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First published online December 14, 2005
Journal of Experimental Biology 209, 103-114 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.01964
On the importance of radiative heat exchange during nocturnal flight in birds
Département de biologie, Université Laval, Québec, Canada, G1K 7P4
* Author for correspondence (e-mail: jacques.larochelle{at}bio.ulaval.ca)
Accepted 21 October 2005
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Summary |
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Our results show that the temperature of the flight and insulation plumages exposed to a radiative sink can be accurately described by multiple regression models (r2>0.96) based only on TAIR, TASK and UWIN. Predictions based on these models indicate that while convection dominates heat loss for a plumage exposed to air moving at flight speed in a thermally uniform environment, radiation may dominate in the presence of a radiative sink comparable to a clear sky.
Our data also indicate that reducing TASK to a temperature 20°C below TAIR can increase the temperature difference across the exposed plumage by at least 13% and thus facilitate heat flow through the main thermal resistance to the loss of internally produced heat in birds. While extrapolation from our experimentally constrained conditions to free flight in the atmosphere is difficult, our results suggest that the sky temperature has been a neglected factor in determining the range of TAIR over which prolonged flight is possible.
Key words: radiation, sky, temperature regulation, flight, bird, pigeon, migration, wind tunnel
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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), the wind tunnel has
become a common environment for the experimental study of flying animals, and
its use has rapidly led to major advances in our understanding of the
energetic, thermal and hydric constraints affecting avian flight (see
Rayner, 1994). By 1978, it was
well established that energy expenditure during flapping flight was typically
an order of magnitude greater than at rest. This result, combined with
estimates of the mechanical efficiency of the pectoral muscles in the 20-25%
range, also implied that flapping flight was accompanied by a large increase
in heat production.
Unless dissipated by convection, radiation and evaporation, this heat would
lead to cessation of flight due to hyperthermia. This thermal challenge is
exacerbated by the fact that only a small fraction (<10%) of the heat
produced during sustained flapping flight can be lost through evaporation
(Torre-Bueno, 1978). Exceeding
this limit, set mainly by the rate of metabolic water production from the
oxidation of lipid fuel, would lead to cessation of flight by reason of
dehydration. In sum, these factors suggested that, at least in a wind tunnel,
the need to dissipate large amounts of heat by convection and radiation would
make flapping flight unsustainable at ambient temperatures higher than about
10°C. This hypothesis was later confirmed by the comprehensive studies of
Nachtigall's group, who nevertheless considered that it was not applicable to
flight made under natural conditions, presumably because `birds in
free-range flights use a form of behavioural thermoregulation not possible in
a wind tunnel' (Biesel and Nachtigall,
1987).
In view of the existence of empirical evidence showing that migrating birds
can cross the Sahara by flapping flight at temeratures above 20°C (e.g.
Klaassen and Biebach, 2000),
the thermal constraints acting on birds during flight in wind tunnels can no
longer be taken as de facto representative of those prevailing during
natural flight, because during free flight either heat production is smaller
or heat dissipation is easier, or both. Several instrumental, meteorological
and biological factors have indeed been considered to explain why the
metabolic rate of flying birds may be higher in a wind tunnel than in the wild
(Bishop et al., 2002). However,
the possibility that the radiative interface to which most birds are exposed
during migration can act as a much better heat sink than the walls of a
standard wind tunnel has been neglected.
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),
it is usually expressed on a temperature scale as the temperature of a black
body having the same emitting power and referred to as the (natural) sky
temperature (TNSK). Since the value of
TNSK is strongly dependent on the atmospheric water
content, itself a function of TAIR, it can easily be
calculated using empirical formulae
(Hatfield et al., 1983). The
difference between TAIR and TNSK can
range from about 40°C (cold dry air under a clear sky;
Hardy and Stoll, 1954) to
nearly 0°C (warm moist air under a cloudy sky;
Nobel, 1991). Values around
20°C are commonly observed under cloudless skies at intermediate relative
humidity. We will refer to such a difference between TAIR
and the equivalent black body temperature of an ambient radiative sink as a
radiative temperature deficit (
TRAD).
