Respiration by buried echidnas Tachyglossus aculeatus

Abstract

Short-beaked echidnas have an impressive ability to submerge completely into soil or sand and remain there, cryptic, for long periods. This poses questions about how they manage their respiration, cut off from a free flow of gases. We measured the gradient in oxygen partial pressure (PO2) away from the snouts of buried echidnas and oxygen consumption (VO2) in five individuals under similar conditions, in two substrates with different air-filled porosities (fa). A theoretical diffusion model indicated that diffusion alone was insufficient to account for the flux of oxygen required to meet measured rates of VO2. However, it was noticed that echidnas often showed periodic movements of the anterior part of the body, as if such movements were a deliberate effort to flush the tidal air space surrounding their nostrils. These ;flushing movements' were subsequently found to temporarily increase the levels of interstitial oxygen in the soil around the head region. Flushing movements were more frequent while VO2 was higher during the burrowing process, and also in substrate with lower fa. We conclude that oxygen supply to buried echidnas is maintained by diffusion through the soil augmented by periodic flushing movements, which ventilate the tidal airspace that surrounds the nostrils.

Full text

938
Introduction
Short-beaked echidnas (Tachyglossus aculeatus) are famous
for many unusual characteristics, among them the ability to
avoid capture or predation by ‘sinking’ into the soil until only
the tips of the dorsal spines are visible (Burrell, 1926) and
remaining there, holding fast against attempts to dislodge
them, for long periods. This behaviour poses questions about
how echidnas manage their respiratory gas exchange, cut off
from a free flow of gases and threatened by the risk of inhaling
particles of soil.
It is clear that echidnas are frequently exposed, at least for
short periods, to increased hypoxia and hypercapnia, either
when digging into soil or within their burrows (Augee et al.,
1971). Previous studies have demonstrated that echidnas are
physiologically well suited for burrowing. Augee et al.
(Augee et al., 1971) covered echidnas with soil to simulate
natural conditions and found them to be very tolerant of high
carbon dioxide (CO
2
) and low oxygen (O
2
) under these
conditions.
However, no studies have explored the processes by which
O
2
supply is maintained while an echidna is buried, completely
surrounded by soil, without any tunnel to facilitate the
convective movements of gas. Presumably echidnas re-breathe
the interstitial gas around them while buried. The diffusive
transport of O
2
to a buried mammal was explored in the Namib
Desert golden mole Eremitalpa granti namibensis (Seymour
and Seely, 1996), which survives long periods buried in sand.
By comparing measurements of the P
O
2 gradient away from
the snout of a buried mole to the P
O
2 gradient predicted from
a mathematical model of gaseous diffusion through sand,
Seymour and Seely (Seymour and Seely, 1996) explained that
golden moles can survive being buried in sand by utilizing O
2
diffusing through sand into the tidal air space that surrounds
the snout. However, their model predicted an upper size limit
of approximately 200·g for resting mammals able to continue
respiration in this manner. Echidnas are commonly 2–4·kg
and can reach 7·kg, so the model used to explain sub-sand
respiration by the golden mole cannot by itself explain the
submergence capabilities observed in echidnas.
In this study we took a similar approach to that of Seymour
and Seely (Seymour and Seely, 1996). We measured the P
O
2
gradient away from the snouts of submerged echidnas and V
O
2
in separate experiments on five individuals under similar
conditions, in two media with differing porosity f
a
values, with
the hope of determining how echidnas can remained buried for
long periods of time.
Materials and methods
Echidnas
Five echidnas Tachyglossus aculeatus Shaw (2.34–4.18·kg)
previously fitted intraperitoneally with calibrated temperature
Short-beaked echidnas have an impressive ability to
submerge completely into soil or sand and remain there,
cryptic, for long periods. This poses questions about how
they manage their respiration, cut off from a free flow of
gases. We measured the gradient in oxygen partial
pressure (P
O
2) away from the snouts of buried echidnas
and oxygen consumption (V
O
2) in five individuals under
similar conditions, in two substrates with different air-
filled porosities (f
a
). A theoretical diffusion model
indicated that diffusion alone was insufficient to account
for the flux of oxygen required to meet measured rates of
V
O
2. However, it was noticed that echidnas often showed
periodic movements of the anterior part of the body, as if
such movements were a deliberate effort to flush the tidal
air space surrounding their nostrils. These ‘flushing
movements’ were subsequently found to temporarily
increase the levels of interstitial oxygen in the soil around
the head region. Flushing movements were more frequent
while V
O
2 was higher during the burrowing process, and
also in substrate with lower f
a
. We conclude that oxygen
supply to buried echidnas is maintained by diffusion
through the soil augmented by periodic flushing
movements, which ventilate the tidal airspace that
surrounds the nostrils.
