FEATURE ARTICLES
The Condor 104:705–724
q The Cooper Ornithological Society 2002
AVIAN FACULTATIVE HYPOTHERMIC RESPONSES: A REVIEW
ANDREW E. MCKECHNIE1
AND
BARRY G. LOVEGROVE
School of Botany and Zoology, University of Natal, Private Bag X01, Scottsville 3209, South Africa
Abstract. Recent evidence suggests that avian facultative hypothermic responses are
more common, and occur in a wider variety of ecological contexts, than previously thought.
The capacity for shallow hypothermia (rest-phase hypothermia) occurs throughout the avian
phylogeny, but the capacity for pronounced hypothermia (torpor) appears to be restricted to
certain taxa. Families in which torpor has been reported include the Todidae, Coliidae,
Trochilidae, Apodidae, Caprimulgidae, and Columbidae. Facultative hypothermia occurs in
species ranging in body mass (Mb) from ,3 g to ca. 6500 g. Minimum body temperature
(Tb) during hypothermia is continuously distributed from 4.38C to ca. 388C. The physiological distinction between torpor and rest-phase hypothermia is unclear. Whereas these two
responses have traditionally been distinguished on the basis of Tb, we find little support for
the biological reality of specific Tb limits. Instead, we argue that emphasis should be placed
on understanding the relationship between metabolic and Tb reduction and the capacity to
respond to external stimuli. Patterns of thermoregulation during avian hypothermic responses
are relatively variable, and do not necessarily follow the entry–maintenance–arousal patterns
that characterize mammalian responses. Avian hypothermic responses are determined by a
suite of ecological and physiological determinants including food availability, ambient temperature, hormone levels, and breeding cycle.
Key words: body size, body temperature, ecological determinants, hypothermia, phylogeny, torpor.
Respuestas Facultativas de la Hipotermia en Aves: Una Revisión
Resumen. Evidencias recientes sugieren que las respuestas facultativas de la hipotermia
aviar son más comunes y ocurren en una gran cantidad de contextos ecológicos, a diferencia
de lo que anteriormente se pensaba. La capacidad de una hipotermia ligera (hipotermia de
descanso) ocurre en toda la filogenia de las aves, pero la capacidad de mantener una hipotermia pronunciada (torpor) aparece sólo en ciertos taxones. El torpor ha sido reportado
en las familias Todidae, Coliidae, Trochilidae, Apodidae, Caprimulgidae y Columbidae. La
hipotermia facultativa ocurre en especies con un peso corporal (Mb) de ,3 g hasta 6.5 kg.
Durante la hipotermia, la temperatura mı́nima corporal (Tb) está distribuı́da contı́nuamente
entre 4.38C y 388C. La diferencia fisiológica entre el torpor y la hipotermia de descanso no
es clara. Tradicionalmente se ha reconocido que las dos respuestas se basan en la Tb. Sin
embargo, nosotros encontramos pocas evidencias biológicas sobre lı́mites especı́ficos de la
Tb. Por el contrario, nosotros argumentamos que el énfasis debe enfocarse en la relación
entre la reducción metabólica y de Tb y la capacidad de responder a estı́mulos externos. Los
patrones de termoregulación de las respuestas hipotérmicas de las aves son relativamente
variables y no necesariamente siguen los patrones de entrada-mantenimiento-elevación que
caracterizan estas respuestas en los mamı́feros. Las respuestas de la hipotermia en aves están
determinadas por la interacción entre factores ecológicos y fisiológicos como disponibilidad
de alimentos, temperatura ambiental, niveles hormonales y ciclo reproductivo.
Manuscript received 14 January 2002; accepted 25 June 2002.
Present address: Department of Biology, 167 Castetter Hall, University of New Mexico, Albuquerque, NM
87131-1091. E-mail: [email protected]
1
[705]
706
ANDREW E. MCKECHNIE
AND
BARRY G. LOVEGROVE
INTRODUCTION
Birds are endothermic homeotherms, and maintain a high body temperature (Tb) by means of
endogenous metabolic heat production. Whereas
a constant high Tb confers fundamental physiological advantages, the elevated metabolic rates
associated with endothermic homeothermy often
represent a substantial cost. These high metabolic costs can potentially be offset by a variety
of behavioral and physiological mechanisms,
such as microhabitat selection, communal roosting, facultative hypothermic responses, and
adaptive changes in metabolic traits (Dawson
and Whittow 2000). In this paper, we review the
occurrence of facultative hypothermia, which
constitutes an important proximate response to
increased thermoregulatory demands or reduced
energy availability, particularly in small species
with high mass-specific energy requirements
(Prinzinger et al. 1991, Reinertsen 1996). Such
facultative hypothermic responses involve an increase in the amplitude of circadian Tb cycles
during which rest-phase (r) Tb is decreased below normothermic levels (Prinzinger et al. 1991,
Reinertsen 1996).
Recent studies suggest that facultative hypothermic responses may be widespread among
birds, and may play a more important role in
avian physiological ecology than was previously
thought. For instance, telemetric studies of thermoregulation in free-ranging caprimulgids indicate that hypothermia is used routinely by Common Poorwills (Phalaenoptilus nuttallii), Australian Owlet-Nightjars (Aegotheles cristatus)
and Tawny Frogmouths (Podargus strigoides;
Brigham 1992, Brigham et al. 2000, Körtner et
al. 2000). Moreover, avian hypothermic responses occur over a larger range of Mb than previously suspected (Körtner et al. 2000, Butler and
Woakes 2001, Schleucher 2001).
The facultative hypothermic responses exhibited by endotherms are commonly categorized
by physiological parameters such as bout length,
minimum Tb, and the extent of metabolic reduction (Geiser and Ruf 1995). The physiological
parameters of avian hypothermia are in many
cases consistent with those of mammalian daily
torpor (Geiser and Ruf 1995). In addition, the
Common Poorwill exhibits multiday torpor
bouts similar to mammalian hibernation (Jaeger
1948, 1949, Brigham 1992). However, several
bird species exhibit relatively shallow hypother-
mia during which Tb is reduced by less than
108C below normothermic levels (Prinzinger et
al. 1991, Reinertsen 1996). This hypothermic response does not appear to occur in mammals and
is referred to as rest-phase hypothermia (Reinertsen 1996) or controlled rest-phase hypothermia (Prinzinger et al. 1991).
The distinction between rest-phase hypothermia and torpor remains controversial. Prinzinger
et al. (1991) and Reinertsen (1996) have argued
that the criteria for torpor, namely a state of inactivity and reduced responsiveness to external
stimuli (Bligh and Johnson 1973), are met below
specific levels of Tb. Whereas Prinzinger et al.
