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Daily Torpor in a Free-ranging Goatsucker, the Common Poorwill (Phalaenoptilus nuttallii)

March 1992
Physiological Zoology 65(2):457-472

Authors:

University of Regina

Numerous laboratory studies show that common poorwills (Caprimulgidae: Phalaenoptilus nuttallii) are capable of entering daily torpor when deprived of food. Using temperature-sensitive radio transmitters, I measured the skin temperature of free-ranging birds under natural conditions to test three hypotheses about the use of torpor by poorwills. I predicted that (1) poorwills would enter torpor only in "energy emergencies" (defined as birds with low body mass), (2) only the nonincubating or brooding member of a pair would use torpor during the breeding season, and (3) poorwills would be less likely to enter torpor on moonlit nights when longer periods of activity can be sustained. My results show that adult poorwills of both sexes enter torpor regularly in April, May, and September, but not during the breeding season. I found no evidence that torpor was used only in energy emergencies or that the lunar cycle influenced the use of torpor. Skin temperatures regularly dropped below 10°C and in one instance fell below 3 C. On one occasion an individual bird remained torpid for at least 36 h. I found limited evidence suggesting that the temperature at twilight, but not insect abundance, can be used to predict whether birds will remain active or enter torpor.

…

a, Distribution of Tmin (0 C)for nights when birds did (n = 29) and nights when they did not (n = 40) enter torpor. Data for June 4August 31 are not included, since this was a period when birds did not enter torpor. b, Distribution of T,,, (oC) for nights when birds did (n = 29) and nights when they did not (n = 40) enter torpor. A KolmogorovSmirnov test shows that the distributions are significantly diferent (see text).

…

a, Distribution of the total number of insects sampled by sticky traps on nights when birds did (n = 12) and nights when they did not (n = 17) enter torpor. Data for June 4-August 31 are not included, since this was a period when birds did not enter torpor. b, Distribution of the number of large insects sampled by sticky traps on nights when birds did (n = 12) and nights when they did not (n = 17) enter torpor.

…

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457

Daily Torpor

in a Free-ranging Goatsucker,

the

Common Poorwill

(Phalaenoptilus

nuttallii)

R. Mark

Brigham*

Division of Ecology (Behavioural

Ecology Group), Department

of Biological

Sciences, University

of Calgary, Calgary,

Alberta T2N 1N4, Canada

Accepted 8/21/91

Abstract

Numerous laboratory

studies show that common

poorwills (Caprimulgidae:

Pha-

laenoptilus nuttallii) are capable of entering daily torpor

when deprived offood.

Using

temperature-sensitive

radio transmitters,

I measured the skin temperature

offree-ranging birds under natural conditions to test three hypotheses

about the

use of torpor by poorwills. I predicted that (1) poorwills would enter torpor only

in "energy emergencies"

(defined as birds

with low body mass), (2) only the non-

incubating or brooding

member

ofa pair would use torpor

during the breeding

season, and (3) poorwills

would be less likely to enter torpor

on moonlit nights

when longer periods of activity can be sustained.

results

show that adult

poor-

wills of both sexes enter torpor

regularly

in April, May,

and September,

but not dur-

ing the breeding

season. Ifound no evidence that torpor

was used only in energy

emergencies

or that the lunar cycle influenced the use of torpor.

Skin temperatures

regularly

dropped

below 100

C and in one instance

fell below

30 On one occa-

sion an individual bird remained torpid

for at least 36 h. Ifound limited evidence

suggesting

that the temperature

at twilight,

but not insect abundance, can be used

predict whether birds

will remain active or enter torpor.

Introduction

The high metabolic rate

of homeothermic animals

has favored the evolution

of a number of ways to minimize energy expenditure and cope with periods

of food shortage.

Torpor,

which allows the reduction of metabolic rate

and

consequently body temperature

(Tb), is one physiological means used by

some homeotherms

to "escape"

conditions

of extreme cold or food shortage.

In birds and mammals, torpor is characterized

by a periodic, facultative

lowering of Tb

resulting in a hypometabolic

state (Wang

1989). Depending

Present address:

Department

Biology, University

Regina,

Saskatchewan

S4S

OA2, Canada.

Physiological

Zoology 65(2):457-472.

1992.

C 1992

The

University

Chicago.

All

rights

reserved.

0031-935X/92/6502-911$02.00

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458 R.M.

Brigham

on the species, environmental

conditions, and ecological situation, Tb may

drop 40-350C below normal, and torpor may last from hours to weeks

(Wang 1989).

Torpor

in birds and mammals is polyphyletic (see Dawson and Hudson

[1970] and Wang [1989] for reviews) and represents an advanced form of

thermoregulation

rather than a reversion to primitive

poikilothermy.

How-

ever, because hypometabolism has been studied almost exclusively in

mammals (Heller 1989), the use of torpor by birds is interesting from a

comparative standpoint.

Dawson and Hudson (1970) and Reinertsen

(1983)

reviewed the occurrence

of facultative

torpor

in birds and listed eight orders

in which the phenomenon has been found. Torpor

in birds typically lasts

less than 24 h and has been characterized

as taking two forms. Nocturnal

hypothermia (see, e.g., Reinertsen and Hafthorn

1983) occurs when indi-

viduals show shallow depressions (5o-100C) in Tb

and return to normal

dawn,

whereas daily torpor typically

involves depression of Tb

by more than

100C. It is likely that these two physiological states represent a continuum

and cannot be clearly differentiated,

as my arbitrary

temperature ranges

suggest. Many

hummingbirds

(Trochilidae;

Krtiger,

Prinzinger,

and Schu-

mann 1982) and goatsuckers (Caprimulgidae;

Bartholomew, Howell, and

Cade 1957) enter daily torpor

under laboratory

conditions. One species that

might not fit this classification is the common poorwill (Caprimulgidae:

Phalaenoptilus nuttallii), the only bird thought to be capable of entering

long-term torpor

or hibernation (Jaeger 1948, 1949; Brauner

1952).

