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. 2017 Dec 14;56:e37. doi: 10.6620/ZS.2017.56-37

Total Evaporative Water Loss in Birds at Different Ambient Temperatures: Allometric and Stoichiometric Approaches

Valery M Gavrilov 1,*
PMCID: PMC6517701  PMID: 31966236

Abstract

Valery M. Gavrilov (2017) Total evaporative water loss (TEWL) in Passeriformes and Non-Passeriformes was estimated by simultaneous measurements of energy expenditure and mass loss in resting birds. It was found that the percentage of heat dissipated by water evaporation depends on body size. Published data for 102 bird species were analyzed together with my own measurements for 157 bird species at thermally neutral temperatures (mostly 25°C) to establish the following relationship between TEWL and body mass: TEWL25°C Aves = 0.28 m0.701, R2 = 0.92, where TEWL is in g H2O/day and m is body mass (g). The scaling exponent 0.701 ± 0.007 is 0.05 greater than for the relationship of basal metabolic rate (BMR) to body mass. It was found that TEWL in passerines is higher than in non-passerines at all ambient temperatures by 50% at 25°C, 30% at 0°C, 39% at the lower critical temperature, and 59% at the upper critical temperature. The dependence of water loss on body mass at different ambient temperatures (TA) was found to vary in the same manner as evaporative heat loss. TEWL in Passeriformes is approximately 25-60% higher than in Non-Passeriformes (particularly at high TA), which is consistent with the ratio of their BMR levels. Within the thermoneutral zone, the proportion of heat dissipated by evaporation increases by approximately 2.6-fold in small passerines and by almost 4.1-fold in large passerines with the transition from the lower to upper critical temperature. In non-passerines, the proportion of evaporative heat losses increases by approximately 2.7 times within the thermoneutral zone in both large and small birds. The high basal metabolic rate in Passeriformes involves benefits like a higher maximum metabolic power and the ability to breed at lower ambient temperatures, but it comes with a cost: a significant expenditure of evaporative water. This cost is important because it is found to increase with body size in Passeriformes due to the forced evaporative heat loss, but it shows virtually no increase with body size in Non-Passeriformes. Thus, despite a high BMR significantly increasing ecological opportunities, this way of expanding the ecological niches is possible for the small size class only. These findings suggest that the high level of basal metabolic rate in Passeriformes in comparison to Non-Passeriformes determines the necessity for the former to utilize considerably larger amounts of water for evaporation to maintain the needed heat balance, especially at higher ambient temperatures and at larger body sizes.

Keywords: Water loss, Heat dissipation, Thermoregulation, Metabolic heat production, Energetic equivalent of the loss body mass, Birds

BACKGROUND

Evaporation is a key component of an organism’s heat balance. It depends on metabolic rate, ambient temperature and relative humidity. Total evaporative water loss (TEWL) is a part of the animal’s heat balance that is especially important under warm conditions. Birds display a broad spectrum of morphological and functional adaptations aimed at improving the water balance. TEWL studies provide insight into those ecological and morphological properties that determine the geographic distribution of avian species. In individual animals of a given species, TEWL is influenced by water availability, feeding patterns and protein content of the diet (Bernstein 1971; Lasiewski et al. 1971; Marder and Ben-Asher 1983; Marder and Gavrieli-Levin 1987; Webster and Bernstein 1987; Wolf and Walsberg 1996; Arieli et al. 2002; Ophir et al. 2002; McKechnie and Wolf 2004; DeNardo et al. 2004; Hoffman et al. 2007). Several studies have shown that rates of evaporative heat loss are correlated with metabolic rates (Hoffman and Walsberg 1999; Marder et al. 1989; McKechnie and Wolf 2004; Webster and King 1987; Withers and Williams 1990; Clark and Dudley 2009, 2010). The rate of heat dissipation is proportional to TEWL and strongly influenced by acclimatization and, presumably, by natural selection; thus, it varies among species (Williams and Tieleman 2002).

The need to maintain water balance restricts certain species to areas with sufficient rainfall, as demonstrated by studies of bird population density in Taiwan’s subtropical mountains (Walther et al. 2017). Rodríguez and Barba (2016) found that various physiological and behavioral adaptations related to water balance allow nestlings of small altricial birds to maintain a stable body temperature at high air temperatures during the breeding season.

Basal metabolic rate (BMR) and TEWL are considered to be fundamental characteristics of the animal life history (Tieleman et al. 2006; Versteegh et al. 2008). It is known that Passeriformes and Non-Passeriformes differ in their BMR: Passeriformes’ BMR is about 1.5 times higher (McNab 2009, 2016). An important question is how this difference in BMR values relates to evaporative heat losses at rest and, especially, during flight. Does a high BMR imply that closely related species or individuals are characterized by a high peak power output and therefore high energy expenditures for ordinary existence and additional works (flight in particular)? Does BMR level determine the ratio of evaporative and non- evaporative heat loss? If BMR determines the other components of the energy budget, the energy expenditures for flight and the level of evaporative cooling in passerine birds should be higher than in non-passerines. In other words, if BMR determines the upper metabolic limit, then the ratio of BMR to the upper metabolic limit should be relatively constant. It could then be expected that the ratio of TEWL to oxygen consumption in passerines is be equal to those in non-passerines. Therefore, at the same ambient temperature, Passeriformes would have a higher TEWL than Non-Passeriformes. In this paper, heat dissipation in resting birds is analyzed at various ambient temperatures using the terms described below (the stoichiometric approach).

