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Evaporative water loss in birds—II. A modified method for determination by direct weighing
Comp. Biochem. Physiol., 1966, Vol. 19, pp. 459 to 470. Pergamon Press Ltd. Printed in Great Britain
EVAPORATIVE W A T E R LOSS IN B I R D S - - I I . A M O D I F I E D M E T H O D FOR D E T E R M I N A T I O N BY D I R E C T W E I G H I N G ROBERT C. LASIEWSKI, ALFREDO L. ACOSTA and MARVIN H. BERNSTEIN Department of Zoology, University of California, Los Angeles, U.S.A. (Received 3 M a y 1966)
A b s t r a c t - - 1 . A direct weighing method of determining avian evaporative water loss under conditions of controlled temperature and humidity was developed. 2. Ambient water vapor pressure and evaporative water loss are inversely related in Excalfactoria chinensis at 32, 25 and 15°C. 3. Evaporative water loss at a given temperature in E. chinensis is proportional to the water vapor pressure gradient between the environment and evaporative surfaces. 4. Maximum rates of gular flutter in a variety of species are roughly inversely related to the size of the gular area. 5. Panting and gular fluttering may occur at rates determined by the resonant characteristics of thoracic cavity and gular region, respectively, or at apparent nonresonant frequencies. INTRODUCTION BIRDS do not sweat, but rely mainly on increased respiratory evaporative water loss for heat dissipation when environmental temperatures exceed body t e m p e r a tures. Birds use gular fluttering and/or panting to increase evaporation w h e n heat stressed, and a thorough analysis of the effectiveness of heat dissipation requires quantification of the a m o u n t of .water evaporated. T h e usual open flow method for studying evaporative water loss ( E W L * ) has serious limitations inherent in its execution (see Lasiewski, Acosta & Bernstein, 1966), so this modified method of determining E W L under controlled t e m p e r a t u r e and humidity conditions by direct weighing was devised. Results from the direct weighing m e t h o d are compared with those obtained by the open flow technique, and the effects of ambient W V P upon E W L in the painted quail, Excalfactoria chinensis, are studied. MATERIALS AND METHODS Specimens of painted quail, Excalfactoria chinensis, Gambel's quail, Lophortyx gambelli, and bobwhite quail, Colinus virginianus were purchased from commercial sources, while the * The following abbreviations will be used: EWL, evaporative water loss; WVP, water vapor pressure; AWVP, water vapor pressure gradient between the evaporative surfaces and the environment; TA, ambient temperature; TB, body (cloacal) temperature; RH, relative humidity; RQ, respiratory quotient; HP, metabolic heat production. 459
460
ROBERTC. LASIEWSKI,ALFREDOL. ACOSTAAND MARVIN H. BERNSTEIN
remainder of species used in this study were caught wild. All birds were maintained indoors on a 12-hr-dark, 12-hr-1ight period with ad lib. food and water for at least 3 days before being used experimentally. Valuable guidance for the direct weighing method was obtained from the studies of Hutchinson & Sykes (1953) and Hutchinson (1954) on evaporation in the domestic fowl. New techniques and equipment have permitted considerable refinement of their original method, but the theory remains the same. Weight loss in a bird exposed to controlled conditions is due to three major factors: (a) Gaseous exchange--any excess of the weight of CO2 produced over the weight of 0 2 consumed. (b) Fecal and urinary loss. (c) Evaporative water loss.
A
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F~G. 1. Spatial configuration of apparatus for determining evaporative water loss by direct weighing: Aminco-Aire control unit (A), environmental chamber (B), smaller chamber to cut down on air currents (C), weighing cage (D), Hygrodynamics humidity indicator (E), and Mettler balance (F). When the metabolic responses of the bird are known, one can easily account for any weight change due to gaseous interchange. If an organism has an RQ of 0'73, the weight of CO2 produced is offset by the weight of 02 utilized, and there is no net weight change due to gaseous exchange. T h e two species studied by the direct weighing method (Excalfactoria
E V A P O R A T I V E W A T E R LOSS I N B I R D S - - I I .
461
chinensis and Passer domesticus) have RQ's near 0-73 (indicating the utilization of fat as a source of energy), so this gaseous exchange factor need not be considered further. Even when RQ values are near 1'0, this factor is generally small. Fecal-urinary losses are easily detected by placing the bird in a small cage which has a wire mesh floor. T h e cage with bird is suspended from the weighing arm of a balance, and the weight change monitored. Feces and urine drop through the wire mesh floor resulting in a sudden marked decrease in weight, in contrast to the gradual weight loss due to evaporative water. Since weight losses due to gaseous exchange and defecation-urination can be accounted for, the remaining weight change is a measure of water evaporation. A system was assembled which permitted determination of E W L by direct weighing under controlled temperature and humidity conditions, and the general configuration of the equipment is illustrated in Fig. 1. T h e desired temperature and humidity are maintained in a 60 fC custom-built environmental chamber (B), by air from an Aminco-Aire control unit (A). T h e Aminco-Aire unit is capable of supplying conditioned air controlled within + 0'5 per cent RH and + 0-75°F dry bulb temperature, at a rate in excess of 100 ft3/min. T h e weighing cage (D) plus bird is suspended from the weighing arm of a Mettler Digital Readout Balance (F) of 0"1 mg sensitivity, and maintained in a smaller chamber (C) within the environmental chamber. The configuration and position of the smaller chamber cuts down on the air currents passing over the bird without interfering with the controlled conditions, and, therefore, permits more accurate weighings. Temperatures and humidities in the chamber are monitored by a Honeywell Electronik 16 potentiometric recorder and a Hygrodynamics Universal Indicator (E), respectively. Body temperatures were registered at the end of most direct weighing water loss determinations with a Schultheis quickregistering thermometer. The chamber surfaces surrounding the bird in the direct weighing determinations were covered with aluminium foil, as they were in the open flow and air tunnel determinations discussed earlier (Lasiewski et al., 1966), to provide comparable environmental radiative properties in all aspects of this study. Postabsorptive birds were permitted to equilibrate in the dark for at least 1 hr at the desired T A and humidity before any measurements were made. All determinations were performed in darkened chambers to minimize activity of the birds. T h e frequency of gular flutter was determined with a stroboscopic tachometer (Strobotac, General Radio). All temperatures are expressed in degrees Centrigrade unless otherwise specified. RESULTS T h e a p p l i c a b i l i t y of t h e d i r e c t w e i g h i n g t e c h n i q u e was t e s t e d b y first m e a s u r i n g E W L as a f u n c t i o n o f TA w i t h t h e m o r e c o n v e n t i o n a l o p e n flow t e c h n i q u e in Excalfactoria chinensis ( X b o d y w e i g h t , 42.7 g). A n air flow rate of 350 cmS/min was u s e d at all t e m p e r a t u r e s , a n d R H ' s in t h e 1-gal c h a m b e r s w e r e c a l c u l a t e d a c c o r d i n g to t h e e q u a t i o n p r e s e n t e d b y L a s i e w s k i (1964). T h e t e m p e r a t u r e a n d h u m i d i t y c o n d i t i o n s w e r e t h e n r e p r o d u c e d in t h e d i r e c t w e i g h i n g s y s t e m a n d E W L d e t e r m i n e d . E v a p o r a t i v e w a t e r loss values m e a s u r e d b y t h e s e t w o d i v e r g e n t m e t h o d s fall in t h e s a m e p o p u l a t i o n of p o i n t s (Fig. 2), i n d i c a t i n g t h a t w h e n t e m p e r a t u r e - h u m i d i t y r e g i m e s are similar, b o t h m e t h o d s y i e l d c o m p a r a b l e results for t h e p a i n t e d quail. R e p r e s e n t a t i v e R H ' s at several t e m p e r a t u r e s are p r e s e n t e d in T a b l e 1. U n d e r t h e s e c o n d i t i o n s , E W L in E. chinensis increases slowly w i t h i n c r e a s i n g TA f r o m 3-5 ° to a p p r o x i m a t e l y 35 °. A b o v e 35 °, t h e r e is a m a r k e d i n c r e a s e in w a t e r loss, reflecting t h e o n s e t of i n c r e a s e d v e n t i l a t i o n rates a n d g u l a r fluttering.
