Camp B~hrm. Phpiol Vol 71 A. No 4. pp 4YS to SOY. lY82 0300-Y62’)~82~W04Y5-15503 00 0 Printed m tireat Britain Pergamon Press Ltd

EVAPORATIVE LOSSES OF WATER BY BIRDS

WILLIAM R. DAWSON Division of Biological Sciences, University of Michigan. Ann Arbor, MI 48109. U.S.A.

(Rrceioed 6 Ju/J’ 1981)

Abstract--l. Birds lose wafer in evaporation from the respiratory tract and, in many species, through the skin. Anatomical arrangements in the nasal passages contribute to conservation of water and heat from the expired air in the absence of heat loads. However, most species still expend more water in evapor- ation than they produce in metabolism when either quiescent or vigorously active. Certain small birds, several of them associated with arid environments, represent exceptions to this and their more favorable situation appears in part to reflect an ability to curtail cutaneous water loss. 2. Birds typically resort to panting in dealing with substantial heat loads developing in hot environ- ments or accumulated over bouts of activity. In a number of species this form of evaporative cooling is supplemented by gular fluttering. 3. The ubiquitousness of active heat defense appears to reflect more the importance for birds of dealing with heat loads existing following flight or sustained running than any universal affinity for hot climates. Panting can be sustained for hours, despite progressive dehydration and, in some instances, hypocapnia and respiratory alkalosis. The prominent involvement of thermoreceptors in the spinal cord in its initiation is of considerable interest.

INTRODUCTION This review of avian evaporative water loss will attempt to summarize current understanding of this High metabolic levels associated with endothermy, process and of adaptations affecting it in various spe- high body temperatures, and the respiratory demands cies. Emphasis is placed upon data for adult birds, but imposed by flight would seem to encumber birds with some information is provided on individuals in the extravagant rates of evaporative water loss. The facts early phases of post hatching life. A recent symposium that most species are diurnal and that the smaller (Carey, 1980, and accompanying articles) can profit- ones seem far less prone than their mammalian ably be consulted for treatment of the water relations counterparts to utilize shelter such as that afforded by of the avian egg. Reviews over the past two decades of underground burrows might be expected to exacer- evaporative water loss in birds include those by bate this problem in hot climates (Dawson & Bartho- Bartholomew and Cade (1963). Salt (1964). Schmidt- lomew, 1968). For the large number of species weigh- Nielsen (1964) Dawson & Schmidt-Nielsen (1964). ing less than approx lOOg, initial measurements of King & Farner (1964), Dawson & Bartholomew evaporative water loss and estimates of metabolic rate (1968), Richards (1970a), Dawson & Hudson (1970) based on an early allometric equation for birds Bartholomew (1972), Lasiewski (1972) Calder & King (Brody, 1945) suggested that such loss tends to exceed (1974). Dawson (1976, 1981). Calder & King (1974) metabolic production of water even at moderate tem- provide a useful consideration of physical factors peratures (Bartholomew & Dawson, 1953). Such a re- governing evaporation in these animals. lation would, of course, make these small birds depen- dent on succulent food or drinking for attaining water balance. ROUTES OF EVAPORATIVE WATER LOSS Inevitably, the substantial growth of information on avian evaporative water loss over the past three The absence of sweat glands and the enclosure of decades has indicated a more complex set of relations the body in a layer of contour feathers have been than originally perceived. A variety of behavioral, taken as indications that birds lose only negligible anatomical and physiological factors have been recog- amounts of water through the skin. This appears true nized that serve to curtail evaporation in birds. The for some birds at least; Schmidt-Nielsen et al. (1969) role of evaporative cooling in heat defense has observed that cutaneous losses accounted for less become better appreciated, and its extent during flight than 2% of the total evaporative output by ostriches more accurately assessed. Better information on the (Struthio camelus) at a T, of 40°C. However, studies dependence of standard metabolic rate on body size on other species indicate a substantial role for peri- and temperature has permitted improved assessment pheral evaporation (Table 1). The relative extent of of the relation of evaporation to the metabolic pro- cutaneous losses can be even higher in young birds, duction of water. Compartmentalization of the cuta- judging by Bernstein’s (1971) observations on young neous and respiratory components of evaporative painted quail (Cotumix chinensis), which underwent water loss has begun. Finally, understanding of such 38-53x reductions in mass-specific cutaneous evapor- loss has been extended back into the prehatching ative water loss over the first 4 weeks after hatching. phase of development, through extensive analysis of In the Japanese quail (Coturnix coturnix), the decline the properties of avian eggs affecting diffusion of in cutaneous water loss over the first 13 days after water vapor and respiratory gases. hatching appears directly related to increased thick- 495 4% WlLLIAM R. DnWsorj

Table I. Cutaneous evaporation in birds*

Body Total Cutaneous mass evaporation evaporation (8) (?, (m&/W as *+o of total Reference

12.5 30 8.9 63 Bernstein, 1971

31.6 30 9.0 59 Bernstein, 1971

42.3 30 4.7 4.5 Bernstein. 1971

42.6 30 6.7 5t Bernstein, 1971

43.2 35 5.9 51 Lasiewski rr

214.2 35 2.9 51 Lasiewski er ul., 1971

(“1. 300 35 13.6 14 Smith. 1969 40B 5.9 84 4313 22.3 67 468 29.8 28 21.500 25 0.7R 75R Taylor et rri., 1371 25 2.9A HA 35 2.2R 23R 35 3.4A 9A 43 4.3A 28R 43 4.5A lfh 8wM 40 2.2 (2 ~brn~dt-~je~se~ or rri., 1969

* Values are exclusively for resting birds except for Rhea americana. Resting values for this species are identified by “R”. Those for individuals studied over 20 min of running at 5 km/hr followed by 40 min recovery are identified by “A”. t Temperature values refer to ambient temperature in most cases. Body temperatures are identified by

ness of the cornified layer of the epidermis (McNabb temperature marking the upper boundary of the zone & McNabb, 1977). of thermal neutrality (the temperature interval over cutaneous evaporation by birds under heat loading which normothermia is maintained with a basal rate can contribute SLlbst~nti~~~~ tu evaporative coohng of heat production) is a convenient reference point (Table l), particularIy in environments or during ac- (Fig. 1). Above this temperature, evaporative water tivities fostering considerable ai, movement over the loss shows a marked thermal dependence that will be body (Smith, 1969). Rautenberg at al.3 (1980) study of examined subsequently. Below the lower critical tem- behavioral thermoregulation by domestic pigeons perature, such loss changes only slowly with tempera- provides further information on the possible impor- ture (Fig. 2). This condition persists even at ambient tance of cutaneous water loss. At an ambient tem- temperatures below the lower critical temperature perature of 50 C and a wind speed of 1.5 m/set, cuta- (Fig. I), where metabolic rate varies inverseiy with neous and pulmonary evaporation served to dissipate temperature. We shall examine avian evaporative ‘.I--3 and 0.6 -0.8 mWig, respectively. The pulmonary values were achieved without panting, owing to the birds” use of instrumentai cooling (see below). When cutaneous evaporation in hot environments was cur- tailed in domestic pigeons by use of a whoie body p~eth~sm~gra~h. t~rnperatur~ regulation was im- paired relative to that of free standing controls (Smith. 1972). The cornea appears to represent another extra-respiratory surface that contributes to evaporative heat loss under certain conditions (Kil- gore et ul., 1973; Kilgore et al., 1979; Bernstein et (II., X97Ya.b) particularly with the rapid air movement 15 25 35 45 over them occurring during flight. T, “C

