Biophysical properties of the pelt of a diurnal marsupial, the numbat (Myrmecobius fasciatus), and its role in thermoregulation
1 1Department of Zoology, University of Western Australia,
Crawley, WA 6009, Australia
2 Department of Biology, Arizona State University, Tempe, AZ 85287-1501,
USA
* Author for correspondence (e-mail: ccooper{at}cyllene.uwa.edu.au)
Accepted 9 May 2003
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Summary |
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Solar heat gain by numbats through the pelt to the level of the skin (6063%) is similar to the highest value measured for any mammal. However the numbat's high solar heat gain is not associated with the same degree of reduction in coat resistance as seen for other mammals, suggesting that its pelt has structural and spectral characteristics that enhance both solar heat acquisition and endogenous heat conservation. Maximum solar heat gain is estimated to be 0.53.6 times resting metabolic heat production for the numbat at ambient temperatures of 1532.5°C, so radiative heat gain is probably an important aspect of thermoregulation for wild numbats.
Key words: pelt, thermoregulation, numbat, Myrmecobius fasciatus, thermal resistance, solar heat gain, marsupial
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Introduction |
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Solar heat gain (SHG) is a potentially important factor in the energy
budget of a diurnal animal (Walsberg,
1988a). If numbats can exploit solar heat to aid in
thermoregulation, then they can reduce their metabolism at ambient
temperatures (Ta) below the thermoneutral zone. This may
be particularly significant for a mammal feeding exclusively on poor quality
food, such as termites, which have a low energy density and variable
availability (McNab, 1984
,
2000
;
Redford and Dorea, 1984
;
Anderson et al., 1997
). There
are anecdotal reports of numbats sun basking, especially on cold winter
mornings (Calaby, 1960
;
Friend, 1993
), suggesting that
SHG may indeed have an important thermoregulatory role for the numbat. SHG by
mammals is determined by a complex array of factors, including selection of
microhabitat and orientation to incident radiation
(Walsberg, 1988a
). For mammals
that have an insulating covering of fur, the pelt plays an important role in
thermoregulation, influencing both passive heat loss and radiative heat gain
(Walsberg, 1988b
).
Consequently, the biophysical characteristics of the pelt, including
insulation, structure, colour, hair spectral properties and skin colour, are
all important determinates of heat balance for a mammal
(Walsberg, 1988b
).
This study investigates the biophysical properties of the numbat's pelt in relation to insulation and SHG and assesses the thermoregulatory importance and potential for energy conservation of exploiting solar heat for this unusual, diurnal, termitivorous marsupial.
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Materials and methods |
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Structural characteristics
Hair density was determined by shaving a 1 cm2 section of pelt
with an electric shaver and counting the numbers of guard and underfur hair
stumps in 10x1 mm2 areas using a compound microscope with an
ocular grid micrometer. The mean hair density (cm-2) was
calculated. Pelt depth was measured with a vernier caliper from the skin
surface to the surface of the hairs for depressed pelts and from the skin
surface to the tips of the guard hairs for erect pelts. Hair length and
diameter were measured using a compound microscope with an ocular micrometer
for the longest and widest point of 10 hairs of each type for each sample.
Spectral characteristics
Pelt samples were placed flat under a solar simulator (SS1000X; Kratos
Analytical, Ramsey, NJ, USA) that generated simulated solar radiation at 900 W
m-2. Coat reflectivity (c) was measured using a
pyroelectric radiometer (model 7080; Oriel, Stratford, CO, USA) held at
45° to the pelt (after Walsberg,
1988b
). A single optical quartz fiber, connected to the radiometer
and an Oriel model 17070 photomultiplier system, was threaded through a tiny
hole in the skin to measure coat transmissivity (
c). The pelt
was mounted on an Oriel precision vertical translator, and
c
was measured at intervals of 5% of the pelt depth from skin surface to fur
surface. Unless otherwise stated,
c refers to transmissivity
through the coat at the level of the skin. Values for reflectivity and
transmissivity are closely repeatable, within 0.51%. Coat absorptivity
(
c) was calculated as
1
c
c. The coat interception
function (I) was calculated using equation 15 of Cena and Monteith
(1975
), after Walsberg
(1988a
).
