ecological energetics of wintering merlins falco columbariusiwarkent/ecological energetics of...

Ecological Energetics of Wintering Merlins Falco columbarius

Ian G. Warkentin'** Nigel H. West2 'Department OF Biology and 2 ~ e p a r t m e n t of Physiology, University of Saskatchewan, Saskatoon, Saskatchewan, S7N OW0 Canada

Abstract The ability to maintain a balanced energ), budget through extendedperiods of thermal stress isa major determinant in the survival of birds resident in the north temperate zone during winter. We developed a time-energy budget for winter-acclimated merlins ( Falco columbarius) to examine the relationship between energy expenditure and temperature, wind, and radiation and to learn how merlins cope with winter on a physiological and behavioral basis. Nine free-living birds were radio tagged and their activities monitored to establish an activity budget for the winterperiod (November I to February 28). The data were combined with thermo- regulator~~ and activity costs of nine other merlins measured in an open-circuit respirometer. Basal metabolic rate was higher in females ( 6 9 6 k J . h-') than males (5.23 k/. h-') and both were more than 50% above levelspredicted from their mass. Lower critical temperatures were 3.4" and 14.3" C forfemales and males, respectiveIy, and thermal conductance in males (0.267m W . [ g . " C]-') wasabout 7% lower than predicted from mass, while for females (0.245 m W . [ g . " q - ' ) it was within 1% of thepredicted value. The allocation of time in the activity budget was based on minimizing foraging activity and energy expenditure, rather than maximizing energy intake. Physiological adaptation shown by merlinssuggests that biotic rather than phjaiological factorspreviously limited merlin abundance on the northern Great Plains in winter.

Introduction

The ability to maintain a balanced energy budget during periods when re- sources are limiting and/or costs are high is a major determinant of an ani-

* Present address: Department of Veterinary Anatomy, University of Saskatchewan, Saskatoon, Saskatchewan, S7N OW0 Canada.

PhysiologicalZoology63(2):308-333. 1990. O 1990 by The University of Chicago. All rights reserved. 0031-935X/90/6302-88157$02.00

Merlin Energetics 309

mal's survival. In the north temperate zone, with its seasonally severe climate, winter residents may face constraints in the form of reduced food and foraging time, thermal stress, or a combination of these. Maximum sustain- able rates of energy expenditure that suggest limiting physiological capaci- ties for energy processing have been hypothesized for birds (Kirkwood 1983). In light of such constraints, modification of behavior patterns during energetically stressful periods may also have a substantial impact on survival. Through the analysis of energy expenditure in free-living birds, it is possible to assess the impact of a variable environment on their energy balance and to examine the physiological and behavioral tactics birds use to minimize the effects of the constraints that they face.

Work on the energetics of wintering raptors is restricted to a few studies. Koplin et al. (1980) developed a deterministic model to predict energy expenditures for wintering American kestrels (Falco sparverius) and the white-tailed kite ( Elanus leucurus). Hayes and Gessaman ( 1980) studied metabolic responses of American kestrels, red-tailed hawks (Buteo jamai- censis), and golden eagles (Aquila chrysaetos) under varying temperature, wind, and radiation regimes. Stalmaster and Gessaman ( 1984) investigated the winter energy requirements of bald eagles (Haliaeetus leucocephalus) in relation to their management. Masman, Daan, and Belduis (1988a) considered the life-history strategies of European kestrels (Falco tinnunculus) in a study of their annual pattern of daily energy expenditure.

We examined the energy expenditure of winter-acclimated merlins ( Falco columbarius) to learn more about the relationship of these expenditures to temperature, wind, and radiation. No previous study has examined the standard respiratory gas-exchange parameters of merlins, and few have considered the energetics of birds at the northern edge of their winter distribution. In addition, we developed a time budget for wintering merlins. This budget was integrated with estimates of activity costs to develop a time- energy budget (TEB). Through the TEB we investigated how merlins cope with winter on a physiological and behavioral basis, and how these compen- satory mechanisms relate to time and energy allocation. The merlin is a small, bird-eating falcon of panboreal distribution. Primarily a migratory species, it breeds in open tracts of land with low or scattered vegetation in temperate and boreal regions of the Northern Hemisphere and moves to more southerly latitudes for the winter. The subspecies of the North Ameri- can prairies ( F . c. richardsonii), on which this study was based, has recently undergone a northward expansion of its wintering range to include many of the towns and cities in the northern Great Plains region where it breeds (James et al. 1987).

310 I. G. Warkentin and N. H. West

Material and Methods

Time Budget

Fieldwork was conducted in Saskatoon, Saskatchewan, Canada (52"07' N, 106" 38'W). The city has a population of about 185,000 people and covers approximately 12,200 ha. Merlins sighted along an 80-km survey route through Saskatoon were trapped with a modified dho-gaza net (Clark 1981 ), with two tethered house sparrows (Passer domesticus) used as lures. Se- lected individuals were fitted with single-stage radio transmitters (AVM model SM-I ). The birds were released and their activities monitored continuously by maintaining visual contact as they moved about their home range. Data for nine merlins (six females and three males), followed between No- vember 1 and February 28,1983-1988, were included in this analysis. Obser- vations were made from the time the birds left the roost at dawn until their return at dusk. Monitoring continued until the transmitter failed, from 3 d to 7 wk later. The amount of time birds spent in each of the following behavioral categories was recorded: (1 ) rest perch (nighttime), (2 ) alert perch (daytime), ( 3 ) body care (preening), (4 ) eating, and (5 ) flight. We assumed that daytime activity patterns recorded during observations were representative of the merlin's overall time budget. All nocturnal activities were presumed to be roosting (rest perch). Rest-perch values were determined from actual departure and entry times at the roost or estimated from the relationship of roosting times to the number of days from the winter solstice (Warkentin 1986). The value for time spent in flight was estimated from the distance traveled. In order to make these estimates, we plotted the locations recorded for each bird on a 1:50,000 topographical map of Saskatoon and, assuming straight-line flight at 50 km - h-' (from observations during telemetry), assigned a duration to each displacement.

Gas-Exchange Measurements

Nine merlins (five males and four females), of which one male was also used for radio tracking, were used in the metabolic portion of this study. Work was conducted from November 1 to March 31,1986-1988. Birds were housed individually in outdoor pens (2.4 X 1.2 X 2.1 m) , sheltered from the wind but exposed to ambient photoperiod and temperature. They were fed house sparrows or Japanese quail (Coturnix japonicus) twice daily (approximately 80 g whole-carcass wt ) , except on test days, when they were limited to one feeding (approximately 40 g) . All remaining food was re-

Merlin Energetics 31 1

moved at 1100 hours on test days to ensure that birds were at least 8-10 h postabsorptive during metabolic measurements.