462
ROBERT C . LASIEWSKI, ALFREDO L . ACOSTA AND M A R V I N H . BERNSTEIN
Kendeigh (1944) published values for EWL determined by the open flow method in the house sparrow as a function of Ta, as well as values for metabolism, RQ, and breathing rate. From the data presented in Kendeigh's pioneering study, 14
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FIG. 2. Relation between evaporative water loss and ambient temperature in the painted quail, measured by open flow and direct weighing methods under similar temperature-humidity regimes. T A B L E 1 - - R E P R E S E N T A T I V E RELATIVE HUMIDITIES IN CHAMBER DURING OPEN FI,OV*' DETERMINATIONS OF EVAPORATIVE WATER LOSS IN PAINTED QUAIL*
Ambient temperature (°C)
Relative humidity (%)
Water vapor pressure (mm Hg)
3.8 10.8 20.5 28.1 33.9 38.5 40.6 42.2
75.9 41.9 29-0 25-4 15-1 40-2 35-4 37-4
4.8 4.1 5.2 7-2 6.0 20.5 20.5 23.2
* Calculated according to equation presented by Lasiewski (1964).
463
EVAPORATIVE WATER LOSS IN BIRDS--II.
it was possible to estimate the RH's in his metabolic chambers. The E W L of house sparrows under comparable temperature-humidity conditions was then determined by the direct weighing technique, and the values from both studies are shown in Fig. 3. As in the case of the painted quail there is good agreement between the values for E W L in the house sparrow obtained by the two diverse methods. The correspondence of values for painted quail and house sparrows obtained by both methods indicate that the direct weighing technique is a reliable method, and can accurately measure EWL under conditions of controlled temperature and humidity. | o o
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the house sparrow measured by open flow (Kendeigh, 1944) and direct weighing methods under similar temperature-humidity regimes. The effects of environmental WVP upon the EWL in E. chinensis were studied at 15, 25, 32 and 40 °. At temperatures within or below the zone of thermal neutrality (32, 25 and 15°), the amount of water evaporated roughly increases as the environmental WVP decreases (Fig. 4), as might be expected from purely physical considerations. In this range of TA's, ambient WVP is the major determinant of the rate of EWL in painted quail, and T~ exerts little or no effect on this rate. The relation between EWL and WVP at 40 ° is more complex than that at lower temperatures, as shown in Fig. 5. Rates of water loss at 40 ° are lowest in both very dry and very humid conditions, with the highest water loss values
464
ROBERT C. LASIEWSKI, ALFREDO L. ACOSTA AND MARVIN
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H20 VP mm Hg F I c . 4. Effects of a m b i e n t water vapor pressure u p o n evaporative w a t e r loss in E. chinensis at t e m p e r a t u r e s w i t h i n or below the t h e r m o n e u t r a l zone.
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EVAPORATIVE WATER LOSS I N B I R D S - - I I .