(1991) argued that Tb , 258C indicates torpor,
Reinertsen (1996) suggested that the criteria for
torpor are usually met at Tb , 308C. However,
it is unclear whether avian rest-phase hypothermia and daily torpor represent discrete physiological phenomena or components of a hypothermic response continuum (Prinzinger et al.
1991, Reinertsen 1996). Moreover, little effort
has been made to differentiate between these responses using physiological parameters such as
minimum Tb or the extent of metabolic reduction.
In this paper, we use the term ‘‘facultative hypothermic responses’’ (or ‘‘hypothermia’’ for
convenience) to include hibernation, torpor, and
rest-phase or controlled hypothermia. This term
describes both the pattern (Tb below normothermic levels) and the mechanism (facultative, regulated Tb reduction, as opposed to unavoidable,
pathological hypothermia) involved.
The objectives of this study were (a) to review
the occurrence, patterns and proximate determinants of avian hypothermia, and (b) to assess
the validity of the widely accepted distinction
between avian daily torpor and rest-phase hypothermia using parameters such as Mb and minimum hypothermic Tb.
METHODS
Records of facultative hypothermic responses
are currently available for 95 avian species (Table 1). From these sources, we obtained as many
of the following data as possible: Mb, normothermic Tb (Tnorm), minimum Tb during hypothermia (Tmin), minimum oxygen consumption
(V̇O2min) during hypothermia, as well as information regarding the apparent proximate determinant(s) of hypothermia. In cases where Mb
was not provided, we obtained it from Dunning
AVIAN FACULTATIVE HYPOTHERMIC RESPONSES
(1993). Initially, we attempted to obtain mean
values for Tmin for each species. However, many
studies did not calculate a mean Tmin value, and
hence we used the lowest Tmin observed in birds
that were able to arouse spontaneously without
any apparent adverse effects. We used Sibley
and Ahlquist’s (1990) average linkage (UPGMA) phylogeny for avian orders and families,
and obtained taxonomic and distribution data
from Sibley and Monroe (1990), as well as regional field guides.
RESULTS AND DISCUSSION
PHYLOGENETIC DISTRIBUTION
Facultative hypothermic responses have been reported in species from 29 families representing
11 orders (Fig. 1). However, the capacity for hypothermia in the majority of the 138 avian families remains unknown. In the infraclass Eoaves,
shallow hypothermia has been reported in two
species (Japanese Quail [Coturnix coturnix] and
Barnacle Goose [Branta leucopsis]; Fig. 1).
However, many species in the Eoaves are large
and their capacity for hypothermia during a single circadian cycle is presumably constrained by
large Mb (Prothero and Jürgens 1986, Geiser
1998). Within the infraclass Neoaves the capacity for moderate hypothermia, during which Tb
is reduced by ,208C, occurs throughout the
phylogeny (Fig. 1). On the other hand, more
pronounced hypothermia during which Tb is reduced by 208C or more has been reported in only
the Trochilidae, Apodidae, and Caprimulgidae
(Fig. 1).
The passerine capacity for hypothermia is
limited, and Tb reduction of .108C below normothermic levels has been reported in only 7 of
28 species for which measurements of Tmin exist.
The lowest values of Tmin in passerines were recorded in the Hirundinidae and Nectariniidae
(Fig. 1; Table 1). In addition, Bartholomew et
al. (1983) calculated a Tb of 26.88C from V̇O2
measurements in a Golden-collared Manakin
(Tyrannidae: Manacus vitellinus).
The capacity for facultative hypothermia
shows considerable variation within the Strigiformes. Body temperature reduction of more
than 6–88C has not been observed in owls (Strigidae and Tytonidae), and hypothermia may be
absent altogether in Tengmalm’s Owl (Aegolius
funereus; Hohtola et al. 1994). In contrast, Tb
reduction of more than 108C appears to be wide-
707
spread in the Caprimulgidae and allies (Podargidae, Eurostopodidae, and Aegothelidae).
Moreover, the Caprimulgidae include the only
known avian hibernator, the Common Poorwill
(Jaeger 1948, 1949, Brigham 1992).
The limited data (ca. 1% of extant species)
are insufficient to objectively infer general patterns in the phylogenetic distribution of the avian capacity for hypothermia, or to reconstruct
the traits of hypothetical ancestors using phylogenetic comparative methods (Garland and Ives
2000). At best, the available data suggest that
the capacity for pronounced hypothermia (i.e.,
torpor) increases with the relative age of taxa
(Fig. 1). However, data on hypothermic responses in the older Neoaves (e.g., Piciformes and
Upupiformes) are necessary to confirm this observation.
A pattern of more pronounced hypothermia in
phylogenetically older taxa is consistent with
current ideas regarding the evolution of heterothermy (daily torpor and hibernation). Malan
(1996) has argued that heterothermy may be
phylogenetically primitive, although it frequently constitutes a functionally advanced adaptation
associated with small body size and unpredictable food supplies (Geiser 1998). A plesiomorphic, monophyletic origin of heterothermy, as
proposed by Malan (1996), predicts that heterothermy should be more widespread and pronounced in phylogenetically older taxa. Observations of daily torpor in the Macroscelidae (elephant shrews), a relatively old mammalian
family, suggest a plesiomorphic origin of mammalian daily torpor (Lovegrove et al. 1999).
Moreover, patterns of thermoregulation in two
species of mousebird appear to represent an intermediate step in Malan’s (1996) hypothesized
origin of heterothermy, and provide circumstantial support for this hypothesis (McKechnie and
Lovegrove 2000).