A commonly cited allometric analysis of TEWL at thermally neutral temperatures is that of Crawford and Lasiewski (1968). They tabulated data for 42 species ranging in size from a 3-g hummingbird to a 100-kg ostrich (Struthio camelus). Williams (1996) noted that the allometric equation in Crawford and Lasiewski relating TEWL to body mass in birds was based on a relatively small sample size and constructed using procedures that might have biased the parameter estimation. In his report, Williams (1996) analyzed TEWL for 102 bird species ranging in size from hummingbirds to ostriches using both least-squares regression and phylogenetically independent contrasts. Using this approach, Williams (1996) established that (1) the slope of the allometric relationship between TEWL and body mass is higher than in the equation of Crawford and Lasiewski (1968), (2) birds from arid environments have lower TEWL than birds from more mesic environments, and (3) small and large birds have similar ratios of TEWL to oxygen consumption. The latter finding negates the idea that small desert birds replenish proportionately less of their TEWL with metabolic water than larger species do. Williams (1996) selected data taken at 25°C because this temperature is (1), at or near the lower critical temperature for many birds (2), not thermally stressful for most birds, and (3), the same temperature chosen by Crawford and Lasiewski (1968) for their analysis.

In this paper we address the following questions: (1) How do TEWL estimates based on the energy equivalent of the body mass loss (q) correspond to TEWL estimates obtained by conventional methods reviewed by Williams (1996)? Since McNab (2009, 2016) convincingly demonstrated that Passeriformes and Non- Passeriformes differ in their basal metabolic rate, we also address these questions: (2) What is the relationship between TEWL and body mass in Passeriformes and Non-Passeriformes birds at different ambient temperatures? And (3) How does the share of evaporative heat loss in Passeriformes and Non-Passeriformes vary from within the thermoneutral zone, i.e. from the lower critical temperature to the upper critical temperature?

MATERIALS AND METHODS

Bird sampling

We analyzed more than 60 species of passerine birds representing the order’s full body size range-from the goldcrest (Regulus regulus, 5.5 g) to the Raven (Corvus corax 1,208 g) - and 30 species of non-passerine birds of a similar size range (25-4,000 g). All birds were kept in big aviaries at natural day lengths and temperatures. For migratory birds and subtropical species, the aviaries were heated in winter to maintain temperatures of 5-10°C. These conditions allow for an accurate analysis of seasonal acclimatization (Proser 1991). Measurements of energy values were made in winter (November-January, February) and summer (late May-June, late August-September) on non-molting birds. Studies of seasonal variation in energy expenditure, both at rest and at ordinary existence levels, were done at experimentally controlled temperatures, where TA varied from -28°C to + 40°C to construct a thermal energy pro le for each species.

Measurements of body mass variations in birds

The following experiments were performed for a more precise determination of the rate at which food passes through the alimentary canal and the magnitude of mass loss at night. Groups of five chaffinches (Fringilla coelebs) and three wood or Carolina ducks (Aix sponsa) were placed immediately after evening feeding into a small light cage with a mesh floor. The excrements dropped sank in a cuvette with liquid mineral oil which prevented evaporation of water. The cage and the cuvette were connected to scale-levers to register body mass changes during the night.

The rate of body mass loss after evening feeding stabilizes at different times in different- sized birds: on average, it occurs 2-4 h after feeding in small birds, and 6-8 h in large birds. Further loss proceeded at constant rates determined by water evaporation. Figure 1 exemplifies this trend, showing that the alimentary canal became empty five hours after feeding in Carolina ducks (body mass 470 g) and three hours after feeding in chaffinches (body mass 21 g). Based on our experiments, we assumed that 3 hours after the last feeding in small birds and 10-12 hours in large birds is sufficient for the alimentary canal to empty.

All birds fasted for at least 3-12 h and were in the postabsorptive state during measurements. We thus assume that during measurements the body mass loss occurred at a constant rate.

Fig. 1.

Fig. 1.

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Fig. 1. Body mass loss per hour as a function of time after feeding for small (upper panel) and large (bottom panel) birds. Data for upper panel were slightly displaced horizontally to prevent overlapping. Body mass was measured every hour and thus body mass loss per hour is a mass difference between two successive measurements.

Metabolic rate measurements

All oxygen consumption values were corrected to standard pressure and temperature according to the equations of Depocas and Hart (1957). Respirometry in our modification is based on measurements of air pressure and is therefore very sensitive to temperature changes. We carefully controlled the temperature in the laboratory and employed sealed chambers during metabolic rate measurements (Gavrilov 1997 2012a b 2014 2015). If temperature fluctuations in the sealed chamber within one hour of measurements exceeded 0.3°C, the corresponding data were not used. The average volume of consumed oxygen from the entire period of metabolic rate measurements was transformed into the volume at standard temperature and pressure and converted to kJ day-1 according to the equation 1 L of O2 = 15.97 + 5.16RQ (kJ) (Schmidt-Nielsen 1997). Oxygen consumption was measured at rest at different ambient temperatures in all species studied.

Measurement of RQ

Respiratory quotient (RQ) was determined by Haldane gas analyzer (Dolnik and Gavrilov 1973 1979; Gavrilov 1997 2015; Gavrilov et al. 2013). We measured energy expenditures at rest and the respiratory quotient in 26 species of passerine birds and 16 species of non-passerine birds in winter and summer. Measurements were made at different temperatures ranging from + 5°C to + 35°C.

The stoichiometric approach for estimating total evaporative water loss

This paper applied the stoichiometric approach for the determination of TEWL developed and described by Gavrilov (2014 2015). This method includes direct simultaneous measurements of the energetic equivalent of body weight loss (q) as the ratio between heat production (metabolic rate, MR, determined by the rate of oxygen consumption) and body weight loss (dm) at various TA:

q = MR/dm

Body weight loss of an animal in the postabsorptive state at a constant relative humidity is primarily determined by water evaporation. Therefore, the caloric equivalent is directly proportional to the specific caloric value of metabolically oxidized compounds and inversely proportional to the body weight loss dm. The latter is the sum of evaporative and cloacal water losses and is equal to the difference between the weights of consumed oxygen and liberated CO2, excreted products of nitrogen metabolism (protein oxidation), and excreted gastroliths. The complete algorithm used to calculate evaporative heat loss (He) from the energetic equivalent of body weight loss at rest for any combination of oxidized compounds was published elsewhere (Gavrilov 2015). In this work, we shall only give exponential equations for the relationships between evaporative heat loss as a percentage of total heat loss (He, %) and the energetic equivalent of the body weight loss at rest. For purely lipid metabolism (lipid oxidation is the main source of energy for birds in winter) we have

% He = 238.3q-0.98, where q is in kJ/g.