465
occurring between 27 and 34 mm Hg. The behavior of the painted quail differed markedly however at different WVP's. The lowest WVP studied (8.1 mm Hg) presented little heat stress at 40 ° to painted quail as evidenced by low ventilation rates of 54 and 60 breaths/min, and only slight, occasional gular flutter. The intensity and duration of the gular flutter and rate of ventilation increased with increasing WVP's, reaching a recordable maximum of 110 breaths/min and continuous flutter at 33"8 mm Hg. At WVP's higher than this, gular flutter was intense and continuous, and obscured the breathing rate usually obtainable from the deflection of the balance scale. At the highest WVP's at 40 °, the painted quail were extremely quiescent in comparison to their behavior at lower humidities and temperatures. They fluttered continuously and intensely, despite the low rates of water loss, and characteristically sat with wings drooped and slightly spread, thereby exposing sparsely feathered axillary areas. By undergoing mild hyperthermia (recorded TB's of 42-9 and 43.2 ° at vapor pressure of 53 mm Hg) E. chinensis is able to balance heat production with heat loss through evaporation, conduction, convection, and radiation, and to maintain thermal equilibrium in very humid environments at 40 °. This high humidity is fatal to painted quail at T~'s of 42.5 ° and above. DISCUSSION The direct weighing method of determining EWL offers several advantages over the more conventional open flow technique, since measurements can be made under controlled conditions with T~'s and RH's varied independently. Air flow past the bird is controlled and essentially constant, while simultaneous control of temperature, humidity and air flow is difficult to maintain in the open flow technique. Breathing rates, duration of gular fluttering, and some estimate of the activity of the bird are obtainable by observation of the balance arm. The usefulness of the technique could be enhanced by utilizing a recording balance, with which highly accurate instantaneous values of E W L could be obtained. The physical inconvenience of obtaining weight changes due to the spatial relationships of the equipment illustrated in Fig. 1 would be removed by utilizing a recording balance. A major disadvantage of the direct weighing method as outlined is that it does not permit the simultaneous determination of the energetic cost of evaporative cooling by monitoring oxygen consumption or carbon dioxide production, as is possible in the open flow method. Ambient WVP seems to be a major determinant of E W L in painted quail, and an inverse relationship exists between these two variables at T4's of 32 ° and below (see Fig. 4). Kayser (1930) and Hutchinson (1955) demonstrated lower rates of E W L in the pigeon and domestic fowl, respectively, at higher humidities than those found at lower humidities, and our results are consistent with their findings. Ambient temperatures below 35 ° do not alter the rate of EWL of painted quail much, as evidenced by the flatness of the lower portion of the E W L - T I curve (Fig. 2), and the large degree of overlap of EWL values at 15, 25 and 32 ° at comparable WVP's as shown in Fig. 4. Several studies on the physiological responses of smaller birds have demonstrated relative insensitivity of rates of EWL to a wide
466
ROBERT C. LASIEWSKI, ALFREDO L. ACOSTAAND MARVIN H. BERNSTEIN
range of TA's (Kendeigh, 1944; Cade et al., 1965; Lasiewski et al., 1964; Calder, 1964; and others). Since oxygenconsumption, and presumablyventilation rates, increases with decreasing TA's, one might expect the amount of water evaporated to increase in a similar fashion. In fact, EWL generally decreases or remains relatively constant with decreasing TA. The most likely explanation for this phenomenon would seem to involve a reduction of the temperature of the expired air below TB as suggested by Cade et al. (1965). Jackson & Schmidt-Nielsen (1964) demonstrated cooling of exhaled air in the nasal passages of kangaroo rats (Dipodomys merriarni and D. spectabilis) and the white laboratory rat, and discussed the implications of their findings for water conservation. Cooling of the exhaled air in the nasal passages of small birds (and mammals) could partially or totally account for the relative insensitivity of EWL to decreasing Ta's , even though the total volume of expired air probably increases as the TA drops. Further studies on the temperatures of exhaled air and nasal passages, and volumes of air respired by birds are needed. The importance of the AWVP between the evaporating surfaces and the environment in determining the rate of evaporation in birds has been commonly recognized (Hutchinson, 1955; Salt, 1964; King & Farner, 1964). Hutchinson likened evaporation of water from the respiratory tract of domestic fowl to Dalton's (1802) dishes of water, and described the relationship between rate of evaporation, rate of ventilation and AWVP in fowl by Dalton's formula: E = Cf(V)(Ps-Pa)
where E is rate of evaporation, C is a constant, f ( V ) is a function of ventilation, Ps is the saturated water vapor pressure at temperature of evaporating surfaces, and Pa is the ambient water vapor pressure. Hutchinson found that in "hyperthermia the respiratory ventilation of a resting bird is correlated with the rectal temperature" and rewrote the relationship as follows: E = e l ( # ) ( ~ - Pa)
where f(tr) is a function of rectal temperature. The generality of this relationship between ventilation and TB is uncertain, since little is known about the mechanism of panting and/or gular fluttering in birds. King & Farner (1964) have constructed a more elaborate formulation regarding the heat transfer characteristics of birds, although few data are available at present to permit analysis of their hypothesis. Since E. chinensis increases both the rate of respiration and the duration and amplitude of gular flutter with increasing heat loads, it is not possible at present to establish any meaningful relation between T• and the amount of air passing over the evaporative surfaces in this species. However, some estimate of the importance of AWVP in determining rates of EWL in painted quail can be obtained by utilizing calculations similar to Salt (1964) in which EWL per unit time is divided by the AWVP. The results from such calculations at 32 and 40 °, over a wide range of ambient WVP are presented in Table 2. The EWL/g body weight/hr/mm Hg AWVP is relatively constant at 32 °, strengthening Hutchinson's contention that
467
EVAPORATIVE WATER LOSS IN B I R D S - - I I .
E W L in b i r d s is p r o p o r t i o n a l t o t h e A W V P . T h e r e s u l t s at 40 ° are m o r e c o m p l e x , since t h e y i n v o l v e different d e g r e e s of h e a t stress a n d g u l a r flutter. N e v e r t h e l e s s w h e n p a i n t e d q u a i l are f l u t t e r i n g c o n t i n u o u s l y , t h e a m o u n t o f w a t e r l o s s / m m H g A W V P is r e l a t i v e l y c o n s t a n t , a n d r o u g h l y t e n t i m e s h i g h e r t h a n w a t e r loss at 32 °. T h e s e d a t a are s i m i l a r to t h o s e r e v i e w e d a n d c a l c u l a t e d b y S a l t (1964) w h i c h s u g g e s t t h a t r e s p i r a t o r y w a t e r loss p e r m m H g A W V P / b r e a t h is r e l a t i v e l y c o n s t a n t at T a ' s a b o v e t h e r m o n e u t r a l i t y in Passer domesticus, Emberiza hortulana, E. citrinella, Pipilo aberti a n d P. fuscus. T A B L E 2 - - E V A P O R A T I V E WATER LOSS IN THE PAINTED QUAIL DIVIDED BY THE WATER VAPOR PRESSURE GRADIENT BETWEEN ENVIRONMENT AND EVAPORATIVE SURFACES*
EWL t mg H 20~ g/hr ]
Breathing rate (resp/min)
Body temp. (°C)
Ps ~
Pa§
P, - Pa
EWL*
(mm Hg)
(mm Hg)
(mm Hg)
Ps-Pa
Ambient temperature = 32°C 2"06 67 39"8 2"92 64 41"5 3"70 69 40"6 1"63 48 39-8 1 "96 65 39"8 1 "72 66 40'2 1 "45 70 41 "2 1"26 63 39-8 1 "12 86 39"8 0-99 80 39-8 1"21 70 40"4
54"7 59"8 57"1 54-7 54-7 55 '9 59"0 54-7 54'7 54"7 56"5
7"0 6"7 16"2 16-1 20"8 22-4 27"0 27-1 32-8 32'8 33"8
47"7 53"1 40"9 38-6 33 "9 33"5 32'0 27"6 21 '9 21 "9 22-7
0'043 0'055 0'090 0.042 0-058 0"051 0"045 0"046 0'051 0"045 0"053
Ambient temperature = 40°C 5"30 Sporadic 41 '2 9"85 flutter 41'0 9-80 42-5 8"95 41-2
59"0 58"3 63"1 59'0
8"1 15"3 21-3 21 "6
50"9 43"0 41 '8 37"4
0"10 0"23 0"23 0"24
59"6 60"5 64"1 60"5 60"9 59"8 64-8 59"8 64"5 65-5
27"8 27"8 33"8 33"6 36"8 40-4 40"1 48-7 52'3 52"5
31"8 32-7 30"3 26"9 24"1 19"4 24"7 11"1 12"2 13"0
0"40 0-32 0"58 0"42 0"40 0-43 0"37 0"45 0"46 0"27
12"56 10"30 17"50 11 "22 9"76 8'28 9'14 5"05 5'65 3-50
Continuous flutter
41"4 41"7 42-8 41 "7 41 "8 41 "5 43"0 41 "5 42"9 43"2
* Expressed in units of mg of water per g body weight per hr per m m Hg water vapor pressure gradient. t Evaporative water loss from direct weighing method. ++Water vapor pressure at evaporating surface, assumed to be at body temperature. § Ambient water vapor pressure.