Studies of daily torpor

in hummingbirds

(Lasiewski 1963; Lasiewski and

Lasiewski

1967; Hainsworth,

Collins, and Wolf 1977;

Withers

1977; Krtiger

et al. 1982) and

goatsuckers

(Marshall

1955;

Bartholomew et al. 1957;

Howell

and Bartholomew

1959;

Bartholomew,

Hudson,

and Howell 1962;

Peiponen

1966;

Austin and Bradley

1969;

Dawson

and Fisher

1969;

Ligon

1970;

Withers

1977) are almost exclusively laboratory investigations.

This is probably

due

to the small

size of these birds and their

inaccessibility

under field conditions.

In one of the few field studies, Calder

and Booser (1973) used thermistors

implanted in synthetic eggs and found that incubating

female broad-tailed

hummingbirds (Selasphorusplatycercus)

entered torpor

on only two of 161

nights. On the two nights, the use of torpor

was correlated

with a reduced

opportunity

for feeding.

On the basis of laboratory

studies, many

authors claim that

torpor

in birds

occurs only when the animal is energetically stressed (Calder and King

1974; Hainsworth et al. 1977; Hainsworth and Wolf 1978; Hudson 1978).

In both hummingbirds

and goatsuckers, torpor

under laboratory

conditions

has been associated with a prior depletion of energy in the form of reduced

body mass (Marshall

1955;

Hainsworth et al. 1977;

although

see Jaeger 1948;

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Torpor

Free-ranging

Poorwills

459

Ligon 1970). Recently

however, Carpenter

and Hixon (1988) found a wild,

healthy, energetically unstressed rufous hummingbird (Selasphorus

rufus)

in torpor.

This is counter to the prediction of the "energy emergency" hy-

pothesis. There are no field data on the use of torpor by goatsuckers

under

natural conditions that allow for an evaluation of this hypothesis.

Heterothermic bats (e.g., vespertilionids and rhinolophids) are ecologi-

cally

similar to goatsuckers

in that

they feed on flying

insects captured during

crepuscular or nocturnal activity periods. Both laboratory (reviewed in

McNab

[1982]) and field studies (Racey and Swift 1981; Audet and Fenton

1988) show that

insectivorous bats use torpor

in situations other than

energy

emergencies (defined by reduced body mass). However, pregnant

and lac-

tating bats, like nesting hummingbirds (Calder and Booser 1973), enter

torpor only under extreme conditions. For bats, the explanation for this is

that it delays parturition

and inhibits lactation

(Racey 1973;

Racey

and Swift

1981; McNab

1982;

Audet and Fenton 1988).

The purpose of this study was to determine, with temperature-sensitive

radio

transmitters,

when or if free-ranging

poorwills

enter

torpor.

If poorwills

enter torpor only in energy emergencies, then torpor should occur rarely

and only in birds with low body masses. If poorwills behave like insectivo-

rous bats (see, e.g., Audet and Fenton 1988), then I predict that they will

enter torpor regularly during periods of low nocturnal temperatures

and

low insect abundance but not, or only rarely, during the incubating or

brooding period, since this may result in hatching delay or the death of

embryos or chicks (Hafthorn 1988). If torpor occurs during the nesting

period, I predict that it will only be used by the nonincubating or non-

brooding member of the pair. Finally, since some goatsuckers, including

poorwills, forage more during moonlit periods of the night (Mills 1986;

Brigham

and Barclay,

in press), torpor,

if used, should occur less often on

"light"

nights when birds have more time available for foraging.

Material and Methods

Study Site

The study was conducted in September 1988 and from April

to September

in 1989 and 1990 in the Okanagan Valley of south-central

British Columbia

(49018'N,

119031'W),

near the northern

limit of the species' breeding range,

where they do not overwinter (Cannings, Cannings,

and Cannings 1987).

Therefore, my observations

represent characteristics

of torpor and not hi-

bernation. The southern

Okanagan Valley comprises a series of lakes linked

by the Okanagan

River.

On the side hills of the valley, where the activities

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460 R.M.

Brigham

of Phalaenoptilus nuttallii are centered, the vegetation consists of open

conifer forest dominated by Pinus ponderosa (Cannings et al. 1987). In

1988 and 1989, I captured

individuals

on the eastern

side of the valley near

Vaseaux

Lake.

In 1990, I trapped

individuals

on the western side, 8 km NW

of the town of Oliver. The two study areas were separated

by less than 10

km. I captured poorwills in mist nets set in foraging areas (usually across

gravel roads) or by luring birds into nets using song playbacks. I distin-

guished males from females by the presence and length of white tips on

the rectrices (Chapman

1925). Females had buff-colored tail tips about half

the length of males' tail tips (J. T. Marshall,

personal communication). All

individuals

included in the analysis

were at least 1 yr old.

Telemetry

I used temperature-sensitive

radio transmitters

(model PD-2T,

Holohil Sys-

tems, Woodlawn, Ontario) to measure the temporal patterns

of activity by

poorwills and to ascertain

when they entered torpor.

Transmitters

(average

mass 2.4 g) were affixed

to the birds with an elastic harness slipped over

the wings (Brigham 1989). The effective range of signal reception varied

from 1 to 4 km depending on terrain. I classified individuals as either moving

or stationary

at 5-min

intervals

using a Merlin 12 telemetry

receiver (Custom

Electronics,

Urbana,

Ill.) and a five-element

Yagi

antenna.

During

each mea-

surement,

a minimum of 20 pulses were monitored and any change in either

the direction or strength

of the signal was defined as a movement.

