Bioenergetics of captive Belding's savannah sparrows (Passerculus sanwichensis beldingi)

Copyright

BIOENERGETICS OF CAPTIVE BELDING’S SPARROWS (PASSERCULUS SANWICHENSIS JOSEPH B. Wm.IAMs*I

and

0300-9629/X 1/0807X3-05J02 00/O c 19x1 Pergamon Press Ltd

SAVANNAH BELDINGI)

HOLLY HANSELL~

*Natural Science

$Department

Division, Pepperdine University, Malibu, CA 90265 and of Biology, University of Oregon, Eugene, OR 97403, U.S.A. (Receiced

23 December

1980)

The basal metabolic rate (BMR) of Belding’s Savannah sparrows averaged 1.48 k 0.07 kJ/g.day and the standard metabolic rate (SMR) below thermoneutrality was best described by the equation y = 4.5 - 0.1x where y equals SMR in kJ/g.day and x ambient temperature in “C. 2. Thermal conductance between 5 and 30°C averaged 4.75 + 0.04 J/“C.g.hr and was higher than most other published accounts for temperate species. 3. During existence energy trials on two different diets, Savannah sparrows ingested more energy as temperature decreased and more energy on the chick starter diet; the equations y = 7.3 - 0.14x and x = 7.0 - 0.14x expressed the relationship of energy intake vs temperature for the chick starter diet and mealworm diet. respectively, where )’ = kJ/g.day. 4. We found no differences in the relationship between existence energy and temperature for the two diets and thus we combined the data; the equation y = 5.1 - 0.1x described the relationship between existence energy and ambient temperature (&30 C). 5. Sparrows metabolized more of the available energy on the mealworm diet (c. 75”/,) than the chick starter diet (c. 69”,). Abstract-l.

quently housed them in individual cages (35 x 25 x 30 cm) within an indoor aviary at 25°C and on a 12 hr photoperiod. We fed birds ad libitium on a diet of chick starter (21.84 kJ/g) or dried (vacuum-dried at 65-C) mealworms (30.01 kJ/g) for at least 30 days prior to experimentation and replenished water supplies daily. During March of each year (1978 and 1979). we released our birds. We determined the basal metabolic rate (BMR) by measuring the rate of CO2 production of postabsorptive birds, at night, in their zone of thermoneutrality (King, 1974) and the standard metabolic rate (SMR) by their CO2 production below their zone of thermoneutrality under the same conditions (Kendeigh, 1977). Our technique, fashioned after Brody (1945), consisted of passing dry, CO,-free air successively via Tygon tubing through a flowmeter, a l-gal metabolism chamber containing a thin layer of mineral oil on the bottom to trap feces, and U-tubes containing Drierite (CaSO,) and Ascarite (NaOH impregnated in asbestos). We placed our metabolism chamber in an environmental chamber that controlled temperature to within 1’C. From the weight lost by the bird and the chamber during the trial (6&90 min) and the weight gained by the tubes. we calculated COZ production, HZ0 loss. and indirectly O2 consumption (see Brody, 1945). From the CO* produced and O2 consumed, we calculated the respiratory quotient (RQ). At O’C water condensed in our Tygon tubing and thus we calculated metabolism using CO, production and an assumed RQ of 0.74 (see below). All birds had food removed 4-6 hr before experimentation and were placed in the l-gal chamber 30min prior to measuring metabolism. The rate of air flow was 1OOOml/min. Using known quantities of COZ, Kendeigh (1939) validated this method and found an accuracy of + 13;. We calculated conductance values (S-35°C) by using the equation of McNab (1980):

