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First published online January 31, 2007
Journal of Experimental Biology 210, 586-592 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.02701
Cooling rates and body temperature regulation of hibernating echidnas (Tachyglossus aculeatus)
1School of Zoology, University of Tasmania, Private Bag 5, Hobart, Tasmania, 7001, Australia and 2Discipline of Anatomy and Physiology, University of Tasmania, Private Bag 24, Hobart, Tasmania, 7001, Australia
* Author for correspondence (e-mail: s.c.nicol{at}utas.edu.au)
Accepted 18 December 2006
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Summary |
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 TOP Summary IntroductionMaterials and methodsResults and data analysisDiscussionList of abbreviationsReferences |
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Key words: echidna, monotreme, hibernation, cooling, thermoregulation, conductance
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResults and data analysisDiscussionList of abbreviationsReferences |
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). When an
endotherm enters hibernation there is a drop in metabolic rate (MR) and
Tb, and as long as ambient temperature
(Ta) is not too low, Tb will fall to a
value typically 1–3°C above ambient. If Tb falls
below a critical value, MR will increase, but when a hibernating endotherm is
undisturbed and its Tb is above the critical value,
Tb will passively follow Ta, i.e. it
will thermo-conform (Geiser,
2004).
When first described in the scientific literature, hibernation in the
egg-laying echidna (Tachyglossus aculeatus) was interpreted as a
confirmation that the echidna was an incomplete homeotherm
(Martin, 1902). Since that
time it has been demonstrated that hibernation in the echidna closely
resembles that of other mammals (Grigg et
al., 2004; Nicol and Andersen,
2002), although with an adult body mass of 2–7 kg the
echidna is one of the largest species to enter deep hibernation
(Geiser, 2004;
Nicol and Andersen, 2007a).
Over the last 10 years we have studied hibernation in free-ranging echidnas in
the field using implanted Tb data-loggers, and have
collected a very large data set of more than 39 echidna years of data from 14
animals. We have previously analysed parts of this data set data to examine
the relationship between Tb and hibernation bout length
(Nicol and Andersen, 2000),
the timing and patterns of hibernation
(Nicol and Andersen, 2002),
and rewarming rates and thermogenesis
(Nicol and Andersen, 2007b).
These data show that during the hibernation season Tb
appears to follow Ta quite closely. In the laboratory, we
noted a slight increase in Tb, MR and ventilation when
Ta fell below 5°C
(Nicol and Andersen, 2003;
Nicol et al., 1992), and if
the low Ta was sustained, or if cooling was too rapid, the
echidna would arouse from hibernation. In this paper we make a detailed
analysis of Tb in hibernating echidnas. Is there any
evidence that echidnas under natural conditions regulate
Tb when Ta falls below a certain
level?
Our data set includes a large number of cooling episodes as echidnas enter
bouts of hibernation. The physiological changes associated with entry into
hibernation and torpor have been the subject of considerable debate,
particularly with respect to the causal relationship between the reduction in
Tb and MR, and the relative timing of these changes
(Geiser, 2004;
Heldmaier and Elvert, 2004).
Although our data do not include measurements of MR, we are able to make some
estimates of thermal conductance (C), which in turn allows some
inferences to be made about MR. It has been argued, for example, that entry
into hibernation and torpor is associated with an initial increase in
C, which is then reduced to levels below the euthermic minimum
(Snyder and Nestler, 1990).
Conductance can be calculated from thermal time constants calculated from
cooling curves (Robertson and Smith,
1981), and this approach has been used extensively in studies on
the thermal properties of ectothermic animals
(Bakken, 1976;
McNab, 2002). Cooling
constants are independent of Ta and
Tb, and are preferable to measures such as the time
required to reach a specific temperature, or rates of change of temperature,
as these will vary with the difference between Tb and
Ta. This approach has had only limited use with
endotherms; it has been used to calculate C of torpid dormice
(Wilz and Heldmaier, 2000) and
to characterise the entry of humming birds into torpor
(Lasiewski and Lasiewski,
1967). Because echidnas normally bury themselves in the substrate
before entering hibernation they are sheltered from convective and radiant
heat exchange with the environment. Under these circumstances Newton's Law of
Cooling should be applicable, and in the second part of this paper we
investigate the use of this model to characterise cooling in echidnas entering
hibernation, and to estimate C.
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Materials and methods |
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TOPSummaryIntroductionMaterials and methodsResults and data analysisDiscussionList of abbreviationsReferences |
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Meteorological data including soil temperature measured at depths of 10, 20 and 50 cm, were obtained from an Australian Bureau of Meteorology (BoM) observation station (Melton Mowbray, 147°11'44''E, 42°29'35''S, elevation 218 m) approximately 4.5 km from the centre of the field site. These data were recorded daily to the nearest 1°C at 09:00 h and in some years at 15:00 h. To check the applicability of the BoM data to the field site itself, soil temperatures were measured at several points in the field site for periods of up to 8 months.