It should be noted that the above interpretation relies on the assumption that the Sibley and
Ahlquist (1990) phylogeny provides a reasonably accurate description of avian phylogenetic
relationships. The Sibley and Ahlquist (1990)
phylogeny is widely accepted and is used routinely in comparative studies of avian energetics
(e.g., Reynolds and Lee 1996, Tieleman and
Williams 2000, Rezende et al. 2002). However,
the phylogeny has been criticized on several
grounds (Mayr 1989, Peterson 1992) and remains controversial. Mapping the above data
Neomorphidae
Greater Roadrunner
Geococcyx californianus
Crotophaga ani
Urocolius macrourus
Blue-naped Mousebird
Cuculiformes
Crotophagidae
Smooth-billed Ani
Urocolius indicus
Red-faced Mousebird
295
113
49
53
51
Colius striatus
6.2
1890
58
35.1
Todus mexicanus
Coraciiformes
Todidae
Puerto Rican Tody
156
38.4
37.9
38.6
36
38.5
35
36.3
40.1
40.5
Tnorm
(8C)
33
32.6
22
18.2
20
26
26
35.1
36.5
Tmin
(8C)
5.4
15.9
17.8
18.5
9
10.3
5
5
0.79
0.83
1.20
3.24
0.65
0.67
0.11
0.09
3.10
17.4
86.8
92.5
4.3
Nearc
Neo
Afro
Afro
Afro
Afro
Afro
Neo
Pal
Pal
Zone
Ohmart and Lasiewski
1971, Vehrencamp
1982
Warren 1960
Prinzinger et al. 1981
McKechnie and Lovegrove 2001a
McKechnie and Lovegrove 2001b
Hoffmann and Prinzinger
1984
Hoffmann and Prinzinger
1984, Schaub et al.
1999
Merola-Zwartjes and Ligon 2000
Butler and Woakes 2001
Hohtola et al. 1991
Reference(s)
AND
Colius castanotus
Colius colius
Branta leucopsis
Anseriformes
Anatidae
Barnacle Goose
Mb (g)
ANDREW E. MCKECHNIE
Coliiformes
Coliidae
Red-backed Mousebird
White-backed Mousebird
Speckled Mousebird
Coturnix coturnix
Galliformes
Phasianidae
Japanese Quail
Species
BMR V̇O2min
Tnorm (mL O2 (mL O2
Reduc2 Tmin
g21
g21
(8C)
hr21)
hr21) tion (%)
TABLE 1. Avian species known to use facultative hypothermia. Where possible, data include body mass (Mb), normothermic body temperature (Tnorm), minimum hypothermic body temperature (Tmin), Tnorm 2 Tmin, basal metabolic rate (BMR), minimum oxygen consumption during hypothermia (V̇O2min), metabolic reduction (V̇O2min as
percentage of BMR) and the zoogeographical zone in which the species occurs. Taxonomy follows Sibley and Monroe (1990). Zone abbreviations: Afro 5 Afrotropics,
Aus 5 Australasia, Indo 5 Indomalaya, Nearc 5 Nearctic, Neo 5 Neotropics, Pal 5 Palearctic.
708
BARRY G. LOVEGROVE
Species
Continued.
Swallow-tailed Hummingbird
White-necked Jacobin
White-chinned Sapphire
Blue-throated Hummingbird
Black Jacobin
Booted Racket-tail
Ecuadorian Hillstar
Andean Hillstar
Costa’s Hummingbird
Blue-chinned Sapphire
Blue-tailed Emerald
Golden-tailed Sapphire
Magnificent Hummingbird
Purple-throated Carib
Trochiliformes
Trochilidae
White-bellied Woodstar
Shining Sunbeam
Plain-bellied Emerald
Versicolored Emerald
Black-throated Mango
Black-chinned Hummingbird
Chestnut-breasted Coronet
Anna’s Hummingbird
Apodiformes
Apodidae
Common Swift
White-throated Swift
TABLE 1.
8.6
6.9
3
8
7.7
2.7
8.1
8.5
Eupetomena macroura
Florisuga mellivora
Hylocharis cyanus
Lampornis clemenciae
Melanotrochilus fuscus
Ocreatus underwoodii
Oreotrochilus chimborazo
Oreotrochilus estella
8
Eulampis jugularis
3.4
Calypte anna
3.2
3
2.9
5
8
7.2
Boissonneaua matthewsii
Calypte costae
Chlorestes notatus
Chlorostilbon mellisugus
Chrysuronia oenone
Eugenes fulgens
3.3
7.2
4
4.1
7.7
3.2
42
31
Acestrura mulsant
Aglaeactis cupripennis
Amazilia leucogaster
Amazilia versicolor
Anthracothorax nigricollis
Archilochus alexandri
Apus apus
Aeronautes saxatilis
Mb (g)
24.7
18
6.5
35.7
18
31
19.6
23.2
18
9
31
18
18
10
8.8
18
32
23.8
18
13.5
20.1
17
Tmin
(8C)
37.3
39
35.7
37.1
35
38.8
38
38.8
39.4
36.8
38.6
Tnorm
(8C)
29.2
12.6
21
16.1
13.9
17
7.8
25.3
7.4
13
21.6
3.03
3.85
3.53
0.75
0.45
1.00
2.05
0.50
0.38
0.17
0.20
87.4
95.6
94.3
BMR V̇O2min
Tnorm– (mL O2 (mL O2
g21
g21
Tmin
Reduc(8C)
hr21)
hr21) tion (%)
Neo
Neo
Neo
Neo
Neo
Neo
Neo
Neo
Neo
Nearc
Neo
Neo
Neo
Neo
Nearc
Neo
Neo
Neo
Neo
Neo
Neo
Nearc
Pal
Nearc
Zone
Bech et al. 1997
Krüger et al. 1982
French and Hodges 1959
Carpenter 1974, Krüger
et al. 1982
Krüger et al. 1982
Morrison 1962
Krüger et al. 1982
Bartholomew 1957, Lasiewski 1963
Lasiewski 1963, 1964
Morrison 1962
Krüger et al. 1982
Krüger et al. 1982
Wolf and Hainsworth
1972
Hainsworth and Wolf
1970
Bech et al. 1997
Krüger et al. 1982
Krüger et al. 1982
Krüger et al. 1982
Morrison 1962
Bech et al. 1997
Krüger et al. 1982
Lasiewski 1963, 1964
Koskimies 1948
Bartholomew et al. 1957
Reference(s)
AVIAN FACULTATIVE HYPOTHERMIC RESPONSES
709
3.3
Selasphorus rufus
Selasphorus sasin
Urosticte benjamini
Allen’s Hummingbird
Purple-bibbed Whitetip
Podargus strigoides
Eurostopodus argusa
Chordeiles acutipennis
Chordeiles minor
Caprimulgus europaeus
Caprimulgus vociferus
Phalaenoptilus nuttallii
Eurostopodidae
Spotted Eared-Nightjar
Caprimulgidae
Lesser Nighthawk
Common Nighthawk
Eurasian Nightjar
Whip-poor-will
Common Poorwill
Aegotheles cristatus
Nyctea scandiaca
Podargidae
Tawny Frogmouth
Aegothelidae
Australian Owlet-Nightjar
Strigidae
Snowy Owl
Tyto alba
19
4
3.4
Patagona gigas
Trochilus polytmus
Selasphorus platycerus
69
55
35
49.9
72.5
88
500
40
2032
316
3.9
39.1
37.4
39.5
37
40.5
36
38.6
39.6
38
38.8
38.7
7
18.5
4.3
15.7
18
29.6
27.2
22
32.6
35.5
28
22
13
6.5
18
10
20.8
Tmin
(8C)
34.8
30.4
23.8
19
10.9
8.8
6
4.1
10
25.8
32.2
18.2
0.83
3.80
3.35
6.01
0.40
1.24
0.43
0.50
1.25
73.0
51.8
67.4
87.2
79.2
Zone
Pal
Nearc
Nearc
Nearc, Neo
Nearc
Aus
Aus
Aus
Pal, Nearc
All
Neo
Nearc
Nearc
Neo
Neo
Nearc
Neo
Neo
Reference(s)
Marshall 1955
Lasiewski and Dawson
1964
Peiponen 1966
Lane 2002
Withers 1977, Brigham
1992
Dawson and Fisher 1969
Körtner et al. 2000
Brigham et al. 2000
Gessaman and Folk 1969
Thouzeau et al. 1999
Lasiewski 1963, Hiebert
1990
Morrison 1962, Lasiewski 1963
Krüger et al. 1982
Wolf and Hainsworth
1972
Krüger et al. 1982
Krüger et al. 1982
Calder and Booser 1973
Krüger et al. 1982
AND
Strigiformes
Tytonidae
Barn Owl
5
Panterpe insignis
39
Tnorm
(8C)
BMR V̇O2min
Tnorm– (mL O2 (mL O2
Tmin
Reducg21
g21
(8C)
hr21)
hr21) tion (%)
ANDREW E. MCKECHNIE
3
2.9
Mb (g)
Orthorhynchus cristatus
Species
Continued.
