critical ambient temperature, or approximately 37°C in the house sparrow. Existence metabolism also decreases linearly to this temperature (Kendeigh, 1969a) where it is only O-529 kcal g-l day-l in summer-acclimatized birds at Champaign, Illinois. Using this value as a reference, the ultimate minimal existence metabolism at each locality at the upper critical temperature may be calculated with equation (4): Churchill Winnipeg Duluth St. James Monticello
0.579 kcal g-l day-r 0.545 0.550 0.530 O-526
Flagstaff Amarillo Tucson Vero Beach
0.549 0.5 14 0.502 O-509
Upper critical temperature No study has been made of relative resistance to high temperature in birds from different localities. Northern birds with their higher metabolism and other adaptations would be expected to have lower tolerance than do birds from southern localities, and this would be expressed in their having lower upper critical temperatures. These can be approximated by substituting for M in equation (2) the metabolic values for the upper critical temperature given above and solving for t. This gives the following upper critical temperatures: Churchill Winnipeg Duluth Flagstaff St. James
33*2”C 35.8 35.4 35.5 36.9
Monticello Amarillo Tucson Vero Beach
37.2 38.2 39.1 38.5
184
S. CHARLES I&WEIGH
AND CHARLES R. BLEM
If the summer equations obtained by Blem (1973) for local populations are used instead of equation (2), Duluth birds have an upper critical ambient temperature of 30*6”C and Vero Beach birds have 36*8”C with other localities falling in between, except for Winnipeg which gives an entirely anomalous value. DISCUSSION
An evaluation A higher rate of metabolism at low ambient temperatures in cold-blooded animals has the obvious advantage of enabling the individuals to maintain greater activity-more nearly equal to that of animals in warmer climates than would otherwise be possible. In warm-blooded animals, activity is not so closely affected by ambient temperatures, and when temperature is not extreme, the surplus heat produced must be dissipated or wasted. There is a further disadvantage in that the higher rate of metabolism requires a higher rate of feeding, and, at times, food is often difficult to find in adequate quantity. The adaptive feature of the higher metabolic rate is that it enables the birds to mobilize energy so that they can tolerate and be active at more extreme low temperatures. This permits the species to maintain permanent residency rather than becoming a migrant and to disperse farther into higher latitudes. The wastage of energy at moderate to high ambient temperatures, where it is not required, is not an excessive penalty to pay for the obvious advantage received. As Packard (1968) points out for northern microtine voles, where an increase in standard metabolism is also joined with a higher “summit” metabolism, this greater cold resistance is the character being subjected to natural selection. A lower rate of metabolism at high ambient temperatures is adaptive in a different way. Maintaining body temperature control at high ambient temperatures requires evaporative cooling which leads to panting and inactivity as temperatures become extreme. This is alleviated by acquiring a lower rate of heat production, and this lightening of requirements for heat loss permits tolerance and activity at higher temperatures. Thus occupancy of warmer lower latitudes or tropical regions becomes possible. A physiological model Using the data for the calculated maximum and minimum potential energy mobilization and ultimate lower limits of temperature tolerance and upper critical temperatures, a physiological model in graph form has been constructed (Fig. 3). The upper line connects the highest ultimate maximum potential at the lowest limit of temperature tolerance with the highest minimum potential at the lowest upper critical temperature, as would be experienced by birds at Churchill. The lower line connects the lowest ultimate maximum potential as might well be shown by birds at Veracruz with the lowest minimum potential as shown by birds in the desert region of Tucson. Regression lines for all localities where the species now occurs fall within these boundaries.
METABOLIC
ADAPTATION
TO LOCAL CLIMATE
185
IN BIRDS
T
3
-Q T 6
IO-
3
s
0.5 I
-40
I
-30
I
-20
I
I
I
-0
0
l10
Temperature
I
tm
I
t30
I
+40
PC)
FIG. 3. Physiological model of inclusive metabolic adjustment to local climates. Balboa Heights (BH) in the Panama Canal Zone and presently outside the distributional limits of the species is represented by a dot at the lower end of the line showing ultimate maximum potential. Heavy lines represent ultimate maximum (U. Max.) and ultimate minimal (U. Min.) potentials.