Measurements of gas exchange were conducted in a 12-L cylindrical Plexi- glas metabolic chamber. A wooden dowel raised above the floor of the chamber enabled the bird to perch naturally without coming in contact with the chamber walls. Air temperature in the chamber was measured with a mercury thermometer (accurate to 1 " C) inserted through a rubber stopper in the lid. The metabolic chamber was housed in a walk-in environmental room capable of maintaining temperatures to *lo C of the desired setting.

Ambient air was drawn into the metabolism chamber from the environmental room through an inlet port in the bottom, past the bird, and through the outlet port, and successively through a 12-cm column of no. 8-mesh Drierite desiccator, out of the environmental room through a flowmeter, and past a four-way connector to the vacuum pump set to maintain constant flows of 2.0 L . min-I. At the four-way connector, air was continuously drawn off in parallel via 5-cm columns of Drierite to a Beckman OM-11 0, analyzer and a Beckman LB-2 CO, analyzer. All volumes were corrected to STPD. Be- cause of the small change in the percentage of CO, with a flow rate of 2.0 L . min-', it was not possible to accurately measure C 0 2 levels. Therefore, the values of VCO, obtained during estimates of respiratory quotient (RQ) made at a flow rate oi'0.5 L . min-' were used. These values were then used in equation (3b) of Withers ( 1977) to calculate v o 2 . From the simultaneous recordings of Vco, and VO,, a mean RQ of 0.75 (SE = k0.005, n = 7 ) was obtained. Rates of metabolic heat production, H,, were calculated, therefore, by assuming that 19.78 kJ of heat was produced per liter of 0, consumed. Evaporative water loss was determined gravimetrically (all desiccator columns being weighed before and after each test). Rates of evaporative heat loss (Ef . H,, where Ef is the fraction of metabolic heat lost evaporatively) were calculated by assuming that 2.43 J of heat was required to liberate 1 mg of water. Gas analyzers were calibrated before each test with primary gas standards of 18.00% 02, 2.00% CO,, and 80.00% N, in the first year and 19.00% O,, 2.00% CO,, and 79.00% N, in the second. Values were recorded on a Cole-Parmer multichannel paper chart recorder.

Birds were allowed to acclimatize to captivity for a minimum of 2 d before tests were initiated. All recordings were made on birds held in complete darkness during the normal rest phase of the daily cycle. An individual was transported from the holding pen to the metabolism chamber at dusk on the day of the tests. On the first night, metabolic rate at +20°C was recorded (flow rate = 2.0 L - min-I), and then an R Q measurement made (flow rate = 0.5 L min-I). After 1.5 h acclimatization, recordings were taken for 0.5

31 2 I. G. Warkentin and N. H. West

h with the lowest 0, consumption maintained for at least 3 min taken as the value for that particular temperature. Estimates of RQ were then made by recording instantaneous values of VO, and ~ c o , at 5-min intervals for 1 h and averaging all values to obtain an overall RQ. Subsequent tests were made every second night, with values for two different temperatures recorded each night: +15" and +1O0C, +5" and O0C, -5" and -lO°C, and -15" and -20" C. In each case, the bird was exposed to the higher temperature first to allow for the potential influence of higher metabolic rates associated with lower temperatures (Pohl 1969). We took measurements for the second temperature beginning 1.5 h after the temperature in the environmental room was adjusted to the lower level (allowing 0.5 h to bring the ambient temperature down 5" C and 1 h for the bird to acclimatize to the new temperature). Birds were weighed ( f 0 . 5 g ) on an electronic balance before and after each night's tests, with the mean of the two measurements used in all further calculations. The bird's cloaca1 temperature was determined (k0 .1 "C; Schultheis Hg thermometer) after all metabolic measurements were completed each night. The entire procedure took a total of 9 d.

Between the fourth and fifth test runs, a separate daytime test was conducted during the daylight phase of the daily cycle to assess the costs of various activities. For 4 h beginning at 0830 hours, birds were placed in the metabolism chamber with prey; the lights of the environmental chamber (fluorescent and incandescent) were turned on, and the ambient temperature was set at +15 "C (in the thermoneutral zone [TNZ] for both males and females). The i.'02 was recorded as previously described, and the bird was observed either from behind a blind inside the environmental chamber or with a video camera. The VO, associated with sustained bouts of activity (>2 min) such as alert perch, feeding, and body care were noted. With an effective chamber space of 10 Land a flow rate of 2.0 L . min-', air turnover was 95% in 15.0 min, 99% in 23.0 min, and 99.8% in 31.1 min. Therefore, energy costs of activity bouts that lasted less than 31 min were calculated by the technique of Bartholomew, Vleck, and Vleck ( 1981 ). Estimates of flight costs were made according to equation (6) of Masman and Klaassen (1987). Based on energy expenditure estimates for free-flying birds of 22 species, this equation explains 84% of the variation in flight costs when related to body mass, wing span, and wing area.

Weather Conditions and the Roost Microclimate

Data, collected on an hourly basis by Environment Canada (Saskatoon Airport) and the Atmospheric Processes Program (Saskatchewan Research


Council, Saskatoon), were used to characterize the weather conditions experienced by merlins during winter.

The microclimate of four roosts actively used by three merlins was monitored in February and March 1988. Variables considered were temperature, wind speed, and the fraction of the upper hemisphere of the roost perch covered by vegetation. Thermocouples were used to monitor temperatures at the roost perch and at the same height immediately outside of the roost tree. Measurements were taken at hourly intervals from 1800 to 0600 hours with an Atkens digital thermometer (model 4900-T) on five nights with differing cloud cover and wind conditions. Rimco three-cup anemometers were used to measure wind speeds outside the roost on the windward and leeward sides of the tree at roost-perch height. At the perch itself, wind speeds were mer~sured with a TSI hot-wire anemometer (model 1650).

Wind speed was recorded for a total of 4 h at each roost in 1- or 2-h sessions to obtain values from near 0 to 7 m . s-l, a range typically encountered on winter nights. Readouts from the three-cup anemometers were taken every 5 min, as were instantaneous values from the hot-wire anemometer at the roost perch. The amount of vegetation cover and, indirectly, radiative expo- sure at the roost perch was assessed by analyzing hemispherical photographs taken at each perch with the camera axis placed vertically and hori- zontally. The amount of cover was determined by methods similar to those of Walsberg and King ( 1978a).