468
ROBERT C. LASIEWSKI, ALFREDO L . ACOSTA AND MARVIN H . BERNSTEIN
More complete analysis of the mechanism of evaporative cooling in birds await data on volumes of tidal air exchanged, characteristics of the tidal air (degree of saturation, temperature of expired air), sites of evaporation, and (hopefully) their relation to environmental conditions. Such data will probably not be available until air sac function is understood more completely than it is at present. Investigations dealing with the mechanism of evaporative cooling and movement of air across evaporative surfaces would probably be simpler if the species studied panted but did not gular flutter, since the volumes of air would be more definable. The available data indicate that at least two types of panting and two types of gular fluttering responses exist in birds. Panting in birds has been defined as an increase in the rate and amplitude of ventilation (Lasiewski & Bartholomew, 1966). Panting rates may increase gradually with increasing T a and TB, as in the fowl (Hutchinson, 1955) and the tawny frogmouth (Lasiewski & Bartholomew, 1966). Other species show a marked increase in panting rates, over respiratory rates at lower temperatures, with no intermediate rates, such as the ostrich (Crawford & Schmidt-Nielsen, 1965) and the pigeon (Calder & Schmidt-Neilsen, 1966). The ostrich and pigeon show a 10- and 20-fold increase in ventilation rate, respectively, between breathing rates at moderate temperatures and panting rates. Presumably, the ostrich and pigeon are panting at rates fixed by the resonant frequency of the thoracic cavity, as found by Crawford (1962) for dogs, and the energy cost of panting is lower in these species than in those showing a gradual increase in respiratory rate with increasing T1¢. TABLE 3--RATES OF GULAR FLUTTER OBSERVED IN SEVERAL SPECIES OF BIRDS
Species Chordeiles minor Phalaenoptilus nuttallii Zenaidura macroura Colinus virginianus Lophortyx gambelii Lophortyx californicus Excalfactoria chinensis Otus trichopsis Columba livia
Gular flutter rate (Cycles/min)
Source
500-700 590-690 630-815 360-770 70-700 200-750 600-915 220-290 650 _+60
Lasiewski & Dawson, 1964 Lasiewski & Bartholomew, 1966 Present study Present study Present study Present study Present study Present study (~alder & Schmidt-Nielsen, 1966
A similar situation exists among birds that gular flutter. The gular flutter frequency is relatively constant and independent of heat load in the common nighthawk (Lasiewski & Dawson, 1964), poorwill (Lasiewski & Bartholomew, 1966), and mourning dove (Lasiewski, unpublished data). The rate of gular flutter increases markedly with increasing heat load in bob-white, California, and Gambel's quail (Lasiewski & Kees, unpublished data). It appears that the poorwill, common
EVAPORATIVE WATER LOSS I N B I R D S - - I I .
469
nighthawk, and mourning dove gular flutter at a rate determined by the resonant characteristics of the gular region, while bobwhite, California, and Gambel's quail, and probably owls, flutter at nonresonant frequencies. T h e effectiveness of evaporative cooling is most likely higher in those avian species which gular flutter and/or pant at resonant frequencies than in those utilizing nonresonant frequencies to increase evaporation of water. A m o n g the limited n u m b e r of species for which data are available, the m a x i m u m rates of gular flutter (see Table 3) are roughly inversely related to the size of the gular area, as might be expected from purely physical considerations. T h e resonant frequencies of panting are also probably inversely related to the general size of the thoracic cage in birds, although much more data on this phenomenon are needed. Acknowledgements--This research was supported by National Science Foundation Grant GB-3017 to R. C. Lasiewski. We thank Mrs. Margaret H. Lasiewski and Miss Carol Muffs for assistance in preparation of this manuscript.
REFERENCES CADET. J., TomN C. A. & GOLDA. (1965) Water economy and metabolism of two estrildine finches. Physiol. Zool. 38, 9-33. CALDER W. A. (1964) Gaseous metabolism and water relations of the zebra finch, Taeniopygia castanotis. Physiol. Zool. 37, 400--413. CALDERW . A. & SCHMIDT-NmLSENK. (1966) Evaporative cooling and respiratory alkalosis in the pigeon. Proc. natn Acad. Sci. U.S.A. 55, 750-756. CRAWFORDE. C. (1962) Mechanical aspects of panting in dogs. J. appl. Physiol. 17, 249251. CRAWFORD E. C. & SCHMIDT-NIELSENK. (1965) Temperature regulation in the ostrich. Fed. Proc. 24, 347. DALTON J. (1802) Experimental essays on the constitution of mixed gases; on the force of steam or vapour from water and other liquids in different temperatures, both in a Toricellian vacuum and in air; on evaporation; and on the expansion of gases by heat. Mem. Proc. Manchr lit. phil. Soc. 5, 535-602. HUTCHINSONJ. C. D. (1954) A simple climatic chamber for physiological work with poultry. J. agric. Sci. 44, 361-368. HUTCHINSONJ. C. D. (1955) Evaporative cooling in fowls. J. agric. Sci. 45, 48-59. HUTCHINSONJ. C. D. & SYKESA. H. (1953) Physiological acclimatization of fowls to a hot humid environment. J. agric. Sci. 43, 294-322. JACKSON D. C. & SCHMIDT-NmLSEN K. (1964) Countercurrent heat exchange in the respiratory passages. Proc. natn Acad. Sci. U.S.A. 51, 1192-1197. KAYSER C. (1930) Contribution/l l'~tude de la r~gulation thermique. L'~mission d'eau et le rapport H20:O~ chez quelques esp~ces hom~othermes adultes et en cours de croissance. Ann. Physiol. Physiochim. biol. 6, 721-744. KENDEIGH S. C. (1944) Effect of air temperature on the rate of energy metabolism in the English sparrow. J. exp. Zool. 96, 1-16. KING J. R. & FARNERD. S. (1964) Terrestrial animals in humid heat: birds. In Handbook of Physiology. Sec. 4. Adaptation to the Environment. (Edited by DiLL D. B.), pp. 603624. Am. Physiol. Soc., Washington, D.C. LASIEWSKIR. C. (1964) Body temperatures, heart and breathing rate, and evaporative water loss in hummingbirds. Physiol. Zool. 37, 212-223.