As shown by the occurrence of radiative freezing at
TAIR several degrees above zero during clear nights
(Nobel, 1991), exposure of an
object to the atmospheric radiative sink can reduce its surface temperature
(TSUR). Since the cooling effect is then proportional to
TSUR4-TNSK4
(Porter, 1969), radiative
exchange in birds flying at night in a cloudless atmosphere may very well
account for a greater fraction of the total heat loss than that reported
during flight in an isothermal wind tunnel (8%;
Ward et al., 1999).
The aims of this study were to establish the effect of exposure to a radiative sink on the heat exchanges at the external surface of an avian plumage, and to examine the possibility that exposure to the low sky temperatures observed during clear nights may raise the maximum TAIR at which flapping flight is sustainable in birds.
To simplify the task, we built a wind tunnel offering the possibility to control wall and air temperatures independently, and used it with pigeons at rest experiencing thermal constraints comparable to those observed during prolonged flight, i.e. having to dissipate a heat load in a flying posture.
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Materials and methods |
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Our protocol was approved by the institutional Animal Protection Committee.
Basic protocol
Each of the 96 experimental runs consisted of four phases over which
TAIR was constant at ca. 15°C or 25°C
(Fig. 1; 25°C). During
phase 1 (30-50 min), the body core temperature (TINT) of
the bird was raised at a maximum rate of 0.1°C min-1. During
phase 2 (5-10 min), TINT was stabilized to a value
(43.7±0.3°C) close to the maximum observed in flying pigeons
(Hart and Roy, 1967;
Butler et al., 1977;
Hirth et al., 1987) and thus
expected to elicit the use of heat dissipation mechanisms. During phase 3 (10
min), the artificial sky temperature (TASK) was set
(nominally -78°C, -30°C, 0°C or TAIR) and wind
speed (UWIN) was selected (0.3, 11 or 20 m s-1)
while the heating power was kept constant at the stabilizing level. During
phase 4 (10 min), heating was stopped while all other parameters were kept
constant.
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To allow control of their radiative temperature and emulate that of a natural sky, the inclined walls of the working space consisted of rectangular tanks (lengthxheightxthickness: 48.5 cmx42.5 cmx6.5 cm; Fig. 2). These tanks were made of 6 mm thick aluminium plates and were insulated with 25 mm of styrene foam except on the air stream side, which was painted flat black. They were put in place at the beginning of phase 3. Nominal values ca. -78°C and 0°C for TASK were obtained by filling the tanks with mixtures of dry ice-methanol and ice-water, respectively. A TASK temperature of ca. -30°C was obtained by covering the exposed surface of the tanks filled with dry ice-methanol mixture with a 4.2 mm thick, black acrylic sheet held at 1.5 mm from the tank surface by a plastic covered metal screen. Effective values of TASK were sensitive to wind and were thus continuously monitored using an IR sensor (model OS36, Omega Canada, Montréal, Québec, Canada). The view factor of the plumage towards the artificial sky formed by the tanks was 0.72 (J.-F. Harbour and D. Rousse, unpublished data).
Maintaining the surface temperature of relatively large plates (0.21 m2 each) several tens of degrees below that of air moving over them at speeds up to 20 m s-1 requires a hefty cooling capacity. In our case, several tons of dry ice were used, and the tanks had to be vented out of the experimental room to avoid any significant build-up of CO2.
A minimum UWIN of 0.3 m s-1 was necessary to
prevent cooling of the plumage surface through natural convection by the
sinking air having been in contact with the tunnel walls at low
TASK. UWIN=11 m s-1 was
chosen because it is close to the minimum-power speed in both pigeons (Rothe
and Nachtigall, 1987) and starlings (Ward et al.,
1999,
2001) flying in wind tunnels.
UWIN=20 m s-1 appears close to the maximum
speeds sustainable for several hours during homing flights in pigeons
(Gessaman and Nagy, 1988).
The performance of our compact wind tunnel was in many respects less
impressive than that of an instrument optimized for aerodynamical studies such
as Lund's 21 m tunnel (Pennycuick et al.,
1997). In the following comparison, values taken from their paper
are shown within parentheses, together with the source figure number. At
UWIN>5 m s-1, a series of freestream air
speeds in our tunnel (taken at least 5 cm away from walls) gave values within
10% (<2%; fig. 3,
Pennycuick et al., 1997) of
the average value, with a maximum turbulence intensity of about 6% (<1%;
fig. 5, Pennycuick et al., 1997).
