Thermoregulation and water loss in the Inca dove

Comp. Biochem. Physiol., 1967, Vol. 20, pp. 263 to 273. Pergamon Press Ltd. Printed in Great Britain

T H E R M O R E G U L A T I O N A N D WATER LOSS IN T H E INCA DOVE R I C H A R D E. M a c M I L L E N

and C H A R L E S H. T R O S T *

Department of Zoology, Pomona College, Claremont, California 91711, U.S.A. (Received 27July 1966)

Abstract--1. The small Inca doves (weight 42 g) of the southern Arizona deserts live an urban existence where water is continually available but where temperature fluctuations are extreme. 2. Nocturnal body temperatures are significantly lower than in daytime, but pulmocutaneous water loss rates are reduced at night primarily by metabolic reductions and extreme quiescence. 3. The standard daytime metabofic rate is 1"11 cm 3 0 J g / h r in thermal neutrality at Ta = 35 °C; this is 21 per cent below that predicted from the KingFarner equation for non-passerine birds, thereby effectively reducing metabolic heat production. 4. Under conditions of high Ta (> 35 °C) hyperthermia is pronounced. But gular flutter commences at Ta=42°C, increasing evaporative cooling and decreasing the T B - T a gradient. At Tx = 44°C metabolic heat is dissipated as fast as it is produced and equality of TB and T a is maintained. INTRODUCTION THE INCA DOVE, Scardafella inca, is one of the smallest of N o r t h American doves, weighing about 42 g. While its general distribution in the United States is wholly desert, the Inca dove's habitat cannot be so defined for it is confined to settlements in Arizona, New Mexico, and Texas (Bent, 1932). This confinement to an urban existence appears to be related to the Inca dove's relatively high water requirements, since hypotonic drinking water must be almost continually available for survival (MacMillen & Trost, 1966). But even an urban existence does not enable an organism to escape completely the extreme heat and aridity of the desert summer days, nor the nocturnal periods when usual avian behavioral limitations preclude drinking and eating. In addition, the small size of the Inca dove imparts further problems related to heat production, heat dissipation, and water loss, particularly during the hot summer days. This study deals, then, with the diurnal and nocturnal relations between body temperature (TB), ambient temperature (T~), oxygen consumption, and pulmocutaneous water loss, in an attempt to understand better the means by which the Inca dove flourishes in an urbanized desert environment. Parts of this study were summarized earlier by MacMillen & T r o s t (1965). * Present address: Department of Zoology, University of California, Los Angeles, California 90024, U.S.A. 263

264

RICHARD E. MACMILLEN AND CHARLES H. TROST

MATERIALS AND METHODS

Experimental animals The 41 adult Inca doves employed in this investigation were all collected in Tucson, Pima County, Arizona between September 1964 and July 1965. They were shipped by air to California, invariably arriving in the laboratory in excellent condition within 24 hrs of initial departure. Except during measurements, the doves were housed in individual cages in a windowless room on a 12-hr photoperiod (lights on from 0600 to 1800 hr). Each animal was provided in excess with tap water for drinking and mixed bird seed for food. The mean initial body weight of postabsorptive doves after at least a week of adjustment to laboratory conditions was 41.5 + S.D. 2.4 g.

Body temperatures Body temperatures were measured simultaneously with measurements of oxygen consumption and pulmocutaneous water loss, using silver-soldered copperconstantan thermocouples connected to a recording potentiometer equipped with a dual-channel switching mechanism. The TB thermocouples were made of annealed wire, 0.0063 or 0.01 in. dia., ensheathed in small-bore polyethylene tubing for insulation. The thermocouples were surgically implanted with the junction embedded in the pectoral musculature at a depth of about 1.2-1.5 cm and immediately against the keel. The thermocouple leads were glued to the skin at their points of exit and then drawn up behind the wings and through a large glass bead which was glued mid-dorsally to the feathers; the loose leads projected freely from the bead for about 6 cm. During measurements of T B the plastic-ensheathed leads were attached to 30 gauge dual thermocouple wire leading through a sealed port in the respirometer chamber to the recording potentiometer. Only healthy animals were used for measurements, allowing at least 5 days for recovery from the implantation. Only rarely was noticeable injury sustained as a result of the implantation procedure, and some of the implanted thermocouples remained usable for several months.

