Cutaneous water evaporation—II. Survival of birds under extreme thermal stress

Camp. Biochm~. Physiol. Vol. 75A. No. 3. pp. 433-439, 1983 0300-9629/83 $3.00 + 0.00 Printed in Great Britain 0 1983 Pergamon Press Ltd

CUTANEOUS WATER EVAPORATION-II. SURVIVAL OF BIRDS UNDER EXTREME

THERMAL STRESS

J. MARDER

Department of Zoology, The Hebrew University of Jerusalem, Jerusalem 91904, Israel

(Rrceit~ci 22 Srprendwr 1982)

Abstract--l. Two birds, the pigeon (Co/~&u Iiciu) and the partridge (Alrrtoris ckukar), differing in their habits and flight ability were compared with regard to their ability to survive extreme high air temperatures (T,‘s). During 270min survival tests birds were exposed to T,‘s between 45 and 60°C and low relative humidities.

2. The pigeon was observed to be unique in its ability to survive 270min of exposure to 60°C while regulating T, at 43.8’C. The partridge could not survive 270 min of exposure at T’s exceeding 48°C.

3. The pigeons were found to be exceptional in their capacity for cutaneous evaporation. Values as high as 20.9 mg H,O/cm-‘!hr were measured at 52°C T, compared to 2.4 mg H,O/cm-‘/hr in the partridge. Total evaporation of the pigeon exposed to 56°C T, was about 20% higher than that in the partridge. Maximum evaporation of the pigeon exposed to 60°C T, was 34.4 mg H,O/gjhr.

4. The significance of cutaneous water loss for survival during extreme high T,‘s is discussed. 5. It is concluded that birds as a class may be divided into two groups with regard to their physiologi-

cal capacity to withstand heat stress: (I) the majority of studied species employ regular physiological mechanisms and are limited in their cooling capacity to withstand ambient temperatures 48°C; (2) a few avian species. which may be of wide ecological distribution, are equipped with major physiological preadaptations to severe heat stress

INTRODUCTIOiX

It has long been demonstrated that many birds exposed to heat stress are capable of regulating their body temperature below hot ambient temperatures. At air temperatures up to 48°C and low relative humidities, the evaporative cooling mechanisms in birds are capable of dissipating the heat produced in metabolic processes and the heat gained from the hot surroundings (see reviews by Dawson & Hudson, 1070; Calder & King, 1974; Dawson, 1982).

The subjects of the present study, the partridge and the pigeon, are birds of wide ecological distribution and are not exceptional with regard to their standard metabolic rate (SMR), body temperature (TJ, pattern of ventilation and panting, or cooling capacity at ambient temperatures (T,) up to 45°C (Calder & Schmidt-Nielsen, 1967; Marder & Bernstein, 1983). In a preliminary study, acclimated pigeons were observed to withstand long-term exposure to T,‘s up to 60°C. Partridges exposed to similar conditions (hlarder & Bernstein, 1983). could not regulate stable T,‘s when behavioral mechanisms could not be employed. Progressive hyperthermia that developed in partridges exposed to 48 and 52°C r,, pointed out the lower cooling ability of their evaporative cooling mechanisms.

Exposure of birds to temperatures as high as 60°C poses a heavy burden on their thermoregulatory mechanisms. Under these conditions, massive amounts of heat will be transferred from the surrounding hot air or to the bird’s body via the skin at

a rate proportional to the thermal gradient. In addition, tremendous amounts of hot air may be de- livered deep into the respiratory system during hyperventilation of the heat-stressed panting bird.

From the standpoint of comparative physiology of thermoregulation, birds are very homogeneous in their characteristics. Unlike desert mammals, they evolved few preadaptations leading to advantageous characteristics (Bartholomew, 1977). Flight enables birds to reach water sources even at long distance; their Tb)s during activity may be higher by 3-5°C than those of mammals, permitting the energetically cheaper avenue of dry heat dissipation. The evaporative cooling mechanisms of small and medium-size birds are more effective in body temperature regulation than those of similar size mammals. From recent literature we may conclude that the majority of birds are limited in their ability to cope with thermal stress developed under air temperatures exceeding 48°C. Within the class Aves just a few birds were observed to regulate their T, at air temperatures higher than 5O”C, i.e. Caprimulgides (Bartholomew et al., 1962; Lasiewski & Dawson, 1964; Dawson & Fisher, 1969), ostrich (Crawford & Schmidt-Nielsen, 1967) and pigeon (Calder & Schmidt-Nielsen, 1967). Their adaptive mechanisms will be discussed in the present study.