Data analyses were carried out using the statistical packages statistiXL (statistiXL, Kalamunda, Western Australia) and Statistica 6.1 (Statsoft Inc, Tulsa, OK, USA), and all results are shown as means ± s.d.
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Results and data analysis |
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TOPSummaryIntroductionMaterials and methodsResults and data analysisDiscussionList of abbreviationsReferences |
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), as has an analysis of rewarming
(Nicol and Andersen, 2007b). A
comparison of the Tb records with the various
environmental measures obtained from the BoM station (air temperature and soil
temperature at 10, 20 and 50 cm) showed that, during hibernation,
Tb varied in parallel with soil temperature at 20 cm,
although the absolute difference between the records would sometimes change.
Air temperature and soil temperatures at 10 cm showed a much greater variance
than Tb, while soil temperature at 50 cm had a lower
variance than Tb (Table
1). Recordings of soil temperature at several locations in the
field site were found to correspond closely with the BoM data: a 4-month
recording of soil temperature in what we judged to be the coldest part of the
field site, when plotted against the BoM data, yielded a regression line with
a slope of 1.04±0.04, and an intercept of –4. Thus although the
absolute values of soil temperature varied around the field area, as would be
expected, the BoM data accurately reflected the pattern of temperature change.
Hence the BoM soil temperature measurements at 20 cm have been used as a
reference substrate temperature (Tref). In the nine
winters over which we collected Tb data (1997–2005)
Tref fell below 5°C on only 23 days, and only once
fell below 4°C. Fig. 1
shows the Tb and Tref records for an
echidna (male 4572) over the 2000 hibernation period, demonstrating the
remarkably close correspondence between the two temperatures.
Fig. 2 shows
Tb records from early in hibernation for echidna 4572, as
well as three other echidnas (females 2753 and 006F and male 1E7C), all
hibernating at different locations, up to about 2 km apart. Each animal
appears to track the changes in Tref although the absolute
temperature varies between echidnas.
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Fig. 1 shows that for an individual echidna the relationship between Tb and Tref may change during the course of a hibernation season, and that these changes occur during arousals. In the initial bout of hibernation, before arousal 1, Tb is lower than Tref. Between arousals 1 and 4, Tb is very close to Tref, and between arousals 4 and 6, Tb was about 4°C above Tref. Between arousals 6 and 8, Tb was again very close to Tref, and then from arousal 8 until the final arousal, Tb was about 1°C above Tref.
In order to analyse the relationship between Tb and Tref further, Fig. 3 shows plots of hibernating Tb against Tref for two echidnas for which we have several years of data. ANOVA showed the relationships between Tb and Tref to be essentially identical for the two animals (comparison of slopes: F=0.17, P=0.68, common slope=0.63; comparison of intercepts: F=0.99, P=0.32). In Fig. 4 the frequency distribution of Tb for six echidnas (five female and one male) is compared with the distribution of Tref for the months of May and July. In May the majority of Tref readings (70%) were in the range 9–12°C, as were 70% of Tb readings, but Tb values less than 9°C are under represented (4%) compared with Tref (17%). In July the distribution of Tb values is offset significantly compared with Tref. 58% of recorded Tref values were between 6 and 8°C, but 62% of Tb values were between 8 and 10°C.
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Discussion |
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TOPSummaryIntroductionMaterials and methodsResults and data analysisDiscussionList of abbreviationsReferences |
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). For echidnas, a comparison of corresponding
Tb and Tref values for the last
hibernation bout before arousal of reproductively active males and females
showed that at any given Tref there was no difference in
Tb between females and males. There were consistent
differences between hibernating sites: echidnas hibernating in the middle of
piles of logs were extremely well buffered from environmental variation, while
the lowest Tb values were observed in echidnas hibernating
in grass tussocks.
The lowest Tb recorded in this study was 4.7°C,
observed in three echidnas, which is close to the minimum of 4.5°C seen in
the laboratory (Nicol and Andersen,
1993). A minimum Tb of 3.7°C was reported
at Mount Kosciuszko at a Ta of 0.8°C
(Grigg et al., 1992), but this
was calculated from the pulse rate of a Tb transmitter
recorded on a tape recorder, which is subject to a number of significant
potential errors, particularly at low temperatures. Our field data give no
indication that echidnas will increase heat production and thermoregulate if
Tb falls below some critical minimum value. Nowhere in the
39+ years of Tb records from 14 echidnas is there any
indication of a change in the relationship between Tb and
Tref occurring anywhere other than during an arousal.
Attempts to measure Ta near hibernating echidnas have
suggested a higher Tb–Ta
difference at low Ta, but the data are inconclusive
(Grigg et al., 1992). Similarly
laboratory data that showed increased metabolic rate and ventilation at low
Ta (Nicol and
Andersen, 1993; Nicol et al.,
1992) may be the result of transient disturbances in response to
the lowered Ta, or the beginning of arousal. In the field,
when Tb falls too far, or too fast, echidnas will arouse
and move to a warmer location to maintain Tb in the
preferred range. Fig. 4 shows
that in the coldest month of the year the preferred Tb of
hibernating echidnas is 8–10°C, with 62% of recorded values being in
that range. In our study area echidnas appear always to select hibernating
conditions that allow them to be thermoconformers.
