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Hibernation and Daily Torpor in Marsupials - a Review

CSIRO Publishing
Australian Journal of Zoology
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Abstract

Most heterothermic marsupials appear to display one of the two patterns of torpor that have been described in placental mammals. During shallow, daily torpor body temperature (T(b)) falls for several hours from about 35-degrees-C to values between 11 and 28-degrees-C, depending on the species, and metabolic rates fall to about 10-60% of the basal metabolic rate (BMR). In contrast during deep and prolonged torpor (hibernation), T(b) falls to about 1-5-degrees-C, metabolic rates to about 2-6% of BMR and torpor bouts last for 5-23 days. Shallow, daily torpor has been observed in the opossums (Didelphidae), the carnivorous marsupials (Dasyuridae) and the small possums (Petauridae). Daily torpor may also occur in the numbat (Myrmecobiidae) and the marsupial mole (Notoryctidae). Deep and prolonged torpor (hibernation) has been observed in the pygmy possums (Burramyidae), feathertail glider (Acrobatidae) and Dromiciops australis (Microbiotheriidae). The patterns of torpor in marsupials are paralleled by those of monotremes, placentals and even birds. These similarities in torpor patterns provide some support to the hypothesis that torpor may be plesiomorphic. However, as endothermy and torpor in birds apparently has evolved separately from that in mammals and as torpor occurrence in mammals can change within only a few generations it appears more likely that torpor in endotherms is convergent.
Aust.
J.
Zool., 1994,
42,
1-16
Hibernation and Daily Torpor in Marsupials:
a Review
Fritz Geiser
Department of Zoology, University of New England,
Armidale, NSW
2351,
Australia.
Abstract
Most heterothermic marsupials appear to display one of the two patterns of torpor that have been
described in placental mammals. During shallow, daily torpor body temperature (Tb) falls for several
hours from about
35°C
to values between
11
and
2g°C,
depending on the species, and metabolic rates
fall to about
10-60%
of the basal metabolic rate
(BMR).
In contrast during deep and prolonged torpor
(hibernation), Tb falls to about
1-5"C,
metabolic rates to about
2-696
of BMR and torpor bouts last
for
5-23
days. Shallow, daily torpor has been observed in the opossums (Didelphidae), the carnivorous
marsupials (Dasyuridae) and the small possums (Petauridae). Daily torpor may also occur in the numbat
(Myrmecobiidae) and the marsupial mole (Notoryctidae). Deep and prolonged torpor (hibernation) has
been observed in the pygmy possums (Burramyidae), feathertail glider (Acrobatidae) and
Dromiciops
australis
(Microbiotheriidae).
The patterns of torpor in marsupials are paralleled by those of monotremes, placentals and even
birds. These similarities in torpor patterns provide some support to the hypothesis that torpor may be
plesiomorphic. However, as endothermy and torpor in birds apparently has evolved separately from that
in mammals and as torpor occurrence in mammals can change within only a few generations it appears
more likely that torpor in endotherms is convergent.
Introduction
A
vast body of scientific literature deals with torpor in placental mammals (Lyman
1982a). Torpor has been observed in at least
5
orders of placentals, the Insectivora (e.g.
hedgehogs, tenrecs, shrews), Chiroptera (Microchiroptera and Megachiroptera), primates
(dwarf lemurs), Carnivora
(e.g. skunk, badger) and Rodentia (e.g. dormice, hamsters, ground
squirrels, deer mice) (Lyman 1982a). Torpor in marsupials has attracted the interest of fewer
scientists although the phylogenetic relationship of marsupials to other mammals may
provide potential insights into the evolution of mammalian torpor (Bartholomew and
Hudson 1962).
Information on torpor in marsupials gathered before 1987 has been summarised by
Hudson
(1973), Wallis (1979, 1982), Lyman (1982a) and Dawson (1989). More data on
torpor in marsupials have been collected in recent years, but our understanding of torpor
in marsupials is still well behind that on torpor in placentals. In the present review current
knowledge on torpor of
33
marsupial species is summarised and compared with observations
on monotremes and placentals. Using these comparative data, interrelations between variables
of torpor in marsupials are investigated and the evolution of torpor in mammals is discussed
from a marsupial perspective.
0004-959X/94/010001$05.00
Table
1.
Torpor
in
marsupials
The minimum body temperature and the longest duration of
a
torpor bout reported for adults of each species are shown. Tor, shallow, daily torpor;
Hib, deep, prolonged torpor (hibernation)
Family
Species
Body Minimum Torpor
Torpor
mass body duration pattern
Source
Didelphidae
Marmosa microtarsus
Marmosa elegans
Marmosa robinsoni
Monodelphis brevicaudata
Microbiotheriidae
Dromiciops australis
Dasyuridae
Dasyunrs geoffroii
Dasyuroides byrnei
Dasycercus cristicauda
Phascogale tapoatafa
Antechinus
flavipes
Antechinus stuartii
Antechinus swainsonii
Sminthopsis murina
Sminthopsis ooldea
Tor
Tor?
Tor?
Tor?
Hib
Tor
Tor
Tor
Tor?
Tor
Tor
Tor
Tor
Tor
Morrison and McNab
(1962)
Morrison and McNab
(1962)
McNab
(1978)
McNab
(1978)
Rosenmann and Ampuero
(1981)
Arnold
(1976)
Geiser and Baudinette
(1987)
Geiser and Masters
(1994)
Dixon and Huxley
(1989)
Geiser
(1985)
Geiser
(1985)
Gotts
(1976)
Geiser
et al.
(1984)
Aslin
(1983)
Sminthopsis longicaudata
Sminthopsis crassicaudata
Sminthopsis macroura
Antechinomys laniger
Planigale maculata
Planigale ingrami
Planigale tenuirostris
Planigale gilesi
Ningaui yvonneae
Myrmecobiidae
Myrmecobius
fmciatus
Notoryctidae
Notoryctes typhlops
Petauridae
Petaum breviceps
Gymnobelideus leadbeateri
Burramyidae
Cercartetus nanus
Cercartetus concinnus
Cercartetus Iepidus
Cercartetus caudatus
Burramys parvus
Acrobatidae
Acrobates pygmaeus
Tarsipedidae
Tarsiw rostratus
Tor
Tor
Tor
Tor
Tor
Tor
Tor
Tor
Tor
Burbidge et al.