Key words: monotreme, burrowing, respiration, gas exchange,
oxygen consumption, echidna.
Summary
The Journal of Experimental Biology 209, 938-944
Published by The Company of Biologists 2006
doi:10.1242/jeb.02063
Respiration by buried echidnas Tachyglossus aculeatus
Courtney A. Waugh, Gordon C. Grigg, David T. Booth* and Lyn A. Beard
School of Integrative Biology, University of Queensland, Brisbane, Australia 4072
*Author for correspondence (e-mail: d.booth@uq.edu.au)
Accepted 22 December 2005
THE JOURNAL OF EXPERIMENTAL BIOLOGY

939Respiration by echidnas while buried
transmitters were used. Animals had been collected previously
from Idalia National Park (latitude 24°53⬘S, longitude
144°46⬘E), 113·km WSW of Blackall in Australia’s semi-arid
zone (Brice et al., 2002), and the Texas area, 50·km SW of
Stanthorpe in SE Queensland (latitude 28°43⬘S, longitude
151°28⬘E). The animals were held in a free-range enclosure
at the University of Queensland’s Pinjarra Hills Veterinary
Farm.
Modelling the diffusive exchange of respiratory gases
The diffusion model (Seymour and Seely, 1996) assumes
that the buried animal is surrounded completely by a medium
that permits O
2
to diffuse radially towards it from all directions.
This assumption is supported by empirical data (Seymour and
Seely, 1996; Wilson and Kilgore, 1978; Withers, 1978). In a
steady state, the amount of O
2
diffusing radially through a
given spherical shell is equal to the rate at which it is
consumed. As O
2
diffuses radially toward the animal, the
volume through which it passed decreases and, therefore, the
changes in ambient P
O
2 shell by shell, with decreasing distance
to the animal, can be calculated from the equation (Seymour
and Seely, 1996):
V
O
2 = K
O
2(P
o
–P
i
)4␲r
o
r
i
/r
o
– r
i
·, (1)
where V
O
2 is the rate of oxygen consumption (cm
3
·min
–1
),
K
O
2 is the diffusion coefficient of oxygen in substrate
(cm
2
·min
–1
·kPa
–1
), P
o
and P
i
are the oxygen partial pressures
(kPa) at the outer (r
o
) and inner (r
i
) radii of a given spherical
shell (cm). The following additional assumptions were
made for the model: (1) K
O
2 was the product of the binary
diffusion coefficient of oxygen in air (D
O
2=12.1cm
2
·min
–1
at 25°C) (Nobel, 1983), the O
2
capacitance of air
␤
O
2=–0.0098cm
3
·cm
–3
·kPa
–1
(Seymour and Seely, 1996) and
the air-filled porosity coefficient=f
a
1.5
(Marshall, 1959;
Seymour and Seely, 1996). K
O
2 was therefore taken as
0.032·cm
2
·min
–1
·kPa
–1
in coarse sand of f
a
=0.42, and
0.053·cm
2
·min
–1
·kPa
–1
in kitty litter (a water absorbent
granular substance made from recycled newspaper) of f
a
=0.580
(see later). (2) P
o
was assumed in the earlier study (Seymour
and Seely, 1996) to be atmospheric at r
o
=100·cm. In our case,
the echidna was in a large plastic bin and the surface through
which diffusion was possible was therefore constrained. The
environment of this experiment is therefore more inimical to
gaseous diffusion than that on which the model is based, and
that needs to be kept in mind when interpreting the results. (3)
The internal radius was the radius of a sphere of sand
containing a volume of interstitial gas equal to the tidal volume
of the animal’s breath (Seymour and Seely, 1996). This
assumption is based on the premise that a volume of interstitial
air in the sand, equal to tidal volume, was constantly being re-
breathed and mixed by the animal. The radius of this ‘tidal
space’ was calculated using the equation (Seymour and Seely,
1996):
r
i
= (3VT/4␲f
a
)
1/3
·, (2)
in which VT is the tidal volume. VT (cm
3
) was calculated from
animal mass (kg) using an equation for echidnas (Bech et al.,
1992), VT=8.96·ml·kg
–1
.