Antillean Crested Hummingbird
Fiery-throated Hummingbird
Giant Hummingbird
Streamertail
Broad-tailed Hummingbird
Rufous Hummingbird
TABLE 1.
710
BARRY G. LOVEGROVE
Species
Continued.
Perisoreus canadensis
Artamus cyanopterus
Corvidae
Dusky Woodswallow
Gray Jay
Lichenostomus virescens
Lichmera indistincta
Meliphagidae
Singing Honeyeater
Brown Honeyeater
75.6
24.6
13
12.3
Pipra mentalis
55.3
2230
15.5
Oceanodroma furcatac
Procellariidae
Fork-tailed Storm-Petrel
117.7
6580
200
38
36
150
44
375
Mb (g)
Manacus vitellinusd
Cathartes aura
Ciconiidae
Turkey Vulture
Passeriformes
Tyrannidae
Golden-collared Manakin
Red-capped Manakin
Falco sparverius
Falconidae
American Kestrel
Gyps fulvus
Drepanoptila holosericea
Geopelia cuneata
Oena capensis
Streptopelia roseogriseab
Cloven-feathered Dove
Diamond Dove
Namaqua Dove
African Collared-Dove
Ciconiiformes
Accipitridae
Eurasian Griffon
Columbina inca
Columba livia
Inca Dove
Columbiformes
Columbidae
Rock Dove
TABLE 1.
39
37.9
37.9
38
39.3
37.9
37.7
38.6
38.4
38.5
39
39.9
Tnorm
(8C)
36.5
29
29
26.8
10.6
34
38.3
35.3
24.8
35.3
34.4
32
28.5
35
Tmin
(8C)
2.5
10.7
8.9
11.1
4
1
2.6
12.9
3.3
4
6.5
10.5
4.9
2.84
2.25
1.80
0.95
1.21
2.69
0.27
0.72
20.8
33.1
22.0
62.2
BMR V̇O2min
Tnorm– (mL O2 (mL O2
g21
g21
Tmin
Reduc(8C)
hr21)
hr21) tion (%)
Nearc
Aus
Aus
Aus
Neo
Neo
Pelagic
Nearc, Neo
Nearc
Pal
Aus
Aus
Afro
Afro
Nearc
Pal
Zone
Maddocks and Geiser
1999
Waite 1991
Collins and Briffa 1984
Collins and Briffa 1984
Bartholomew et al. 1983
Bartholomew et al. 1983
Boersma 1986
Heath 1962
Shapiro and Weathers
1981
Bahat et al. 1998
Graf et al. 1989, Rashotte et al. 1995
MacMillen and Trost
1967
Schleucher 2001
Schleucher 1994
Schleucher 2001
Walker et al. 1983
Reference(s)
AVIAN FACULTATIVE HYPOTHERMIC RESPONSES
711
16.5
7.3
11
Nectarinia famosa
Nectarinia mediocris
Nectarinia tacazze
Amadina erythrocephala
Passer domesticus
Passer montanus
Passeridae
Red-headed Finch
House Sparrow
Eurasian Tree Sparrow
21.5
27.3
22
7
11
16
14.6
14.2
Nectarinia chalybea
Zosterops lateralis
Hirundo rustica
Riparia riparia
Tachycineta thalassina
Nectariniidae
Lesser Double-collared
Sunbird
Malachite Sunbird
Eastern Double-collared
Sunbird
Tacazze Sunbird
Zosteropidae
Silvereye
Barn Swallow
Sand Martin
Violet-green Swallow
14.8
22
11.13
39.6
39.5
37.3
37.5
38.9
38.4
39
38.9
38.6
Tnorm
(8C)
34.8
35
30
27
25.4
24
23.3
35.2
27
31.6
25.7
32.5
30
32.1
29
33.8
35
Tmin
(8C)
4.8
14.1
13.3
5.9
13.2
5.9
10
5.1
3.6
20.0
Afro
Pal
Pal, Indo
Afro
Afro
Afro
Afro
Aus
All
All
Nearc
Aus
Pal, Nearc
Pal
Nearc
Pal
Pal
Nearc
Pal
Zone
McKechnie 2001
Steen 1958
Steen 1958
Cheke 1971
Leon and Lighton, unpubl. data
Downs and Brown 2002
Cheke 1971
Maddocks and Geiser
1997
Serventy 1970
Prinzinger and Siedle
1988
Keskpaik 1981
Keskpaik 1972
Lasiewski and Thompson
1966
Chaplin 1976, Grossman
and West 1977
Mayer et al. 1982
Haftorn 1972
Reinertsen 1985, Reinertsen and Haftorn 1986
Reinertsen and Haftorn
1986
Biebach 1977
Reference(s)
AND
Cheramoeca leucosternus
Delichon urbica
Parus montanus
Willow Tit
10.1
12.4
16.75
12.7
118.3
Mb (g)
BMR V̇O2min
Tnorm– (mL O2 (mL O2
Tmin
Reducg21
g21
(8C)
hr21)
hr21) tion (%)
ANDREW E. MCKECHNIE
Hirundinidae
White-backed Swallow
Northern House-Martin
Poecile carolinensis
Poecile cincta
Parus major
Poecile atricapilla
Carolina Chickadee
Siberian Tit
Great Tit
Turdus merula
Paridae
Black-capped Chickadee
Species
Continued.