(1983)
Geiser and Baudinette
(1987)
Geiser and Baudinette
(1987)
Geiser
(1986)
Morton and
Lee
(1978)
Dawson and Wolfers
(1978)
Dawson and Wolfers
(1978)
Geiser and Baudiiette
(1988)
Geiser and Baudinette
(1988)
Tor?
Serventy and Raymond
(1973)
Tor?
Wood-Jones
(1923);
Tyndale-Biscoe
(1973)
Tor
Tor?
Fleming
(1980)
Smith
(1980)
Hib
Hib
Hib
Hib?
Hib
Geiser
(1993)
Geiser
(1987)
Geiser
(1987)
Atherton and Haffenden
(1982)
Geiser and Broome
(1991)
Hib Jones and Geiser
(1992)
Tor Withers et al.
(1990)
F.
Geiser
The Patterns of Torpor in Marsupials
The patterns of torpor in most marsupials can be divided into two major groups, as has
been described for placental mammals (Wang 1989): (1) shallow, daily torpor with minimum
Tb (the body temperature that is metabolically defended during torpor) from 11 to 28OC
and torpor bouts from 2 to 19.5 h and (2) deep and prolonged torpor (hibernation) with
minimum Tb from
1
to 6OC and torpor bouts between 1 and
3
weeks (Table 1; Figs 1, 2).
Species displaying deep and prolonged torpor at low ambient temperature
(T,)
may display
daily torpor at high T, or at the beginning of the hibernation season. Other species show
daily torpor exclusively independent of the prevailing T, or the time of year.
Hibernation
Daily torpor
Duration of torpor bout
(h)
Fig.
1.
Frequency distribution of the duration of the longest torpor bout
of
20
marsupial species from Table
1.
All species displaying daily torpor had
torpor bouts shorter than
20
h, whereas all species displaying prolonged torpor
(hibernation) had torpor bouts longer than
100
h.
As in placentals, torpor in marsupials may occur when food and water are freely available
(spontaneous torpor) or may occur after withdrawal or restriction of food and water
(induced torpor).
South American Marsupials
Torpor in South American marsupials has been observed in two families, the Didelphidae
and the Microbiotheriidae. Although torpor has not been observed in the third South
American family, the Caenolestidae (McNab
1978), it is possible that some species in this
family of small marsupials are heterothermic.
Didelphidae
Several species of the Didelphidae display daily torpor (Table 1). The best information
is available for the murine opossum
Marmosa microtarsus
(13
g),
which entered daily torpor
with Tbs of 16°C and torpor bouts up to 8 h after food deprivation (Morrison and McNab
Torpor in Marsupials
Hibernation
Daily torpor
Minimum
body
temperature
("C)
Fig.
2.
Frequency distribution of the minimum body temperature
(Tb)
of
23
marsupial species from Table
1.
All but one species displaying daily
torpor had minimum Tbs higher than
1l0C,
whereas all species displaying
prolonged torpor (hibernation) had minimum Tbs lower than
6°C.
1962).
Marmosa elegans
(30 g) also displayed daily torpor with
Tb
remaining above 15°C
(Morrison and McNab 1962). Shallow torpor has also been observed in
Marmosa robinsoni
(122 g) and
Monodelphis brevicauda
(40-111 g) (McNab 1978).
Microbiotheriidae
During torpor of
Dromiciops australis
(30 g) metabolic rates fell to about 1% of that in
normothermic ani\mals (Rosenmann and Ampuero 1981), which is similar to the metabolic
rare of small torpid hibernators (Geiser
1988b). Torpor bouts lasted for about
5
days
(Rosenmann and Ampuero 1981) and during spontaneous torpor in the laboratory skin
temperatures fell below 10°C (Grant and Temple-Smith 1987). This species fattens before
winter and apparently shows a torpor season during winter (Nowak and Paradiso 1983).
These observations strongly suggest that
D. australis
is a deep hibernator.
Australian Marsupials
Torpor in AustraIian marsupials has been observed in
5
of 16 families (Table 1; Fig. 4)
and it has been suggested that species of two additional families also display torpor.
Most information is available for the
insectivorous/carnivorous
marsupials (Dasyuridae)
and the pygmy possums (Burramyidae) (Table 1).
Dasyuridae
To date, all members of the Dasyuridae in which torpor has been investigated have
displayed shallow, daily torpor. Torpor has been observed in many species, ranging in body
mass from only about
5
g (long-tailed planigale,
Planigale ingrami,
Dawson and Wolfers
F.
Geiser
1978) to about 1000 g (western quoll, Dasyurus geoffroii, Arnold 1976). Depending on the
species,
Tb during torpor fell to values between 11°C (kultarr, Antechinomys laniger)
and 28°C (dusky antechinus, Antechinus swainsonii) and metabolic rate to 10-6046 of the
BMR. Torpor bouts lasted for up to 19.5 h, but 2-8 h were more common. Spontaneous
torpor occurred quite regularly in some species
(e.g. stripe-faced dunnart, Sminthopsis
macroura; A. laniger; paucident planigale, Planigale gilesi) (Godfrey 1968; Geiser 1986;
Geiser and Baudinette 1987, 1988). In other species food and/or water had to be withdrawn
or restricted to induce torpor while spontaneous torpor was observed only occasionally
(e.g. fat-tailed dunnart, Sminthopsis crassicaudata, and Antechinus spp.) (Godfrey 1968;
Wallis 1976, 1982; Geiser and Baudinette 1987; Geiser 1988~). Torpor in the laboratory
reduced average daily metabolic rates of S.
crassicaudata by about 20-40% in comparison
to normothermic animals (Holloway 1992). Field studies revealed that torpor patterns and
energy saving due to torpor in free-ranging S. crassicaudata were similar to those observed
in the laboratory (Frey 1991). Groups of S. crassicaudata have been observed to undergo
social torpor together with the house mouse,
Mus musculus, in the field (Morton 1978).
When food was withheld for several hours Planigale maculata apparently became poi-
kilothermic (Morton and Lee 1978), similar to naked mole-rats, Heterocephalus glaber
(Buffenstein and Yahav 1991). However, when torpor occurred spontaneously the animals
were able to rewarm and showed pronounced daily
Tb rhythms similar to those of other
dasyurid marsupials (Morton and Lee 1978).