Тhe oxidized substrate ratio is different in summer and the following coefficients were assumed: 0.7 for lipids, 0.1 for carbohydrates, and 0.2 for proteins (Dolnik and Gavrilov 1979; Gavrilov 2014 2015). Therefore, the energetic equivalents of body weight loss at rest were 0.7q for lipids, 0.lq for carbohydrates, and 0.2q for proteins. Тhе exponential equation for summer is

% He = 239.3q-1.05, where q is in kJ/g.

The evaporative heat loss (as a percentage of total heat loss) can be derived from the energetic equivalent of body weight loss at rest. From this relationship, we can determine the ratio between evaporative and non-evaporative heat losses at any ambient temperature.

We used the above exponential equations to calculate the percentage of evaporative heat loss (He) from experimental measurements of q. Using the obtained percentage of evaporative heat loss and total heat production (SMR or BMR), we calculated the evaporative heat loss at various ambient temperatures: He0°С, HeTlc-the lower critical temperature, He25°С, and HeTuc-the upper critical temperature. Taking into account that the evaporative heat of 1 gram of water is equal to 2.4 kJ (Garai 2009), total evaporative water loss can be represented as

TEWL = (BMR *% He /100)/2.4,

where BMR is the total heat produced at any thermoneutral temperature TA and %He is the percentage of total heat loss through evaporation at this TA.

Scaling analysis and statistic

We performed a scaling analysis of evaporative water loss in Passeriformes and Non-Passeriformes birds at different ambient temperatures and seasons. First, we studied the relationship between TEWL and body mass by collating TEWL data at various ambient temperatures.

We tested the ANOVA difference between the model in R statistic (R Development Core Team 2014) for log-transformed values of TEWL (g H2O/ day) and body mass (g).
The study was performed according to the laws of the Russian Federation and Moscow State University regarding the capture and maintenance of wild animals. All birds were released after the experiment.

RESULTS

RQ measurements

RQ values estimated in 26 species of passerine birds and 16 species of non-passerine birds at night in winter at ambient temperatures 5-35°C fell within the range 0.69-0.75 and averaged 0.72 ± 0.03 (n = 1024). These data confirmed that lipids were the primary source of energy expenditure in winter at night.

Summer RQ values for the same species at night with ambient temperatures 5-35°C fell within the range 0.74-0.82 and averaged 0.77 ± 0.08 (n = 1024). Such RQs can be measured at the following ratios of oxidizable substrates: 0.7 for fat, 0.2 for carbohydrates and 0.1 for proteins, such that RQ = 0.7*0.7 + 0.2*1 + 0.1*0.82 = 0.77.

Measurements of metabolic rate, energetic equivalent of body mass loss, and total evaporative water loss

All the data obtained on heat loss at rest (BMR, SMR) and the associated values measured (Tlc, Tuc,q, and TEWL) for all bird species for two seasons are summarized in appendix 1. As an example, the energy metabolism values obtained in summer for one passerine species, the goal tit (Parus ater), are presented graphically in Figure 2.

The dependence on TA of the resting metabolic indices at night (Fig. 2 top) corresponds exactly to Scholander’s model: SMR decreases with rising TA and theoretically attains zero at a certain TA equal to body temperature (TB) under moderately cold stress, which corresponds to the beginning of the thermoneutral zone. Quantitatively, the metabolism or heat loss (SMR) is related to TA by a linear equation

SMR = hl(TB-TA),

where hl is the heat transfer coefficient or thermal conductance; it includes losses of heat by radiation, conduction and convection at low ambient temperatures where hl is minimal. The decrease in SMR discontinues at TA = Tlc, (Tlc is the lower critical temperature). At this point, SMR becomes equal to basal metabolic rate (BMR). With a further increase in TA, the energy expenditure remains unchanged, whereas the bird passes from the minimal wet thermal conductance (hl) to the maximal (hu) attained at TA = Tuc (Tuc is the upper critical temperature): hu = (BMR)/(TB-Tuc).

Evaporative heat loss (He) dissipates 9.3% of heat at 0°C, 16.2-16.7% at Tlc and 35.1- 60.2% at Tuc. At low TA, the role of heat loss via evaporation is minor: virtually all of the energy used in thermoregulation (SMR-BMR) is expended by conduction, convection, and radiation. Evaporative heat loss increases significantly in the thermoneutral zone, even though the birds increase thermal conductance.

Fig. 2.

Fig. 2.

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Fig. 2. (A) energy expenditure at rest (SMR, BMR, kJ per day, left scales) and the energy equivalent of lost body mass (q, kJ per g, right scales) as the functions of ambient temperature (TA, °C). Each symbol is a mean for several measurements in several birds at a given TA, vertical bars are SD. (B) Evaporative heat loss (He, kJ per day, right scale), non-evaporative heat loss (Hs, kJ per day, right scales) as the functions of ambient temperature (TA, °C) and percentage of heat loss through evaporation (He, %, left scales) as the functions of ambient temperature (TA, °C) in the Goal Tits (Parus ater) in winter.

Allometric analysis

Our data for 157 bird species (Appendix 1) with a thermally neutral temperature (25°C) indicate the following relationship between TEWL and body weight: TEWL at 25°C Aves = 0.27m0.71, r2 = 0.93, where the TEWL is expressed as g H2O g/day, and body weight is expressed as g (Fig. 3A).

Fig. 3.

Fig. 3.

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Fig. 3. (A) total evaporative water loss (TEWL) at TA = 25°C as a function of body mass in all birds (this study and Willams, 1996). (B) total evaporative water loss (TEWL) at TA = 25°C as s function of body mass in Passeriformes and Non-Passeriformes (this study and Willams 1996).