The data on cutaneous water loss of pigeons and doves (Smith & Suthers, 1969; Marder & Ben-Asher, 1983) may justify classifying them in a different cate- gory having special ability for cutaneous evaporation. The doves and pigeons are larger than the majority of

433

434 J. MARIER

birds observed by Bernstein (1971) and Lasiewski ef a/. (1971) and their capacity for cutaneous evaporation is greater. The amounts of water evaporated from skin in Columbiformes points to its possible significance in thermoregul~tion.

It is of advantage that the physiologic~~l responses to high T,‘s of both the pigeon and the partridge have been extensively discussed in the liaterature. This enables us to compare the ph~lsiologic~~l capacity of pigcons and partridges to adjust their homeostasis during long-term exposure to extreme thermal stress.

Pigeons and partridges appear to differ in thermoregulatory ability in heat stress; therefore we decided to compare evaporation and tolerance time in thcsc two species, for correlation with ability to regulate body temperature.

MATERIALS Ah0 METHODS

Wild adult pigcons were trapped in Jerusalem during the

summer. These birds were part of a flock of rock pigeons

(Colurrdu livicc) mixed with domestic pigeons (Coim~~ho /it&

ifo~nrsi~ctr). The average body weight was 2X5 g (215-320 g).

Two pigeons were raised from the age of about 12 days in captivity. Because of the daily care they were most cooper-

ative during the experiments.

The partridges (.;Ilec~roris ch~rl~trr) were raised in captivity

from I to 7 days after hatching to adulthood. Two groups were raised in separate periods. The younger. about I yr old. had a mean mass of 364 g (305-414 g). the older group

had ;i mean mass of 475 g (322 hi 1 g). Birds were housed

in outdoor pens. where food and water uere ;tvnilnhle rrct iih. Heat exposure experiments t~erc carried out in a Hot-

pack XX3 13 tempcr~iturc controlled room ( to.5 C). More details were described previously (Marder & Ben-Asher.

1983).

During a period of 1 month all birds underwent acciima-

tion by exposure of at least five periods of X hr to T.,‘s of

41 4X’C. Exposures to 7‘,i’s higher than 5O’C were carried out very carefully with special attention devoted to the

partridges. The pigeons needed just a few days of high T:,

exposure. in order to be able to withstand 60 C 7;. Since aggressive behavior \VBS well developed in pigeons exposed

to T,‘s higher than 50 C. these individuals were housed and tested separately.

Continuous 7, me~~surements of partridges were taken with u~,n -e#tlst~lt~t~~n th~rnloeo~lples inserted 3.5 cm into

the abdominal cavity viit chronic polyethylene cannulae (Marder & Bernstein. 19X3). Continuous Ths of pigeons

were determined with a Yellow Spring Instruments (Model No. 46 TUC) T&thermometer and small animal thermis-

tor probes. The probes were inserted 5 cm into the cloaca and fastened to tail feathers. These experiments were carried out in darkness while pigeons were maintained separately in stnnll cages.

Body temperature measurements (of birds maintained in big cages) taken at the end of experiments were carried out

by fast insertion of small animal thermistor probes, into the cloaca. or by quick mtroduction of a hypodermic (74(i) probe, parnllel to the cloac:~ to a depth of 3-5 cm. The use of hypodermic probes enabled rapid and accurate mtasure- ment.

Respiratory rates of h~perthermic birds were counted with the aid of a stopwatch.

Total evnporativc water loss was determined by wneigh-

ing the birds. prior to experimentatmn and at the end 01 I hr exposure. No measures were taken to prevent the

birds from normal excretion. Mcasurcments of cxcreta

weight enabled calculation of net evaporated \%atcr loss.

For hyperthermic partridges :i correction for excluding not]-ev~ipor~~tive water loss was made. This ~nvtti\:cd

me~~surin~ the ~~rnollnts of water lost via excrete (in the

form it dilute excretes) and through drooling from the beak. T~chllic~~ll~ the rn~~~~urcrnclits arc difticult hut the

amounts, 0.X 1.5 ghr. may be of si~ilil~c~il~cc for accurate

evaluation of total evaporative Mittcr loss (for dct;iils see

Marder & Bernstein. 19X3).