Ambient temperatures Ambient temperature was monitored with a thermocouple projecting through a sealed port into the respirometer chamber and connected to the potentiometer. TA was recorded for 5-min periods alternating with 5-min recordings of TB, and was controlled within + 0.1 °C by placing the respirometer chamber in an insulated constant-temperature cabinet equipped with automatic heating and cooling units, blowers and lights.

Oxygen consumption Measurements of oxygen consumption were made on an animal in an air-tight 3-8 1. (1 U.S. gal) respirometer chamber, placed within the constant-temperature cabinet, and equipped with TB and Ta thermocouples as well as ports for the introduction and removal of air. The animal rested on a hardware-cloth platform

T H E l t M O R E G U L A T I O N A N D W A T E R LOSS I N T H E I N C A DOVE

265

6 cm above the bottom of the chamber which was covered to a depth of 1 cm with mineral oil to prevent evaporation from excreta. Air which had been dried by passage through indicating Drierite was metered to the respirometer chamber, through which it flowed at a rate of 500 cm3/min. Samples of air flowing from the chamber were then delivered to a Beckman Model E2 paramagnetic oxygen analyzer for measurements of oxygen consumption. Oxygen consumption was corrected to S.T.P. All measurements of oxygen consumption were made on post-absorptive but non-starved animals at least 1 hr after having been placed in the respirometer chamber. Animals were allowed at least 1 hr of adjustment to a given T A prior to measurements at that T~; 5-7 measurements were made at intervals of 10-15 min over a period of 1 hr at each T a. The two lowest measurements for each animal at each T a were used in the calculations of oxygen consumption. The means of all the measurements for a 1-hr period at each T~ were used in representing water loss as a function of oxygen consumption, and in relating heat production to evaporative heat dissipation. Pulmocutaneous water loss

Pulmocutaneous water loss was measured for 1-hr periods at each Ta simultaneously with, and using the same experimental procedures employed in, the measurements of oxygen consumption. A relatively high flow of dried air was delivered through the respirometer chamber at a rate of 500 cm3/min to minimize the rebreathing of expired air. Air leaving the respirometer chamber was passed through a 150 mm desiccating tube containing small-mesh calcium chloride in order to capture water vapor contained in the expired air. Water loss was measured gravimetricaUy to the nearest 0-01 rag. In representing water loss as a function of oxygen consumption, and in relating heat production to evaporative heat loss the collected water vapor was treated as a gas volume and corrected to S.T.P. Diurnal measurements

Simultaneous measurements of Ta, oxygen consumption, and pulmocutaneous water loss were made during the daytime (between 0600 and 1800 hr) under both illuminated (daytime-light measurements) and darkened (daytime-dark measurements) conditions. In addition, measurements of T B were obtained from daytimedark birds, but not from daytime-light birds whose activity invariably resulted in extreme twisting of thermocouple leads. Under illuminated conditions, presumably eliciting near normal diurnal responses, animals were housed in a clear glass respirometer chamber and the interior of the constant temperature cabinet was illuminated with a 15 W incandescent light bulb. Under darkened conditions, presumably yielding standard diurnal physiological data, the animals were housed in an opaque respirometer chamber constructed from a metal paint can and the interior of the constant-temperature cabinet was not illuminated.

266

RXCX-lXaDE. MAcMILLmq~,tqDCrmagm H. Taosr

Nocturnal measurements Since it was determined that Inca doves could not readily be photo-reversed (at least in their T B and metabolic responses), nocturnal measurements of all the parameters outlined above were made between 1900 and 0400 hr under darkened (eliciting normal nighttime responses) conditions using an opaque respirometer chamber. RESULTS Body temperatures T h e responses of body temperatures of both daytime-dark and nighttime birds to various ambient temperatures and after at least 1 hr exposure to each T a are summarized in Fig. 1. Below T a = 30°C (approximating the usual range of natural nighttime temperatures) mean TB of nighttime birds is generally and significantly 41t

o 0

46

~ 44 5

n~ 4~ w o~

II 6

6

5

4c

?