Boundary layer properties of our tunnel, however, particularly above the
critical floor area covered by the bird, were quite decent. Average air speeds
measured above this critical area at 1 cm from the floor (wall) were reduced
by 
13% (12%; fig. 8,
Pennycuick et al., 1997) with
respect to those obtained at 10 cm. Turbulence intensity at 1 cm was 7-9%
(6%; fig. 8,
Pennycuick et al., 1997), an
expected increase over the values observed at 10 cm.
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Measurement of TAIR was made in the wind tunnel using a thermocouple that also controlled the cooling unit of the room. The only light in this room came from a standard 60 W bulb unviewable from the bird position.
Posture control
Within the working section of the wind tunnel, the bird was held in a
posture similar to that observed during gliding flight. The body trunk was
supported by a basket-like mould, made of rubber strips. The inside of the
mould was padded with a cotton liner, while the outside was covered by heating
wires taken from a common heating pad. The mould was embedded in the floor of
the working space of the wind tunnel at a depth such that the opened wings
were positioned flat on the wind tunnel floor. To maximize heat loss by the
upper facing surfaces of the bird, the mould was kept at a temperature
slightly above that of the bird body, and the (unheated) floor that supported
the wings was made of 7.5 cm thick insulating foam to minimize downward heat
loss.
The wings were held opened by pinching the distal primary feathers between
padded bars (Fig. 3). Based on
measurements made in starlings by Ward et al.
(1999), we estimated that the
upper-facing surface of our constrained birds was 36% of the total surface
exposed during free flight. The exposed frontal area of the bird (ca. 20
cm2) determined a blocking factor of about 2%, as compared with the
cross-sectional area of the working space of the tunnel.
Body heating system
To simulate the heat load observed during flapping flight, the bird was
exposed to a low-power microwave (MW) source located below the mould. This
source consisted of an 800 W domestic oven facing upwards, with its door
window removed. The MW load delivered to birds (PMW) was
reduced to a maximum value of about 10 W (at 100% duty cycle) by a metallic
screen replacing the door window and by a bottle of water acting inside the
oven as a phantom load maintained at 20°C by an external cooling
circulator. The variable PMW level required for adequate
control of the pigeon TINT was obtained by adjusting the
duty cycle of the MW source via a computer-activated relay replacing
the door switch. Supplementary metallic screens and plates were used to
prevent direct MW irradiation of the underwings and legs. Since the
penetration depth of 2.45 GHz MW is about 1 cm, this arrangement was expected
to favour the preferential heating of the pectoral muscles and therefore the
maximum recruitment of the heat dissipation mechanisms used during flight. The
pectoral skin was consistently warmer than the intestine (by up to 3°C)
during MW irradiation, indicating that thermal absorption was indeed higher
near the site where most of the heat is produced during flight.
The experimental birds showed no reaction to indicate any possible non-thermal effects of MW exposure. No sign of cutaneous damage was observed, even in the pectoral area where the highest temperatures were recorded.
To prevent personal exposure to MW, the wind tunnel was installed in a metal-walled room, from which leaks were found to be negligible using a MW meter (model HI-1501, HOLADAY, Eden Prairie, MN, USA).
Measurement of biological temperatures
Plumage temperature was measured using an infrared thermometer accurate to
0.1°C (model MX4, Raytek, Santa Cruz, CA, USA; bandwidth, 8-14 µm;
average spot size, 2 cm; reading time: 0.25 s) through a slit between the
upper edges of the side walls in the working space of the wind tunnel.
Preliminary measurements were made at various points over the bird, and three
locations were selected as representative of the average temperature of back
insulation plumage (TPIB), wing insulation plumage
(TPIW) and wing flight plumage (TPFW),
respectively (Fig. 3). In this
paper, insulation plumage refers to the feather coat directly overlying the
skin and flight plumage refers to the primaries and secondaries. Precise
aiming of the infrared thermometer was achieved using a custom device made
with two printing head carriers taken from dot-matrix printers. The stepping
motors were controlled by a computer, allowing reproducible measurements both
within and between the wings.
