Partitioning heat loss from mallard ducklings swimming on the airwater interface
1 Department of Ecology and Organismal Biology, Indiana State University,
Terre Haute, Indiana 47809 USA
2 Department of Biological Sciences, University of Northern Colorado,
Greeley, Colorado 80639 USA
3 South Vermillion High School, 770 West Wildcat Drive, Clinton, Indiana
47842, USA
* Author for correspondence (e-mail: LSGSB{at}isugw.indstate.edu)
Accepted 22 September 2004
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Summary |
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Key words: thermoregulation, swimming, mallard, Anas platyrhynchos, down, waterfowl, metabolism, feather
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Introduction |
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Most observed mortality occurs in class I, and class I dabbling ducklings,
such as mallards, normally swim on the surface and forage by surface skimming
and gleaning insects from emergent vegetation for the first week or two after
hatching (e.g. Pehrsson, 1979;
Ringelman and Flake, 1980
).
Despite its apparent ecological importance, thermoregulation of downy
waterbird chicks during surface swimming has received limited attention
(Eppley, 1984
;
Steen et al., 1989
;
Sutter and MacArthur, 1992
).
None of these studies attempted to partition heat loss to air and water, even
though a large fraction of North American ducks breed in the pothole prairie
area of the central plains, where the continental climate is characterized by
widely varying combinations of air and water temperature. The relative
importance of air vs water temperature for thermoregulation is
largely unknown. Thus, knowledge of how heat loss is partitioned to air and
water could significantly improve our understanding of the physiological
ecology of hatchling waterfowl.
To address this question, we conducted experiments using swimming 23-day-old mallard ducklings exposed to various combinations of air and water temperature. This allowed us to make separate estimates of the heat transfer coefficients to air and to water. These coefficients determine the relative importance of heat loss to air vs water for young ducklings.
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Material and methods |
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Experimental apparatus
Ducklings swam in an acrylic respirometry box mounted in a water flow tank
(cf. Vogel and LaBarbera,
1978; Fish, 1995
).
A female decoy identical to the one used for imprinting was positioned just
above the water surface in front of the respirometry chamber to guide the
ducklings. A trolling motor (MinnKota Endura 50, Johnson Outdoors Inc.,
Sturtevant, WI, USA) generated a flow of
0.25 m s1. A
purpose-built turbine meter with optical pulse readout was calibrated against
a Prandtl-design Pitot tube and used to monitor water velocity during
experiments. Fairings and screens were used to create a smooth flow with
±10% or less velocity variation across the working section. The flow
tank was placed in a walk-in environmental chamber. A thermostatically
controlled heater and fan in the respirometry box allowed fine control of air
temperature within the respirometry box. Water temperature,
Tw, was regulated by a thermostat controlling the flow of
refrigerated propylene glycol solution from a recirculating chiller (Icewagon
30 WCLT, GCI Industrial Refrigeration, Wilmington, DE, USA) through copper
heat-exchange tubing in the flow tank. The tank was filled from the city water
supply and changed regularly to avoid accumulating contaminants that might
increase down wetting (Stephenson and
Andrews, 1997
; Stephenson,
1997
).
The open-circuit respirometry equipment and procedures used in this study
generally followed Bakken et al.
(1991,
1996
,
2002
) with some changes in
instrumentation. Prior studies have reported that exchange of oxygen between
water and air in the animal enclosure is not significant
(Woakes and Butler, 1983
;
Ancel et al., 2000
), and we
found no effects in empty chamber trials using nitrogen dilution to simulate
metabolism. Nevertheless, we allowed for this possibility by using a reference
chamber of the same volume and with the same area exposed to the water in the
flow tank. The animal enclosure and reference enclosures were each supplied
with dry, CO2-free outdoor air at 1.5 l min1.
Flow rates were regulated by a mass flow controller (Tylan FC-260, Coastal
Instruments, Burgaw, NC, USA), calibrated on-site against a bubble meter
(Levy, 1964
).