Dispersal into tropics No work has been done with birds occurring still farther south. Veracruz, Mexico, lies just within the known southernmost limit of the species along the Gulf of Mexico. Mean summer temperatures here average 27*O”C, comparable to Vero Beach and slightly lower than at Tucson. Mean winter temperatures average 22*3”C, which is considerably higher than at these two localities. By equations (12) and (13), the ultimate lower limit of temperature tolerance should be - 22*4”C and the ultimate maximum potential, 1.209 kcal g-l day-l. Balboa Heights in the Panama Canal Zone lies outside the present distributional Its summer temperature of 26+X is within the limits range of the house sparrow. analyzed for other localities. Temperature remains very uniform through the year. The average winter temperature of 26*7”C would imply an ultimate lower limit of temperature tolerance of -21*6”C and an ultimate maximum potential of l-187 kcal g-l day-l. The winter season should present no obstacle for the existence of the species. There is no reason, as far as bioenergetics is concerned, why the house sparrow should not eventually spread through the American subtropics and tropics. Inter-species differences The differences between local populations in metabolic adaptations demonstrated to occur intra-specifically appear also to occur inter-specifically between birds occurring in different climates. Several species of desert birds (Rising, 1969 ; Dawson & Bennett, 1973) have been shown to have rates of metabolism below those predicted from equations based on a large number of species inhabiting a
186
S. CHARLESKENDEIGHAND CHARLESR. BLEM
variety of climates. Likewise northern species adapted to cold climates have been shown with higher than predicted rates of metabolism (West, 1972) and to have greater potentialities for mobilizing energy than southern species (Kendeigh, 1969b). It is suggested that, in predicting the rate of metabolism of a species from its known weight, allowance always be made for higher rates for birds from cold regions and lower rates for birds from warm regions. With further study, perhaps this correction factor can also be quantified for other species. The varying ability of species to adapt metabolically, as well as by modifying their insulative control of heat loss and their behavioral responses, needs to be considered in understanding the differences in their distributional limits, relative population levels and migratory status. CONCLUSIONS
With dispersal from temperate to cold (Arctic) climates, birds (house sparrows) evolve higher rates of metabolism, lower limits of temperature tolerance and greater capacities for mobilizing energy. This is in addition to their better insulation and behavioral responses for avoiding extreme cold. With dispersal from temperate to warm (and tropical) climates, birds (house sparrows) evolve lower rates of metabolism and higher upper critical temperatures. The extreme present northward dispersal of the house sparrow in the western hemisphere is closely correlated with behavioral adjustments (such as use of grain elevators) to avoid full exposure to macroclimates. Further southward dispersal of the house sparrow in the western hemisphere into the tropics is not limited by metabolic factors and may be expected to occur.
REFERENCES BARNETTL. B. (1970) Seasonal changes in temperature acclimatization of the house sparrow, Passer domesticus. Comp. Biochem. Physiol. 33, 559-578. BARTHOLOMEWG. A. (1972) Body temperature and energy transformation. In Animal Physiology: Principles and Adaptations (Edited by GORDONM. S.), 2nd Edn., pp. 298368. Macmillan, New York. BLEM C. R. (1973) Geographic variation in the bioenergetics of the house sparrow. Omith. Monogr. 14, 96-121. BLEM C. R. (1974) Geographic variation in thermal conductance in the house sparrow, Passer domesticus. Comp. Biochem. Physiol. 47A, 101-108. DAWSONW. R. & BENNETTA. F. (1973) Roles of metabolic level and temperature regulation in the adjustment of western plumed pigeons (Lophophapsferruginea) to desert conditions. Comp. Biochem. Physiol. 44A, 249-266. HUDSONJ. W. & KIMZEY S. W. (1966) Temperature regulation and metabolic rhythms in populations of the house sparrow, Passer domesticus. Comp. Biochem. Physiol. 17, 203217. KENDEIGHS. C. (1969a) Energy responses of birds to their thermal environment. Wilson Bull. 81, 441-449. KENDEIGHS. C. (1969b) Resistance to cold and Bergmann’s rule. Auk 86, 13-25. KENDEIGHS. C. (1970) Energy requirements for existence in relation to size of bird. Condor 72, 60-65.
METABOLICADAPTATION TO LOCALCLIMATEIN BIRDS
187
KENDEIGHS. C. (1973) Latitudinal trends in the metabolic adjustments of the house sparrow to its environment in North America. (To be published.) PACKARDG. C. (1968) Oxygen consumption of ik?icrotus montunus in relation to ambient temperature. J. Mammal. 49, 215-220. RISING J. D. (1969) A comparison of metabolism and evaporative water losses of Baltimore and Bullock orioles. Comp. Biochem. Physiol. 31, 915-925. SCHOLANDERP. F., HOCK R., WALTERSV. & IRVING L. (1950) Adaptation to cold in Arctic and tropical mammals and birds in relation to body temperature, insulation, and basal metabolic rate. Biol. Bull., mar. biol Lab., Woods Hole 99, 259-271. TROST C. H. (1972) Adaptations of horned larks (Eremophilu alpestris) to hot environments. Auk 89, 506-527. WEST G. C. (1972) Seasonal differences in resting metabolic rate of Alaskan ptarmigan. Comp. Biochem. Physiol. 42, 867-876. Key Word Index-Birds; house sparrow, Passer domesticus; energy metabolism; logical adaptation; temperature; physiological model.
physio-