Upper wing skin (TSIW; Fig. 3) and pectoral temperatures were read with 36 gauge copper-constantan thermocouples kept in contact with the skin by gluing or tying to adjacent feathers. TSIW was taken as representative of the temperature of the whole wing skin. TINT was measured in the intestine using a lubricated thermistor inserted cloacally to a depth of 6 cm.
All temperatures were obtained by reading the sensors every 40 s with a computer and calculating the values from polynomial curves established through calibration against a certified thermometer over the whole experimental temperature range. IR emissivity of all surfaces was assumed to be 0.97. The MW heating was suspended a few seconds before reading the sensors to eliminate any MW interference.
Heat flow calculations
The level of PMW was crudely estimated from
measurements of the maximum value of the rate of change of
TINT (TINT/t;
in deg. s-1) following switching the MW source off after
TINT stabilization:
 | (1) |
where a value of 3.47 J g-1 K-1 was used for heat
capacity (cP) of the pigeon body
(Hart, 1951).
To quantify the heat exchanges made by the upper facing surface of the plumage with the skin and the surroundings, we considered the capacity for heat storage at this surface as well as the influence of evaporative and conductive (downward) processes to be negligible. Heat loss to the surroundings by the plumage could then be assumed to occur through convection (via the external boundary layer of air; subscript CP) and radiation (for the sake of simplicity, only the loss to the artificial sky was considered; subscript RP). The relative importance of these two processes in dissipating the heat gained from the skin by transplumage flow (subscript TP) could then be defined on a percent scale as FCP (=100xPCP/PTP) and FRP (=100-FCP), where P refers to the magnitude of a heat flow.
Since heat flow through the plumage as well as that through its external
boundary layer can be described by a simple transfer law
(P=GxT), where G corresponds
to thermal conductance, it follows that:
 | (2) |
At a given TAIR and UWIN, when
GCP and GTP can be reasonably
considered as stable, their ratio (and the percent factor) can be replaced by
a constant KCT to give:
 | (3) |
The value of KCT can be calculated at
TAIR=TASK=25°C and
UWIN=10 m s-1 from the values of
TCP (2.0°C) and TTP
(8.1°C) predicted by our models for pigeons
(Table 1) and from a reference
value for FCP taken from the study of starlings flying
under comparable conditions (91%; Ward et
al., 1999). Values of FCP for various values
of TASK could then be calculated for pigeons from the
relevant predicted T values and used to determine the values
of FRP (9% under reference conditions). We assumed that
doubling UWIN increased GCP (and thus
KCT and FCP) by 20.5.
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Data analysis
The experimental sequence among the 4 birds and the 24 conditions was
chosen randomly. Multiple linear regression models
(SAS, 1994) were prepared
using the forward procedure of SAS (version 8) applied on all raw measurements
made during phase 3 and 4 of each experiment. Best-fit exponents for
UWIN and TASK were determined as those
maximizing r2 values when calculating the regression with
the variables raised to powers between 0 and 4 by 0.1 steps. This procedure
gave 0.5 for the exponent of UWIN, a value commonly
observed in both inert objects (Holman,
1990) and living animals
(Goldstein, 1983). It gave 1.6
for the exponent of TASK, a value theoretically expected
to be smaller than the commonly observed one (4;
Holman, 1990) as only 72% of
the total ambient surface emitting IR towards the upper surface of the bird
was at TASK, the remaining part being at
TAIR.
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) on starlings at flight
in a thermally uniform wind tunnel
(TASK
TAIR). These authors also
found that the plumage surface temperatures can be described precisely by
multiple regression models based on TAIR and
UWIN (r2>0.91; table 3 in
Ward et al., 1999). The three
sites used to measure plumage temperature in our study are comparable to
equivalent sites in Ward et al.
(1999). But although the
temperatures recorded at these sites reacted similarly to
TAIR (Fig.
5) and UWIN (data not shown) in both studies,
the temperature differences (T) between plumage and air were
often larger in the starling, putatively reflecting the higher thermal load
imposed by flapping flight with respect to that imposed by our artificial
heating system.