Seasonal changes in the patterns and occurrence of torpor have been observed in
some dasyurids. Metabolic rates measured at the same T, and Tbs during torpor of
S.
crassicaudata (17 g) and S. macroura (20-28 g) housed in outdoor pens were lower
during winter than during summer, suggesting a seasonal change of thermal physiology in
these species (Geiser and Baudinette 1987). In the field torpor in S. crassicaudata was
observed more frequently in late autumn and winter (May-July) when
T,
was low than in
early autumn (April) (Frey 1991).
Seasonal changes in the occurrence and depth of torpor in the dasyurids Antechinus
stuartii (brown antechinus, 20-26 g) and A. jlavipes (yellow-footed antechinus, 30-70 g)
differ from those in Sminthopsis spp. (Geiser
1988~). Members of the genus Antechinus
reproduce only once a year in winter and all males die after mating. Offspring are weaned
in summer and grow until the mating season in the following year (Lee and Cockburn 1985).
Torpor in juvenile A. stuartii and A. flavipes in summer, when they were small in size,
was more frequent and deeper than in winter when they had grown to adult size (Geiser
1988~). These observations suggest that the seasonal change of torpor patterns in these
species is strongly influenced by body size; the seasonal change of climate appears to have
less impact.
Reproduction and torpor appear to be mutually exclusive in many rodents (Steinlechner
et al. 1986;
Goldman et al. 1986). This is not the case in several dasyurid marsupials that
have been observed in torpor during either pregnancy or lactation of females and during the
reproductive season of males. Torpor was observed in a lactating S. crassicaudata in
the wild that subsequently raised her young with success (Morton 1978). Exposure of
S.
crassicaudata to long photoperiod resulted in an increase of testes size, but did not appear
to have any impact on torpor patterns (Holloway 1992). Females of the mulgara, Dasycercus
cristtcauda (70-100 g), displayed spontaneous torpor frequently (76% of observations) during
the period of pregnancy as did males regularly (47% of observations) throughout the
reproductive season (Geiser and Masters 1994). It is not known why some insectivorous
dasyurids, in contrast to many rodents, show torpor during the reproductive season.
However, it is possible that the relatively slow development of marsupial young may allow
females to enter torpor. Furthermore, the low supply of insects during part of their
reproductive season may make constant homeothermy energetically impossible.
Torpor in Marsupials
Myrmeco biidae
The numbat,
Myrmecobius fasciatus
(about 500 g), also appears to enter torpor. No
detailed field or laboratory studies have been conducted. However, observations of cold and
immobile individuals that were found in hollow logs on cold winter mornings and rewarmed
after a few hours in the sun (Serventy and Raymond 1973) indicate that they undergo
periods of torpor.
Notoryctidae
Tyndale-Biscoe (1973) suggested that observations by Wood-Jones (1923) on activity
patterns of the marsupial mole,
Notoryctes typhlops
(40-70 g), may indicate that this
species exhibits torpor. However, no detailed study has been conducted to verify whether
this species is heterothermic.
Petauridae
Daily torpor has also been observed in the relatively large (about 130 g) petaurids, the
sugar glider,
Petaunts breviceps,
and the Leadbeater's possum,
Gymnobelideus leadbeateri
(Fleming 1980; Smith 1980). Spontaneous torpor was only occasionally observed in
P. breviceps.
Food restriction increased the proportion of individuals undergoing periods
of torpor (Fleming 1980). The metabolic rate of torpid
P.
breviceps
was reduced to about
10% of that in normothermic resting animals and the lowest
Tb
measured was 15.6"C
(Fleming 1980). Daily fluctuation of abdominal and brain temperatures were similar in
P. breviceps
and the lowest brain temperature recorded was about 14°C (Dawson and May
1984). Torpor in groups of
P.
breviceps
reduced metabolic rates at low
T,
(Fleming 1980),
suggesting that social torpor may be used to reduce metabolic costs of thermoregulation
in winter.
Burramyidae
Torpor in the pygmy possums differs substantially from that of the dasyurid and petaurid
marsupials (Table 1). All species that have been investigated in some detail displayed deep
and prolonged torpor (hibernation) (Hickman and Hickman 1960; Bartholomew and Hudson
1962; Wakefield 1970; Dimpel and Calaby 1972; Fleming 1985a; Geiser 1987, 1993; Geiser
and Broome 1991, 1993). The
Tb
fell as low as 1-6°C and torpor bouts lasted between one
and
three
weeks,
and
in
the eastern pygmy possum,
Cercartetus nanus,
up to five weeks
(Geiser 1993). All species of the family fattened extensively and, when hibernating, could
survive without food for up to seven months. Species of the genus
Cercartetus
appear
to enter torpor at any time of the year. In contrast the rare mountain pygmy possum,
Burramys parvus,
which is restricted to high altitudes of the Great Dividing Range, appears
to undergo a seasonal cycle of hibernation during winter and reproduction and growth
in summer (Mansergh 1984; Broome and Mansergh 1990). While most individuals in the
laboratory also hibernated in winter, a fat individual was observed to display multiday
torpor bouts in summer when held at relatively high
T,
(14°C) and under long photoperiod
(Kortner and Geiser 1994).
Body fat content appears to be important for hibernation of
B.
parvus
in winter (Fleming
1985a; Geiser and Broome 1991). Very fat individuals began hibernation with free access to
food and water at relatively high
T,,
intermediately fat individuals began hibernation at
low
T,
when food was available, individuals with little fat began hibernation at low
T,
when food was withheld and lean individuals never displayed torpor (Geiser and Broome
1991).
Energy expenditure during hibernation of
B. parvus
is strongly influenced by environ-
mental temperature (Geiser and Broome 1993). The duration of torpor bouts was longest
F.
Geiser
and the metabolic rate of torpid individuals was lowest at Ta of 2"C, which is similar to the
Ta experienced in winter by wild individuals in their snow-covered boulder fields. At Tas
above and below 2"C, torpor bouts shortened and metabolic rate increased. Because T, had
such a strong effect on hibernation and in particular energy expenditure, a change in climate
would most likely increase winter mortality of this endangered species.