Cooling during entry into hibernation
In euthermic endotherms below their thermoneutral zone, C is
minimal and Tb is regulated by adjusting heat production
as described by the familiar Scholander–Irving model
(McNab, 2002):
 | (1) |
O2 is rate of heat
production, expressed as oxygen consumption. During thermoconforming
hibernation, this equation can be rearranged with Tb as
the dependent variable:
 | (2) |
Fig. 5 shows arousal events
and the subsequent re-entry into hibernation for two echidnas, with semi-log
plots of the cooling phase. The slope of the regression line fitted to these
data is the exponent a, or cooling constant, in the equation for
Newton's law of cooling (McNab,
2002):
 | (3) |
 | (4) |
):
 | (5) |
The average value of a calculated from 28 cooling curves was
–0.079±0.010 h–1. The reciprocal of the cooling
constant is the time constant, and the average time constant was
12.9±1.9 h. An exponential curve falls by 1/e (
0.37)
during one time constant, and three time constants represent a 95% response,
providing a useful measure of the time required to equilibrate. The 95%
response time for echidna cooling was 39±6 h (N=28). Because
cooling takes several days, daily torpor with a stable torpid
Tb is clearly not an option for echidnas. The low rate of
cooling contrasts strongly with what would be expected from an ectotherm: for
an alligator of a similar mass (approx. 4 kg) the 95% cooling time in air
would be about 3.25 h (Smith,
1976), demonstrating that a hibernating echidna has a very low
conductance.
The cooling constant, a, for an animal is a function of its body
mass (Mb), specific heat (h) and its thermal
conductance (C) (Bakken,
1976), i.e. a=C/hMb. With a
body fat composition of 25–35% (Green
et al., 1992), specific heat of echidna tissues would average 3.35
J g–1 °C–1, and the average C
during the cooling episodes would be 0.024±0.003 J g–1
° h–1 C–1. Assuming a heat equivalent of
oxygen of 20.1 J ml–1, this can be expressed in terms of
oxygen consumption as 0.013±0.002 ml O2 g–1
h–1 °C–1, identical to the value of
0.013±0.0005 measured in cold-exposed, non-hibernating Tasmanian
echidnas (McNab, 1984).
Similarly, when C of dormice (Glis glis) was calculated
from cooling curves, no change was found in C during entry into
torpor and during hibernation, and daily torpor C was identical to
the value measured in cold exposed euthermic dormice
(Wilz and Heldmaier, 2000).
Our results for the echidna provide no support for the suggestion
(Snyder and Nestler, 1990)
that entry into torpor is facilitated by changes in C.
The very close fit of a Newtonian cooling curve to our data
(Fig. 5), supports the comment
(Lasiewski and Lasiewski,
1967) for humming birds entering torpor: "The lowering
of body temperature during entry into torpor approximates a Newtonian cooling
curve, suggesting that once entry into torpor is initiated, the rate of entry
is determined by physical phenomena." Although the slope of the
line, and thus the calculated C, will not be affected by a constant
rate of heat production, it will be affected if MR varies with
Tb (Bakken and Gates,
1974), but in previous laboratory experiments, we were unable to
find any relationship between Tb and MR in hibernating
echidnas (Nicol et al., 1992).
A similar independence of MR from Tb has been observed in
a variety of hibernating rodents during thermoconforming hibernation at low
Tb (Buck and Barnes,
2000; Heldmaier and Elvert,
2004; Heldmaier et al.,
1993; Ortmann and Heldmaier,
2000). Although some small hibernators show a temperature effect
on hibernating MR, particularly at high Tb
(Geiser, 2004), the linearity
of the semi-log plots of the echidna cooling curves
(Fig. 5) implies that there is
no significant change in echidna heat production or conductance during the
cooling period.
These results help us to understand how echidnas use hibernation. It has
been well documented that echidnas do not hibernate to avoid periods of
extreme cold or absolute food shortage
(Grigg and Beard, 2000;
Nicol and Andersen, 1996;
Nicol and Andersen, 2002).
Grigg and Beard (Grigg and Beard,
2000) have described echidnas as "using cold as a
resource"; they use hibernation to conserve energy, although food
is available, and conditions may be mild, when there is no necessity for them
to be active. Early in the hibernation season when soil temperatures are high,
echidnas will seek out cooler places to hibernate, but in the coldest months
they prefer hibernacula where they can maintain Tb in the
range 8–10°C. Thermal buffering against excessive variation in
Tb may be just as important as maintaining a low
Tb.
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List of abbreviations |
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TOPSummaryIntroductionMaterials and methodsResults and data analysisDiscussionList of abbreviationsReferences |
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O2
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Acknowledgments |
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References |
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TOPSummaryIntroductionMaterials and methodsResults and data analysisDiscussionList of abbreviationsReferences |
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