~al 38 J 5

I0 AMBIENT

L 15

20

25

J 50

35

40

45

TEMPERATURE ,°C

FIG. 1. The relationship between body temperature and ambient temperature in postabsorptive Inca doves in the dark by day and by night. The vertical lines represent the ranges. The horizontal lines represent the means. The rectangles inclose the intervals ,~ + 2 S.E. The numbers represent the number of animals measured. The solid line connects the means of daytime-dark birds, and the broken line connects the means of nighttime birds. In this and in all subsequent Figures all measurements were made within +_0.5 °C of the ambient temperatures indicated. lower than mean T B of daytime birds at the same Ta, with essentially no overlap of ranges. At T a = 30°C nighttime Tn is slightly elevated but still substantially lower than that of daytime birds. At T a = 35 °C (thermal neutrality) T B of nighttime birds is increased still further and is very close to the slightly elevated level of daytime birds (40.2 versus 40"7°C, respectively). Above T a = 35°C both nighttime and daytime birds experience pronounced hyperthermia of equal magnitude; at T a = 40°C, nighttime TB = 42"7°C and daytime TB = 43"0°C. Although not measured in nighttime birds, hyperthermia in daytime birds at T~ = 44°C is still more pronounced with TB = 44"3°C.

THERMOREGULATION AND WATER LOSS IN THE INCA DOVE

267

Oxygen consumption Measurements of oxygen consumption over a wide range of Ta in daytime and nighttime birds indicate that nighttime birds are generally lowest, daytime-light birds are generally and significantly highest, and daytime-dark birds are intermediate in position (Fig. 2). Although oxygen consumption rates of nighttime birds are lowest they are very similar to those of daytime-dark birds and are significantly lower only at T ~ = 15°C. Both nighttime and daytime-dark birds have a very narrow thermal neutral zone of Ta=ca. 32-35°C, with standard metabolic rates of 1.16 + S.D. 0.08 and 1-11 + S.D. 0.11 cm 3 O2/g/hr, respectively. 5.0 N= 18-22 (9-li)

4.0

~ 5.0

........... %.i°........... !O~o

....,......

I.G

AMBIENT TEMPERATURE,°C

FIo. 2. The relationship between oxygen consumption and ambient temperature in postabsorptive Inca doves by day and by night. The horizontal lines represent the means (.~). The vertical lines represent the intervals X + 2 S.E. The broken line composed of open squares connects the means of daytime-light birds; the solid line connects the means of daytime-dark birds; the broken line composed of closed circles connects the means of nighttime birds. N = the number of measurements at each temperature and for each sample (the number of birds employed). B-P represents the level of standard metabolism for birds of the size of these Inca doves predicted by the equation of Brody & Proctor (1932); K - F represents the level of standard metabolism predicted by the equation for non-passerine birds of King & Farrier (1960). T h e more active daytime-light birds have a broader thermal neutral zone extending from 30 ° to at least 40°C, with a mean metabolic rate within that zone of 1.68 _+ S.D. 0.37 cm 8 O2/g/hr. Above thermal neutrality both nighttime and daytimedark birds demonstrate a slight but steady increase in oxygen consumption which, in daytime-dark birds at Ta = 44°C, represents an increase of 38.7 per cent above standard metabolism ( T ~ = 3 5 ° C : l ' l l + S . D . 0.11 cm a O2/g/hr vs. T ~ = 4 4 ° C : 1"54_+ S.D. 0-35 cm a OJg/hr). Also included in Fig. 2 for comparative purposes are standard metabolic rates for birds of the mean weights of these Inca doves (daytime-light, 37.9 g; daytimedark and nighttime, 40.5 g) predicted by the equations of Brody & Proctor (1932), and King & Farner (1960). T h e equations employed are restatements of the

268

RICHARD E. MAcMILLEN AND CHARLES H . TROST

originals, expressing metabolism in cm 3 O2/g/hr after Hudson & Brush (1963). In these terms the Brody-Proctor equation is cm 3 0 ~ / g / h r - 9 - 3 g-0.36; that by King-Farner (cm 3 0 J g / h r = 3 . 7 8 g-0.266) is a restatement of their equation 6 (King & Farner, 1960) for predominantly non-passerine birds weighing more than 125 g. All of the standard metabolic rates measured in Inca doves are considerably below the rate predicted by the Brody-Proctor equation. While the daytimelight active birds exhibit a standard metabolism higher than the King-Farner extrapolation for birds of that weight, standard metabolisms of both daytime-dark and nighttime birds are about 20 per cent below the King-Farner extrapolation (1"11 and 1.16 versus 1.41 cm 30~/g/hr, respectively).

45 4O >.- 35 Q

"~ 3 0 125 I

I--: ~ 2O 0 IXI

IOi

.......... .................... '

......

~

L5

, 2b

.

15

~

3~

4'o

AMBIENT TEMPERATURE,"C

FIG. 3. The relationship between pulmocutaneous water loss and ambient temperature in postabsorptive Inca doves by day and by night. N = the number of birds measured; otherwise symbols as in Fig. 2. The broken line composed of open circles conneets the means of daytime-light birds; the solid line connects the means of daytime-dark birds; the broken line composed of closed circles connects the means of nighttime birds.