Thermal resistance and solar heat gain
The 6 cm2 sections of pelt were mounted on the upper surface of
a temperature-controlled stage with a 1 cm2 heat-flux transducer
embedded on its upper surface (after Walsberg,
1988a,b
).
Laminar wind flow was produced using a wind tunnel with an 18 cm2
cross section (after Walsberg,
1988b
; Walsberg and Schmidt,
1989
), and wind speed was measured with a thermoanemometer (HHF
52; Omega, Stamford, CO, USA) held 2 cm above the pelt surface. Air flowed in
an anterior-to-posterior direction across the pelt sample, at velocities of
0.25, 0.5, 1, 2 and 3 m s-1. Room temperature was
23±0.5°C for the duration of the experiments. Signal output from
the heat flux transducer was measured with a datalogger (CR21x; Campbell
Scientific, Loughborough, UK).
Conductance (W m-2 °C-1) was determined from heat
flux across the pelt, as a function of skin to environment temperature
gradient (Walsberg, 1988b),
and was then converted to total thermal resistance (s m-1) as a
function of the volumetric specific heat of air at 20°C (1200 J
m-3 K-1): total thermal resistance
(rt) = 1200/(heat flux/temperature gradient). Coat
resistance (rc) was calculated from rt
by subtracting environmental resistance (re), calculated
as 1/re=1/rr+1/ra,
where rr (radiative heat transfer resistance) was
calculated after Campbell
(1977
) and the aerodynamic
(boundary layer) resistance (ra) was approximated after
Webster and Weathers
(1988
).
Solar heat gain (SHG) was determined as for thermal resistance, but
measurements were carried out under the Kratos SS1000X solar simulator at 900
W m-2. SHG was calculated as the net heat flux with radiation minus
the net heat flux without solar radiation
(Walsberg, 1990).
The proportion of metabolic heat production met by SHG for numbats was
predicted by (SHG x PSA)/MR, where MR is metabolic rate (W;
Cooper and Withers, 2002) and
PSA is projected surface area (m2). PSA for numbats was calculated
as 1.69M0.667 after Walsberg and Wolf
(1995
), where mass
(M) was 550 g (Cooper and Withers,
2002
). This equation was validated for numbats by tracing the
shadow area of a deceased numbat (frozen into a natural position with a
depressed pelt and illuminated from directly overhead), held normal to a
horizontal surface, onto paper of known mass per unit area and then weighing
the paper. The measured PSA was 96% of that predicted using Walsberg and
Wolf's equation (Walsberg and Wolf,
1995
).
Statistics
Repeated-measure analysis of variance (ANOVA) with the
GreenhouseGeisser test for sphericity was used to determine any effect
of fur section (anterior or posterior), state (erect or depressed) or wind
speed on the structural, spectral and thermal properties of the numbat pelts
using SPSS version 10. Values are presented as means ± 1
S.E.M.
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Results |
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Thermal resistance
Mean rt across all wind speeds and sections of pelt was
90.3 s m-1 for depressed pelts and 124.9 s m-1 for erect
pelts (Fig. 2). Erecting the
fur significantly increased rt
(F1,2=187, P=0.005) to 138% of the
rt for depressed pelts. The rt
decreased significantly (F1.2,2.3=1042,
P<0.001) as wind speed increased from 0.25 m s-1 to 3 m
s-1. There was no difference in rt between the
anterior and posterior sections of pelt.
|
Calculated re decreased with increasing wind speed; re=48.1 x wind speed-0.44 (r2=0.997). Mean rc across all wind speeds and sections of pelt was significantly higher for erect pelts (71 s m-1) than for depressed pelts (37 s m-1; F1,2=187, P=0.005). There was no difference in rc between anterior and posterior sections of the pelt. rc decreased significantly (F1.2,2.3=50, P=0.011) as wind speed increased above 0.5 m s-1.
