Iowa State University

From the SelectedWorks of Carol Vleck

July, 1983

Energy Metabolism and Nocturnal Hypothermia in Two Tropical Frugivores, Manacus vitellinus and Pipra mentalis George A. Bartholomew, University of California, Los Angeles Carol M. Vleck, University of California, Los Angeles Theresa L. Bucher, University of California, Los Angeles

Available at: https://works.bepress.com/carol-vleck/19/ Division of Comparative Physiology and Biochemistry, Society for Integrative and Comparative Biology

Energy Metabolism and Nocturnal Hypothermia in Two Tropical Passerine Frugivores, Manacus vitellinus and Pipra mentalis Author(s): George A. Bartholomew, Carol M. Vleck and Theresa L. Bucher Source: Physiological Zoology, Vol. 56, No. 3 (Jul., 1983), pp. 370-379 Published by: The University of Chicago Press. Sponsored by the Division of Comparative Physiology and Biochemistry, Society for Integrative and Comparative Biology Stable URL: http://www.jstor.org/stable/30152601 Accessed: 23-05-2016 21:08 UTC

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This content downloaded from 129.186.176.217 on Mon, 23 May 2016 21:08:30 UTC All use subject to http://about.jstor.org/terms ENERGY METABOLISM AND NOCTURNAL HYPOTHERMIA IN TWO TROPICAL PASSERINE FRUGIVORES, MANACUS VITELLINUS AND PIPRA MENTALIS'

GEORGE A. BARTHOLOMEW, CAROL M. VLECK,2 AND THERESA L. BUCHER

Department of Biology, University of California, Los Angeles, California 90024 (Accepted 12/3/82)

Oxygen consumption (Vo2) and body temperature (Tb) were measured in Manacus vitellinus (mean mass, 15.5 g) and Pipra mentalis (mean mass, 12.3 g) on Barro Colorado Island, Panama. The two species had the same mean euthermic nocturnal Tb (37.9 C). During activity Tb sometimes reached 43 C. In both species, nocturnal basal metabolic rate (BMR) (41.69 cm3 O2/h in M. vitellinus and 34.9 cm3 02/h in P. mentalis) was significantly less than predicted on the basis of mass. At night fasted frequently, and unfasted birds occasionally, became hypothermic, with Tb rang- ing between 27 and 36 C. Their Tb always remained several degrees above ambient temperature (Ta). The lowest Tb recorded was 26.8 C at a Ta of 14.6 C. Thermal conductance was the same in euthermic and hypothermic birds. save substantial amounts of energy by their nocturnal hypothermia. During a 12-h night a 14-g M. vitellinus maintaining a Tb of 27 C in a Ta of 22 C for 10 h would expend 6.4 kJ less than if it maintained its Tb at the mean euthermic nocturnal level. This represents a savings of 58%. The selective pressures that have favored nocturnal hypothermia in manakins have probably operated on other small tropical frugivorous birds. We predict that the main components of the metabolic pattern of manakins will also be found in other small tropical with similar food habits.

INTRODUCTION the annual period of food scarcity (Wor- Relatively little is known about the en- thington 1983). ergy metabolism of birds of the humid The limited physiological information tropics. However, data are available on available suggests that some manakins manakins, a group of small, fruit-eating have adaptations for minimizing energy passerines resident in tropical, wet forests. requirements. Under some circumstances, The manakins (family Pipridae) are among they have lower metabolic rates than most the most widespread and abundant of the other passerines of similar size (12-20 g), small, neotropical, avian frugivores. They and they can experience an atypically large are characterized by small clutches and depression in body temperature at night unusually long life spans; their mobility is (Vleck and Vleck 1979; Bucher and Wor- minimized by their attachment to tradi- thington 1982). tional breeding sites, i.e., leks (Snow 1962a, The present study was undertaken to 1962b). Fruits that are important in their examine more closely the energy metabo- diet are seasonally in short supply, and en- lism and thermoregulation, expecially the ergy requirements may restrict reproduc- occurrence and utility of nocturnal hy- tive activity in a given population during pothermia (defined in this context as body temperatures of 36 C or less), in golden- I This study was supported by NSF grant DEB- collared and red-capped manakins, Ma- 81-03513 to G. A. Bartholomew and a grant from nacus vitellinus and Pipra mentalis. the American Philosophical Society to C. M. Vleck. The work was carried out using facilities of the MATERIAL AND METHODS Smithsonian Tropical Research Institute on Barro Colorado Island, Panama. The manakins were captured in mist nets 2 Present address: Department of Ecology and during June and July 1981 on Barro Col- Evolution, University of Arizona, Tuscon, Arizona orado Island, Panama, and housed indi- 85721. vidually, or in pairs, in cages made of wood battens and mosquito netting. The cages Physiol. Zool. 56(3):370-379. 1983. C 1983 by The University of Chicago. All were pyramidal in shape, 75 cm high and rights reserved. 0031-935X/83/5603-8264$02.00 30 cm wide at the base. They had two