Pulmocutaneous water loss

In pulmocutaneous water loss (Figs. 3 and 4) the same general relationship between daytime-light, daytime-dark, and nighttime birds exists as did in the studies of oxygen consumption (Fig. 2), with the former active birds exhibiting the highest rates and the latter inactive birds having the lowest rates.

TITERMOREGULATION

269

AND WATER LOSS IN THE INCA DOVE

Expressed in terms of per cent body weight in water lost per day (Fig. 3) the rate of water loss under each condition is nearly stable between T a = 5 and 35°C. Above thermal neutrality the water loss rates increase markedly, and at T~ = 44°C the mean water loss rate for daytime-dark birds is 37-7 per cent of body weight per day, or approximately 5 times that of the same birds in thermal neutrality (37.7 versus 7.5 per cent body weight per day, respectively). 10.C

,zOo() x c) (z.

:oo F / 60)

8.0

/

6.0

F

P ,.'~ 6o!= ILl -r' -...

F

/

c~ o

N =9-11

¢,o o~

= ,~Oi=

2.0

--" L~.I' 20'k 5

I0 CMBiENT

15

20

25

TEMPERATURE

50

35

40

45

, °¢

FIG. 4. The relationship between evaporative cooling, metabolic heat production, and ambient temperature (or between pulmocutaneous water loss as a function of oxygen consumption and ambient temperature) in postabsorptive Inca doves. Symbols as in Fig. 3. In Fig. 4 are pulmocutaneous water loss data expressed both in terms of its significance in heat dissipation, and as a function of oxygen consumption. In expressing the relation between metabolic heat production and heat dissipation through evaporative water loss it is assumed that 1 cm 8 02 consumed yields 4.8 cal, and 1 mg H~O evaporated dissipates 0-58 cal. Under all conditions of time and illumination tested the results are nearly identical with a direct relation between the effectiveness of evaporative water in heat dissipation (or water loss as a function of oxygen consumption) and ambient temperature (Fig. 4). There is a marked increase above thermal neutrality and at T~t =44°C daytime-dark birds are able to dissipate on the average 107.2 per cent of the metabolic heat that is produced. Although previously dried air was monitored to the animal in the respirometer chamber, each animal introduced water vapor into the chamber through its pulmocutaneous water loss. Therefore the air passing through the chamber was not consistently dry, its degree of saturation with water vapor depending upon T~, flow rate, and water-loss rate of the experimental subject. The approximate relative humidities inside the respirometer chambers for the various experimental conditions were calculated after the method employed by Bartholomew & Dawson (1953) relating the humidity mixing ratio of saturated air to that in the respirometer chamber; the relative humidities achieved under experimental conditions are summarized in Table 1.

270

RICHARDE. MACMILLENAND CHARLESH. TROST

TABLE 1--MF~aLNRELATIVE H U M I D I T Y

INSIDE RESPIROMETER CHAMBER DURING MEASUREMENT OF PULMOCUTANEOUS WATER LOSS, OXYGEN CONSUMPTION~ AND BODY TEMPERATURE

Daytime-light (% R.H.) Daytime-dark (% R.H.) Nighttime (% R.H.)