INTRODUCTION

The Belding’s

Savannah chensis be/din@) resides

sparrow year-round

(Pqsserculus

sandwi-

in the coastal salt marshes of southern California and Baha Mexico (Van Rossen, 1947). Following the destruction of large areas of their habitat in this region (Macdonald, 1977). the population has declined resulting in the addition of this bird to California’s list of endangered species (Massey. 1979). With only 1600 pairs now extant, information about the biology of this subspecies is of crucial importance. In 1977 Williams initiated a study of the ecology of the Belding’s Savannah sparrow; this report concerns a laboratory investigation of it’s bioenergetics. Our specific goals focused on the determination of basal metabolism, standard metabolism, and existence metabolism, and to compare our calculated values with those predicted by allometric equation from the literature. Weathers (1977) suggested a low basal metabolic rate (BMR) and Kendeigh (1977) hypothesized a high lower critical temperature (T,,) for birds adapted to warm climates; we tested these hypotheses by comparing our results with published data for similar sized birds from different localities. Additionally, since most studies of existence energy (sensu Kendeigh, 1949) have employed one food type, we asked how diet would influence the amount of energy ingested, metabolized, and excreted. MATERIALS AND METHODS We mist-netted 12 individuals in the salt marsh of Pt. Mugu lagoon (34 07’ N, 119 07’ W) in October of 1977 and an additional 12 birds in October of 1978. and subset Present address: Labs-G7, University 19104, U.S.A.

C=

Department of Biology, Leidy of Pennsylvania, Philadelphia, PA

where

(assuming

- H, T.)(M)(l)

the thermal conductance (J/T.g.hrX H, (J), H, the heat lost by evaporation 2.44 kJ/g.H*O), Tb and T. the body and

C equals

the heat of metabolism 783

H, (Tb -

JOSEPH B. WILLIAMS and HOLLY HANSELL

784

temperature, respectively. M the mass of the bird in g. and r the time in hr. We did not measure T,, immediately after respiration trials. but rather by inserting a flexible thermistor into the proventriculus of birds living at each respective temperature (N = 3). The average weight of birds during our respirometry trials was 17.4 & 0.2g (+_I SE). ambient

For diets of drired mealworms or chick starter mash. our measurements of the amount of energy ingested, metabolized and excreted by Savannah sparrows caged at various temperatures followed Kendeigh (1949. 1975). Essentially we placed birds in environmental chambers for 3 days on a I2 hr photoperiod and monitored their food intake and fecal output. At the end of the trial. food and feces were dried at 65 C under vacuum for 24 hr and weighed to the nearest mg. We subtracted the caloric value of the feces (excretory energy) from the ingested energy (gross energy intake) to obtain the amount of energy used (metabolized energy). If birds maintained constant weight ( + l.S’,). then metabolized energy equals existence energy. All caloric determinations were made in duplicate on an adiabatic bomb calorimeter and all values are expressed on an ash-free basis (Paine. 1971). When duplicate values differed by more than 2.5”,, we made additional determinations. Humidity was not controlled but monitored and ranged from 5&75”,, rn our chambers, A total of 136 trials were completed for which 39 and 33 qualified for existence energy on the chick starter diet and mealworm diet. respectively. Birds averaged 17.7 +_ 0.2 g for these experiments, Kendeigh (1949) proposed that the amount of food a bit-d could process had a fixed upper limit determined by inherent physiological constraints. Since we did not want to kill these birds. we estimated the maximum potential energy intake on the chick starter diet by placing birds in environmental chambers at progressively lower temperatures (5 C increments) until they lost weight for 2 consecutive days (N = 4). Birds maintained weight (+2.5”,,) at - IO C for 5 days but all lost weight at - 15 C; 2 birds dted at this temperature after 2 days. We extrapolated from our equations to determine the maximum caloric intake at -10 C. a procedure which seems reasonable since most studies have found gross energy intake to be a linear function of ambient temperature up to the maximum potential energy intake (Kendeigh. 1949. 1977: Owen. 1970).

For quantifying the relationship between energy and T.. we used least-squares regression analysis with ANOVA to test the null hypothesis that h = 0. Slopes and elevations of regression equations were compared with r-tests. ANOVA was employed to test for overall differences between means and the Newman-Keuls test for differences between pairs of means (Zar. 1974). All ratios were transformed by the arcsine transformation before analysis (Sokal & Rohlf. 1969). and we present all mean values + I SE. For purposes of conversion, I kcal = 4.184 kJ. RESULTS

Our respirometry experiments revealed that Belding’s Savannah sparrows possessed a rather narrow range of thermoneutrality around 30’C and their BMR (N = 6) averaged 1.48 f 0.07 kJ/g.day (x wt for birds at 30’C = 16.7 + 0.7 g). Thermogenesis, presumably by shivering (West, 1965), increased with temperatures below 3OC and at OC required an energy expenditure of 4.5 kJ/g.day, a value 2.9 x BMR (Fig. 1. Table 1). Birds also increased their metabolism at 35C (2.1 i 0.01 kJ/g.day) above the basal level at 30’C (t = 4.2, P < O.OOl), indi-