To apply the model to echidnas, V
O
2 values and P
O
2
gradients away from buried animals were measured separately,
and the assumption made that the V
O
2 measured while
submerged was indicative of the V
O
2 during measurement of
the P
O
2 gradient, as was done previously with the golden mole
(Seymour and Seely, 1996).
Measurement of
V
O
2
V
O
2 was measured using a flow-through respirometry
system, at an ambient temperature of 25°C. Each animal was
placed in an air tight, 50·cm deep and 40·cm in diameter,
cylindrical chamber k-filled with a test medium into which
the echidnas could burrow. Gas entered the chamber into an
air space above the burrowing medium and was extracted
from below the burying medium through a wire mesh-
covered hole at the base of the chamber. Two media with
differing f
a
values were used and each animal was exposed to
each medium. The f
a
of each of the two media was measured
by filling a 1000·ml graduated cylinder with the medium and
slowly adding it to 1000·ml of water in a 2000·ml cylinder,
avoiding any bubbles (Seymour and Seely, 1996). The kitty
litter, which would otherwise have absorbed water, was first
sprayed with a water repellent spray (Motortech, Balchan
International, Australia). While this method discounted any
porosity of the kitty litter itself, we consider this to have been
negligible.
The lid of the respirometry chamber was transparent, so lung
ventilation movements could be directly observed during these
experiments even when the animal was completely buried (the
surface of the substrate moved slightly with each breath). The
behaviour of an animal on introduction to the respirometry
chamber, whether for V
O
2 or P
O
2 gradient measurements, was
to burrow immediately vertically downward until submerged
completely in the substrate, a behaviour identical to that of
echidnas burying themselves in the wild. V
O
2 was measured
while the animal remained buried. Resting metabolic rate was
considered to have been reached when the animal had been
submerged and resting for 4·h and the fractional concentration
of O
2
in the excurrent air was stable. Air from the chamber was
passed through small diameter tubing to a CO
2
absorbent (Soda
Lime) and then a desiccant (Drierite
TM
) before passing into a
mass flow meter (MFS-1; Sable Systems, Las Vegas, NV,
USA). The mass flow meter pulled air though the chamber and
its exhalent air was sampled via an oxygen analyser (Sable
Systems PA-1B) calibrated with oxygen-free gas (0.00% O
2
)
and room air (20.95% O
2
). The flow rate through the
respirometry chamber was 750·ml·min
–1
in all cases. Body
temperature T
b
was monitored throughout the measurement
period using the implanted temperature transmitter and a radio
receiver connected to a pulse meter. The output voltage from
the O
2
analyser and pulse meter were fed into PowerLab
hardware (ADInstruments, Sydney, NSW, Australia)
connected to a computer running Chart5 software (v5.0.1.
ADInstruments).
THE JOURNAL OF EXPERIMENTAL BIOLOGY

940
Measurement of P
O
2
at different distances from the snout in
buried echidnas
Measurements of P
O
2 within the substrate surrounding
buried echidnas were performed in a large cylindrical plastic
bin (measurements given above) at an ambient temperature of
25°C. Experiments were commenced by placing the animal on
top of the substrate and, in all cases, echidnas burrowed
immediately until they were completely submerged.
Gas samples from the snout region were collected through
silicone tubing (1·mm i.d.) after flushing dead space from the
tubing into 3·ml plastic syringes. The tip of this tube was
secured onto the nose of the animal above the nostril using a
combination of medical glue (collodian) and micropore tape.
To measure the P
O
2 gradient within the medium away from
the snout region, further lengths of silicon tubing were attached
at 2·cm intervals along the initial tubing, up to 10·cm away
from the snout tip.
Gas samples (2·ml) were analysed for O
2
content with
a thermally stabilised Clarke Oxygen Electrode (DOX,
Analytical Sensors, Inc., Sugarland, TX, USA), connected to
a Radiometer PHM73 gas analyser (Copenhagen, Denmark),
calibrated with outside air (20.95% O
2
) and oxygen-free gas.