370

This content downloaded from 129.186.176.217 on Mon, 23 May 2016 21:08:30 UTC All use subject to http://about.jstor.org/terms ENERGETICS 371 perches, each with a small shelf on which SAMPLING SYSTEM I REFERENCE SYSTEM Outdoor Air food could be placed. The cages were kept in a screened shelter that allowed the birds Desiccant Pump to experience the natural photoperiod and temperature. The diet of the captive birds consisted of local rain-forest fruits supple- Pump mented with fresh grapes, preserved blue- berries, and rehydrated dried currents. Flowmeter When this diet was available ad lib. the body mass of the birds usually remained Respirometer V Chamber within 10% of that at capture. DIDesiccant The manakins were kept in captivity for

3-6 days, then released at the site of cap- Thermomete T.C. C02 Absorbant Desiccant V C02 Abs(rbant ture. Two individual manakins had to be Flowmeter force-fed the first day after capture; the V others fed almost immediately.

At approximately 0600, 1800, and 2400 02 Sensor hours each day, we weighed the birds with and Analyzer a Pesola scale and determined their body A-D temperatures (Tb). A 40-gauge copper-con- Converter Pump stantan thermocouple was inserted to a Computer depth of about 2 cm in the cloaca. The Flowmeter thermocouple was connected to a Bailey Printer Bat thermocouple thermometer, and the output was either read directly or recorded FIG. 1.-Apparatus used for measuring effects of temperature on the energy metabolism of manakins. with a microprocessor as described below. The systems were calibrated against a mercury thermometer traceable to the U.S. autoranging voltmeter equipped with an Bureau of Standards. A/D converter. The recording interval, We also measured mass and Tb at the which was controlled by the microproces- beginning and end of each determination sor, was usually 30 s but was varied from of oxygen consumption. The time that 10 min to 10 s depending on the variability elapsed between opening the metabolic in the Vo, of the . Instantaneous rates chamber and measuring Tb was less than of oxygen consumption were calculated and 1 min. During some oxygen consumption printed at each sample interval, as were determinations, continuous records of Tb time and signal voltage. The instantaneous were obtained by inserting a thermocouple rates, which were based on the exponential into the cloaca and tying the thermocouple wash-out characteristics that were mea- leads to the base of one of the bird's rec- sured for each system (see Bartholomew, trices with thread. Vleck, and Vleck [1981] for description), Rates of oxygen consumption (Vo2) were allowed us to follow Vo, closely during measured with an open flow system using entry into and arousal from the hypo- an Applied Electrochemistry S3A two- thermic state. channel oxygen analyzer with sensors, The respirometer chambers were lucite drying trains, CO2 scrubbers, pumps, and cylinders with a volume of about 800 ml. flowmeters arranged as shown in figure 1. The bottom of each chamber was covered Ambient temperature (Ta) was controlled with wire mesh. Input and output mani- to within 0.5 C with a constant-tempera- folds that extended the entire length of the ture cabinet and monitored with thermo- chamber facilitated thorough mixing of couples like those used for measuring Tb. chamber air. Airflow (150 ml/min) was The thermocouple thermometers and monitored upstream from the chambers oxygen analyzer were connected to a four- with flowmeters calibrated against a channel switching device that was con- Brooks Mass Flowmeter. trolled by a Rockwell AIM-65 micropro- Some birds were fasted by depriving cessor and connected to a Fluke 8810A them of food from 1300 or 1400 hours until

This content downloaded from 129.186.176.217 on Mon, 23 May 2016 21:08:30 UTC All use subject to http://about.jstor.org/terms 372 G. BARTHOLOMEW, C. VLECK, AND T. BUCHER the following morning. Otherwise food was returning to a perch. The manakins strug- continuously available during daylight gled hardly at all when handled and settled hours. Birds were put into the respirom- down almost immediately when put in a etry chambers between 1730 and 1800 respirometer chamber. hours, corresponding to dusk when birds would normally cease feeding. The Vo, of EUTHERMY a few birds was measured during daylight Body temperature.-The body temper- hours at Ta's in their thermal neutral zone atures of euthermic Manacus vitellinus and (TNZ). All measurements were made in Pipra mentalis did not differ significantly. the dark. For all measurements that we The cloacal Tb of birds at night was 37.9 report, the birds had been in the respi- C + 0.9, no. = 29. As in other small rometry chamber for at least 1 h. passerines, the Tb of manakins rises when Unless otherwise stated, all numerical they become excited or active. On several results are reported as means + standard occasions we recorded cloacal tempera- deviations. Means are compared using two- tures of more than 43 C. tailed Student t-tests; P-values less than Basal metabolic rate.-At night in ther- .05 are treated as significant. If the 95% mal neutrality, the resting Vo2 of M. vi- confidence interval of a measured quantity tellinus (mean mass, 15.5 g) was 41.69 + included the predicted value of that quan- 7.85 cm3/h. The corresponding daytime tity, we assumed that the measured and value (42.85 + 8.12 cm3/h) was not sig- predicted values were statistically indistin- nificantly different (see table 1 for SI val- guishable. ues). The two values are significantly less than those predicted on the basis of mass RESULTS (Aschoff and Pohl 1970). BEHAVIOR In P. mentalis (mean mass, 12.3 g) night- Both species of manakins were remark- time BMR (34.91 + 5.11 cm3/h) was sig- ably quiet in captivity. They showed little nificantly less than the daytime BMR (45.93 of the incessant activity typical of many + 8.78 cm3/h), and it is also significantly small, captive passerines. They remained less than the corresponding value pre- motionless much of the time, perching qui- dicted on the basis of mass (table 1). Day- etly for 15-20 min, then briefly visiting the time BMR was not significantly different food tray to take a berry or two before from predicted.