Muscicapidae
Eurasian Blackbird
TABLE 1.
712
BARRY G. LOVEGROVE
Prinzinger et al. 1991
Merola-Zwartjes 1998
Pal
Neo
Pal
Steen 1958
Ketterson and King 1977
Steen 1958
Reinertsen and Haftorn
1986, Steen 1958
Clemens 1989
Pal
Nearc
Pal
Pal
onto an alternate phylogeny, such as that proposed by Morony et al. (1975), leads to different
conclusions regarding the phylogenetic distribution of avian facultative hypothermic responses.
ZOOGEOGRAPHICAL DISTRIBUTION
Facultative hypothermic responses have been reported in species from all zoogeographic zones,
except the Indomalayan zone, for which there
are no data on avian hypothermia (Table 2). Of
the 95 species in the data set, 54 (57%) occur at
latitudes ,308N or S. Fourteen species occur between 308 and 608N or S, and only four species
occur exclusively at latitudes .608N or S. The
available data set is clearly biased toward the
Holarctic, in terms of both the number of species
and taxonomic diversity (Table 2). Although the
number of species in which hypothermia has
been investigated is greatest in the Neotropics
(29 species), 24 of these are hummingbirds.
5.1
2.7
34
35.4
a Formerly E. guttatus.
b Formerly S. risoria.
c Measurements from chicks only.
dT
min calculated from V̇O2 measurements.
36.5
10
Loxia curvirostra
Coereba flaveola
39.1
38.1
1.4
37.6
39
23.4
Leucosticte tephrocotis
Gray-crowned RosyFinch
Red Crossbill
Bananaquit
7.8
3.6
38
35.4
33
32
38
39
33
39.8
27
28
31.3
11.3
Fringillidae
Brambling
White-crowned Sparrow
European Greenfinch
Common Redpoll
Fringilla montifringilla
Zonotrichia leucophrys
Carduelis chloris
Carduelis flammea
Mb (g)
Continued.
TABLE 1.
713
BODY SIZE
Species
Tnorm
(8C)
Tmin
(8C)
BMR V̇O2min
Tnorm– (mL O2 (mL O2
g21
g21
Tmin
Reduc(8C)
hr21)
hr21) tion (%)
Zone
Reference(s)
AVIAN FACULTATIVE HYPOTHERMIC RESPONSES
Facultative hypothermic responses have been recorded in species in the Mb range of 2.7 g (Booted Racket-tail [Ocreatus underwoodii]) to 6500
g (Eurasian Griffon [Gyps fulvus]). The Mb frequency distribution of species in which hypothermia has been reported is right-skewed (Fig.
2). A comparison of this Mb distribution with a
rescaled distribution for approximately 6200
avian species (dotted line in Fig. 2) shows that
hypothermia occurs across almost the entire avian Mb range. The higher relative frequency of
hypothermic responses in small species probably
reflects the greater number of measurements on
small birds (e.g., hummingbirds).
To determine whether species that employ
rest-phase hypothermia (sensu Prinzinger et al.
1991, Reinertsen 1996) versus daily torpor (sensu Geiser and Ruf 1995) are distinguishable on
the basis of Mb, we compared the Mb of species
in which observed Tmin . 27.58C with those in
which Tmin , 27.58C. This body temperature is
midway between the two Tb values previously
proposed as the lower limit of rest-phase hypothermia (Prinzinger et al. 1991, Reinertsen
1996). The mean Mb of species in which Tmin ,
27.58C was significantly lower than species in
which Tmin . 27.58C (Kolmogorov-Smirnov test,
P , 0.05). However, the frequency distributions
of these two groups show a high degree of overlap (Fig. 2), and Mb is not a reliable criterion for
714
ANDREW E. MCKECHNIE
AND
BARRY G. LOVEGROVE
FIGURE 1. Phylogenetic distribution of avian facultative hypothermic responses. The phylogeny is based on
Sibley and Ahlquist (1990). The extent of body temperature reduction (DTb) is given as the difference between
normothermic rest-phase body temperature (Tnorm) and minimum hypothermic body temperature (Tmin), i.e., DTb
5 Tnorm 2 Tmin. An asterisk indicates that Tmin was recorded in chicks, not adult birds.
distinguishing between rest-phase hypothermia
and torpor.
BODY TEMPERATURE
TABLE 2. Summary of zoogeographic distribution
of avian species and families in which facultative hypothermic responses have been reported. The number
of species and families is given for each zone.
Zone
Afrotropics
Australasia
Indomalaya
Nearctic
Neotropics
Palearctic
Species that occur in .1 zone
Number Number
of
of
species families
12
11
0
18
29
16
9
4
8
0
10
5
10
7
Minimum Tb recorded during avian facultative
hypothermic responses ranges from 4.38C in the
Common Poorwill (Brigham 1992) to over
388C. Although the overall avian Tmin frequency
distribution is fairly continuous (Fig. 3), the distributions for specific taxa differ markedly from
each other (Fig. 4). For instance, Tmin values observed in 8 species of nightjars and allies are
continuously distributed between 4.38C and
29.68C (Fig. 4). In contrast, the distribution of
Tmin in the Trochiliformes has a clear mode at
18–208C (Fig. 4). Hence, the overall avian Tmin
frequency distribution (Fig. 3) represents the
AVIAN FACULTATIVE HYPOTHERMIC RESPONSES
FIGURE 2. Frequency histogram of log body mass
(Mb) of avian species in which facultative hypothermic
responses have been reported (lower graph). The dotted line shows the logMb frequency for approximately
6200 species (redrawn from Blackburn and Gaston
1994, and rescaled to fit the y-axis). The upper graph
shows the frequency histograms of log body mass of
avian species for which minimum body temperature
during facultative hypothermic responses (Tmin) is less
than 27.58C and greater than 27.58C respectively.
sum of several taxon-specific subsets. The frequency distributions of Tnorm 2 Tmin and Tmin (Fig.
3) are continuous, with no discernible gaps or
obvious modality. These continuous distributions do not support the argument that avian hypothermic responses fall into physiologically
discrete categories that are distinguishable on
the basis of minimum Tb alone.
