Temperature Regulation in the Speckled Mousebird, Colius Striatus
TEMPERATURE REGULATION IN THE SPECKLED MOUSEBIRD, COLIUS STRIATUS
GEORGE A. BARTHOLOMEW
AND CHARLES H. TROST ’
Department of Zoology University of California Los Angeles, California 99024
Mousebirds, or colies, comprise a monogeneric Oxygen consumption and evaporative water loss order, Coliiformes, containing six species, all of were measured simultaneously. A bird was fasted for at least 2 hr, then placed on a wire mesh platform in which are confined to subsaharan Africa. a l-gal glass respirometer chamber. Any excreta Field observations of the communal roosting produced fell through the platform and sank beneath of colies, their frequent sunbathing, and oc- a 2-cm layer of mineral oil in the bottom of the casional instances of hypothermia (often in chamber, thus minimizing fecal contributions to the birds with wet plumage), have led to the sug- measurement of evaporative water loss. The respirom- eter chamber was equipped with ports for the intro- gestion that they may undergo periods of duction and removal of air, a thermocouple, and an torpor (McAtee 1947; Bartholomew et al. electic humidity sensor. Dried air was passed 1957; Cowles 1959). Their thermoregulatory through the respirometer chamber at 700 cc/min capacity, however, has never systematically at ambient temperatures of 5-40°C; at 42°C the rate was increased to 1590 cc/min. Evaporative water been studied, and despite their abundance and loss was determined from the change in weight of the many unusual features of their structure tubes of Drierite (anhydrous CaSO,) through which and behavior, only isolated fragments of data the effluent air was passed for either 30 or 60 min. are available on any aspect of their physiology. Oxygen consumption was measured by passing a The best source of information on their biology fraction of the dried effluent air (Cot not removed) through a Beckman G-2 recording paramagnetic is the comprehensive treatment by Rowan oxygen analyzer. The values used represent the mini- (1967) of Colius striates, C. colius, and C. mum stable levels attained during a period of at least indicus in southern Africa. 2 hr. Ambient temperature was controlled to within 0.2% by an Aminco bacteriological incubator. Tem- MATERIALS AND METHODS peratures were measured to within O.l”C with 20- gauge copper-constantan thermocouples connected to The Speckled Colies (C. s. minor) used in this study a recording potentiometer, with a thermistor tele- were reared in an aviary and were two and three thermometer, or with a quick registering mercury generations removed from the wild. The original thermometer. Heart rates were recorded on a Grass stock was captured in Natal, South Africa, by Dr. Polygraph from EKG leads secured to right and left Raymond B. Cowles who kindly gave us four second- pectoral areas and to the scapular region. Breathing generation individuals. Our physiological measure- rates were counted by eye and timed with a stop ments were made on two of the second-generation watch or, in some cases, determined from EKG birds and on five third-generation individuals reared records. by Bruce Bartholomew. During the period of study, 12 Body temperatures were measured cloacally. Con- Tnlv 1966-16 Tune 1967. all of the birds were at tinuous records were obtained by inserting a vinyl- ie
r1411 The Condor, 72:141-146, 1970 142 GEORGE A. BARTHOLOMEW AND CHARLES H. TROST
1
FIGURE 1. The relation of body temperature ( TB) to ambient temperature (Ta). The circles represent temperatures of individual birds huddled in an outdoor aviary at night. All other body temperatures were determined at the end of periods of measurement of FIGURE 3. The relation of evaporative water loss oxygen consumption, either during daytime (unshaded) (EWL) to Ta. Symbols and displacement of nocturnal or at night (shaded). Vertical lines show ranges; hori- values as in figure 1. See text for humidities. zontal lines show means; rectangles enclose the 95 per cent confidence interval (li: & t x SE). For graphic purposes the symbols for the night TB at 20 and 35°C are plotted 1” below the Tn at which they were mea- measured was about 25 per cent lower than sured. the value predicted by the equation of Lasiew- ski and Dawson (1987) for nonpasserine birds. Oxygen consumption at all tempera- about 39°C but at ambient temperatures tures measured was slightly lower at night above 35°C they became hyperthermic (fig. than during the day. 1). During the nocturnal measurements of The slope of the least squares regression of oxygen consumption, body temperatures were daytime GO, on T* below thermal neutrality more variable and lower than during the day. extrapolates to zero at a temperature of Most of the measurements fell between 35 and 38.5”C which is very close to the mean body 38°C and Tn varied directly with T* between temperature at rest. Thermal conductance 5 and 35°C. Body temperatures of birds huddled in groups at night in the outdoor (?OP/TB-TA) below neutrality was con- aviary ranged from 34 to 38°C (mean = stant at 0.1 cc 02/g-hr-“C during the day 35.7” ) * and decreased slightly to 0.09 at night. These figures are slightly but insignificantly lower OXYGEN CONSUMPTION (GO,) than the value (0.12 cc 0*/g-hr-“C) predicted by the equations of Herreid and Kessel (1967) The general shape of the curve describing the and Lasiewski et al. ( 1967). relation of $0, to TA is typical of that for small birds (fig. 2). The thermal neutral zone EVAPORATIVE WATER LOSS (EWL) extends approximately from 25” to beyond Evaporative water loss (fig. 3) was inde- 40°C. The mean minimal daytime oxygen pendent of ambient temperatures of 530°C consumption ( 1.2 cc/g-hr ) of the six birds and was of the magnitude (5-6 per cent of body weight per day) expected for 50-g non- passerine birds (Crawford and Lasiewski 1968). Above 35°C evaporative water loss in- creased markedly. At all temperatures mea- sured, it averaged lower at night than during the day. The humidity in the respirometer 7 chamber, which is a function of the flow rate ‘\ and rate of water loss by birds, was approxi-
