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Animal Science Journal (2012)<br />

doi: 10.1111/j.1740-0929.2011.00993.x<br />

ORIGINAL ARTICLE<br />

Regional and circadian variations of sweating<br />

rate and body surface temperature in camels<br />

(Camelus dromedarius)asj_993 1..6<br />

Khalid A. ABDOUN, Emad M. SAMARA, Aly B. OKAB and Ahmed A. AL-HAIDARY<br />

Department of Animal Production, College of Food and Agricultural Sciences, King Saud University, Riyadh,<br />

Kingdom of Saudi Arabia<br />

ABSTRACT<br />

It was the aim of this study to investigate the regional variations in surface temperature and sweating rate and to visualize<br />

body thermal windows responsible for the dissipation of excess body heat in dromedary camels. This study was conducted<br />

on five dromedary camels with mean body weight of 450 20.5 kg and 2 years of age. Sweating rate, skin and body<br />

surface temperature showed significant (P < 0.001) circadian variation together with the variation in ambient temperature.<br />

However, daily mean values of sweating rate, skin and body surface temperature measured on seven regions of the camel<br />

body did not significantly differ. The variation in body surface temperature compared to the variation in skin temperature<br />

was higher in the hump compared to the axillary and flank regions, indicating the significance of camel’s fur in protecting<br />

the skin from daily variation in ambient temperature. Infrared thermography revealed that flank and axillary regions had<br />

lower thermal gradients at higher ambient temperature (T a) and higher thermal gradients at lower T a, which might indicate<br />

the working of flank and axillary regions as thermal windows dissipating heat during the night. Sweating rate showed<br />

moderate correlation to skin and body surface temperatures, which might indicate their working as potential thermal<br />

drivers of sweating in camels.<br />

Key words: camel, infrared thermography, surface temperature, sweating rate, thermal window.<br />