TABLE 1

BASAL METABOLIC RATE (BMR) AND TOTAL THERMAL CONDUCTANCE (Ct) IN Manacus vitellinus AND Pipra mentalis

M. vitellinus P. mentalis

Observed Predicteda Observed Predicteda

BMR, night (mW) ...... 233 + 43 270 195 - 29 229 95% confidence interval 211-255 213-343 178-212 180-291 Mass (g)...... 15.5 + 1.6 ... 12.3 + .4 No.a ...... 17; 7 ... 13; 7 BMR, day (mW) ...... 239 + 45 367 256 + 49 310 95% confidence interval 194-284 268-504 188-324 225-427 Mass (g)...... 15.8 + 1.6 ... 12.4 + .7 No.a ...... 6; 6 ... 4; 4 Ct (mW/C) ...... 17.8 13.7 16.2 12.3 95% confidence interval 10.9-24.6 9.7-19.4 -2.8-35.2 7.1-19.6 Mass (g)...... 14.7 + 2.1 ... 12.1 + .9 N o.a ...... 12; 7 ... 5; 3

NOTE.-BMR is based on stable minimum values of Vo2 of birds in thermal neutrality. Ct is based on simultaneous measurement of Vo2, Ta, and Tb below thermal neutrality when Ct appears to be minimal. (See text for details.) Predicted values of BMR are from Aschoff and Pohl (1970). Daytime BMR, kcal/h = 0.045g.704; nighttime BMR, kcal/h = 0.032g.726. We have assumed that consumption of 1 ml 02 yields 0.0048 kcal or

20.097BMR and J. PredictedCt are calculated values offor Ct the are individual from Aschoff prediction (1981); at nighttime the given Ct, mass. cm3/(h " g C) = 0.576 g-.461. The 95% confidence intervals for predicted a Number of observations at different temperatures; number of birds.

This content downloaded from 129.186.176.217 on Mon, 23 May 2016 21:08:30 UTC All use subject to http://about.jstor.org/terms MANAKIN ENERGETICS 373

Effect of Ta on !Vo2.-In M. vitellinus and 35 C. The lowest temperature we re- corded was 26.8 C in an M. vitellinus at at night the lower critical temperature (Tc) is approximately 25 C (fig. 2). The slope a Ta of 14.6 C; Vo, in this bird was only of mass-specific Vo2 on Ta below T, was 44% of the mean Vo2 of euthermic birds -0.230 _ .025 cm3/(g - h C). In P. men- at the same Ta. talis T~c was approximately 27 C (fig. 3). We obtained a number of continuous The slope of mass-specific Vo2 on Ta below records of Vo, during cycles of nocturnal Tc was -0.315 + .42 cm3/(g h C). hypothermia, including entry into and arousal from hypothermia (fig. 4). In our HYPOTHERMY most complete set, we simultaneously re- Unlike most other passerines for which corded Vo2 and Tb for 11 h from a P. men- data are available, the nocturnal body talis whose Tb dropped to 34.2 C during temperatures of M. vitellinus and P. men- the night (fig. 5). This record is noteworthy talis sometimes fall below the levels char- for the close correspondence between the acteristic of the euthermic state (Bucher short-term variations in Vo, and the os- and Worthington 1982). We frequently cillations in Tb, and the steady upward measured cloacal temperatures between 30 trend of Tb and slight upward trend in Vo, for 3 h before the normal time of daybreak. The rates of entry into and arousal from Manacus hypothermia vary substantially (figs. 4, 5). During episodes of hypothermia Tb always remained several degrees C above Ta, and Vo, never fell to less than about 30% of BMR. When hypothermic were taken from the respirometer, they were le- thargic but responsive. If released, they