Effects of TAIR on plumage temperature
Our data show that the superficial temperatures of the upper-facing plumage
were very responsive to TAIR, with
TPIW, TPIB and
TPFW decreasing by 9-10°C following a 10°C
reduction of TAIR (=TASK) at flight
UWIN (10-20 m s-1;
Fig. 4). The effect was
slightly greater in TPFW and at higher
UWIN. In flying starlings (table 3 in
Ward et al., 1999), a
reduction of 10°C resulted in decreases of 8.0°C in the area
corresponding to TPIW (dorsal brachials) and 9.3°C in
those corresponding to TPIB (back) and
TPFW (dorsal secondaries).
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T
responsible for dry (non-evaporative) heat loss from skin to environment
(TSIW-TAIR) was observed across the
feather coat. At flight UWIN, this proportion was 80-88%
across the insulation plumage (Fig.
6A,B) and 91-96% across the flight plumage
(Fig. 7A,B), with the highest
values obtained at low TAIR and high
UWIN. The T values responsible for the
main radiative heat loss
(TRP=TSUR-TASK)
and for the convective heat loss
(TCP=TSUR-TAIR)
from the external surfaces of the plumage to the environment were therefore
rather small, typically 1-3°C. In starlings flying under similar
conditions, the corresponding T values were higher (on
average, by 50%) but generally still less than 3°C, with the notable
exception of those associated to the brachials, where higher values were
commonly observed (fig. 5 in
Ward et al., 1999).
Effects of TASK on plumage temperature
The superficial temperature of the upper-facing plumages was reduced in the
presence of a radiative sink (Fig.
4), producing opposite changes on TRP
and TCP. In the upper-facing insulation plumage of
the wing, for example, creating a radiative temperature deficit
(TRAD) of 20°C by lowering
TASK to 5°C while keeping TAIR at
25°C caused a 10- to 14- fold increase in TRP
and a 50-55% decrease in TCP at flight
UWIN (Fig.
6C). The effect was stronger in the flight plumage where a
reversal of TCP was observed at
TRAD larger than 10°C
(Fig. 7C). A similar reversal
could also be observed across the insulation plumage, but it required a larger
TRAD (>42°C;
Fig. 4).
The distinctive effects of TRAD of 20°C at
TAIR=25°C on TRP and
TCP resulted in marked changes in the relative
contributions of radiation and convection to the loss of the heat gained from
the skin by the external surface of the plumage exposed to the radiative sink
(Fig. 8). The predicted values
of FRP for the insulation plumage then increased from less
than 10% to 58% at UWIN=10 m s-1 and to 53% at
UWIN=20 m s-1. For the flight plumage, the
corresponding increase was from below 10% to above 100%, as its
TSUR remained below TAIR when
TRAD was larger than 10°C.
In pigeons, the predicted balance TRAD (at which
FRP=FCP) was 16°C for the
insulation plumage exposed to the radiative sink at a UWIN
of 10 m s-1 and a TAIR at 25°C. Its value
was relatively insensitive to the value arbitrarily chosen for reference
FRP (9%; see Materials and methods), changing by about
1°C when this FRP was either decreased to 5% or
increased to 15%. As expected, doubling UWIN increased the
predicted balance TRAD, but only by 2°C.
The predicted balance TRAD for the flight plumage
was only 4-5°C under the same conditions.
Exposure to a TRAD of 20°C at a
TAIR of 25°C and a UWIN of 10 m
s-1 also facilitated transplumage heat flow, as
TTP increased by 13% and 22% for the exposed
insulation and flight plumages, respectively (Figs
6C,
7C,
8). The increases, however,
were reduced by about 40% when TAIR was lowered to
15°C at constant TRAD
(TASK=-5°C) but they were essentially unaffected by
doubling UWIN at a given TAIR.
Effects of the thermal environment on TSIW and TINT
The variability of measured TSIW was relatively high
with respect to that of other temperatures, mainly due to a large
between-experiments component (Fig.