Gas samples were taken immediately on submergence of the
echidna, and further samples were taken at 15·min intervals for
a 5·h period. Each animal was measured individually in each
of the media. T
b
was also monitored throughout these
experiments using the implanted temperature transmitter.
Measurement of P
O
2
and movement
During trial measurements of O
2
tensions around buried
echidnas, the animals would move periodically. Such
movements would be followed by a rise in P
O
2 levels in the
substrate, seemingly as a result of these movements. To
determine if there was a causal relationship between the
movements of echidnas in different substrates and the P
O
2
measured in the snout region while submerged, a piezoelectric
movement sensor (Sigma Delta technologies, Perth, Western
C. A. Waugh and others
Australia) was attached to the echidnas. This sensor was
wrapped in electrical tape and glued to a dorsal spine on the
shoulder region of the animal. The output voltage from the
movement sensor was recorded, simultaneously with T
b
and measured P
O
2 samples, using PowerLab hardware
connected to a computer running Chart5 software (v5.0.1.
ADInstruments). Respiration rate and larger ‘flushing
movements’ were detected by the movement sensor (Fig.·1).
Statistics
All results are presented as means ± s.d. Differences
between empirical and theoretical values of P
O
2 in substrate
surrounding buried echidnas were tested using paired t-tests.
Significance was assumed at P<0.05.
Results
Data were collected on V
O
2 of each echidna, the P
O
2 in the
snout region, and movement and activity level while
submerged in two different substrates, coarse sand (f
a
=0.42)
and kitty litter (f
a
=0.58).
V
O
2
measurements while submerged
V
O
2 measurements were taken at a chamber temperature of
25°C. As would be expected, V
O
2 was greater during burrowing
than resting, and substrate type did not influence resting rate
of V
O
2 (Table·1). T
b
and respiration rate always decreased
during the course of V
O
2 measurements. T
b
of echidnas at the
start of the experiments ranged from 27.0 to 34.5°C and, on
average, decreased 2.2±1.3°C (N=5) during a trial. Respiration
decreased from 12.0±0.5 to 4.6±2.2·breaths·min
–1
over the 5·h
measurement period.
P
O
2
gradient in substrate while submerged
P
O
2 measurements were taken at an ambient temperature of
25°C. The mean atmospheric P
O
2 was 19.7·kPa (range
19.3–19.9·kPa) in water-saturated air. The P
O
2 level in each
0
0 10203040506070
5 101520253035
–0.02
–0.01
0
0.01
0.02
–0.02
–0.01
0
0.01
0.02
Voltage (V)
Time (s)
AB
Fig.·1. Voltage output from the movement sensor when attached to the shoulder region of a buried echidna. (A) Lung ventilation movements;
increase in voltage represents inspiration, and decrease, expiration. (B) ‘Flushing movements’, indicated by dark horizontal bars as well as lung
ventilation movements.
THE JOURNAL OF EXPERIMENTAL BIOLOGY

941Respiration by echidnas while buried
substrate, without an echidna, was atmospheric. P
O
2 levels of
gas samples from near the snout of echidnas buried in the
medium were always below the atmospheric level, even
immediately after burial. The mean minimum P
O
2 values at the
tip of the echidna’s snout during burrowing in each substrate
were 12.1±1.4·kPa in coarse sand (f
a
=0.42, N=5) and
12.3±1.4·kPa in kitty litter (f
a
=0.58, N=5). Gas samples taken
at a series of distances away from the snout revealed a P
O
2
gradient within the substrate (Table·2).
T
b
and respiration rate always decreased over time,
independent of medium, during experiments that measured P
O
2
gradients. T
b
of echidnas at the start of the experiments ranged
from 28.0 to 35.0°C and, on average, decreased 1.2±0.5°C
(N=5) during a trial. Respiration decreased from 12.0±0.5 to
4.7±3.3·breaths·min
–1
over the 5·h measurement period.
Comparison of measured P
O
2
values with those predicted by
modelling diffusive exchange of oxygen
Measured V
O
2 data and published values for tidal volume
(Bech et al., 1992) were used to generate theoretical diffusion
gradients away from the snout for each of the substrates, using
Eqn·1. These theoretical P
O
2 values at distances away from the
snout were compared with empirically measured P
O
2 values
around buried echidnas (Figs·2, 3).