Cutaneous evaporation was dctermincd by measuring

the skin resistance to vapor difluslon. The measurements

were carried out on an unfeathered spot of skin of the

pectoral muscle using Lambda Instrument. Li Cor Models Li-60 and Li-65. diffusive resistance meter. Further details

and calculations were presented in a previous study

(Marder & Bert-Asher. 19X?).

Acclimated birds were cxposed to 35. 4X. 57. 56 and 60 <‘

r,,. and low relattve humiditic~ (Fig. 1). Each telnpcr~ittlrc exposure continued for a maximum of 770 mm. Water w;ts supplied for I5 min once every 2 hr. Birds were watched

through a small window. Any necessary activity inside the

hot room was carried out in darkness. Respiratory frcyucn- ties were often taken as 2% measure for stable state of the

birds. When rates declined to lf)l~-200 per min, birds \~ere

taken out of the hot room because this event has been correlated with explosive r, increases (Mnrdcr & Bcrn- stein. 1983). At the end of the survival test. body tempcrn-

ture was taken. Hyperthermic birds wcrc rapidly cooled under running water.

RESt!LTS

The capacity of the pigeon and p~lrtridge to regulate body temperatures during heat stress is dcmon- strated in Table I. During IX- I50 min exposure to T,‘s up to 48’C both species were able to regulate normal 7”ds (43.1 and 40.4-‘C in the pigeon and pur- tridge respectively). At T,‘s of 52, 56 and 60 C. the pigeon successfully regulated stable T,,‘s of 43.0. 43.6 and 43.8’C. The partridge exposed to 52 and 56 C suffered from progressive hyperthcrmia with mean 7’,, values at the critical range, i.e. 45.4 and 45.X C rc- spectively.

In a survival test (Fig. I ) birds were exposed to long-term heat stress. During 170 min of exposure birds were carefully kept under close inspection for appearance of the typical behavioral phenorneil~l stag- gesting the oncoming critical situation. Lowering of respiration frequencies to I I?(&-200 heats per minute. increased depth of sternal movements and obvious imbalance of the walking, bird wcrc obvious signs that T, had reached the range of 45.8 46.5 C. The partridge regulated a normal 7‘, of 43.7’C at the end of the survival test, i.e. 270 min exposure to 45 C T,,. At higher :T,s progressive hyperthermia developed. and was accompanied by hyperactivity that dictated the immediate cessation of the test. No partridge could survive 170 min exposure to T,,‘s exceeding 4X C. Six partridges out of 17 participants died from hypcrther-

mia in spite of the fast cooling. The prcsentcd 7‘, values (Table I) for the partridges exposed to 52.-56 C are approximate values as it was diflicult to ac- complish good measurements inside the hot room

Survival of birds under thermal stress 435

436 J. MAKDEK

0 2 4 6 0 2 4 6

l-b=42.9i0.!Z°C(9)

Tb=43.7k04°CC(II)

Rh=lO%

Tb=432zk0,3’CC(ll)

Tb=45.7~0.4*CCfll)

Rh =20 %

Tb=43. 1~0.4°C(IIl

Tb = 45.4 +-0.6°C’c(5

I Ta=56”C Rh=8% I Ta=sO”c Rh= 5%

Tb=45 8+0.5*CW Tb= 45SiO 6 *Cl61

I I 1 I I I I 1

0 2 4 6 0 2 4 6

Time, hr

Fig. 1. Survival test: The exposure time :md body tempe~ltures (+SDI of pigeons El and partridges Ii2 under extreme thermal conditions. Ambient temperatures (r.,) and relative humidities (Rh) indicibting experimental thermal conditions. Body temperature (T,) ws taken upon removal of birds. Number of

birds exposed is given in parcntheses.

without endangering the animals, urgently reyuiring lowering of body temperature. The pigeons, by contrast, stood very quietly on their perches, unbothered by the extremely hot surrounding air. At the end of 270 min exposure to 60°C T., the pigeons had a mean r, value of 43.X’C.

1 + 35 40 45 50 55 60

To, “c

Fig. 2. Evaporative wter loss of pigeons (0) nnd pnrtridges (e) exposed to extreme ambient temperatures (T.,). Lines

connect mew values.