4). Although this led to low r2 values in
regression models (Table 1),
its impact on data interpretation should be marginal in view of the low
sensitivity of TSIW to environmental variables. For
example, predicted TSIW at
TAIR=25°C and UWIN=10 m
s-1 was 34-35°C, and it changed by less than 1°C from
increasing UWIN to 20 m s-1 or from decreasing
TASK by 20°C.
The value of TSIW was more sensitive to that of
TAIR, a 10°C reduction in TAIR
bringing a 2-3°C decrease in TSIW at
UWIN=10 m s-1. But since the values of
TSIW were much less sensitive to TAIR
than that of the plumage TSUR, large increases in
TTP (74-92%) were observed when
TAIR was reduced by 10°C at flight
UWIN. Predicted values of TSIW under a
very low wind (0.3 m s-1) were 37.0 and 33.0°C, at
TAIR of 25°C and 15°C, respectively.
Unlike that of other body temperatures, changes in TINT were poorly correlated to environmental variables (r2=0.018), but their prediction based on internal variables was significant (r2=0.523), with contributions coming from PMW (r2p=0.517) and Mb (r2p=0.006; results not shown).
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), may be
the dominant heat dissipation mode for the plumage surfaces exposed to a
typical cloudless sky at night. Secondly, our data indicate that exposure to a
radiative temperature deficit may also facilitate heat dissipation in a flying
bird by reducing the temperature of its exposed surfaces. A higher heat loss
from these surfaces then offers a bird the possibility to reduce its
dependance on evaporative heat loss, explaining why exposure to a low
TNSK may extend the range of TAIR over
which flapping flight can be sustained. Finally, our study demonstrates that
standard wind tunnels are inappropriate thermal environments to measure the
capacity of animals to dissipate heat during free nocturnal flight, i.e. under
conditions where many migratory flights take place.
Since lowering TSUR of an object reduces its capacity
to lose heat through convection and IR emission, it may at first glance appear
disadvantageous to a bird threatened by hyperthermia. It must however be
recalled that the main thermal input to the surface of a flying bird is the IR
absorbed from the surroundings. For example, assuming a plumage area of 0.0493
m2, a metabolic rate of 12.7 W, a mechanical efficiency of 19% and
an evaporative water loss of 0.9 W (bird 19 in Ward et al.,
1999,
2001), the plumage surface of
a 0.090 kg starling flying in a black wind tunnel would receive 200 W
m-2 of heat from the internal organs. At the same time, this
surface would receive 450 W m-2 from tunnel walls at 25°C,
but only 340 W m-2 from walls at 5°C. A surface exposed to
a radiative sink thus exhibits a lower TSUR because its
thermal gain through radiation is reduced more than its thermal loss through
convection and radiation.
Since plumage has the high insulating capacity required to keep resting
birds warm under cold and windy conditions, it constitutes the main thermal
resistance between the flight muscles and the environment. This is well
illustrated by our results showing that in pigeons at least 80% of the total
T responsible for dry heat loss from skin to environment
appears across the feather coat at flight UWIN. A reduced
TSUR can then facilitate the loss of internally produced
heat by increasing the transplumage T. For instance, at a
TAIR value known to be limiting for sustained flapping
flight (25°C), exposure to a typical clear night sky, with a
radiative temperature deficit of 20°C, can increase
TTP in the exposed plumages by 13-22% according to
our results. This effect is larger than that caused by increasing
UWIN from 10 to 20 m s-1 (3-7%). In flight
feathers, it may lead to a reversal of the plumage-to-air temperature
difference, implying that air would then heat the plumage surface (Figs
4,
8).
The use of our results to describe what happens during nocturnal migratory flight obviously depends on how well our biological model matches a flying bird and on how well our custom wind tunnel simulates the relevant radiative and convective characteristics of the atmosphere on a clear night. To address this point, we must first show in the absence of comparable data that our predicted values of FRP are acceptable estimates of those that could be determined for the corresponding surfaces of flying pigeons.
The first limitation of our experimental approach arises from the fact that
the convective environment to which our birds were exposed was different from
that experienced during flight. On the one hand, while the posture of our bird
was closer to that observed during gliding rather than flapping flight, there
is no apparent reason why this could per se affect the thermal
properties of the upper-facing surfaces of the plumage. On the other hand, the
potential of the wings and adjacent surfaces for convective heat loss was
certainly reduced by the absence of wing movements and underwing exposure.