INTRODUCTION<br />

In camels, sweat glands are distributed over nearly the<br />

entire body except the lips, external nares and perianal<br />

region (Lee & Schmidt-Nielsen 1962; Taha & Abdalla<br />

1980). Several studies have shown a regional anatomical<br />

difference in sweat gland density of relative species.<br />

The guanaco showed higher densities of sweat glands<br />

around the shoulder, lower part of the upper limb and<br />

lower flank (Morrison 1966; de Lamo et al. 2001).<br />

However, no difference in distribution or number of<br />

sweat glands was found in samples taken from both<br />

genders of guanaco at different times of the year. It has<br />

been demonstrated that the axillary and flank regions<br />

which are covered with very short and sparse pelage<br />

are potentially more effective in evaporative heat dissipation<br />

in guanaco (Morrison 1966).<br />

The major transport mechanism for controlling heat<br />

loss in camels seems to be the convective mechanism<br />

of cutaneous blood flow (Al-Haidary 2006). Exposure<br />

of camels to high ambient temperature (T a) would lead<br />

to an increase in cutaneous blood flow due to peripheral<br />

vasodilatation. Thereby, blood is shifted all over<br />

camel’s body to create a thermal gradient between the<br />

body and the external environment. Surface temperature<br />

is normally used as a reflex index of body thermal<br />

gradient (Curtis 1983). Local superficial venous circulation<br />

is the main source of surface temperature<br />

(Cameron et al. 2004). Vasomotor tone of peripheral<br />

blood vessels in specialized heat exchanger regions<br />

depends on the surrounding T a (Tattersall et al. 2009;<br />

Weissenbock et al. 2010).<br />

Controlling surface temperature is an important<br />

mechanism in temperature regulation of homeotherms<br />

(Phillips & Heath 1992). The major mechanism<br />

of sensible heat loss is cutaneous vasodilatation<br />

in specialized body regions which serves as a heat<br />

Correspondence: Khalid A. Abdoun, Department of Animal<br />

Production, College of Food and Agriculture Sciences, King<br />

Saud University, PO Box 2460, Riyadh 11451, Kingdom<br />

of Saudi Arabia. (Email: abdounn@yahoo.com; kabdoun@<br />

ksu.edu.sa)<br />

Received 20 June 2011; accepted for publication 26 September<br />

2011.<br />

© 2012 The Authors<br />

Animal Science Journal © 2012 Japanese Society of Animal Science


2 K. A. ABDOUN et al.<br />

exchanger with the environment. Such specialized<br />

regions are characterized by high surface-to-volume<br />

ratio, absence of fur, dense network of blood vessels<br />

and the presence of arteriovenous anastomoses<br />

(Wright 1984; Romanovsky et al. 2002; Mauck et al.<br />

2003). The term ‘thermal window’ has been applied<br />

to describe these regions (Williams 1990; Klir & Heath<br />

1992). Later, the term ‘thermal window’ has referred<br />

to any surface area of the body that is responsible<br />

for efficient heat exchange (Sumbera et al. 2007).<br />

Recently, thermal window has been defined as a<br />

restricted surface area which is visible as a hot spot in<br />

a thermal vision and differs by more than 5 o C from its<br />

adjacent regions (Weissenbock et al. 2010).<br />

The thermal camera is considered a state-of-theart<br />

device. It absorbs infrared radiation and generates<br />

images based on the amount of heat generated rather<br />

than reflected (Eddy et al. 2001; Mazur & Eugeniusz-<br />

Herbut 2006). Infrared thermography (IRT) has been<br />

successfully used to visualize body thermal windows<br />

on animal surfaces (Mauck et al. 2003; Tattersall et al.<br />

2009; Weissenbock et al. 2010). IRT may also have<br />

merit for assessing welfare (Stewart et al. 2005), resulting<br />

from changes in body surface temperature associated<br />

with adaptation to microclimate changes<br />

(Kimmel et al. 1992; Knizkova et al. 1996; 2002).<br />

Exchanging body heat with the surrounding environment<br />

through thermal windows is achieved by<br />

modifying blood flow in these regions via controlling<br />

vasomotor tone (Sumbera et al. 2007). The camel’s<br />

skin has numerous arteriovenous anastomoses which<br />

could facilitate heat dissipation via high cutanoeus<br />

blood flow. However, it is still questionable which<br />

regions of the camel’s body are engaged in dissipation<br />

of excess body heat. Therefore, this study was designed<br />

to investigate the regional variations in surface temperature<br />

and sweating rate and to visualize body<br />

thermal windows responsible for the dissipation of<br />

excess body heat in dromedary camels.<br />

MATERIALS AND METHODS<br />

