Ecological correlates of torpor use among five caprimulgiform birds

Abstract

We review recent studies of torpor use by free-ranging caprimulgiform birds in North America and Australia: common poorwill (45 g), whip-poor-will (55 g), common nighthawk (80 g), Australian owlet-nightjar (50 g), and Tawny Frogmouth (500 g). Reproductive activity, ambient temperature, body size, and prey abundance influence the energy status of endotherms and may be correlated with torpor use under natural conditions; our review suggests that no one factor is most important. To date, most studies have been correlational in the wild, and experimental studies at multiple locales are now needed to resolve uncertainties concerning the evolutionary and ecological significance of torpor.

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Acta Zoologica Sinica
© 2006 Acta Zoologica Sinica
S22-3 Ecological correlates of torpor use among five caprimulgiform
birds
R. Mark BRIGHAM1, Christopher P. WOODS1, Jeffrey E. LANE1, Quinn E. FLETCHER1, Fritz
GEISER2
1. Dept. of Biology, University of Regina, Regina, SK S4S 0A2, CANADA; mark.brigham@uregina.ca;
ChrisWoods@velocitus.net; jelane@ualberta.ca; fletcher@utsc.utoronto.ca
2. Dept. of Zoology, BBMS, University of New England, Armidale, NSW 2351, Australia; fgeiser@metz.une.edu.au
Abstract We review recent studies of torpor use by free-ranging caprimulgiform birds in North America and Australia:
common poorwill (45 g), whip-poor-will (55 g), common nighthawk (80 g), Australian owlet-nightjar (50 g), and Tawny
Frogmouth (500 g). Reproductive activity, ambient temperature, body size, and prey abundance influence the energy status of
endotherms and may be correlated with torpor use under natural conditions; our review suggests that no one factor is most
important. To date, most studies have been correlational in the wild, and experimental studies at multiple locales are now
needed to resolve uncertainties concerning the evolutionary and ecological significance of torpor.
Key words Torpor, Caprimulgiformes, Ecology, Energetics, Temperature, Foraging
1 Introduction
Endothermy is a process of thermoregulation charac-
terized by a high, controlled rate of heat production which
helps mammals and birds maintain an elevated body tem-
perature (Tb; IUPS Thermal Commission, 2001). While a
constant elevated Tb provides a thermally stable internal
environment for optimizing physiological functions, it re-
quires a metabolic rate (MR) 10–30 times (Nagy et al.,
1999) greater than the standard MR of ectothermic reptiles.
The cost is especially pronounced in small endotherms,
which lose most endogenously produced heat to the envi-
ronment (Song et al., 1998). To conserve energy or other
resources, many mammals and a growing list of birds aban-
don normal elevated Tb. Such facultative heterothermy or
torpor is a physiological state characterized by reduced MR
and Tb. To date, the vast majority of studies have focused
on the ability of mammals to reduce energy expenditure
through daily or seasonal bouts of torpor (hibernation;
Geiser and Ruf, 1995). Prolonged torpor of 1–3 weeks by
hibernators typically occurs during winter at low ambient
temperatures (Ta; Geiser, 1998). In contrast to hibernation,
daily torpor is employed at a variety of Tas and throughout
the year (Geiser, 1998).
Until recently, birds were thought to be less prone to
use torpor than mammals (McKechnie and Lovegrove,
2002). Daily torpor has now been recorded from seven or-
ders of birds, most commonly in hummingbirds (Trochilidae;
Calder and Booser, 1973; Calder, 1994; Bech et al., 1997)
and nightjars (Caprimulgiformes; Bartholomew et al., 1957;
Peiponen, 1966; Reinertsen, 1983). In both orders, daily
torpor bouts typically last several hours, Tb dropping by 4–
35°C and metabolic rate by 5%–90%. “Hibernation” has
been anecdotally reported for only one species, the com-
mon poorwill (Jaeger, 1948; 1949). The factors that prompt
birds to use torpor or hibernation, however, remain unclear.
Daily torpor and hibernation appear to be outwardly
similar among birds and mammals, except for greater re-
ported frequency in mammals (McKechnie and Lovegrove,
2002). Reinertsen (1983) postulated that the apparent rarity
of torpor in birds might be related in part to migration, which
allows them to avoid adverse weather conditions and pro-
longed food shortages. Geiser (1998) recently addressed
the evolution of torpor and concluded that in birds, unlike
mammals, it occurs in modern rather than ancestral orders,
suggesting that it is not an ancestral avian condition.
However, there are qualitative similarities in ecology, and
morphology and physiology between heterothermic birds
and mammals. For example, torpor in both groups appears
most commonly in small, temperate-zone species that ex-
ploit a fluctuating food supply (e.g., nectar and insects;
Reinertsen, 1983). This suggests that predictable ecologi-
cal constraints, resulting in periodic energy shortfalls, rep-
resent important selection pressures for both groups.
Thus the purpose of our paper is to review hypotheses,
drawn from the mammalian literature, concerning
ecological, behavioral and morphological determinants that
may account for patterns of torpor use by birds. We also
review recent data for five species of free-ranging noctur-
nal caprimulgiforms and specifically address the influence
of body size, Ta, prey availability, foraging strategy, and
reproductive activity on torpor use (Table 1).
52(Supplement): 401–404, 2006