In kitty litter, which had the highest porosity (f
a
=0.58), the
theoretically calculated P
O
2 values away from the snout were
not significantly different from the measured values (Fig.·2),
implying that diffusion into the tidal space was sufficient in
this porous medium to accommodate the oxygen requirements
of a resting, buried echidna.
In the natural substrate, coarse sand (f
a
=0.42) the theoretical
calculated values were significantly different from the
measured values (Fig.·3). In coarse sand, supply of oxygen by
diffusion alone was apparently insufficient to account for the
measured rates of V
O
2.
P
O
2
in relation to body movements
A behavioural pattern was observed in the experiments that
measured P
O
2 profiles in the substrate surrounding buried
echidnas. P
O
2 at any measurement distance from the snout did
Table·1. V
O
2
measurements from each echidna buried in sand and kitty litter substrates
V
O
2 (ml·g
–1
·h
–1
)
Burrowing Resting
Echidna Mass (g) Sand Kitty litter Sand Kitty litter
E1 4175 0.194 0.110 0.161 0.097
E2 2950 0.114 0.202 0.096 0.137
E3 2600 0.190 0.196 0.102 0.204
E4 2420 0.197 0.217 0.028 0.154
E5 2360 0.271 0.292 0.155 0.223
Mean 2901±748 0.193±0.056 0.203±0.065 0.108±0.054 0.163±0.051
Sand, f
a
=0.42; kitty litter, f
a
=0.58.
Mean values are ± s.d. (N=5).
A one-way ANOVA indicated that resting V
O
2 was not significantly different in different substrates (P=0.102).
Table·2. P
O
2
profiles surrounding echidnas buried in kitty litter and course sand
Distance from snout (cm)
Minimum P
O
2 (kPa) Equilibrium P
O
2 (kPa)
Echidna Mass (g) 0 246810 0 24 6810
Kitty litter
E1 4175 12.56 15.3 16.37 18.1 18.77 19.4 15.44 16.3 17.6 18.4 19 19.24
E2 2950 12.2 14.5 14.95 15.6 16.79 17.5 14.2 15.6 16.1 17.2 18 18.4
E3 2600 12.87 15.6 16.99 17.1 17.27 18 14.11 15.2 16.2 16.6 16.8 17.8
E4 2420 13.86 16.4 17.83 18.2 18.34 18.7 14.49 17.3 18.4 18.7 18.7 19.16
E5 2360 10.07 15.5 17.21 18.3 18.54 18.9 12.98 15.3 17.1 18.2 18.6 19.15
Sand
E1 4175 11.52 13 15 16.5 19.43 19.7 14.8 17.5 18 19 19.8 19.82
E2 2950 11.47 13.4 15.25 16.6 17.07 18.5 15.57 17 17.3 17.9 18.6 19.05
E3 2600 14.6 16 16.63 16.8 16.85 17.7 17.32 18 18.8 19 19 19.5
E4 2420 13.56 15 17.51 18.4 19.1 19.2 15.8 16.3 17.3 18.5 19.1 19.75
E5 2360 9.27 14 14.68 15.9 16.66 19.6 11.15 15.8 16.7 17.5 18.3 19.34
Sand, f
a
=0.42; kitty litter, f
a
=0.58.
THE JOURNAL OF EXPERIMENTAL BIOLOGY

942
not remain constant, it fluctuated in a cyclic manner and mean
values tended to increase as the experiment progressed (Fig.·4).
When first introduced to the burrowing medium, echidnas
immediately dug down until completely encased in the
substrate. At this stage, animals had a relatively high V
O
2, T
b
and respiration rate, and the minimum P
O
2 near the snout was
always lowest during this early phase of an experiment. The
minimum P
O
2 rose over time as V
O
2 fell to a resting rate
(Fig.·4). Periodic movements of the anterior body were more
common early in these experiments when oxygen consumption
rates were higher, and these movements were followed soon
after by an increase in P
O
2 close to the snout and further away
from the snout (Fig.·4) indicating that such ‘flushing
movements’ caused the convective movement of oxygen from
the atmosphere to the snout area.