lb5 mately 2.0 g HzO/m3 at all ambient tempera- tures of 5-30X, and increased to 15.8 at 40”. At 42” the rate of air flow was changed from 700 to 1500 cc/min, which reduced the FIGURE 2. The relation of oxygen consumption to humidity in the chamber to 11.5 g HzO/m3 Tn. Symbols and displacement of nocturnal values as despite the increased water loss by the birds. in figure 1. The line was fitted by the method of least squares to daytime values. The fraction of metabolic heat dissipated by TEMPERATURE REGULATION IN THE SPECKLED MOUSEBIRD 143
FIGURE 4. The ratio of evaporative water loss to oxygen consumption and the relation of evaporative cooling to metabolic heat production as functions of TA. It is assumed that the oxidation of 1 cc of 02 yields 4.8 cal and that 0.58 cal are required to evapo- rate 1 mg of HsO. See text for humidities.
FIGURE 6. The rates of breathing and gular flutter evaporation increased slowly from less than in relation to TB. 10 per cent at 5°C to 33 per cent at 35°C. When exposed to heat stress the birds em- ployed gular flutter (see below), and at 40°C for enhancing evaporative cooling under con- and a water vapor pressure of 17 mm of Hg ditions of heat stress (Bartholomew et al. they were able to lose all of their metabolic 1968). Occasional brief and intermittent heat by evaporation (fig. 4). episodes of gular flutter occurred at ambient temperatures of 35°C. At higher ambient BREATHING RATE AND GULAR FLUTTER temperatures the duration of the periods of At ambient temperatures of 535°C breathing gular flutter increased but the rate of flutter rate averaged about 50 per min, but between remained relatively uniform (fig. 5). At 35 and 40°C it increased approximately two ambient temperatures of 35-4O”C, the birds occasionally twitched the gular area slightly fold (fig. 5). The increase in breathing rate at a frequency of about 200 per min with at the higher ambient temperatures was as- the mouth either open or closed, and they sociated with an increase in amplitude of often gaped the mouth without gular flutter. breathing and a progressive elevation in body At ambient temperatures above 40°C gular temperature. However, under the conditions flutter was almost continuous. of measurement there was no regular relation Intermittent gular flutter was observed in between breathing rate and degree of hy- birds with body temperatures as low as perthermia (fig. 6). 40.1”C. Sustained gular flutter commenced at Like members of several other nonpasserine body temperatures of 42.5” and was char- orders, colies employ gular flutter as a device acteristic of all body temperatures above this level. The frequency of gular flutter appears to be virtually independent of extent of hy- perthermia or degree of heat stress (fig. 6) and probably is a function of the natural resonant frequency of the gular area (see Lasiewski and Bartholomew 1966 for discussion). Calius striotur HEART RATE Minimal resting heart rates were inversely related to ambient temperature between 5 and 35” (fig. 7). The slopes of the least squares regressions of heart rate on T* for the two birds from which complete sets of data could be obtained were similar and, unlike the curve for ?O,, do not extrapolate to zero at TA = Tg. FIGURE 5. The rates of breathing and gular flutter in relation to Ta. The mean minimal resting heart rates of four 144 GEORGE A. BARTHOLOMEW AND CHARLES H. TROST
TORPIDITY Although the significance of the phenomenon under natural conditions cannot yet be as- sessed, in the laboratory C. striatus can suc- cessfully enter and arouse from a state of torpor in which oxygen consumption is far below normal levels and body temperature falls 15°C or more (figs. 8 and 9). We were able to induce daily cycles of torpor by gradually reducing the food ration until the weight of the birds fell 10-15 per cent below their customary weight of about 50 g. The onset of torpor always occurred during the night and arousal usually preceded FIGURE 7. The minimal heart rates of two mouse- the time when the lights came on in the birds in relation to Ta. The lines are fitted by the morning. The colies were able spontaneously method of least squares. to increase their oxygen consumption while in a condition of profound hypothermia and produce sufficient heat by their own metab- individuals in the zone of thermal neutrality olism to arouse to normal levels of body tem- was 244 per min (range, 220-285). No perature within W-90 min in ambient tem- systematic effort was made to determine peratures of lQ-20°C. During arousal, oxygen maximal heart rates. However, the maximum consumption rose to more than twice the rates observed were 580590 per min. Both standard level at 20°C and peaked prior to the minimal and maximal rates are lower than the attainment of the normothermic body tem- expected on the basis of size. peratures (fig. 9).