Transmitters were affixed

so that the harness

kept the temperature

sensor

in contact

with the bird's skin on the back between the wings (interscapular

region). Thus, I measured skin temperature

(Tsk) in a manner analogous

to that

of Audet

and Fenton (1988). Transmitters

were calibrated to measure

temperature

from 0o to 400C (+0.5oC). I determined Tsk

by averaging

three

timings of the interval

required

for 10 transmitter

pulses and then using the

calibration curves prepared

for each transmitter

by the manufacturer.

This

was done every 20 min during nightly activity periods and opportunistically

during the daytime. Because of the transient fluctuations in avian Tb'S

(Reinertsen

and Hafthorn

1983) and the fact that

the Tb

active poorwills

varies between 350 and 44oC under laboratory

conditions (Bartholomew

al. 1962), I followed Hudson (1978) and operationally

defined poorwills

as having

entered torpor

when Tsk

fell below 30 C. In this study,

birds

with

skin temperatures

below 300C

were never found or measured

to be active.

Thirteen adult

birds

(six females,

seven males) were captured

and outfitted

with transmitters.

I monitored individual birds carrying

transmitters for 165

bird-nights. On 108 of these nights, I monitored movements and the Tsk

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Torpor

Free-ranging

Poorwills 461

of the individual all night (from approximately

sunset until activity

ceased

at dawn).

Environmental and Lunar Conditions

I measured the minimum

nightly temperature

(Tmin;

+0.50C), using a Taylor

maximum-minimum thermometer

mounted 1 m above the ground. In both

years the thermometer was placed within 1 km of the day roost or nest

locations of birds carrying

transmitters. There was a significant

correlation

in both 1989 and 1990 (r2 = 0.73 and P< 0.05 in both years) between Tmin

and the minimum temperature

measured at the Penticton airport,

located

15 km north of the study

area.

a relative indication of twilight temperatures

(Tow)

I used measurements from Penticton. At the same time that I measured

Tsk,

I used a Taylor laboratory

thermometer at the tracking

position to mea-

sure ambient temperature

(Ta)

to the nearest 20C.

Nightly lunar conditions were grouped into five categories based on the

percentage of the moon face illuminated (%MFI)

at midnight (0%, 1%-

25%,

26%-50%, 51%-75%, 76%-100%;

Mills 1986). Values of %MFI were

taken from tables published in the Astronomical Almanac (e.g., Anawalt

and Boksenberg 1987). The times of sunset, nautical

twilight, and sunrise

were calculated for the study site by the Dominion Astrophysical

Obser-

vatory,

Victoria,

British Columbia.

I used the end of nautical

twilight (when

the sun is 120 below the horizon) as the time delineating dusk or dawn

from

true night (Mills 1986). Cloud cover was not taken into account, since

it was rarely

cloudy in the study area and because Mills showed it did not

influence activity by whippoorwills (Caprimulgus vociferus).

In 1989, I assessed the influence of insect abundance on the use of torpor

by poorwills. Four sticky traps (coated with Tangletrap;

Southwood 1978;

Kunz 1988) were suspended approximately

1, 2, 3, and 5 m above a gravel

road where poorwills commonly foraged. On nights when birds were

tracked,

the traps

were hung at sunset and collected at sunrise. I recorded

the total number of insects captured, identified each insect to order, and

characterized them as large (>4 mm) or small (4 mm) in body length.

Results

On 16 occasions I measured Tsk

while simultaneously measuring cloacal

temperature

(Tc),

using a quick-registering

thermometer inserted 1 cm into

the cloaca. There was a highly significant

relationship between Tsk

and Tc

(Tc = 1.58 + 0.9598 Tsk; r2 = 0.99, P < 0.01; fig. 1). This illustrates the

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462 R.M.

Brigham

Skin Temperature ('C)

40 OO

10 - O

5 O

5 10 15 20 25 30 35 40

Cloacal Temperature

('C)

Fig. 1. Relationship between simultaneous measurement of Tsk

( C) and

T, (oC). The diagonal represents Tsk

= Tc.

reliability

of using Tsk

to assess Tb. Generally, Tc

was between 10 and 20C

higher than Tsk

(intercept = 1.58).

Individual

poorwills entered torpor

on 29 of the 165 bird-nights.

Ten of

the 13 birds that carried transmitters

(six males, four females) used torpor.

Twelve of the 13 birds carrying

transmitters

participated

in at least one

nesting attempt. One male apparently

did not acquire a mate and did not

nest. The incidence of torpor was not evenly distributed throughout the

summer

(table 1). No individual male or female used torpor

while incubating

eggs or brooding chicks or during periods not spent on the nest. The latest

date in the spring that an individual entered torpor

was June 3, 1990, and

the earliest date in the fall was September 1, 1989. The body mass of nine

males and six females captured

during April,

May,

and September,

the period

when torpor

was used, varied

between 36.9 and 54.5 g, with males weighing

44.7 and females 48.3 g, on average.

TABLE

Distribution of torpor

bouts during the summers of 1989 and 1990

April-May June July-August September

Bird-nights ... 55 44 58 7

Torpor ...... 24 2 0 3

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Torpor

Free-ranging

Poorwills

463

Usually

(28 of 29 torpor

bouts), individuals were active

at dusk and entered

torpor at the end of nautical twilight (fig. 2). This suggests that the birds

use cues available during the dusk foraging period to determine whether

or not to enter torpor.

With

one exception, torpor

bouts lasted less than 12

h. On May

22-23, 1990, a male bird remained torpid for at least 36 h and

did not forage during the dusk period of May

23.

The use of torpor

on a given night varied among individuals. On five of

the nine nights when I monitored the Tb

of more than one bird simulta-

neously (two birds on eight nights and three birds on one night) one in-

dividual remained homeothermic while one entered torpor. On the night

when three birds were tracked,

two remained homeothermic and one en-

tered torpor.