Further evidence that Tb is not a reliable indicator of physiological state is provided by Merola-Zwartjes and Ligon (2000). These authors
distinguished between ‘‘heterothermy’’ (apparently atypically labile normothermic Tb) and torpor in Puerto Rican Todies (Todus mexicanus)
by the degree to which the birds responded to
external stimuli. Todies which did not respond
to handling were considered to be torpid. On the
715
FIGURE 3. Frequency histogram of the difference
between normothermic and minimum hypothermic
body temperature (Tnorm 2 Tmin) in the 59 avian species
for which both normothermic and hypothermic body
temperature data are available (lower graph). The upper graph shows the frequency distribution of Tmin in
the 85 species for which hypothermic body temperature data are available.
other hand, todies which remained alert, responsive to stimuli, and capable of flight were considered to be in a state of ‘‘heterothermia.’’ The
minimum Tb observed in a nontorpid tody was
27.98C, whereas the Tb of torpid birds ranged
from 23.58C to 29.38C. The overlap of the torpid
and nontorpid Tb ranges in Puerto Rican Todies
calls into question the notion of specific Tb limits
for daily torpor and rest-phase hypothermia. Although large differences in avian Tb undoubtedly
reflect different physiological states, the biological reality of specific Tb limits, such as those
proposed by Prinzinger et al. (1991) and Reinertsen (1996), is doubtful.
The question of whether avian rest-phase hypothermia and torpor represent discrete physiological states or components of a hypothermic
response continuum is difficult to answer with
716
ANDREW E. MCKECHNIE
AND
BARRY G. LOVEGROVE
FIGURE 4. Frequency histograms of minimum hypothermic body temperature (Tmin) in 28 species of
hummingbirds and swifts, 8 species of nightjars and
allies, and 28 passerines. Note that the frequency distribution of Tmin varies across taxa, and that the overall
avian Tmin distribution is made up of several taxonspecific subsets.
the available data. The continuous distribution
of avian Tmin (Fig. 3) supports Reinertsen’s
(1996) view that rest-phase hypothermia and torpor represent components of a continuum, rather
than discrete physiological phenomena. However, the clear behavioral distinction between
torpid and nontorpid Puerto Rican Todies (Merola-Zwartjes and Ligon 2000) supports Prinzinger et al.’s (1991) assertion that rest-phase hypothermia and torpor represent totally different
physiological states. Similarly, Austin and Bradley’s (1969) observation that a Common Poorwill was capable of flight at a Tb of 27.48C suggests that instances of Tb below 308C are not
necessarily associated with torpidity. The ecological consequences of torpor, during which a
bird is lethargic and unable to rapidly respond
to external stimuli, are clearly different from
those of a hypothermic state during which a bird
remains alert and capable of flight. Collectively,
these data highlight the need to accurately distinguish between different categories of avian
hypothermic response. Barclay et al. (2001) pro-
posed that any Tb below an individual’s normothermic range constitutes torpor. We argue that
this definition of torpor is too broad, because the
available avian data suggest that Tb below normothermy can be associated with several distinct
physiological states. A distinction needs to be
made between torpor, during which the ability
to rapidly respond to changes in the external environment is lost, and rest-phase hypothermia,
during which this ability is at least partially retained.
Few studies have investigated the relationship
between avian Tb and the ability to respond to
external stimuli. An interesting avenue for future
research will be to investigate this question under laboratory or seminatural conditions, and to
distinguish between torpid and nontorpid birds
on the basis of behavior, rather than Tb (MerolaZwartjes and Ligon 2000). Most studies of thermoregulation in free-ranging birds involve measurements of Tb alone, and a better understanding of the relationship between Tb and physiological state will be useful in interpreting these
data.
METABOLIC REDUCTION
Whereas hypothermic Tb data are available for
approximately 80 species, metabolic rates during
hypothermia have been reported for relatively
few species. The lowest measured V̇O2min was
0.09 mL O2 g21 hr21 in the Red-backed Mousebird (Colius castanotus; Prinzinger et al. 1981).
The greatest extent of metabolic reduction
(V̇O2min equivalent to 4.4% of basal metabolic
rate [BMR]) was observed in Anna’s Hummingbird (Calypte anna; Lasiewski 1963). Metabolic
rates during hypothermia are available for 13
species which reduce Tb by 108C or more; these
rates range from 4.4–96% of BMR, similar to
Geiser and Ruf’s (1995) range of 4.4–67% for
all avian and mammalian species known to use
daily torpor.
Body temperature during hypothermia depends on the degree of metabolic reduction as
well as the Mb-dependent thermal conductance.
Hence, a continuous frequency distribution of
Tmin (Fig. 3) does not necessarily reflect a continuous underlying frequency distribution of
metabolic reduction. It may be possible to distinguish between avian hypothermic states using
a metabolic parameter, such as metabolic rate
during hypothermia expressed as a percentage of
normothermic resting metabolic rate (RMR) at
AVIAN FACULTATIVE HYPOTHERMIC RESPONSES
the same ambient temperature (Ta). Geiser and
Ruf (1995) used metabolic rate expressed as a
percentage of BMR to distinguish between daily
torpor and hibernation. However, many birds reduce Tb only a few degrees below normothermic
levels. Hence, expressing metabolic rate as a
percentage of BMR is probably not useful for
distinguishing between torpor and rest-phase hypothermia. At present, there are too few data to
investigate the distinction between rest-phase
hypothermia and torpor on the basis of metabolic reduction.
It may be possible to distinguish between restphase hypothermia and torpor on the basis of the
relationship between metabolic rate, Tb, and Ta.
Whereas the physiological mechanism responsible for reduction of metabolic rate during torpor remains controversial (Geiser 1988, Snyder
and Nestler 1990, Heldmaier and Ruf 1992,
Song et al. 1995), the relationship between metabolic rate, Tb, and Ta during torpor is similar in
birds and mammals. In most species investigated
to date, there is evidence for a critical Ta during
torpor (e.g., Hiebert 1990, Song et al. 1995). At
Ta . critical Ta, Tb does not differ from Ta by
more than 1–28C, and metabolic rate is directly
related to Ta (Hiebert 1990, Song et al. 1995).