This study was conducted during the summer season at the<br />

experimental station of the Animal Production Department,<br />

College of Food and Agricultural Sciences, King Saud University,<br />

Riyadh region, Kingdom of Saudi Arabia. Five dromedary<br />

camels of native breed (Majaheem) with mean body<br />

weight of 450 20.5 kg and 2 years of age, were used in this<br />

study. Animals were housed individually in shaded pens, fed<br />

twice a day at 07.00 and 16.00 hours and had free access to<br />

clean tap water.<br />

Ambient temperature (T a), relative humidity (RH), sweating<br />

rate (SR), skin temperature (T skin) and body surface temperatures<br />

(T surface) were measured every 3 h for 2 successive<br />

days. Ambient temperature and RH were recorded continuously<br />

at 10 min intervals using two data loggers (HOBO<br />

Pro Series data logger, Model H08-032-08, ONSET Co.,<br />

Wareham, MA, USA) placed inside the pens. Thereafter,<br />

temperature–humidity index (THI) was calculated according<br />

to LPHSI (1990). Seven body regions (head, neck, shoulder,<br />

axillaries, hump, flank and hip) were shaved and used as<br />

sites for measurements of sweating rate and skin temperature.<br />

Skin temperature was recorded using an infrared thermometer<br />

(Traceable MiniIR Thermometer, Friendswood,<br />

Texas, USA) with an accuracy of 1.0 o C and emissivity<br />

of 0.95. The ratio of distance to the size of the spot being<br />

measured was 1:1. Sweating rate was determined according<br />

to the method proposed by Schleger & Turner (1965) and<br />

modified by Pereira et al. (2010). Different body region<br />

surface temperatures were recorded using a forward-looking<br />

and automatically calibrating infrared camera (VisIR-Ti200<br />

infrared vision camera, Thermoteknix Systems Ltd, Cambridge,<br />

UK) placed perpendicular and approximately 50 cm<br />

from the camels’ surfaces. This camera was equipped with a<br />

25° lens, 1.3 Mpx visible camera, and LCD touch screen, and<br />

had a 7.5–13 mm spectral range, and thermal accuracy of<br />

2°C in addition to thermo-electrically cooling systems.<br />

After capturing, thermograms were stored inside a 250 MB<br />

internal memory, read out and analyzed using a special thermogram<br />

analysis program (TherMonitor, Thermoteknix<br />

Systems). For all thermograms, a rainbow color scheme was<br />

chosen. Thermograms were analyzed by defining areas circumscribed<br />

by hand with the software polygon function. The<br />

software then gave back the average T surface within the defined<br />

areas of the thermograms (Fig. 3).<br />

The collected data were analyzed using Proc GLM; the<br />

general linear models (GLM) procedure for analysis of variance<br />

(ANOVA) of Statistical Analysis System (SAS 2003).<br />

Completely randomized design with eight treatments (time<br />

of the day) and five replicates (animals) was applied for<br />

analysis. Factors that were used in the model included the<br />

influence of study treatment (natural circadian variation of<br />

T a), time of the day, body region, and their respective interactions.<br />

Statistical means were compared using Duncan’s<br />

multiple range test (DMRT). The overall level for statistical<br />

significance was set at P < 0.05. All values are presented<br />

as least square means standard error of the mean<br />

(LSM SE).<br />

RESULTS<br />

The recorded T a and RH during this study showed<br />

significant (P < 0.001) circadian variation with an<br />

average value of 35.40 2.49°C and 10.95 1.99%,<br />

respectively. The calculated average THI (29.50 <br />

1.70) indicated that animals had been exposed to<br />

severe heat stress throughout the study (LPHSI 1990).<br />

Ambient temperature and THI exhibited a circadian<br />

rhythm (Fig. 1) with minimum values recorded early<br />

in the morning (06.00 hour), and then gradually<br />

increased to reach the maximum values at the middle<br />

of the day (12.00–15.00 hours). Meanwhile, overall<br />

mean of RH showed maximum values early in the<br />

morning (06.00 hour) and minimum values at the<br />

middle of the day (12.00–15.00 hours).<br />

The regions of mean sweating rate, skin temperature<br />

and body surface temperature showed significant<br />

(P < 0.001) circadian variation together with the variation<br />

in ambient temperature (Fig. 2). Sweating rate<br />

showed a minimum value at 03.00 hour and a<br />

maximum value at 15.00 hour. Skin and body surface<br />

temperatures were minimum at 06.00 hour and<br />

© 2012 The Authors<br />

Animal Science Journal © 2012 Japanese Society of Animal Science<br />

Animal Science Journal (2012)