The effect of high T$‘s on total evaporative water loss (EWL) is shown in Table I and Fig. 2. EWL in the pigeon increased about ten times as a result of T, elevation from 35 to 60-C, and reached a maximum of 34.4 mg H,O:‘g- hr. The partridge increased its EWL by about eight times between 35 and 56-C T, and reached a maximum mean of 25.0 mg H,O,/g, hr. Under our experimental procedures the pigeon EWL rtt 56 C T, is 17.0”;, higher than the partridges. The actual difFerences may reach about Zh”:, if we delete the non-evaporative water loss by the hyperthermic partridges. These included dripping fluid from the beak and the dilute excreta, and did not participate in body cooling. The corrected value for EWL difference between the two species should be smaller than 26”;, because the pigeon. being a smaller bird, has ;I higher rate of metabolic heat production and EWL per unit weight. From comparable calculation of maximum ev3porttion (E = 25X.6 Pa” ‘ ‘ In.%* ~~c~ordin~ to falder & King, 1974) the pigeon’s phredicted EWL should be 7”,, higher than the partridge’s,

Taking into account the above assumptions, we suggest that the pigeon has about 20”/, higher potential cooling capacity compared to the p~~rtridge.

Figure 3 demonstrates the relationship of water ev~~por~~tion via the skin to elevation of ambient temperature. At 20 36 C both birds had low CWL, the level increasing slightly with increasing air tempera-

Survival of birds under thermal stress 437

mg. H,O. cm-‘.hr-’

I

25

l -d/ 1 a

20 35 40 45 50 55

Ta, ‘C

Fig. 3. Skin evaporation of pigeons (0) and partridges (0) exposed to high ambient temperatures (r,). Values were calculated from skin resistance to vapor diffusion. The data is from Marder & Ben-Asher (1983). The value for par-

tridges at S2^C” is an averrige of two measurements.

tures. During heat stress (36-52°C T,) the partridge increased skin evaporation from a minimum of 0.5 to a maximum of 2.4 mg H,O/cm’/hr.

Unlike the partridge, the pigeon displayed pro- nounced evaporation from 36 to 52-C T,. The skin evaporation increased by about fourteen times (from 1.5 to 20.9 mg H,O/cm’/hr). This high evaporation of water from skin may amount to 57”” of the total EWL.

While investig~4tjllg pigeons during the ~~cclinlation period and the survival test, pigeons would stop panting for several minutes (5-l 5 min). In two exceptions, pigeons were observed to stop panting during long- term exposure to 52°C. We concluded that under cer- tain conditions (low relative humidities) skin evaporation may be the dominant aveune of cooling in pigeons exposed to hot and dry conditions.

DISCUSSION

The data presented in this paper show clearly that heat-stressed pigeons are exceptional in their ability to regulate body heat balance. It is obvious that their impressive cooling capacity is the main characteristic which preadapts them and therefore enables them to confront the intense thermal stress developed at T,‘s of 52-60°C. By contrast, the partridge cannot survive under conditions where T, exceeds 48°C. To our best understanding, the absence of efficient cutaneous evaporative cooling mechanjsm accounts for the infer- iority of the partridges (compared to the pigeons) when under severe heat stress.

We believe that the results discussed in this paper were obtained from birds affected mainly by the en- vironmental conditions and minimally disturbed by the experimental procedure. Under these conditions the pigeons and the partridges could demonstrate their physiological thermoregulatory mechanisms to best advantage.

The information on cutaneous evaporation in pigeons (Smith. 1969. quoted by Lasiewski et ul., 1971), suggest the existence of a very high potential

for water evaporation via the skin. Smith’s pigeons exposed to 35°C lost 10.1 mg H,O/gjhr via cutaneous evaporation. This value is very close to the maximum cutaneous evaporation (13.6 mg H,O/g/hr) of our pigeons exposed to 52°C T,. The maximum total evaporation measured by Smith (1969). quoted by Sturkie (1976). was about 32 mg H,O,/g/hr. It was measured when body temperatures reached about 45.5 C. Our pigeons lost a total of 34.4 mg H,O/g/hr when exposed to 60°C T, and regulated T,, at 43.8’C.

Birds inhabiting hot dry deserts may gain marked amounts of heat from the extremely hot environment by radiation, forced convection and conduction. According to Mount (1979). earth surface temperatures may reach 7O’C and air temperatures may exceed normal body temperature by 21-25’C. Com- pared to the above-described conditions, the thermal stress developed at 45’C T,, low relative humidities and minimum radiation is much easier to survive. Many birds can regulate their body temperature at 44.46°C r, (Dawson 6i Hudson, 1970) by evaporative cooling under conditions where practically no heat is gained from the environment, but few were observed to withstand ambient temperatures at 50°C or higher.