This potential was also likely reduced owing to the presence of a preformed
boundary layer on the windward side of the wind tunnel floor, over which the
wings were lying flat. For instance, UWIN measured at a
height of 0.5 cm above the floor was reduced by 19% with respect to freestream
speed (10 m s-1), indicating a 10% decrease in convective heat loss
if the 0.5 exponent applies to this case. These conditions may therefore lead
to an overestimate of the importance of radiative heat loss, though only to a
small extent in view of the low sensitivity of the plumage temperatures to
wind speed. For example, halving UWIN within the flight
speed range changed the temperature of the insulating plumage by about
0.5°C and the transplumage temperature difference by less than 10%
(Fig. 6). This sensitivity to
air speed also appears small in starlings, as halving the flight speed
resulted in changes of about 1.4°C in the plumage temperature
(fig. 6 in
Ward et al., 1999) and of less
than 5% in the metabolic power (fig.
2 in Ward et al.,
2001). It is also possible that in our setup the effect on heat
exchange by the wings of the preformed boundary layer was to some extent
compensated by an increase in turbulence favored by the high turbulence
intensity observed in the freestream of our wind tunnel (see Materials and
methods).
A second limitation of our approach that may favor overestimation of
FRP comes from the fact that our resting birds had less
heat to dissipate than flying ones. Taking the minimal metabolic rate of
flying pigeons as 100 W kg-1
(Rothe et al., 1987), the
mechanical efficiency of their flight muscles as 15%
(Dial et al., 1997), the
fraction of the heat loss taking place through non-evaporative means as 90%
(Biesel and Nachtigall, 1987;
Ward et al., 1999), and that
the upper-facing surface our constrained birds was 36% of the total surface
exposed during flight, we estimate that flying pigeons have to dissipate about
10 W through the upper surfaces of their body. Given the thermal load imposed
by our heating system and the possibility that most of the heat produced by
the pigeons was lost through evaporation (as in
Martineau and Larochelle,
1988), we estimate that our birds had to dissipate heat through
their (dry) upper surfaces at a rate corresponding roughly to half of that
during flapping flight at a TAIR of 25°C. Such a
difference is expected to be largely reflected in the surface temperature of
the plumage; more so in areas specialized in heat dissipation during flight
such as the dorsal brachials and the legs. Assuming then in the absence of
relevant data that the thermal image of pigeons during flight at a
TAIR of 25°C is similar to that of starlings, this
would imply values of TCP
(Fig. 5) about 50% higher than
those observed in our experiments under isothermal conditions
(TASK=TAIR). At a
TRAD of 20°C (TAIR=25°C
and UWIN=10 m s-1), this would translate into
increases of about 50% for PCP and 5% for
PRP in the exposed insulation plumage. This would give a
value of FRP of 42% for this plumage, suggesting that our
models overestimate its importance of radiative heat loss (predicted
FRP of 58%). However we think that the effect of higher
TSUR would be largely compensated by the fact that a
pigeon flying in the atmosphere would be exposed to an hemispheric sink at
least 140% larger than the one imposed by our experimental setup, where the
view factor of the plumage towards the radiative sinks was only 0.72.
Furthermore, in the flight plumage, increasing the value of
TCP by 50% under isothermal conditions would not
prevent it from becoming negative under a TRAD of
20°C. Its FRP would thus not be lowered below
100%.