Fig. 1. Relation of nocturnal metabolic rate (PC&i to EVAPORATIVE WATER LOSS IN THE ambient temperature (X,) for post absorptive western ABSENCE OF HEAT LOADING plumed pigeons resting in the dark. Shaded circles: Feb.-- Int~~~fjz~~ti(~}l Mar. (au&al. summer) determinations. unshaded circles: May (austral. fall) determinations. The zone of thermal In birds studied while resting and t&sting in the neutrality extends from approx 33 to 37°C (from Dawson inactive (p) phase of their daily cycle. the ambient 81 Bennett, 1973). Evaporative losses of water 491 water loss in the absence of heat loads, paying par- ticular attention to its impact upon the water budgets of birds. $J42 _* Fuctors serving to minimize evuporutiue water loss +A0 It would be advantageous for birds to minimize losses of 38 . heat and water from the respiratory tract under ambient conditions that do not require substantial evaporative 365; T, ‘C cooling. They are assisted in this by capacities for oxygen extraction that allow substantially lower ventilation than in mammals of comparable size (see, e.g., Bernstein & Fig. 3. Relation of body temperature (T,,) at conclusion of Schmidt-Nielsen, 1974; Beth & Johansen, 1980a). Events metabolic tests (Fig. 1) to ambient temperature (r,) in occurring in the upper respiratory tract also contribute to western plumed pigeons. Shaded circles: Feb.-Mar. (aus- conservation of water and heat when appropriate. As air is tral summer) determinations. Unshaded circles: May (aus- inspired it becomes heated nearly to body temperature and tral fall) determinations. The one fatally high Tb observed saturated with water vapor while still in the nasal passages. is identified by an “L” (from Dawson & Bennett, 1973). As heat is removed from the walls of these passages, their surface temperature falls below body temperature and they may become even cooler than the inhaled air. Expired air, essentially saturated with water vapor, leaves the lungs at and fasting individuals. As Weathers (1981) has established body temperature. As it passes over the cool nasal surfaces, through analysis of results for several species, body tem- it is cooled and a portion of its water content condensed in perature of birds under standard conditions tends to rise the mucosa. Schmidt-Nielsen et al. (1970) have established with ambient temperature in the upper portion of the zone that the recondensation is quantitatively important in a of thermal neutrality (Fig. 3). Despite this, metabolic rate variety of birds. For example, at 15°C and 257” relative remains essentially at the basal level (cf. Figs 1 and 3). The humidity, the cactus wren (Campylorhynchus hrunneicapil- rise in body temperature and the absence of a substantial /urn) recovered 74:” and 75%. respectively, of the water and Van’t Hoff effect for metabolism serve to displace the heat added on inspiration. The heat conserved corresponds upper critical temperature upward slightly, thereby defer- to 16:~”of the metabolic heat production noted at 15°C. ring the onset of active evaporative cooling. This mechanism also operates in penguins (Pygoscelis spp.). reclaiming >80”,, of the water and heat added to inspired Evaporatice wuter losses of various species air (Murrish, 1973). Schmidt-Nielsen et al. (1970) view the Variation in the humidities under which observations nasal passages of birds (and mammals as well) as counter- are made could hinder interspecific comparisons of total current heat exchangers in which flow is separated in time, evaporative water losses (ti,,) of birds. However. Bernstein unlike the vascular heat exchangers found in the extremi- et ul. (1977) found that rir,, by pigeons at 2OC was inde- ties of many aquatic animals in which the separation of pendent of absolute humidity between vapor pressures of 3 flow is spatial. The action of the nasal passages is strikingly and 8 torr. As will be discussed subsequently, this is not the effective below the lower critical temperature in particular, case at high ambient temperatures. Presumably the situ- where evaporative water loss tends to decline with decreas- ation at 2o’C involves adjustments of respiratory venti- ing temperature even though metabolic rate rises (see Figs lation or temperature of the expired air in a manner serv- 1 and 2). ing to conserve both water and body heat. Although heat storage and hyperthermia will be dis- Crawford & Lasiewski (1968) have analyzed evaporative cussed more fully in connection with responses of birds to water losses of birds at 25 C and obtained the following heat loading, it is important here to note briefly their general equation: occurrence below the upper critical temperature in resting nr,,. = 24.6M0 5’S (1) where i,, is total evaporative water loss in g/24 hr and A4 is body mass in kg. Water losses predicted with this equa- tion for birds of various sizes are given in Table 2. The rate of evaporation predicted for a 1 kg bird represents about 23’4 of the total daily output anticipated from measure- ments of tritiated water dilution (Ohmart et al., 1970). Evaporative water loss may vary with other factors than body mass. The loggerhead shrike (Lunius ludooicianus) shows a rate of pulmocutaneous evaporation approxi- mately 1.5 times that anticipated for other passerines of comparable size (48 g). a circumstance permitted by its suc- culent diet consisting of small vertebrates and insects (Cunningham. 1982).

Impact of ecuporation on wuter budgets, with emphasis on small xerophilic birds Since Bartholomew & Dawson (1953) first pointed out that avian evaporative loss per gram varies inversely with Fig. 2. Relation of nocturnal rate of evaporative water loss body mass, perceptions of the impact of this function upon (tiit,,) to ambient temperature (i?,) for post absorptive the water balance of birds in the absence of thermal load- western plumed pigeons resting in the dark at absolute ing have undergone some modification. Crawford & humidities of 3-10 torr (aqueous vapor pressure). Measure- Lasiewski’s (1968) analysis indicated that the evaporative ments were made simultaneously with those on metab- water loss in birds ranging from 3 to 100,OOOgis propor- olism (Fig. 1). Shaded circles: Feb.-Mar, (austral summer) tional to M0.59 (see equation 1) whereas basal metabolic determinations, Unshaded circles: May (austral fall) deter- rate varies with Mo.72 (Lasiewski & Dawson, 1967). The minations (from Dawson & Bennett, 1973). shallower slope of the curve for evaporative water loss than 498 WILLIAMR. DAWSON

Table 2. Predicted rates of evaporative water loss (ti,,) at 25‘C for birds of various body masses*

Predicted water Body mass Predicted ti,, turnover (kg) (g/24 hr) (“Abody mass/24 hr) (gi24 hr)

0.003 0.8 2-l 0.01 1.7 17 0.1 6.4 6 21.4 1.0 24.6 2 104.7 10.0 94.6 0.9 100.0 363.9 0.3

* Predicted for unstressed birds with equation (1). It should be noted that 25’C_will be below the lower critical temperatures, associ- ated with the smaller body masses, whereas it will be within the zones of thermal neutrality associated with the larger ones. The figures on water turnover are calculated with the equation: total water loss = 104.7M0~h’. where the loss is in g/24 hr and A4 body mass in kg (Ohmart et (II.. 1970). Only the two values are presented. as only 0.1 and 1.0 kg are in the range of body masses over which turnover was determined.