Manacus 10 14 18 22 26 30 34 36 Meosured AMBIENT TEMP. (C) FIG. 2.-The relation of oxygen consumption to ambient temperature in Manacus vitellinus. Filled circles represent measurements of euthermic birds below TNZ. Unfilled circles represent euthermic birds in TNZ. Triangles represent hypothermic birds. The 0.2 0.0 horizontal line represents the mean Vo2 in the thermal 2000 2200 2400 0200 0400 0600 neutral zone. The diagonal line is the regression of TIME

Vo2 of euthermic birds on Ta below the lower critical temperature; the dotted lines enclose the 95% FIG. 4.-Continuous record of instantaneous Vo2 confidence limits. in a Manacus vitellinus showing sharply defined periods of hypothermia. Ta = 23.5-24.5 C. See Discussion for method of predicting Tb during hypothermia. Pipra

40 2 36 36 '034

1.2

1.0

-0.6

. 0.6

co 0.4 Pipra 0.2 Mass, 12.1g.

10 14 18 22 26 30 34 38 0.0 . 2000 2400 0400

AMBIENT TEMP. (C) TIME

FIG. 3.-The relation of rates of oxygen FIG. 5.-Simultaneous records of instantaneous Vo, consumption to ambient temperature in Pipra and Tb in a Pipra mentalis showing moderate nocturnal mentalis. Symbols and lines as in fig. 2. hypothermia. Ta = 22.5-24.0 C.

This content downloaded from 129.186.176.217 on Mon, 23 May 2016 21:08:30 UTC All use subject to http://about.jstor.org/terms 374 G. BARTHOLOMEW, C. VLECK, AND T. BUCHER fluttered to the ground, maintained a nor- Short-term fluctuations in body mass are mal posture, and attempted to avoid cap- related to the high water content of the ture. fruit that manakins eat and to the rapidity During arousal, Vo, sometimes showed with which they move food through the a substantial overshoot, particularly if gut (passage time, approximately 18 min; arousal was rapid (fig. 4). This overshoot Worthington 1982). Long-term decreases appeared to be associated with activity and/ in body mass, however, presumably are or unusually intense shivering. If the re- associated with loss of fat and, hence, a turn to euthermy was gradual, no over- decrease in total stores of available chem- shoot occurred (fig. 5). ical potential energy. Body mass, fasting, and nocturnal hy- Every midnight when we weighed the pothermia.-When deprived of food, manakins and measured Tb, we scored manakins lost body mass rapidly (fig. 6). them as being either hypothermic or eu- thermic on the basis of their behavior. The mean nighttime Tb of individuals (both species) scored as hypothermic (32.4 + 2.8 C, no. = 24) was significantly less (P < .001) than that (37.9 + 0.9 C, no. = 29) of individuals scored as euthermic.

120 Manakins that had been deprived of food for 4-5 h before dusk had a significantly greater drop in nighttime body mass (ex- 0 45 pressed as percentage of mass at time of S 40- capture) than did nonfasted birds. More- over, birds whose mass was substantially i- 35- reduced were significantly more likely to become hypothermic than birds showing

1 2 3 4 5 6 only slight reductions in body mass (table DAYS 2). The mean mass of birds that were hy- FIG. 6.-Characteristic pattern of changes in body pothermic at midnight (80.5 + 6.1% of mass and body temperature in a captive Pipra mass at capture, no. = 24) was signifi- mentalis. The was fasted during the afternoons cantly less (P < .001) than the mass of of days 3, 5, and 6. Continuous line, food available birds that were euthermic at midnight (89.1 ad libitum during daylight; dashed lines, bird not eating because of darkness (nighttime) or being fasted + 6.4% of mass at capture, no. = 29). (daytime). The occurrence of hypothermia in man-

TABLE 2

FREQUENCY OF REDUCED BODY MASS AT MIDNIGHT IN FASTED AND NONFASTED MANAKINS AND FREQUENCY OF OCCURRENCE

OF NIGHTTIME HYPOTHERMIA AND EUTHERMIA IN

MANAKINS WITH REDUCED BODY MASS

BODY MASS (% of capture mass)

<80% 80%-90% >90% G-STATISTICa

Fasted birds ...... 8 12 1 13.98 (P < .001) Nonfasted birds ...... 3 9 13

Hypothermic birds ...... 8 12 1 13.98 (P < .001) Euthermic birds ...... 3 9 13

NOTE.-Ta was between 22 and 27 C. a Sokal and Rohlf 1981.