470
ROBERTC. LASIEWSKI, ALFREDO L. ACOSTA AND MARVIN H. BERNSTEIN
LASIEWSKI R. C., ACOSTA A. L. & BERNSTEIN M. H. (1966) Evaporative water loss in b i r d s - - I . Characteristics of the open flow method of determination, and their relation to estimates of thermoregulatory ability. Comp. Biochem. Physiol. 19, 445-457. LASIEWSKI R. C. • BARTHOLOMEW G. A. (1966) Evaporative cooling in the poorwill and tawny frogmouth. Condor 68, 253-262. LASlEWSKI R. C. & DAWSON W. R. (1964) Physiological responses to temperature in the common nighthawk. Condor 66, 477-490. LASIEWSKI R. C., HUBBARD S. H. & 1VIOBERLYW. R. (1964) Energetic relationships of a very small passerine bird. Condor 66, 212-220. SALT G. W. (1964) Respiratory evaporation in birds. Biol. Re*;. 39, 113-136.
EVAPORATIVE W A T E R LOSS IN B I R D S - - I I . A M O D I F I E D M E T H O D FOR D E T E R M I N A T I O N BY D I R E C T W E I G H I N G ROBERT C. LASIEWSKI, ALFREDO L. ACOSTA and MARVIN H. BERNSTEIN Department of Zoology, University of California, Los Angeles, U.S.A. (Received 3 M a y 1966)
A b s t r a c t - - 1 . A direct weighing method of determining avian evaporative water loss under conditions of controlled temperature and humidity was developed. 2. Ambient water vapor pressure and evaporative water loss are inversely related in Excalfactoria chinensis at 32, 25 and 15°C. 3. Evaporative water loss at a given temperature in E. chinensis is proportional to the water vapor pressure gradient between the environment and evaporative surfaces. 4. Maximum rates of gular flutter in a variety of species are roughly inversely related to the size of the gular area. 5. Panting and gular fluttering may occur at rates determined by the resonant characteristics of thoracic cavity and gular region, respectively, or at apparent nonresonant frequencies. INTRODUCTION BIRDS do not sweat, but rely mainly on increased respiratory evaporative water loss for heat dissipation when environmental temperatures exceed body t e m p e r a tures. Birds use gular fluttering and/or panting to increase evaporation w h e n heat stressed, and a thorough analysis of the effectiveness of heat dissipation requires quantification of the a m o u n t of .water evaporated. T h e usual open flow method for studying evaporative water loss ( E W L * ) has serious limitations inherent in its execution (see Lasiewski, Acosta & Bernstein, 1966), so this modified method of determining E W L under controlled t e m p e r a t u r e and humidity conditions by direct weighing was devised. Results from the direct weighing m e t h o d are compared with those obtained by the open flow technique, and the effects of ambient W V P upon E W L in the painted quail, Excalfactoria chinensis, are studied. MATERIALS AND METHODS Specimens of painted quail, Excalfactoria chinensis, Gambel's quail, Lophortyx gambelli, and bobwhite quail, Colinus virginianus were purchased from commercial sources, while the * The following abbreviations will be used: EWL, evaporative water loss; WVP, water vapor pressure; AWVP, water vapor pressure gradient between the evaporative surfaces and the environment; TA, ambient temperature; TB, body (cloacal) temperature; RH, relative humidity; RQ, respiratory quotient; HP, metabolic heat production. 459
460
ROBERTC. LASIEWSKI,ALFREDOL. ACOSTAAND MARVIN H. BERNSTEIN
remainder of species used in this study were caught wild. All birds were maintained indoors on a 12-hr-dark, 12-hr-1ight period with ad lib. food and water for at least 3 days before being used experimentally. Valuable guidance for the direct weighing method was obtained from the studies of Hutchinson & Sykes (1953) and Hutchinson (1954) on evaporation in the domestic fowl. New techniques and equipment have permitted considerable refinement of their original method, but the theory remains the same. Weight loss in a bird exposed to controlled conditions is due to three major factors: (a) Gaseous exchange--any excess of the weight of CO2 produced over the weight of 0 2 consumed. (b) Fecal and urinary loss. (c) Evaporative water loss.
A
Y
F~G. 1. Spatial configuration of apparatus for determining evaporative water loss by direct weighing: Aminco-Aire control unit (A), environmental chamber (B), smaller chamber to cut down on air currents (C), weighing cage (D), Hygrodynamics humidity indicator (E), and Mettler balance (F). When the metabolic responses of the bird are known, one can easily account for any weight change due to gaseous interchange. If an organism has an RQ of 0'73, the weight of CO2 produced is offset by the weight of 02 utilized, and there is no net weight change due to gaseous exchange. T h e two species studied by the direct weighing method (Excalfactoria
E V A P O R A T I V E W A T E R LOSS I N B I R D S - - I I .