The lowest Tsk

I recorded

was 2.80C

for a male bird at 0650 hours on May

13, 1989, when Tmin reached -1lC. From

the regression equation this cor-

responds to a predicted Tc

of 4.3 C. Not surprisingly,

I never recorded min-

imum predicted Tc

below Tmin (fig. 3); however, there was no significant

correlation between Tmin and predicted Tc (r2 = 0.38, n = 16, P> 0.10).

On nine occasions I measured

the cooling rates of poorwills entering

torpor.

The values ranged from a minimum of 4.20C per hour to a maximum of

13.20C

per hour.

Skin

temperature

('C)

40-

2000 2100 2200 2300 2400 0100 0200 0300 0400 0500

- Active

birds -- Torpid

birds

Fig. 2. Mean Ts, (O C) for three male poorwills during the period from

April

30-May 20, 1989. Abscissa values show the time of the night. The

Tsk

was measured

for at least one bird all night on 15 dates during this

period, with a total sample of 20 bird-nights

(11 active and nine torpid).

Error

bars represent

+ 1 SE. The

arrow indicates the end of nautical twi-

light.

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464 R.M.

Brigham

Predicted

cloacal

temperature

(C)

16 0 0

12 o

O O

4- O

-2 0 2 4 6 8 10 12

Minimum

temperature

(0C)

Fig. 3. Minimum

Tc ("C) predicted by the equation

fromfig. 1,

plotted

against Tmin

(o C). The diagonal represents T, = Tm:n,.

In an attempt

to identify

the cues birds

might use in determining

whether

or not to enter torpor, I compared the distributions of Tmin,

Twi, total insect

abundance, and the abundance of large insects for nights when birds did

and did not enter torpor

using two-sample Kolmogorov-Smirnov

tests (figs.

4, 5). These distributions

represent 29 bird-nights

when torpor was used

and 40 nights when it was not for the same 10 individual birds (six males

and four females). For those nights when some individuals entered torpor

and some did not, I included data for the relevant individuals in both dis-

tributions. As

poorwills never became torpid

during

the nesting or brooding

period (between June 4 and August 31), this period was not included in

the analysis.

There were no significant

differences between the torpid and nontorpid

distributions with respect to the Tmin, total insect, or large insect variables

(Kolmogorov-Smirnov

D's of 0.20, 0.10, and 0.20, respectively;

P> 0.05 in

all cases). There was, however, a significant

difference in the distributions

of Tw measured at the Penticton airport

for nights when birds did and

nights when they did not enter torpor (D = 0.43; P < 0.01). The nonover-

lapping portion of the distributions

suggests that, when Trwi

at the airport

was below 80C,

poorwills entered torpor,

while, above 120C,

birds

generally

remained homeothermic.

Homeothermic

poorwills are more active on nights with moonlight than

on "dark"

nights (Brigham

and Barclay,

in press). Therefore, I compared

the distribution of %MFI

for just

the nights when birds entered torpor

with

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Torpor Non torpor

-1 0 1 2 3 4 5 6 7 8 9 10 11 12 13

Temperature (oC)

Torpor M Non torpor

30 b

c 15

L-

o 10

4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19

Temperature (OC)

Fig. 4. a, Distribution of Tmin

(0 C)for nights when birds did (n = 29)

and nights when they did not (n = 40) enter torpor.

Data for June 4-

August 31 are not included, since this was a period when birds did not

enter torpor.

b, Distribution of T,,, (oC) for nights when birds did (n =

29) and nights when they did not (n = 40) enter torpor.

A Kolmogorov-

Smirnov test shows that the distributions

are significantly diferent (see

text).

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S Torpor Non torpor

60 -

- 40 -

c 30

o 20

1 -5 6-10 11 -20 21+

Total number

of insects

Torpor Non torpor

70 b

0 1-5 6-10 11+

Number of large insects

Fig. 5. a, Distribution of the total number of insects sampled by sticky

traps on nights when birds did (n = 12) and nights when they did not (n

= 17) enter torpor. Data for June 4-August 31 are not included, since

this was a period when birds did not enter torpor.

b, Distribution of the

number of large insects sampled by sticky traps on nights when birds did

(n = 12) and nights when they did not (n = 17) enter torpor.

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Torpor

Free-ranging

Poorwills 467

the distribution of %MFI on all nights that I tracked on (excluding the

period from

June 4 to August

31, when torpor

was never recorded). I found

no significant

relationship

between the lunar condition and the use of torpor

(%2

= 0.66, P> 0.10; table 2).

Discussion

Adult free-ranging poorwills of both sexes enter torpor regularly except

during the breeding season. Body temperature

of torpid birds regularly

dropped below 10oC,

and in one case a bird remained torpid for at least 36

h. I found limited evidence that Twi,

but not the abundance of insects, can

be used to predict whether poorwills will remain active or enter torpor

any given night.

On 97%

of the nights

when individuals

ultimately

entered torpor, foraging

activity

occurred at dusk. Foraging

occurred at dusk on every night when

birds did not enter torpor. Activity

levels at dusk were lower for individuals

that ultimately became torpid, but the birds appeared to compensate for

this lower activity by initiating foraging activity significantly

earlier (R. M.

Brigham,

unpublished data). This difference in behavior

may be a result of

poorer foraging conditions on those nights when torpor is subsequently

used. Activity

at dusk and the almost complete cessation of activity

at the

beginning of true night by birds using torpor suggests that environmental

conditions near the end of the dusk foraging

bout influence the likelihood

of entering torpor.