Air leaving the chambers flowed continuously to a sampling manifold adjacent to the oxygen analyzer. We measured the oxygen content of a dry, CO2-free 200 ml min1 subsample of air leaving the animal and reference chambers during the last 10 s of alternating 1 min intervals. The electrochemical oxygen analyzer (FC-1, Sable Systems, Henderson, NV, USA) equilibrated 2030 s after switching gas sources. We corrected all O2 exchange data to STP. Switching allowed pseudo-differential operation that provided continuous baseline correction for changes in building pressure and any oxygen exchange with water in the flow tank.
Oxygen consumption was computed for each consecutive 2 min sample interval
during the experiment using standard Z-transform methods to avoid chamber
washout issues (Bakken et al.,
1981; Bartholomew et al.,
1981
). Overall respirometry errors from all sources were 2% or
less, directly validated by using an infusion pump, which added either
nitrogen or oxygen at known rates (Fedak
et al., 1981
; Bakken,
1991
). As our ducklings were not fasting, we converted oxygen
consumption to heat production rate M (W) assuming 20.9 J
ml1 O2. Data were averaged over the 20 min data
collection period to smooth transients, as this procedure gives improved
estimates of thermoregulatory demands
(Bakken et al., 1981
).
We used copperconstantan thermocouples (type TT, Omega Engineering, Stamford, CT, USA) to measure air and water temperatures. All data were recorded with a digital data logger (CR-21X, Campbell Scientific, Logan, UT, USA). Data logger control outputs were used to regulate air and water temperatures, step through a predetermined air temperature sequence and switch the sampling valve.
Each duckling was randomly assigned to one of six water temperatures (5, 10, 15, 20, 25 or 30°C). During two consecutive 30 min runs, each duckling was exposed to two air temperatures in random order, one low (5°C above Tw) and the other high (either 15 or 20°C above Tw). Metabolic rate was recorded during the last 20 min of each run, so that ducklings had 10 min to adjust to new conditions before data were recorded. Experiments were conducted during active phase with 300 lux illumination. At the end of the trial (on or before 1700 h), each duckling was returned to the holding pool. Any ducklings that had become hypothermic (<37°C) while swimming were first placed in an incubator, where they quickly recovered normal body temperature and behavior.
Thermographic measurement of body temperature
Body temperature was estimated from the thermographic temperature of a
shaved area of scalp directly over the brain. Creating this bare spot may
result in a slight increase in convective heat loss to air. However,
thermography was particularly useful in our study because it avoids both
abdominal surgery and cloacal thermocouples, either of which could disrupt the
structure of the down in contact with water and increase wetting
(Fabricius, 1956;
Nye, 1964
). Mallard ducklings
are dependent on air retained in the down for insulation when swimming, and
quickly become hypothermic when the down is saturated (G.S.B., unpublished
data; Nye, 1964
).
We recorded overhead thermograms of the duckling using a radiometric thermal imager with an 80° lens attachment (FLIR ThermaCam PM575, FLIR Systems, North Billerica, MA, USA) placed in an opening in the top of the metabolism enclosure. Images (0.1°C resolution over a 20 to 350°C range) were recorded every 5 s or 10 s and transmitted to a laptop computer and stored on the hard drive. These images were then analyzed with proprietary software (IRwin Research 2.1, FLIR Systems, North Billerica, MA, USA) to obtain apparent scalp temperature (Fig. 1A). These temperatures were corrected for zero drift and the transmission of the 80° lens attachment to obtain true scalp temperatures (Fig. 1B). A preliminary series of experiments on N=30 ducklings of the same age swimming in the same apparatus were used to generate a regression model that predicted cloacal temperature (measured with a thermocouple) with a standard deviation of less than 1°C (Fig. 1C). Averaging values derived from multiple images gave Tb with a 95% accuracy of ±1°C or better.
|
Data analysis
For heat transfer analysis, the duckling is divided into two areas, aerial
and aqueous, and analyzed using a two-dimensional heat transfer model
(Bakken, 1981). The operative
temperature acting on the aerial surface of the duckling,
Te, is equal to air temperature Ta in
our experimental enclosures (Bakken,
1976
; appendix C). Thus, the equation has the form:
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![]() | (2) |
The thermal conductances can be obtained using multiple linear regression with (TbTa) and (TbTw) as the independent variables and Ke and G as the regression coefficients. Because evaporative cooling may occur even when ambient air is saturated, the actual thermal conductances are smaller than these estimates, but the ratio of heat loss to air vs water is unaffected.