Evaporative water loss in Aves (based on combined data from this and Williams' (1996) review)

Comparison of our results for TEWL-obtained using measurements of the energy equivalent to body mass loss (q) and calculated for the same temperature (25°C)-with the results obtained by conventional methods (Williams 1996) revealed a good agreement between the two approaches, as shown in figure 3A: TEWL25°C (Willams), all = 0.29m0.68, r2 = 0.90; TEWL25°C (This study), all = 0.27m0.71, r2 = 0.93. The differences are not

significant (the difference in slope is ns F = 1.4578, p = 0.2284; the difference in the y-intercepts is ns F = 0.8987, p = 0.344).

The data comparison demonstrates that determinations by the stoichiometric approach of total evaporative water loss yielded estimates that fit into the confidence intervals of all equations from the literature.

After combining the data from table 1 of Williams (1996) for 102 species of birds with my data for 157 species of birds (Appendix 1) at a thermally neutral temperature (25°C), the resulting relationship between TEWL and body weight is: TEWL at 25°C Aves = 0.28m0.70, r2 = 0.92, where the TEWL is expressed as g H2O g/day, and m is body mass (g) (Fig. 3A).

If the dichotomy between passerines and non-passerines is taken into account, we have TEWL at 25°C = 0.225m0.792 (n = 152 r2 = 0.874) SD = 0.025 for Passeriformes and TEWL at 25°C = 0.233m0.715 (n = 107 r2 = 0.929) SD = 0.019 for Non-Passeriformes. The differences are statistically significant for both the slope and y-intercept. On average, at TA = 25°C passerines expend 50% more water than non-passerines. The difference grows with increasing body size (Fig. 3B).

Note that the highest slope of the regression line of the TEWL on body mass is in passerines at 25°C, because 25°C in some species is outside the thermoneutral zone.

Table 1. Fitted curves (TEWL = amb, TEWL g/day, a - intersept, b - slope, m - body mass, g) for total evaporative water loss in various avian groups of species and comparison of TEWL in Passeriformes and non-Passeriformes birds at different ambient temperatures.

Groups of species Ambient temperatures TA N Lim m, g a - intersept b - slope r2 Differences between Passeriformes and non-Passeriformes
Differences in slope Differences in intersepts Excess of TEWL in Passeriformes by
Aves, N + D, S + W TA = 25oC 259 2.7-100000 0.28 0.70 0.917
Non-Passeriformes, N + D, S + W TA = 25oC 107 2.7-100000 0.23 0.747 0.874 t = 2.458 DF = 255 p = 0.01464 The slopes are DIFFERENT at p < 0.05 t = -2.846 DF = 255 p = 0.00479 The intercepts are DIFFERENT at p < 0.05 50%
Passeriformes, N + D, S + W TA = 25oC 152 5.5-1208 0.225 0.792 0.929
Non-Passeriformes, N, S + W TA = 0oC 53 25.2-4010 0.21 0.710 0.970 t = 1.549 DF = 153 p = 0.12343 The slopes are NOT different at p < 0.05 t = -38.336 DF = 153 p = 0.00000 The intercepts are DIFFERENT at i < 0.05 30%
Passeriformes, N, S + W TA = 0oC 103 5.5-1208 0.32 0.68 0.982
Non-Passeriformes, N, S + W TA = Tlc 53 25.2-4010 0.25 0.71 0.930 t = 1.264 DF = 153 p = 0.20804 The slopes are NOT different at p < 0.05 t = -42.675 DF = 153 p = 0.00000 The intercepts are DIFFERENT at p < 0.05 39%
Passeriformes, N, S + W TA = Tlc 103 5.5-1208 0.16 0.74 0.910
Non-Passeriformes, N, S + W = Tuc TA = Tuc 53 25.2-4010 0.45 0.73 0.985 t = -1.178 DF = 153 p = 0.24052 The slopes are NOT different at p < 0.05 t = -9.823 DF = 153 p = 0.00000 The intercepts are DIFFERENT at p < 0.05 59%
Passeriformes, N, S + W TA = Tuc 103 5.5-1208 0.56 0.78 0.969
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D - Measurements were made during the active (daytime) phase of the avian circadian cycle; N - Measurements were made during the resting (nighttime) phase of the avian circadian cycle; W - Measurements were made during the nonproductive “winter” phase of the avian annual cycle; S - Measurements were made during the nonreproductive “summer” phase of the avian annual cycle.

Total evaporative water loss in Passeriformes and non-Passeriformes at different ambient temperatures

The established allometric relationships for three different ambient temperatures for passerines and non-passerine birds are shown in figures 4A, B, C. Table 1 shows the statistical significance of each pair of equations as the slope and y-intercept for Passeriformes and Non-Passeriformes.
The smallest amount of water evaporates at TA = Tlc in Passeriformes as well as in non-

Passerifomes. The corresponding equations are: for Non-Passeriformes TEWL at TA = Tlc, TEWL = 0.155m0.739 (n = 53 r2 = 0.985) SD = 0.013,
for Passeriformes TEWL at TA = Tlc, TEWL = 0.245m0.716 (n = 104 r2 = 0.969) SD = 0.013.
The slopes are not different at p < 0.05, the intercepts are different at p < 0.05. Passerine birds on average expend 39% more water than non- passerines.

At TA = 0°C, the amount of evaporated water somewhat increases, while the exponents of the equations decrease (more in passerines than in non-passerines):

for Non-Passeriformes TEWL at 0°C = 0.210m0.707 (n = 53 r2 = 0.983) SD = 0.013,
for Passeriformes TEWL at 0°C = 0.316m0.680 (n = 104 r2 = 0.970) SD = 0.012.

The slopes are not different at p < 0.05, the intercepts are different at p < 0.05.
Passerine birds on average expend 30% more water than non-passerines.

At TA = Tuc, the amount of evaporated water rises sharply, especially in passerine birds:
for Non-Passeriformes TEWL at TA = Tuc, TEWL = 0.445m0.735 (n = 53 r2 = 0.928) SD = 0.029,

for Passeriformes TEWL at TA = Tuc, TEWL = 0.560m0.780 (n = 104 r2 = 0.908) SD = 0.025.
The slopes are not different at p < 0.05, the intercepts are different at p < 0.05. Passerine birds on average spend 59% more water than non- passerines.

