SHORT COMMUNICATIONS 99

The Condor 88:99-100 0 The CooperOrnithological Society 1986

CUTANEOUS EVAPORATION IN HEAT-STRESSED SPOTTED ’

JACOB MARDER, IDIT GAVRIELI-LEVIN AND PNINA RABER Department of Zoology, The Hebrew Universityof Jerusalem,Jerusalem 91904,

Key words: Body temperature;thermoregulation; cu- enabled rapid and accurate measurements.Our prelimi- taneousevaporation: hyperthermia. nary experimentshave shown that the procedureused for T, measurescore tissuetemperature and avoids punctur- Many speciesof are relatively small (< 500 ing the abdominal air sacs. We determined cutaneous g), diurnally active ground dwellers that are naturally ex- evaporation by measuringskin resistanceto vapor diffu- posed to high ambient temperatures(T,) and low relative sion using Lambda Instrument Li-Cor Model Li-700 humidities (RH). Sandgrouse(Pteroclididae), being small Transient porometer (diffusive resistance meter). Mea- birds (weighingbetween 200 and 400 g) having a relatively surementswere done by gently pressingthe sensor head high standard metabolic rate (SMR), would have to pos- on about 6 cm* of breast skin (feathersfrom this spot had sessan effective mechanism for dissipatingheat. been pluckedtwo weeksearlier). The instrument,equipped Spotted Sandgrouse( senegallus), like other with a quick response Vaisala humidity sensor, makes of the Pteroclididae, are successfuldesert birds possiblerapid (15 to 20 set each) and accuratereadings; (Thomas 1983, Maclean 1984). Thomas and Robin (1977) in addition it enables high resolution (kO.05 set cm-l) reported that in incubating female sandgrouse(P. sene- within a diffusive resistancerange of 0.5 to 20.5 cm-l. gallus, P. coronatus,P. alchata) neither gular-fluttering Instantaneoustemperature readingsof both the humidity nor gapingwere observedin birds exposedin the open to sensorand evaporating surfacewere taken using built-in 40 to 50°C T,. This strongly suggestedthat body and egg thermister probes. Calibration and measurements were coolingcould be achievedonly if a very efficient cutaneous done under isothermal conditions. The calibration plate evaporative water loss (CE WL) mechanism existed in in- temperatureswere regulatedto those measuredby the po- cubating sandgrouse. rometer humidity sensor. During measurementsthe po- Certain birds evaporate considerableamounts of water rometer temperaturewas adjustedclose to T. (+ 1°C). Cu- via the skin (Bernstein 1969, 197la, b; Smith and Suthers taneousevaporation can be calculatedwhen the following 1969; Marder and Ben-Asher 1983), a mechanism that values are known: (1) the resistanceto diffusion of vapor appearsto be important for survival under extremely hot through the skin, r,, (2) feather coat resistance,r,, (3) air (T, > 45oC)environmental conditions (Marder 1983).Since resistance,r,, (4) skin surfacevapor density, (5) T,, and the Spotted Sandgrouseis active during hot summer days (6) T, (Monteith 1973, Cena and Monteith 1975, Camp- (Thomas and Robin 1977). one can hvnothesize that this bell 1977). has specialthermoregulatory capabilities. To test this, Most measurementswere done on six birds. The results we studied CE WL in this bird exposedto high T,. are presentedas means *SD. Further details of measuring proceduresand calculationshave been reported elsewhere MATERIAL AND METHODS (Marder and Ben-Asher 1983). Six adult Spotted Sandgrouse,three females and three males, were trapped during the winter in the southern RESULTS AND DISCUSSION Negev Desert of Israel, about 80 km south of Beer Sheba. Mean body mass was 260 g (? 