461
chinensis and Passer domesticus) have RQ's near 0-73 (indicating the utilization of fat as a source of energy), so this gaseous exchange factor need not be considered further. Even when RQ values are near 1'0, this factor is generally small. Fecal-urinary losses are easily detected by placing the bird in a small cage which has a wire mesh floor. T h e cage with bird is suspended from the weighing arm of a balance, and the weight change monitored. Feces and urine drop through the wire mesh floor resulting in a sudden marked decrease in weight, in contrast to the gradual weight loss due to evaporative water. Since weight losses due to gaseous exchange and defecation-urination can be accounted for, the remaining weight change is a measure of water evaporation. A system was assembled which permitted determination of E W L by direct weighing under controlled temperature and humidity conditions, and the general configuration of the equipment is illustrated in Fig. 1. T h e desired temperature and humidity are maintained in a 60 fC custom-built environmental chamber (B), by air from an Aminco-Aire control unit (A). T h e Aminco-Aire unit is capable of supplying conditioned air controlled within + 0'5 per cent RH and + 0-75°F dry bulb temperature, at a rate in excess of 100 ft3/min. T h e weighing cage (D) plus bird is suspended from the weighing arm of a Mettler Digital Readout Balance (F) of 0"1 mg sensitivity, and maintained in a smaller chamber (C) within the environmental chamber. The configuration and position of the smaller chamber cuts down on the air currents passing over the bird without interfering with the controlled conditions, and, therefore, permits more accurate weighings. Temperatures and humidities in the chamber are monitored by a Honeywell Electronik 16 potentiometric recorder and a Hygrodynamics Universal Indicator (E), respectively. Body temperatures were registered at the end of most direct weighing water loss determinations with a Schultheis quickregistering thermometer. The chamber surfaces surrounding the bird in the direct weighing determinations were covered with aluminium foil, as they were in the open flow and air tunnel determinations discussed earlier (Lasiewski et al., 1966), to provide comparable environmental radiative properties in all aspects of this study. Postabsorptive birds were permitted to equilibrate in the dark for at least 1 hr at the desired T A and humidity before any measurements were made. All determinations were performed in darkened chambers to minimize activity of the birds. T h e frequency of gular flutter was determined with a stroboscopic tachometer (Strobotac, General Radio). All temperatures are expressed in degrees Centrigrade unless otherwise specified. RESULTS T h e a p p l i c a b i l i t y of t h e d i r e c t w e i g h i n g t e c h n i q u e was t e s t e d b y first m e a s u r i n g E W L as a f u n c t i o n o f TA w i t h t h e m o r e c o n v e n t i o n a l o p e n flow t e c h n i q u e in Excalfactoria chinensis ( X b o d y w e i g h t , 42.7 g). A n air flow rate of 350 cmS/min was u s e d at all t e m p e r a t u r e s , a n d R H ' s in t h e 1-gal c h a m b e r s w e r e c a l c u l a t e d a c c o r d i n g to t h e e q u a t i o n p r e s e n t e d b y L a s i e w s k i (1964). T h e t e m p e r a t u r e a n d h u m i d i t y c o n d i t i o n s w e r e t h e n r e p r o d u c e d in t h e d i r e c t w e i g h i n g s y s t e m a n d E W L d e t e r m i n e d . E v a p o r a t i v e w a t e r loss values m e a s u r e d b y t h e s e t w o d i v e r g e n t m e t h o d s fall in t h e s a m e p o p u l a t i o n of p o i n t s (Fig. 2), i n d i c a t i n g t h a t w h e n t e m p e r a t u r e - h u m i d i t y r e g i m e s are similar, b o t h m e t h o d s y i e l d c o m p a r a b l e results for t h e p a i n t e d quail. R e p r e s e n t a t i v e R H ' s at several t e m p e r a t u r e s are p r e s e n t e d in T a b l e 1. U n d e r t h e s e c o n d i t i o n s , E W L in E. chinensis increases slowly w i t h i n c r e a s i n g TA f r o m 3-5 ° to a p p r o x i m a t e l y 35 °. A b o v e 35 °, t h e r e is a m a r k e d i n c r e a s e in w a t e r loss, reflecting t h e o n s e t of i n c r e a s e d v e n t i l a t i o n rates a n d g u l a r fluttering.
462
ROBERT C . LASIEWSKI, ALFREDO L . ACOSTA AND M A R V I N H . BERNSTEIN
Kendeigh (1944) published values for EWL determined by the open flow method in the house sparrow as a function of Ta, as well as values for metabolism, RQ, and breathing rate. From the data presented in Kendeigh's pioneering study, 14
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FIG. 2. Relation between evaporative water loss and ambient temperature in the painted quail, measured by open flow and direct weighing methods under similar temperature-humidity regimes. T A B L E 1 - - R E P R E S E N T A T I V E RELATIVE HUMIDITIES IN CHAMBER DURING OPEN FI,OV*' DETERMINATIONS OF EVAPORATIVE WATER LOSS IN PAINTED QUAIL*
Ambient temperature (°C)
Relative humidity (%)
Water vapor pressure (mm Hg)
3.8 10.8 20.5 28.1 33.9 38.5 40.6 42.2
75.9 41.9 29-0 25-4 15-1 40-2 35-4 37-4
4.8 4.1 5.2 7-2 6.0 20.5 20.5 23.2
* Calculated according to equation presented by Lasiewski (1964).
463
EVAPORATIVE WATER LOSS IN BIRDS--II.
it was possible to estimate the RH's in his metabolic chambers. The E W L of house sparrows under comparable temperature-humidity conditions was then determined by the direct weighing technique, and the values from both studies are shown in Fig. 3. As in the case of the painted quail there is good agreement between the values for E W L in the house sparrow obtained by the two diverse methods. The correspondence of values for painted quail and house sparrows obtained by both methods indicate that the direct weighing technique is a reliable method, and can accurately measure EWL under conditions of controlled temperature and humidity. | o o
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the house sparrow measured by open flow (Kendeigh, 1944) and direct weighing methods under similar temperature-humidity regimes. The effects of environmental WVP upon the EWL in E. chinensis were studied at 15, 25, 32 and 40 °. At temperatures within or below the zone of thermal neutrality (32, 25 and 15°), the amount of water evaporated roughly increases as the environmental WVP decreases (Fig. 4), as might be expected from purely physical considerations. In this range of TA's, ambient WVP is the major determinant of the rate of EWL in painted quail, and T~ exerts little or no effect on this rate. The relation between EWL and WVP at 40 ° is more complex than that at lower temperatures, as shown in Fig. 5. Rates of water loss at 40 ° are lowest in both very dry and very humid conditions, with the highest water loss values
464
ROBERT C. LASIEWSKI, ALFREDO L. ACOSTA AND MARVIN
H.
BERNSTEIN
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H20 VP mm Hg F I c . 4. Effects of a m b i e n t water vapor pressure u p o n evaporative w a t e r loss in E. chinensis at t e m p e r a t u r e s w i t h i n or below the t h e r m o n e u t r a l zone.
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EVAPORATIVE WATER LOSS I N B I R D S - - I I .