It is interesting that breeding in captivity under artificial environmental conditions
appears to render individuals of
B.
parvus incapable of hibernation. First-generation
offspring of wild individuals maintained during autumn under environmental conditions
identical to those for wild-caught individuals that fattened and hibernated did not show
pre-hibernation fattening nor hibernation in two consecutive winters (Geiser et al. 1990b).
However, captive-bred
B.
parvus held in outdoor cages in Canberra showed short bouts of
torpor when exposed to low environmental temperatures (Fleming 1985a).
Acrobatidae
The feathertail glider, Acrobates pygmaeus (12 g), also displayed deep and prolonged
torpor lasting for several days at low Tas with Tbs falling to 2°C. At high Ta, the species
displayed daily torpor (Jones and Geiser 1992). Torpor in the laboratory may occur in
groups of up to eight individuals (Fleming
19858) and group torpor has also been observed
in the wild (Frey and Fleming 1984).
A.
pygmaeus could be classified as a deep hibernator,
since torpor lasted for several days and Tbs fell below 10°C (see Hudson 1973; Lyman
1982b), but
A.
pygmaeus lacks the characteristic pre-hibernation fattening of many hiber-
nating species (Mrosovsky 1971; Jones and Geiser 1992). It appears that this species does
not have a prolonged hibernation season, but may use prolonged torpor bouts during cold
weather spells when daily torpor, interrupted by foraging and feeding, does not guarantee
metabolic homeostasis.
The pattern of torpor in A. pygmaeus is influenced by dietary fats. Individuals main-
tained on a diet rich in polyunsaturated fatty acids showed lower minimum
Tbs and longer
torpor bouts than individuals maintained on a diet rich in saturated fatty acids (Geiser
et al. 1992). It appears that as in other heterothermic mammals dietary fatty acids may alter
tissue and cell membrane composition, which may in turn influence torpor patterns (Geiser
et al. 1992).
Like the dasyurids, A. pygmaeus displayed torpor during the reproductive season.
Lactating females of the species were observed to undergo torpor in the wild (Frey and
Fleming 1984).
Tarsipedidae
The pattern of torpor in the honey possum,
Tarsipes rostratus (10 g), may differ from
the other marsupials. This species exhibited very low Tbs of about S°C, but torpor bouts did
not exceed about 10 h (Withers et al. 1990). Metabolic rates during torpor were in the lower
range of those of dasyurids (Withers et al. 1990). Torpor in this species has also been
observed in wild-caught individuals in pitfall traps during the cold season between March
and September (Collins et
al. 1987; Withers et al. 1990).
Interrelations between Variables of Torpor
The above comparison shows that most marsupials with high Tbs during torpor display
short torpor bouts and most marsupials with low Tbs during torpor display long torpor bouts
(Table 1, Figs 1, 2). The duration of torpor bouts of 14 marsupial species falls into two
distinct groups (Fig. 1). Species displaying prolonged torpor (hibernation) show no overlap
with species displaying daily torpor. The longest torpor bout observed in a species displaying
daily torpor (19.5 h,
S.
crassicaudata) was only
16%
of the shortest multiday bout in a
hibernator (120 h,
A.
pygmaeus) (Table 1). Most of the minimum Tbs also fell into two
groups, but one species displaying daily torpor (T. rostratus) fell within the upper end
Torpor in Marsupials
of the species displaying prolonged torpor (hibernation) (Fig. 2). To determine possible
correlations between the longest duration of torpor bouts and the minimum Tbs, which are
widely used for defining patterns of torpor, regression analyses were performed on these
two variables available for 18 species (Table 1). The duration of torpor bouts increased
curvilinearly with decreasing
Tb (Fig. 3). When both variables were log-transformed a linear
regression appeared to provide an appropriate fit
(r2=0.79, P<~O-0001) (Fig. 3; insert).
Because of the good correlation between the two variables it is likely that duration of torpor
bouts and the minimum
Tb in marsupials are physiologically linked. It appears that, in
marsupials, duration of torpor bouts and the minimum
Tb respond simultaneously to
environmental selective pressures.
1
10
100
Body temperature
("C)
Body temperature
("C)
Fig.
3.
Relationship between the minimum body temperature (Tb) and the longest torpor
bout of
18
marsupial species for which data on both variables were available (Table
1).
When both variables were log-transformed a straight line fit appeared appropriate and
the equation for the linear regression was log(D)
=
2.88
-
1
5
1
log Tb
(r2
=
0.79,
P<O.0001),
where D is torpor bout duration in hours, and Tb is in
OC.
Torpor in Marsupials: comparisons with Monotremes and Placentals
The pattern of deep and prolonged torpor (hibernation) in marsupials is paralleled by
species of both the monotreme and placental mammals. Furthermore, at least one bird
species, the poorwill,
Phalaenoptilus nuttallii, appears to hibernate (Ligon 1970; French
1993). The minimum Tbs and metabolic rates of torpid pygmy possums and
A.
pygmaeus
are similar to those of short-beaked echidnas; Tachyglossus aculeatus (Monotremata) (Augee
and Ealey 1968; Grigg et al. 1989; Nicol et al. 1992), hedgehogs, Erinaceus europaeus
(Thati 1978; Fowler and Racey 1990), insectivorous bats (Hock 1951; see Geiser 1988b) and
many hibernating rodents (Heller and Hammel 1972; Florant and Heller 1977; Geiser et al.
1990). A prolonged hibernation season, interrupted by periodic arousals as in the marsupial
pygmy possums, is also found in echidnas (Grigg et al. 1989) and all hibernating placentals
that have been studied to date (Twente and Twente 1965; French 1985; Geiser et al. 1990a).
F.
Geiser
The pattern of daily torpor in the Dasyuridae and Petauridae
(P.
breviceps) is similar
to that of several placental orders, for example, insectivores (shrews, Nagel 1985), primates
(Russell 1975) and many rodents (e.g. MacMillen 1965; Morhardt 1970; Buffenstein 1985;
Ruf et
al.
1991). Daily torpor also occurs during the night in many birds (see Dawson and
Hudson 1970; Reinertsen 1983). However, exclusively daily torpor has not yet been observed
in the Monotremata.
In the past, rewarming from torpor using endogenous heat production was thought
Xo be slower in marsupials than in placental mammals (Wallis 1982; Fleming 198513).