Temperature

and insect abundance are the two most obvious potential

cues birds might use to "decide" whether to enter torpor. However, my

measures of prey abundance, especially of large insects, which make up

the vast majority

of the diet (R. D. Csada,

unpublished data) and therefore

TABLE 2

The

relationship between %MFI and the use of torpor by poorwills

%MFI

0 1-25 26-50 51-75 76-100

Bird-nights ... 21 4 4 8 8

Torpor ...... 9 2 3 4 4

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468 R.M.

Brigham

should be related to the rate of energy intake and Tmin, could not be used

to reliably

predict

the nights when birds entered torpor.

Although

there was

a significant difference between the distributions of Tw,

for nights when

poorwills did and nights when they did not enter torpor,

there was no ob-

vious threshold temperature

that

would allow the prediction of whether an

individual would enter torpor on any given night. This is not surprising,

given that moths, which are commonly consumed by poorwills (Bent 1940;

R. D. Csada,

unpublished data), emerge at different times of the year (see,

e.g., Yack

1988) and are influenced

by Ta

differently

(Heinrich

and Mommsen

1985). Similarly,

there is no precise threshold temperature

that can be used

to predict activity

or the entry into torpor by insectivorous

bats (Audet and

Fenton 1988). Variation

in the use of torpor between individuals is also

important,

illustrated

by the fact that, on the same night, some individuals

used torpor

whereas others did not. Unfortunately,

my small sample size of

nights when torpor

was used precludes rigorous analysis for the effects of

gender, time of year,

and foraging

success on the previous night on the use

of torpor by individual birds. However, it is worth noting that Audet and

Fenton (1988) found variation

between individual bats in the use of torpor

on the same night, which they ascribed to differences in reproductive

con-

dition.

Poorwills did not enter torpor in energy emergencies only, as some lab-

oratory

studies suggested they would (e.g., Marshall

1955). Except during

the nesting period, all tagged individuals (n = 10), with a range of body

masses, used torpor at one time or another. Thus, the data for poorwills

support the conclusions of Carpenter

and Hixon (1988), who rejected the

hypothesis that under natural conditions torpor is used by hummingbirds

only in energy emergencies.

To my knowledge, a Tsk

2.80C, which corresponds to a Tc

of 4.30

C, is

the lowest naturally

recorded temperature

for any species of bird. Withers

(1977) found that captive poorwills could not spontaneously arouse them-

selves from

torpor

when Tb

was below 50C.

field data

suggest that,

under

natural

conditions, Tb

can fall below 50C and individuals can still sponta-

neously rewarm.

This inconsistency in results could be due to the difference

in body mass between individuals in Wither's

study (35 g) and the free-

living birds in my study (46 g on average). Heavier

birds

should have larger

energy reserves and may be able to generate the heat required to rewarm

from low temperatures.

Therefore, these birds should be at less risk when

lowering Tb

below 50C.

Another

possible explanation is that Wither's

birds

were captured in southern California

and thus could have been less cold

tolerant than birds from the Okanagan.

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Torpor

Free-ranging

Poorwills 469

measurements of cooling rates for poorwills entering torpor

are similar

to those measurements made in the laboratory.

Cooling rates measured

under laboratory

conditions range from 1.80C to 17.1"C

per hour (Howell

and Bartholomew 1959; Lasiewski and Lasiewski

1967;

Austin and Bradley

1969; Ligon 1970) and are highly dependent on Ta.

This suggests that the

mechanism by which captive birds enter torpor is similar to the process

used under natural conditions.

I found no evidence to support the hypothesis that poorwills use torpor

less often on nights with moonlight than dark

nights. The use of torpor

was

not related to the relative illumination

provided by the moon, even though

this significantly

influences the foraging activity of these birds (Brauner

1952;

Brigham

and Barclay,

in press) and other

goatsuckers (Wynne-Edwards

1930; Mills 1986). It appears

that lunar condition has no effect on the use

of torpor by poorwills.

Although the southern Okanagan Valley of British Columbia is close to

the limit of the northern

range of the poorwill, the climate is moderate for

its latitude (Cannings

et al. 1987). Still, I expected that individual

birds not

attending eggs or chicks would enter torpor

to conserve energy on nights

with low Ta

and low insect abundance.

Tracking

data confirm that

both male

and female members of the pair participate

in incubation and brooding

(Aldrich 1935; Orr 1948). There was no obvious gender-related

pattern

the way nesting activity

was shared.

In some pairs,

the duties were unequally

divided (R. M. Brigham,

unpublished data). I predict that the probability

of finding

torpid birds during

the nesting period will increase in areas with

more continental climates than the Okanagan.

However, if this is not the

case, it suggests that the regular

occurrence of conditions requiring

the use

of torpor during

the nesting cycle may

be an ultimate constraint

determining

the northern

extent of the breeding range of this species.

In conclusion, this paper is the first

to provide field data about the use of

torpor by the poorwill, a bird whose physiological capabilities have long

attracted interest. The study demonstrates the critical

need for field data to

confirm or reject

the conclusions from

laboratory

studies of thermoregulation

(e.g., Carpenter

and Hixon 1988). In the case of poorwills, the large body

of laboratory

data does not completely account for the manner in which

poorwills use torpor

under natural

conditions. The apparently

unique attri-

butes of poorwills studied under laboratory

conditions prompted Heller

(1989) to suggest that conclusions regarding

the mechanisms of avian

torpor

should consider the poorwill as a special case. Whether

torpor

in these birds

really does represent a special case among birds or, for that matter,

verte-

brates should be addressed

by comparing

Phalaenoptilus

nuttallii with other

caprimulgids

and insectivorous bats. The depth and duration of bouts of

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470 R. M.

Brigham

torpor by poorwills appears to be similar to those used by bats (Audet and

Fenton 1988), an ecologically similar group of animals. It remains to be

determined whether the apparent hibernation by poorwills also resembles

that of bats. Heller (1989) and Wang (1989) both conclude that there is

strong evidence for physiological homology between all forms of avian and

mammalian torpor. Only with further work in the field will it be determined

whether this conclusion holds true.