The ability of echidnas to respire while submerged in different
media
The frequency of flushing movements varied between kitty
litter and course sand (Fig.·4). In kitty litter there were
approximately two movements h
–1
for the first hour and then
one movement h
–1
for the rest of the experiment (Fig.·4A),
while in course sand there were on average 6.2 movements h
–1
for the first hour, 4.6 movements h
–1
for the second hour, and
two movements h
–1
for the rest of the trial (Fig.·4B).
C. A. Waugh and others
Discussion
Modelling of diffusive exchange of respiratory gases
Comparison of measured and theoretical P
O
2
gradient
It appeared that echidnas were able to maintain their O
2
supply while encased in substrate, including while they were
digging in, by a combination of diffusion through the substrate
Fig.·2. The relationship between theoretical values, as predicted by
the model (Seymour and Seely, 1996), and mean empirical
measurements, from five echidna buried in kitty litter (f
a
=0.58). The
curves are calculated from an equation for echidna tidal volume (Bech
et al., 1992) and V
O
2 of a 2.9·kg echidna buried in kitty litter. The
upper curve represents an individual with a resting metabolic rate at
steady state. The lower curve represents an individual with higher
metabolic rate while actively burrowing into the substrate. Theoretical
and empirically measured values were compared using paired Student
t-test (minimum values, P=0.067; steady state values, P=0.241).
Fig.·3. The relationship between theoretical values, as predicted by
the model (Seymour and Seely, 1996), and mean empirical
measurements from five echidna buried in coarse sand (f
a
=0.42). The
curves are calculated from an equation for echidna tidal volume (Bech
et al., 1992) the V
O
2 of a 2.9·kg echidna buried in sand. The upper
curve represents an individual with a resting metabolic rate at steady
state. The lower curve represents an individual with higher metabolic
rate while actively burrowing into the substrate. Theoretical and
empirically measured values were compared using paired Student t-
test (minimum values, P=0.010; steady state values, P=0.001).
Table·3. Resting V
O
2
values for T. aculeatus from different
studies
Range V
O
2
Mass* (kg) (kg) (ml·g
–1
·h
–1
) Reference
2.901±0.75 2.34–4.18 0.108 Present study
3 2.5–3.5 0.217 Schmidt-Nielsen et al.,
1966
2.3 2–2.8 0.18 Parer and Hodson,
1974
2.64–4.22 0.132 Dawson et al., 1979
2.73±0.85 1.54–4.27 0.174 Bech et al., 1992
3.126±0.633 0.206 Frappell et al., 1994
*Values are means ± s.d.
THE JOURNAL OF EXPERIMENTAL BIOLOGY

943Respiration by echidnas while buried
augmented by periodic movements, which flush the interstitial
air space around the nose. Measured V
O
2 and published values
for tidal volume (Bech et al., 1992) were used to generate
theoretical P
O
2 profiles away from the snout region, with which
measured P
O
2 values could be compared. In kitty litter, at rest,
there was no significant difference between the measured and
the predicted gradients, suggesting that diffusion was sufficient
to meet the O
2
requirements when buried in this high porosity
medium, as for golden moles buried in fine sand (Seymour and
Seely, 1996). Even in this high porosity medium, however,
resting echidnas chose to make periodic movements, albeit
infrequently.
In the natural substrate, empirically measured and theoretical
P
O
2 values were significantly different. The actual mean
minimum P
O
2 values at the snout region and along the gradient
were significantly greater than predicted by the model,
suggesting that diffusive oxygen transport through the sand
alone was insufficient to account for the measured V
O
2. The
higher than predicted P
O
2 values appear to result from the
periodic flushing movements during submergence, which caused
temporarily increased interstitial O
2
levels closer to the snout.
The effect of periodic movement on the P
O
2
profiles
surrounding buried echidnas
Periodic movements were more frequent in coarse sand,
particularly in the earlier phase of an experiment when V
O
2 was
highest. The higher frequency of ‘flushing’ movements at the
beginning of the burying trials enabled the echidna to stay
submerged while experiencing higher O
2
demand, but as O
2
demand decreased later in trials, the frequency of flushing
movements decreased. Once a resting rate of V
O
2 was achieved,
a steady state was achieved and flushing movements were
regular but less frequent and the P
O
2 profiles became more or
less constant.