With temperature increasing from Tlc to Tuc, the amount of evaporated water increases in the smallest passerines by 2.5 times compared to 4 times in the largest passerines. Meanwhile in non- passerines, the amount of evaporated water rises by approximately 3 times in both large and small birds. The established relationship between TEWL and body mass indicates that TEWL in passerine birds is higher than in non-passerine birds at all ambient temperatures (0°C, Tlc, 25°C, and Tuc). Passerines spend more water for evaporation than non-passerines: by 50% at 25°C, by 30% at 0°C, by 39% at the lower critical temperature, and by 59% at the upper critical temperature.

Evaporative heat loss in Passeriformes and Non-Passeriformes at different ambient temperatures

The share of heat dissipated by evaporation (%He) is the smallest at TA = 0°C:

for Non-Passeriformes %He at 0°C, %He = 4.379m0.154 (n = 53 r2 = 0.738) SD = 0.013,for

Passeriformes %He at 0°C, %He = 4.679m0.183 (n = 104 r2 = 0.655) SD = 0.013.

Passerines average a 1.2-fold higher %He than non-passerines.

At TA = Tlc the share of heat dissipated by evaporation is almost independent of body mass; it is about 14-18% and slightly higher in non- passerine birds:

for Non-Passeriformes %He at TA = Tlc, %He = 13.919m0.033 (n = 53 r2 = 0.131) SD = 0.012,

for Passeriformes %He at TA = Tlc, %He = 13.467 m-0.019 (n = 104 r2 = 0.004) SD = 0.030.

At TA = Tuc the share of heat dissipated by evaporation increases by 38-60%, especially in passerines:

for Non-Passeriformes %He at TA = Tuc, %He = 38.001m0.039 (n = 53 r2 = 0.062) SD = 0.021,

for Passeriformes %He at TA = Tuc, %He = 35.950m0.083 (n = 104 r2 = 0.177) SD = 0.018.

The share of heat dissipated by evaporation increases within the thermoneutral zone (i.e. with temperature rising from Tlc to Tuc) by approximately 2.6-fold in small passerines and by almost 4.1-fold in large passerines. In non-passerines, both large and small birds increase the share of evaporative heat losses within the thermoneutral zone by approximately 2.7 times. At the lower critical temperature Tlc, the share of heat dissipated by evaporation is approximately similar in passerine and non-passerine birds (14-18%) and is the same for large and small birds (the regression slopes practically do not differ from 0). At the upper critical temperature Tuc in non-passerine birds, the regression slopes only slightly differ from 0, while in passerines it is much higher. It is much more difficult for large passerine birds to maintain their heat balance at high ambient temperatures (Figs. 5, 6).

DISCUSSION

This paper presents a stoichiometric approach to the calculation of total evaporative water loss in Passeriformes and Non-Passeriformes. Body mass loss of a bird in the post-absorptive state at а constant relative humidity is primarily determined by water evaporation (Lasiewski et al. 1966a b; Dawson 1982). Comparison of the data obtained in this study with previously published data in the literature is shown in gure 3. A major advantage of the present method for determining TEWL at low ambient temperatures is that condensation or freezing of water vapor does not affect the accuracy of the resulting estimates in contrast to estimates based on measurements of humidity, dew point, or water vapor pressure. This method eliminates error caused by different gradients of water absorption at various temperatures and the differеnсе between the density of saturating vapor and the actual density of vapor fed into the system from the surfaces of respiratory organs and skin. The experiments were performed at а constant relative humidity; we did not use dry air because it would stimulate evaporation. In traditional methods, as a rule, dry air is used. Also, there was no conflict between the theoretical oxidation constants of the substrates when q was measured over а long period because the birds were in the post absorptive state throughout the experiment. The measurements were performed in seasons in which the bird did not reproduce; therefore, birds did not transform the energy-rich compounds within their bodies and did not absorb water from the environment. The birds only expended the substrates ingested with foods (lipids, carbohydrates, and proteins) and transformed them within their bodies.

Thus, the stoichiometric approach provides adequate data for TEWL compared with conventional methods. The initial postulates remain the same as in the work of Lasiewski et al. (1966b), but we now include the energy expenditures of birds. The relationship between TEWL and the body mass for birds in the study of Williams (1996) (n = 102) at TA = 25°C gives the slope of the regression line equal to 0.68. A slope of 0.70 was found for all birds-combining the data of Williams with our own (n = 102 + 157 = 259) at TA = 25°C. Separating data into groups (non-passerines and passerines) increases the exponent in the equations for TEWL similar to what happens with the basal metabolic rate (Lasiewski and Dawson 1967; McNab 2009 2016; Gavrilov 2014). There are differences between Passeriformes and Non-Passeriformes at TA = 25°C, TA = 0°C, TA = Tlc, and TA = Tuc.

The dependencies of TEWL on body mass in Passeriformes and Non-Passeriformes were analyzed concerning the differences in the BMR levels of these two groups (Table 1). The dependencies of the evaporative water loss on body mass at various TA (0°C, 25°C, Tlc, and Tuc) are statistically significant for both the slope and y-intercept for passerine and non-passerine birds, as were the ratios between evaporative and non-evaporative heat dissipation (Fig. 2). The dependences of the basal metabolic rate on body mass for all birds at various thermoneutral ambient temperatures Tlc, 25°C and Tuc are the same: BMR (kJ/day) = 3.48m0.652 (McNab 2009). When the distinction between passerines and non-passerines is taken into account, the BMR McNab obtained was (kJ/day) = 2.14m0.724 for non-passerines and (kJ/day) = 3.12m0.713 for passerines. Whether or not the difference in BMR between passerines and other birds is due to “phylogeny” their mass- independent basal rates are different (McNab 2009 2016). In Passeriformes, only at Tlc did the evaporative water loss increase in parallel with the metabolic rate; at Tuc, the larger birds dissipated more heat by evaporation than the smaller birds. The slopes of the regression lines for TEWL increased for passerine birds, reflecting increasing difficulties in maintaining heat balance in large-bodied birds at high TA. The calculations performed using these equations gave the following exponents: 0.68-0.71 at TA = 0°C; 0.71- 0.74 at TA = Tlc; 0.73-0.78 at TA = Tuc (Table 1). These data indicate that the mass exponents for BMR and TEWL are approximately equal at Tlc but differ at other temperatures. At higher and lower temperatures, evaporative heat loss increases with body size more rapidly than metabolic rate does.

