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Thermoregulation on the air–water interface—II: Foot conductance, activity metabolism and a two-dimensional heat transfer model
ARTICLE IN PRESS
Journal of Thermal Biology 31 (2006) 491–500 www.elsevier.com/locate/jtherbio
Thermoregulation on the air–water interface—II: Foot conductance, activity metabolism and a two-dimensional heat transfer model Matthew J. Van Sant1, George S. Bakken Department of Ecology and Organismal Biology, Indiana State University, Terre Haute, Indiana 47809, USA Received 16 February 2006; accepted 2 May 2006
Abstract We used a quasi-adiabatic calorimeter and respirometry apparatus to measure heat loss from the feet of 3- to 4-d-old mallard ducklings (Anas platyrhynchos). We found that, at cool (o20 1C) operative temperatures, foot conductance increased in proportion to operative temperature, Te, rather than water temperature. We combined these results with those of an earlier study to develop a heat transfer model for swimming ducklings. This model includes separate thermal conductances to air (0.027 W/1C-animal), to water through the down (0.035[1+2.05 107T4e ]) W/1C-animal, and to water through the feet (2.01 108T4e W/1C-animal). The overall conductance by all three routes is only 21% greater when swimming compared to standing in air at the same operative temperature. Interestingly, ducklings can maintain body temperature 439 1C while swimming in 5 1C water, but not when restrained in a calorimeter with 5 1C water. Peak oxygen consumption is greater when swimming, and apparently exercise metabolism substitutes almost completely for thermoregulatory heat production. r 2006 Elsevier Ltd. All rights reserved. Keywords: Thermoregulation; Swimming; Mallard; Anas platyrhynchos; Down; Feet; Vasomotor; Waterfowl; Metabolism; Heat transfer model; Thermal conductance; Air temperature; Water temperature; Operative temperature; Activity and thermoregulation
1. Introduction In complex environments, different parts of an animal experience different thermal conditions. Further, different parts of an animal have different physiological heat transfer characteristics (e.g. Scholander and Krog, 1957; Howell and Bartholomew, 1962; Steen and Steen, 1965; Bartholomew, 1966; Ohmart and Lasiewski, 1971). Thus, local heat transfer characteristics interact with the local thermal environment to determine the effective operative temperature of a thermally complex habitat. Two-dimensional heat transfer models (Bakken, 1981) indicate that animals have significant potential to thermoregulate by increasing thermal conductance to body surfaces exposed to favorable parts of their thermal environment and decreasing thermal conductance elsewhere. Corresponding author. Tel.: +812 237 2396; fax: +812 237 4480.
E-mail address: [email protected] (G.S. Bakken). Present address: Department of Biology, University of California, Riverside, CA, USA. 1
0306-4565/$ - see front matter r 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.jtherbio.2006.05.002
Birds swimming on the water surface present an interesting study system. Different parts of the body are exposed to radically different environments, and thus could effectively utilize regional thermoregulatory mechanisms. This is particularly true for many species of dabbling ducks that inhabit mid-continental areas characterized by rapid air temperature changes and ponds and rivers of varying depth and hence water temperatures. Banta et al. (2004) simultaneously measured the thermal conductance of swimming mallard ducklings (Anas platyrhynchos) to air and to water. This was accomplished by measuring metabolic rate under different combinations of air and water temperature and fitting a regression model based on heat transfer physics, with the thermal conductances represented by the multiple regression coefficients. This study found that thermal conductance to air was essentially constant, while conductance to water increased at higher water temperatures. This indicated that the swimming ducklings were varying thermal conductance to water for thermoregulation. However, this study did not distinguish between heat lost to the water through the
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ventral down and heat lost through the unfeathered legs and feet. There is no obvious physiological mechanism for regulating heat loss to water through the down, as the down fibers are too soft to be much affected by ptiloerection when in contact with water. It may be possible to vary the thermal conductance of the subcutaneous fat layer under the down by varying circulation, but it is not clear that this could have a large effect on heat transfer (Scholander et al., 1950; Wilson et al., 1992). A number of studies have shown that birds can adjust heat loss from their legs and feet (e.g. Steen and Steen, 1965; Bernstein, 1974; Kilgore and Schmidt-Nielsen, 1975; Baudinette et al., 1976; Torre-Bueno, 1976; Midtga˚rd, 1980; Udvardy, 1983; Brent et al., 1985; Martineau and Larochelle, 1988; Wilson et al., 1998). Regulation is accomplished by varying total blood flow, by diverting blood flow through a countercurrent heat exchanger (Steen and Steen, 1965; Kilgore and Schmidt-Nielsen, 1975; Midtga˚rd, 1980), or both. Adult mallard ducks have a rudimentary rete tibiotarsale for countercurrent heat exchange, and blocking blood flow through the rete somewhat reduced their ability to vary heat loss (Midtga˚rd, 1980). The purpose of our study was to extend the work of Banta et al. (2004) and develop a three-component, twodimensional heat transfer model of mallard ducklings. We measured respiratory gas exchange and heat loss from the legs and feet of 3- to 4-d-old mallard ducklings simultaneously. In order to combine our data with those from earlier studies (Kilgore and Schmidt-Nielsen, 1975; Banta et al., 2004) we used similar animals and methods. This allowed us to combine our data with data from these studies to address three questions. First, what is the thermal conductance of the feet and legs, and are thermoregulatory vasomotor responses regulated primarily by overall thermal stress or by local temperature? Second, over the 5–30 1C range of temperatures for which comparative data are available for adult mallards (Kilgore and Schmidt-Nielsen, 1975), does the ability to regulate heat loss through feet and legs differ between hatchlings and adults? Third, how are the thermal conductances to air through the down, to water through down, and to water through the feet and legs best described mathematically in a heat transfer model of a 3- to 4-d-old surface-swimming mallard duckling?
turing, Savannah, GA, USA). Parents were derived from wild stock (ca. fifth generation). After hatching, ducklings were maintained under the same conditions and in the same apparatus as before, except that ducklings were imprinted on the experimenters in order to facilitate handling during testing. Food (20% protein poultry crumble, Graham Feed Company, Terre Haute, IN, USA) and water were available ad libitum. Ducklings were tested when 3–4 d old, and were not post-absorptive when metabolic measurements began. During experiments, body temperature was measured with a cloacal thermocouple (Bakken et al., 2005).
2.2. Calorimeter To make measurements of foot heat loss from hatchling mallards, we constructed a quasi-adiabatic calorimeter similar to that used by Kilgore and Schmidt-Nielsen (1975) in their study of adult mallards (Fig. 1). A central waterfilled Dewar flask constituted the calorimeter. To reduce heat gain or loss from the room to negligible levels, it was surrounded by a two-piece shield regulated at nearly the same temperature as the water in the flask. The main part of the shield surrounded the Dewar flask. A 10-mm-thick hollow copper top with two holes for the duckling’s legs was sealed over the flask and lower shield assembly with
2. Materials and methods 2.1. Animal care and housing Experimental procedures were approved by the Institutional Animal Care and Use Committee, and closely followed those used by Banta et al. (2004). Fertilized duck eggs were obtained from a commercial breeder (Whistling Wings, Hanover, IL, USA) and incubated in the laboratory in a commercial incubator (Model 1202, GQF Manufac-
Fig. 1. Schematic diagram of calorimeter and metabolic chamber (for clarity, not to exact scale). A hollow lid was cemented to a 350-ml Dewar flask, and this assembly sealed inside a larger container to form a water jacket. Water was circulated through the lid and between the large container and the flask to maintain jacket temperature 0.170.1 1C above Tw. The duckling was secured with mesh cloth and its feet were inserted through holes in the calorimeter lid. An acrylic metabolic chamber was then mounted directly over the duckling.
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silicone rubber. The calorimeter shield was kept slightly warmer (0.170.1 1C) than the water in the calorimeter to prevent latent heat transfer to the lid by water evaporating from the calorimeter, diffusing through the 8–10-mm air space between the water and lid, and condensing on the lid of the calorimeter shield. Preliminary tests verified that this could occur and was quantitatively significant when the water in the calorimenter was warmer than the shield, but did not occur when the water was cooler than the shield. Latex diaphragm seals minimized both latent heat transfer and respiratory gas exchange between the respirometer and the water in the calorimeter, while allowing some movement of the feet. The water surface was ca. 8–10 mm below the lid, and we estimated that the foot and tarsometatarsus would be completely immersed with the legs extended normally. An 8-junction type TT differential thermopile using a stirred distilled-water ice bath as the reference measured temperature change in the calorimeter with a theoretical temperature resolution of o0.01 1C. Type TT (precision copper-constantan) thermocouples measured air, water, and body (cloacal) temperatures. A digital data logger (CR-23X, Campbell Scientific, Logan, UT, USA) recorded absolute temperatures to 70.1 1C and thermopile output to 71 mV, and regulated calorimeter jacket temperature. Heat added to the calorimeter by either the duckling or an electrical calibration heat source, Hw (W), was calculated as Hw ¼ mcp(DTw/Dt), where mc is the mass (g) of water in the calorimeter, cp is the specific heat of water (4.18 J/g1C), and the change in calorimeter water temperature during a measurement interval was DTw/Dt (1C/s). Heat is also stored in the glass wall of the Dewar flask. Initial calibrations using an electronic resistor immersed in the calorimeter and agitated by a low-speed motor determined that increasing mc by 15 g accounted for this additional heat capacity and gave correct readings over the range of heat flow rates expected in this study. The continuing accuracy of the calorimeter was validated after each duckling trial by using the same resistor to generate a known heat flow comparable to that generated by ducklings. With the 15 g adjustment to mc, the mean difference between measured and known heat flow rates was 0.0070.014 (s.d.) W for N ¼ 55 post-trial calibrations. The change in calorimeter water temperature over the course of the experiment was 1–2 1C or less. For calculations involving water temperature, we used the average temperature during the experiment as Tw. 2.3. Respirometry We placed an acrylic metabolic chamber over the calorimeter in order to make concurrent measurements of respiratory gas exchange (Fig. 1). A heater coil and a 12 V, 2.2 W desktop computer processor cooling fan (model 273–153, Radio Shack, Fort Worth, TX USA) operated at 6 V, 0.6 W regulated air temperature and mixed the air in the chamber.