1 Colius striatus
2200 2400 0200 0400 0600 0800 1000 tp’ LIGHTS OFF -4 TIME OF DAY
FIGURE 8. Continuous records of CO, of two mousebirds (A and B) on consecutive nights in a Ta of 192%. The daily food ration was insufficient for weight maintenance and the birds were about 10 per cent below their usual weights. Three of the four arousals were spontaneous, but one (As) was caused by the attachment of a cloaca1 thermocouple. A detailed record of the course of TB and +O, in A, is shown in figure 9. TEMPERATURE REGULATION IN THE SPECKLED MOUSEBIRD 145
sidered elsewhere (e.g., Pearson 1950, 1960; Bartholomew et al. 1962; Lasiewski 1963) and need not be re-examined here. However, it is noteworthy that colies are neither very small, like hummingbirds, nor do they feed on airborne insects, like swifts and capri- mulgids. Consequently, they do not have the necessity of maintaining a very high weight- relative metabolism, nor do they face the prob- lem of short-term food shortages associated with poor weather, which presumably favor the evolution of the capacity for torpidity. Ex- cept for the instances mentioned above, ex- perimental documentation’ for a nocturnal de- cline in body temperature of as much as 15°C 0 FIGURE 9. The course of TB and VO, during is available only for the Inca Dove (Scarda- arousal of A2 (see fig. 8) in a Ta of 19.2%. The fella incu), and this species has extremely torpid bird was removed from the respirometer at limited capacity for arousal to normothermic minute zero, a cloaca1 thermocouple was attached, temperatures ( MacMillen and Trost 1987). and the bird was returned to the respirometer chamber by minute 3. The ecological importance of the capacity of colies to become torpid remains unknown. Their torpor cannot be attributed to an in- ability to thermoregulate. Our data and the DISCUSSION observations of Rowan ( 1987:80) show that Even from this limited and exploratory study colies remain normothermic in temperatures it is apparent that in thermoregulation, as in near 0°C. The experimental instances of behavior and anatomy, colies are of unusual torpor were induced neither by cold nor wet, interest. Their body temperature, weight- but occurred after a modest loss in body relative oxygen consumption, and heart rate weight caused by a reduction in daily food all average lower than those of passerines of ration. However, nothing is known about similar size. Like other birds which employ weight variation in colies under natural con- fixed-frequency gular flutter they are able ditions. Cowles (1959:X34) has pointed out to use evaporative cooling at a minimal meta- that colies are almost exclusively vegetarian, bolic cost (Lasiewski and Bartholomew 1966; and Rowan ( X%7:89) has emphasized that Bartholomew et al. 1968). Indeed, at an because of their relatively generalized food ambient temperature of 40°C and water vapor habits they are normally assured of an ade- pressure of 17 mm Hg they dissipated by quate “succession of indigenous fruit through- evaporation all of their metabolic heat at such out the year.” small energetic cost that it was not measurable About all that can be said at present is that under the experimental conditions employed individuals of one species of mousebird have (fig. 2). However, like all birds, colies become the capacity for nocturnal torpidity at ambient hyperthermic when ambient temperatures ap- temperatures near 20°C and that the ecological proach or exceed the usual range of body importance of this capacity awaits further temperatures. Hyperthermia, of course, facili- study. tates heat loss by conduction and convection and reduces dependence on evaporative cool- SUMMARY ing. Body temperature in quiet normothermic The most interesting result of the present mousebirds averaged about 2°C lower than study is the demonstration that adult colies, in passerine birds of similar size and showed like some humming birds, swifts, and capri- a more marked nocturnal decline. The