The percentage of heat dissipated by water evaporation also depends on body size (Figs. 5, 6). At Tlc, it was equal to 14-18% in birds of various sizes. Experiments showed that the evaporative heat loss accounts for approximately 40-60% of the heat produced by BMR at TA = Tuc. This fraction increased slightly with body size (m0.007) in passerines and showed virtually no increase in non-passerines. The water loss increased with body size (m0.17) in passerines because of forced evaporative heat loss. In non-passerine birds, there were nearly equal increases in evaporative water loss and metabolic rate: m0.73 in summer and m0.69 in winter, suggesting that birds from this group maintained the heat balance even at Tuc.

Several studies showed that levels of energy expenditure and water loss in birds vary with the overall phenotypic variation, the sum of inter- and intra-individual environment (Klaassen 1995; Wikelski et al. 2003; Tieleman et al. 2003). Variations in BMR and TEWL are caused by inter- individual interactions (Lessells and Boag 1987) and season (Weathers and Sullivan 1993; Webster and Weathers 2000). Here we have shown that at all ambient temperatures passerine birds have to consume significantly more water to maintain their heat balance than non-passerine birds.

The high basal metabolic rate in Passe- riformes involves benefits like a higher maximum metabolic power and the ability to breed at lower ambient temperatures (Gavrilov 2014), but it comes with a cost: a significant expenditure of evaporative water. The dependence of water loss on body mass at different TA illustrates this cost. These dependencies at TA = 0°C, Tlc, and Tuc vary in the same way as the relationships between the evaporative and non-evaporative heat losses (Gavrilov 1995 2014). Total amount of water evaporated in the thermoneutral zone (at Tlc or Tuc) was considerably greater in passerines than in non-passerines (by approximately 40-60%). This is consistent with the differences in BMR at Tlc between the two groups. Thus, a high expenditure of evaporative water represents the cost of a high BMR. In spite of the fact that a high BMR may significantly increases ecological opportunities of a species, this way of expanding ecological niches is possible only in the small size class.

Fig. 4.

Fig. 4.

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Fig. 4. (A) total evaporative water loss (TEWL) at TA = 0°C as function of body mass in Passeriformes and Non-Passeriformes (this study). (B) total evaporative water loss (TEWL) at TA TA = Tlc as function of body mass in Passeriformes and Non-Passeriformes (this study). (C) total evaporative water loss (TEWL) at TA TA = Tuc as function of body mass Passeriformes and Non-Passeriformes (this study).

Fig. 5.

Fig. 5.

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Fig. 5. Total evaporative water loss (TEWL) and share of heat dissipated by evaporation (%He) in non-Passeriformes at TA TA = Tlc and at TA TA = Tuc as function of body mass.

Fig. 6.

Fig. 6.

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Fig. 6. Total evaporative water loss (TEWL) and share of heat dissipated by evaporation (%He) in Passeriformes at TA TA = Tlc and at TA TA = Tuc as function of body mass.

CONCLUSIONS

We showed that the stoichiometric approach to estimating TEWL yields adequate results for TEWL in comparison to conventional methods. The equations obtained give similar values of evaporative water losses within the range of actually existing body sizes determined by the above-described equations (Crawford and Lasiewski 1968; Williams 1996).

The BMR and TEWL are two fundamental parameters of energetics that determine the level of physiological organization in the animal. BMR and TEWL are dependent on the architecture of circulatory and respiratory systems and on plumage insulation (Gavrilov 2012a b). TEWL is more applicable as a characteristic at the taxonomic level. It is thermal conduction that determines ecological adaptation of species to humid environments. Thus, TEWL and BMR are integrated parameters of the system that involve the assimilation of oxygen and maintenance of constant body temperature. We showed that Passeriformes need to expend more water than Non-Passeriformes because they have higher level of basal metabolic rate: by 50% at 25°C, 30% at 0°C, 39% at the lower critical temperature, and 59% at the upper critical temperature.

High BMR requires considerable amounts of water for evaporation to maintain a heat balance at high ambient temperatures. This requirement imposes strong limitations on the range of sizes in this group (Gavrilov 1997 2014 2015).

Supplementary materials

Appendix 1.

Thermoregulation energetics at rest at night, energetic equivalent of loss body mass at rest (q, kJ/g upon TA) and total evaporative water loss (TEWL, g/day) at different ambient temperatures in non-Passeriformes and Passeriformes in different seasons. (download)

Acknowledgments

Acknowledgments: I am grateful to the researchers of the Department of Vertebrate Zoology and its head, L.P. Korzun, for the opportunity to perform research and for assistance and helpful discussions. I would like to thank A.I. Shilov for help with the drawings and A.V. Bushuev for assistance with the statistical calculations. I would also like to thank the Russian Foundation for Basic Research for long-term support of my research. I thank T.B. Golubeva for support and patient help with my studies. The author is also grateful is to Benny Kwok Kan Chan and anonymous reviewers for valuable criticism, which allowed the manuscript improve considerably.

Footnotes

Authors’ contributions: VMG designed the study and wrote the manuscript.

Competing interests: VMG declares he has no con ict of interest.

Availability of data and materials: Materials are deposited in collections of several research institutions, database are presented in Appendix 1 in manuscript.

Consent for publication: Not applicable.

Ethics approval consent to participate: Not applicable.