The possible reason for this perceived low rate of heat production was thought to be the
lack of brown fat in adult marsupials (Wallis 1982; Hayward and Lisson 1992). However,
two recent analyses that compared rewarming rates of a large number of marsupials,
placentals and monotremes concluded that, despite the apparent lack of brown fat in
monotremes and marsupials, there appear to be no major differences in rewarming rates
among the three subclasses (Geiser and Baudinette 1990; Stone and
Purvis 1992).
Thus, the patterns of torpor observed in the marsupials are similar to those observed in
placental mammals, monotremes and even in birds. Differences between daily torpor and
hibernation in species within some mammalian groups are greater than the differences in
torpor patterns among the three mammalian subclasses.
Evolution of Torpor
The Monotremata (Prototheria), Marsupialia (Metatheria) and Placentalia (Eutheria)
have been separated for more than 100 million years. The origin of monotremes is some-
what obscure, but it is likely that they split from the branch leading to the marsupials
and placental mammals about 180 million years ago (Dawson 1983) (Fig.
4).
Marsupials
and placentals are believed to have separated about 120 million years ago (Archer 1984).
Australian marsupials are
all
possibly derived from microbiotheriid stock
in
the late Cretaceous
(about 70 million years ago) (Archer 1984) whereas the didelphids and caenolestids developed
independently from that time (Fig. 4).
Because of their phylogenetic position, the physiology of marsupials is often used to make
predictions about the evolution of mammalian endothermy (Hulbert 1988; Dawson 1989).
Torpor in particular has attracted attention of some researchers. The original view was that
torpor, as it occurs in 'primitive' mammals such as marsupials, is both functionally and
phylogenetically a primitive trait
(Kayser 1961). Over the last decades this view was rejected.
Torpor was and still is seen by many as a sophisticated adaptation to the environment of
particular endothermic groups or species. It was proposed that torpor evolved independently
in many mammalian taxa and birds when environmental conditions required a reduction of
the high endothermic metabolism for survival (Twente and Twente 1964; Bartholomew 1986).
However, in a recent paper Augee and Gooden (1992) argue that convergent evolution
of a complex phenomenon such as hibernation seems unlikely. They point out that the
parsimonious explanation is that hibernation in mammals is a plesiomorphic (=ancestral)
trait, but that it is not functionally primitive (Augee and
Gooden 1992). If this interpretation
is correct hibernation in mammals has evolved only once and therefore must have been
modified in species displaying daily torpor or lost in strictly homeothermic species.
If torpor is plesiomorphic, all Australian marsupials, which were most likely derived from
microbiotheriid stock (Archer
1984), are descendants of a small hibernator. As all poly-
protodont Australian marsupials do not appear to enter deep and prolonged torpor the
ability to do so must have been lost; shallow, daily torpor in the dasyurids and perhaps
myrmecobiids and notoryctids would be vestigial hibernation. Most of the diprotodont
marsupials (Phascolarctidae, Vombatidae, Phalangeridae, Pseudocheiridae, Potoroidae and
Macropodidae) would have lost the ability to enter torpor entirely, two or three families
retaining the ability to undergo deep and prolonged torpor (Burramyidae, Acrobatidae and
perhaps Tarsipedidae) and one or two families retaining the ability to enter shallow daily
Torpor in Marsupials
Monotremes
1
Marsupials
I
Zaglossidae
Tachyglossidae (Hib)
Ornithorhynchidae
Didelphidae (Tor)
Caenolestidae
Microbiotheriidae (Hib)
Thylacinidae
Dasyuridae (Tor)
Myrmecobiidae (Tor?)
Notoryctidae (Tor?)
Peramelidae
Thylacomyidae
Phascolarctidae
Vombatldae
Phalangeridae
Burramyidae (Hib)
Pseudocheiridae
Petauridae (Tor)
Acrobatidae (Hib)
Tarsipedidae (Tor)
Potoroidae
Macropodidae
Placentals (Hib, Tor)
J
I
I
I
J
200
150 100 50 0
Million
years
Fig.
4.
A
phylogenetic tree of extant monotreme and marsupial families, and placentals.
The tree was largely based on Archer's
(1984)
interpretation. 'Hib' indicates that the group
contains species that have been observed in deep and prolonged torpor (hibernation);
'Tor' indicates that the group contains species that have been observed in daily torpor.
torpor (Petauridae and perhaps Tarsipedidae). Since marsupials of a particular family appear
to display the same general pattern of torpor, torpor patterns must be influenced somewhat
by phylogenetic relationships. It does not, however, prove that torpor evolved only once.
Similarities of torpor patterns could have evolved during the radiation of marsupial families.
While the argument of monophyletic evolution of torpor in mammals may be feasible,
it is inconceivable that torpor in birds, which had a separate development from mammals
for about
300
million years and appear to have developed endothermy independently from
mammals (Pough
et
al.
1989),
also are derived from this proto-hibernator. If torpor in birds
has evolved independently from mammals and torpor patterns of birds really are as similar
to those of mammals
as
has been suggested (French
1993),
there appears to be no logical
reason why torpor in various mammalian groups also evolved independently when it was
required for survival. It is possible that similarities in patterns of torpor do not reflect a
common root but a restricted number of physiological options for function at low body
temperature and metabolism in endotherms.
F.
Geiser
Apart from the available comparative data on mammalian and avian heterotherms
there is little other evidence that would help to solve the evolutionary puzzle. However,
Chaffee
(1966)
provided experimental results on breeding of hibernators in the laboratory,
which may contribute some substance to the argument. He selected hamsters,
Mesocricetus
auratus,
into 'super-hibernators' and 'non-hibernators' and concluded that already after
two generations significant differences in the occurrence of hibernation could be observed
between the two experimental groups. Although both the super-hibernators and the non-
hibernators showed a reduction in torpor occurrence from the parent generation to the
second generation, this reduction was more pronounced in the non-hibernator group.
If changes in torpor patterns do change within a few generations, a convergent development
of torpor in different taxa may be a more likely explanation than a plesiomorphic derivation
of torpor. Convergent evolution of torpor is also supported by climatic change over the last
200
million years. During the times when the various mammalian taxa separated, environ-
mental temperatures were believed to be considerably warmer than at present (Pough
et
al.
1989).