for metabolic rate in the absence of temperature stress fos- is effected is unknown. The ability to maintain water ters a tendency for the amount of water evaporated per balance during water restriction also depends importantly unit of oxygen consumed to be greater in smaller birds upon the favorable relation between the curtailed evapor- than in larger ones (Bartholomew, 1972). Other things ative water loss and metabolic production of water that being equal, this should mean that less metabolic water develops at moderate and cool temperatures. Under these should be produced relative to evaporation in the former conditions, the standard metabolic rate of such birds with animals. This relation is complicated by the fact that pas- their relatively high lower critical temperatures rises with serine birds have basal metabolic rates about a third higher decreasing ambient temperatures while evaporative water than those of non-passerine species of comparable size loss slowly declines (see Figs I and 2 for an illustration of (Lasiewski & Dawson, 1967). However, in the zone of ther- this type of relation). Evaporative water loss evidently falls mal neutrality, birds of whatever taxonomic affinities below 0.67 mgjml O2 consumed and thus can be offset by generally lose more water in evaporation than they pro- metabolic production of water. This is verified by obser- duce in metabolism and the discrepancy becomes greater vations on hydropenic zebra finches (Lee & Schmidt-Niel- as size decreases (see Bartholomew, 1972, for discussion). sen, 1971) and Brewer’s sparrows, Spizdla breweri (Dawson Practically speaking, this means that the evaporative water et al.. 1979). in which pulmocutaneous water loss at 25’C losses routinely exceed 0.67 mg/ml of oxygen consumed, amounts to 0.59 and 0.45 mg/ml O2 consumed, respect- the maximal value at which metabolic water could offset ively. The ability of the birds considered in this section the loss (Schmidt-Nielsen. 1964). When water losses via to survive water restriction at cool and moderate tempera- urine and feces are added to those from evaporation, the .tures appears to be a reserve capacity; all will readily use situation is even less favorable, suggesting a broad require- surface water and/or succulent food in nature even when ment among birds for use of succulent food or drinking in heat is not a problem (Dawson, 1976). The main value of maintaining water balance. such a capacity may occur when they move between Exceptions do exist to the preceding generalization that sources of surface water in the course of nomadic or migra- birds must rely on drinking or use of succulent food in tory movements or when they encounter dry periods dur- maintaining water balance. Species are known that can do ing the cooler parts of the year. It is doubtful that any bird so in the absence of heat stress while subsisting solely on preferentially refrains from drinking and utilizes a dry diet seeds with a moisture content of approx lo”, by mass, if water or succulent food is available (Dawson, 1976). These birds are small (generally < 50 g), have the relatively narrow zones of thermal neutrality and high lower critical temperatures typifying their size, and are for the most part xerophilic or associated with osmotically stressful situ- Calder & King (1974) provide an analysis of the impact ations such as salt marshes (Bartholomew, 1972). They in- of evaporative water loss on the heat budget of birds, based clude certain parrots (Cade & Dybas. 1962; Lindgren, on analysis of data for 20 species ranging in size from 6 to 1973). larks (Willoughby, 1968: Trost, 1972), and finches 100,ooOg. Between approx 1 and 38’C. the percentage of (Cade & Bartholomew. 1959; Calder. 1964: Cade er t/l.. metabolic heat dissipated evaporatively under standard 1965; Smyth & Bartholomew. 1966: Willoughby & Cade. conditions increases exponentially from 7 to 45”,,. The 1967; Edmonds, 1968: Willoughby. 1969; Ohmart & equation for this interval is: Smith, 1970, 1971; Lee SCSchmidt-Nielsen, 1971; Molden- hauer & Taylor, 1973; Dawson et al., 1979). Their ability to lOO(Ij,/ti,) = 5 + 1.48 e”.087r~ (2) contend successfully with water restriction depends upon abilities to reduce cloaca1 (Smyth & Bartholomew. 1966: Willoughby. 1968; Dawson et crl., 1979) and evaporative where Hi, and Hi,,, are evaporative cooling and metabolic (Calder. 1964; Willoughby, 1968, 1969; Lee & Schmidt- heat production, respectively, expressed in the same units: Nielsen, 1971: Dawson er trl.. 1979) water losses. The latter T, is ambient temperature in ‘C and e is the base of natural appears to depend exclusively on reduction of cutaneous logarithms. It should be noted that evaporation will exceed losses, judging by Lee & Schmidt-Nielsen’s (1971) study of metabolic production of water at percentages exceeding the zebra finch (Poephiltr gutrccra). Just how this reduction approx 8” ,,. Evaporative losses of water 499

EVAPORATIVE WATER LOSS UNDER HEAT able differential for non-evaporative heat loss exists LOADS RESULTING FROM EXERCISE AND/OR between the animal’s temperature and the operative tem- EXPOSURE TO HOT ENVIRONMENTS perature of its surroundings). A number of activities can contribute to this adjustment: compressing the contour Introduction plumage (Dawson, 1954). holding the wings away from the The ubiquitousness of effective mechanisms for body so that the thinly feathered sides of the thorax are evaporative cooling among birds suggests that they exposed (Dawson, 1954; Hutchinson, 1954; Bartholomew. 1966; Bartholomew et ul., 1968; Marder, 1973a; Butler rt may be more fundamentally linked with dissipating al., 1977). elevating the scapular feathers in such a manner heat loads resulting from physical activity than with that convective heat loss is facilitated while a barrier to hot climates (Calder & Schmidt-Nielsen, 1967). What- solar radiation is retained (Bartholomew. 1966; Bartho- ever their origin, they can place a potentially severe lomew & Dawson, 1979) increasing blood flow to the legs drain on water resources. It therefore seems useful and feet (Bartholomew & Dawson, 1954, 1958; Steen & prior to reviewing the extent of evaporative cooling in Steen, 1965; Bernstein, 1974), shading these structures birds, to consider some behavioral and physiological while exposing them to air flow (Howell & Bartholomew, factors that lessen the demand for it. 1961) and, in certain cases, increasing perfusion of combs or wattles (Yeates et ul., 1941). Heat dissipation becomes a more formidable problem Behaviorul mechanisms serving to minimize evuporution during flight owing to as much as a IO-fold increase in A diverse set of behavioral patterns serve to reduce metabolic rate over resting values (Berger & Hart, 1974). demands for expenditure or water (see Table XV in Calder Non-evaporative heat dissipation appears to be augmented & King, 1974). In hot climates, birds characteristically in several ways. The thinly feathered sides of the thorax are reduce activity in the middle of the day and seek the exposed during movement of the wings (see, e.g.. Tucker, coolest microclimates available. This is seen even in 1968). The rate of heat loss through the contour plumage domesticated birds; the Bedouin fowl (Callus gal/us) seeks itself appears to be increased 5-7-fold in flying birds, judg- shade during the middle of hot summer days in the Negev ing from results obtained with heat flow discs implanted Desert and becomes prone in contact with the cooler soil subcutaneously over the pectoral muscles of pigeons which (Marder, 1973a). In some birds retreat from the heat entails were allowed to fly at 617.5”C (Hart & Roy, 1967). Blood use of the shelter afforded by vegetation, as noted for flow to the webbed feet of herring gulls (Larus argentatus) Abert’s Towhee (Pipilo aberti) in southeastern California is increased to approx 3.5 times resting values during (Dawson, 1954). Rock wrens (Salpinctes obsoletus) utilize fliahts at 20.2-28.6”C. This results in dissioation of 46 W in the shelter provided by rocks in the deserts of southwestern th&e birds, 807; of the estimated heat production during United States @myth & Bartholomew, 1966). Raptorial flight (Baudinette et al.. 1976). Even when the feet are not birds may employ a different strategy, soaring to great webbed, they appear to serve as important sites of heat loss heights and cooler temperatures during the middle of the during flight. Tucker (1968) describes the tendency of bud- day as Madsen (1930) noted for hawks in the Sudan. gerigars (Melopsittacus undulatus) flying at 37’C to extend Where surface water is available, some species may bathe their feet into the slipstream. Coupled with the increased in it, thereby effecting evaporation behaviorally rather than rates of air movement over the body in flight, these activi- physiologically (Dawson & Bartholomew, 1968). Wetting ties contribute to the substantial increase in the heat the plumage may also be important in allowing nesting transfer coefficient noted in flying birds such as the budger- birds to protect their eggs from overheating. For example, igar, in which this coefficient increases approx 5-fold killdeer (Charadrius uociferus) on hot days crouched over (Tucker, 1968). their nests with wings slightly extended. Cooling of the Birds tolerate hyperthermia up to or slightly exceeding eggs was enhanced by the adult’s wetting its breast feathers 46’C without apparent ill effect (see, e.g., Taylor et (I/., before assuming incubation duty (Schardien & Jackson, 1971; Kilgore et (11.. 1973; Torre-Bueno, 1976). This toler- 1979). ance of elevations of up to 46’C (cf. normothermic values The tendency of birds under heat loads to utilize behav- provided by Neumann et (II., 1968) appears of considerable ioral options before initiating extensive evaporative cooling functional significance, for these animals at rest almost uni- is well illustrated by domestic pigeons, These birds can be versally store heat during exposure to hot environments trained to perform an instrumental response that provides (Bartholomew, 1964; Dawson & Schmidt-Nielsen, 1964: convective cooling during an environmental heat load Dawson & Bartholomew, 1968; Dawson & Hudson. 1970). (Schmidt & Rautenberg, 1975; Richards, 1976). This is used The ostrich ordinarily represents an exception. However. it enough to reduce greatly or eliminate the need for evapor- resorts to hyperthermia when dehydrated (Crawford & ative cooling at ambient temperatures as high as 58’C Schmidt-Nielsen, 1967). Hyperthermia appears as though it (Schmidt & Rautenberg, 1975). Water deprivation could reduce demand for evaporative cooling in warm en- enhances instrumental cooling at 55°C. However, instru- vironments by either improving capacity for non-evapora- mental responses providing food or water lead to neglect of tive heat dissipation when the operative temperature of the behavioral thermoregulation in fasted or hydropenic environment is below body temperature, or by reducing pigeons (Rautenberg et al., 1980). Such thermoregulation heat gain when it exceeds Tb. The opportunity also exists thus seems affected by initial physiological state. Interest- for reducing evaporative water loss further by deferring ingly, the preference that normally fed and watered pigeons dissipation of stored heat until it can be accomplished non- show for behavioral over physiological temperature regu- evaporatively during the cooler night-time hours, Calder & lation in warm environments is not seen in cool environ- King (1974) conclude that hyperthermia is advantageous to ments, where shivering and postural adjustments are all birds in hot environments. However, the importance to clearly preferred over instrumental responses providing water economy attendant upon elevated body temperature warming (Richards, 1976; Schmidt, 1978). varies directly with body size (M”.28), whereas the signifi- cance of the reduced thermal gradient for heat loading is Physiological characteristics serving to reduce the demand inversely related to size (M-“.“). for evaporative cooling Many birds also store heat during running (Taylor et ol.. Birds show excellent capacities for adjusting heat 1971) or flying (Farner, 1956; Howell &-Bartholomew, transfer and they thereby can reduce substantially the re- 1962; Hart & Roy, 1967; Berger et al., 1971; Aulie. 1971; quirements for evaporative cooling during exercise or ex- Baudinette et al., 1976; Torre-Bueno, 1976; Butler et r/l., posure to warm environments, (i.e. ones in which a favor- 1977; Bernstein et al.. 1979b; Butler & Woakes. 1980). par- 500 WILLIAM R. DAWSON