Composition a n d Energy Content ofprey Items

House sparrows and Bohemian waxwings (Bombycilla garrulus) caught in the field from November through January, and Japanese quail obtained from a captive-reared population, were analyzed to determine body composition with respect to water, fat, and protein content, as well as gross energy value. Before analysis, the bill, tarsi and feet, wings, rectrices, and most body feathers were removed. These parts are generally not eaten by merlins ( I . G. Warkentin, personal observation). Processed carcasses were then weighed, freeze-dried, reweighed to determine water loss, and then ground in a ham- mer mill for chemical analysis. Extraction overnight with anhydrous diethyl ether yielded the crude fat content, and the Kjeldahl method was used to determine protein content. Ash values were ascertained by heating a 2-g sample of the freeze-dried material at 600" C for 2 h and determining mass loss. The caloric values of the samples were obtained in single or double determinations with a Parr oxygen bomb calorimeter. Assimilation quotients were taken from other studies of raptors which have shown close


agreement on quotients of 0.67 for mammalian and 0.75 for avian prey of several species (Wijnandts 1984; Masman et al. 1986).

Time-Energy Budget Analysis

In the annual cycle of a bird, energy is required for maintenance, molt, re- production, physical activities, and thermoregulation. However, since this study encompassed only birds that were not migrating or preparing to mi- grate, at times well outside regular reproductive and molting periods, all types of tissue synthesis (body mass, eggs, and feathers) were ignored in our determination of the daily energy expenditure ( t jTD) . Following Weath- ers et al. (1984):

where t is the portion of the 24-h dayspent in activity, the subscripts indicate the type of activity (RP = rest perch, AP = alert perch in field conditions, E

= eating, BC = body care, F = flight, and API = alert perch measured in the lab at thermoneutral temperatures), and d is the energetic expenditure rate for each activity. The first term in the equation after the equal sign represents the combined basal and thermoregulatory requirements of merlins through the night under field conditions; the second term represents the basal and thermoregulatory costs of merlins perched during the active phase of the daily cycle under field conditions. The final term brings together the costs of activities above and beyond that necessary for simple alert perching in the thermoneutral zone. This is a simplification because it does not take into account the heat produced by extended or intense levels of activity, such as flight, which may substitute for normal thermoregulatory costs. However, owing to the limited amount of time merlins spend in flight, we assumed that this substitution does not occur in the model.

The model is based on an electrical analog of heat-transfer theory in which the properties of the animal are integrated with the radiative and convective characteristics of the environment through the use of heat-transfer resist- ances ( r ) , rather than conductances, to establish the route and magnitude of heat loss (Robinson, Campbell, and King 1976). When the operative temperature ( Te) was above the lower critical temperature ( Ti,), I&, was assumed equal to the basal metabolic rate ( Hr,) regardless of wind speed. In the more common condition for this study, when Te < T,,, IjRp and kP were


calculated to include the variation due to changes in both wind speed and temperature through the equation

where H, is metabolic heat production expressed in W m-', with H,,, con- verted to these units on the basis of surface area calculated from the equation of Walsberg and King (19786). Since Ef is the fraction of metabolic heat production lost evaporatively, Ef . H, is the latent heat loss. The volumetric heat capacity of air, pc,, is a constant (1,200 J . m-3 . " C-I) , while Tb is the body temperature, and Te is the operative temperature of the merlin's environment. Total resistance is represented by 6 .

For tests in the metabolic chamber, with wall temperature within l o C of air temperature ( T , ) and its thermal emissivity greater than 0.9, T, = T, (Robinson et al. 1976). Otherwise, T, for field conditions was calculated as

where Kbs is the absorbed environmental long-wave radiation. Since nighttime roost positions were almost completely sheltered overhead, shortwave radiation was assumed to be making a negligible contribution to nighttime energetic requirements. However, during daylight hours, hourly values of global radiation (measured with an Epply pyranometer) were used to determine radiation levels for the active phase. The Merlin's thermal emissivity, E, is 0.98 (Hammel 1956), and o is the Stefan-Boltzman constant (5.67 X lop8 W mP2 . " K - ~ ) . Total resistance ( r,) is composed of the animal's whole-body thermal resistance ( rb) and the parallel equivalent resistance ( r,), both measured in s . m-I, such that

T, is the surface temperature of the plumage as estimated from T, = 12.5 + 0.7 T, (Veghte and Herreid 1965). The characteristic dimension, d, is the diameter of the bird's body at the widest point (females: 0.081 f 0.001 m, n = 11; males: 0.073 + 0.004 m, n = 11 ). Under conditions of low wind speeds the constant for turbulent airflow (k ) is 307. To account for the increased wind turbulence under field conditions and the associated decreased resistance (Nobel 1974 ), a 20% decrease in the constant over that found for lami- nar flow was assumed; thus, k = 246. Air speed (p) was 0.006 m . s-' at the center of the metabolic chamber. Field calculations were based on wind-

31 6 1. G. Warkentin and N. H. West

speed values obtained from the Environment Canada weather office in Sas- katoon, which were adjusted to account for perch positions (see Results). The re is composed of the apparent radiative resistance (r,) and parallel resistance to convective heat flow (r,), which includes both free (rfr) and forced ( rfo) components. Thus,

and

with

and

so that

To extrapolate from chamber to field conditions, r,'s were recalculated to account for the effects of wind. Robinson et al. (1976) found a 10%-15% reduction in r, for every unit increase in p0.5. Therefore, to calculate r, under field conditions,

Thus, rb (field whole-body thermal resistance), along with re (calculated from field conditions), forms r,, which is combined with T, and T, in equation ( 2 ) to determine the net metabolic heat production (H, - Ef . H,). This value was used in the calculation of &, and H,,:

EjAp (or t jRP) = (.Fj, - E ~ . ~,,,)[l/(l - E ~ ) ] . (11)

While it is generally assumed in time-budget analysis that birds carry out roughly the same daily behavior patterns when observed as when not observed, this does not necessarily hold true on an hourly basis for birds of prey. Because meals tend to consist of large quantities of high-energy food consumed over relatively short periods (when compared with many other birds, which spend a large portion of their day eating many smaller meals), missing these feeding periods during observations can have a dramatic im-


pact on the energy-intake values assigned a given bird. The average meal of a wintering merlin lasted about 0.5 h, with a distended crop resulting from the meal distinguishable for at least 0.75 h. We therefore considered a day with ( 1 ) visual contact for at least 70% of the active phase, and ( 2 ) gaps in observations no longer than 1 h, to be a "complete day" (following Masman, Daan, and Dijkstra 19886) in which we had a representative sample of the behavior patterns and confidence that all meals had been recorded. The result was a total of 38 complete days available for analysis. We compared daily energy budget values obtained from the TEB model, derived from actual activity budgets and weather conditions of the complete days, with those values based on observations of food intake during complete days. In addition, we used the model of energetics developed above, in conjunction with the overall merlin activity budget and the mean monthly weather conditions for Saskatoon, to determine monthly and seasonal energy budgets for male and female merlins wintering in Saskatoon.