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Respiratory gas exchange was measured using an open-circuit system with a dry, CO2-free airflow rate of 1.0 liter/min. Instruments and procedures were as described in Banta et al. (2004). Overall accuracy was checked periodically by substituting a known oxygen flow from a syringe pump for the duckling (Fedak et al., 1981; Bakken, 1991). The agreement was better than 3%. Oxygen consumption was converted to heat production M (W) assuming 20.9 J/ml O2. Evaporative cooling was not measured, as we had no way of preventing evaporation from excreta, and nearly all animals defecated during experiments. Neither could evaporative cooling be measured in the swimming study (Banta et al., 2004). However, true heat transfer coefficients require that evaporative cooling be subtracted from metabolic heat production. Therefore, we estimated evaporative cooling, Eest (W), by using regression model for 1- to 2-d-old ducklings studied under similar humidity conditions (Ereg, Table 1 in Bakken et al., 1999). These equations were used directly (Eest ¼ Ereg) for the present calorimeter study. When using data from Banta et al. (2004), we adjusted this evaporative cooling estimate for the higher humidity in the swimming experiment by the ratio of the vapor density differences, E est ¼ E reg ½rð40 CÞ rðT w Þ=½rð40 CÞ rð10 CÞ.
(1)
Here, r(T) is the saturation vapor density over water at temperature T. Normothermic duckling body temperature averaged around 40 1C (range 39–42 1C) during the swimming study (Banta et al., 2004), and the dewpoint during the evaporative water loss measurements was less than or equal to 10 1C (Bakken et al., 1999). 2.4. Experimental procedure Regional thermoregulatory mechanisms or ‘‘thermal windows’’ may be regulated by total heat stress (including heat produced by activity, e.g. Scholander and Krog, 1957; Baudinette et al., 1976; Bakken, 1980), by temperatures acting on the same region of the body (particularly if tissue injury is imminent, e.g. Kilgore and Schmidt-Nielsen, 1975; Barber and Crawford, 1979), or both (Scholander et al., 1950; Scholander, 1955). To determine whether swimming mallard ducklings regulated foot heat loss in response to the water temperature acting on the foot or to total thermal load, we used different combinations of air and water temperature and analyzed the metabolic data as did Banta et al. (2004) to determine separate heat transfer coefficients to air and water. We then used these coefficients to compute operative temperature (Te, equal to standard operative temperature Tes under our experimental conditions) for use as the index of total environmental thermal load (Bakken, 1976; Banta et al., 2004). Also, these data allowed us to verify that the distribution of heat flows between air and water was similar to that while swimming. Each trial used one duckling randomly assigned to one of six water temperatures (T w ¼ 5, 10, 15, 20, 25 and
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30 1C). At the start of each trial, the calorimeter was filled to within 1 cm of the lid with a known amount of water. The duckling was then weighed, fitted with a cloacal thermocouple, placed in the calorimeter, and restrained with strips of plastic window screen and Velcros fasteners. The metabolism chamber was then secured over the duckling. Ducklings were tested during the active phase under room illumination (300 lux). During each trial, the duckling was exposed to two air temperatures (Ta) in random order, one low (5 1C above Tw) and the other high (20 or 25 1C above Tw). At each air temperature, ducklings were allowed 10 min to adjust to experimental conditions before data were recorded for 20 min. The total duration of each trial was 1 h. Restraining the duckling on the flat calorimeter lid compressed ventral down over the area in contact with the calorimeter lid, in contrast to the ventral down of swimming ducklings which remains dry and is little compressed (Bakken et al., 2006). In order that surface temperatures and heat loss through the ventral down would be comparable to those in the swimming study, we compensated for down compression by covering the calorimeter lid with a 3-mm-thick sheet of foam-rubber insulation (Fig. 1). In the analysis, this insulation was treated as part of the down. We selected this material because it gave about the same 14 W/m2 1C conductance as down samples in water (Bakken et al., 2006). We measured conductance by stacking a factory-calibrated thin film heat flux sensor (model HGS-4, Omega Engineering, Stamford, CT, USA) and samples of foam rubber and excised duckling skin and down between two aluminum blocks of known, different, temperatures. The upper block was sized to apply roughly the same pressure as would the restrained duckling, and both blocks were insulated on the five sides not in contact with the sample to ensure that heat flow was perpendicular to the samples. 2.5. Data selection and analysis Data were discarded if ducklings struggled enough to force water from the calorimeter. Struggling has been shown to increase metabolic rate and heat loss through the legs and feet (Steen and Steen, 1965) and wet down could increase both evaporative cooling and thermal conductance to the lid (Webb and King, 1984). Data from trials where body temperature fell below 39 1C were also discarded. This included all ducklings tested at Tw ¼ 5 1C and some tested at 10 and 15 1C. A total of 31 ducklings (N ¼ 62 measurements) remained for analysis. These averaged 78.77s.d. 9.6 h old and 52.37s.d. 8.4 g mass. Thermal conductance to the water through the legs and feet, Gf (W/1C) was calculated as G f ¼ H w =ðT b T w Þ,
(2)
where Hw is the rate of heat flow to the calorimeter, Tb the cloacal temperature, and Tw the calorimeter water temperature.
Swimming ducklings immerse their feet and legs fully, and the motion of paddling increases convective heat transfer. Consequently, thermal conductances measured in the calorimeter may be lower because the leg is not as thoroughly immersed, and foot position and movement in the calorimeter may differ. Thus, the calorimeter data may follow a ‘‘factor ceiling distribution’’ (Thompson et al., 1996), which results when a number of unknown and variable limiting factors reduce the measured value of the parameter of interest, such that the correct bivariate relationship is best approximated by the upper margin of the response. Several procedures have been proposed for fitting the upper margin of the data, all for linear relationships. The most appropriate for nonlinear relationships appears to be the logistic slice method proposed by Blackburn et al. (1992). Respirometry data were analyzed as in Banta et al. (2004). The duckling was divided into two areas, one contacting air and the other contacting things at calorimeter temperature (i.e., the calorimeter lid and water). Thermal conductance through each area was estimated by fitting metabolic data to a two-dimensional heat-transfer model (Bakken, 1981). We present our results as both ‘‘wet’’ conductances computed without correcting for evaporative cooling, and true or ‘‘dry’’ thermal conductances computed using estimated evaporative cooling. The equations are M ¼ cðm mo Þ þ GðT b T w Þ þ KðT b T a Þ,
(3a)
and M E est ¼ cðm mo Þ þ Gd ðT b T w Þ þ K d ðT b T a Þ. (3b) In these equations, M is the metabolic heat production and Eest the estimated evaporative cooling (both W/ animal). Both are known to vary with mass, so the difference between individual mass, m(g), and the average mass of all ducklings in the study, mo, was used as a covariate with c as the regression coefficient. Body temperature is Tb, water temperature is Tw, and air temperature is Ta (all in 1C). The regression coefficients are the wet thermal conductance to the calorimeter lid and water, G, the corresponding dry conductance, Gd, the wet thermal conductance to air, K, and the corresponding dry conductance, Kd (all W/1C-animal). Heat storage was neglected because we used data only from normothermic animals with stable Tb439 1C. Any of these conductances may vary with Tw, Ta or the rate of overall heat loss from the animal (Banta et al., 2004). Therefore, we used nonlinear regression to test for nonlinear change with ambient temperatures and overall heat loss rate. We used SYSTAT 8.0 (Wilkinson, 1996) for all statistical procedures. We determined heat transfer coefficients by using regression to fit data to heat transfer models linearized on the basis of the nonlinear model results. Confidence limits are presented as either the standard deviation about the mean or as the standard error of the
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estimate (s.e.e.), i.e., the standard deviation of data points about the regression model. The data presented here apply to the ducklings used in our study, although we believe they are generally representative of mallard ducklings. Captive-bred ducklings hatched in a constant-temperature incubator are typically heavier than wild ducklings, and may not be representative in other ways. Also, making two measurements on each duckling creates the possibility of pseudo-replication and consequent inflation of error degrees of freedom when addressing the question of how well our sample of ducklings represents all mallards. However, the significance levels we obtained are so high that this is not a real concern. 3. Results 3.1. Preliminary metabolic estimates of thermal conductances Thermal conductance to the calorimeter water and lid, G, increased as a curvilinear function of Tw. We tested power models with Tw exponents from 2 to 5 for G. All were statistically equivalent (F 4;57 ¼ 61:8267:9), but a nonlinear regression model gave a best-fit exponent of 4.2. Therefore, we used the same model as Banta et al. (2004), G ¼ G 0 (1+bT4w), where the minimum thermal conductance in cold water is G0, and b is a regression coefficient. We tested 1st–5th order polynomial models for wet thermal conductance to air, K, but only the constant term was significantly different from 0. Incorporating the best-fit regression coefficients into Eq. (3a), M ¼ 0:016ðm 52Þ þ 0:037ð1 þ 1:12 106 T 4w ÞðT b T w Þ þ 0:026ðT b T a Þ, ð4Þ s.e.e. ¼ 0.130 W, adj. r2 ¼ 0:82, F 4;57 ¼ 67:9, po0:0001. The coefficients are similar to those measured for swimming ducklings (Eq. (3), Banta et al., 2004). 3.2. Does foot heat loss respond to local temperature or overall thermal stress? The environmental thermal load can be represented by operative temperature (Bakken and Gates, 1975; Bakken, 1976, 1980). This index assigns a single effective temperature to a complex thermal environment, and can be computed for situations where different parts of the animal have different heat transfer properties and experience different thermal conditions (Bakken, 1981). For our ducklings, the appropriate model for operative temperature, Te (1C), is T e ¼ K=ðG þ KÞT a þ G=ðG þ KÞT w .