titularly when the activity takes place in warm environ- internal threshold for this panting response lies between 41 ments (Tucker, 1968; Taylor et al., 1971; Torre-Bueno, and 44°C (King & Farner, 1964). Panting is supplemented 1976; Hudson & Bernstein, 1981). Body temperatures in in birds of several orders (see Dawson & Hudson, 1970) by flight are as much as 4’C higher than at rest and appear gular fluttering, a rapid vibration of the membranous gular independent of T,, in cool and moderate environments region. which is driven by the hyoid apparatus. Much of (Torre-Bueno, 1976; Hudson & Bernstein, 1981), insulation the information concerning neural control of these activi- apparently being adjusted to establish and maintain the ties has been reviewed by Richards (1970a, 1975) Ldsiewski particular temperature elevation. Terre-Bueno (1976) sug- (1972) Calder & King (1974) and Richards & Avery gests that the primary role of this type of hyperthermia is (1978). whose articles should be consulted. With respect to to provide thermal conditjons within the tissues, which heat defense and particularly ~nting, this control displays serve to enhance capacities for physical exertion, Conserva- several features. some of which differ from those in mam- tion of water by storage of heat is regarded as being of mals. The anterior hypothaiamic~preoptic area contains secondary importance. However, at high ambient tempera- warmth receptors comparable in sensitivity to those found tures, the same considerations outlined for resting birds in mammals (Simon et o(., 1977). However, the area exerts would apply. This latter circumstance is well illustrated by a weaker control on heat defense than is the case in mam- analysis of the performance of the rhea (Taylor et ul., 1971). mals (Simon-Oppermann et al., 1978) and it operates in Three-quarters of the heat produced by this bird while conjunction with deep body and peripheral temperature running for 20 min at 10 km/hr and 43°C (T,,) was stored receptors (Richards, 1970b. 1971a, 1975: Richards & Avery, and body temperature exceeded 45°C. In resting rheas, in 1978). Many or all of the former lie within the spinal cord which body temperature rose only slightly above 40°C with (Rautenberg, 1969; Rautenberg cr [II., 1978) where a 1 hr exposure to 43°C heat amounting to 60”,;, of meta- examples have been directly demonstrated (Necker. 1975). bolic heat production was gained from the environment. In Spinal thermosensitivity persists in pigeons even after spi- contrast, running individuals, which became heated to nal dedfferentation (Necker & Rautenberg, 1975). Warming above 45 C, gained virtually no heat from their surround- the rostra1 brain stem or spinal cord will lead properly ings (Taylor et ai., 197i). The situation in birds flying in trained domestic pigeons to initiate the behavioral re- hot environments appears less stable. When Rying at 37°C sponses producing cooling (Schmidt. 1976) which have (T,) the budgerigar stored 137, of its heat production, pro- been described earlier. Selective heating of the vertebral ducing a rise in body temperature of O.Z”Cjmin. The bird cotumn can elicit panting without any change in hypo- could not be made to fly more at 37°C once its body thalamic temperature. At 27-3o’C (7,) selective heating of temperature reached 44°C. Starlings (Sfurnus vulyaris) the spinal cord evokes thermal panting and vasodilation of showed similar reluctance to fly at 35°C presumably the feet. On the other hand, cooling of the spinal cord of because of an Inability to achieve heat balance (Torre- animals panting at 36-37’C (7,) lowers respiratory fre- Bueno, 1976). quency to resting values (Rautenberg, 1969). Experimental manipulation of both skin and spinal cord temperatures provides evidence of a proportional control system in The ability of birds to resort successfully to heat storage which the thermal set point for the spinal cord can be during exercise and exposure to hot environments is un- modified by changes in skin temperature (Rautenberg. doubtedly aided by a mechanism that maintains the tem- 1971). Manipulation of temperatures of both the brain perature of the brain somewhat below that of the body stem and spinal cord provides further indication of the core. Most birds thus far studied (Ri~~rds, 1970b; Scott & importance of the latter region in thermoregu~ation. Selec- van Tirnhoven, t971; Kilgore et it!., 1973, 1976: Bernstein tive heating of the brain stem to 44’C seldom produces YI ut.. 1979a) can maintain the temperature of the anterior panting in pigeons. whereas heating the spinal cord to hypothalamus approx 1’C cooler than the body core over 42-43-C generally results in polypnea under thermoneutral a range of cloaca1 and ambient temperatures. All of these conditions. In hot environments, heating the spinal cord animals possess well developed reria mirabife ophthalmica and cooling the brain stem inhibit panting in only a in the temporal regions of the skull. The reria consist of quarter of the cases. On the other hand, cooling the spinal multiple branches of the external ophthalmic artery which cord often inhibits panting (Rautenberg et u(., 19i2). Sig- lie in intimate contact with a venous network whose affer- nals generated in the brain stem of the pigeon seem pri- ent vessels originate in the orbit and buccopharyngeal marily to affect ptilomotor and vasomotor activities serv- cavity (Wingstrand & Munk, 1965: Richards, 1970b; Kil- ing to stabilize body temperature under mild thermal &ore rf trl., 1973, 1976). These vascular arrangements loads. Under more severe heat stress, heating of the spinal strongly suggest that the reriu act as countercurrent heat cord serves to activate panting. The preoptic area appears exchangers, permitting warm blood flowing toward the to function as a center of integration of temperature signals brain to Lose heat to the cooler venous blood returning in the thermoregulatory system (Rautenberg rt czi.. 1978). from the evaporative surfaces of the head. As noted pre- In pigeons. this area includes neurons whose activity is viously, these surfaces appear to include the cornea (Bern- influenced by thermal stimulation of the spinal cord stein et ~tf,. 1979a.b) as well as those associated with the (Rosner, 1975). Perhaps the important role of extracranial anterior respiratory tract. The anatomical indications that receptors in heat defense is linked with the elaborate vascu- the rrtirr function as effective countercurrent heat lar arrangements for cooling the hypothalamic area de- exchangers for the brain are supported by physiological scribed previously. observations (Kilgore rr al.. 1979: Bernstein et ol., 1979b). The control of panting in birds also has other features. An area in the dorsal midbrain, which was first described by von Saalfeld (1936), functions as a panting center which Physiological factors affecting cutaneous evaporation of Richards (1971b) suggests__ as a possible avian counteruart birds are not well understood. Thus knowledge concerning of the mammalian pneumataxic center. This midbrain area mechanisms serving to increase evaporative cooling in re- is the dominant frequency controller in panting (Richards sponse to heat loads produced by exercise or exposure to & Avery, 1978). The vagal aRerent system also seems hot environments is mainly confined to the respiratory sys- prominently involved in panting. Sectioning of one vagus tem. As Lasiewski (1972) notes, all birds thus far studied during hyperthermia reduced respiration frequency in the respond to substantial heat loads by increasing respiratory domestic pigeon. domestic fowl, Japanese quail, and duck frequency and opening the mouth. Tidal volume generally (Antis p~ur~~~~n~~os).Bilateral vagotomy had little further appears to be reduced, sometimes to a value matching the effect in the panting pigeon but abolished rapid respiration dead space of the