V
O
2
and T
b
of buried echidnas
Monotremes are characterized by metabolic rates and T
b
that
are lower than those typical of eutherian mammals (Bech et al.,
1992; Griffiths, 1978; Schmidt-Nielsen et al., 1966) and this
was confirmed in our study. Basal metabolic rates of echidnas
have been reported to be only 25–50% of that predicted for
eutherian mammals (Bech et al., 1992; Dawson et al., 1978;
Dawson et al., 1979; Schmidt-Nielsen et al., 1966). However,
10
11
12
13
14
15
16
17
18
19
20
0 0.5 1 1.5 2 2.5 3 3.5 4 4.5 5
B
A
P
O
2
(kPa)
0 cm (kPa)
2 cm
4 cm
6 cm
8 cm
10 cm
Movement
10
11
12
13
14
15
16
17
18
19
20
Time (h)
P
O
2
(kPa) 0 cm
2 cm
4 cm
6 cm
8 cm
10 cm
Movement
0 0.5 1 1.5 2 2.5 3 3.5 4 4.5 5
P
O
2
(kPa)
Fig.·4. The relationship between
flushing movements and the P
O
2
profiles surrounding echidnas
while buried in two different
media. Movements, shown by
the dotted vertical lines, are
associated with fluctuations in
P
O
2 until a steady state is reached
where the P
O
2 levels stay
constant over time. Different
symbols represent the P
O
2 values
in the medium away from the
snout region of the echidna. (A)
Typical echidnas buried in kitty
litter. (B) Typical echidnas
buried in coarse sand.
THE JOURNAL OF EXPERIMENTAL BIOLOGY

C. A. Waugh and others
mechanical problem of breathing in loose material also
needs to be explored. The porosity of coarse sand was
low due to a discontinuity of pore spaces and the smaller
particles filling in the void spaces between the larger
particles. The echidna apparently used this discontinuity to
stay submerged and was able to use its snout to create a small
air space and prevent the inhaling of soil particles into the
nose.
We thank Peter Brice and Clare Stawski for helpful
discussions and ideas on the project, and other researchers in
the Physiological Ecology Laboratory at the University of
Queensland. Animal collection and experimentation were
approved by the University of Queensland Animal Ethics
Committee (AEC approval number: ZOO/ENT/122/04/URG),
and Queensland Parks and Wildlife Service (Permit number:
WISP02184504).
References
Augee, M. L., Elsner, R. W., Gooden, B. A. and Wilson, P. R. (1971).
Respiratory and cardiac responses of a burrowing animal, echidna. Respir.
Physiol. 11, 327-334.
Bech, C., Nicol, S. C. and Andersen, N. A. (1992). Ventilation in the echidna,
Tachyglossus aculeatus. In Platypus and Echidnas (ed. M. L. Augee), pp.
134-139. Sydney: The Royal Zoological Society of NSW, Sydney.
Bentley, P. J., Herrid, C. F. and Schmidt-Neilsen, K. (1967). Respiration
of a monotreme, the echidna, Tachyglossus aculeatus. Am. J. Physiol. 212,
957-961.
Brice, P. H., Grigg, G. C., Beard, L. A. and Donovan, J. A. (2002). Patterns
of activity and inactivity in echidnas (Tachyglossus aculeatus) free-ranging
in a hot dry climate: correlates with ambient temperature, time of day and
season. Austr. J. Zool. 50, 461-475.
Burrell, H. (1926). The burrowing habits of Tachyglossus aculeatus. Austr.
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Dawson, T. J., Fanning, D. and Bergin, T. J. (1978). Metabolism and
temperature regulation in the New Guinea monotreme Zaglossus bruijni.
Austr. Zool. 20, 99-103.
Dawson, T. J., Grant, T. R. and Fanning, D. (1979). Standard metabolism
of monotremes and the evolution of homeothermy. Austr. J. Zool. 27, 511-
515.
Frappell, P. B., Franklin, C. E. and Grigg, G. C. (1994). Ventilatory and
metabolic responses to hypoxia in the echidna, Tachyglossus aculeatus. Am.
J. Physiol. 267, R1510-R1515.
Griffiths, M. (1978). The Biology of the Monotremes. London: Academic
Press.
Grigg, G. C., Beard, L. A. and Augee, M. L. (2004). The evolution of
endothermy and its diversity in mammals and birds. Physiol. Biochem. Zool.
77, 982-997.