5

15

75.5 78.2 60"6

52.9 36"1 27"2

Ambient temperature (°C) 25 30 35 30.5 20"0 17"3

19-8 14"6 13"6

20.1 12"4 12.6

40

44

25.8 20"7 26"5

-53"0 --

DISCUSSION In spite of the Inca dove's urban environment and its apparent dependence upon an abundant source of fresh drinking water these birds have several rather remarkable attributes which enhance survival under general desert conditions. These attributes are primarily related to manipulations of thermoregulation rather than to water economy, which is consistent with the Inca dove's confinement to urban situations: there, water is in continual abundance and water deficits can be readily made up, but seasonal and daily temperature fluctuations are nearly as great as in rural desert areas. The one notable water-conserving mechanism evident in the Inca dove is the reduction in pulmocutaneous water loss during the night (Fig. 3). Although accompanied by a significant reduction in T B in the range of T~ typical of southern Arizona nights (5-25°C), both oxygen consumption and pulmocutaneous water loss rates of nighttime birds are only slightly and insignificantly reduced below those of daytime-dark birds within the same T~ range (Figs. 2 and 3). This rather great nocturnal reduction in T B is not due to circadian differences in thermal conductance, which remains essentially constant both day and night and across a wide range of T a (Table 2). Instead the reduction in T B apparently is related to the slight reduction in nighttime metabolism together with greater quiescence. Nocturnal quiescence seems to be the primary key to water saving compared to daytime-light birds whose greater activity results in increased metabolism, very likely increased TB, and greatly increased pulmocutaneous water loss (Figs. 2 and 3). This nocturnal reduction in pulmocutaneous water loss would be particularly meaningful during the hot, dry summer period in southern Arizona when diurnal T~ continually exceeds thermal neutrality and nocturnal Ta is well below thermal neutrality. These circadian differences in T~ and water loss might consistently result in daytime active birds losing three to five times more water than quiescent nocturnal birds; such losses can readily be made up by drinking in the daytime, but nighttime birds must tolerate the reduced water losses until dawn. The diurnal adaptations of metabolism and thermoregulation are more striking than the nocturnal ones, at least as revealed in this investigation. At T~ below thermal neutrality Inca doves show typical avian responses, but in and above thermal neutrality they deviate significantly from the typical avian pattern. As shown in Fig. 2 the standard metabolic rates are about 20 per cent below those

271

THERMOREGULATION AND WATER LOSS I N THE INCA DOVE

predicted by extrapolation of the K i n g - F a r n e r equation for non-passerine birds. This reduction correspondingly minimizes heat production which is particularly meaningful during the hot summer days in southern Arizona when T a consistently exceeds thermal neutrality. TABLE 2--THERMAL

CONDUCTANCE* OF DAYTIME--DARK AND N I G H T T I M E INCA DOVES AT VARIOUS AMBIENT TEMPERATURES

Thermal conductance (cm 8 O2(g.hr.°C) -1) Daytime-dark Nighttime

Ambient temp. (°C) 5 15 25 30 35 40 44

0"11 0.11 0"11 0-14 0"20 0-46 5"13

0-10 0.11 0.12 0.14 O.22 O.54 -

-

* Thermal conductance was calculated from the relationship C = M R (Metabolic rate)/ T B - Ta, after Hudson & Brush (1964).

4°F!

-+5

t

~.< 20l

5

I0

15

20

25

30

35

40

45

AMBIENT TEMPERATURE .~*C

FIG. 5. The relation of the difference between body temperature and ambient temperature to ambient temperature in daytime-dark, postabsorptive Inca doves. The broken line represents the level at which T~ = Ta. The vertical lines represent ranges. Horizonal lines represent means. Rectangles inclose the intervals ,Y+ 2 S.E. Numbers represent the number of animals measured. Like most birds Inca doves undergo a marked hyperthermia above thermal neutrality(Fig. 1). But unlike most birds studied, and even though 2 doves survived for 1 hr each with T B = 47°C only to die at TB > 47"0°C, this hyperthermia generally extends only up to T a = 44°C at which T B = T a (Fig. 5). Hyperthermia is accompanied by a marked increase in the rate of pulmocutaneous water loss; this is particularly evident in daytime-dark birds at T a > 4 0 ° C (Fig. 3). At T a = 4 2 ° C Inca doves become very quiescent and commence fluttering the gular area rapidly

272

RICHARD E. MACMILLEN AND CHARLES H . TROST

to promote maximal evaporative cooling; the cooling effects of gular flutter become even more evident at T a = 4 4 ° C . This relative inactivity together with gular flutter results in a very favorable relationship between evaporative cooling and metabolic heat production such that at T a = 44°C Inca doves are able to dissipate heat as fast as it is produced (Fig. 4). Figure 6 shows the course of body temperature in 11 daytime-dark Inca doves for 110 min following a rapid increase in T4 from 40 to 44°C. One of the 11 birds remained hyperactive, became extremely hyperthermic, and died at T B = 47.6°C ; the remainder became quiescent, increased the rate of heat dissipation through gular flutter, and after 110 rain had mean T B = 44.3 °C. Although Inca doves were not subjected to T a > 44°C, extrapolation of the relation between T B - T ~ and T a (Fig. 5) suggests that at T a = 4 5 ° C at least equality of T B and T a would be maintained.