system (Beth & Johansen, 1980b). The in the other three birds. Appropriate aRerent stimuiation of Evaporative losses of water 501 the vagi in vagotomized fowl maintained normal respir- be low and this may curtail cutaneous evaporation, result- ation or thermal panting. Of the four species studied, the ing in underestimation of evaporative capacities (Smith. pigeon seems least reliant on vagal stimulation for produc- 1969). tion of a panting response (Richards, 1968). The thermal dependence of evaporative water loss above Despite the obvious importance of peripheral thermo- the upper critical temperature is illustrated for the western reception in avian temperature regulation, relatively little is plumed pigeon (Lophophapsferrugineu) in Fig. 2. The rise known of the units involved. Richards (1975) and Dawson in the rate of this function with ambient temperatures (1975) cite some examples of peripheral warmth receptors above thermal neutrality appears primarily linked with in- in birds. creased movement of air over the mucosal surface of the mouth and other structures referred to previously. How- Ptrttrrns of trcticr hart &fensr ever, one should not ignore the probable contribution of Lasiewski (1972) has identified several patterns by which cutaneous water loss. which can represent 67”” of the evap evaporative cooling of birds is augmented in response to orative output of this substance by the domestic pigeon heat loads (Table 3). The extent to which evaporative cool- under a heat load producing a body temperature of 43°C ing can beneficially affect the heat budgets of birds operat- (Table 1). The respiratory movements producing the in- ing under heat loads is in part determined by the heat creased ventilation of the mucosal surfaces culminate in production associated with this process. The metabolic panting and gular flutter with sufficient heat loading of cost of panting and, in certain cases, gular flutter would be birds. Calder & King (1974) have assembled information minimized if the oscillations of the thorax and hyoid on evaporative water losses of various birds at ambient apparatus were to occur at their respective resonant fre- temperatures exceeding body temperature. The rates under quencies in the manner documented for panting in dogs these conditions appear to approximate the maximal ones (Crawford, 1962). The use of panting and, particularly, flut- for these birds. The following allometric equation relates ter frequencies occupying a narrow range and relatively them to body size: independent of heat load (e.g. in panting by ostriches, gular = 258.6M0.80 flutter by poor-wills, and panting and gular flutter by ?%,%. (3) pigeons [see Tables 3 and 41) is suggestive of such an where rit,,_ is the maximal evaporative water loss in arrangement in certain birds. Calder & King (1974) discuss mg/min and M is body mass in kg. The exponent in this an unpublished altometric analysis concerning the mass equation is greater than that in equation (lb which dependence of respiratory frequency in resting and panting becomes +t,, = 17.11V”.~~~, when rit,, is expressed in birds, which they believe indicates an underlying relation- mg/min. The difference in exponents means that the factor ship to mechanical efficiency that would be afforded by by which maximal evaporative water loss exceeds rir,, at oscillation at a natural resonant frequency. However Lacey 25’C will vary directly with body size (Table 5). Unfortu- (1965) and Lacey & Burger (1972) tested and rejected the nately, estimates of this factor obtained by use of equations hypothesis that panting of the domestic fowl proceeds at (1) and (3) seriously misestimate actual values for some the resonant frequency of the thorax-lung system. Craw- species (Table 5). Clearly, further analysis of evaporative ford & Kampe (1971) do provide evidence that pigeons capacities of birds is needed. abruptly change from rest to panting at the resonant fre- The rates of evaporative water loss by birds under stress quency of the respiratory system. However. Weathers that have been discussed thus far represent integrated (1972) noted transition from resting respiration to values that provide little information concerning the man- synchronized panting and gular flutter in pigeons during a ner in which birds manage their evaporative cooling min- gradual rise in ambient temperature. Smith (1969) likewise ute by minute. A better view of this is afforded by reported a gradual increase in panting frequency of pigeons Lasiewski’s (1969) study of a 45.9 g poor-will (Pholuenop- in a whole body plethysmograph, which Calder & King tilus nutttrllii) whose evaporative water loss was monitored (1974) feel might be an artifact arising from constriction of continuously by direct weighting with a recording balance. the gular area in the collar of the apparatus. The surfaces When not gular fluttering, the bird evaporated 3.4mg from which evaporation occurs during panting and gular H,O/min, a rate independent of ambient temperature. The fluttering are discussed bv Lasiewski (1972). For panting, amount of water evaporated during gular flutter increased these include the nasal.- buccal. and upper pharnygeal linearly at the rate of 1.3(mg/min/C) with ambient regions. as well as the trachea. The air sacs may be temperatures between 36 and 5O’C. Rates of evaporation involved in ostriches (Schmidt-Nielsen et cd., 1969). but were correlated with the proportion of time gular flutter Menuam and Richards’ (1975) observation indicate that was utilized, flutter amplitude, and size of the area moved they do not contribute to evaporative water loss during during flutter. Lasiewski (1969) viewed gular flutter of the panting by the domestic fowl. Gular fluttering leads to poor-will as a graded on-off system, capable of accounting enhancement of evaporation from the moist surfaces of the for more than half of the evaporative cooling required pharynx and anterior esophagus. as well as those of the under severe heat stress with very little metabolic cost; buccal cavity. These surfaces may be several degrees cooler oxygen consumption of a poor-will at 47’C. where flutter- than the body core (see, for example, Lasiewski & Snyder, ing was nearly continuous. was only 13% higher than at 1969) allowing them to act as a sink for heat ultimately 35°C whereas evaporative water loss had increased by produced in the brain or other tissues. This, of course, more than 750”;. Not all species show this level of effec- makes them subject to convective heat gain if the air pass- tiveness, Weathers and Schoenbaechler (1976) have deter- ing over them is at a temperature approximating or mined that gular flutter of Japanese quail accounts for 20”,, exceeding core temperature (Seymour, 1972). of evaporative cooling above 4O’C (r,). The proportion of metabolic heat dissipated evaporat- ively at various temperatures by several species is summar- ized in Table 6. Performance of most at the highest tem- Evaporative water loss by birds has generally been peratures ranges between 100 and 200?,, though-some, e.g. measured in open circuit metabolism systems. For mini- the poor-will and spotted nightjar (Eurosropodus gutttrtus), mally realistic appraisal of evaporative water loss in hot can do substantially better than this. However, this ability environments, it is crucial that rates of air flow through may be as importantly influenced by metabolic level as such systems be high enough to maintain appropriately evaporative capacity, judging from an analysis provided by low atmospheric humidities. Lasiewski et (11.(1966a) have Lasiewski & Seymour (1972). They compared birds of four provided a useful background for such studies. The linear species, each weighing approx 40g. The sociable weaver rate of air movement through metabolism systems tends to bird (Ploceus cucullatus) with the high metabolic level Table 3. Patterns of heat defense in birds