465
occurring between 27 and 34 mm Hg. The behavior of the painted quail differed markedly however at different WVP's. The lowest WVP studied (8.1 mm Hg) presented little heat stress at 40 ° to painted quail as evidenced by low ventilation rates of 54 and 60 breaths/min, and only slight, occasional gular flutter. The intensity and duration of the gular flutter and rate of ventilation increased with increasing WVP's, reaching a recordable maximum of 110 breaths/min and continuous flutter at 33"8 mm Hg. At WVP's higher than this, gular flutter was intense and continuous, and obscured the breathing rate usually obtainable from the deflection of the balance scale. At the highest WVP's at 40 °, the painted quail were extremely quiescent in comparison to their behavior at lower humidities and temperatures. They fluttered continuously and intensely, despite the low rates of water loss, and characteristically sat with wings drooped and slightly spread, thereby exposing sparsely feathered axillary areas. By undergoing mild hyperthermia (recorded TB's of 42-9 and 43.2 ° at vapor pressure of 53 mm Hg) E. chinensis is able to balance heat production with heat loss through evaporation, conduction, convection, and radiation, and to maintain thermal equilibrium in very humid environments at 40 °. This high humidity is fatal to painted quail at T~'s of 42.5 ° and above. DISCUSSION The direct weighing method of determining EWL offers several advantages over the more conventional open flow technique, since measurements can be made under controlled conditions with T~'s and RH's varied independently. Air flow past the bird is controlled and essentially constant, while simultaneous control of temperature, humidity and air flow is difficult to maintain in the open flow technique. Breathing rates, duration of gular fluttering, and some estimate of the activity of the bird are obtainable by observation of the balance arm. The usefulness of the technique could be enhanced by utilizing a recording balance, with which highly accurate instantaneous values of E W L could be obtained. The physical inconvenience of obtaining weight changes due to the spatial relationships of the equipment illustrated in Fig. 1 would be removed by utilizing a recording balance. A major disadvantage of the direct weighing method as outlined is that it does not permit the simultaneous determination of the energetic cost of evaporative cooling by monitoring oxygen consumption or carbon dioxide production, as is possible in the open flow method. Ambient WVP seems to be a major determinant of E W L in painted quail, and an inverse relationship exists between these two variables at T4's of 32 ° and below (see Fig. 4). Kayser (1930) and Hutchinson (1955) demonstrated lower rates of E W L in the pigeon and domestic fowl, respectively, at higher humidities than those found at lower humidities, and our results are consistent with their findings. Ambient temperatures below 35 ° do not alter the rate of EWL of painted quail much, as evidenced by the flatness of the lower portion of the E W L - T I curve (Fig. 2), and the large degree of overlap of EWL values at 15, 25 and 32 ° at comparable WVP's as shown in Fig. 4. Several studies on the physiological responses of smaller birds have demonstrated relative insensitivity of rates of EWL to a wide
466
ROBERT C. LASIEWSKI, ALFREDO L. ACOSTAAND MARVIN H. BERNSTEIN
range of TA's (Kendeigh, 1944; Cade et al., 1965; Lasiewski et al., 1964; Calder, 1964; and others). Since oxygenconsumption, and presumablyventilation rates, increases with decreasing TA's, one might expect the amount of water evaporated to increase in a similar fashion. In fact, EWL generally decreases or remains relatively constant with decreasing TA. The most likely explanation for this phenomenon would seem to involve a reduction of the temperature of the expired air below TB as suggested by Cade et al. (1965). Jackson & Schmidt-Nielsen (1964) demonstrated cooling of exhaled air in the nasal passages of kangaroo rats (Dipodomys merriarni and D. spectabilis) and the white laboratory rat, and discussed the implications of their findings for water conservation. Cooling of the exhaled air in the nasal passages of small birds (and mammals) could partially or totally account for the relative insensitivity of EWL to decreasing Ta's , even though the total volume of expired air probably increases as the TA drops. Further studies on the temperatures of exhaled air and nasal passages, and volumes of air respired by birds are needed. The importance of the AWVP between the evaporating surfaces and the environment in determining the rate of evaporation in birds has been commonly recognized (Hutchinson, 1955; Salt, 1964; King & Farner, 1964). Hutchinson likened evaporation of water from the respiratory tract of domestic fowl to Dalton's (1802) dishes of water, and described the relationship between rate of evaporation, rate of ventilation and AWVP in fowl by Dalton's formula: E = Cf(V)(Ps-Pa)
where E is rate of evaporation, C is a constant, f ( V ) is a function of ventilation, Ps is the saturated water vapor pressure at temperature of evaporating surfaces, and Pa is the ambient water vapor pressure. Hutchinson found that in "hyperthermia the respiratory ventilation of a resting bird is correlated with the rectal temperature" and rewrote the relationship as follows: E = e l ( # ) ( ~ - Pa)
where f(tr) is a function of rectal temperature. The generality of this relationship between ventilation and TB is uncertain, since little is known about the mechanism of panting and/or gular fluttering in birds. King & Farner (1964) have constructed a more elaborate formulation regarding the heat transfer characteristics of birds, although few data are available at present to permit analysis of their hypothesis. Since E. chinensis increases both the rate of respiration and the duration and amplitude of gular flutter with increasing heat loads, it is not possible at present to establish any meaningful relation between T• and the amount of air passing over the evaporative surfaces in this species. However, some estimate of the importance of AWVP in determining rates of EWL in painted quail can be obtained by utilizing calculations similar to Salt (1964) in which EWL per unit time is divided by the AWVP. The results from such calculations at 32 and 40 °, over a wide range of ambient WVP are presented in Table 2. The EWL/g body weight/hr/mm Hg AWVP is relatively constant at 32 °, strengthening Hutchinson's contention that
467
EVAPORATIVE WATER LOSS IN B I R D S - - I I .