CAMEL SWEATING AND BODY SURFACE TEMPERATURE 3<br />

50<br />

40<br />

30<br />

20<br />

10<br />

0<br />

T a ( o C)<br />

RH (%)<br />

THI<br />

0 3 6 9 12 15 18 21 24<br />

Day time (hour)<br />

Figure 1 Circadian rhythm of ambient temperature (T a),<br />

relative humidity (RH) and temperature humidity index<br />

(THI).<br />

(°C)<br />

50<br />

45<br />

40<br />

35<br />

30<br />

25<br />

20<br />

SR (g·m -2·h -1 )<br />

T skin (°C)<br />

T surface (°C)<br />

0 3 6 9 12 15 18 21<br />

Day time (hour)<br />

Figure 2 Circadian variations in skin temperature (T skin),<br />

body surface temperature (T surface) and sweating rate (SR).<br />

160<br />

140<br />

120<br />

100<br />

80<br />

60<br />

40<br />

20<br />

0<br />

(g·m -2·h -1 )<br />

maximum at 15.00 and 12.00 hours, respectively. The<br />

correlation of sweating rate versus skin and body<br />

surface temperatures revealed moderate correlation<br />

with a coefficient of 0.60 and 0.57 (P < 0.001) for skin<br />

and body surface temperatures, respectively.<br />

Daily mean values of sweating rate, skin temperature<br />

and body surface temperature measured on seven<br />

regions of the camel’s body did not differ significantly<br />

(Table 1). However, daily average variation in body<br />

surface temperature (10.01 1.56 o C) was significantly<br />

(P < 0.001) higher than the variation in skin<br />

temperature (2.92 0.37 o C). Circadian variation in<br />

body surface temperature (Fig. 3) was greatest in the<br />

hump region (18.8 o C) and lowest in the axillary and<br />

Table 1 Regional variation in average daily skin<br />

temperature, body surface temperature and sweating rate<br />

Regions SR T skin T surface<br />

(g·m -2·h-1 ) ( o C) ( o C)<br />

Head 82.21 10.49 35.68 0.13 34.38 0.56<br />

Neck 84.98 11.17 35.28 0.19 34.28 0.55<br />

Shoulder 89.50 11.35 35.33 0.22 34.32 0.57<br />

Axillary 83.38 10.89 35.11 0.20 34.74 0.45<br />

Hump 85.08 12.09 35.70 0.31 34.41 1.16<br />

Flank 86.56 11.72 35.50 0.37 35.68 0.41<br />

Hip 83.81 10.15 35.93 0.24 34.99 0.64<br />

SR, sweating rate; T skin, skin temperature; T surface, body surface<br />

temperature.<br />

Table 2 Regional correlation of skin temperature versus<br />

body surface temperature<br />

Region<br />

Correlation<br />

P-value<br />

coefficient<br />

Head 0.35 0.049<br />

Neck 0.55 0.001<br />

Shoulder 0.71 < 0.001<br />

Axillaries 0.51 0.003<br />

Hump 0.85 < 0.001<br />

Flank 0.22 0.238<br />

Hip 0.76 < 0.001<br />

27.5∞C<br />

46.3∞C<br />

33.8∞C<br />

32.2∞C<br />

39.6∞C<br />

39.1∞C<br />

6:00 am (T a = 25.12∞C)<br />

12:00 am (T a = 45.40∞C)<br />

Figure 3<br />

Variation in body surface temperature at different ambient temperatures (T a).<br />

Animal Science Journal (2012)<br />

© 2012 The Authors<br />

Animal Science Journal © 2012 Japanese Society of Animal Science


4 K. A. ABDOUN et al.<br />

10<br />

(a)<br />

10<br />

(b)<br />

5<br />

5<br />

T s<br />

- T a<br />

(°C)<br />

0<br />

-5<br />

T s<br />

- T a (°C)<br />

0<br />

-5<br />

-10<br />

-10<br />

20 25 30 35 40 45 50 20 25 30 35 40 45 50<br />

T a<br />

(°C)<br />

T a (°C)<br />

10 (c)<br />

10<br />

(d)<br />

5<br />

5<br />

T s - T a<br />

(°C)<br />

0<br />

-5<br />

T s<br />

- T a<br />

(°C)<br />

0<br />

-5<br />

-10<br />

-10<br />

20 25 30 35 40 45 50<br />

T a<br />

(°C)<br />

20 25 30 35 40 45 50<br />

T a<br />

(°C)<br />

10 (e)<br />

10 (f)<br />

5<br />

5<br />

T s<br />

- T a<br />

(°C)<br />

0<br />

-5<br />

T s<br />

- T a<br />

(°C)<br />

0<br />

-5<br />

-10<br />

-10<br />

20 25 30 35 40 45 50 20 25 30 35 40 45 50<br />

T a<br />

(°C)<br />

T a<br />

(°C)<br />

10<br />

(g)<br />

10 (h)<br />

5<br />

5<br />

T s<br />

- T a<br />

(°C)<br />

0<br />

-5<br />

T s<br />

- T a<br />

(°C)<br />

0<br />

-5<br />

-10<br />

-10<br />

20 25 30 35 40 45 50<br />

T a<br />

(°C)<br />

20 25 30 35 40 45 50<br />

T a<br />

(°C)<br />

Figure 4 Regional variation in thermal gradient between camel’s body surface and ambient temperatures (a = head,<br />

b = neck, c = shoulder, d = axillary, e = flank, f = hip, g = hump, h = mean).<br />

flank regions (6.9 and 5.8 o C, respectively). However,<br />

daily variation in thermal gradient between camel’s<br />

body surface and the surrounding environment was<br />

lowest in the hump region and highest in the flank<br />

and axillary regions (Fig. 4).<br />

Body surface temperature showed significant correlation<br />

with skin temperature in most of the studied<br />

regions with an average correlation coefficient of 0.69<br />

(P < 0.001). The highest correlation coefficient was<br />

calculated for the hump and hip regions (Table 2).<br />

However, body surface temperature was found to be<br />

higher than skin temperature at high ambient temperatures<br />

and lower than skin temperatures at low<br />

ambient temperatures (Fig. 2).<br />

© 2012 The Authors<br />

Animal Science Journal © 2012 Japanese Society of Animal Science<br />

Animal Science Journal (2012)