References

  1. Arieli Y, Peltonen L, Ophir E. Cooling by cutaneous water evaporation in the heat-acclimated rock pigeon (Columba livia) Comp Biochem Physiol. 131:497–504. doi: 10.1016/s1095-6433(01)00502-5. [DOI] [PubMed] [Google Scholar]
  2. Bernstein M H. Cutaneous and respiratory evaporation in the painted quail, Excalfactoria chinensis, during ontogeny of thermoregulation. Comp Biochem Physiol. 38:611–617. doi: 10.1016/0300-9629(71)90128-9. [DOI] [PubMed] [Google Scholar]
  3. Clark C J, Dudley R. Flight costs of long, sexually selected tails in hummingbirds. Proc R Soc Lond B. 276:2109–2115. doi: 10.1098/rspb.2009.0090. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Clark C J, Dudley R. Hovering and forward flight energetics in Anna's and Allen's Hummingbirds. Physiol Biochem Zool. 83:654–662. doi: 10.1086/653477. [DOI] [PubMed] [Google Scholar]
  5. Lasiewski R C. Oxygen consumption and respiratory evaporation of the Emu and Rhea. Condor. 70:333–339. [Google Scholar]
  6. Dawson W R. Evaporative losses of water by birds. Comp Biochem Physiol A. 71:495–509. doi: 10.1016/0300-9629(82)90198-0. [DOI] [PubMed] [Google Scholar]
  7. Denardo D F, Zubal T E, Hoffman Tcm. Cloacal evaporative cooling: a previously undescribed means of increasing evaporative water loss at higher temperatures in a desert ectotherm, the Gila monster Heloderma suspectum. J Exp Biol. 207:945–953. doi: 10.1242/jeb.00861. [DOI] [PubMed] [Google Scholar]
  8. Depocas F, Hart J S. Use of the Pauling oxygen analyzer for measurement of animals in open circuit systems and in a short-lag, closed-circuit apparatus. J App Physiol. 10:338–392. doi: 10.1152/jappl.1957.10.3.388. [DOI] [PubMed] [Google Scholar]
  9. Dolnik V R, Gavrilov V M. Caloric equivalent of body weight variations in chaffinch Pages 273-287 in Bird Migration: Ecological and Physiological Factors. New York): Wiley; 1973. [Google Scholar]
  10. Dolnik V R, Gavrilov V M. Bioenergetics of molt in the chaffinch (Fringilla coelebs) Auk. 2:253–264. [Google Scholar]
  11. Garai J. Physical model for vaporization. Fluid Phase Equilibria. 283:89–97. [Google Scholar]
  12. Gavrilov V M. Evaporative water loss in the class of birds: method of measurement and allometric dependencies at various ambient temperatures in passerine and nonpasserine birds. Doklady Biological Sciences. 345:621–626. [Google Scholar]
  13. Gavrilov V M. Energetics and Avian Behavior. Harwood; 1997. 11 [Google Scholar]
  14. Gavrilov V M. Fundamental energetics of birds: 1. The maximum ability of birds to change their thermal conductance and the efficiency of metabolic energy transformation into mechanical work. Biology Bulletin. 39:569–578. [Google Scholar]
  15. Gavrilov V M. Ecological and scaling analysis of the energy expenditure of rest, activity, flight, and evaporative water loss in Passeriformes and Non-Passeriformes in relation to seasonal migrations and to the occupation of boreal stations in high and moderate latitudes. Quarterly Review of Biology. 89:25–69. doi: 10.1086/676046. [DOI] [PubMed] [Google Scholar]
  16. Gavrilov V M. The stoichiometric approach in determining total evaporative water loss and the relationship between evaporative and non-evaporative heat loss in two resting bird species: passerine and non-passerine. Avian research; 2015. 6 [Google Scholar]
  17. Gavrilov V M. Fundamental avian energetics: 2. The ability of birds to change heat loss and explanation of the mass exponent for basal metabolism in homeothermic animals. Biology Bulletin. 39:659–671. [Google Scholar]
  18. Gavrilov V M, Dolnik V R. Basal metabolic rate, thermoregulation and existence energy in birds: world data. Pages in 421-466 Acta XVIII Congress Internationalis Ornithologici. Moscow (Russia): Nauka; 1985. [Google Scholar]
  19. Gavrilov V V, Veselovskaya E O, Gavrilov V M, Mya Goretskaya, Morgunova G V. Diurnal Rhythms of Locomotor Activity, Changes in Body Mass and Fat Reserves, Standard Metabolic Rate, and Respiratory Quotient in the Free-Living Coal Tit (Parus ater) in the Autumn-Winter Period. Biology Bulletin. 40:678–683. [Google Scholar]
  20. Hoffman Tcm, Walsberg G E. Inhibiting ventilatory evaporation produces adaptive increase in cutaneous evaporation in mourning doves, Zenaida macroura. J Exp Biol. 202:3021–3028. doi: 10.1242/jeb.202.21.3021. [DOI] [PubMed] [Google Scholar]
  21. Hoffman Tcm, Walsber G E, Denardo D F. Cloacal evaporation: an important and previously undescribed mechanism for avian thermoregulation. J Exp Biol. 210:741–749. doi: 10.1242/jeb.02705. [DOI] [PubMed] [Google Scholar]
  22. Klaassen M. Molt and basal metabolic costs in males of 2 subspecies of stonechats-the European Saxicola torquata rubicola and the East African Saxicola torquata axillaris. Oecologia. 104:424–432. doi: 10.1007/BF00341339. [DOI] [PubMed] [Google Scholar]
  23. Lasiewski R C, Acosta A L, Bernstein M H. Evaporative water loss in birds. I. Characteristics of the open flow method of determination and their relation to estimates of thermoregulatory ability. Comp Biochem Physiol. 19:445–457. [Google Scholar]
  24. Lasiewski R C, Acosta A L, Bernstein M H. Evaporative water loss in birds. II-A modified method for determination by direct weighing. Comp Biochem Physiol. 19:459–506. [Google Scholar]
  25. Lasiewski Rc Bernstein M H, Ohmart R D. Cutaneous water loss in the road-runner and poor-will. Condor. 73:470–472. [Google Scholar]