Below the critical Ta, a torpor Tb setpoint is defended by means of metabolic heat production,
and metabolic rate increases with decreasing Ta,
as occurs during typical endothermic homeothermy (Hiebert 1990, Song et al. 1995). An examination of the relationship between metabolic
rate and Ta in laboratory studies, or Tb and Ta in
free-ranging birds, may reveal whether patterns
of thermoregulation represent torpor or merely
rest-phase hypothermia. If thermoregulation is
studied in free-ranging individuals of a species
for which the critical torpor Ta is known, the
distinction between torpor and rest-phase hypothermia should be relatively clear. Following the
initial reduction in Tb, a situation where a bird’s
Tb tracks Ta above the critical torpor Ta indicates
torpor, whereas the maintenance of a constant Tb
over the same Ta range more likely indicates
rest-phase hypothermia. This is well illustrated
by Figure 1 in Carpenter (1974). The Tb of torpid
Andean Hillstars (Oreotrochilus estella) roosting in a cave in the Peruvian Andes tracked Ta
at Ta . ca. 88C, but was regulated with respect
to a setpoint Tb at lower ambient temperatures
(Carpenter 1974).
717
PATTERNS OF HYPOTHERMIC
THERMOREGULATION
In mammals, facultative hypothermic responses
typically comprise three distinct phases. The entry phase is characterized by metabolic downregulation and a concomitant decrease in Tb, and
is followed by a maintenance phase during
which Tb is regulated with respect to a reduced
Tb setpoint (Lyman et al. 1982). The arousal
phase involves an increase in metabolic heat
production, which returns Tb to normothermic
levels (Lyman et al. 1982).
Some traces of avian hypothermic Tb or V̇O2,
such as those shown by a Rufous Hummingbird
(Selasphorus rufus, Fig. 5a; Hiebert 1990) do fit
the ‘‘entry–maintenance–arousal’’ pattern. However, in many cases avian hypothermia does not
follow this pattern, and there may be substantial
variation in the patterns of thermoregulation
within species and individuals (Fig. 5b–e). For
instance, the patterns shown by three hummingbird species under seminatural conditions (Fig.
5b) were variable. In addition to variability in
the number of bouts exhibited during a single
rest phase, cooling rate during the entry phase
varied among individual bouts. Moreover, in
some traces a maintenance phase was largely absent (Fig. 5b; Bech et al. 1997). The reasons for
the variability in cooling rate were unclear (C.
Bech, pers. comm.). Similarly, traces of skin
temperature from an Australian Owlet-Nightjar
(Fig. 5c; Brigham et al. 2000) showed considerable variability. Whereas on some occasions a
maintenance phase of several hours was apparent (e.g., night of 27–28 June), during other
bouts the arousal phase followed the entry phase
immediately (e.g., 28 July). A lack of initial
metabolic reduction and concomitant rapid reduction in Tb was evident in two species of
mousebirds, and approximately linear decreases
in Tb preceded arousal (Fig. 5d, e; McKechnie
and Lovegrove 2001a, 2001b). The unusual patterns of thermoregulation in mousebirds appear
to be related to their distinctive communal roosting behavior (McKechnie and Lovegrove 2000,
2001a, 2001b).
Collectively, these data suggest that avian hypothermic thermoregulation is variable compared to that observed during mammalian daily
torpor and hibernation (Lyman et al. 1982). The
factors responsible for determining the pattern
of thermoregulation during a particular hypothermic response have received little attention.
718
ANDREW E. MCKECHNIE
AND
BARRY G. LOVEGROVE
FIGURE 5. Traces of avian body temperature (Tb) or oxygen consumption (V̇O2) during facultative hypothermic responses. (A) V̇O2 during torpor in a Rufous Hummingbird (reprinted from Hiebert 1990). Note distinct
entry, arousal, and maintenance phases; (B) Multiple torpor bouts under seminatural conditions in three species
of hummingbirds (Bech et al. 1997); (C) Skin temperature (dotted line) and ambient temperature (solid line) in
a free-ranging Australian Owlet-Nightjar (reprinted from Brigham et al. 2000); (D) Rest-phase thermoregulation
under laboratory conditions in a White-backed Mousebird at Ta 5 58C (reprinted from McKechnie and Lovegrove
2001a); (E) Torpor bout under laboratory conditions in a Speckled Mousebird (reprinted from McKechnie and
Lovegrove 2001b). Figures reprinted by permission from University of Chicago Press and Springer-Verlag.
Elucidating the mechanisms underlying variability in patterns of thermoregulation in free-ranging birds will probably require experimental manipulations under seminatural or natural conditions. In many laboratory studies, facultative hypothermic responses were induced by means of
restricted feeding (e.g., Hiebert 1990, McKechnie and Lovegrove 2001b), and patterns of
thermoregulation under such conditions proba-
bly do not reflect patterns under natural conditions (see below).
PROXIMATE DETERMINANTS OF
FACULTATIVE HYPOTHERMIC RESPONSES
Shallow hypothermia in response to food deprivation has been reported in several species, and
has been particularly well-studied in pigeons
(Graf et al. 1988, 1989, Phillips and Berger
AVIAN FACULTATIVE HYPOTHERMIC RESPONSES
1988, Rashotte et al. 1988, 1995, Jensen and
Bech 1992a, 1992b). Food deprivation also appears to be the proximate determinant of torpor
in mousebirds (Bartholomew and Trost 1970,
Hoffmann and Prinzinger 1984, McKechnie and
Lovegrove 2001b). Whereas laboratory studies
suggest that food scarcity is the proximate determinant of torpor in nightjars and allies, recent
field data indicate that torpor is used routinely
and that several factors other than food availability determine whether a bird enters torpor
(Brigham 1992, Csada and Brigham 1994, Geiser et al. 2000, Körtner et al. 2000).
A link between diet and the occurrence of avian torpor has been suggested by McNab (1988),
and it is noteworthy that almost all species in
which torpor has been reported are nectarivores,
aerial insectivores, or frugivores. The spatial and
temporal predictability of food resources is likely to be an important determinant of avian hypothermia. Whereas predictable, seasonal food
shortages can be avoided by means of migration,
unpredictable periods of food scarcity are likely
to result in strong selection for the ability to reduce energy requirements. Hence, species feeding on food resources sensitive to short-term
variability in rainfall (nectar and fruit) or temperature (aerial insects) presumably experience
the strongest selection for facultative hypothermia. In granivorous species, short-term fluctuations in food availability are likely buffered by
plant reproductive patterns (annual vs. perennial) and the existence of a seed bank. The availability of vertebrate prey (e.g., rodents) is presumably less temperature-dependent than that of
invertebrate prey. Hence, we argue that the occurrence of torpor in avian nectarivores, aerial
insectivores, and frugivores reflects the relative
predictability of different avian diets.