It therefore seems unlikely that the environmental pressure was strong enough to
evolve a sophisticated adaptation like hibernation. While it is possible that the first mammals
became torpid when exposed to cold temperatures or when inactive, it seems unlikely that
their pattern of heterothermy was identical to that of modern mammals with endothermic
arousal and metabolic defence of
T,
during both torpor and normothermia. Heterothermy
in ancestral mammals was most likely due to a small metabolic scope and thermoregulatory
sophistication, the pattern that was originally equated with hibernation in modern mammals.
Acknowledgments
This work was supported by the Australian Research Council. I thank Peter Baverstock
and Tim Flannery for discussions on evolution, Ian Medcalf for paleobiological data, Mike
Augee for constructive comments on the marsupial family tree and Bronwyn
McAllan
and two referees for constructive comments on the manuscript. Ian Hume and Tony Lee
provided ideas on content of the review and Francisco Bozinovic and Mario Rosenmann
provided information on
Dromiciops.
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... Hibernation or multi-day torpor is utilised by many species and has been observed for marsupials, placentals and monotremes (Geiser 1994). Echidnas living in eastern Australia have been documented utilising deep hibernation, where Tb is reduced to below 10°C, and the duration is up to several months Nicol and Andersen 1996;. ...
... Previous studies have found that the rate of rewarming from torpor is similar for marsupials, placentals and monotremes, despite the apparent lack of brown fat in marsupials and monotremes (Geiser and Baudinette 1990;Stone and Purvis 1992). Many aspects of torpor are quite similar between these subclasses, and even birds, and the differences between daily torpor and hibernation in species within mammalian groups are often greater than the differences between the subclasses (Geiser 1994). For example, minimum Tb and MR during torpor are quite similar for eastern states short-beaked echidnas Grigg et al. 1989;Nicol et al. 1992), pygmy possums (Geiser 1994), hedgehogs (Thati 1978, rodents (Heller and Hammel 1972;Florant and Heller 1977;) and even some insectivorous bats (Hock 1951;Geiser 1988). ...
... Many aspects of torpor are quite similar between these subclasses, and even birds, and the differences between daily torpor and hibernation in species within mammalian groups are often greater than the differences between the subclasses (Geiser 1994). For example, minimum Tb and MR during torpor are quite similar for eastern states short-beaked echidnas Grigg et al. 1989;Nicol et al. 1992), pygmy possums (Geiser 1994), hedgehogs (Thati 1978, rodents (Heller and Hammel 1972;Florant and Heller 1977;) and even some insectivorous bats (Hock 1951;Geiser 1988). However, species within the same mammalian group may show more of a difference in these variables and it is therefore of interest to examine torpor and hibernation in W.A. short-beaked echidnas, to determine if this geographically distinct group varies from their eastern states counterparts. ...
... While they may be more common after rain, their population sizes do not fluctuate to the same extent as the highly-fecund rodents (Dickman et al., 2001(Dickman et al., , 1999. Arid adapted dasyurids can conserve energy and water loss in unpredictable environments with fat stored in heavily incrassated tails, they have generalist diets requiring no extra water, and they exhibit heterothermy as they undergo torpor on a daily basis (Geiser, 1994;Morton, 1982). They have also evolved successful breeding strategies to exploit the unpredictable conditions of the arid zone, with extended breeding seasons, polyoestry and increased nipple number in arid species compared to non-arid species (Cardillo et al., 2003;Krajewski et al., 2000b;Morton, 1982). ...
... They exhibit extended breeding seasons (6-8 months) during which polyoestrous females can produce two litters of multiple offspring (6-10), the young of which either reach reproductive maturity in the season of their birth or the following season (Krajewski et al., 2000b;Lee et al., 1982). Persistence during drought is enhanced by physiological adaptations, such as caudal fat storage and daily periods of torpor, reducing energy requirements and water loss (Geiser, 1994;Morton, 1982). Some 30 dasyurid species occur in arid habitats and Sminthopsis, Planigale and Ningaui (subfamily Sminthopsinae) are particularly diverse with over 20 species (Van Dyck & Strahan, 2008). ...
... In this study we did not find evidence of highly fragmented or declining populations, but rather showed that gene flow within each of the study species is high and maintained by large well-connected populations throughout their distributions, though they are not truly panmictic. This is likely due to demographic and physiological adaptations of dasyurid marsupials to persist in the challenging and unpredictable conditions of the Australian arid-zone (Dickman, 2003;Geiser, 1994;Morton, 1982) which is significant, given high ...
Thesis
Full-text available
The evolution and diversification of many taxa is poorly understood in the arid regions of Australia. In this thesis, I explore the evolutionary responses of arid-occurring dasyurids to Quaternary climate change. I first review the morphology and subspecific status of the endangered northern quoll. I then generate comprehensive molecular sequences to investigate the phylogeography of six small dasyurid species (subfamily Sminthopsinae) occurring in the western arid regions of Australia. Finally, I explore contemporary gene flow in four of these species using a ddRADseq next-generation sequencing approach. The findings will have important implications for the management of arid-occurring dasyurids.
... Torpor, also known as controlled heterothermy, is characterised by inactivity, a controlled reduction in metabolic rate (hypometabolism) and body temperature (hypothermia), as well as a reduced responsiveness to external stimuli (Bligh & Johnson 1973, Lyman 1982, Geiser & Ruf 1995, Boyer & Barnes 1999. These attributes of torpor enable animals to maintain their energy balance or to minimise the rate of depletion of body energy reserves under conditions of high thermoregulatory demand or low food or water availability (Lyman 1982, Buffenstein 1985, Geiser 1994, Geiser & Ruf 1995. Controlled heterothermy is especially used in areas where climate and availability of resources are unpredictable, as well as in those areas where winters are predictably long and harsh (Lyman 1982, Lovegrove 2000. ...