Acta Zoologica Sinica
402
2 Torpor occurrence in five
caprimulgiform birds
2.1 Common poorwill (Phalaenoptilus nuttallii)
Outside of the breeding season, bouts of daily torpor
are routinely used by common poorwills (45 g) throughout
their range in western North America (Brigham, 1992; Csada
and Brigham, 1994; Woods, 2002). Both sexes typically for-
age for 30–240 minutes after dusk before entering torpor
and remain in torpor throughout the night, foregoing a for-
aging bout at dawn. Torpor bouts typically last 8–12 h, with
arousals triggered by increasing Ta the following morning.
In Arizona, most birds use torpor when minimum Ta falls
below 10°C; and there is a clear relationship between Ta and
the abundance of flying insects (Woods, 2002). On a given
night, however, some individuals remain euthermic whereas
others fall into torpor (Brigham, 1992; Woods, 2002). Indi-
viduals of both sexes rarely enter torpor when incubating
and brooding (Brigham, 1992; Kissner and Brigham, 1993;
Csada and Brigham, 1994; Woods, 2002).
Jaeger (1948, 1949) reported that some poorwills in
the southern California desert remain in the same location
for weeks during winter, and was the first to suggest that
they hibernate. French (1993) characterized such hiberna-
tion as “seasonal dormancy” based on individuals remain-
ing inactive for prolonged periods without foraging. Woods
(2002) followed radio-tagged birds near Tucson, Arizona,
and found a range of thermoregulatory and behavioral re-
sponses to low Ta. Some individuals remained inactive for
weeks without interruption. Inactive birds used deep torpor
every day but invariably warmed to near euthermic levels
on sunny days, principally due to exposure to solar radiation.
However, when inactive birds were shaded to prevent solar
exposure, birds aroused about every five days using endog-
enous heat, resembling the periodic arousal pattern of clas-
sic mammalian hibernators. This suggests that periodic
arousals may be common to both birds and mammals, but
that birds rely more on an exogenous heat source to facili-
tate re-warming and reduce arousal costs.
2.2 Common nighthawk (Chordeiles minor)
High mortality in captive birds forced into torpor (3
of 4; Lasiewski and Dawson, 1964), and a lack of evidence
for it in free-ranging common nighthawks (80 g) in British
Columbia, Canada (Firman et al., 1993), suggests that tor-
por is not used regularly by this species. Brigham et al.
(1995) anecdotally reported torpor in two nighthawks, and
Fletcher et al. (in review) found two free-ranging birds in
southwest Saskatchewan, Canada, using shallow torpor at
night during late August prior to migration. Taken together,
these observations suggest that while nighthawks can enter
shallow torpor if stressed, they probably do not normally
use heterothermy for conserving energy.
2.3 Whip-poor-will (Caprimulgus vociferus)
Whip-poor-wills (55 g) are marginally larger than
poorwills and are found throughout deciduous woodlands
in eastern North America. A short-term study in Ontario
failed to record torpor (Hickey, 1993), but Lane (2002),
working in southeast South Dakota, recorded occasional
torpor use in spring (May) and fall (September) by both
sexes, beginning at dawn. The lowest body temperature re-
corded was about 18°C. Passive re-warming by the sun ap-
peared to be important but not essential for re-warming.
2.4 Australian owlet-nightjar (Aegotheles cristatus)
The Australian owlet-nightjar (50 g) is ubiquitous in
Australian woodlands where it roosts in cavities that may
offer protection from predators and greater thermal stabil-
ity than exposed roosts (Brigham et al., 1998). Free-rang-
ing birds regularly use shallow bouts of torpor during win-
ter (May–September) near Armidale NSW (Brigham et al.,
2000) but not during the breeding season (October to
January). Like whip-poor-wills, owlet-nightjars rarely use
torpor during normal activity at night; most (95%) torpor
bouts begin at dawn (Geiser et al., this symposium).
No Ta threshold delineates days on which owlet-night-
jars do or do not enter daytime torpor. The individual moni-
tored over the winter of 1998 used torpor every morning
for 64 consecutive days from June–August, despite vari-
able minimum Tas from –7 to 11°C (Brigham et al., 2001). The
regularity of torpor implies that it is used for more than
energetic emergencies (sensu Carpenter and Hixon, 1988).
Night torpor was uncommon and then only on very cold
nights (Ta < 5°C). This, when combined with data on activity,
suggests that foraging is profitable on most nights (Brigham
et al., 1999).
2.5 Tawny frogmouth (Podargus strigoides)
Despite avoiding torpor in the laboratory (Bech and
Nicol, 1999), free-ranging tawny frogmouths (500 g) regu-
larly use shallow torpor in bouts about 7 hours after forag-
ing at dusk (Körtner et al., 2000, 2001). At dawn, frogmouths
re-warmed and resumed foraging or moved to new roosts
and re-entered torpor (Körtner and Geiser, 1999). The mini-
Mass (g) Roost Foraging Torpor use Depth Duration Timing
Common poorwill 45 Ground Sally Common Deep > One day Night
Whip-poor-will 55 Ground Sally Rare Shallow Hours Morning
Common nighthawk 80 Ground/branch Hawk Very rare Very shallow Hours Night
Aust. owlet-nightjar 50 Cavity Sally/walk Common Shallow Hours Morning
Tawny frogmouth 500 Branch Sally/pounce Common Shallow Hours Night
Table 1 Summary of data on life history and thermoregulatory parameters for five free-ranging caprimulgiform birds