Examples ~---~- ~-_ Pattern* Genus Family Order Reference

I. Gradual increase ofJ to panting freq. with Passcriformes Kendeigh, 1944 rising Th; no g.f. Salt, 1964 Potluryrrs Podargidae Caprimulgiformcs Lasiewski et ~1.. t970 2. Two discrete levels of’Sassociate with rest Struthio Struthionidac StrLlthioniformes Crawford & Schmidt-Nielsen, 1967 and panting, respectively; no g.f. Schmidt-Nielsen et rd.. 1969 3. Gf. freq. increasing with Th: apparently C0linu.s Phasianidae Gatliformes Lasiewski er rrl., 1966b synchronized with f tophort_w Phasianidae Ga~liformes 4. G.f. freq. relatively independent of Tb and Phulu~r(~~(~rff.~ ~halacrocoracidae Pel~caniFormes Lasiewski & Snyder. 1969 higher than panting freq., which increases ~rtholomew VI trl,, 1968 graduaijy with rr, Colius Coliidae Coliiformes Bartholomew & Trost. 1970 ~h~l(t~~optilzfs Caprimulg~dae Caprimulgiformes Lasiewski & ~rthotomew. 1966 Bartholomew et al., 1968 5. Synchronous panting and g.f. in narrow range Geococcyx Cuculidae Cuculiformes Calder & Schmidt-Nielsen, 1967 of freq. no intermediate freq. between panting Cffiumba(?~~ Columbidae Columbiformes Caldcr & Schmidt-Nielsen, 1967 and rest Loph~p~up~ ~~olumbidae Columbiformes Dawson & Bennett, 1973 Tytof?)? Tytonidae Strigiformes Bartholomew ef ctl., 1968 Bubo(?f Strigidae Strigiformes Bartholomew er uL, 1968 Coturnix Phasianidae Gailiformes tasiewski & Seymour, 1972

6. G.f. freq. relatively independent Pelecunus Pelecanidae Peleca~iform~s Bartholomew ef tri., 1968 of T,;fincreases continuously over narrow tange of r, to panting level

* Abbreviations represent the following:f, respiratory frequency; freq., frequency; g.$ gular flutter; Tb, body temperature. t Weathers (1972) provides evidence for birds subjected to gradual heating. which would place them in pattern 3. Evaporative losses of water 503

Table 4. Frequencies of respiration (S) and gular flutter in panting birds

Gular / flutter Species (cycles/min) (cycles/min) Reference

Pelecanus occidentalis co. 135* 239-2907 Bartholomew et al., 1968 brown pelican Pholacrocorax auritus 20-60 645-730 Bartholomew et al., 1968 double-crested cormorant Buhulcus ibis 44-100 86~1000 Hudson et u/., 1974 cattle eeret Lophorty; gumbelii 7ck700 Lasiewski rt al., 1966b Gambel’s quail Lophophaps ferruyinea western plumed pigeon 565-750 Dawson & Bennett. 1973 Columba liciu 650 ( + 60) 650 ( + 60)t Calder & Smidt-Nielsen, 1967 domestic pigeon Geoc,occyx cal$ornianus 356 ( + 58) 356 ( + 58)t Calder & Schmidt-Nielsen, 1967 greater roadrunner Tyro ulha 245-285 245-285 Bartholomew et al., 1968 barn owl Buho oiryinianus 24&255 21c255t Bartholomew et a/., 1968 great horned owl Phalaenoptilus nutfallii 59&690t Lasiewski & Bartholomew, 1966 poor-will Colius striatus 510-610t Bartholomew & Trost, 1970 speckled mouse bird

* Approximate rate for body temperatures exceeding 41°C. Between 40.2 and 41’C,Sincreases from 9 to 100 cycles/min. t Rate appears essentially independent of heat load.

characteristic of passerines, must evaporate considerably 200% of metabolic rate results in factors of 12.4 and 24.8 more water during heat stress to dissipate a given percent- for the extent to which evaporation exceeds metabolic pro- age of its metabolic heat production than would be duction of water. required of the non-passerine doves and quail. The poor- will can evaporate the least amount of water in achieving The detuils of panting responses this percentage owing to the very low metabolic level Normal panting by birds entails a large increase in res- characterizing it and other members of the family Capri- piratory frequency (f) as well as a decline in tidal volume mulgidae (Bartholomew et (II., 1962; Lasiewski & Dawson, (VT) over resting values in the absence of heat stress 1964; Dawson & Fisher, 1969; Lasiewski & Seymour, (Table 7). The increase in / is sufficient to produce the 1972). Regarding water balance, it should be remembered increased ventilation (P) serving to enhance evaporative that evaporative cooling at rates equivalent to 100 and loss of water (Table 6). Beth & Johansen (1980b) note the

Table 5. Predicted* and observed factors by which maximum evaporative water loss (tiWe,,,) exceeds mWcat 25’C

Body i,, Max. mass at 25°C tiWe,ai Species (kg) (mg/min) (mg/min) alb MIP Reference

Poephila guttata 0.012 2.4M 10.2M 4.2M Calder, 1964 zebra finch 1.3P 7.5P 5.8P 0.72 LophophupsJerruginea 0.081 2.6M 30.2M 11.6M Dawson & Bennett, 1973 western plumed pigeon 3.9P 34.6P 8.9P 1.31 Eurostopodus guttatus 0.088 1.9M 40M 21.OM Dawson & Fisher, 1969 spotted nightjar 4.1P 37.OP 9.OP 2.34 Geococcyx call$ornianus 0.285 7.lM 62.7M 8.8M Calder & Schmidt- greater roadrunner 8.2P 94.7P 11.5P 0.77 Nielsen, 1967 Columba livia 0.359 8.9M 135.OM 15.2M Calder & Schmidt- domestic pigeon 9.4P 113.9P 12.1P 1.25 Nielsen, 1967 Corws corm 0.610 32.OMt 297.4M 9.3M Marder, 1973b raven 12.8P 174.1P 13.6 0.97