(5)
Because G is a function of Te, the coefficients in Eqs. (3) and (5) must be determined recursively. Therefore, we substituted numerical values of G0 and b from Eq. (4) into Eq. (5) to obtain a first approximation to Te. The models
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for G in Eqs. (3a) and (3b) were then changed to the form G ¼ G0 (1+bT4e ), and the regression analysis repeated. The new values of the coefficients were then used to recalculate Te. This process was repeated iteratively 3–4 times until we obtained stable values of G0, b, and Te. The final models were M ¼ 0:017ðm 52Þ þ 0:013ð1 þ 2:59 106 T 4e ÞðT b T w Þ þ 0:055ðT b T a Þ,
ð6aÞ
s.e.e. ¼ 0.14 W, adj. r2 ¼ 0:82, F 4;57 ¼ 61:6, Po0:0001, and M E est ¼ 0:017ðm 52Þ þ 0:018ð1 þ 1:079 106 T 4e Þ ðT b T w Þ þ 0:044ðT b T a Þ, ð6bÞ s.e.e. ¼ 0.14 W, adj. r2 ¼ 0:82, F 4;57 ¼ 62:2, Po0:0001. We then tested whether foot heat loss Hw is determined by the local environment (Tw) or aggregate thermal stress (Te) by using a mass-adjusted model for heat loss to calorimeter water that included all environmental temperature variables in the basic foot conductance relation G ¼ G0 (1+bT4w), H w ¼ cðm mo Þ þ ½G 0 ð1 þ be T 4e þ ba T 4a þ bw T 4w Þ ½ðT b T w Þ.
ð7Þ
Forward regression found Te to be the best predictor, while backward regression selected a linear combination of Tw and Ta, with coefficients close to the weightings of Tw and Ta in the Te calculations. In essence, the backward regression generated an approximation to the Te formula. As one might expect, the forward model using the exact values of Te computed with Eq. (5) was somewhat better than the approximate model (F 2;58 ¼ 17:8 vs. 12.04). We therefore conclude that, over our range of experimental conditions, foot heat loss varies in response to aggregate thermal stress rather than to water or air temperature. Fitting measured conductance directly, thermal conductance to the water through the feet is best described by Gf ¼ 5:30 104 ðm 52Þ þ 8:01 109 T 4e ,
(8)
s.e.e. ¼ 0.008 W, F 2;59 ¼ 15:4, P ¼ 0:0002. This regression is plotted in Fig. 2A, along with individual Gf values. Because these data may form a factor ceiling distribution (Thompson et al., 1996), we fitted the upper margin of the data using the logistic slice method (Blackburn et al., 1992). Data selection in this method is somewhat arbitrary, but to avoid excessive weighting of fluctuations, we selected the three largest foot conductance values in each 5 1C interval of Te from 15 to 40 1C. We then fitted these N ¼ 15 data points with the same model. The result is an approximate doubling of estimated foot conductance to Gfmax ¼ 5:3 104 ðm 52Þ þ 2:01 108 T 4e .
(9)
This relation is plotted in Fig. 2A as the short dashed line. Eqs. (8) and (9) will be tested for general consistency with other measurement in Section 4. For comparison with earlier studies, we also computed Pw (%), the percentage of total heat production M lost to
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Percentage of heat loss from feet
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0.08
0.06
0.04
0.02
0.0 10 (A)
20 30 Operative temperature, °C
50 40 30 20 10 0 10
40 (B)
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Fig. 2. (A) Conductance from foot to calorimeter water. Best-fit model (Eq. (8)) shown in long dash; fit to highest points only (Eq. (9)) shown in short dashes. (B). Percentage of total metabolic heat production lost to calorimeter water via feet (Eq. (10)).
the water through the feet. The data are shown in Fig. 2B, along with the best-fit regression: Pw ¼ 1:82ð1 þ 6:99 10
6
T 4e Þ,
(10)
s.e.e. ¼ 9.7%, F 1;59 ¼ 26:8, Po0:0001.
Using the high foot heat loss estimate, the models are M H w max ¼ 0:015ðm 48Þ þ 0:041ð1 þ 3:4 107 T 4e Þ ðT b T w Þ þ 0:028ðT b T a Þ, ð12aÞ s.e.e. ¼ 0.19 W, adj. r2 ¼ 0:88, F 4;61 ¼ 121, Po0:0001, and M E est H w max ¼ 0:015ðm 48Þ þ 0:035
3.3. Heat transfer model of swimming ducklings
ð1 þ 2:05 107 T 4e Þ
To generate a complete three-component model of heat transfer from swimming ducklings, we combined the results from the present study with the data from Banta et al. (2004). We first computed the operative temperature appropriate to each data point in the swimming duckling study. Using these operative temperatures, we estimated Gf with Eq. (8) or (9) (see below) for each data point in the swimming study. We then computed foot heat loss as H w ¼ G f ðT b 2T w Þ and subtracted it from the measured heat production. This gave use the heat production of the swimming ducklings (average mass mo ¼ 48 g) corrected for foot heat loss. We fitted these corrected data with the a priori heat loss model (Eq. (3)). The thermal conductances through down to air and through the down to water are again found as the regression coefficients to the adjusted data. We generated models for wet and dry conductances assuming either best-fit or maximum foot heat loss. Using the best-fit foot heat loss estimate, the swimming duckling models are
ðT b T w Þ þ 0:027ðT b T a Þ,
M H w ¼ 0:015ðm 48Þ þ 0:041ð1 þ 6:9 107 T 4e Þ ðT b T w Þ þ 0:028ðT b T a Þ,
ð11aÞ
s.e.e. ¼ 0.19 W, adj. r2 ¼ 0:85, F 4;61 ¼ 91, Po0:0001, and M E est H w ¼ 0:015ðm 48Þ þ 0:034ð1 þ 6:2 107 T 4e Þ ðT b T w Þ þ 0:027ðT b T a Þ, ð11bÞ s.e.e. ¼ 0.18 W, adj. r2 ¼ 0:86, F 4;61 ¼ 104, Po0:0001.
ð12bÞ 2
s.e.e. ¼ 0.18 W, adj. r ¼ 0:90, F 4;61 ¼ 138, Po0:0001. The conductances for individual data points were then calculated by dividing partial residuals by the appropriate temperature difference. Some of the dry conductances from these models have been plotted in Fig. 3. 3.4. Area measurements for heat transfer comparisons We measured the area of the foot as twice the area of a traced outline of the feet of specimens, plus the area of the tarsometatarsus estimated as the area of a cylinder of the same length and average diameter. We found the surface area of the feet and associated tarsometatarsi for both legs to be 111.979.6 (s.d.) cm2 for N ¼ 2 adults and 30.873.8 (s.d.) cm2 for N ¼ 4 ducklings. To estimate the surface area of down in contact with water while swimming, we photographed a 64-g duckling, swimming in a narrow glass channel using a telephoto lens to minimize parallax errors. We then estimated the area of the ellipsoidal surface below the water line as the area of the sector of a sphere with the same sector depth and a sector radius equal to the average of the major and minor elliptical semi-axes. We scaled this area to the 48-g average mass of ducklings in the swimming study using the ratio of the total outer surface areas estimated from body mass (Walsberg and King, 1978). The area in contact with the water so estimated was 38 cm2.
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Fig. 3. (A) Dry conductance to water with heat loss from foot removed, as estimated from the best-fit regression (Eq. (11b)). (B) Conductance to water with heat loss from foot removed, as estimated from the high estimate regression (Eq (12b)). (C) Conductance to swim tank air (Eq. (12b)). This is lower than conductance to the air as measured in calorimeter test, probably because of less surface area while swimming. (D) Comparison of conductances in Eq. (12b) via down to air (solid), via down to water (medium dash), and via feet to calorimeter water (short dash, from Fig. 2A) assuming the higher foot conductance.