We used SYSTAT 7.0 for all statistical analyses
(Wilkinson, 1996). We used a
preliminary linear regression model to test possible experimental covariates
(mass, order of air temperatures, date, gender, time since hatching, area of
down showing surface wetting, and measures of swimming performance). We
screened the data for potential outliers (data points with large
Z-transformed residuals), which may result from experimental problems
or data copying errors (Draper and Smith,
1981
).
Previous studies have found that metabolic rate may have a nonlinear dependence on body mass, and most thermoregulatory metabolism studies have found thermal conductance to have a nonlinear dependence on ambient temperature. Therefore, we examined partial residual plots for such effects and, where appropriate, constructed and tested models with nonlinear terms.
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Results |
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Calibrated thermographic body temperatures have been plotted in
Fig. 2. Ducklings that had no
wetting or slight surface wetting that did not penetrate to the skin were able
to defend a normothermic body temperature of 39.5±0.8°C for 1 h in
water as cold as 5°C as long as their down was not penetrated by water.
Body temperature increased to an average of 41.5±0.5°C in 30°C
water. Typical body temperatures for 3-day-old mallard ducklings are
4042°C, and Tb=39°C is considered to be the
minimum homeothermic value (Ostnes and
Bech, 1997).
|
Metabolic rate and heat loss to air and water
Various regression procedures, including forward and backward stepwise
analysis and all-possible-models, found mass to be the only significant
covariate. The average mass of ducklings in this study was 48±5.7 g,
and this range of variation was too small to allow us to assign an exponent to
the mass dependence. It is not clear that there is a universal `best'
intraspecific exponent for the variation of metabolic rate with mass. Thus, we
express the variation of M with mass as a linear function of the
deviation of individual mass from the mean (m48). Over a small
range of mass variation, this model is indistinguishable from an otherwise
similar model using any reasonable mass exponent.
Thermal conductance typically increases as a curvilinear function of
ambient temperature (e.g. Bakken et al.,
1991,
1999
). To test for this, we
made rough estimates of the heat transfer coefficients Ke
and G in Equation 2 by
first fitting a linear model and plotting model residuals vs
Tw. These showed the expected curvilinear increase of duckling
thermal conductance with Tw. There is no theoretical
expectation for the exact form of the increase of conductance with
temperature. Therefore, we first tested a variety of 2nd to 5th order
polynomial models for G, as heat loss to the water is the dominant
avenue of heat loss. All such models gave a significantly better fit than a
linear model (P to enter or remove <0.0001), but
r2 varied little among the curvilinear models (range
0.988>r2>0.986). With no clear statistical basis for
selecting a particular curvilinear model, we arbitrarily used the model that
gave the largest r2 and best visual fit,
G=Go(1+bTw4).
Here, Go is the minimum thermal conductance at low water
temperatures, and b is a regression coefficient. A similar analysis
found that the best-fit model for conductance to air, Ke,
was a simple constant. Incorporating the best-fit values of the regression
coefficients:
![]() | (3) |
This model is plotted together with the mass-adjusted data in Fig. 3. The main effect, the variation in heat loss to the water as a function of water temperature, is indicated by the slope of the lines. The additional effect of variation in Ta is indicated by the vertical separation of the lines. Even at a water temperature of 30°C and an air temperature of 45°C, metabolic rate data give no evidence of a thermal neutral zone.
|
To visualize the variation of G with Tw, we calculated partial residuals of this model with respect to (TbTw) and divided by TbTw to obtain individual estimates of G. These estimates are plotted in Fig. 4, together with the conductance model from Equation 3, G=0.0450(1+1.059x106 Tw4). The measured thermal conductance to air, computed similarly, is also plotted in Fig. 4, together with the conductance model from Equation 3, Ke=0.0188.
|
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Discussion |
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The use of infrared thermography to make remote measurement of
Tb using calibrated scalp temperatures
(Bakken et al., 2005) was
particularly valuable in our study because it avoided the problem that
indwelling cloacal thermocouples disrupt the down structure and increase the
probability of serious wetting.