0

IO

20 Temperature,

30

35

*C

Fig. I. Regression lines showing the relationship between gross energy intake, existence energy. excretory energy. standard metabolism, and temperature (G3O’C) for Belding’s Savannah sparrows. The lines with single dots and with single dashes represent gross energy intake on chick starter mash and dried mealworms. respectively. The solid line shows existence energy for both diets combined, the dashed line. standard metabolism. The line with two dots represents excretory energy on the chick starter diet, with two dashes represents mealworm diet. Statistics and equations and in Table 1. Mean values for gross energy intake, existence energy and excretory energy for birds feeding on chick starter mash. and standard metabolism at 35 C are also shown, The 95”/, confidence intervals for these values are +0.2, kO.2, +0.3. 50.2, respectively. (N = 8 all cases.)

eating perhaps that they increased evaporative cooling by panting, an activity which requires added energy expenditure (Calder & Schmidt-Nielsen, 1967). Because we noticed birds occasionally moving in our metabolism chambers at this temperature, we cannot attribute all of the increase in energy expenditure to panting. Water toss and the resulting heat loss by evaporation remained relatively constant from 5-30 C but markedly increased at 35 C (Table 2). The heat loss due to evaporation averaged 0.46 kJ/g.day from 5-30 C but rose to 0.98 kJ/g.day at 35’C. By averaging conductance values measured at 5 - 30°C (Table 2) we estimated conductance (McNab, 1980) to be 4.75 + 0.04 J/C g. hr (N = 30). King & Farner (1961) suggested that the best estimate of RQ for fasting, postabsorptive birds was 0.73. a value close to our measurement of 0.74 _I 0.01 (N = 36) for Belding’s Savannah sparrows. During existence energy trials, sparrows ingested more energy as temperature decreased and more energy on the chick starter diet than on dried mealworms (Fig. 1, Table 1). Similarly, the energy content of the feces increased with decreasing T. and was higher on the chick starter diet. For existence energy on the two diets, we found no difference between regression equations (Table 1). At 35 C birds consumed 3.2 _t 0.1 kJ/g.day). metabolized 2.3 rt_ 0.1 kJ/

785

Bioenergetics of captive Belding’s Savannah sparrows Table 1. The relationship between temperature (&3O”C) and a number of variables for Belding’s savannah sparrows living on two diets, chick starter mash and dried mealwormst

Equation (+ Sy .x) 1. Gross energychick starter 2. Gross energymealworms 3. Existence energydata combined 4. Excretory energychick starter 5. Excretory energymealworms 6. Standard metabolism

(N)

(kJ/g day)

I-2

F-slope$

(39)

y = 7.3 - 0.14x If: 0.58

0.90

296.6*

(33)

y = 7.0 - 0.14x + 0.50

0.89

348.1*

(72)

y = 5.1 - 0.10x _+0.40

0.89

591.38

(39)

y = 2.3 - 0.40x + - 0.20

0.90

228.6*

(33)

y = 1.8 - 0.04x + 0.16

0.87

224.2*

(36)

y = 4.5 - 0.10x + 0.31

0.90

422.7+

r-test comparison elevation5 1 “S 2 (t = 4.3*)

4 (t = 6 (t =

“S 5 10.4*) vs 3 lo.o*)

t We found no difference between comparisons of slope (r = 0.48) or elevation (t = 0.09) for regression equations of existence energy. $* Indicates P < 0.001. 4 For all comparisons, slopes were insignificantly different, P z 0.1.

g .day, and excreted 0.98 + 0.01 kJ/g .day; these are similar to values at 30°C (t = 0.6,0.2, 1.6, respectively, P > 0.05 in all cases). Existence energy, which integrates basal metabolism, thermoregulation, the heat increment of feeding, and minimal locomotor activity over several days, was 1.1 x higher than standard metabolism at temperatures of 0-30°C (Table 1). Data for the efficiency of energy utilization, defined as the ratio of metabolized to ingested energy (Zimmerman, 1965), indicated that birds assimilated a constant proportion of energy over the range of temperatures that we tested them for both diets, but their efficiency was higher for the insect diet (Table 3). Birds averaged c. 69% efficiency on the chick starter diet and c. 75% on the mealworm diet.