Thesis
Full-text available
In many endotherms, i.e. birds and mammals, torpor is a common physiological response to changes food quantity and quality, environmental temperatures and water availability. Torpor is characterised by controlled reduction in metabolic rate and body temperature, as well as a reduced responsiveness to external stimuli, and inactivity of an animal. Traditionally, torpor (or controlled heterothermy) is associated with the high latitudes of the Northern Hemisphere, but also occurs in many endotherms in the tropical and subtropical latitudes of the Southern Hemisphere and at high ambient temperatures, possibly not only to reduce energy expenditure, but to conserve water. However, the inactivity and unresponsiveness to external stimuli of a torpid animal possibly leads to an animal’s loss of ability to avoid predation. Therefore, torpor might increase an animal’s vulnerability to predation and thus have high costs in terms of an animal’s fitness. In this study, African woodland dormice (Graphiurus murinus) were exposed to high temperatures in order to find out whether they employ torpor (by means of hypometabolism) not only at low ambient temperature, but also when exposed to increased ambient temperature. Moreover, the dormice were exposed to food reduction at different ambient temperatures in their environmental room to detect employment of torpor. Furthermore, we intended to determine whether metabolic rates of resting and torpid woodland dormice will change when the animals are exposed to olfactory predator cues. The animals’ metabolic rate and evaporative water loss were measured through open-flow respirometry, and recorded the skin temperatures of the dormice with external datalogger collars. The animals did not show signs of metabolic depression at high ambient temperatures. However, the dormice in this study showed remarkable tolerance to high ambient temperatures up to 42 °C, as well as to hyperthermia. The dormice employed torpor at moderate temperatures with free food availability. Under different ambient temperatures and food reduction, torpor employment changed by means of more, longer, and deeper torpor bouts at colder temperatures and under food restriction. Metabolic responses of both resting as well as torpid dormice to different olfactory cues were significant. The responses were strongest to cues from a predator, intermediate to herbivore cues, and lowest to odours from conspecifics of the same sex. This suggests that torpid dormice are responsive to predation risk. Moreover, our results suggest that woodland dormice are able to distinguish between different olfactory cues, and therefore possibly between predators and non-predators.
... To survive in this challenging environment, monito del monte exhibits daily torpor and hibernation (multiday torpor, Geiser 1994). This strategy helps energy storage during winter by saving 40-60% of their total daily energy needs by maintaining a decreased core temperature (Geiser 1994). ...
... To survive in this challenging environment, monito del monte exhibits daily torpor and hibernation (multiday torpor, Geiser 1994). This strategy helps energy storage during winter by saving 40-60% of their total daily energy needs by maintaining a decreased core temperature (Geiser 1994). ...
Chapter
New World marsupials have a striking diversity of activity patterns. Until now, knowledge on diel activity was normally granted by means of simple classifications, like diurnal or nocturnal. Although most activity occurs during the night, diurnal and crepuscular activities are not uncommon. New World marsupials tend to be active soon after sunset, using the first half of the night more intensely. A second peak of activity is also observed. Temporal plasticity in the group is evident: activity varies in response to changes in abiotic factors (e.g., temperature, food availability, moonlight) and intra- and interspecific interactions (e.g., predators, competitors). Several studies have focused on the effects of moonlight on suppressing activity of potential preys like marsupials. Results, however, are inconclusive; some species reduce while others increase activity in bright moon nights. The effect of seasonality in food availability and temperature were also highly investigated. Overall, marsupials increase activity in periods of reduced food availability and avoid exposure to cold environments. Future studies should focus on new methodologies which will open new possibilities for investigating activity patterns and for testing hypotheses concerning the response of New World marsupials to anthropogenic changes in the environment.
... In some species, this process is called daily torpor, which is encompassed within the circadian cycle and last less than 24 h. In contrast, some animals maintain the hypometabolism for several weeks, which is known as hibernation (Geiser, 1994;Royo et al., 2019). The behavior during these hypometabolic states resembles sleep, i.e., animals adopt a sleep-like posture, remain inactive and show substantially higher arousal thresholds (Heller and Ruby, 2004). ...
Chapter
On a daily basis, our brain alternates between several states of vigilance (or arousal) that are internally generated or, more often, generated in response to environmental cues and challenges. In this chapter, we focus on states of sleep and wakefulness, general anesthesia, as well as other nonpathological states of vigilance that occur in response to extreme environmental conditions such as torpor and hibernation. Each of these states has several unique and distinctive parameters that can be objectively assessed by observation (body posture and behaviors), as well as with more sophisticated analytical approaches (cardiorespiratory and electroencephalographic features). Here we provide operational definitions and distinctive characteristics, and introduce some quantitative analytical tools used in research and clinical settings to study these states of vigilance.
... Although this hypothesis has never been tested in hummingbirds at this scale, mass has been shown to predict the frequency of torpor use in marsupials (Geiser, 1994). Through the combination of extensive field sampling and meta-analysis, we aim to obtain a broader understanding of torpor in hummingbirds across different environments and the phylogeny. ...
Article
Full-text available
Torpor, or a regulated drop in body temperature and metabolic rate, allows animals to inhabit energetically costly environments, but among torpor‐using species, we have a poor understanding of how plasticity in torpor use relates to the experienced environment. To better understand the ecology of daily torpor, we completed the largest study to date on the intraspecific variation of daily torpor use in hummingbirds by exposing 149 individuals of two hummingbird species to ambient or experimentally cooled temperatures in a field setting. The smaller species, a latitudinal migrant, used daily torpor frequently under ambient conditions. The larger species, an elevational migrant, also used daily torpor regularly, but further increased the frequency of daily torpor use when experiencing colder temperatures and prior to migration—indicating a facultative adaptation. To place our results within a broader phylogenetic context, we combined our experimental results with a meta‐analysis, including 31 species and all major hummingbird clades, and found a broad taxonomic pattern in which smaller hummingbirds are more likely to use daily torpor than their larger counterparts. Smaller hummingbirds may be physiologically constrained, requiring nearly obligate daily torpor use, while larger hummingbirds are physiologically more flexible and can facultatively respond to changing environmental conditions. Our results reveal how physiological traits, such as the frequency and depth of daily torpor, can provide a mechanism to understand how hummingbird species have established and persisted across broad environmental gradients. A free Plain Language Summary can be found within the Supporting Information of this article.