* Values obtained through use of equations (1) and (3) are followed by P. Those obtained by direct measurement are followed by M. t Measured at 30°C (r,), where ti,, shows relatively little temperature dependence. 504 WILLIAM R. DAWSON

Table 6. Evaporative cooling by quiescent birds

Body Percent of ti,,, lost by mass evaporation at various T,%(‘C)’ Species (g) 10 20 30 40t 43.5t 44.5t Reference

Srrurhio ctrrnclus Crawford & Schmidt- 100,000 < 10 10 50 82 100 ostrich Nielsen, 1967 Rhrrr umericunu 21.500 39 117 147 Taylor t’f ul.. 1971 rhea Coturniz chinensis 43 116 Lasiewski ef (I/., l966a painted quail Lrrrus deln+vurmsis ring-billed gull 35 25 80 168 Dawson et al., 1976 (hatchling) Columhu lilitr Calder & Schmidt- 315 16 78 118 domestic pigeon Nielsen, 1966 Lopkophc~ps ferruyinrrt Dawson & Bennett, 81 <20 85 140 western plumed pigeon (1973 Scurdufrlla incti 42 8 12 19 53 108: MacMillen & Trost, 1967 Inca dove 42 120: Lasiewski & Seymour, 1972 Cucntutr roseicupilla >I5 13 85 I48 Dawson & Fisher, 1982 Galah cockatoo Geococc~x californiunus Calder & Schmidt- 285 10 10 21 78 137 greater roadrunner Nielsen. 1967 Phaltrenopril~ts nutrcdlii 40 36 175 Bartholomew et ul., 1962 poor-will Eurostopodus gurtatus 88 20 80 120# Dawson & Fisher, 1969 spotted nightjar Poduryu.5 ocellatus little Papuan 145 12 25 40 120 180 Lasiewski et crl..1970 frogmouth Cal!ptr (‘ost0< 3 11 66 Lasiewski. 1964 Costa’s hummingbird Colius strialus 44 8 13 23 99 Bartholomew & Trost, 1970 speckled coly Corrus corux 610 40 101 1329 Marder. l979b raven Poephiltr gurrtrtu l&13 26 32 72 12311 Calder, 1964 zebra finch 23 29 53 137,l Poephila gouldiue 12-15 I7 58 10s Dawson and TordotT, 1970 Gouldian finch Crrrpodacus mexicunus 20 130 Lasiewski et ul., 1966a house finch

* fi,,, = metabolic heat production; T, = ambient temperature. Relative humidities vary among the studies. t *0.5-c. 1 Macmillen & Trost’s value was obtained at an aqueous vapor pressure of 23 torr (34”/, RH). whereas Lasiewski & Seymour’s was obtained at 9-15 torr (13-243, RH). *At 52.8’C (T,) and 13 torr (120, RH) aqueous vapor pressure, the spotted nightjar can evaporatively dissipate heat at a rate 3.1 times the rate of metabolic heat production. At 50-C r, and an aqueous vapor pressure lower than 28 torr ( <30”/;, RH), the raven can evaporatively dissipate heat at a rate 1.6 times metabolic heat production. 1’123 and 137”” pertain to hydrated and hydropenic individuals, respectively.

complexity of panting in birds, concluding that three basic Tidal volume may rise above resting values under severe patterns can be discerned in the normal expression of this heat stress as Smith (1972) has shown for the domestic activity (Phase 1 panting). Many species, including the pigeon. This Phase II panting appears to represent an mute swan (Cygnus olor). which they studied, decrease the extreme response that Beth & Johansen (1980b) regard as tidal volume to a value near the dead space volume of the manifesting a breakdown in homeostasis associated with respiratory tract. The pigeon employs a compound pattern very high body temperatures. In the pigeon the rise of VT involving biphasic breathing in which a very fast and shal- associated with the onset of phase II panting allows further low component is superimposed upon a much slower and increase in i/ up to 45.9’ C, even though f reaches a maxi- deeper breathing rhythm (Ramirez & Bernstein, 1976; mum at 45.o’C and declines between there and 45.9 C. Bernstein & Samaniego, 1981). Finally there is the pattern The increased ventilation associated with panting evident in the greater flamingo, Phoenicoprerus ruher (Beth exceeds metabolic requirements for gas exchange in a et al., 1979) which involves breathing at tidal volumes less number of birds under severe heat stress and marked hypo- than the dead space. At regular intervals this rhythm is capnia and respiratory alkalosis ensue (Calder & Schmidt- interrupted by a short sequence of deeper breaths. Nielsen, 1966. 1968). A growing number of observations Evaporative losses of water SO5

Table 7. Ratios of respiratory frequency (f) and tidal volume (VT)of panting birds to resting* values

f Vr ri Species pant/rest pant/rest pant/rest Reference

Columha livia Calder & Schmidt-Nielsen. 1966; 22 0.48 10.6 domestic pigeon Smith, 1972 Anas platyrhynchos 26 0.25 6.50 Bouverot er al., 1974 Pekin duck Phoenicopterus ruher 23 0.15 3.45 Beth et d.. 1979 greater flamingo Cygnus o/or 29 0.18 5.40t Beth & Johansen. I980b mute swan

* Without heat stress. t This figure given by Beck & Johansen for this species although the product of the factors for J and VT (29 x 0.18) is actually 5.22.

document the fact that major shifts in acid-base balance balance during flight. Total evaporative water losses of fly- are not a universal accompaniment of panting activities. ing budgerigars and evaporation relative to metabolism in These pertain to the ostrich (Schmidt-Nielsen et a/., 1969). these and representatives of two other species are presented Bedouin fowl (Marder et d., 1974); Pekin duck (Bouverot in Table 8. The rates for the buderigars exceed resting et al.. 1974); Abdim’s stork, Sphenorhynchus ubdimii values by several fold and increase with ambient tempera- (Marder & Arad, 1975); rock partridge, Alectoris chukar ture. Information on total evaporative water loss for the (Krausz et al., 1977); greater flamingo (Beth et a/., 1979): three species included in Table 8 and on respiratory water mute swan (Beth & Johansen, 1980b); and domestic pigeon loss for others (Berger et a/.. 1971; Berger & Hart. 1972; (Bernstein & Samaniego, 1981). The various patterns de- and Bernstein, 1976) exceed the estimated concurrent pro- scribed in connection with phase I panting appear ad- duction of metabolic water, except in three species studied equate in at least some of these species to restrict venti- at cool or cold ambient temperatures. In the starling the lation of the exchange surfaces of the lungs sufficiently to compensation point occurs at approx 7’C. below which resist hypocapnia without the invocation of special shunt- production of water in oxidation would exceed evapor- ing arrangements. However, vascular connections do exist ation. The tendency of birds to incur water deficits during in the panting fowl that appear capable of shunting blood flight at moderate and warm ambient temperatures seems away from these exchange surfaces (Abdalla & King, 1976). paradoxical, given that most long distance migrants do not Beth & Johansen (1980b) suggest that the tendency of appear dehydrated when they arrive at their destinations Calder & Schmidt-Nielsen’s (1966, 1968) birds to undergo (see Torre-Bueno, 1978, for discussion). Torre-Bueno (1978) marked hypocapnia and consequences might result from suggests that migrating birds may remain in water balance resorting to type II panting with its increased VT, in the by ascending to altitudes where temperatures are cool face of severe heat stress. However. the ostrich (Schmidt- enough to foster a favorable relation between the gain of Nielsen et a/., 1969) Abdim’s stork (Marder et a/., 1975), water by oxidation and by its loss by evaporation. He cites and rock partridge (Krausz et a/., 1977) were also exposed altitudes at which migrating birds have been observed fly- to quite severe heat stress without any major shift in acid- ing, which are consistent with such a pattern. base balance. It would be interesting to determine whether these birds, which inhabit very hot climates, are less prone to shift to type II panting than the birds studied by Calder & Schmidt-Nielsen (1968). SUMMARY AND OVERVIEW