Kuhnen, G. (1986). O-2 and CO-2 concentrations in burrows of euthermic
and hibernating golden-hamsters. Comp. Biochem. Physiol. 84A, 517-522.
Marshall, T. J. (1959). The diffusion of gases through porous media. J. Soil
Sci. 10, 79-82.
Nobel, P. S. (1983). Biophysical Plant Physiology and Ecology. San
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Parer, J. T. and Hodson, W. A. (1974). Respiratory studies of monotremes.
5. Normal respiratory functions of echidnas and ventilatory response to
inspired oxygen and carbon-dioxide. Respir. Physiol. 21, 307-316.
Schmidt-Nielsen, K., Dawson, T. J. and Crawford, E. C. (1966).
Temperature regulation in the echidna (Tachyglossus aceuleatus). J. Cell.
Physiol. 67, 63-72.
Seymour, R. S. and Seely, M. K. (1996). The respiratory environment of the
Namib Desert golden mole. J. Arid Envir. 32, 453-461.
Wilson, K. J. and Kilgore, D. L. (1978). Effects of location and design on
diffusion of respiratory gases in mammal burrows. J. Theor. Biol. 71, 73-
101.
Withers, P. C. (1978). Models of diffusion-mediated gas-exchange in animal
burrows. Am. Nat. 112, 1101-1112.
echidnas are notoriously difficult subjects in which to measure
resting V
O
2, usually being very restless and attempting to escape
while in classical respirometry chambers. This is the first study
to measure V
O
2 in echidnas buried in substrate. Indeed, further
work in our laboratory has shown that providing echidnas with
even a small quantity of material in the respirometer, into which
they can bury their head, makes it much easier to achieve
measurements at apparently resting levels (P. H. Brice, G. C.
Grigg and L. A. Beard, unpublished observations).
Accordingly, we think that buried echidnas are more relaxed
than echidnas in a respirometer without anywhere to ‘hide’ and
are more likely to provide good data on resting metabolic rates.
The V
O
2 measured from echidnas in this study were also
somewhat more variable than might be expected for metabolic
rate measured in a typical mammal at rest. The variability may
be explained in terms of their heterothermy. Echidnas have
the advantages of endothermy, including the capacity for
impressive homeothermic endothermy during incubation
(Grigg et al., 2004). The modal T
b
of active echidnas is 32°C
(Grigg et al., 2004). However, they are very relaxed about
using thermoregulatory mechanisms to maintain a stable T
b
and periods of rest are typically accompanied by a drop in T
b
.
Accordingly, cyclic changes in daily T
b
of 3–6°C are routine.
They also show both short- and long-term torpors (Grigg et al.,
2004). In our study, T
b
at the start of a trial differed between
echidnas and this is likely to account for much of the variability
in measured V
O
2. The declines in T
b
during each experimental
trial reflect the expected drops, which occur in echidnas at rest
after a period of activity.
The magnitude of the decrease in ambient P
O
2
surrounding
burrowed echidnas
The P
O
2 of the immediate O
2
environment of the burrowing
echidna showed a decrease in ambient oxygen to about 11·kPa,
substantially below atmospheric (21·kPa). This is a much
greater drop than was found in golden moles buried in sand
(Seymour and Seely, 1996), where ambient P
O
2 values were
about 20·kPa. Kuhnen (1986) summarized published data on
the burrow O
2
and CO
2
levels for 13 species of burrowing
mammals. Typically, these species were exposed to P
O
2 values
between 17–20·kPa, but values down to 10·kPa have
occasionally been recorded (Kuhnen, 1986). The results from
the present study showed that the immediate O
2
environment
of buried echidna near the snout was 12.3±0.2·kPa while active
and 14.9±0.2·kPa while resting. A P
O
2 of 11·kPa was recorded
(Augee et al., 1971) in an echidna encased in substrate for a
period of 4·h at a depth of 20·cm, which is in good agreement
with our study. Bentley et al. (Bentley et al., 1967) found a P
O
2
of 13.9·kPa in an echidna completely encased in crushed
corncobs at a depth of 30–60·cm. The O
2
environment tolerated
by buried echidnas seems to put them at the extreme end
among fossorial and semi-fossorial mammals.
Behavioural adaptations of echidnas while submerged in
different substrates
O
2
supply is one aspect of survival under soil, but the
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