Acknowledgments

I am grateful

to R. L.

Mackey,

M. C. Firman,

T. S. Collard,

S. D. Grindal,

Kershaw, A. L. MacKinlay, D. R. C. Prescott, D. W. Thomas, R. M. R. Barclay,

and H. N. Matthews for their help catching birds and timing beeps. The

study

was supported by Natural Sciences and Engineering

Research Council

(Canada)

operating grants

to R. M. R. Barclay,

a University

of Calgary

short-

term research grant, and an NSERC postdoctoral fellowship to myself. The

comments of R. D. Csada, A. C. Brigham, M. B. Fenton, M. B. C. Hickey, D.

Audet, P. A. Faure, R. M. R. Barclay, S. D. Wilson, and two anonymous re-

viewers greatly improved earlier versions of the manuscript.

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Thesis

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Audrey Le Pogam

Organisms are confronted with multiple environmental constraints to which they can respond through phenotypic adjustments that can potentially lead to physiological trade-offs. Contrary to species living only in temperate environments, the mechanisms underlying the phenotypic adjustments of species confronted with cold temperatures during most of the year are still poorly understood. My thesis focuses on the phenotypic adjustments of snow bunting's (Plectrophenax nivalis), a migratory passerine that winters in temperate zones (between 40° and 60°N) and migrates in spring to Arctic regions to breed. More specifically, I was interested in the variations of body composition (body mass, lipid and lean mass, pectoral muscle thickness), oxygen transport capacity (hematocrit) and metabolic performance (physiological maintenance costs - BMR and thermogenic capacity - Msum) among the winter, migratory and reproductive stages. 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However, lean mass declined and BMR remained stable over the winter, suggesting that buntings may also minimize the energetic costs of living in cold environments. In Chapter 2, I analyzed the phenotypic adjustment patterns of captive buntings during periods corresponding to migration and reproduction and compared them to the winter phenotype. The objective was to see if, and by what mechanism, traits associated with winter cold acclimation could be transferred to later stages of the annual cycle. The results show that although body mass, lipid mass and BMR increase for migration, traits related to cold endurance do not change in parallel since they are already elevated at the end of winter. This is the first direct demonstration that phenotypic traits associated with winter acclimation can transfer to the migratory phenotype and even be maintained during the breeding season. Through Chapter 3, I compared the phenotype of free-living buntings caught during winter at Rimouski and during pre-breeding at Alert. The objective was to determine whether cold endurance and associated traits could be maintained at a winter level during migration and pre-breeding. Results indicate that despite a decline in muscle thickness and hematocrit between winter and pre-breeding, cold endurance and energy reserves were maintained. These results support the hypothesis that migratory cold specialist species could maintain their cold endurance at a winter level until pre-breeding. Finally, in Chapter 4, I examined the change in phenotype between the pre-breeding and chick provisioning periods at Alert to determine how the transition between life stages on the breeding grounds, in interaction with spring thermal conditions, could influence cold endurance. Results show that buntings maintain a high thermogenic capacity as long as temperatures remain below 0-2°C, whether or not they actively reproduce. These observations therefore suggest that buntings likely experience a double physiological cost in late spring, when reproductive activities (i.e., egg production and incubation) begin and air temperatures are still below 0-2°C. Overall, this study demonstrates that not all thermal acclimation mechanisms established to date are generalizable to Arctic species. It therefore provides a reference point for future comparative research. Les organismes sont confrontés à de multiples contraintes environnementales auxquelles ils peuvent répondre par des ajustements phénotypiques menant potentiellement à des compromis physiologiques. Contrairement aux espèces vivant uniquement en milieux tempérés, les mécanismes sous-jacents aux ajustements phénotypiques des espèces confrontées au froid la majeure partie de l'année sont encore mal compris. Ma thèse porte sur les ajustements phénotypiques du plectrophane des neiges (Plectrophenax nivalis), un passereau migrateur qui hiverne en zone tempérée (entre 40° et 60°N) et migre au printemps vers les régions arctiques pour se reproduire. Plus particulièrement, je me suis intéressée aux variations de composition corporelle (masse corporelle, lipidique et maigre, épaisseur des muscles pectoraux), de capacité de transport de l'oxygène (hématocrite) et de performance métabolique (coûts de maintenance physiologiques - BMR et de capacité thermogénique - Msum) au cours de l'hiver, de la migration et de la reproduction. Pour cela, j'ai effectué de 2013 à 2019, des mesures (1) sur des individus maintenus captifs en volière extérieure à Rimouski (QC, 48°N), (2) sur des individus capturés sur leur aire d'hivernage à Rimouski et (3) à l'extrême nord de leur aire de reproduction, à Alert au Nunavut (82°N). Dans le chapitre 1, j'ai étudié les ajustements phénotypiques hivernaux des plectrophanes maintenus captifs en zone tempérée. L'objectif était de déterminer si le patron d'ajustements de cette espèce associée au froid la majeure partie de sa vie se conformait à celui des espèces résidentes aux mêmes latitudes. Les augmentations de masse corporelle et lipidique, d'épaisseur des muscles pectoraux, d'hématocrite et de Msum observées entre l'été et l'hiver suggèrent que la flexibilité phénotypique des traits associés à l'acclimatation thermique chez les espèces nordiques est comparable à celle des passereaux résidents des zones tempérées et donc que ces ajustements ne sont pas contraints par la vie dans un environnement froid. Toutefois, le déclin de masse maigre et la stabilité du BMR observés au cours de l'hiver suggèrent que les plectrophanes peuvent aussi minimiser les coûts énergétiques de la vie en milieux froids. Au chapitre 2, j'ai analysé les patrons d'ajustements phénotypiques de plectrophanes maintenus captifs au cours des périodes correspondant à la migration et la reproduction et je les ai comparées au phénotype hivernal. L'objectif était de voir si et par quel mécanisme, les traits associés à l'acclimatation au froid hivernal pouvaient être transférés aux stades ultérieurs du cycle annuel. Les résultats montrent que, bien que la masse corporelle, la masse lipidique et le BMR augmentent pour la migration, les traits liés à l'endurance au froid ne changent pas en parallèle puisqu'ils sont déjà élevés à la sortie de l'hiver. Il s'agit de la première démonstration directe que des traits phénotypiques associés à l'acclimatation hivernale peuvent se transférer au phénotype migratoire et même se maintenir en période de reproduction. Au travers du chapitre 3, j'ai comparé le phénotype de plectrophanes capturés en milieu naturel en hiver à Rimouski et en pré-reproduction à Alert. L'objectif était de déterminer si l'endurance au froid et les traits associés pouvaient se maintenir à un niveau hivernal durant la migration et la pré-reproduction. Les résultats indiquent que malgré un déclin d'épaisseur des muscles et d'hématocrite, l'endurance au froid et les réserves énergétiques étaient maintenues. Ces résultats confirment l'hypothèse selon laquelle les espèces migratrices spécialistes du froid pourraient maintenir leur endurance au froid à un niveau hivernal jusqu'à la pré-reproduction. Enfin dans le Chapitre 4, j'ai examiné l'évolution du phénotype entre la période de pré-reproduction et d'approvisionnement des oisillons à Alert afin de déterminer comment la transition entre les stades de vie sur les aires de reproduction, en interaction avec les conditions thermiques printanières, pouvait influencer l'endurance au froid. Les résultats montrent que les plectrophanes maintiennent une capacité thermogénique élevée tant que les températures demeurent inférieures à 0-2°C, qu'ils se reproduisent activement ou non. Ces observations suggèrent donc que les plectrophanes subissent probablement un double coût physiologique à la fin du printemps, lorsque les activités de reproduction (c.-à-d., production et incubation des œufs) commencent alors que les températures sont encore inférieures à 0-2°C. De manière générale, cette étude démontre que les mécanismes d'acclimatation thermique établis jusqu'à maintenant ne sont pas tous généralisables aux espèces arctiques. Elle constitue donc un point de référence pour de futures recherches comparatives.