Spectral characteristics
Depressed coats had a higher c
(F1,2=49, P=0.02) than erect coats, while there
was no significant difference in
c or
c
between erect and depressed coats (Table
2). Anterior and posterior pelt sections differed significantly in
c (F2,4=97, P=0.003) but not in
c or
c. For erect coats,
c
increased gradually from the skin surface to approximately 4050% of the
coat depth, before increasing sharply to approach 100% at depths of >50%
from the skin. I was significantly greater for depressed pelts (mean
for all animals and all sections=66±17; N=6,
P<0.05) than for erect pelts (10±2).
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Solar heat gain
Mean SHG at the level of the skin, across all pelts, anterior and posterior
sections and wind speeds was 60% of total irradiance for depressed pelts and
63% for erect pelts. Neither the state of the fur (erect or depressed) nor the
section of the pelt (anterior or posterior) had a statistically significant
effect on SHG (Fig. 3). SHG
significantly decreased (F1,2.1=71, P=0.012) as
wind speed increased from 0.25 m s-1 to 3 m s-1. Solar
absorption efficiency (SAE), calculated as SHG (% irradiation)/(1
reflectivity/100), was very high, ranging from 85% at a wind speed of 0.25 m
s-1 to 55% at 3 m s-1, with a highly significant
reduction with increasing wind speed (F1,2.1=71,
P=0.012).
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Discussion |
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Resistance
Numbats have poor coat insulation compared with other marsupials. Their
rc of 40 s m-1 at a wind speed of 1 m
s-1 is much lower than that of the euro (Macropus
robustus; 145 s m-1; Dawson
and Brown, 1970), red kangaroo (Macropus rufus; 161 s
m-1; Dawson and Brown,
1970
) and koala (Phascolarctos cinereus; 605 s
m-1; Degabriele and Dawson,
1979
), as expected for a thin pelt
(Hofmeyr and Louw, 1987
). This
low rc is consistent with the high thermal conductance
(C) of the numbat (131% of that predicted for a marsupial of
equivalent mass; Cooper and Withers,
2002
). Pelt depths, densities and resistances appear to be
correlated with the general habits of marsupials and their degree of exposure
to the elements. The koala, which does not shelter from inclement weather
conditions, living in the exposed treetops, has a deep, dense pelt, high
rc and low C
(Degabriele and Dawson, 1979
).
At the other extreme, the numbat, with a sparse, thin pelt, low
rc and high C, avoids undesirable weather by
sheltering in hollow logs or burrows during cold, wet and windy conditions
(Friend, 1982
,
1993
).
Numbats are similar, with respect to pelt structure and
rc values, to a number of diurnal North American ground
squirrels, which have thin, sparse fur and rc values of
between 13 s m-1 (Walsberg,
1988a) and 63 s m-1
(Walsberg, 1988b
). These
ground squirrels, which inhabit extremely hot environments with high incident
solar radiation, have thin coats and low r values to avoid
overheating. Like the numbat, they are active during the day and are also
semi-fossorial, avoiding inclement weather by sheltering below ground
(Walker, 1975
).
Both rt and rc decreased for the
numbat as wind speed increased from 0.5 m s-1 to 3 m s-1
(Fig. 2), presumably due to
forced convection disrupting insulation within the pelt
(Walsberg, 1988a) and, in the
case of rt, the additional effect of a reduction in the
still air boundary layer above the pelt. The unexpectedly low
rc for both erect and depressed pelts measured at 0.25 m
s-1 (Fig. 2) may be
due to overestimation of re and difficulty in controlling
the airflow velocity at very low wind speeds. A similar reduction in
rc was reported by Dawson and Brown
(1970
) for red kangaroo and
euro pelts at wind speeds of <1 m s-1.
Wind speed had a much greater effect on rc for numbats
than has been measured for other marsupials (koala, red kangaroo and euro;
Dawson and Brown, 1970;
Degabriele and Dawson, 1979
)
and for ground squirrels (Walsberg,
1988a
,
1990
;
Walsberg and Schmidt, 1989
).