4. Discussion 4.1. Heat transfer from feet and legs Because both individual thermal conductances and their sum (total conductance) are similar when the same model is used in the calorimeter (Eq. (4)) as in the swimming studies (Eq. (3), Banta et al., 2004), it is likely that vasomotor responses in the feet while swimming would be similar to those measured in the calorimeter apparatus at the same Te. The shorter legs of ducklings compared to adults might make it more difficult for ducklings to reduce heat loss via their legs and feet at low temperatures. This can be tested by comparing, on a unit-area basis, our data on duckling foot heat loss and the heat loss data for adults in Kilgore and Schmidt-Nielsen (1975; note that their apparatus was isothermal, so that in their study Tw ¼ Ta ¼ Te). The minimal thermal conductances of the feet are ca. 1.7 W/1C m2 for adults at Teo20 1C vs. 0.9970.6 W/1C m2 for N ¼ 11 ducklings at Teo25 1C. Duckling unit-area conductance would be close to that of adults if the high-margin assumption (cf. Eq. (9)) is
used. In either case, ducklings appear to do as well as adults in minimizing foot heat loss. Prior studies of the ability of water birds to thermoregulate by varying heat loss through the foot reported the percentage of total metabolic heat production lost to the water. For ducklings (Fig. 2B), the percentages were 3% and 10% at operative temperatures of 15 and 27 1C, respectively (roughly 6–20% if the high margin assumption is used), while for adult mallards the percentages were 4% and 12% at 15 and 25 1C (Kilgore and Schmidt-Nielsen, 1975). The percentage of total metabolic heat production lost to the water from the legs and feet of ducklings is thus similar to or somewhat greater than that measured for adult ducks at low temperatures. There are no data above 30 1C in Kilgore and Schmidt-Nielsen (1975), so we cannot compare the ability of adults and ducklings to dump excess heat in hot conditions. 4.2. Heat loss in aquatic vs. terrestrial environments To compare total thermal conductance of ducklings in different environmental situations using data from
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different studies, we adjusted for differences in duckling size by converting data to area-specific values based on total feather surface area as estimated from body mass by Walsberg and King (1978). At low temperatures (Teo20 1C), the average overall conductance of swimming ducklings (5.90 W/m2 1C) was 22% greater than that of younger (1- to 2-d-old) ducklings standing in air with wind o0.2 m/s (4.85 W/m2 1C, Bakken et al., 1999), and 21% higher than that of 3–4-d-old ducklings standing in air with wind o0.4 m/s (4.88 W/m2 1C, N ¼ 20 ducklings, unpubl. data from Bakken et al., 2005). The strikingly low increase in conductance while swimming is possible because several factors minimize heat loss to water. First, at low temperatures, little heat is lost from the legs and feet. However, the conductance does not approach zero as implied by Eqs. (8) and (9). Other studies have found that conductance increases to prevent tissue injury as Tw approached 0 1C, (e.g. Kilgore and Schmidt-Nielsen, 1975). Second, the down in contact with the water remained largely dry during the swimming studies, and clearly retained considerable insulation value (Bakken et al., 2006). Third, the buoyancy of a duckling with dry down is such that only about 1/3 of the feather surface area is in contact with the water. An independent estimate of conductance through down to water clarifies whether the regression to all data (Eq. (8)) or the upper margin of the data cloud (Eq. (9)) most accurately describes the thermal conductance of the feet and legs. The average thermal conductance to water through dry down is 14.371.4 W/m2 (N ¼ 12, Bakken et al., 2006). Multiplying by the 0.0038-m2 area in contact with water gives a maximum conductance estimate of 0.053 W/1C-animal. This result has been plotted in Fig. 3A and B as a dotted horizontal line. The conductance of live birds could be lower because of peripheral vasoconstriction and tissue cooling, as the skin side of the down sample was regulated at body core temperature in the apparatus used to measure down conductance. However, measured conductance can exceed this estimate only if down is wetted or if foot heat loss was underestimated in the calorimeter study. Comparison of Figs. 3A and B shows that the metabolic estimate of the conductance through down to water exceeds the 0.053 W/1C-animal estimate at higher temperatures when all data points (Eq. (8)) are used to estimate foot heat loss, but not when the upper margin of the data cloud (Eq. (9)) is used. As the down was not significantly wetted in the study by Banta et al. (2004), we suspect that our calorimeter data underestimate foot and leg heat loss while swimming because the leg was not as fully immersed in the calorimeter water as it would have been while swimming. Further, the variation in our data (Fig. 2A) suggests that the degree of immersion or movement of the feet may have differed among ducklings. Therefore, Eq. (9) is probably the better model of our data for foot conductance of swimming ducklings. At low temperatures (Teo20), the metabolic estimate of thermal conductance to water in Fig. 3B is lower than the
computation using heat flow plate data on down. This indicates that either the ventral tissues make a significant contribution to tissue insulation, that Eq. (9) underestimates heat loss from the feet, or both. Resolution of this residual uncertainty will require an improved calorimeter design that reduces the dead space between the animal and the water surface and allows observation of foot position and motion. 4.3. Substitution of activity metabolism for thermoregulation An interesting unanticipated result of this study is that gross motor activity appears to be necessary for ducklings to be able to thermoregulate below ca. 10–15 1C. None of the ducklings could maintain homeothermy (T b 439 1C, Ostnes and Bech, 1997) for 1 h when the calorimeter was filled with 5 1C water, nor could some individuals tested at 10 and 15 1C. In contrast, ducklings of the same age and mass remained homeothermic while swimming in 5 1C water for 1 h (Banta et al., 2004). The highest measured metabolic rates of free-swimming ducklings (ca. 2.2–2.5 W/ animal) were greater than those of the slightly larger ducklings in the present experiment (ca. 1.5–1.7 W/animal). We conclude that the inability to thermoregulate at low temperatures is because the ducklings’ range of leg movement was more restricted in the calorimeter than when swimming, which reduced activity-related metabolism. Birds are known to use heat generated by motor activity for thermoregulation (Woakes and Butler, 1983; Paladino and King, 1984; Webster and Weathers, 1990; Bevan and Butler, 1992; Zerba and Walsberg, 1992; Chai et al., 1998). However, there is no evidence of non-shivering thermogenesis (see review by Hohtola, 2002). Thus, if one assumes a substantial fraction of the heat generated by activity can be used for thermoregulation (Paladino and King, 1984), then actively swimming ducklings would have greater peak thermogenesis and better cold tolerance than ducklings restrained in the calorimeter, as observed. 4.4. Ecological significance The down of mallard ducklings in contact with the water remains dry while swimming, and consequently heat transfer is low (ca. 14 W/m2 1C, Bakken et al., 2006). In contrast, approximating a naked paddling foot as a 2 cm 2 cm flat plate moving at 1 m/s in water gives a conductance of ca. 500–600 W/m2 1C. Clearly, thermoregulation while swimming in water requires that heat transfer to the body core be minimized. While some terrestrial birds have feathered legs, it is unlikely that feathers could remain unsaturated while paddling, and feathers would probably interfere with hydrodynamic efficiency while paddling. Thus, vasomotor mechanisms for minimizing heat transfer through the legs (e.g. Scholander and Krog, 1957; Steen and Steen, 1965) are critical for the ability of mallard ducklings to forage in cold water.
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Because foot heat loss can be reduced to negligible levels, swimming mallard ducklings can thermoregulate effectively as long as the down remains dry (Banta et al., 2004). Dabbling ducklings less than 1 to 2 weeks old normally feed on the surface and rarely use adult foraging behaviors such as tip-up and diving that result in substantial immersion (e.g. Chura, 1961; Sugden, 1973; Pehrsson, 1979; Ringelman and Flake, 1980). Swimming with dry down minimizes thermoregulatory costs and maximizes the amount of food energy available for growth. Conductance is greatly increased when the down is saturated. This may also account for the preference of dabbling ducklings for evading predators by hydroplaning over the surface rather than diving (Beard, 1964; Aigeldinger and Fish, 1995). Nevertheless, ducklings may become saturated while diving to pursue high-value food such as minnows (Pietz and Buhl, 1999) or to escape predators (Chura, 1961; Pietz and Buhl, 1999). Thus, total energy budgets based on our data for dry ducklings may underestimate field energetic requirements.
Acknowledgments This work was supported by NSF Grant IBN 99-82076 to GSB, by a grant from the Indiana Academy of Sciences to MJVS, and by Indiana State University. Experimental protocols were approved by the Indiana State University Institutional Animal Care and Use Committee, 06-132003:GB.
References Aigeldinger, T.L., Fish, F.E., 1995. Hydroplaning by ducklings: overcoming limitations to swimming at the water surface. J. Exp. Biol. 198, 1567–1574. Bakken, G.S., 1976. A heat transfer analysis of animals: unifying concepts and the application of metabolism chamber data to field ecology. J. Theor. Biol. 60, 337–384. Bakken, G.S., 1980. The use of standard operative temperature in the study of the thermal energetics of birds. Physiol. Zool. 53, 108–119. Bakken, G.S., 1981. A two-dimensional operative-temperature model for thermal energy management by animals. J. Therm. Biol. 6, 23–30. Bakken, G.S., 1991. Time-resolved respirometry: equations for the simultaneous measurement of all respiratory gases and the calibration of oxygen consumption using variable inert gas flow rates. J. Therm. Biol. 16, 313–315. Bakken, G.S., Gates, D.M., 1975. Heat-transfer analysis of animals: some implications for field ecology, physiology, and evolution. In: Gates, D.M., Schmerl, R.B. (Eds.), Perspectives of Biophysical Ecology. Springer, New York, pp. 255–290. Bakken, G.S., Reynolds, P.S., Kenow, K.P., Korschgen, C.E., Boysen, A.F., 1999. Metabolic response to air temperature and wind in day-old mallards and a standard operative temperature scale. Physiol. Biochem. Zool. 72, 656–665. Bakken, G.S., Van Sant, M.J., Lynott, A.J., Banta, M.R., 2005. Predicting small endotherm body temperatures from scalp temperatures. J. Therm. Biol. 30, 221–228. Bakken, G.S., Banta, M.R., Higginbotham, C.M., Lynott, A.J., 2006. It’s just ducky to be clean: the water repellency and water penetration resistance of swimming mallard ducklings. J. Avian Biol., in press.