This content downloaded from 129.186.176.217 on Mon, 23 May 2016 21:08:30 UTC All use subject to http://about.jstor.org/terms MANAKIN ENERGETICS 375 akins is linked to their energy stores, but scribed above requires that Tb remain con- the relationship does not appear to be stant, which is often not the case in obligatory since not all fasted birds, or birds manakins. The C, can also be estimated with reduced mass, became hypothermic from simultaneous measurements of Vo,, (fig. 7). Ambient temperature and energy Tb, and Ta below T,c. The slope of the stores both appear to influence the occur- regression of Vo, on (Tb - Ta) is Ct. rence of hypothermia. Of 21 birds fasted at Ta's between 22 and 27 C, six remained Vo2, = Ct(Tb - Ta). (1) euthermic on the night following fasting. Six other manakins were fasted and then In M. vitellinus the mean value of C, held at Ta's between 14.2 and 16.4 C for calculated using equation (1) for all cases 1-2 h; half remained euthermic. The three where Vo,, Tb, and Ta were measured si- euthermic birds had a mean mass of 87.1% multaneously while Ta < T,, (fig. 8) was + 6.9% of their mass at time of capture. 3.18 cm3 02/(h - C). This value converted The three hypothermic birds had a mean to SI units (17.8 mW/C) is within the 95 % mass of 79.7% + 5.2% of mass at time of confidence interval for the value of C, (ta- capture. In each case the hypothermic birds ble 1) predicted on the basis of mass by had normal body temperatures on the fol- Aschoff (1981). It is also not significantly lowing morning. different from the value for C, (19.9 mW/ Thermal conductance.--The slope of C) calculated as the slope of the relation- regression of Vo2 on Ta below T,c is fre- ship between Vo2 and Ta below T,c in eu- quently used as a measure of total, or wet, thermic birds (fig. 2). In the thermal neutral thermal conductance (C,). In both M. vi- zone, C, (22.4 + 3.17 mW/C, no. = 8) is tellinus and P. mentalis, extrapolation of higher than it is below thermal neutrality. the curves for V02 below thermal neutral- For P. mentalis, C, computed from equa- ity intercept the ambient temperature axis tion (1) as the slope of the relationship be- 1 or 2 C below the euthermic body tem- tween Vo0 and Tb - Ta (2.90 cm3 0,/[h-C]), perature (figs. 2, 3). Consequently the the- or 16.2 16.2 mW/C, is also within the 95% oretical conditions for using this method confidence interval for the value predicted of determining C, are only approximately on the basis of mass (table 1) and is not fulfilled (see McNab [1980] for review). significantly different from the value for However, in both M. vitellinus and P. C, (21.63 mW/C) calculated from the slope mentalis the value of the euthermic body of Vo, on Ta in euthermic birds (fig. 3). temperature (37 C) falls within the 95% The C, in the thermal neutral zone (21.9 confidence interval of the X-axis intercept + 4.52 mW/C, no. = 6) is slightly higher of the regression. than it is below thermal neutrality. Thermal conductance calculated as de- Below T, thermal conductances of hy-

100 Manacus 40

36 -

6020 70 80 900 100 08 2 16 24 % FIELD-CAUGHT MASS BODY TEMP -AMBIENT TEMP. (C) FIG. 7.-Tb as a function of body mass at midnight FIG. 8.-Regression of Vo, on (Tb - Ta) at ambient expressed as percentage of field-caught mass in Pipra temperatures below TNZ in M. vitellinus. Unfilled and Manacus (Ta, 22-27 C). Unfilled circles are circles are hypothermic birds. Filled circles are hypothermic birds (Tb < 36 C). Filled circles are euthermic birds. Slope of regression, cm3 O,/(h-[Tb - euthermic birds. Ta]), is thermal conductance.