Water /ass during locomotion Birds are well represented in all but the most Running and flight are vigorous activities which have a unproductive environments on the earth’s surface. significant impact on evaporative water loss by birds, However, they may even occupy some of these owing to the substantial increases in ventilation required unpromising situations transiently during breeding or for metabolic support. This impact may even extend migration. As active, terrestrial homeotherms, birds beyond the bout of activity as birds initiate panting in must deal with evaporation as a significant com- ridding themselves of heat stored during flight (Butler et ponent of their water budgets. al., 1977; Butler & Woakes, 1980). Knowledge of evapor- Contrary to earlier assumptions, losses by this pro- ation during running is based on Taylor et u/.‘s (1971) cess reflect cutaneous as well as respiratory evapor- study of the rhea. Respiratory evaporation of this bird ation in many species. In the absence of heat loading, exercising at 25543°C (7,) varies with temperature. How- ever, cutaneous evaporation remains relatively constant countercurrent arrangements in the nasal passages over this range (Table 1). The proportion of heat lost by allow for significant conservation of water and heat. evaporation at 35 and 43’C declines with running velocity, However, most species still lose more water in evap- this trend being associated with increasing heat storage. In oration than they produce in metabolism. Certain a run of 20 min at IO km/hr, and 43’C (T,), only 27% of the small birds, several of which are associated with arid heat produced was dissipated evaporatively. On the other situations, represent prominent exceptions to this. hand, heat equivalent to 1200,; of heat production was dis- One factor in this appears to be an ability to restrict sipated by evaporation in rheas resting at 43,-C, which cutaneous losses of water. stored substantially smaller quantities of heat than during running. With environmental heat loads, birds can resort to Energetics, breathing patterns, and heat dissipation of various behavioral and physiological devices that les- flying birds are reviewed by Berger & Hart (1974). We sen the demand for evaporative cooling. Among the should confine ourselves here mainly to questions of water physiological stratagems is a widespread reliance on 506 WILLIAM R. DAWSON

Table 8. Evaporation relative to metabolism in flying birds

Ambient Total temp. m,, Species (’ C) (mg/g/hr) E/hi Reference

Columha lioiu 9.9 0.10 LeFebvre. 1964 domestic pigeon? Melopsittacus undulatus 19 20.4 0.11 Tucker, 1968 budgerigart 30 25.0 0.14 35 63.9 0.35 Sturnus vulgaris 5 0.07 Torre-Bueno, 1978 starling 18 0.10 25 0.16 27 0.19

* f? and hi (expressed in the same power units) represent evaporation and metabolism. respectively. At values of E/hi exceeding 0.064, evaporation will exceed metabolic produc- tion of water when fat serves as the energy substrate. The figure rises to 0.081 when carbohydrate is used. Note that these ratios do not reflect the fraction of heat production (Hi,) dissipated by evaporative cooling, since approx 25”6 of ni is directed toward the work of flight (see Tucker, 1968). t Resting evaporative water loss by pigeons is 0.86 mg (g.hr)-’ (Hart & Roy, 1967) and the corresponding value for E/M is 0.12. Values for evaporative water loss by resting budgerigars range from 4.2 to 5.3 mg/g/hr at 20 and 35’C, respectively, according to Tucker (1968). The values of E/h for these birds are 0.11 (2O-‘C) and 0.19 (35-C).

controlled hyperthermia, which has a beneficial effect REFERENCES on water conservation. These animals can also initiate ABDALLA M. A. & KING A. S. (1976) The functional ana- vigorous evaporative cooling through panting and, in tomy of the bronchial circulation of the domestic fowl. J. certain cases, gular flutter. Cutaneous water loss can Anat., Lottdon 121, 537-550. represent a significant component of heat defense, as AULIE A. (1971) Body temperatures in pigeons and budgeri- gars during sustained flight. Camp. Biochrm. Phxciol. well. Cases of unusually effective evaporative cooling 39A. 173-l 76. typically reflect effortless panting, and perhaps, gular BARTHOLOMEW G. A. (1964) The roles of physiology and flutter, coupled with inherently low metabolic levels. behaviour in the maintenance of homeostasis in the Birds appear able to sustain panting activity for desert environment. SJxmp. Sot. exp. Biol. 18, 7~29. hours, despite progressive dehydration and, in certain BARTHOLOMEW G. A. (1966) The role of behavior in the instances, hypocapnia and respiratory alkalosis. temperature regulation of the masked booby. Condor 68, Apparently, all birds augment their evaporative 523-535. cooling in response to heat loads. The ubiquitousness BARTHOLOMEW G. A. (1972) The water economy of seed- of this appears to reflect more the importance of cop- eating birds that survive without drinking. Proc. XVth int. ornith. Congr. 237-254. ing with heat loads at the conclusion of bouts of run- BARTHOLOMEW G. A. & CADE T. J. (1963) The water econ- ning or flight, than any universal affinity for hot cli- omy of land birds. Auk 80, 504-539. mates. The panting response is of interest from the BARTHOLOMEW G. A. & DAWSON W. R. (1953) Respiratory standpoint of control, for thermoreceptors in the spi- water loss in some birds of southwestern LJnited States. nal cord play a dominant role, operating in conjunc- Physiof. Zool. 26, 162-166. tion with elements in the rostra1 brain stem and the BARTHOLOMEW G. A. & DAWSON W. R. (1954) Body tem- skin. perature and water requirements in the mourning dove, Under most conditions, birds appear to incur water Zentriduru macrourtr marginella. Ecology 35, 181-187. deficits through evaporation in flight. yet most BARTHOLOMEW G. A. & DAWSON W. R. (1958) Body tem- migrants do not arrive at their destinations in a dehy- peratures in California and Gambel’s quail. Auk 75, 150.- 156. drated state. The suggestion that individuals engaging BARTHOLOMEW G. A. & DAWSON W. R. (1979) Thermo- in long distant flights ascend to elevations where regulatory behavior during incubation in Heermann’s cooler temperatures allow a more favorable relation gulls. Physiol. Zoo/. 52, 422-437. between evaporation and metabolic production of BARTHOLOMEW G. A. & TROST C. H. (1970) Temperature water is an intriguing one consistent with some obser- regulation in the speckled mousebird. Colius striutus. vations of flight patterns. It appears to provide Condor 72,, 141-146. another example of the role of behavior in enhancing BARTHOLOMEW C. A.. HUDSON J. W. & HOWELL T. R. physiological capacity. (1962) Body temperature, oxygen consumption. evapor- ative water loss, and heart rate in the poor-will. Condor 64, 117-125. Acknowledgements-Preparation of this review was sup- BARTHOLOMEWG. A., LASIEWSKI R. C. & CRAWFORD E. C., ported in part by a grant from the National Science Foun- JR (1968) Patterns of panting and gular flutter in cor- dation (DEB 80-21389). The skilful assistance of MS San- morants, pelicans, owls and doves. Condor 70, 31-34. dra K. Schaerer in typing the manuscript is gratefully ac- BAUDINETTE R. V., LOVERIDGE J. P.. WILSON K. J., MILLS knowledged. I am grateful to Professor R. A. Suthers. C. D. & SCHMIDT-NIELSEN K. (1976) Heat loss from feet Indiana University, Bloomington. for providing a copy of of herring gulls at rest and during flight. Am. J. Physiol. pertinent parts of R. M. Smith’s (1969) dissertation. 230, 920.-924. Evaporative losses of water 507

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