  26. Lasiewski R C, Dawson W R. A re-examination of the relation between standard metabolic rate and body weight in birds. Condor. 69:13–23. [Google Scholar]
  27. Lessells C M, Boag P T. Unrepeatable repeatabilities-a common mistake. Auk. 104:116–121. [Google Scholar]
  28. Marder J, Ben-Asher J. Cutaneous water evaporation I. Its significance in heat-stressed birds. Comp Biochem Physiol. 75:425–431. doi: 10.1016/0300-9629(83)90105-6. [DOI] [PubMed] [Google Scholar]
  29. Marder J, Gavrieli-Levin I. The heat-acclimated pigeon: an ideal physiological model for a desert bird. J Appl Physiol. 62:952–958. doi: 10.1152/jappl.1987.62.3.952. [DOI] [PubMed] [Google Scholar]
  30. Marder J, Arieli Y, Ben-Asher J. Defense strategies against environmental heat stress in birds. Is J Zool. 36:61–75. [Google Scholar]
  31. Mckechnie A E, Wolf B O. Partitioning of evaporative water loss in white-winged doves: plasticity in response to short-term thermal acclimation. J Exp Biol. 207:203–210. doi: 10.1242/jeb.00757. [DOI] [PubMed] [Google Scholar]
  32. Mcnab B K. Ecological factors affect the level and scaling of avian BMR. Comp Biochem Physiol. 152:22–45. doi: 10.1016/j.cbpa.2008.08.021. [DOI] [PubMed] [Google Scholar]
  33. Mcnab B K. Avian energetics: The passerine/nonpasserine dichotomy. Comp Biochem Physiol. 191:152–155. doi: 10.1016/j.cbpa.2015.10.005. [DOI] [PubMed] [Google Scholar]
  34. Ophir E, Arieli Y, Marder J, Horowitz M. Cutaneous blood flow in the pigeon Columba livia: its possible relevance to cutaneous water evaporation. J Exp Biol. 205:2627–2636. doi: 10.1242/jeb.205.17.2627. [DOI] [PubMed] [Google Scholar]
  35. Prosser C L. Comparative Animal Physiology (Prosser, C.L., ed.) Philadelphia: W.B. Saunders. 1991.
  36. Development Core R. R: A language and environment for statistical computing. Vienna, Austria): R Foundation for Statistical Computing; 2014. [Google Scholar]
  37. Rodríguez S, Barba E. Nestling growth is impaired by heat stress: An experimental study in a Mediterranean great tit population. Zool Stud; 2016. 55. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Schmidt-Nielsen K. Animal physiology: adaptation and environment. New York): Cambridge University Press; 1997. [Google Scholar]
  39. Tieleman B I, Dijkstra T H, Lasky J R, Mauck R A, Visser G H, Williams J B. Physiological and behavioural correlates of life-history variation: a comparison between tropical and temperate zone House Wrens. Funct Ecol. 20:491–499. [Google Scholar]
  40. Tieleman B I, Williams J B, Bloomer P. Adaptation of metabolism and evaporative water loss along an aridity gradient. Proc R Soc Lond. 270:207–214. doi: 10.1098/rspb.2002.2205. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Versteegh M A, Helm B, Dingemanse N, Tieleman B I. Repeatability and individual correlates of basal metabolic rate and total evaporative water loss in birds: A case study in European stonechats. Comp Biochem Physiol. 150:452–457. doi: 10.1016/j.cbpa.2008.05.006. [DOI] [PubMed] [Google Scholar]
  42. Walther B A, Chen Jrj, Lin H S, Sun Y H. The Effects of Rainfall, Temperature, and Wind on a Community of Montane Birds in Shei-Pa National Park. Taiwan. Zool Stud; 2017. 56. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Weathers W W, Sullivan K A. Seasonal patterns of time and energy allocation by birds. Physiol Zool. 66:511–536. [Google Scholar]
  44. Webster M D, Bernstein M H. Ventilated capsule measurements of cutaneous evaporation in mourning doves. Condor. 89:863–868. [Google Scholar]
  45. Webster M D, King J R. Temperature and humidity dynamics of cutaneous and respiratory evaporation in pigeons, Columba livia. J Comp Physiol. 157:253–260. doi: 10.1007/BF00692370. [DOI] [PubMed] [Google Scholar]
  46. Webster M D, Weathers W W. Seasonal changes in energy and water use by verdins, Auriparus flaviceps. J Exp Biol. 203:3333–3344. doi: 10.1242/jeb.203.21.3333. [DOI] [PubMed] [Google Scholar]
  47. Wikelski M, Spinney L, Schelsky W, Scheuerlein A, Gwinner E. Slow pace of life in tropical sedentary birds: a common-garden experiment on four stonechat populations from different latitudes. Proc R Soc Lond. 270:2383–2388. doi: 10.1098/rspb.2003.2500. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Williams J B. A phylogenetic perspective of evaporative water loss in birds. Auk. 113:457–472. [Google Scholar]
  49. Williams J B, Tieleman B I. Ecological and evolutionary physiology of desert birds. Integ Comp Biol. 42:68–75. doi: 10.1093/icb/42.1.68. [DOI] [PubMed] [Google Scholar]
  50. Withers P C, Williams J B. Metabolic and respiratory physiology of an arid-adapted Australian bird, the Spinifex pigeon. Condor. 92:961–969. [Google Scholar]
  51. Wolf B O, Walsberg G E. Respiratory and Cutaneous Evaporative Water Loss at High Environmental Temperatures in a Small Bird. J Exp Biol. 199:451–457. doi: 10.1242/jeb.199.2.451. [DOI] [PubMed] [Google Scholar]

Associated Data

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Supplementary Materials

Appendix 1.

Thermoregulation energetics at rest at night, energetic equivalent of loss body mass at rest (q, kJ/g upon TA) and total evaporative water loss (TEWL, g/day) at different ambient temperatures in non-Passeriformes and Passeriformes in different seasons. (download)

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