Using skin temperature and activity profiles to assign chronotype in birds

Article

Full-text available

Sep 2022

Chronotypes describe consistent differences between individuals in biological time-keeping. They have been linked both with underlying variation in the circadian system and fitness. Quantification of chronotypes is usually by time of onset, midpoint, or offset of a rhythmic behaviour or physiological process. However, diel activity patterns respond flexibly to many short-term environmental influences, which can make chronotypes hard to identify. In contrast, rhythmic patterns in physiological processes, such as body temperature, may provide more robust insights into the circadian basis of chronotypes. These can be telemetrically recorded from skin-mounted, temperature-sensitive transmitters, offering minimally invasive opportunities for working on free-ranging animals in the wild. Currently, computational methods for deriving chronotype from skin temperature require further development, as time series are often noisy and incomplete. Here, we investigate such methods using simultaneous radio telemetry recordings of activity and skin temperature in a wild songbird model (Great Tit Parus major) temporarily kept in outdoor aviaries. Our aims were to first develop standardised selection criteria to filter noisy time series of skin temperature and activity, to second assign chronotype based on the filtered recordings, and to third compare chronotype as assigned based on each of the two rhythms. After the selection of rhythmic data using periodicity and autocorrelation parameters, chronotype estimates (onset and offset) were extracted using four different changepoint approaches for skin temperature and one approach for activity records. The estimates based on skin temperature varied between different approaches but were correlated to each other (onset: correlation coefficient r = 0.099–0.841, offset: r = 0.131–0.906). In contrast, chronotype estimates from skin temperature were more weakly correlated to those from activity (onset: r = −0.131–0.612, offset: r = −0.040– −0.681). Overall, chronotype estimates were less variable and timed later in the day for activity than for skin temperature. The distinctions between physiological and behavioural chronotypes in this study might reflect differences in underlying mechanisms and in responsiveness to external and internal cues. Thus, studying each of these rhythms has specific strengths, while parallel studies of both could inform broadly on natural variation in biological time-keeping, and may allow assessment of how biological rhythms relate to changes in the environment.

Using facial infrared thermography to infer avian body temperatures in the wild

Article

Full-text available

May 2022
MAR BIOL

Studies performed in humans and farm animals indicate that infrared thermography can be used to estimate the body temperature of homeotherms. However, this method has seldom been validated for wild animals in their natural environment. To fill this major gap, we shot facial infrared thermograms of red-footed boobies (Sula sula) in situ, while remotely recording their internal body temperatures. We identified strong linear relationships between the surface temperatures of six facial regions and the internal body temperatures of the birds. At the individual level, maximum facial temperatures, corresponding to the corner of the bill and the internal cantus of the eye, provided the best relationships with internal temperatures. At the species level, minimal and mean temperatures of the eyeballs provided the best estimates of internal temperatures. Wind speed, ambient temperature, sun exposure and shooting distance influenced bird facial surface temperatures as inferred through infrared thermography. Our study underlines the practicability of using facial infrared thermography to infer avian body temperatures, and opens new perspectives for the conservation physiology of wild species.