Birds exposed to extreme hot environments have to dissipate body heat originating from various sources: (I) basal heat prodilction plus the excess heat produced by the hyperthermic bird due to Q IO combined with the intensive respiratory muscle activity; (2) heat gained from the surroundings through the outer surface; (3) heat penetrating into the respiratory system during intensive hyperventilation.

The last source of heat can be calculated quantit~~t- ively if the specific heat capacity, the specific gravity of air and the mass of vapor in the air are known (Lange, f952). Our calculations are made for a bird similar to a partridge, i.e. weighing 45Og, exposed to 60°C r, and 57; relative humidity, having T, of 44°C and minute volume, calculated per hour, equal to 150 liters. During the process of panting this animal will lower the inspired air temperature by 16’C.

According to our calculations, the bird will have to evaporate 1080 mg Hz0 in order to absorb 626.6 cal from the inspired hot air. This amount equals 4O.2%8 of the standard heat production of a partridge and may pose a significant burden on the evaporative cooling mechanisnls. On the other hand, a bird, like the pigeon, having a highly developed capacity for cutaneous evapaporation, may decrease respiratory water evaporation by about SO”:, and therefore may decrease the need for augmentation of respiratory system ventilation at extreme thermal stress.

The possibility that a bird will regulate low respiratory ventilation when under heat stress may be considered an advantage of major importance. The above process will be accompanied by a decrease of heat gained from hot inspired air, lowering of heat production by respiratory muscle activity and, in addition, may diminish the danger of CO2 washout and the possible respiratory alkalosis effects.

In mammals (sheep, cattle and man) cutaneous water loss may be a combined process of both sweating and insensible perspiration. The vaporization by insensible perspiration is a process of passive diffusion

438 J. MARIXR

through the epidermis and is mainly under physical control. The rate of vaporization through this route is small in comparison with sweating. During heat stress the insensible vaporization in humans (Grice et trl.. 1971) and pigs (Ingram & Mount, 1975) will not exceed 3 mgH,0/cm2/hr. On the other hand, the rates of vaporization via sweating in heat-stressed mammals may amount to 10 mg H,O/cm*/hr in cattle and 100 mgH20/cm2/hr in humans (Ingram & Mount. 1975).

In birds maintained in neutral environments the cutaneous water loss (calculated per unit area) is low (0.5-2.5 mg H20/cm2/hr) (Bernstein, 1971; Lasiewski ct ul., 197 I ; Dawson, 1982) and the resistance to water diffusion is high. Campbell (1977) has calculated values of 76560 secjcm and Marder & Ben-Asher (1983) have measured values between 62 seq’cm and 301 secicm. Under heat stress the majority of birds elevate rates of water loss to about 2-4 mg Hz01 cm’fhr. This type of vaporization is very similar to insensible perspiration found in mammals, It seems as if the cutaneous water loss is a process of passive diffusion because neither sweat glands nor sebaceous glands were observed in birds (Rawles. 1960; Jenkin- son & Blackburn, 1968).

The pigeon. the palm dove and the collared dove (members of the Colunthidar) differ in their capacity to evaporate water from skin. Their cutaneous water loss may increase fourteen-fold and may reach 6.X20.9 mg H,O/cm’jhr (Marder & Ben-Asher, 1983). According to Smith (1969, cited by Sturkie, 1976) this process is effected by T, changes. Our findings suggest that ambient temperature is the primary factor in determining the CWL activity. From theoretical consideration. it may be shown (Marder & Ben-Asher. 1983) that the bird will achieve maximum efficiency in hot and very dry air.

In recent studies Wolfenson rt trl. (1978) showed that in domestic fowl exposed to thermal stress a peripheral vasodilation is accompanied by 20”,, increase in cardiac output and marked decrease in blood flow to the core. The blood flow to the comb and wattles, to the back and pectoral skin were augmented 2-7 times. A major portion of that blood was observed to flow through arterio-venous anastomoses and the rest via the capillary system.

If similar peripheral vasodilation exists in the pigeon, we may expect the necessary water supply to the skin vvill be accomplished by a similar process.

Birds are very homogeneous endotherms with regard to their physiological characteristics. In gen- eral, comparable species from different thermal environments have similar body temperatures; more- over, the metabolic rate and evaporative water loss are not climate-dependent, but size-dependent characteristics (Dawson & Hudson. 1970; Calder & King. 1974).