Overall, the lower limit for the temperature tolerance of swimming
ducklings with minimal or no wetting of the down was 5°C or less
(Fig. 2). This is similar to
the 010°C low air temperature limit reported for dabbling ducks in
prior studies (e.g. Koskimies and Lahti,
1964; Untergasser and Hayward,
1972
; Bakken et al.,
1999
). The effectiveness of air within the down as insulation from
water contact, coupled with very low blood flow to the tibiotarsus and feet
(Kilgore and Schmidt-Nielsen,
1975
) apparently accounts for the similar low temperature
tolerances of swimming and non-swimming ducklings.
Heat transfer properties
As shown in Fig. 4, our
ducklings had a low and constant conductance to the air,
Ko=0.0188 W/°C-animal at all air temperatures
(Ta). Conductance to the water is approximately constant
for Tw<20°C at G=0.0450 W/°C-animal.
Thus, assuming Tw=Ta,
Equation 3 predicts that 70% of
total metabolic heat production is lost to the water under cold (<15°C)
conditions. This estimate is conservative, as our ducklings maintained air
within the ventral plumage and heat loss to air may have been increased by
trimming the down for scalp thermography. Thermal conductance, and thus heat
loss to water, increased at higher temperatures. Presumably this is the result
of increasing blood flow to the feet. The increase in heat loss from ducklings
appears to begin (Fig. 4) at
the same or somewhat higher temperatures (1823°C), as does the
increase in heat loss from feet to water in adult mallards (18°C;
Kilgore and Schmidt-Nielsen,
1975).
Comparison with other studies of birds swimming on the airwater
interface is difficult because these used constant air temperatures close to
water temperature and therefore could not partition heat loss between air and
water (e.g. Prange and Schmidt-Nielsen,
1970; Eppley,
1984
; Steen et al.,
1989
; Sutter and MacArthur,
1992
; de Vries and van Eerden,
1995
). We can make limited comparisons by noting that the overall
conductance of our 23-day-old ducklings swimming with little or no down
wetting, assuming Ta=Tw
10°C,
is 0.065 W/°C-animal. This is 1.51.6 times the conductance of
12-day-old mallard ducklings in 10°C air
(Bakken et al., 1999
). This
increase in conductance is comparable to that of adult mallards resting in
water, which have a metabolic rate 1.4 times that in air at the same
temperature (Prange and Schmidt-Nielsen,
1970
). The metabolic rate of 12-day-old eider ducklings
(Somateria mollissima) at 0°C shows a 1.4-fold increase when
their feet are in salt water (Steen et
al., 1989
). Eider ducklings are larger (5075 g) than
mallards of similar age, have dense down, and are notably cold hardy.
Consequently, it is surprising that the ratio is only slightly better than for
our mallards. A possible explanation is that they were tested in 0°C salt
water, and may have begun to increase blood flow to their feet to prevent
freezing as do adult mallards (Kilgore and
Schmidt-Nielsen, 1975
).
Heat transfer from adult carcasses of an assortment of water birds in
simulated swimming postures showed a greater ratio of overall conductance in
water to conductance in air, ranging from 2.0 to 2.5
(de Vries and van Eerden,
1995). The substantial difference between live animal and carcass
studies suggests that carcass studies may not be useful predictors of live
animal responses.
Class Ia dabbling ducklings, i.e. 15-day-old ducklings (such as
mallards), normally swim on the surface and forage by surface skimming and
gleaning insects from emergent vegetation (e.g.
Pehrsson, 1979;
Ringelman and Flake, 1980
).
Although water temperature has the largest effect on metabolic rate, ambient
air temperature significantly modifies heat loss. Thus, environmental factors,
weighted by the time spent swimming, must be included in environmental
energetics studies of young dabbling ducklings.
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Acknowledgments |
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