Statistical Analyses

All values reported are mean -+ SE, unless otherwise noted. Changes in metabolic rate as a function of T, were analyzed by least-squares regression analysis. This compared equations for all combinations of points to form the sloped and flat portions of the model. The set with the smallest total sum of squares was selected. Slopes of the regressions were compared by Student's t-test. Differences between males and females in E,, H,: and energetic costs for each activity category were compared by Hotelling's T2 test (Morrison 1967). Use of this test overcame the problem of dependent data created by making multiple observations of individual merlins. Differences between temperatures inside and outside the roost were compared by paired t-

test, while wind speeds were analyzed by ANOVA and Duncan's multiple range test.

Time Budget

The time-budget data, based on 542 h of direct observation, are summarized in table 1. Day length varied from roughly 7.7 h at the winter solstice to 10.7 h at the end of February. However, the active phase of the daily cycle extended beyond these times according to the relationship established by Warkentin (1986) for merlins wintering in Saskatoon. Merlins stopped their

318 1. G. Warkentin and N. H. West

TABLE 1 Daily time budget of wintering merlins divided into the percentage time spent in each activity for both the 24-h day and for the active phase of the daily cycle

Rest Alert Body Perch Perch Eating Care Flight

Females (N = 6 ) : Percentage of 24-

h day . . . . . . . .

Percentage of active phase

Males ( N = 3 ) : Percentage of 24-

h day . . . . . . . .

Percentage of active phase

Note. Values are means. The range of values is reported below each mean.

activities and entered the roost at roughly the same time relative to sunset through the winter (approximately 20 min after sunset), but departure from the roost in the morning ranged from nearly 40 min before sunrise at the winter solstice to 4 min before by the end of February. Thus, the length of the active day ranged from 8.7 h in December to 11 h in February.

Gas-Exchange Measurements

There was a difference between male and female merlins in several metabolic parameters. Whereas the TNZ of females extended from 3.4 " to at least 20°C, that for males was much more restricted, with a 7 , of 14.3"C. Figure 1A and 1 B represents the rest-phase metabolic heat production values as a function of T, for female and male merlins, respectively. Within the TNZ of females, averaged 6.96 + 0.23 kJ . h-' ( n = 16) (equivalent mass-specific H, = 7.92 f 0.20 mW . g-I; average mass of birds tested = 241 g; n = 4) .

Operative temperature (OC)

Operative temperature ("C)

Fig. I . Relation of H, to operative temperature for wintering male ( A ) and female ( B) merlins. Points represent minimal values forpostabsorptive birds held in the dark during the restphase of the daily cycle. Multiple recordings of the same or similar values are indicated by numbers to the right of the point. The regression lines for data below the lower critical temperature were fitted by means of the least-squares method. Horizontal lines represent Hb.


Below the TNZ, the least-squares regression equation for standard metabolic rate ( H,,) as a function of Te was

On the basis of this relationship, extrapolation to zero metabolism was approximately 34.4 " C, suggesting that thermal conductance was not constant below the ir;,. This is potentially attributable to changes in Tb with lower Te (not seen here; nighttime female Tb = 39.6 f 0.2" C; n = 2 0 ) , changes in insulation through behavioral adjustments, or changes in metabolism due to muscular activity.

In contrast, the & of males averaged 5.23 k 0.19 kJ . h-' ( n = 1 0 )

(equivalent mass-specific H, = 8.49 f 0.28 mW . g-I; average mass of birds tested = 176 g; n = 5 ) . The least-squares regression equation of H,, versus T, for males at temperatures below the TNZ was

fk, (kJ . h-') = 7.57 - 0.164 T,. ( 1 3 )

At H, = 0, Te = 46.2"C, which is higher than the mean Th (nighttime male Th = 39.4 f 0.1 "C; n = 24 ) ; thus, in response to lower temperatures thermal conductance is decreased by male merlins and metabolic heat production is increased in order to maintain Tb. The male H, is significantly lower than that of female merlins (Hotelling's T2 test; F(1,24) = 28.0; P < 0.001). The slope for female H,, , related to T,, is greater than that of males, although not at a statistically significant level (Student's t-test = 1.961; 0.10 > P > 0.05) .

Because the slope of metabolism on T, equals thermal conductance only when the line extrapolates to T, = Tb, at H = 0 (McNab 1980) , values for thermal conductance were recalculated by forcing the metabolism curve through Tb. This brought the value for females to within 1% of the predicted value, while the value for males remained lower than predicted by about 7% (see table 8 ) .

The El in the TNZ averaged 21.3% f 2.3% in females and 24.5% f 3.2% in males (Hotelling's T2 test; F(1,24) = 0.74; P > 0.40). Below the TNZ the relationship of E f to Te for females was

while that for males was

TABLE 2 Cost of activities for rnerlins in an open-circuit respirometer and related to H b

Activity

Females Males

Energy Energy Cost CostC

N a n (kJ - h-') Energy cost/Hb Na n (kJ . h-') Energy cost/&

~2 . . . . . . . . . . . 4 16 Alert perch . . . . 4 31 Body care . . . . . 4 12 Eating . . . . . . . . 3 4 Flighte . . . . . . . . . . . . . .

" N = number of individuals. n = number of observations. Mean + SE of thermoneutral metabolic measurements.

"s determined in the rest phase of the daily cycle. As determined from eq. ( 6 ) of Masman and Klaassen (1987); for females, based on a mass of 272.1 g, wingspan of 65.5 cm, and wing area of 482.8 cmZ; for

males, based on a mass of 184.2 g, wingspan of 59.2 cm, and wing area of 378.4 cmZ.


TABLE 3 Monthly weather conditions, recorded a t the Environment Canada Weather Station in Saskatoon, averaged for the winters of 3983- 3984 t h r o ~ g h 1987-1988

November December January February

T, ("C): Diurnal . . . . . . . . . . . . . . -7.3 -11.4 -11.9 -10.3

Nocturnal . . . . . . . . . . . . -8.9 -12.2 -12.8 -12.3

. . . . . Wind speed (m s-') 3.69 4.06 4.22 3.81

Data on sex-related differences in energetic costs of the different activities assessed during the time-budget study are presented in table 2. The actual rates of energy expenditure for each category measured in the metabolism chamber were not significantly different between male and female (P > 0.05

for all comparisons). Aside from the H,, which was ascertained on postabsorptive birds held in the dark during the rest phase of the daily cycle, all other measurements were made in the TNZ on birds feeding or recently fed. Therefore, these energy costs comprise the H,, the cost of the activity, and the heat increment of feeding.

Meteorological Measurements

Mean monthly nocturnal and diurnal temperatures as well as average wind speed and average total precipitation recorded at the Saskatoon Weather Station for the study period are reported in table 3.