In several species, hypothermia has been correlated with low Ta. Both shallow hypothermia
(Merola-Zwartjes 1998) and torpor (MerolaZwartjes and Ligon 2000) have been observed
in tropical species in response to cold. Surprisingly, almost all facultative hypothermic responses to cold in Arctic and sub-Arctic species
are fairly shallow, particularly those observed in
the Paridae (Reinertsen 1983, 1985, Reinertsen
and Haftorn 1983, 1986). However, hypothermic
responses of Arctic species have only been investigated in passerines. Passerines in general do
not exhibit the capacity for pronounced hypothermia (Fig. 1), and the absence of torpor in
719
these species may be due to a phylogenetic limitation.
Early studies suggested that energy reserves
were the sole proximate determinant of torpor in
hummingbirds (Hainsworth et al. 1977). However, recent studies suggest that hummingbird
torpor is determined by a suite of factors including seasonal variation in the propensity for torpor (Carpenter 1974, Hiebert 1991, 1993), the
perceived availability of food (Hiebert 1991),
and temporal variation in assimilation efficiency
(Hiebert 1991, McWhorter and Martı́nez del Rio
2000). A possible mechanism for a circannual
cycle in the propensity for torpor involves seasonal physiological suppression of the stress response through variation in the sensitivity of the
hypothalamic–pituitary–adrenal axis (Hiebert et
al. 2000).
Testosterone levels appear to be responsible
for gender-specific variation in the use of torpor
and hibernation in several mammalian heterotherms (Hall and Goldman 1980, Lee et al.
1990, Barnes 1996, Mzilikazi and Lovegrove
2002). Mzilikazi and Lovegrove (2002) found
that castrated Afrotropical pouched mice (Saccostomus campestris) readily entered torpor,
whereas the application of testosterone inhibited
torpor. Potential endocrine determinants of avian
torpor have received little attention. MerolaZwartjes and Ligon (2000) found that torpor in
the Puerto Rican Tody was restricted to females,
and suggested that gender-specific variation in
the use of torpor was related to the effects of
reproductive hormones, as well as the energetic
stress of breeding experienced by the females.
Elevated corticosterone levels increased the use
of torpor in Rufous Hummingbirds, but the relationship between corticosterone concentration
and torpor frequency varied between seasons
(Hiebert et al. 2000).
Hypothermia appears to be avoided during incubation in some species. Carpenter (1974) and
Prinzinger and Siedle (1988) noted incidences of
torpor in incubating Broad-tailed Hummingbirds
(Selasphorus platycerus) and Northern HouseMartins (Delichon urbica), respectively, but torpidity adversely affected breeding success in
Common Poorwills and was avoided during incubation (Brigham 1992, Kissner and Brigham
1993, Csada and Brigham 1994). Incubating
male Greater Roadrunners (Geococcyx californianus) maintained normothermic Tb, whereas
females and nonincubating males used hypo-
720
ANDREW E. MCKECHNIE
AND
BARRY G. LOVEGROVE
thermia routinely (Vehrencamp 1982). Incubating Blue Petrels (Halobaena caerulea) showed
no evidence of hypothermia, even when experiencing severe energy stress (Ancel et al. 1998).
There is evidence that reductions in energy
requirements by means of hypothermia may be
important in migratory species. Carpenter and
Hixon (1988) observed torpor in a Rufous Hummingbird that was apparently in good condition,
and argued that torpor may reduce the time required to accumulate fat reserves prior to a migratory flight. More recently, Butler and Woakes
(2001) showed that Barnacle Geese used shallow hypothermia before and during their autumn
migration. In the latter case, hypothermia was
apparently used to reduce the rate at which fat
reserves were depleted during migration (Butler
and Woakes 2001).
Elucidating the proximate determinants of
avian facultative hypothermia is complicated by
the fact that most studies have been carried out
under artificial, laboratory conditions. There is
increasing evidence that data on hypothermic responses collected in the laboratory are not representative of patterns in free-ranging individuals, and need to be treated with caution. Geiser
et al. (2000) reviewed patterns of torpor and hibernation in free-ranging and captive mammals
and birds, and concluded that laboratory studies
tend to underestimate the depth, frequency, and
duration of torpor bouts. Moreover, Geiser and
Ferguson (2001) found that the use of torpor in
captive-bred feathertail gliders (Acrobates
pygmaeus) was considerably reduced in comparison to wild-caught individuals. These authors urged caution in extrapolating data from
captive-bred or acclimated individuals to the
field. It is likely that future studies of thermoregulation in free-ranging birds will reveal that
many species use facultative hypothermic responses more frequently, and in a wider variety
of ecological contexts, than laboratory studies
currently suggest.
CONCLUSIONS
The limited data on avian facultative hypothermic responses suggest that (a) hypothermia occurs throughout the avian phylogeny, (b) hypothermia occurs in species over most of the avian
Mb range, and (c) the use of hypothermia is determined by a suite of ecological and physiological determinants. Collectively, these observations support recent views that facultative hy-
pothermic responses are more widespread and
play a more important role in avian energy balance than previously thought (Geiser et al. 2000,
Körtner et al. 2000).
Several key questions regarding avian hypothermic responses remain unresolved. How did
the avian capacity for facultative hypothermia
evolve? The known phylogenetic distribution of
pronounced hypothermia (torpor), as well as the
patterns of thermoregulation in two species of
mousebirds (McKechnie and Lovegrove 2000,
2001b) provide circumstantial evidence for a
monophyletic, plesiomorphic origin of avian
heterothermy, as proposed by Malan (1996).
However, the absence of data on hypothermic
responses in most avian families, and in particular the older Neoaves, precludes the rigorous
testing of Malan’s (1996) hypothesis.
The distinction between various categories of
avian hypothermic response also remains controversial. Although Tb is widely used as the criterion for distinguishing between rest-phase hypothermia and torpor, the available data seriously question the notion of specific Tb limits. However, a more important issue, particularly in the
context of the increasing number of studies on
thermoregulation in free-ranging birds, is the relationship between physiological state and the
ability of a bird to respond to external stimuli.
The responsiveness of a hypothermic bird to external stimuli has far greater ecological significance than Tb per se, since reduced responsiveness presumably increases a bird’s vulnerability
to predation.
ACKNOWLEDGMENTS
We thank Elke Schleucher for faxing us copies of several of the articles cited in this paper, which we were
unable to obtain locally. We also thank Gerardo Suzan
for translating the title and abstract into Spanish. This
study was funded by National Research Foundation
and University of Natal Research Fund grants to BGL.
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