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Banta, M.J., Lynott, A.J., VanSant, M.J., Bakken, G.S., 2004. Thermoregulation on the air–water interface. J. Exp. Biol. 207, 4551–4557. Barber, B.J., Crawford, E.C., 1979. Dual threshold control of peripheral temperature in the lizard Dipsosaurus dorsalis. Physiol. Zool. 52, 250–263. Bartholomew, G.A., 1966. The role of behavior in the temperature regulation of the masked booby. Condor 68, 523–535. Baudinette, R.V., Loveridge, J.P., Wilson, K.J., Mills, C.D., SchmidtNielsen, K., 1976. Heat loss from feet of herring gulls at rest and during flight. Am. J. Physiol. 230, 920–924. Beard, E.B., 1964. Duck brood behavior at the Seney National Wildlife Refuge. J. Wildlife Manage. 23, 492–521. Bernstein, M.H., 1974. Vascular responses and foot temperature in pigeons. Am. J. Physiol. 226, 1350–1355. Bevan, R.M., Butler, P.J., 1992. The effects of temperature on the oxygen consumption, heart rate, and deep body temperature during diving in the tufted duck Aythya fuligula. J. Exp. Biol. 163, 139–151. Blackburn, T.M., Lawton, J.H., Perry, J.N., 1992. A method of estimating the slope of upper bounds of plots of body size and abundance in natural animal assemblages. Oikos 65, 107–112. Brent, R., Pedersen, P.F., Bech, C., Johansen, K., 1985. Thermal balance in the European Coot, Fulica atra exposed to temperatures from 28 1C to 40 1C. Ornis Scand. 16, 145–150. Chai, P., Chang, A.C., Dudley, R., 1998. Flight thermogenesis and energy conservation in hovering hummingbirds. J. Exp. Biol. 201, 963–968. Chura, N.J., 1961. Food availability and preferences of juvenile mallards. Trans. N. Am. Wildlife Natural Resourc. Conf. 26, 121–134. Fedak, M.A., Rome, L., Seeherman, H.J., 1981. One-step N2-dilution technique for calibrating open-circuit VO2 measuring systems. J. Appl. Physiol. 51, 772–776. Hohtola, E., 2002. Facultative and obligatory thermogenesis in young birds: a cautionary note. Comp. Biochem. Physiol. A 131, 733–739. Howell, T.R., Bartholomew, G.A., 1962. Temperature regulation in the sooty tern Sterna fuscata. Ibis 104, 98–106. Kilgore, D.L., Schmidt-Nielsen, K., 1975. Heat loss from ducks’ feet immersed in cold water. Condor 77, 475–517. Martineau, L., Larochelle, J., 1988. The cooling power of pigeon legs. J. Exp. Biol. 136, 193–208. Midtga˚rd, U., 1980. Heat loss from the feet of Mallards Anas platyrhynchos and arterio-venous heat exchange in the Rete tibiotarsale. Ibis 122, 354–359. Ohmart, R.D., Lasiewski, R.C., 1971. Roadrunners: energy conservation by hypothermia and absorption of sunlight. Science 172, 67–69. Ostnes, J.E., Bech, C., 1997. Ontogeny of deep-cold sensitivity in Pekin ducklings Anas platyrhynchos. J. Comp. Physiol. B 167, 241–248. Paladino, F.V., King, J.R., 1984. Thermoregulation and oxygen consumption during terrestrial locomotion by White-crowned sparrows Zonotrichia leucophrys gambelii. Physiol. Zool. 57, 226–236. Pehrsson, O., 1979. Feeding behavior, habitat utilization, and feeding efficiency of mallard ducklings (Anas platyrhynchos L.) as guided by a domestic duck. Viltrevy 10, 193–218. Pietz, P.J., Buhl, D.A., 1999. Behaviour patterns of mallard Anas platyrhynchos pairs and broods in Minnesota and North Dakota. Wildfowl 50, 101–122. Ringelman, J.K., Flake, L.D., 1980. Diurnal visibility and activity of bluewinged teal and mallard broods. J. Wildlife Manage. 44, 822–829. Scholander, P.F., 1955. Evolution of climatic adaptation in homeotherms. Evolution 9, 15–26. Scholander, P.F., Krog, J., 1957. Countercurrent heat exchange and vascular bundles in sloths. J. Appl. Physiol. 10, 405–411. Scholander, P.F., Walters, V., Hock, R., Irving, L., 1950. Body insulation of some arctic and tropical mammals and birds. Biol. Bull. 99, 225–236. Steen, I., Steen, J.B., 1965. The importance of the legs in the thermoregulation of birds. Acta Physiol. Scand. 63, 285–291. Sugden, L.G., 1973. Feeding ecology of pintail, gadwall, American widgeon and lesser scaup ducklings in southern Alberta. Can. Wildlife Serv. Rep. Ser. 24, 1–43.
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Wilkinson, L., 1996. Statistics: Systat 6.0 for Windows. SPSS, Chicago, IL. Wilson, R.P., Hustler, K., Ryan, P.G., Burger, A.E., No¨ldeke, E.C., 1992. Diving birds in cold water: do Archimedes and Boyle determine energetic costs? Am. Nat. 140, 179–200. Wilson, R.P., Adelung, D., Latorre, L., 1998. Radiative heat loss in gentoo penguin (Pygoscelis papua) adults and chicks and the importance of warm feet. Physiol. Zool. 71, 524–533. Woakes, A.J., Butler, P.J., 1983. Swimming and diving in tufted ducks, Aythya fuligula, with particular reference to heart rate and gas exchange. J. Exp. Biol. 107, 311–329. Zerba, E., Walsberg, G.E., 1992. Exercise-generated heat contributes to thermoregulation by Gambel’s quail in the cold. J. Exp. Biol. 171, 400–422.
Journal of Thermal Biology 31 (2006) 491–500 www.elsevier.com/locate/jtherbio
Thermoregulation on the air–water interface—II: Foot conductance, activity metabolism and a two-dimensional heat transfer model Matthew J. Van Sant1, George S. Bakken Department of Ecology and Organismal Biology, Indiana State University, Terre Haute, Indiana 47809, USA Received 16 February 2006; accepted 2 May 2006
Abstract We used a quasi-adiabatic calorimeter and respirometry apparatus to measure heat loss from the feet of 3- to 4-d-old mallard ducklings (Anas platyrhynchos). We found that, at cool (o20 1C) operative temperatures, foot conductance increased in proportion to operative temperature, Te, rather than water temperature. We combined these results with those of an earlier study to develop a heat transfer model for swimming ducklings. This model includes separate thermal conductances to air (0.027 W/1C-animal), to water through the down (0.035[1+2.05 107T4e ]) W/1C-animal, and to water through the feet (2.01 108T4e W/1C-animal). The overall conductance by all three routes is only 21% greater when swimming compared to standing in air at the same operative temperature. Interestingly, ducklings can maintain body temperature 439 1C while swimming in 5 1C water, but not when restrained in a calorimeter with 5 1C water. Peak oxygen consumption is greater when swimming, and apparently exercise metabolism substitutes almost completely for thermoregulatory heat production. r 2006 Elsevier Ltd. All rights reserved. Keywords: Thermoregulation; Swimming; Mallard; Anas platyrhynchos; Down; Feet; Vasomotor; Waterfowl; Metabolism; Heat transfer model; Thermal conductance; Air temperature; Water temperature; Operative temperature; Activity and thermoregulation
1. Introduction In complex environments, different parts of an animal experience different thermal conditions. Further, different parts of an animal have different physiological heat transfer characteristics (e.g. Scholander and Krog, 1957; Howell and Bartholomew, 1962; Steen and Steen, 1965; Bartholomew, 1966; Ohmart and Lasiewski, 1971). Thus, local heat transfer characteristics interact with the local thermal environment to determine the effective operative temperature of a thermally complex habitat. Two-dimensional heat transfer models (Bakken, 1981) indicate that animals have significant potential to thermoregulate by increasing thermal conductance to body surfaces exposed to favorable parts of their thermal environment and decreasing thermal conductance elsewhere. Corresponding author. Tel.: +812 237 2396; fax: +812 237 4480.
E-mail address: [email protected] (G.S. Bakken). Present address: Department of Biology, University of California, Riverside, CA, USA. 1
0306-4565/$ - see front matter r 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.jtherbio.2006.05.002
Birds swimming on the water surface present an interesting study system. Different parts of the body are exposed to radically different environments, and thus could effectively utilize regional thermoregulatory mechanisms. This is particularly true for many species of dabbling ducks that inhabit mid-continental areas characterized by rapid air temperature changes and ponds and rivers of varying depth and hence water temperatures. Banta et al. (2004) simultaneously measured the thermal conductance of swimming mallard ducklings (Anas platyrhynchos) to air and to water. This was accomplished by measuring metabolic rate under different combinations of air and water temperature and fitting a regression model based on heat transfer physics, with the thermal conductances represented by the multiple regression coefficients. This study found that thermal conductance to air was essentially constant, while conductance to water increased at higher water temperatures. This indicated that the swimming ducklings were varying thermal conductance to water for thermoregulation. However, this study did not distinguish between heat lost to the water through the
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ventral down and heat lost through the unfeathered legs and feet. There is no obvious physiological mechanism for regulating heat loss to water through the down, as the down fibers are too soft to be much affected by ptiloerection when in contact with water. It may be possible to vary the thermal conductance of the subcutaneous fat layer under the down by varying circulation, but it is not clear that this could have a large effect on heat transfer (Scholander et al., 1950; Wilson et al., 1992). A number of studies have shown that birds can adjust heat loss from their legs and feet (e.g. Steen and Steen, 1965; Bernstein, 1974; Kilgore and Schmidt-Nielsen, 1975; Baudinette et al., 1976; Torre-Bueno, 1976; Midtga˚rd, 1980; Udvardy, 1983; Brent et al., 1985; Martineau and Larochelle, 1988; Wilson et al., 1998). Regulation is accomplished by varying total blood flow, by diverting blood flow through a countercurrent heat exchanger (Steen and Steen, 1965; Kilgore and Schmidt-Nielsen, 1975; Midtga˚rd, 1980), or both. Adult mallard ducks have a rudimentary rete tibiotarsale for countercurrent heat exchange, and blocking blood flow through the rete somewhat reduced their ability to vary heat loss (Midtga˚rd, 1980). The purpose of our study was to extend the work of Banta et al. (2004) and develop a three-component, twodimensional heat transfer model of mallard ducklings. We measured respiratory gas exchange and heat loss from the legs and feet of 3- to 4-d-old mallard ducklings simultaneously. In order to combine our data with those from earlier studies (Kilgore and Schmidt-Nielsen, 1975; Banta et al., 2004) we used similar animals and methods. This allowed us to combine our data with data from these studies to address three questions. First, what is the thermal conductance of the feet and legs, and are thermoregulatory vasomotor responses regulated primarily by overall thermal stress or by local temperature? Second, over the 5–30 1C range of temperatures for which comparative data are available for adult mallards (Kilgore and Schmidt-Nielsen, 1975), does the ability to regulate heat loss through feet and legs differ between hatchlings and adults? Third, how are the thermal conductances to air through the down, to water through down, and to water through the feet and legs best described mathematically in a heat transfer model of a 3- to 4-d-old surface-swimming mallard duckling?
turing, Savannah, GA, USA). Parents were derived from wild stock (ca. fifth generation). After hatching, ducklings were maintained under the same conditions and in the same apparatus as before, except that ducklings were imprinted on the experimenters in order to facilitate handling during testing. Food (20% protein poultry crumble, Graham Feed Company, Terre Haute, IN, USA) and water were available ad libitum. Ducklings were tested when 3–4 d old, and were not post-absorptive when metabolic measurements began. During experiments, body temperature was measured with a cloacal thermocouple (Bakken et al., 2005).