Erecting the pelt increased the numbat's rc by an average
of 92% across all wind speeds (Fig.
2). The reduction in rc with wind speed
(between 0.5 m s-1 and 3 m s-1) was greater for
depressed pelts (34%) than for erect pelts (19%). By erecting their fur when
exposed to low Tas
(Cooper and Withers, 2002
),
numbats are potentially able to double the thermal resistance of their pelts
and also reduce the effect of wind, therefore reducing the loss of metabolic
heat.
Spectral properties
Coat reflectivity of the numbat, measured for the mid dorsal region (19%,
on average, for red and black-and-white sections of depressed pelts), was less
than that measured for other marsupials (20.157%;
Dawson and Brown, 1970;
Dawson and Degabriele, 1973
).
Coat absorptivity (71.7% on average) is within the wide range of 1885%
measured for placental mammals (Walsberg,
1988a
,b
,
1990
,
1991
;
Hofmeyr and Louw, 1987
;
Walsberg and Schmidt; 1989
)
and is consistent with that of several ground squirrel species (6781%;
Walsberg
1988a
,b
,
1990
;
Walsberg and Schmidt, 1989
).
Like the structural and thermal characteristics, the low
c and
high
c of numbat pelts are more similar to those of diurnal
ground squirrels than to nocturnal marsupials, suggesting that the numbat's
pelt may be adapted to the acquisition of solar heat, which is not available
to nocturnal marsupials.
Numbat c was significantly reduced by erecting the pelt,
probably as a result of a decrease in I, resulting in an overall
increase of penetration of radiation through the pelt. This must be
accompanied by an increase in
c and/or
c, so
the lack of a statistically significant change in either of these factors with
pelt erection is likely to be an artefact of the small (N=3) sample
size.
White stripes reflect more solar radiation (32%) than do black (7%)
stripes, but the overall reflectance, weighted for the relative proportions of
white and black (16%), is very similar to that of anterior, reddish fur (18%;
Table 2). So, the fraction of
sunlight reflected by the striped portion of the pelt is similar to that of
non-striped regions, and the striking banded pattern of the numbat might not
have any role in thermal radiative relations. Rather, it may have evolved for
crypsis, breaking up the outline of the numbat when it is foraging in dappled
light. The low reflectivity of the numbat's pelt may also enhance crypsis, as
the albedo for woodlands of about 1618%
(Campbell, 1977) is the same as
the reflectivity of numbat pelts, thereby minimising the contrast between the
numbat and its background.
Solar heat gain
The SHG of numbats is potentially remarkably high. Indeed, SHG for erect
coats (62%) is the highest value measured for mammals, equivalent to the very
high values measured for the round-tailed ground squirrel of 59% for erect and
61% for depressed pelts (Walsberg,
1988a). However, despite differences in
c and
rc, erection of the pelt did not significantly increase
SHG for numbat pelts (Fig. 3),
in contrast to the increased SHG by fur erection in some ground squirrels
(Walsberg, 1988a
). This may be
due to the lower
c (and increased penetration of radiation
into the pelt) of an erect coat being opposed by increased free convection
with coat erection, resulting in a reduced heat load at the skin surface, with
the end result being no net change in SHG. Increasing wind speed significantly
reduces SHG, as forced convection increases
(Fig. 3).
The significant negative relationship between rc and SHG for the depressed pelts of ground squirrels at a wind speed of 1 m s-1 (SHG=-0.36rc+64.3; r2=0.97, P=0.0028) indicates a trade off between the conservation of metabolic heat (by high rc) and the acquisition of solar heat (by low rc) for these mammals. Surprisingly, the numbat falls well outside the predicted relationship, with a much higher SHG than ground squirrels based on rc (Fig. 4). Therefore, the numbat's pelt is remarkably effective in trapping heat from insolation, without as much of a decrease in rc. How this is achieved is unclear, but it does suggest that the numbat's pelt has some special combination of structural and spectral properties not measured here. Further investigation would require analysis of changes in the biophysical properties of the pelt with depth, but this is challenging for such a shallow (1.2 mm) pelt.