All roosts used by merlins were in conifers, either white (Picea glauca) or blue spruce ( Picea pungens). Overhead cover of the roost perch by fo- liage averaged 79% k 5% at the four roosts analyzed with hemispherical photographs (table 4 ) . Photographs taken with the camera axis placed hori- zontally against the tree trunk showed that 65% ? 2% ( n = 4 ) of the side view from the roost perch was occluded by vegetation. Air temperatures were significantly higher inside the roost at all four sites by an average of 0.4" C over the five nights tested (table 4) . This moderation of temperature was included in the TEB such that nighttime roost temperature was assumed to be T, + 0.4" C. Wind speeds in the roost, and on the leeward edge of the roost tree, were significantly less than those on the windward side (table 4) .


TABLE 4 Meteorological conditions at and immediately adjacent to rnerlin nocturnal roosts

Wind velocityb (m . S-')

Vegetation Cover (%I

Site In Roost Adjacent In Roost Leeward Windward Above Side

Note. Values are means, with SEs in parentheses. "<" or ">" indicates that values are significantly different ( T , , paired t-test, I.'< 0.05; wind velocity, ANOVA, and Duncan's multiple range test, P < 0.05). " n = 60 for each value. n = 48 for each value.

Reduction in wind speed averaged 71% k 9% in the roost, although this value is likely less than that actually experienced by merlins. Merlins have been observed to spend several minutes upon entering the roost tree select- ing a branch and apparently searching for the leeward side of the tree (I . G. Warkentin, personal observation). Our measurements of wind speed did not take this into account and were made on a roost perch regardless of the wind direction in relation to the orientation of that perch. Because merlins have also been observed to perch more often on the leeward side of spruce trees during the daytime, particularly on windy days ( I . G. Warkentin, personal observation), the 80% reduction in wind speed recorded for the leeward side of spruce trees was included in the TEB for merlins that perched on spruce. All other daytime perches were assumed to be exposed to ambient wind conditions.

Time-Energy Budget Analysis

Estimates of daily metabolism for wintering merlins from two different as- pects are presented in table 5: daily energy consumption (DEC), as determined from food intake or energy input (based on the nutritive values of common prey reported in table 6) , and the TEB, which is used in calculating the DEC. The values for DEC are based on observations made during 38


TABLE 5 Daily energy expenditure of wintering merlins for females and males during complete days in Saskatoon, Saskatchewan, determined on the basis offood intake and TEBs

Femalea Male

Number of prey . d-' . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1 1.2 Biomass of prey . d-' (g) . . . . . . . . . . . . . . . . . . . . . . . . . . . 58.4 40.8 Energy ingested (kcal . d-') . . . . . . . . . . . . . . . . . . . . . . . . 98.4 74.9 Energy assimilated (kcal . d-') . . . . . . . . . . . . . . . . . . . . 73.1 56.2 DEC (kJ . d-I) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 305.8 235.1 TEB (kJ . d-I) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 305.6 279.3 Percentage difference (TEB - DEC)/TEB X 100 . . . . . .O +15.8

" Includes six Microtuspenn.~ylvanicusconsumed by one female over 3 d; calculations are based on weight of 32 g and 4.148 kcal . g-' gross energy (Bird, Ho, and ~ a r & 1982). Also includes two common redpolls (CardtrelisjTammea) of approximately 12.2 g whole-carcass weight. hAssimilation quotient is assumed to be 0.75 for avian prey and 0.67 for marrmalian prey (see text).

complete days when 68 birds and 6 voles were eaten by the merlins we observed. The conversion to biomass is made on the basis of weights obtained from prey species caught in the study area or from study skin collec- tions. The average tjTD for female merlins was 305.6 * 9.9 kJ . d-' ( n = 32), or 1.8 X (range = 1.2-2.6 X H ~ ) . Males averaged 279.3 + 14.8 kJ . d-' ( n = 6 ) or 2.2 X tjh (range = 1.8-2.6 X E j b ) . The extent of agreement between estimates produced by the two techniques is represented by the value for percentage difference in table 5.

Monthly and seasonal energy budgets are presented in table 7. Mean monthly energy expenditures for male and female merlins in November and February were lower than during December or January (table 7 ) . The total energy expenditure by a male exposed to average winter conditions was 0.3% more than that of females; these values represent 198 and 197 house sparrows per winter for males and females, respectively.

Discussion Ecological Metabolism

Merlins resident in Saskatoon encounter temperature extremes ranging from about 40°C in summer to -40°C in winter. Mugaas and King (1981)


TABLE 6 Nutritive value of two common prey and food used to feed birds in captivity

House Bohemian Japanese Sparrow Waxwing Quail

N . . . . . . . . . . . . . . . . . . . . . . . . . . . 10 10 10 2 biomass available (g) . . . . . . 26.6 46.2 77.7 Percentage dry matter (DM) . . 33.84 33.97 26.35 Crude fat (% of DM) . . . . . . . . . . 19.33 27.62 14.61

. . . . . Crude protein (% of DM) 56.75 53.37 69.25 ~ s h (% of DM) . . . . . . . . . . . . . . . 12.67 8.06 9.18 Gross energy (kcal a g-') . . . . . 4.915 5.788 4.958

concluded, from their study of black-billed magpie (Picapica) thermal and behavioral energetics, that it was possible for birds to alleviate heat stress by finding shade, but cold stress could not be avoided. Since winter conditions cannot be avoided by nonmigratory birds, physiological and behavioral ad- aptations, which ameliorate the affect of cold, must be used to contend with winter and ensure survival. Three means have been noted by which animals may adapt physiologically to cold and improve their tolerance: reducing thermal conductance, lowering their 7;,, and increasing fib (Calder and King 1974; Weathers 1979). Our mass-specific Ejb values were 54%-57% higher than estimates based on the allometric relationship of metabolism and body mass derived by Aschoff and Pohl (1970; table 8 ) . But while our values were high, they were not unexpectedly so. In fact, they were similar in magnitude to those on a list of comparisons, assembled from the literature

TABLE 7

Monthly and totalseasonal energy budgets (kJ) of male and female merlins wintering in Saskatoon

November December January February Total

Female . . . . . 8,667.9 9,506.6 9,576.7 8,762.3 36,513.5 Male . . . . . . . 8,815.1 9,434.3 9,548.1 8,822.6 36,620.1


by Weathers (1979), between actual and predicted metabolic values of H,

for species exposed to cold climates for at least part of the year. Although the actual H,'S of male and female merlins show similar proportional increases over the predicted values, their Hb's are significantly different. This was not unexpected, because of the pronounced difference in body mass. Merlins were also distinctly different in terms of the 7;, both between the sexes (fig. 1 ), where females averaged 10.9"C lower than males, and between actual and predicted values (table 8 ) . The other notable difference between predicted and observed values was that while adjusted female thermal conductance was within 1% of the predicted value, that of males was about 7% lower than predicted (table 8 ) . This lower conductance, indicat- ing a higher insulative value, is one mechanism by which birds may adjust physiologically to cold climates. Considering the three physiological adap- tations discussed above, male and female merlins appear to have adopted different means of coping with cold climate. Both sexes have elevated Hbls, but females have a lower 7;, and males have reduced thermal conductances.

