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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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