This content downloaded from 129.186.176.217 on Mon, 23 May 2016 21:08:30 UTC All use subject to http://about.jstor.org/terms 376 G. BARTHOLOMEW, C. VLECK, AND T. BUCHER pothermic and of euthermic manakins of one female Nectarenia mediocris experi- both species are statistically indistinguish- enced a drop of 17.5 C from its daytime able. For example, in three M. vitellinus body temperature of 41 C (Cheke 1971). with a mean Tb of 30.7 + 4.7, C, = 17.2 At a Tb of 24 C this bird did not respond + 4.03 mW/C (calculated as the mean of at all to handling. Nocturnal hypothermia individual measures of Vo,/[Tb - T]). In of 5-10 C has also been reported in swal- seven euthermic birds, mean C, = 18.4 + lows (Hirundo, Delichon, and Riparia) ex- 2.9 mW/C. The data from both euthermic posed to very low temperatures (Kespiak and hypothermic birds were combined to and Lyuleeva 1968). estimate C, for each species (table 1). The best-documented cases of avian hy- pothermia occur at low ambient temper- DISCUSSION atures. In birds such as Temperate Zone In Manacus and Pipra, as in other small or montane hummingbirds and swifts that heterothermic birds, the characterization become torpid, Tb often declines to within of BMR is difficult. Even in the thermal 1 C of Ta, even when the latter is 10 C or neutral zone of these manakins there is no lower. In our experiments manakins be- sharply defined minimum level of energy come hypothermic at relatively moderate metabolism. Moreover, there is no clearly ambient temperatures, even at tempera- defined level of resting body temperature tures within the TNZ. Moreover, the Tb over a range of Ta's extending at least from of hypothermic manakins remained from 14 to 31 C. The physiological response of 4 to 20 C above Ta and never fell below these manakins to decreases in Ta below 25 C. Even such limited hypothermia can thermal neutrality can simultaneously in- result in substantial energy saving (see be- volve an increase in Vo2, a minimization low). Nocturnal hypothermia has been re- of thermal conductance, and a decline in ported in two other birds of the tropics. body temperature. Mousebirds, Colius striatus (Bartholomew and Trost 1970), and smooth-billed anis, HYPOTHERMIA Crotophaga ani (Warren 1960), became hy- Daily or seasonal hypothermia as a pothermic at Ta between 19 and 25 C and mechanism for energy conservation has spontaneously warmed up the following been less thoroughly studied among birds morning. In both cases the birds were on than among mammals, but the occurrence moderately restricted food rations. of daily (or nightly) hypothermia accom- At least two physiological models could panied by torpor (a state characterized by account for the pattern of hypothermia dormancy, Vo, reduced to 10% of BMR found in manakins: (1) they could increase or less, Tb close to Ta, and apnea) has been thermal conductance at night, allowing Tb documented by physiological measure- to fall and allowing-the Q,, effect of low- ments in hummingbirds, swifts, capri- ered Tb to depress the rate of energy me- mulgids, colies, and sunbirds (see tabolism, or (2) they could hold thermal Bartholomew [1972, 1981] and Hains- conductance at or near its minimal level worth and Wolf [1978] for reviews of het- while reducing the rate of energy metab- erothermy and energy conservation). olism and allowing Tb to fall to a level Body temperature drops by 1-2 C at determined by the reduced level of heat night in all passerines that have been ex- production. amined, and with prolonged fasting or un- A combination of the two mechanisms der laboratory conditions of reduced food would be especially frugal energetically. availability, body temperature may drop 3 During entry into torpor, a combination of or 4 C (see, e.g., Biebach 1977). Nocturnal temperature-independent reduction of me- hypothermia of 5 C has been found during tabolism and increased thermal conduc- winter in the Paridae (Chaplin 1976). An tance would assure rapid development of even more marked hypothermia accom- hypothermia. Whereas, during hypother- panied by at least partial torpor has been mia and resumption of euthermia, mini- reported in several species of sunbirds ex- mal thermal conductance would allow the posed to temperatures between 0 and 10 lowest possible rate of metabolism for C; the usual decline in Tb was 5-12 C, but maintenance of any given difference be-

This content downloaded from 129.186.176.217 on Mon, 23 May 2016 21:08:30 UTC All use subject to http://about.jstor.org/terms MANAKIN ENERGETICS 377 tween Tb and Ta. Our data are consistent ing a bout of hypothermia can be com- with the hypothesis that manakins in- puted by dividing the energy saved by the crease thermal conductance during entry amount of energy that would have been into hypothermia and that they vary ther- consumed by the bird had it remained eu- mal conductance during periods of shallow thermic at the same Ta. The latter quantity hypothermia of the sort shown in figure 4. can be determined from the regression of However, when hypothermia is more fully Vo, on Ta (figs. 2, 3). The energy savings developed, C, below T,, is at or near its during a time interval different from the minimum level. We do not know whether period of hypothermy (e.g., during an en- or not C, remains above minimum levels tire 24-h period) can be calculated by di- when the birds are hypothermic at ambient viding the energy saved during the bout temperatures within the TNZ. of hypothermy by the energy that would have been consumed during euthermy over ENERGY SAVINGS the entire time interval being considered. So far, marked hypothermia in passer- If Ta is constant, which is substantially true ines other than manakins has been re- at night in a tropical forest, the nocturnal ported only at low ambient temperatures. metabolic savings that a hypothermic In both M. vitellinus and P. mentalis hy- manakin with constant and minimal ther- pothermia regularly occurs at ambient mal conductance will realize is directly temperatures that are only 3 or 4 C below proportional to Tb. thermal neutrality. The populations of Our model is conservative. It calculates manakins on Barro Colorado Island rarely the difference between the energy spent are exposed to air temperatures below 20 during a period of hypothermia at a given C, and the lowest temperature ever re- AT and a period of euthermia of the same corded in the forested part of the island is duration. It ignores any energy savings that 14 C (Croat 1979). may accrue during entry into hypothermia By using the values of Ct, it is possible as a consequence of Vo, being below the to calculate Tb during nocturnal reduction euthermic level. It also ignores the fact in Vo2 in those cases where it was not mea- that during much of warm-up, Vo2 is be- sured: low the euthermic level. Even if there is an overshoot in Vo2, as sometimes occurs Tb = T+ VO2/C , (2) when warm-up is rapid, the total energy spent during entry and warm-up is less where Vo2 is cm3 O,/h and C, is cm3 02/ than would be spent during the same time (h C). if the bird remained euthermic (see Tucker Hypothermia is defined in terms of a [1965] for a similar analysis for a rodent). drop in body temperature. However, the Despite the warm environment in which significance of nocturnal hypothermia lies they live, manakins achieve a substantial in the energy savings to the animal. The savings from nocturnal hypothermia. For absolute savings in energy expenditure af- example, during a 12-h night, a 14-g M. forded by the moderate nocturnal hypo- thermia of manakins can be estimated from vitellinus spending 10 h with a body tem- their minimal thermal conductance and the perature of 27 C would expend about 6.4 kJ less than if it kept body temperature at magnitude and duration of hypothermia at 37 C. An energy savings of 6.4 kJ is equal a given Ta. The amount of energy saved is to 58% of its nocturnal euthermic energy the difference between the Vo2 of the eu- expenditure at a Ta of 22 C. Hypothermia thermic bird and the Vo2 of the hypo- of only 2 C for 6 h would yield a savings thermic bird. Therefore, of 0.8 kJ, or about 7% of the energy it energy saved = CATb, t , (3) would have expended had it remained eu- thermic for a 12-h night (fig. 9). where energy saved is kJ (1 J/s = 1 W), C, is kW/C, ATb is the difference between ENERGY RESOURCES AND NOCTURNAL euthermic Tb (= 37 C) and hypothermic Tb, HYPOTHERMIA and t is the duration of hypothermia in The ability of manakins to reduce daily seconds. The relative energy savings dur- energy consumption by means of limited