17 SD). The birds were During long term experiments (6 to 8 hr each), T, varied kept in a 1 m3 cageinside a temperature-controlledroom between 41.4 + 0.6 and 42.6 * 0.5”C at T, of 27,42,45, (16L8D) where food and water were freely available. The and 51”C, respectively (Table 1). In these experiments, front wall of the cage was covered with black cloth, en- birds were exnosed for 2 to 3 hr to each T,. Stable T. of abling the investigatorto move freely outside the cage.In 42.0 + 0.8”CZwasmeasured in five birds after 240-&n not to disturb the birds, especially at high T,, all exposureto 5 1°C and low RH (< 10%). Skin temperatures activities inside the cagewere carried out in darkness. were always lower than Tb, by between 1.1 and 0.5”C at Under these conditions we exposedthe birds daily to a T,s between 27 and 51°C T,, respectively. Similar phe- series of temperatures between 27 and 51°C. On a few nomena have been observed in Rock Pigeons (Columba occasionsT. was elevated to 60°C for two hours. For five livia) exposedto moderate and high T, 30 to 50°C (Marder weeks,birds were exposedon six days per week to 8 hr of and Ben-Asher 1983, Webster et al. 1985). elevated air temperatures. Skin temperatures (T,) were High frequency panting and gular-fluttering (>300 determined with a calibrated YSI 24-gauge hypodermic min-I) were observedat T., of 40 to 60°C. In two survival probe (No. 524), the edge of which was lightly pressedto tests,birds were exposedfor 240 min to 5 1°C and for 120 the skin so that about half the needle shaft was in contact min to 60°C (RH < 10%). In each case, the sandgrouse with the skin. The probe was attached to the skin for stood quietly during the entire test, and showed no be- several seconds until stable readings were reached. We havior suggestingthe onset of a critical situation. measuredskin temperaturesduring or immediately after The rate of skin evaporation of the sandgrouseat 27°C skin resistancemeasurements were completed. Body tem- was 1.6 mg H,O cm-2 hr-I, and the correspondingresis- perature (T& measurementswere taken last in this series. tance value was 103.0 set cm-l (Table 1). During heat They were carried out by quick insertion of the hypoder- stress,resistance decreased to 20.5, 13.5, and 15.0 set cm-’ mic probe parallel to the vent through the lower intestinal and water evaporation increasedto 11.1, 14.3, and 13.6 tissueto a depth of 3 to 5 cm. The use of the needle probe mg H,O cm-2 hr-l at T, of 41,45, and 5 1°C respectively. The valuesfor CE WL were calculatedfrom measurements of skin resistanceto vapor diffusion determined on un- LReceived 20 February 1985. Final acceptance13 Au- feathered skin of the pectoral region. However, the actual gust 1985. evaporation may be lower by about 30% if the resistance 100 SHORT COMMUNICATIONS