2.2. Calorimeter To make measurements of foot heat loss from hatchling mallards, we constructed a quasi-adiabatic calorimeter similar to that used by Kilgore and Schmidt-Nielsen (1975) in their study of adult mallards (Fig. 1). A central waterfilled Dewar flask constituted the calorimeter. To reduce heat gain or loss from the room to negligible levels, it was surrounded by a two-piece shield regulated at nearly the same temperature as the water in the flask. The main part of the shield surrounded the Dewar flask. A 10-mm-thick hollow copper top with two holes for the duckling’s legs was sealed over the flask and lower shield assembly with
2. Materials and methods 2.1. Animal care and housing Experimental procedures were approved by the Institutional Animal Care and Use Committee, and closely followed those used by Banta et al. (2004). Fertilized duck eggs were obtained from a commercial breeder (Whistling Wings, Hanover, IL, USA) and incubated in the laboratory in a commercial incubator (Model 1202, GQF Manufac-
Fig. 1. Schematic diagram of calorimeter and metabolic chamber (for clarity, not to exact scale). A hollow lid was cemented to a 350-ml Dewar flask, and this assembly sealed inside a larger container to form a water jacket. Water was circulated through the lid and between the large container and the flask to maintain jacket temperature 0.170.1 1C above Tw. The duckling was secured with mesh cloth and its feet were inserted through holes in the calorimeter lid. An acrylic metabolic chamber was then mounted directly over the duckling.
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silicone rubber. The calorimeter shield was kept slightly warmer (0.170.1 1C) than the water in the calorimeter to prevent latent heat transfer to the lid by water evaporating from the calorimeter, diffusing through the 8–10-mm air space between the water and lid, and condensing on the lid of the calorimeter shield. Preliminary tests verified that this could occur and was quantitatively significant when the water in the calorimenter was warmer than the shield, but did not occur when the water was cooler than the shield. Latex diaphragm seals minimized both latent heat transfer and respiratory gas exchange between the respirometer and the water in the calorimeter, while allowing some movement of the feet. The water surface was ca. 8–10 mm below the lid, and we estimated that the foot and tarsometatarsus would be completely immersed with the legs extended normally. An 8-junction type TT differential thermopile using a stirred distilled-water ice bath as the reference measured temperature change in the calorimeter with a theoretical temperature resolution of o0.01 1C. Type TT (precision copper-constantan) thermocouples measured air, water, and body (cloacal) temperatures. A digital data logger (CR-23X, Campbell Scientific, Logan, UT, USA) recorded absolute temperatures to 70.1 1C and thermopile output to 71 mV, and regulated calorimeter jacket temperature. Heat added to the calorimeter by either the duckling or an electrical calibration heat source, Hw (W), was calculated as Hw ¼ mcp(DTw/Dt), where mc is the mass (g) of water in the calorimeter, cp is the specific heat of water (4.18 J/g1C), and the change in calorimeter water temperature during a measurement interval was DTw/Dt (1C/s). Heat is also stored in the glass wall of the Dewar flask. Initial calibrations using an electronic resistor immersed in the calorimeter and agitated by a low-speed motor determined that increasing mc by 15 g accounted for this additional heat capacity and gave correct readings over the range of heat flow rates expected in this study. The continuing accuracy of the calorimeter was validated after each duckling trial by using the same resistor to generate a known heat flow comparable to that generated by ducklings. With the 15 g adjustment to mc, the mean difference between measured and known heat flow rates was 0.0070.014 (s.d.) W for N ¼ 55 post-trial calibrations. The change in calorimeter water temperature over the course of the experiment was 1–2 1C or less. For calculations involving water temperature, we used the average temperature during the experiment as Tw. 2.3. Respirometry We placed an acrylic metabolic chamber over the calorimeter in order to make concurrent measurements of respiratory gas exchange (Fig. 1). A heater coil and a 12 V, 2.2 W desktop computer processor cooling fan (model 273–153, Radio Shack, Fort Worth, TX USA) operated at 6 V, 0.6 W regulated air temperature and mixed the air in the chamber.
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Respiratory gas exchange was measured using an open-circuit system with a dry, CO2-free airflow rate of 1.0 liter/min. Instruments and procedures were as described in Banta et al. (2004). Overall accuracy was checked periodically by substituting a known oxygen flow from a syringe pump for the duckling (Fedak et al., 1981; Bakken, 1991). The agreement was better than 3%. Oxygen consumption was converted to heat production M (W) assuming 20.9 J/ml O2. Evaporative cooling was not measured, as we had no way of preventing evaporation from excreta, and nearly all animals defecated during experiments. Neither could evaporative cooling be measured in the swimming study (Banta et al., 2004). However, true heat transfer coefficients require that evaporative cooling be subtracted from metabolic heat production. Therefore, we estimated evaporative cooling, Eest (W), by using regression model for 1- to 2-d-old ducklings studied under similar humidity conditions (Ereg, Table 1 in Bakken et al., 1999). These equations were used directly (Eest ¼ Ereg) for the present calorimeter study. When using data from Banta et al. (2004), we adjusted this evaporative cooling estimate for the higher humidity in the swimming experiment by the ratio of the vapor density differences, E est ¼ E reg ½rð40 CÞ rðT w Þ=½rð40 CÞ rð10 CÞ.
(1)
Here, r(T) is the saturation vapor density over water at temperature T. Normothermic duckling body temperature averaged around 40 1C (range 39–42 1C) during the swimming study (Banta et al., 2004), and the dewpoint during the evaporative water loss measurements was less than or equal to 10 1C (Bakken et al., 1999). 2.4. Experimental procedure Regional thermoregulatory mechanisms or ‘‘thermal windows’’ may be regulated by total heat stress (including heat produced by activity, e.g. Scholander and Krog, 1957; Baudinette et al., 1976; Bakken, 1980), by temperatures acting on the same region of the body (particularly if tissue injury is imminent, e.g. Kilgore and Schmidt-Nielsen, 1975; Barber and Crawford, 1979), or both (Scholander et al., 1950; Scholander, 1955). To determine whether swimming mallard ducklings regulated foot heat loss in response to the water temperature acting on the foot or to total thermal load, we used different combinations of air and water temperature and analyzed the metabolic data as did Banta et al. (2004) to determine separate heat transfer coefficients to air and water. We then used these coefficients to compute operative temperature (Te, equal to standard operative temperature Tes under our experimental conditions) for use as the index of total environmental thermal load (Bakken, 1976; Banta et al., 2004). Also, these data allowed us to verify that the distribution of heat flows between air and water was similar to that while swimming. Each trial used one duckling randomly assigned to one of six water temperatures (T w ¼ 5, 10, 15, 20, 25 and
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30 1C). At the start of each trial, the calorimeter was filled to within 1 cm of the lid with a known amount of water. The duckling was then weighed, fitted with a cloacal thermocouple, placed in the calorimeter, and restrained with strips of plastic window screen and Velcros fasteners. The metabolism chamber was then secured over the duckling. Ducklings were tested during the active phase under room illumination (300 lux). During each trial, the duckling was exposed to two air temperatures (Ta) in random order, one low (5 1C above Tw) and the other high (20 or 25 1C above Tw). At each air temperature, ducklings were allowed 10 min to adjust to experimental conditions before data were recorded for 20 min. The total duration of each trial was 1 h. Restraining the duckling on the flat calorimeter lid compressed ventral down over the area in contact with the calorimeter lid, in contrast to the ventral down of swimming ducklings which remains dry and is little compressed (Bakken et al., 2006). In order that surface temperatures and heat loss through the ventral down would be comparable to those in the swimming study, we compensated for down compression by covering the calorimeter lid with a 3-mm-thick sheet of foam-rubber insulation (Fig. 1). In the analysis, this insulation was treated as part of the down. We selected this material because it gave about the same 14 W/m2 1C conductance as down samples in water (Bakken et al., 2006). We measured conductance by stacking a factory-calibrated thin film heat flux sensor (model HGS-4, Omega Engineering, Stamford, CT, USA) and samples of foam rubber and excised duckling skin and down between two aluminum blocks of known, different, temperatures. The upper block was sized to apply roughly the same pressure as would the restrained duckling, and both blocks were insulated on the five sides not in contact with the sample to ensure that heat flow was perpendicular to the samples. 2.5. Data selection and analysis Data were discarded if ducklings struggled enough to force water from the calorimeter. Struggling has been shown to increase metabolic rate and heat loss through the legs and feet (Steen and Steen, 1965) and wet down could increase both evaporative cooling and thermal conductance to the lid (Webb and King, 1984). Data from trials where body temperature fell below 39 1C were also discarded. This included all ducklings tested at Tw ¼ 5 1C and some tested at 10 and 15 1C. A total of 31 ducklings (N ¼ 62 measurements) remained for analysis. These averaged 78.77s.d. 9.6 h old and 52.37s.d. 8.4 g mass. Thermal conductance to the water through the legs and feet, Gf (W/1C) was calculated as G f ¼ H w =ðT b T w Þ,
(2)
where Hw is the rate of heat flow to the calorimeter, Tb the cloacal temperature, and Tw the calorimeter water temperature.