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70 such birds do not necessarily become hy- pothermic overnight. Moreover, even when 7- Manacus -60 o food is provided ad libitum and manakins mass, 14g E can feed until sunset, some individuals be- 6 To= 22 C come moderately hypothermic at night, -502 with Tb as low as 35 C. From our data we .-1o5-- infer that manakins can integrate infor- V40 < mation about (1) physiological energy stores, (2) nocturnal Ta, and (3) other fac- )30 0 tors such as anticipated foraging success, b 3 - to estimate both future energy demands (I) z -20 and available energy resources. From this 2O integration, they fix the extent and dura- 10 tion of nocturnal hypothermia necessary 1 1cr for them to remain in energy balance. A z somewhat analogous proportional control

0 O2 4 6 80o 10 12 system has been proposed recently for the daily energy regulation of some humming- HOURS OF NOCTURNAL HYPOTHERMIA birds (Hainsworth, Tardiff, and Wolf 1981). FIG. 9.-Energy savings associated with nocturnal The behavioral responsiveness of man- hypothermia in a manakin. In this model, if Tb is 10 C less than euthermic Tb, hypothermia = 10 C. See akins during their episodes of shallow noc- Discussion for method of computing energy savings. turnal hypothermia contrasts sharply with the inertness of sunbirds, hummingbirds, nocturnal hypothermia provides a way to and caprimulgids during their periods of match metabolic energy expenditure to food hypothermia, in which Tb is much lower. resources. For much of the year fruit is Manakins respond to disturbance by abundant (and easily located), and man- warming up rapidly. Even before they akins spend little time foraging; an adult warm up and when Tb may be as low as male may spend only about an hour a day 26 C, they attempt to escape by fluttering feeding (Snow 1962a, 1962b; Foster 1977). away. The absolute energy savings that However, at least on Barro Colorado Is- manakins obtain from nocturnal hypo- land, late in the rainy season from August thermia is not as great as it would be if through December, they may face an en- their Tb were lower. Nevertheless, they ac- ergy shortage because fruit availability is crue substantial energy savings without limited and the time available for foraging having to give up the possibility of rapid is often restricted by heavy afternoon rains. arousal or losing their ability to attempt to Under these circumstances, manakins escape from predators. could have difficulty meeting energy needs We have demonstrated that manakins in on a day-to-day basis if they did not resort the laboratory have the physiological ca- to nocturnal hypothermia (Worthington pacity to lower energy expenditure sub- 1983). Thus, despite the warm and equa- stantially by means of hypothermia. We ble environment in which they live, the have no data concerning the extent and adaptive advantage of hypothermia to duration of hypothermia used by free-living manakins is the same as that of the daily manakins, but the adaptive significance of and seasonal torpor that has been well doc- hypothermia as a means of remaining in umented in birds and mammals that live energy balance during periods of food in areas characterized by seasonal drought shortage is obvious. The selection pres- or low temperatures. sures that have favored the evolution of Under laboratory conditions, the hy- limited nocturnal hypothermia are pre- pothermia of manakins is correlated with sumably not unique to manakins, and we afternoon fasting, reduced body mass, and predict that the major components of the relatively low Ta. Body temperatures of 30 pattern of metabolic response which they C or less are most likely to occur in birds exemplify will be found in other small whose body mass is at least 20% less than tropical passerines that must contend with it was at the time of capture. However, periods of reduced energy availability.