Biogeographical patterns of some birds in winter are directly related to their physiological capability to tolerate cold (Root 1988). Hayworth and Weathers (1984) found black-billed magpie distribution to be directly linked to climate and the species' metabolic physiology. An elevated H, suggests that food is not a limiting factor for merlins through the year (Weathers 1979). The physiological capabilities of merlins suggest that there have been changes in biotic (i.e., ecological) factors (rather than physiological), which have previously acted to limit merlin abundance on the northern Great Plains in winter. The change in merlin winter distribution may ulti- mately be the result of greater food abundance and availability. The towns and cities of the northern Great Plains have provided merlins with large, concentrated, and relatively dependable food sources that were not previously available in winter. James et al. (1987) found increases in merlin numbers in urban centers that paralleled significant increases over the last 30 yr in the number of Bohemian waxwings, a common prey item, found during winter.

Consideration of the results in table 5 and the literature on TEB estimates (for review, see Walsberg 1983) may give some clue as to the value of our metabolic measurements and HTD estimates. We obtained a high level of agreement between the daily energy intake values for complete-day observations and the estimates based on TEB. Because of the limited amount of time spent in activities other than perching, the contributions of basal and thermoregulatory costs toward the total &, are considerable and can represent anywhere from 40% to 85% of the I&, (Walsberg 1983). Studies have


TABLE 8

Predicted and observedphysiologicalparameters for male and female merlins based on weight

Predicted Observed Predicted Observed

. . . . . . . . . . . . & (mW g-')c 5.55 8.49 5.09 7.92 Thermal conductance

. . . . . . . . (mW [g " c]-') .289 ,257 .251 .285 (.267)' (.245Ie

Lower critical temperature . . . . . . . . . . . . . . . . . . ("c)' 20.2 14.3 19.3 3.4

"Average weight = 176 g ( n = 5). "verage weight = 24 1 g ( n = 4 ) . 'Calculated from the relation mW . g-' = 22.42 w-02', after Aschoff and Pohl (1970).

Calculatetl from the relation mW . (g . "C)-' = 2.96 w - O ~ ~ , after Wasser (1986) Determined by forcing the line of metabolism vs. T, below the TNZ through T, at H,,, = 0 .

'Calculated from the relation 7;, = T, - 7.57 W0 '" modified from eq. (1) of Calder and King (1974, p. 278) by substituting predictive equations for basal metabo!ism and thermal conductance.

shown that using a TEB model can provide estimates of &, that are significantly correlated and highly accurate when compared with concurrently run doubly labeled water trials (Weathers et al. 1984; Buttemer et al. 1986). The extent of agreement demonstrated by our TEB analysis, along with the accuracy of IjTD estimates using similar models (Weathers et al. 1984), suggest that our estimates are reasonable.

Changes in energy expenditures for male and female merlins through winter are not unexpected. With no monthly changes in activity budget, higher energy costs in December and January could be directly attributed to increased thermoregulatory expenditures. Given average weather conditions with the maximum winter population seen during this study present (38 merlins; Warkentin, James, and Oliphant, 1990), the overall seasonal consumption of the most common prey would total 200 kg, or 7,524 house sparrows. Whereas the daily TEB of females could be extrapolated to a value closely approximating our seasonal estimate for energy expenditure, that of males falls short of the seasonal value when extrapolated to the entire 120- d season. This difference was the result of when the data on complete days


for the sexes were available to create TEBs. Whereas samples for females were available from the entire winter season, those of males all fell within the month of February, when conditions were somewhat milder and energy expenditures less (table 7). Overall, the average seasonal expenditures for males and females were quite similar. This was surprising, given the distinct differences in body size between the sexes and similarities in the allocation of time to the five behavioral categories over the winter period (table 1 ) . However, Masman et al. (1988a) found that European kestrels have annual energy expenditures of similar magnitude for the sexes, despite considerable differences in body size. They found that the lower basal energy cost of males was offset by their higher thermoregulatory costs when compared with females. The same situation occurred in merlins. Males had lower basal energy costs but higher thermoregulatory costs, which resulted in nearly equal overall seasonal costs for male and female merlins.

Time Allocation

The principle of stringency developed by Wilson (1975, p. 142) states that time budgets have evolved to meet the needs of periods with the greatest energetic stress. According to the hypothesis, these periods may be infre- quent and unpredictable but require that all available time be devoted to foraging; under more benign circumstances the daylight phase will be typi- fied by large periods of inactivity. Merlins spent a great deal of time idle (table I ) , as do other wintering raptors (Koplin et al. 1980; Stalmaster and Gessaman 1984; Wid& 1984; Masman et al. 1988a). Since the merlin hunts from perches, and typically moves from perch to perch while searching for prey, the percentage of the active phase devoted to flight by wintering merlins may be used as an indicator of active ("productive") periods. The average amount of time spent in flight for merlins fell within the range of those found in bald eagles (Stalmaster and Gessaman 1984), European kestrels (Masman et al. 1988a), and northern goshawks (Accipiter gentilis; wid& 1984). This left periods, in the range of 80%-90% of the daylight phase, when merlins were simply perched.

On the basis of Wilson's hypothesis (1975), one might predict that days with high thermal stress would be stringent periods characterized by much higher activity levels than average. To test this we looked at data from a radio-tagged adult female. During three complete days when energetic stress was high (temperatures averaging between -17.3" and -30.7" C) , she ate four house sparrows on each day. It generally took about 30 min to ingest each meal and then 45 to 60 min for her crop to empty. When these observa-


tions were made, the active phase length ranged from 8.6 to 9.3 h, giving an average of one meal every 2.2-2.3 h. Considering these factors, it appears that this female was approaching the maximum intake possible, given the day length available. In addition, with a consumption estimated at 740.4 kJ . d-', she exceeded the theoretical upper limit of food-processing rate, suggested by Kirkwood (1983), of 1,713 kg0." (= 670.8 kJ . d-' for a 272-g female merlin). For two of these days, time spent in flight took up 6.1% and 6.9% of the active phase when she left the city to hunt at a cattle feedlot 13 km from her nighttime roost. On the third day she did not leave the city and spent only 2.9% of her active phase in flight. Although all of these values exceed the average of 2.3% flight time for females, these days still had long periods of inactivity.