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Hibernation (i.e., seasonal or multiday torpor) has been described in mammals from five continents and represents an important adaptation for energy economy. However, direct quantifications of energy savings by hibernation are challenging because of the complexities of estimating energy expenditure in the field. Here, we applied quantitative magnetic resonance to determine body fat and body composition in hibernating Dromiciops gliroides (monito del monte). During an experimental period of 31 d in winter, fat was significantly reduced by 5.72±0.45 g, and lean mass was significantly reduced by 2.05±0.14 g. This fat and lean mass consumption is equivalent to a daily energy expenditure of hibernation (DEEH) of 8.89±0.6 kJ d-1, representing 13.4% of basal metabolic rate, with a proportional contribution of fat and lean mass consumption to DEEH of 81% and 18%, respectively. During the deep heterothermic bouts of monitos, body temperature remained 0.41°C ± 0.2°C above ambient temperature, typical of hibernators. Animals shut down metabolism and passively cool down to a critical defended temperature of 5.0°C ± 0.1°C, where they begin thermoregulation in torpor. Using temperature data loggers, we obtained an empirical estimation of minimum thermal conductance of 3.37±0.19 J g-1 h-1 °C-1, which is 107% of the expectation by allometric equations. With this, we parameterized body temperature/ambient temperature time series to calculate torpor parameters and metabolic rates in euthermia and torpor. Whereas the acute metabolic fall in each torpor episode is about 96%, the energy saved by hibernation is 88% (compared with the DEE of active animals), which coincides with values from the literature at similar body mass. Thus, estimating body composition provides a simple method to measure the energy saved by hibernation in mammals.
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Invertebrates dominate the animal world in terms of abundance, diversity and biomass, and play critical roles in maintaining ecosystem function. Despite their obvious importance, disproportionate research attention remains focused on vertebrates, with knowledge and understanding of invertebrate ecology still lacking. Due to their inherent advantages, usage of camera traps in ecology has risen dramatically over the last three decades, especially for research on mammals. However, few studies have used cameras to reliably detect fauna such as invertebrates or used cameras to examine specific aspects of invertebrate ecology. Previous research investigating the interaction between wolf spiders (Lycosidae: Lycosa spp.) and the lesser hairy-footed dunnart ( Sminthopsis youngsoni ) found that camera traps provide a viable method for examining temporal activity patterns and interactions between these species. Here, we re-examine lycosid activity to determine whether these patterns vary with different environmental conditions, specifically between burned and unburned habitats and the crests and bases of sand dunes, and whether cameras are able to detect other invertebrate fauna. Twenty-four cameras were deployed over a 3-month period in an arid region in central Australia, capturing 2,356 confirmed images of seven invertebrate taxa, including 155 time-lapse images of lycosids. Overall, there was no clear difference in temporal activity with respect to dune position or fire history, but twice as many lycosids were detected in unburned compared to burned areas. Despite some limitations, camera traps appear to have considerable utility as a tool for determining the diel activity patterns and habitat use of larger arthropods such as wolf spiders, and we recommend greater uptake in their usage in future.
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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.
Article
Body temperatures, oxygen consumption and the thermal response of liver mitochondrial membranes of the Common Dunnart, Sminthopsis murina, were measured during winter and the summer mating season. In winter body temperatures for S. murina during spontaneous torpor were as low as 15oC and oxygen consumption was reduced to 6% of normothermic resting animals. In summer animals remained normothermic. For the winter animals liver mitochondrial succinate oxidase and succinate: cytochrome c reductase showed a constant apparent Arrhenius activation energy (Ea) over the temperature range 6 to 40oC. For summer animals Ea increased below about 20oC. The temperature coefficient for the motion of spin labels intercalated with membrane lipids increased below about 8oC for membranes from winter animals and below 20oC for summer animals.
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Long-tailed Pygmy Possums Cercartetus caudatus were bred in captivity. Twice yearly breeding was indicated by the births of young to captive females, and by peaking and regression of the testes width of the male. Litter sizes were up to four, and young were first recorded emerging from the pouch at 34 ± 5 days. Young become independent at 92 ± 10 days. Females raised in captivity first bred at the age of 15 months. Maximum longevity of captive born individuals was 38 months. Torpidity was observed in a tropical climate.
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Tarsipes rostratus is a 5-15 g marsupial with a natural distribution restricted to shrublands and heathlands of southwestern Australia. In the laboratory, it has metabolic rates that vary from 150-350 J (g.h)-1, and does not become torpid if artificial nectar is available. When nectar is removed, animals ultimately become torpid for intervals of several hours, during which metabolic rates are often reduced by more than 90%. The time taken by animals to become torpid is reduced, and the duration of torpor bouts increased, if body size and ambient temperature are decreased. By becoming torpid under the experimental conditions imposed, animals reduce their total daily energy expenditures by approximately 70%. It is suggested that torpor occurs when the energy reserves of animals fall below a critical level. In the field, torpor is most prevalent in animals the weight less than 7 g, and occurs predominantly during the period from March to September. Evidence relating to possible causes of torpor in the field is equivocal.
Article
The Mountain Pygmy-possum Burramys parvus is restricted to the Australian alpine region. Laboratory studies of the thermo-physiology of this species found that body temperature (Tb) was tightly regulated at 36.1oC, but animals quickly become hyperthermic at ambient temperatures (Ta) above 30oC, causing the thermal neutral zone to be truncated. Basal metabolic rate was 2.15 W kg -0.75 (mean body mass 44.3 g) and weight-specific thermal conductance was 0.112 ml O2, g-1 h-1 oC-1. These values are 9% and 44% lower, respectively, than the mass predicted value for a marsupial, showing that the overall rate of energy expenditure is considerably reduced in this species. Huddling also reduces individual rates of energy expenditure. Burramys parvus enters prolonged bouts of deep torpor lasting up to one week, during which Tb is very low and close to Ta and the rate of oxygen consumption greatly reduced. Spontaneous arousal occurred from a Tb as low as 6oC and the overall rate of rewarming was 0.17 oC /min. Attainment of a critical body mass appeared to be necessary before an animal would enter torpor. Burramys parvus shows physiological adjustments similar to that described in many placental mammals from cold climates and this species represents a true marsupial hibernator.
Chapter
The temperature drop and the subsequent energy conservation is the key to the biological success of hibernation. The state of torpor is, however, accompanied by other dramatic changes. During the winter some species of hibernator hardly touch food during their periodic arousals even though it is present. In contrast to this prolonged anorexia, they eat voraciously in the prehibernation stage and routinely achieve spectacular metabolic prosperity. Their body weights show corresponding fluctuations. Water intake generally parallels food intake. Reproduction does not normally occur in the winter, and there is a seasonal atrophy of the gonads and of various other glands. Kayser (1961) lists such endocrine changes and also weight loss as useful in characterizing a species as a hibernator.