TABLE 1. Body temperature (r,, “C), skin temperature (T$. “C), skin resistanceto vapor diffusion (r$, set cm-‘), and skin evaporation (E,, mg H,O cm hrl) of six* Spotted Sandgrouseexposed to high ambient temperatures (TA. Measurements were made after five weeks of acclimation.

T. Tb T* Ta - T, r, CE WL 21 41.4 + 0.6 40.3 + 0.2 1.1 * 0.3 103.0 * 26.0 1.6 t 0.4 42 42.0 + 0.2 (4) 41.3 ? 0.6 (4) 0.7 + 0.5 (4) 11.1 f 6.5 (4) 45 42.4 f 0.3 41.6 * 0.4 0.8 _t 0.2 14.3 ? 5.2 51 42.6 * 0.5 42.1 + 0.6 (10) 0.5 * 0.3 13.6 -t 5.1 (10) * Numberof dataobtained on lessor mire thansix exposures are gven in parentheses. of the feathers and the air boundary layer are taken into nensisduring ontogeny of thermoregulation. Comp. account. Biochem. Physiol. 38A:6 1 l-6 17. Of six birds exposedto heat stress,only one evaporated BERNSTEIN,M. H. 1982. Temperature regulation in ex- water at a stable rate. In four heat-stresstrials at 42, 45, ercising birds, p. 189-197. In C. R. Taylor, K. Jo- and 51°C T,, the resistanceand evaporation values for hansen, and L. Bolis [eds.], A companion to bared skin were r, = 8.6 + 0.7 set cm-l and CEWL = physiology.Cambridge Univ. Press, Cambridge, En- 19.8 f 1.9 mg H,O cm-2 hr-I. For feather-coated skin gland. the correspondingvalues were 10.6 set cm-l and 15.9 mg CAMPBELL,G. S. 1977. An introduction to environmen- H,O cm-* hr-I. These data are close to those measured tal biophysics. Springer-Verlag,New York. in pigeonsexposed to 52°C (Marder and Ben-Asher 1983). CENA,K., ANDJ. L. MONTEITH. 1975. Transfer processes We anticipate that, with improved experimental condi- in animal coats III. Water vapour diffusion. Proc. R. tions, a better evaluation of the cutaneouscooling mech- Sot. Lond. B 188:413-423. anism of the sandgrousewould be achieved. DAWSON, W. D. 1984. Physiological studies of desert Hyperthermia appears routinely to accompany sus- birds: present and future considerations.J. Arid En- tained vigorousactivity in birds (Bernstein 1982). Hyper- viron. 7:133-155. thermia in resting birds is widely believed (see Dawson MACLEAN, G. L. 1984. Arid-zone adaptationsof waders 1984) to representan efficient mechanism for dissipating (Aves: Charadrii). S. Afr. J. Zool. -19:78-8 1. dry heat. Our observations(carried out at T. 45 to SO’C) MARDER, J. 1983. Cutaneouswater evaporation. II. Sur- on a variety of small birds suggestan alternative inter- vival of birds under extreme thermal stress.Comp. pretation of hyperthermia. Under conditions of extreme Biochem. Phvsiol. A Comn. Phvsiol. 75:433-439. heat stress,when T, cannot be stabilized,it appearsequally MARDER, J., AND j. BEN-ASH&. 19i3. Cutaneouswater likely that hyperthermia may develop as a consequence evaporation. I. Its significancein heat stressedbirds. of the insufficientcapacity of the evaporative cooling sys- Comp. Biochem. Physiol. A Comp. Physiol. 75:425- tem to dissipate both metabolic and external heat. This 431. view is further supportedby previous (Thomas and Ma- MONTEITH,J. L. 1973. Principlesof environmental phys- clean 1981) and present investigationswhere Tb between ics. Edward Arnold, London. 40 and 42.5”C have been observed in desert sandgrouse SMITH,R. M., ANDR. SUTHERS. 1969. Cutaneouswater even after prolongedexposure to T, > 50°C. The absence loss as a significantcontribution to temperature reg- of marked hyperthermia (41.2 to 42.4% Tb), at T,s of 45 ulation in heat stressedpigeons. Physiologist 12:358. to 50°C. was also observedin acclimated .-pigeons (Marder THOMAS,D. H. 1983. Adaptations of desert birds: sand- and Ga&ieli-Levin, unpubl.). grouse(Pteroclididae) as highly successfulinhabitants The nresentfindings and nreviousstudies (Marder 19831 of Afro-Asian arid lands. J. Arid Environ. 7: 157-l 8 1. suppo; the view that cutaneouswater evaporation in des: THOMAS, D. H., AND A. P. ROBIN. 1977. Comparative ert sandgrouseand pigeons is an important mechanism studies of thermoregulatoryand osmoregulatorybe- for surviving hot environmental conditions. havior and physiology of five speciesof sandgrouse We thank A. Shirihai for trappingthe experimentalbirds. (Aves: Pteroclididae)in . J. Zool. Lond. 183: i29-249. LITERATURE CITED THOMAS, D. H., AND G. L. MACLEAN. 198 1. Comparison of physiologicaland behavioral thermoregulationand BERNSTEIN, M. H. 1969. Cutaneous and respiratory osmoregulationin two sympatric sandgrousespecies evaporation in Painted Quail Excalfactoriachinensis. (Aves: Pteroclididae). J. Arid Environ. 4:355-358. Am. Zool. 9: 1099. WEBSTER,M. D., G. S. CAMPBELL,AND J. R. KING. 1985. BERNSTEIN,M. H. 197la. Cutaneouswater loss in small Cutaneousresistance to water vapor diffusion in pi- birds. Condor 731468-469. geonsand the role of the plumage. Physiol. Zool. 58: BERNSTEIN,M. H. 1971b. Cutaneous and respiratory 58-71. evaporation in the Painted Quail, Excalfactoria chi-