P dt w tw IM la. t/./ I).O m

20

40

60

80

I00

120

MIN

FIG. 6. The relationship between body temperature and time in eleven Inca doves whose ambient temperature was increased rapidly from 40 ° to 44°C. The shaded area incloses the range of body temperatures of 10 of the 11 birds; the solid line within the shaded area represents the mean body temperature of all 11 birds. The solid line above the shaded area represents the response of the eleventh Inca dove which became abnormally hyperthermic and perished after about 70 min. Maximum daytime summer temperatures in Tucson seldom exceed 44°C, although on 19 June 1960 a record high of 46.1°C was recorded (O'Connor, 1960). T h u s gular flutter must be looked upon as an emergency cooling device with a primary reliance upon hyperthermia and behavioral thermoregulation. The role of behavioral thermoregulation is supported by the observation that during the hottest part of the summer Inca doves are active in the mornings and evenings, and spend the midday periods of maximal T a quietly sitting in the shade in trees. When T a approaches 44°C gular flutter is employed but only to the extent that T B = T~, thus there is an appropriate compromise between hyperthermia and evaporative cooling (or water conservation and water expenditure) resulting in

THERMOREGULATIONAND WATERLOSS IN THE INCADOVE

273

essentially no further heat gain f r o m the environment as would occur if T B < T a. I t m u s t be mentioned, however, that the effectiveness of gular flutter as a heatdissipating m e c h a n i s m at 44°C was measured in an atmosphere with a relative humidity of about 53 per cent (see T a b l e 1), which is at least two to three times greater than that of a m i d s u m m e r day in southern Arizona at T4 = 44°C. I n lower humidities at T A = 44°C gular flutter would result either in T B < T~ or, with a controlled reduction of heat dissipation, T B = T~. While the rate of gular flutter was not measured it is clear that its energy cost is very low when operating at maximal efficiency as a heat dissipating mechanism. T h e low energy expenditure is particularly apparent for d a y t i m e - d a r k birds in comparing the increases in T~, rate of oxygen consumption, and rate of p u l m o cutaneous water loss from T A = 3 5 to 44°C (Figs. 1,2,3). T h e Q-10's of the slopes of these increases in TB, oxygen consumption, and water loss are 1.1, 1.4, and 5.6, respectively; thus in this TA range water loss by gular flutter increases at a rate four times that of oxygen consumption and five times that of T B. T h e s e observations augment the suggestion of Lasiewski & Bartholomew (1965) that gular flutter acts as a resonating system in birds, and hence operates with minimal energy cost. While the rate of energy expenditure is low during gular flutter, the rate of water loss is very high. However, an urban existence ensures a continual availability of drinking water for the Inca dove, with which water expenditures are readily replenished. Acknowledgements--We are grateful to Dr. L. H. Blankenship, Mr. J. C. Truett, and Mr. G. L. Richardson of the Cooperative Wildlife Unit, University of Arizona for aid in obtaining birds. This investigation was supported by National Science Foundation Grant GB-2459.

REFERENCES BARTHOLOMEWG. A. & DAWSONW. R. (1953) Respiratory water loss in some birds of southwestern United States. Physiol. Zo61. 26, 162-166. BENT A. C. (1932) Life histories of North American gallinaceous birds. Bull. U. S. natn. iYIus. 162, 490. BRoDY S. & PROCTOR R. C. (1932) Growth and development, with special reference to domestic animals. XXIII. Relation between basal metabolism and mature body weight in different species of mammals and birds. Res. Bull. Mo. Agric. Exp. Stn. 166, 89-101. HuDsoN J. W. & BRUSH A. H. (1963) A comparative study of the cardiac and metabolic performance of the dove, Zenaidura macroura, and the quail, Lophortyx californicus. Comp. Biochem. Physiol. 12, 157-170. KIN(; J. R. & FARNERD. S. (1960) Energy metabolism, thermoregulation and body temperature. In Biology and Comparative Physiology of Birds. (Edited by MARSHALLA. J.) Vol. II, pp. 215-288. Academic Press, New York. LASlV;WSKI R. C. & BARTHOLOMEWG. A. (1965) Gular flutter in the poorwill, Phalaenoptilus nuttalli. Am. Zool. 5, 208. MAcMILLEN R. E. & TROST C. H. (1965) Oxygen consumption and water loss in the Inca dove, Scardafella inca. Am. Zool. 5, 208-209. MAcMILLEN R. E. & TROST C. H. (1966) Water economy and salt balance in white-winged and Inca doves. Auk 83, 451-455. O'CONNOR J. (Sec.) (1960) Climatological data-Arizona: Annual Summary. U.S. Dept. Commerce, Weather Bureau, Vol. 64.