E W L in b i r d s is p r o p o r t i o n a l t o t h e A W V P . T h e r e s u l t s at 40 ° are m o r e c o m p l e x , since t h e y i n v o l v e different d e g r e e s of h e a t stress a n d g u l a r flutter. N e v e r t h e l e s s w h e n p a i n t e d q u a i l are f l u t t e r i n g c o n t i n u o u s l y , t h e a m o u n t o f w a t e r l o s s / m m H g A W V P is r e l a t i v e l y c o n s t a n t , a n d r o u g h l y t e n t i m e s h i g h e r t h a n w a t e r loss at 32 °. T h e s e d a t a are s i m i l a r to t h o s e r e v i e w e d a n d c a l c u l a t e d b y S a l t (1964) w h i c h s u g g e s t t h a t r e s p i r a t o r y w a t e r loss p e r m m H g A W V P / b r e a t h is r e l a t i v e l y c o n s t a n t at T a ' s a b o v e t h e r m o n e u t r a l i t y in Passer domesticus, Emberiza hortulana, E. citrinella, Pipilo aberti a n d P. fuscus. T A B L E 2 - - E V A P O R A T I V E WATER LOSS IN THE PAINTED QUAIL DIVIDED BY THE WATER VAPOR PRESSURE GRADIENT BETWEEN ENVIRONMENT AND EVAPORATIVE SURFACES*
EWL t mg H 20~ g/hr ]
Breathing rate (resp/min)
Body temp. (°C)
Ps ~
Pa§
P, - Pa
EWL*
(mm Hg)
(mm Hg)
(mm Hg)
Ps-Pa
Ambient temperature = 32°C 2"06 67 39"8 2"92 64 41"5 3"70 69 40"6 1"63 48 39-8 1 "96 65 39"8 1 "72 66 40'2 1 "45 70 41 "2 1"26 63 39-8 1 "12 86 39"8 0-99 80 39-8 1"21 70 40"4
54"7 59"8 57"1 54-7 54-7 55 '9 59"0 54-7 54'7 54"7 56"5
7"0 6"7 16"2 16-1 20"8 22-4 27"0 27-1 32-8 32'8 33"8
47"7 53"1 40"9 38-6 33 "9 33"5 32'0 27"6 21 '9 21 "9 22-7
0'043 0'055 0'090 0.042 0-058 0"051 0"045 0"046 0'051 0"045 0"053
Ambient temperature = 40°C 5"30 Sporadic 41 '2 9"85 flutter 41'0 9-80 42-5 8"95 41-2
59"0 58"3 63"1 59'0
8"1 15"3 21-3 21 "6
50"9 43"0 41 '8 37"4
0"10 0"23 0"23 0"24
59"6 60"5 64"1 60"5 60"9 59"8 64-8 59"8 64"5 65-5
27"8 27"8 33"8 33"6 36"8 40-4 40"1 48-7 52'3 52"5
31"8 32-7 30"3 26"9 24"1 19"4 24"7 11"1 12"2 13"0
0"40 0-32 0"58 0"42 0"40 0-43 0"37 0"45 0"46 0"27
12"56 10"30 17"50 11 "22 9"76 8'28 9'14 5"05 5'65 3-50
Continuous flutter
41"4 41"7 42-8 41 "7 41 "8 41 "5 43"0 41 "5 42"9 43"2
* Expressed in units of mg of water per g body weight per hr per m m Hg water vapor pressure gradient. t Evaporative water loss from direct weighing method. ++Water vapor pressure at evaporating surface, assumed to be at body temperature. § Ambient water vapor pressure.
468
ROBERT C. LASIEWSKI, ALFREDO L . ACOSTA AND MARVIN H . BERNSTEIN
More complete analysis of the mechanism of evaporative cooling in birds await data on volumes of tidal air exchanged, characteristics of the tidal air (degree of saturation, temperature of expired air), sites of evaporation, and (hopefully) their relation to environmental conditions. Such data will probably not be available until air sac function is understood more completely than it is at present. Investigations dealing with the mechanism of evaporative cooling and movement of air across evaporative surfaces would probably be simpler if the species studied panted but did not gular flutter, since the volumes of air would be more definable. The available data indicate that at least two types of panting and two types of gular fluttering responses exist in birds. Panting in birds has been defined as an increase in the rate and amplitude of ventilation (Lasiewski & Bartholomew, 1966). Panting rates may increase gradually with increasing T a and TB, as in the fowl (Hutchinson, 1955) and the tawny frogmouth (Lasiewski & Bartholomew, 1966). Other species show a marked increase in panting rates, over respiratory rates at lower temperatures, with no intermediate rates, such as the ostrich (Crawford & Schmidt-Nielsen, 1965) and the pigeon (Calder & Schmidt-Neilsen, 1966). The ostrich and pigeon show a 10- and 20-fold increase in ventilation rate, respectively, between breathing rates at moderate temperatures and panting rates. Presumably, the ostrich and pigeon are panting at rates fixed by the resonant frequency of the thoracic cavity, as found by Crawford (1962) for dogs, and the energy cost of panting is lower in these species than in those showing a gradual increase in respiratory rate with increasing T1¢. TABLE 3--RATES OF GULAR FLUTTER OBSERVED IN SEVERAL SPECIES OF BIRDS
Species Chordeiles minor Phalaenoptilus nuttallii Zenaidura macroura Colinus virginianus Lophortyx gambelii Lophortyx californicus Excalfactoria chinensis Otus trichopsis Columba livia
Gular flutter rate (Cycles/min)
Source
500-700 590-690 630-815 360-770 70-700 200-750 600-915 220-290 650 _+60
Lasiewski & Dawson, 1964 Lasiewski & Bartholomew, 1966 Present study Present study Present study Present study Present study Present study (~alder & Schmidt-Nielsen, 1966
A similar situation exists among birds that gular flutter. The gular flutter frequency is relatively constant and independent of heat load in the common nighthawk (Lasiewski & Dawson, 1964), poorwill (Lasiewski & Bartholomew, 1966), and mourning dove (Lasiewski, unpublished data). The rate of gular flutter increases markedly with increasing heat load in bob-white, California, and Gambel's quail (Lasiewski & Kees, unpublished data). It appears that the poorwill, common
EVAPORATIVE WATER LOSS I N B I R D S - - I I .
469
nighthawk, and mourning dove gular flutter at a rate determined by the resonant characteristics of the gular region, while bobwhite, California, and Gambel's quail, and probably owls, flutter at nonresonant frequencies. T h e effectiveness of evaporative cooling is most likely higher in those avian species which gular flutter and/or pant at resonant frequencies than in those utilizing nonresonant frequencies to increase evaporation of water. A m o n g the limited n u m b e r of species for which data are available, the m a x i m u m rates of gular flutter (see Table 3) are roughly inversely related to the size of the gular area, as might be expected from purely physical considerations. T h e resonant frequencies of panting are also probably inversely related to the general size of the thoracic cage in birds, although much more data on this phenomenon are needed. Acknowledgements--This research was supported by National Science Foundation Grant GB-3017 to R. C. Lasiewski. We thank Mrs. Margaret H. Lasiewski and Miss Carol Muffs for assistance in preparation of this manuscript.
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