Several recent studies on birds have shown the existence of physiological mechanisms that may be regarded as heat adaptive. Wallgren (1954) observed a decline in metabolic rate of the ortolan bunting after acclimation to 32.5’C. Hudson & Kinsey (1966) showed the existence of lower metabolic rate in house sparrows from warmer climates, In a very interesting

study Pinshow cr ~1. (1982) demonstrated the existence of an elhcient cooling mechanism of the central nervous system via water evaporation from the eyes. A few authors demonstrated the existence of urohy- drosis in storks (Kahl, 1963), cormorants and turkey vultures. This method of body cooling seems to be energetically cheaper than either panting or gular Rut- tering (Bartholomew, 1977). In recent studies it was

demonstrated that birds are capable of regulating acid-base status during heat stress (Marder or (II.. 1974; Marder & Arad. 1975: Krausz et trl., 1977; Beth ct id.. 1979: Bernstein & Samaniego, 198 I). These capabilities, in addition to their ability to regulate body temperature at high T,,‘s. suggest that many birds can maintain normal homeostatis during heat stress.

It is possible that careful study will show that physiological adaptations similar to those discussed above may be found in many other bird species.

From the fruitful information concerning cooling capacity of birds published in recent years and reviewed by Lasiewski (I 972). Calder & King (I 974) and Dawson (1982). it may be concluded that many birds are capable of regulating T, at T,‘s up to 48‘ C. but only few have the capability to regulate normal T, at ambients higher than 50’C T,.

To our best understanding, the caprimulgids, the pigeon and the ostrich belong to the last group. being conspicuous with regard to their capability for heat tolerance. Each of these birds is equipped vvith a unique physiological preadaptation of major significance in thermoregulation.

The caprimulgids (Bartholomew Ed (I/.. 1962; Lasiewski & Dauson, 1964; Dawson & Fisher, 1969) have metabolic rates about SO”;, of the predicted and an energetically inexpensive method for water evaporation, i.e. gular Hutter. The X6g nightjar (Dawson & Fisher. 1969) was observed to regulate T, of 43.1 C after 2 hr exposure to 52.X C. The ostrich maintained T, below 40 C throughout long-term exposure to 51 C (Crawford & Schmidt-Nielsen, 1967). Being a larger bird. the ostrich has the advantage of having low metabolic rate and a relatively high capacity for respiratory water evaporation.

The advantage of the above characteristics may be emphasized by the following comparison, Based on predicted values (Calder & King, 1974) for maximum evaporation (E,,,, = 25X.6 .V”.“) and metabolic heat production during heat stress (150”,, of SMR = H, = 7X.3 MO.““, we can make a con- venient evaluation of the evaporative cooling etli- ciency in small. medium and large-size birds. Thus, 0.3. 3.0 and 100 kg birds will dissipate 167. 200 and 260’:” of metabolic heat by evaporation respectively. This theoretical consideration should be examined experimentally in order to determine whether a 3.0 kg bird can survive extreme heat stress.

Pigeons were observed (Gilder & Schmidt-Nielsen, 1967) to regulate T, of 43.1’C after long-term exposure to 51’C. In the present study the pigeons were found to survive 270 min at 60 ‘C while regulating T, at 43.X ‘C. It is believed that the pigeons are capable of efficiently using a highly developed mechanism for water evaporation via the skin in addition to a controlled activity of respiratory mechanisms.

Meanwhile. we can suggest that the pigeon exposed

Survival of hirds un lder therm:rl stress 439

to heat stress should be considered as an endotherm wearing a cooling garment that processes the following advantages: (1) dissipation of excess heat production. (2) prevention of heat flux from the hotter environment, (3) reduced necessity for intensive hyper- ~enti~~~ti~n.

A~,~rto\\,/c,~/c/c~~~i~,/~~.~ -The authors wish to thank Mr R. L. Kagon and Mrs E. Lehman for helpful comments in pre- paring the manuscript. We are also grateful to Professor H. hfendelssohn and Mr U. Marder of the Department of Zoology. Tel Aviv University. for helpful suggestions and kindness in rearing the experimental ~~nin,~~i~~~nd to Pro- fessor J. Gil of the Deoartment of Botanv. The Hebrew llniversitv of Jerusalem~ for enablmg use of his Ditfusive Resistance Meter. We also wish to thank Mrs P. Raber for her technical ;tssistancc.

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Cutaneous water evaporation—II. Survival of birds under extreme thermal stress