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For a numbat, SHG to the skin surface is high compared with metabolic heat
production. SHG at the skin surface is predicted to range from 135% to 580% of
the resting energetic requirements (RMR;
Cooper and Withers, 2002) of a
numbat, at Tas between 15°C and 32.5°C, with
incident radiation of 900 W m-2 and at wind speeds between 0.25 m
s-1 and 3 m s-1. However, predictions of whole animal
SHG made from isolated coat samples may be 3248% higher than values
measured for live animals (Walsberg and
Wolf, 1995
). Measurement of whole-animal SHG is not possible for
live numbats, due to their endangered status, but we can estimate it.
Calculations of SHG to the animal's core (QA) were made
after Walsberg and Wolf
(1995
), using two values for
tissue thermal resistance (rtissue; 100 W m-2
and 75 W m-2; Monteith and
Unsworth, 1989
; Walsberg and
Wolf, 1995
), which provide a range of estimations of
QA. Predicted SHG to the numbat's core range from 50% to
357% of RMR, dependent on Ta and wind speed
(Table 3). The proportions of
RMR met by SHG at higher wind speeds may be overestimated if there is an
increase in RMR at high wind speed, so these values represent maximal
proportions of SHG/RMR at higher wind speeds.
|
The ratio of SHG to basal metabolic rate (BMR) is high for the numbat (i.e.
QA=1.5-3.6xBMR) compared with other species. Ground
squirrels (e.g. Spermophilus saturatus and S. lateralis)
have a much lower ratio (0.8-1.0xBMR for S. saturatus;
1.31.7xBMR for S. lateralis;
Walsberg and Wolf, 1995).
Thus, for numbats, potential SHG can be a substantial fraction of their heat
budget compared with resting/basal metabolism, due to a combination of high
radiative heat gain and low basal metabolism (numbat BMR is only 48% of that
predicted for a typical placental mammal of equivalent mass;
Cooper and Withers, 2002
).
Pelt specialisations
The biophysical properties of numbat pelts presumably reflect adaptation to
their diurnal lifestyle. Compared with other marsupials, their pelt is sparse
and shallow and has poor insulative and low reflective properties, probably to
maximise SHG. As termites are a poor quality food source (MacNab,
1984,
2000
;
Redford and Dorea, 1984
;
Anderson et al., 1997
), it is
beneficial for the exclusively termitivorous numbat to conserve energy by
utilising SHG in preference to metabolic heat production for thermoregulation.
The structural and spectral properties of numbat pelts in comparison to other
marsupials suggest that SHG may indeed be a major source of heat, and the
numbat's pelt is adapted to favour SHG at the expense of resistance to
metabolic heat loss. Foraging timing of numbats is closely timed with diurnal
termite activity in shallow sub-surface soil galleries (Friend,
1986
,
1993
), so numbats are active
under environmental conditions that favour SHG. During summer, numbats (like
the termites they feed on) are most active in early morning and evenings and
seek shelter during the heat of the day. In winter, the pattern is reversed,
and numbats remain in their hollows or burrows in the mornings and evenings,
emerging only during the warmest part of the day
(Friend, 1986
). Thus, numbats
may avoid potential overheating in the hot summer and utilize solar radiation
for thermoregulation during the cooler winter.
Considering the differences in ecophysiology between diurnal numbats and other nocturnal marsupials, it is not surprising that the structural, spectral and thermal properties of numbat pelts are more like those of small diurnal placental mammals. Ground squirrels make the best comparison. They have similar coat absorptivity and rc values to those of the numbat, and their high fractional SHG is like that of the numbat. The similarity in coat structure and function for numbats and desert-dwelling ground squirrels is a clear case of convergent evolution, responding to selection pressures to use solar radiation in balancing the energy budget. However, the numbat has achieved a high level of heat gain without the same extent of reduction in rc of ground squirrel pelts, indicating different structural and spectral properties that adapt the numbat for both heat acquisition and conservation.
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Acknowledgments |
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