DISCUSSION

Belding’s Savannah sparrows live in a maritime climate where they rarely experience cold tempera-

tures; ambient air temperatures average around 20 and 15°C during the breeding (April-July) and nonbreeding (September-March) seasons, respectively (de Violini, 1975). When they forage along tidal creeks and on salt pans during the summer, they at times experience temperatures of 3040°C (personal observation). Since birds living in warmer climates often possess a lower BMR (Hudson & Kimzey, 1966; Weathers, 1977) we predicted that the BMR of the Belding’s race (1.48 kJ/g . day) would be lower than species of similar size adapted to cooler environments. The data of Table 3 supports this idea. For example, birds from temperate areas such as the redpoll (A. jamma), goldfinch (C. carduelis), and chaffinch (F. coelebs) showed a higher BMR than Belding’s Savannah sparrows but species from warm climates did not. Unfortunately Kendeigh (1977) did not publish estimates of variability for the BMR of C. carduelia and F. coelebs and therefore we cannot statistically compare our results with his.

Table 2. Evaporative water loss, conductance and efficiency of energy use on two diets for Belding’s Savannah sparrows*

0 Water loss! (N = 36) Conductancef Efficiency of5 energy usechick starter diet (N = 44) Efficiency of energy usemealworm diet (N = 33)

68.7 k 0.2

75.lkO.6

Temperature (“C) 20

5

10

8.8 + 0.4”

7.3 * 0.3b

7.8 k 0.4’

3.95 * 0.3a.’ -

4.52 f 0.2b 69.3 + 0.5

4.84 f 0.1’ 67.0 + 1.5

5.6 t 0.4d.’ 69.0 f 0.5

73.5 + 0.5”

75.5 + 1.5

16.4 + 0.5”

-

30 7.8 * 4d

35 16.8 + l.la.b*c.d 7.32 + 0.8”.b.c.d 71.1 + 0.5

* Letters indicate values significantly different, P c 0.05. All values + 1 SE. t Values for evaporative water loss in mg H,O/g.hr. F = 41.6, P < 0.001. 1 Values for conductance in J/“C.g.hr. F = 11.2, P c 0.005. 5 Efficiency of energy use defined as metabolized energy divided by gross energy intake. After arcsine transformation, F = 2.4, P < 0.05 chick starter mash; F = 5.5, P -t 0.01, mealworm diet.

JOSEPH B. WILLIAMS and HOLLY HANSELL

786

Table 3. A comparison

of the BMR (kJ:g,day)

of the Belding’s Savannah

sparrow

with species of similar

size from other localities*t

Species

(N)

Acanthij jlammea (7) Carduelib cardurlis (‘?) Frinrtilltr wrlrhs (‘!) Pusskulus auntlrrichmsis Ptr.ucrcul~rs stmdrvichmsis ;~l~~ntrcus ritrllim4.s (1 1)

(6) (3)

Location

Mean Wt (9)

Alaska Russia Russia Southern California Florida Central Panama

15.6 16.5 20.8 16.7 15.9 15.6

BMR 2.27 i 0.11 1.83 1.83 1.48 _t 0.07 1.2 * 0.07 1.53 f 0.07

f-value 6.42**

2.35* 0.50

Source: Pohl & West (1973) Kendeigh (1977) Kendeigh (1977) This study Yarbrough (1971) Vleck & Vleck (1979)

* Indicates P < 0.05: **P < 0.001 t All data taken in winter during the night except for M. citrllinu.s which was taken during September. : Conversions to kJ:g.day were made by assuming 20.08 kJ,ccOz.