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LITERATURE CITED

ASCHOFF, J. 1981. Thermal conductance in mam- HAINSWORTH, F. R., M. F. TARDIFF, and L. L. mals and birds: its dependence on body size and WOLF. 1981. Proportional control of daily energy circadian phase. Comp. Biochem. Physiol. regulation in hummingbirds. Physiol. Zool. 69A:611-619. 54:452-462. ASCHOFF, J., and H. POHL. 1970. Der Ruheumsatz HAINSWORTH, F. R., and L. L. WOLF. 1978. The von Vogeln als Funktion der Tagezeit und der economics of temperature and torpor in non- Korpergrosse. J. Ornithol. 111:38-47. mammalian organisms. Pages 147-184 in L. WANG BARTHOLOMEW, G. A. 1972. Aspects of timing and and J. W. HUDSON, eds. Strategies in cold. Ac- periodicity of heterothermy. Pages 663-680 in F. E. ademic Press, New York. SOUTH, J. P. HANNON, J. R. WILLIS, E. T. PEN- KESPIAK, J., and D. LYULEEVA. 1968. Reguirue- GELLEY, and N. R. ALPERT, eds. Hibernation maya gipotermiya u ptits semeistva lastochek. and hypothermia, perspectives and challenges. Commun. Baltic Comm. Bird Migration 5:122- Elsevier, New York. 142. 1981. A matter of size: an examination of LASIEWSKI, R. C., W. W. WEATHERS, and M. H. endothermy in and terrestrial vertebrates. BERNSTEIN. 1967. Physiological responses of the Pages 46-78 in B. HEINRICH, ed. ther- giant hummingbird, Patagona gigas. Comp. moregulation. Wiley, New York. Biochem. Physiol. 23:797-813. BARTHOLOMEW, G. A., and C. H. TROST. 1970. McNAB, B. K. 1980. On estimating thermal con- Temperature regulation in the speckled mouse- ductance in endotherms. Physiol. Zool. 53:145- bird, Colius striatus. Condor 72:141-146. 156. BARTHOLOMEW, G. A., D. VLECK, and C. M. SNOW, D. W. 1962a. A field study of the black and VLECK. 1981. Instantaneous measurements of ox- white manakin, Manacus manacus, in Trinidad, ygen consumption during pre-flight warm-up and West Indies. Zoologica 47:65-104. post-flight cooling in sphingid and saturniid moths. . 1962b. A field study of the golden-headed J. Exp. Biol. 90:17-32. manakin, Pipra erythrocephala, in Trinidad, West BIEBACH, H. 1977. Reduktion des Energiestoff- Indies. Zoologica 47:183-198. wechsels und der Korpertemperatur hungernder SOKAL, R. R., and F. J. ROHLF. 1981. Biometry. 2d Amseln (Turdus merula). J. Ornithol. 118:294- ed. W. H. Freeman, San Francisco. 300. TUCKER, V. A. 1965. The relation between the torpor BUCHER, T. L., and A. WORTHINGTON. 1982. Noc- cycle and heat exchange in the California pocket turnal hypothermia and oxygen consumption in mouse, Perognathus californicus. J. Cell. Comp. manakins. Condor 84:327-331. Physiol. 65:405-414. CHAPLIN, S. B. 1976. The physiology of hypothermia VLECK, C. M., and D. VLECK. 1979. Metabolic rate in the black-capped chickadee, Parus atricapillus. in five tropical bird species. Condor 81:89-91. J. Comp. Physiol. 112:335-344. WARREN, J. W. 1960. Temperature fluctuation in the CHEKE, R. A. 1971. Temperature rhythms in African smooth-billed ani. Condor 62:293-294. montane birds. Ibis 113:500-506. WORTHINGTON, A. 1983. Population sizes and CROAT, T. B. 1979. Flora of Barro Colorado Island, breeding rhythms of two species of manakins in Panama. Stanford University Press, Stanford, relation to food supply. In E. G. LEIGH, JR., D. Calif. WINDSOR, and A. S. RAND, eds. The ecology of FOSTER, M. S. 1977. Ecological and nutritional ef- a neotropical forest: seasonal rhythms and longer- fects of food scarcity on a tropical frugivorous bird term changes. Smithsonian Institution, Washing- and its fruit source. Ecology 58:73-85. ton, D.C.

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