It seems unlikely that this time spent perching will ever be fully utilized by a bird of prey for productive activity. Some other explanation must be found to account for "idle" time. In fact, the merlin and other birds of prey in these periods may not actually be inactive. Certainly, in part, some consideration must be given to the handling time required for food in terms of digestion. The foraging rates of hummingbirds are directly limited by the time required to empty their crop (Diamond et al. 1986). Because hummingbirds are able to fill their crops much faster than they empty, birds foraging at maximal rates are still found simply perche for about 80% of the active phase (Stiles 1971), despite the quick turn 3 ver of crop contents (Diamond et al. 1986). In addition, inactivity itself may be an important behavioral mechanism in wintering birds for coping with energetic stress. Norberg ( 1977) predicted that foraging effort would increase during times when prey densities decline and/or thermoregulatory requirements increase. However, greatly reduced foraging activity has been noted over the winter period in black ducks (Anas rubripes; Hickey and Titman 1983) and European starlings ( Sturnus vulgaris; Lundberg 1985). It has also been suggested that, during extreme conditions in winter, the costs of foraging may be higher than the energy gained (Evans 1976; Lundberg 1985). Under these circumstances, complete inactivity may be advantageous, at least on a short-term basis. Rather than maximize energy intake, birds may attempt to minimize energy expenditure, particularly for expensive activities like flight. Such an explanation matches the conclusions of Masman et al. (1988b) regarding stringent periods in the annual cycle of European kestrels. They postulated that there was no proof of such periods, and that the annual activity budget of the kestrel was most easily understood when divided into two phases. During summer, kestrels attempt to maximize energy gain and thus maximize their reproductive output. In winter, their


strategy is to minimize energy costs and inputs in order to minimize activity costs.

Roost Energetics

The nighttime roost provided an energy savings of about 6% per night for males and females when TEB models were compared for birds using pro- tected roosts and birds using exposed perches. This value corresponded with that for estimates of energy savings of nearly 10% by dark-eyed juncos (Junco hyemalis) (Webb and Rogers 1988) and of about 5% by bald eagles in winter roosts (Stalmaster and Gessaman 1984). Both Webb and Rogers (1988) and Walsberg (1986) made detailed examinations of winter roost- site microclimate and selection, and concur that the major reason for energy savings is the increased convective shielding provided by the roost tree. The reduction in wind speed (table 4) , along with the behavioral responses to wind by merlins, suggests that shielding from convective cooling is important in the selection of roosting positions. Although we did find statistically warmer temperatures in the roosts of merlins, it is highly unlikely, because of their magnitude (0.09 kJ - h-' for females and 0.07 kJ . h-' for males), that the values are of any biological significance. These slightly warmer temperatures are most likely the result of an inability of low-velocity winds to flush stagnant warm air out of the roost (Francis 1976; Stalmaster and Gessa- man 1984).

The savings derived from urban roosts may be one reason why all birds wintering in the city, which left the urban environment to hunt in farmyards and cattle feedlots in the country, returned each night to roost in the city. Even birds as far as 15 km from their nighttime roosts in the city re tuned. The lack of available coniferous trees for roosting in the country may be one explanation for this behavior; conifers d o not grow naturally in this region, and few have been planted outside the city. If a merlin could not find a conifer or other suitably sheltered position for roosting in the rural area where it was foraging, it could travel as far as 22 km to the city (the energetic equivalent in distance flown to the average saving of 6% HTD from a night roost) before the energetic advantages of the typical night roost were ne- gated. Although the hypothesis is untested, there may also be some amelio- rating urban effect on winds and temperature, as suggested by Gyllin, Kal- lander, and Syler (1977), which draws birds back to urban areas. Other factors, such as winter home range or territory maintenance, may also favor return to a roost in the city.


Acknowledgments

We thank the following people for generously providing the equipment and technical assistance that made this project possible: C. P. Hedlin and E. W. Underhill, National Research Council of Canada; E. A. Ripley, Department of Plant Sciences, D. Deutscher, Department of Mechanical Engineering, L. W. Oliphant, Department of Veterinary Anatomy, S. Hodgson, Depart- ment of Animal Sciences, all of the University of Saskatchewan; R. Begrand, Saskatchewan Research Council; and R. G. Clark and A. Didiuk, Canadian Wildlife Service. The Prairie Migratory Bird Research Centre of the Canadian Wildlife Service kindly provided waxwing carcasses. R. C. Kruger calculated the washout curve for the metabolism chamber. Thanks are due to L. W. Oliphant, P. C. James, and R. G. Clark for helpful advice and discussions at various stages of the project. R. J. F. Smith, M. Rever-DuWors, R. W. Nero, B. R. Neal, W. J. Maher, M. W. Collopy, and G. R. Bortolotti also commented on an earlier draft. Funding was provided by the Natural Sciences and Engi- neering Research Council of Canada, the University Research Support Fund of the Canadian Wildlife Service, the Frank M. Chapman Fund of the Ameri- can Museum of Natural History, and the Canadian Plains Research Centre. SupporL during the project was provided to I.G.W. through a University of Saskatchewan Graduate Scholarship. N.H.W. was supported by operating grants from NSERC and MRC (Canada).

Literature Cited

ASCHOFF, J., and H. POHL. 1970. Der Ruheumsatz von Vogeln als Funktion der Tages- zeit und der Korpergrosse. J. Ornithol. 111:38-47.

BARTHOLEMEW, G. A, , D. VLECK, and C. M. VLECK. 1981. Instantaneous measurements of oxygen consumption during pre-flight warm-up and post-flight cooling in sphin- gid and saturniid moths. J. Exp. Biol. 90:17-32.

BIRD, D. M., S.-K. Ho, and D. PAR& 1982. Nutritive values of three common prey items of the American kestrel. Comp. Biochem. Physiol. 73A:513-515.

BUTTEMER, W. A,, A. M. HAYWORTH, W. W. WEATHERS, and K. A. NAGY. 1986. Time- budget estimates of avian energy expenditure: physiological and meteorological considerations. Physiol. 2001. 59:131-149.

CALDER, W. A., and J. R. KING. 1974. Thermal and caloric relations of birds. Pages 259-413 in D. S. FARNER and J. R. KING, eds. Avian biology. Vol. 4. Academic Press, New York.

CLARK, W. S. 1981. A modified dho-gaza trap for use at a raptor banding station. J. Wild. Manage. 45:1043 -1044.

DIAMOND, J. M., W. H. KARASOV, D. PHAN, and F. L. CARPENTER. 1986. Digestive physi-


ology is a determinant of foraging bout frequency in hummingbirds. Nature 320: 62-63.