The allometric equations of Lasiewski & Dawson (1967). AshoR & Pohl (1970). and Kendeigh (1977) predict a BMR of 1.67 _t 0.3 kJig,day. 1.47 & 0.2 kJ’ g’day. and 1.77 + 0.3 kJ;g.day, respectively. for a 16.7 g Savannah sparrow. Though these values are statistically indistinguishable from the BMR that we measured (r = 0.3, 0.03. 0.4. respectively: P > 0.05 all cases). the equation of AshofT & Pohl (1970) varied the least ( -c l”,,) and that of Kendeigh (1977) the most GO”,,). InhabItants of warmer environments often display a higher r,, defined as the temperature at which the tnetabolic rate increases in order to maintain constant body temperature (Kendeigh, 1977). than species living at cooler latitudes (Schmidt-Nielsen. 1979). For Belding’s Savannah sparrows the allometric equation of Kendeigh (1977) predicts a T,, of 19.9 C. a value much lower than we measured. This indicates that the insulating ability of their plumage is relatively low. WC suggest that the plumage of the Belding’s race may be adapted to meet periods of heat stress when heat dissipation may be important, for example. when they are actively foraging on salt pans. Two other studies on birds at southern latitudes. Trost (1972) working with horned larks (Eremophil~l ulprsrris) from southern California and MacMillen (1974) with two species of honeycreeper (Locops tirens and L. parra) from Hawaii, found a T,, around 30 C. That Savannah sparrows have a high T,, suggests a high rate of heat loss to their surrounding: two lines of evidence indicate that this is true for Belding’s. First. our measure of the temperature coefficient h (h = the rate at which the SMR changes per degree change in T,) is higher than the coefficient predicted by the allometric equations of Kendeigh ~lt trl. (1977) (h = 0.082 kJ,g.day, Kendeigh: b = 0.10 kJ/g.day, this study). Second, our measure of conductance is higher than most of the published accounts for birds living at more northerly latitudes (Drent & Stonevalue house. 1971). and higher than the 3.98 J’ C’g’hr predicted by the allometric equation published by Lasiewski er al. (1967). All avian species studied thus far increase their rate of breathing during heat stress. thereby facilitating evaporative cooling (Lasiewski. 1972). However. we interpret our results of increased water loss ccupled with increased energy expernditure at 35 C with some caution because we noticed birds were not completely quiescent at this temperature. Therefore. we do not

August

and

attribute the increased HZ0 evaporation and energy expenditure at 35-C solely to panting but also to an increase in activity. During our existence energy trials at 35 C, we observed birds panting but this behavior did not increase the quantity of energy they metabolized. In experiments on the roadrunner (Geococc!x californicus) and the pigeon (Colt&u licia). metabolism did not increase until these birds experienced temperatures of 4o’C (Calder & Sct?midt-Nielsen. 1967) and Kendeigh (1939) found that house sparrows (Passer domesticus) lost a constant amount of water at ambient temperatures of 24-35 C. Sparrows ingested more total energy on the chick starter diet suggesting that they could not digest this food as efficiently as dried mealworms and the data of Table 2 supports this idea. Yet inspite of the differences in digestive efficiency between diets and differences in the caloric content and presumably in nitrogen content, birds required the same quantity of energy for existence on each diet. Kendeigh (1977) showed that caged birds usually require an existence energy expenditure of about 1.3-1.4 times greater than their SMR. Our values indicate that caged Savannah sparrows mobilized 1.1 x more energy than they did under standard conditions. Birds living at - 15-C rapidly lost weight, but those caged at - 1O’C maintained weight. Kendeigh (1949) postulated that the lowest temperature at which birds could sustain themselves gave an indication of the maximum amount of energy that their physiological machinery could process, and that the difference between the maximum potentially available energy and the existence energy at a given temperature represented the energy available for reproductive processes. This hypothesis. supported by the studies of Kontogiannis (1968) and Hart & Heroux (1955), predicts that the daily energy expenditure of free-living Belding’s Savannah sparrows cannot exceed 8.1 kJ, g.day or 145 kJ/day for an 18.0 bird. the average weight of free-ranging sparrows at Pt. Mugu. We are currently testing this hypothesis using the doubly labelled water technique (Nagy, 1975, 1980). The allometric equations presented by Kendeigh (1977) predict an existence eneru expenditure of 4.71 and 2.43 kJ/g.day for a 17.7 g (X wt of birds during existence energy experiments) Savannah sparrow caged at 0 and 3O’C, respectively. These values represent 7-14% deviations from our measured values.

Bioenergetics

of capiive

Betding’s

A~hno~oledgrm~nts-We wish to express appreciation to Pepperdine University for computer time and for funds for laboratory equipment. Drs J. Quinn, R. Ricklefs, L. Clark and S. C. Kendeigh provided comments on an earlier draft. Dr George Bartholomew kindly gave us advice about our experimental design.

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