Swimming ducklings immerse their feet and legs fully, and the motion of paddling increases convective heat transfer. Consequently, thermal conductances measured in the calorimeter may be lower because the leg is not as thoroughly immersed, and foot position and movement in the calorimeter may differ. Thus, the calorimeter data may follow a ‘‘factor ceiling distribution’’ (Thompson et al., 1996), which results when a number of unknown and variable limiting factors reduce the measured value of the parameter of interest, such that the correct bivariate relationship is best approximated by the upper margin of the response. Several procedures have been proposed for fitting the upper margin of the data, all for linear relationships. The most appropriate for nonlinear relationships appears to be the logistic slice method proposed by Blackburn et al. (1992). Respirometry data were analyzed as in Banta et al. (2004). The duckling was divided into two areas, one contacting air and the other contacting things at calorimeter temperature (i.e., the calorimeter lid and water). Thermal conductance through each area was estimated by fitting metabolic data to a two-dimensional heat-transfer model (Bakken, 1981). We present our results as both ‘‘wet’’ conductances computed without correcting for evaporative cooling, and true or ‘‘dry’’ thermal conductances computed using estimated evaporative cooling. The equations are M ¼ cðm mo Þ þ GðT b T w Þ þ KðT b T a Þ,
(3a)
and M E est ¼ cðm mo Þ þ Gd ðT b T w Þ þ K d ðT b T a Þ. (3b) In these equations, M is the metabolic heat production and Eest the estimated evaporative cooling (both W/ animal). Both are known to vary with mass, so the difference between individual mass, m(g), and the average mass of all ducklings in the study, mo, was used as a covariate with c as the regression coefficient. Body temperature is Tb, water temperature is Tw, and air temperature is Ta (all in 1C). The regression coefficients are the wet thermal conductance to the calorimeter lid and water, G, the corresponding dry conductance, Gd, the wet thermal conductance to air, K, and the corresponding dry conductance, Kd (all W/1C-animal). Heat storage was neglected because we used data only from normothermic animals with stable Tb439 1C. Any of these conductances may vary with Tw, Ta or the rate of overall heat loss from the animal (Banta et al., 2004). Therefore, we used nonlinear regression to test for nonlinear change with ambient temperatures and overall heat loss rate. We used SYSTAT 8.0 (Wilkinson, 1996) for all statistical procedures. We determined heat transfer coefficients by using regression to fit data to heat transfer models linearized on the basis of the nonlinear model results. Confidence limits are presented as either the standard deviation about the mean or as the standard error of the
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estimate (s.e.e.), i.e., the standard deviation of data points about the regression model. The data presented here apply to the ducklings used in our study, although we believe they are generally representative of mallard ducklings. Captive-bred ducklings hatched in a constant-temperature incubator are typically heavier than wild ducklings, and may not be representative in other ways. Also, making two measurements on each duckling creates the possibility of pseudo-replication and consequent inflation of error degrees of freedom when addressing the question of how well our sample of ducklings represents all mallards. However, the significance levels we obtained are so high that this is not a real concern. 3. Results 3.1. Preliminary metabolic estimates of thermal conductances Thermal conductance to the calorimeter water and lid, G, increased as a curvilinear function of Tw. We tested power models with Tw exponents from 2 to 5 for G. All were statistically equivalent (F 4;57 ¼ 61:8267:9), but a nonlinear regression model gave a best-fit exponent of 4.2. Therefore, we used the same model as Banta et al. (2004), G ¼ G 0 (1+bT4w), where the minimum thermal conductance in cold water is G0, and b is a regression coefficient. We tested 1st–5th order polynomial models for wet thermal conductance to air, K, but only the constant term was significantly different from 0. Incorporating the best-fit regression coefficients into Eq. (3a), M ¼ 0:016ðm 52Þ þ 0:037ð1 þ 1:12 106 T 4w ÞðT b T w Þ þ 0:026ðT b T a Þ, ð4Þ s.e.e. ¼ 0.130 W, adj. r2 ¼ 0:82, F 4;57 ¼ 67:9, po0:0001. The coefficients are similar to those measured for swimming ducklings (Eq. (3), Banta et al., 2004). 3.2. Does foot heat loss respond to local temperature or overall thermal stress? The environmental thermal load can be represented by operative temperature (Bakken and Gates, 1975; Bakken, 1976, 1980). This index assigns a single effective temperature to a complex thermal environment, and can be computed for situations where different parts of the animal have different heat transfer properties and experience different thermal conditions (Bakken, 1981). For our ducklings, the appropriate model for operative temperature, Te (1C), is T e ¼ K=ðG þ KÞT a þ G=ðG þ KÞT w .
(5)
Because G is a function of Te, the coefficients in Eqs. (3) and (5) must be determined recursively. Therefore, we substituted numerical values of G0 and b from Eq. (4) into Eq. (5) to obtain a first approximation to Te. The models
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for G in Eqs. (3a) and (3b) were then changed to the form G ¼ G0 (1+bT4e ), and the regression analysis repeated. The new values of the coefficients were then used to recalculate Te. This process was repeated iteratively 3–4 times until we obtained stable values of G0, b, and Te. The final models were M ¼ 0:017ðm 52Þ þ 0:013ð1 þ 2:59 106 T 4e ÞðT b T w Þ þ 0:055ðT b T a Þ,
ð6aÞ
s.e.e. ¼ 0.14 W, adj. r2 ¼ 0:82, F 4;57 ¼ 61:6, Po0:0001, and M E est ¼ 0:017ðm 52Þ þ 0:018ð1 þ 1:079 106 T 4e Þ ðT b T w Þ þ 0:044ðT b T a Þ, ð6bÞ s.e.e. ¼ 0.14 W, adj. r2 ¼ 0:82, F 4;57 ¼ 62:2, Po0:0001. We then tested whether foot heat loss Hw is determined by the local environment (Tw) or aggregate thermal stress (Te) by using a mass-adjusted model for heat loss to calorimeter water that included all environmental temperature variables in the basic foot conductance relation G ¼ G0 (1+bT4w), H w ¼ cðm mo Þ þ ½G 0 ð1 þ be T 4e þ ba T 4a þ bw T 4w Þ ½ðT b T w Þ.
ð7Þ
Forward regression found Te to be the best predictor, while backward regression selected a linear combination of Tw and Ta, with coefficients close to the weightings of Tw and Ta in the Te calculations. In essence, the backward regression generated an approximation to the Te formula. As one might expect, the forward model using the exact values of Te computed with Eq. (5) was somewhat better than the approximate model (F 2;58 ¼ 17:8 vs. 12.04). We therefore conclude that, over our range of experimental conditions, foot heat loss varies in response to aggregate thermal stress rather than to water or air temperature. Fitting measured conductance directly, thermal conductance to the water through the feet is best described by Gf ¼ 5:30 104 ðm 52Þ þ 8:01 109 T 4e ,
(8)
s.e.e. ¼ 0.008 W, F 2;59 ¼ 15:4, P ¼ 0:0002. This regression is plotted in Fig. 2A, along with individual Gf values. Because these data may form a factor ceiling distribution (Thompson et al., 1996), we fitted the upper margin of the data using the logistic slice method (Blackburn et al., 1992). Data selection in this method is somewhat arbitrary, but to avoid excessive weighting of fluctuations, we selected the three largest foot conductance values in each 5 1C interval of Te from 15 to 40 1C. We then fitted these N ¼ 15 data points with the same model. The result is an approximate doubling of estimated foot conductance to Gfmax ¼ 5:3 104 ðm 52Þ þ 2:01 108 T 4e .
(9)
This relation is plotted in Fig. 2A as the short dashed line. Eqs. (8) and (9) will be tested for general consistency with other measurement in Section 4. For comparison with earlier studies, we also computed Pw (%), the percentage of total heat production M lost to
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Percentage of heat loss from feet
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0.08
0.06
0.04
0.02
0.0 10 (A)
20 30 Operative temperature, °C
50 40 30 20 10 0 10
40 (B)
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Fig. 2. (A) Conductance from foot to calorimeter water. Best-fit model (Eq. (8)) shown in long dash; fit to highest points only (Eq. (9)) shown in short dashes. (B). Percentage of total metabolic heat production lost to calorimeter water via feet (Eq. (10)).
the water through the feet. The data are shown in Fig. 2B, along with the best-fit regression: Pw ¼ 1:82ð1 þ 6:99 10
6
T 4e Þ,
(10)
s.e.e. ¼ 9.7%, F 1;59 ¼ 26:8, Po0:0001.
Using the high foot heat loss estimate, the models are M H w max ¼ 0:015ðm 48Þ þ 0:041ð1 þ 3:4 107 T 4e Þ ðT b T w Þ þ 0:028ðT b T a Þ, ð12aÞ s.e.e. ¼ 0.19 W, adj. r2 ¼ 0:88, F 4;61 ¼ 121, Po0:0001, and M E est H w max ¼ 0:015ðm 48Þ þ 0:035
3.3. Heat transfer model of swimming ducklings
ð1 þ 2:05 107 T 4e Þ
To generate a complete three-component model of heat transfer from swimming ducklings, we combined the results from the present study with the data from Banta et al. (2004). We first computed the operative temperature appropriate to each data point in the swimming duckling study. Using these operative temperatures, we estimated Gf with Eq. (8) or (9) (see below) for each data point in the swimming study. We then computed foot heat loss as H w ¼ G f ðT b 2T w Þ and subtracted it from the measured heat production. This gave use the heat production of the swimming ducklings (average mass mo ¼ 48 g) corrected for foot heat loss. We fitted these corrected data with the a priori heat loss model (Eq. (3)). The thermal conductances through down to air and through the down to water are again found as the regression coefficients to the adjusted data. We generated models for wet and dry conductances assuming either best-fit or maximum foot heat loss. Using the best-fit foot heat loss estimate, the swimming duckling models are
ðT b T w Þ þ 0:027ðT b T a Þ,
M H w ¼ 0:015ðm 48Þ þ 0:041ð1 þ 6:9 107 T 4e Þ ðT b T w Þ þ 0:028ðT b T a Þ,
ð11aÞ
s.e.e. ¼ 0.19 W, adj. r2 ¼ 0:85, F 4;61 ¼ 91, Po0:0001, and M E est H w ¼ 0:015ðm 48Þ þ 0:034ð1 þ 6:2 107 T 4e Þ ðT b T w Þ þ 0:027ðT b T a Þ, ð11bÞ s.e.e. ¼ 0.18 W, adj. r2 ¼ 0:86, F 4;61 ¼ 104, Po0:0001.