Torpor During Reproduction and Development

Chapter

Aug 2021

Fritz Geiser

Reproduction and development are energetically expensive and risky processes in most organisms. Animals typically must increase the acquisition of nutrients and energy, which results in high energy expenditure. This may result in increased predator exposure due to more foraging needed by the parents to obtain food for the growing young. In birds and mammals it also often includes an increase in Tb and MR during the mating period or during various stages of the reproductive cycle (Tyndale-Biscoe and Renfree 1987; Monaghan and Nager 1997; Speakman 2008). Generally in small placental mammals, energy expenditure increases with pregnancy, the increase is usually more pronounced after parturition and, during the period of lactation, may about double in comparison to energy expenditure without reproduction (Speakman 2008; Rödel et al. 2016). In monotremes and marsupials the change in energy expenditure during the typically long reproductive period is less pronounced, but it occurs over a longer time (Munks and Green 1995; Nicol 2017). In flying birds and bats extra costs arise from carrying an egg or growing foetus as well as allocating nutrients to the young. Mammalian reproduction is also associated with an increase in circulating reproductive hormones, such as steroids and specifically testosterone, which are known to inhibit torpor in at least some heterothermic species, especially sciurid and cricetid rodents (Goldman et al. 1986), and sperm production is negatively affected by deep torpor (Gagnon et al. 2020). All of these requirements and physiological changes seem to preclude the use of torpor of adults during the reproductive cycle and it is of little surprise that reproduction in birds and mammals and expression of torpor have been widely viewed as mutually incompatible (Landau and Dawe 1960; Wimsatt 1969). This tenet applies especially to areas at high latitudes with strong seasonal cycles of temperature and food availability and only a narrow window of time that is suitable for reproduction, growth and development.

Nocturnal hypothermia and its energetic significance for small birds living in the Arctic and subarctic regions. A review

Article

Full-text available

Dec 1983

Randi Eidsmo Reinertsen

Nocturnal hypothermia is demonstrated in a number of small northern birds. These birds utilize hypothermia among other energy-saving mechanisms and lower the body temperature by some 10°C. In most bird species hypothermia is utilized only in conjunction with a state of inanition. However, hypothermia has also been demonstrated in birds with satisfactory feeding conditions and body weight. For none of the small northern birds utilizing nocturnal hypothermia. is inanition necessary for the induction of a state of hypothermia. A seasonal effect on the hypothermic response has been demonstrated for two species of tits, the black-capped chickadee Parus atricapillus and the willow tit Parus monfanus, and also for an Andean hummingbird. The depth of hypothermia achieved significantly and linearly was correlated with the ambient temperature for the same two species of tits. By the use of nocturnal hypothermia, birds living in temperate zones can save as much as 75% of their energetic costs, compared with their energy consumption at normal body temperature. The reduction in the nightly expenditure of energy is considerable also in small-sized arctic and subarctic birds that utilize nocturnal hypothermia. The saving of energetic costs may easily represent the margin between life and death for such small birds living under the combined stresses of hunger, cold and long nights.

The Influence of Moonlight on the Behavior of Goatsuckers (Caprimulgidae)

Article

Apr 1986

Alexander M. Mills

Whip-poor-wills (Caprimulgus vociferus) showed significantly higher levels of locomotory, vocal, and nest activity during twilight and bright moonlight than under moonless conditions. Field observations and nest record card data indicated that Caprimulgus species usually synchronize their reproductive cycle with the lunar cycle. Hatching tends to occur during young waxing moons, presumably so that moonlight-enhanced foraging will be at a maximum while the dependent nestlings are an energy burden on the parents. Observations of foraging Whip-poor-wills suggest they are primarily visually oriented, unlike the bats (Chiroptera).

Further observations on the hibernation of the poorwill

Article

May 1949

E.C. Jaeger

Oxygen Consumption of Torpid, Resting, Active, and Flying Hummingbirds

Article

Apr 1963
Physiol Zool

Robert C. Lasiewski

The Function of Torpor in Hummingbirds

Article

Jul 1977
Physiol Zool

We constructed estimates of daily energy budgets for male Eugenes fulgens and female Archilochus alexandri from daily time budgets, energetic rate functions, measurements of food intake, and nocturnal oxygen consumption. These budgets permitted us to examine the relationship between net energy gains and the occurrence of torpor. Results indicated that torpor was used only in "energy emergency" situations at a minimum "threshold" of energy reserves and not to reduce nocturnal energy expenditures when net energy gains during the day were sufficient for overnight expenditures.The feeding behavior of hummingbirds together with a threshold model of torpor generates a scheme of daily energy balance which produces the relationship between torpor and reduced net energy gains that is characteristic of several species exhibiting daily torpor. The absence of torpor except in energy emergencies suggests either a loss in energetic efficiency due to torpor or a constraint from entering torpor due to predation or some physiological risk.

Heterothermy and the Use of Torpor by the Bat Eptesicus fuscus (Chiroptera: Vespertilionidae): A Field Study

Article

May 1988
Physiol Zool

Radiotelemetry studies of free-living Eptesicus fuscus demonstrated that the occurrence of daily torpor was influenced by ambient temperature and varied with the reproductive state of the bat. Lactating females were torpid significantly less often than pregnant and nonpregnant bats. Although the bats had the potential for behavioral thermoregulation, there was evidence that they actively controlled entry into and arousal from torpor. For pregnant females, prolonged periods of torpor coincided with prolonged gestation.

Hibernation in Captive Goatsuckers

Article

May 1955
CONDOR

Joe T. Marshall

Evolutionary Alternatives in the Physiological Ecology of Bats

Article

Jan 1982

Brian K Mcnab

Bats are often thought to have poor temperature regulation, to feed on insects, and to enter hibernation. This combination of characteristics is typical only of temperate species. In the last two decades intensive work in the tropics, especially in the New World, has shown the great ecological diversity existing among bats, which in turn permits us to place temperate species in their appropriate ecological and evolutionary perspective and to examine some of the physiological and ecological alternatives available to bats when living in a physically benign environment.

Additional Responses of the Poor-Will to Low Temperatures

Article