A further limitation of our experimental approach concerns the source of
the heat dissipated by the plumage, as heat was supplied to our experimental
birds by microwave irradiation rather than by muscular activity. The heat
distribution within the body of our birds as well as the way thermoreceptors
and thermoregulatory controls operate are likely to differ from that observed
during flight. We consider these effects are largely irrelevant to our
predictions as long as direct microwave heating of the upper facing skin and
feathers is negligible. This was shown to be the case, as close examination of
graphs such as Fig. 4 revealed
that the variations in TPIW and TPFW
induced by discrete changes in microwave power level were slow and did follow
those observed in core temperature. Comparison of our TSIW
with the rare relevant values found in the literature also indicate that they
are representative of those obtained in flying birds. The wing skin
temperatures measured by Eliassen
(1962) in seagulls held in a
gliding posture in a wind tunnel at a UWIN of 12 m
s-1 and TAIR of 15-19°C are quite similar
to those predicted for our pigeons under the same conditions (31.5-32.6°C
vs 32.2-33.3°C). The breast skin temperatures reported by Hirth
et al. (fig. 2B in
Hirth et al., 1987) in pigeons
during flapping flight in a wind tunnel at TAIR=16.1°C
and UWIN=12-18 m s-1 are also close to our
predictions for wing skin under the same conditions (30.8-32.7°C
vs 32.2-32.5°C).
Given these considerations, we feel confident that our
FRP values for the insulation (58%) and flight (100%)
plumages constitute valuable starting points to estimate the overall
contribution of the radiative heat loss to the thermal budget of a bird
engaged in a flight under a typical cloudless sky
(TRAD=20°C) during a warm night
(TAIR=25°C). To obtain a whole-body value for
FRP, we must first combine the values for both plumage
types according to their relative contributions to dry heat loss. Estimating
the contribution of flight plumage at 10%, a conservative value when compared
to that (>30%) suggested by the data of Ward et al. (table 6 in
Ward et al., 1999), we obtain
FRP=62% for the total plumage surface exposed to the
radiative sink (36% of total body surface). Assuming that the rest of the body
surface is exposed to surfaces having a radiative temperature equal to
TAIR would give a value for whole body
FRP=28%.
While a value of 28% is much higher than that of 9% obtained in the absence
of a radiative temperature deficit, we think that larger values may be
obtained by avian migrants by choosing when and where they will fly. Since
water vapour is the major contributor to the downward radiation flux from the
sky (Monteith and Unsworth,
1990), TRAD increases with air dryness.
For example, as calculated using Brunt's formula
(Hatfield et al., 1983), at
TAIR=25°C, TRAD at a
relative humidity of 20% is 9°C greater than at a relative humidity of
50%. As water vapour is more concentrated in the bottom part of the
atmosphere, TRAD is expected to increase with
height. Flight at high altitude should also increase the relative importance
of radiative heat loss because convective loss is then reduced (8-9%
km-1) owing to the proportionality between the thermal
conductibility of air and its specific gravity
(Holman, 1990). Finally,
subjected to radiative cooling like any other body exposed to the atmosphere
at night, the ground may act as secondary radiative sink and increase the
value of FRP for the downward surface of a flying
bird.
Conclusion
It can now be considered highly probable that radiation plays a much
greater role than previously thought in the heat dissipation of birds during
nocturnal flight in warm weather under clear skies. In spite of the
limitations imposed by our experimental approach, there is no reason to
believe that the main physical phenomena responsible for heat removal from the
plumage surface in our setup are different from those occurring in the
atmosphere.
All other variables being constant, an increase in radiative heat loss due to exposure to a radiative sink will necessarily be accompanied in a bird by a decrease in surface temperature and an increase in transplumage heat flow. However, because of the experimental limitations of our approach, a precise determination of the extent to which natural radiative sinks can increase the range of TAIR over which prolonged flight is possible will await future study. Chances are that radiative cooling will be found most useful for birds needing it most, i.e. for those having to cross desert areas where air is warm but dry.
The radiative interface offered to nocturnal migrants can thus be more
complicated than previously thought, and this can make the decision to engage
in a prolonged flight more complex. Humbly said, this interface may deserve to
be recognized as a `neglected interface', sensu Schmidt-Nielsen
(1969).
t
T
TCP
TRAD
TRP
TTP
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Acknowledgments |
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References |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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the
increase (%) in transplumage heat gain by this surface. Black bars, fractions
of the heat loss attributed to radiation (FRP); grey bars,
fractions attributed to convection (FCP), expressed
relative to the transplumage gain (solid line; taken as 100%). At very low
values of TASK
(TAIR-TASK>42°C),
FRP exceeds 100% because radiation also accounts for the
dissipation of the heat gained by the plumage surface from the air through
convection.