ð12bÞ 2
s.e.e. ¼ 0.18 W, adj. r ¼ 0:90, F 4;61 ¼ 138, Po0:0001. The conductances for individual data points were then calculated by dividing partial residuals by the appropriate temperature difference. Some of the dry conductances from these models have been plotted in Fig. 3. 3.4. Area measurements for heat transfer comparisons We measured the area of the foot as twice the area of a traced outline of the feet of specimens, plus the area of the tarsometatarsus estimated as the area of a cylinder of the same length and average diameter. We found the surface area of the feet and associated tarsometatarsi for both legs to be 111.979.6 (s.d.) cm2 for N ¼ 2 adults and 30.873.8 (s.d.) cm2 for N ¼ 4 ducklings. To estimate the surface area of down in contact with water while swimming, we photographed a 64-g duckling, swimming in a narrow glass channel using a telephoto lens to minimize parallax errors. We then estimated the area of the ellipsoidal surface below the water line as the area of the sector of a sphere with the same sector depth and a sector radius equal to the average of the major and minor elliptical semi-axes. We scaled this area to the 48-g average mass of ducklings in the swimming study using the ratio of the total outer surface areas estimated from body mass (Walsberg and King, 1978). The area in contact with the water so estimated was 38 cm2.
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Fig. 3. (A) Dry conductance to water with heat loss from foot removed, as estimated from the best-fit regression (Eq. (11b)). (B) Conductance to water with heat loss from foot removed, as estimated from the high estimate regression (Eq (12b)). (C) Conductance to swim tank air (Eq. (12b)). This is lower than conductance to the air as measured in calorimeter test, probably because of less surface area while swimming. (D) Comparison of conductances in Eq. (12b) via down to air (solid), via down to water (medium dash), and via feet to calorimeter water (short dash, from Fig. 2A) assuming the higher foot conductance.
4. Discussion 4.1. Heat transfer from feet and legs Because both individual thermal conductances and their sum (total conductance) are similar when the same model is used in the calorimeter (Eq. (4)) as in the swimming studies (Eq. (3), Banta et al., 2004), it is likely that vasomotor responses in the feet while swimming would be similar to those measured in the calorimeter apparatus at the same Te. The shorter legs of ducklings compared to adults might make it more difficult for ducklings to reduce heat loss via their legs and feet at low temperatures. This can be tested by comparing, on a unit-area basis, our data on duckling foot heat loss and the heat loss data for adults in Kilgore and Schmidt-Nielsen (1975; note that their apparatus was isothermal, so that in their study Tw ¼ Ta ¼ Te). The minimal thermal conductances of the feet are ca. 1.7 W/1C m2 for adults at Teo20 1C vs. 0.9970.6 W/1C m2 for N ¼ 11 ducklings at Teo25 1C. Duckling unit-area conductance would be close to that of adults if the high-margin assumption (cf. Eq. (9)) is
used. In either case, ducklings appear to do as well as adults in minimizing foot heat loss. Prior studies of the ability of water birds to thermoregulate by varying heat loss through the foot reported the percentage of total metabolic heat production lost to the water. For ducklings (Fig. 2B), the percentages were 3% and 10% at operative temperatures of 15 and 27 1C, respectively (roughly 6–20% if the high margin assumption is used), while for adult mallards the percentages were 4% and 12% at 15 and 25 1C (Kilgore and Schmidt-Nielsen, 1975). The percentage of total metabolic heat production lost to the water from the legs and feet of ducklings is thus similar to or somewhat greater than that measured for adult ducks at low temperatures. There are no data above 30 1C in Kilgore and Schmidt-Nielsen (1975), so we cannot compare the ability of adults and ducklings to dump excess heat in hot conditions. 4.2. Heat loss in aquatic vs. terrestrial environments To compare total thermal conductance of ducklings in different environmental situations using data from
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different studies, we adjusted for differences in duckling size by converting data to area-specific values based on total feather surface area as estimated from body mass by Walsberg and King (1978). At low temperatures (Teo20 1C), the average overall conductance of swimming ducklings (5.90 W/m2 1C) was 22% greater than that of younger (1- to 2-d-old) ducklings standing in air with wind o0.2 m/s (4.85 W/m2 1C, Bakken et al., 1999), and 21% higher than that of 3–4-d-old ducklings standing in air with wind o0.4 m/s (4.88 W/m2 1C, N ¼ 20 ducklings, unpubl. data from Bakken et al., 2005). The strikingly low increase in conductance while swimming is possible because several factors minimize heat loss to water. First, at low temperatures, little heat is lost from the legs and feet. However, the conductance does not approach zero as implied by Eqs. (8) and (9). Other studies have found that conductance increases to prevent tissue injury as Tw approached 0 1C, (e.g. Kilgore and Schmidt-Nielsen, 1975). Second, the down in contact with the water remained largely dry during the swimming studies, and clearly retained considerable insulation value (Bakken et al., 2006). Third, the buoyancy of a duckling with dry down is such that only about 1/3 of the feather surface area is in contact with the water. An independent estimate of conductance through down to water clarifies whether the regression to all data (Eq. (8)) or the upper margin of the data cloud (Eq. (9)) most accurately describes the thermal conductance of the feet and legs. The average thermal conductance to water through dry down is 14.371.4 W/m2 (N ¼ 12, Bakken et al., 2006). Multiplying by the 0.0038-m2 area in contact with water gives a maximum conductance estimate of 0.053 W/1C-animal. This result has been plotted in Fig. 3A and B as a dotted horizontal line. The conductance of live birds could be lower because of peripheral vasoconstriction and tissue cooling, as the skin side of the down sample was regulated at body core temperature in the apparatus used to measure down conductance. However, measured conductance can exceed this estimate only if down is wetted or if foot heat loss was underestimated in the calorimeter study. Comparison of Figs. 3A and B shows that the metabolic estimate of the conductance through down to water exceeds the 0.053 W/1C-animal estimate at higher temperatures when all data points (Eq. (8)) are used to estimate foot heat loss, but not when the upper margin of the data cloud (Eq. (9)) is used. As the down was not significantly wetted in the study by Banta et al. (2004), we suspect that our calorimeter data underestimate foot and leg heat loss while swimming because the leg was not as fully immersed in the calorimeter water as it would have been while swimming. Further, the variation in our data (Fig. 2A) suggests that the degree of immersion or movement of the feet may have differed among ducklings. Therefore, Eq. (9) is probably the better model of our data for foot conductance of swimming ducklings. At low temperatures (Teo20), the metabolic estimate of thermal conductance to water in Fig. 3B is lower than the
computation using heat flow plate data on down. This indicates that either the ventral tissues make a significant contribution to tissue insulation, that Eq. (9) underestimates heat loss from the feet, or both. Resolution of this residual uncertainty will require an improved calorimeter design that reduces the dead space between the animal and the water surface and allows observation of foot position and motion. 4.3. Substitution of activity metabolism for thermoregulation An interesting unanticipated result of this study is that gross motor activity appears to be necessary for ducklings to be able to thermoregulate below ca. 10–15 1C. None of the ducklings could maintain homeothermy (T b 439 1C, Ostnes and Bech, 1997) for 1 h when the calorimeter was filled with 5 1C water, nor could some individuals tested at 10 and 15 1C. In contrast, ducklings of the same age and mass remained homeothermic while swimming in 5 1C water for 1 h (Banta et al., 2004). The highest measured metabolic rates of free-swimming ducklings (ca. 2.2–2.5 W/ animal) were greater than those of the slightly larger ducklings in the present experiment (ca. 1.5–1.7 W/animal). We conclude that the inability to thermoregulate at low temperatures is because the ducklings’ range of leg movement was more restricted in the calorimeter than when swimming, which reduced activity-related metabolism. Birds are known to use heat generated by motor activity for thermoregulation (Woakes and Butler, 1983; Paladino and King, 1984; Webster and Weathers, 1990; Bevan and Butler, 1992; Zerba and Walsberg, 1992; Chai et al., 1998). However, there is no evidence of non-shivering thermogenesis (see review by Hohtola, 2002). Thus, if one assumes a substantial fraction of the heat generated by activity can be used for thermoregulation (Paladino and King, 1984), then actively swimming ducklings would have greater peak thermogenesis and better cold tolerance than ducklings restrained in the calorimeter, as observed. 4.4. Ecological significance The down of mallard ducklings in contact with the water remains dry while swimming, and consequently heat transfer is low (ca. 14 W/m2 1C, Bakken et al., 2006). In contrast, approximating a naked paddling foot as a 2 cm 2 cm flat plate moving at 1 m/s in water gives a conductance of ca. 500–600 W/m2 1C. Clearly, thermoregulation while swimming in water requires that heat transfer to the body core be minimized. While some terrestrial birds have feathered legs, it is unlikely that feathers could remain unsaturated while paddling, and feathers would probably interfere with hydrodynamic efficiency while paddling. Thus, vasomotor mechanisms for minimizing heat transfer through the legs (e.g. Scholander and Krog, 1957; Steen and Steen, 1965) are critical for the ability of mallard ducklings to forage in cold water.
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Because foot heat loss can be reduced to negligible levels, swimming mallard ducklings can thermoregulate effectively as long as the down remains dry (Banta et al., 2004). Dabbling ducklings less than 1 to 2 weeks old normally feed on the surface and rarely use adult foraging behaviors such as tip-up and diving that result in substantial immersion (e.g. Chura, 1961; Sugden, 1973; Pehrsson, 1979; Ringelman and Flake, 1980). Swimming with dry down minimizes thermoregulatory costs and maximizes the amount of food energy available for growth. Conductance is greatly increased when the down is saturated. This may also account for the preference of dabbling ducklings for evading predators by hydroplaning over the surface rather than diving (Beard, 1964; Aigeldinger and Fish, 1995). Nevertheless, ducklings may become saturated while diving to pursue high-value food such as minnows (Pietz and Buhl, 1999) or to escape predators (Chura, 1961; Pietz and Buhl, 1999). Thus, total energy budgets based on our data for dry ducklings may underestimate field energetic requirements.
Acknowledgments This work was supported by NSF Grant IBN 99-82076 to GSB, by a grant from the Indiana Academy of Sciences to MJVS, and by Indiana State University. Experimental protocols were approved by the Indiana State University Institutional Animal Care and Use Committee, 06-132003:GB.
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