EVANS, P. R. 1976. Energy balance and optimal foraging strategies in shorebirds: some implications for their distributions and movements in the non-breeding season. Ardea 64:117-139.

FRANCIS, W. J. 1976. Micrometeorology of a blackbird roost. J . Wild. Manage. 40:132- 136.

GYLLIN, R., H. KALLANDER, and M. SYLER. 1977. The microclimate explanation of town centre roosts of jackdaws (Corvus monedula). Ibis 119:358-361.

HAMMEL, H. T. 1956. Infrared emissivities of some arctic fauna. J. Mammal. 37:375- 378.

HAYES, S. R., and J. A. GESSAMAN. 1980. The combined effects of air temperature, wind and radiation on the resting metabolism of avian captors. J. Therm. Biol. 5:119- 125.

HAYWORTH, A. M., and W. W. WEATHERS. 1984. Temperature regulation and climatic adaptation in black-billed and yellow-billed magpies. Condor 86: 19-26.

HICKEY, T. E., and R. D. TITMAN. 1983. Diurnal activity budgets of black ducks during their annual cycle in Prince Edward Island. Can. J. Zool. 61:743-749.

JAMES, P. C., A. R. SMITH, L. W. OLIPHANT, and I. G. WARKENTIN. 1987. Northward expansion of the wintering range of Richardson's merlin. J . Field Omithol. 58: 112-117.

KIRKWOOD, J . K. 1983. A limit to metabolizable energy intake in mammals and birds. Comp. Biochem. Physiol. 75A:l-3.

KOPI.IN, J . R., M. W. COLLOPY, A. R. BAMMANN, and H. LEVENSON. 1980. Energetics of two wintering raptors. Auk 97:795-806.

LUNDBERG, P. 1985. Time budgeting by starlings Sturnus vulgaris: time minimizing, energy maximizing and the annual cycle organization. Oecologia 67331-337.

MCNAB, B. K. 1980. On estimating thermal conductance in endotherms. Physiol. Zool. 53:145-156.

MASMAN, D., S. DMN, and H. BELDHUIS. 1988a. Ecological energetics of the kestrel: daily energy expenditure throughout the year based on time-energy budget, food intake and doubly labeled water methods. Ardea 76:64-81.

MASMAN, D., S. DAAN, and C. DIJKSTRA. 19886. Time allocation in the kestrel, Falco tinnunculus, and the principle of energy minimization. J. Anim. Ecol. 57:411-432.

MASMAN, D., M. GORDIJN, S. DAAN, and C. DIJKSTRA. 1986. Ecological energetics of the European kestrel: field estimates of energy intake throughout the year. Ardea 74:24-39.

MASMAN, D., and M. KLAASSEN. 1987. Energy expenditure during free flight in trained and free-living Eurasian kestrels, Falco tinnunculus. Auk 104:603-616.

MORRISON, D. F. 1967. Multivariate statistical methods. McGraw-Hill, New York. MUGMS, J. N., and J. R. KING. 1981. Annual variation of daily energy expenditure by

the black-billed magpie: a study of thermal and behavioral energetics. Stud. Avian Biol., no. 5.

NOBEL, P. S. 1974. Boundary layers of air adjacent to cylinders. Plant Physiol. 54:177- 181.


NORBERG, R. A. 1977. An ecological theory o n foraging time and energetics and choice of optimal food-searching method. J . Anim. Ecol. 46:511-529.

Porr~., H. 1969. Some factors influencing the metabolic responses to cold in birds. Fecl. Proc. Fed. Am. Soc. Exp. Biol. 28:1059-1064.

ROBINSON, D. E., G. S. CAMPBEI.~., and J . R. KING. 1976. An evaluation of heat exchange in small birds. J . Comp. Physiol. 105:153-166.

ROOT, T. 1988. Energyconstraints o n avian distribution and abundances. Ecology 69: 330-339.

STAI.MASTER, M. V., and J . A. GESSAMAN. 1984. Ecological energetics and foraging behavior of overwintering bald eagles. Ecol. Monogr. 54:407-428.

STII.ES, F. G. 1971. Time, energy and territoriality of the Anna hummingbird (Calypte a n n a ) . Science 173:818-821.

VEGHTE,J. H., and C. F. HERHEID. 1965. Radiometric determination of feather insulation and metabolism of arctic birds. Physiol. Zool. 38:267-275.

WAI.SRERG, G. E. 1983. Avian ecological energetics. Pages 161-220 in D. S. FARNER, J. R. KING, and K. C. PARKES, eds. Avian biology. Vol. 7. Academic Press, New York.

. 1986. Thermal consequences of roost-site selection: the relative importance of three modes of heat conservation. Auk 103:l-7.

WALSDERG, G. E., ancl J . R. KING. 1978a. The heat budget of incubating mountain white-crownecl sparrows (Zo~zotrichia l eucophr~a oriantha) in Oregon. Physiol. Zool. 51:92-103.

. 19786. The relationship of the external surface area of birds to skin surface area and body mass. J . Exp. Biol. 76:185-189.

WARKENTIN, I . G. 1986. Factors affecting roost departure and entry by wintering merlins. Can. J. Zool.64:1317-1319.

WARKENTIN, I. G., P. C. JAMES, and L. W. O L I P J ~ A N T . 1990. Body morphometrics, age structure and partial migration of urban Merlins (Falco co[umbarius). Auk (in press).

WASSER, J . S. 1986. The relationship of energetics of falconiform birds to body mass and climate. Condor 88:57-62.

W E K ~ I ~ I E ~ S , W. W. 1979. Climatic adaptation in avian standard metabolic rate. Oeco- logia 42:81-89.

WEATHERS, W. W., W. A. BUTTEMER, A. M. HAYWORTH, and K. A. NAGY. 1984.An evaluation of time-budget estimates of daily energy expenditure in birds. Auk 101:459- 472.

WEBB, D. R., and C. M. ROGERS. 1988. Nocturnal energy expenditure of dark-eyed juncos roosting in Indiana during winter. Condor 90: 107-1 12.

W I D ~ N , P. 1984. Activity patterns ancl time-budget in the goshawk Accipitergentilis in a boreal forest area in Sweden. Ornis Fennica 61:109-112.

WUNANDTS, H. 1984. Ecological energetics of the long-eared owl (Asio otus). Ardea 72:l-92.

WILSON, E. 0 . 1975. Sociobiology: the new synthesis. Harvard University Press, Cam- bridge.

WITHERS, P. C. 1977. Measurement of VO,, ~ c o , and evaporative water loss with a flow-through mask. J . Appl. Physiol. 42:120-123.

ecological energetics of wintering merlins falco columbariusiwarkent/ecological energetics of...

Documents