CAMEL SWEATING AND BODY SURFACE TEMPERATURE 5<br />

DISCUSSION<br />

This study was designed to investigate the regional<br />

variation in body surface temperature and sweating<br />

rate, in addition to the effect of natural daily circadian<br />

variation of T a on body surface temperature and sweating<br />

rate.<br />

The results of the present study confirmed the existence<br />

of a T a circadian rhythm during the study period<br />

with a minimum T a (25.12 o C) observed early in the<br />

morning and maximum T a (45.4 o C) observed at the<br />

middle of the day, which produced concomitant<br />

changes in body surface and skin temperatures and<br />

sweating rate (Figs 1,2). This could be attributed to the<br />

dependence of vasomotor tone of peripheral blood<br />

vessels and the consequent skin blood flow on the<br />

surrounding T a (Tattersall et al. 2009; Weissenbock<br />

et al. 2010). However, the average daily surface and<br />

skin temperatures and sweating rate did not show<br />

significant regional variation (Table 1), which could be<br />

due to the reported distribution of sweat glands over<br />

nearly all body regions in camels (Taha & Abdalla<br />

1980).<br />

The daily average variation in body T surface was higher<br />

than the variation in T skin, confirming that body T surface<br />

is affected mainly by the variation in T a, while T skin is<br />

regulated by vasomotor control (Curtis 1983). Further,<br />

it has been demonstrated that T skin in the trunk region<br />

of ox does not change very much at different T a<br />

(Whittow 1962). The variation in body T surface (Fig. 3)<br />

compared to T skin was higher in the hump compared to<br />

the axillary and flank regions, indicating the significance<br />

of camel’s fur in protecting the skin from the<br />

daily variation in T a. This study has also discussed<br />

the possible use of body T surface measured by infrared<br />

thermographic technique as a representative of T skin.<br />

Although, body T surface showed significant correlation<br />

with T skin (r = 0.69), the body T surface showed high circadian<br />

variation compared to the relatively stable T skin.<br />

Therefore, body T surface could not be used as a representative<br />

of T skin.<br />

It is still unclear which regions of the camel’s body<br />

function as the main avenues for the dissipation of<br />

excess body heat. Therefore, infrared vision was taken<br />

every 3 h throughout the day, and the daily variation<br />

in thermal gradient between camel body surface and<br />

the surrounding environment was been monitored<br />

during the present study. The thermal vision (Fig. 3)<br />

showed that body surface temperature was higher at<br />

high T a and lower at low T a. However, the variation in<br />

the body T surface was lowest in the flank and axillary<br />

regions. Moreover, variation in thermal gradient was<br />

lowest in the hump region and highest in flank and<br />

axillary regions (Fig. 4). The flank and axillary regions<br />

showed lower thermal gradients at higher T a (during<br />

the day) and higher thermal gradients at lower T a<br />

(during the night), indicating continuous blood flow to<br />

the naked skin in the flank and axillary regions. This<br />

indicates that flank and axillary regions might work as<br />

thermal windows dissipating heat during the night.<br />

This observation supports the previous reports on<br />

guanaco which demonstrated that axillay and flank<br />

regions with very short and sparse pelage are potentially<br />

more effective in heat dissipation (Morrison<br />

1966). Furthermore, this observation confirms the<br />

earlier report that heat gained during the hot day is<br />

dissipated during the cool night as a water economy<br />

mechanism in camels (Lee & Schmidt-Nielsen<br />

1962).<br />

Correlation of sweating rate versus skin and body<br />

surface temperatures revealed moderate correlation<br />

(r = 0.60 and 0.57, respectively). This indicates that<br />

skin and body surface temperature might work as<br />

potential thermal drivers of sweating in camels.<br />

Similar results have been reported for lactating cows<br />

(Berman 1971) and ox (Whittow 1962). However,<br />

thermal modulation of sweating in camels needs<br />

further, more-oriented research.<br />

Conclusion<br />

Skin and body surface temperatures and sweating rate<br />

in dromedary camels showed circadian variation concomitant<br />

to the circadian rhythm of ambient temperature.<br />

However, no regional variation across the camel’s<br />

body was detected for the daily average skin and body<br />

surface temperatures and sweating rate. Thermal gradient<br />

between the surrounding environment and body<br />

surface was lowest at high ambient temperature and<br />

highest at low ambient temperature at the flank and<br />

axillary regions, which indicates the probable working<br />

of these regions as thermal windows dissipating heat<br />

during the night.<br />

ACKNOWLEDGMENTS<br />

This work has been supported by the National Plan for<br />

Science and Technology (NPST) program by King Saud<br />

University, project number 09-BIO 885–02.<br />

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