403
mum Tb of frogmouths was about 29°C. Its timing was mark-
edly different from that in owlet-nightjars, although the stud-
ies were done at the same time of year at the same site.
3 Ecological determinants
3.1 Body size
It is generally thought that small animals are more
likely to use deep torpor than large ones because of their
large surface area to volume ratio (Geiser, 1998). This as-
sumption is not supported by the data for tawny frogmouths
(Körtner et al., 2000, 2001). Recent work on geese and pi-
geons corroborates the finding that large birds do use tor-
por (Butler and Woakes, 2001; Schleucher, 2001). These
discoveries demonstrate that body size does not account
for patterns of torpor in birds alone. Future studies of other
large caprimulgiform birds are imperative. Clearly, the ener-
getic savings of torpor need to be treated as an integrative
function because depth, duration and frequency of bouts all
influence the energy savings. Thus, while deep torpor ap-
pears restricted to small endotherms, shallow bouts appear
important for the energy budgets of larger species.
3.2 Breeding
The five caprimulgiforms studied in the field to date
rarely use torpor when nesting. It is not clear whether this
reflects active avoidance of torpor by reproducing birds, or
a consequential result of usually greater abundance of prey
and more favorable weather during the nesting period. High
concentrations of particular hormones (e.g., testosterone)
were thought to be incompatible with the regular use of
seasonal or daily torpor in mammals (Lee et al., 1990), al-
though this does not appear true for bats, ecologically per-
haps most similar to caprimulgids (Willis, 2006). In birds,
prolonged bouts of torpor may compromise the develop-
ment of embryos and chicks (Webb, 1987; Csada and
Brigham, 1994), in connection with which the non-incubat-
ing member of a breeding pair will occasionally use torpor
during the nesting period (Woods, 2002). Laboratory and
field studies addressing torpor use by animals living in rela-
tively non-seasonal climates will help to separate the effect
of reproduction from Ta as proximate determinants of torpor
use.
3.3 Foraging strategy
Of the five caprimulgiforms so far known to use tor-
por naturally, four are strictly nocturnal; nighthawks are
mostly crepuscular. Whip-poor-wills, poorwills and owlet-
nightjars sally after prey, owlet-nightjars also searching for
it while walking on the ground. Frogmouths commonly
pounce on terrestrial arthropods while nighthawks catch
flying insects on the wing. Apart from an insectivorous life-
style, there is no obvious connection between torpor use
and foraging strategy in these birds. Furthermore, foraging
style does not explain the differences in timing of torpor
bouts (Table1). In this context, studies that address the
importance of Ta and roost selection to facilitate passive re-
warming are needed.
3.4 Ambient temperature and prey abundance
Among endotherms generally and in caprimulgiforms
specifically, torpor is assumed to represent an energy sav-
ing strategy to cope with low Ta. However, most studies
have been conducted in temperate areas where it is difficult
to separate Ta and prey abundance as proximate factors.
Furthermore, most studies make no attempt to measure prey
abundance. In a tantalizing experiment, Woods (2002)
erected lights to create prey concentrations within the terri-
tories of poorwills. Despite a small sample size, he found
that poorwills occupying territories with prey concentra-
tions entered torpor less often than controls. Experimental
studies like this, especially at sites that remain warm year-
round, hold promise for teasing apart the ecological basis
for torpor use.
In conclusion, this review suggests that no single
ecological, behavioral or morphological factor single-
handedly explains patterns of torpor observed in free-rang-
ing birds. Rather, it seems that the interactive effects of a
number of environmental and evolutionary constraints com-
bine to shape avian heterothermy. We suggest that three
approaches will be useful for futures studies. First, experi-
mental manipulations such as hormone treatment and shad-
ing of roosts, secondly, comparative studies of sympatric
species to address the importance of phylogeny, and thirdly,
data from tropical species and wide-ranging conspecifics.
Acknowledgements We gratefully acknowledge the finan-
cial support of the Natural Sciences and Engineering Re-
search Council, Canada, and the Australian Research
Council. G. Körtner, D. Gummer and C. Willis provided
constructive comments on drafts of the paper.
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