stan- mulgids, can enter a state of torpor in which dard oxygen consumption for this nonpasserine body temperature falls 15°C or more below species (I.2 cc/g-hr) was about 25 per cent normothermic levels, and are then capable less than predicted on the basis of weight, and of arousing from this profound hypothermia thermal conductance (0.1 cc 02/g-hr-C‘ dur- by means of their own metabolic heat produc- ing the day, and 0.09 at night) was slightly but tion without the addition of heat from any insignificantly lower than the predicted value. external source. The potential energy saving Oxygen consumption was essentially inde- in birds of such a capacity has been con- pendent of ambient temperature from 25” to 146 GEORGE A. BARTHOLOMEW AND CHARLES H. TROST beyond 40°C but evaporative water loss in- Anna Hummingbird, and Poor-will. Condor 59: creased markedly at ambient temperatures 145-155. BARTHOLOMEW, G. A., J. W. HUDSON, AND T. R. above 35°C. Below 35X, evaporative water HOWELL. 1962. Body temperature, oxygen con- loss was of the magnitude expected on the sumption, evaporative water loss, and heart rate basis of body weight. Mousebirds employ in the Poor-will. Condor 64:117-125. gular flutter. At an ambient temperature of BARTHOLOMEW, G. A., Il. C. LASIEWSKI, AND E. C. 40°C and a water vapor pressure of 17 mm CRAWFORD, JR. 1968. Patterns of panting and gular flutter in cormorants, pelicans, owls, Hg they were able to dissipate all of their and doves. Condor 7th31-34. metabolic heat by evaporation of water, at a COWLES, R. B. 1959. Zulu journal. Univ. Calif. negligible metabolic cost. The frequency of Press, Berkeley. gular flutter, which is probably related to the CRAWFORD, E. C., AND R. C. LASIEWSKI. 1968. natural resonant frequency of the gular area, Oxygen consumption and respiratory evaporation of the Emu and Rhea. Condor 70:33%339. was independent of the degree of heat stress HERREID, C. F., AND B. KESSEL. 1967. Thermal or extent of hyperthermia. conductance in birds and mammals. Comp. Heart rate was inversely related to body Biochem. Physiol. 21:405-414. temperature below the thermal neutral zone, LASIEWSKI, R. C. 1963. Oxygen consumption of and the mean minimal resting rate in thermal torpid, resting, active, and flying hummingbirds. Physiol. Zool. 36: 122140. neutrality was 244 per min. LASIEWSK~, R. C., AND G. A. BARTHOLOMEW. 1966. Captive colies maintained at about 20°C Evaporative cooling in the Poor-will and the on a reduced food ration will enter a state of Tawny Frogmouth. Condor 68:253-262. nocturnal torpor in which body temperature LASIEWSKI, R. C., AND W. R. DAWSON. 1967. A re-examination of the relation between standard falls almost to air temperature and oxygen metabolic rate and body weight in birds. Condor consumption is profoundly reduced. They are 69: 13-23. capable of arousing to a normothermic state in LAS&SK& R.C., W. W. WEATHERS, AND M. H. 60-90 min by metabolically produced heat. BERNSTEIN. 1967. Physiological responses of The significance of their capacity for dor- the giant hummingbird, Patagoniu gigas. Comp. Biochem. Physiol. 23:797-813. mancy in nature remains to be assessed. MACMILLEN, R. E., AND C. H. TROST. 1967. Noc- turnal hypothermia in the Inca Dove, Scurdafella ACKNOWLEDGMENTS incu. Comp. B&hem. Physiol. 23:243-253. This study was supported in part by NSF Grant MCATEE, W. L. 1947. Torpidity in birds. Amer. GB-5139. We are grateful to Dr. R. B. Cowles for Midland Naturalist 30: 191-206. giving us the colies which made this study possible PEARSON, 0. P. 1950. The metabolism of hum- and to B. Bartholomew for rearing the additional mingbirds. Condor 52: 145-152. colies which we used. PEARSON, 0. P. 1966. Torpidity in birds. Bull. Mus. Comn. Zool. 124:9%103. LITERATURE CITED ROWAN, M. K.- 1967. A study of colies in southern Africa. Ostrich 38:63-115. BARTHOLOMEW, G. A., T. R. HOWELL, AND T. J. CADE. 1957. Torpidity in the White-throated Swift, Accepted for publication 16 July 1969.