Adaptive Thermophysiological Adjustments of Gazelles to Survive Hot Summer Conditions.
Abstract This study was conducted to identify the adaptive thermophysiological adjustments of 24 gazelles (15 - 20 kg and 3 - 4 years old) belonging to 2 gazelle species (Gazella gazelles and Gazella leptoceros) for 3 months during both summer and winter seasons.
The obtained results indicated that gazelles were exposed to heat stress during the summer season, based on the findings that calculated average temperature-humidity index (THI) prevailed during summer season surpass the THI threshold above which most animals enter a state of severe heat stress.
Under these supra-neutral conditions, gazelles of both species had manifested noticeable (PLess than0.05) changes in their thermophysiological responses as demonstrated by pronounced elevations in rectal and skin temperatures as well as marked reductions in internal, external, and total body thermal gradients compared to the winter season.
Notably, the use of body heterothermy by gazelles resulted in heat storage of 109.65 and 31.92 kJ/day/animal in summer and winter, respectively.
Dissipation of these amounts of heat by insensible evaporative avenue would require 45.61 and
13.82 ml H2O/day/animal in summer and winter, respectively. Furthermore, exposure of gazelles to hot environmental conditions during the summer season elicited marked (PLess than0.05) alterations in blood haematological and biochemical parameters as revealed by the reduced (PLess than0.05) erythrocytic indices, total protein and globulin concentrations as well as the elevated (PLess than0.05) heterophil/lymphocyte ratio, serum albumin, glucose and haptoglobin concentrations compared to the winter season.
These findings collectively prove that gazelles can apply remarkable adaptive thermophysiological adjustments in order to survive the harsh bioclimate at their habitats.
Key words: Adaptation, gazelle, heterothermy, thermal gradients, thermoregulation
Most climatologists agree that the ongoing aridification and global warming constitute the major factors that possess a clear and notable danger to the abundance and distribution of wildlife animal's worldwide (Johnson, 1997; Thompson,
2010; Chowdhury and Al-Zahrani, 2013).
Therefore, these animals are expected to adjust their body physiology (either by short-term acclimation through functional changes or by long-term evolutionary shifts in their phenotype through natural selection) as well as to alter their behaviour patterns in order to survive (Chown et al., 2010; Qiao et al., 2011; Renaudeau et al., 2012).
Extended periods of high temperature and drought that extend for more than seven months with erratic precipitation and presence of low- quality forages clearly describe the bioclimatic
conditions of any arid environment such as the Arabian Peninsula. Camels, goats, and gazelles are the most suitable desert animals that live in such habitats.
Although thermophysiological mechanisms that enabled camels and goats to cope with this harsh bioclimate are well documented (Alamer,
2006; Abdoun et al., 2012; Samara et al., 2012),
comparably little is known about the ecophysiology of gazelles.
These animals, as homeotherms, demand to maintain a state of body thermal homeokinesis within a specific range of ambient temperatures; the thermo-neutral zone (Robertshaw,
Exposure of gazelles to supra-neutral conditions is therefore expected to force these animals to reduce their water expenditure and thermogenic mechanisms as well as to recruit their water conservation and thermolytic mechanisms (Al-Johany et al., 1998; Williams et al., 2001; Ostrowski et al., 2003, 2006; Hetem et al., 2012).
Subsequently, noticeable changes would thereby be observed in their body temperature and biophysiological responses. Failure to do so, however, can result in severe body hyperthermia, denaturation of body protein, loss of organ functions, and eventually the death of animals (Renaudeau et al., 2012).
The present study was designed with the aim to determine the effect of seasonal variation on some thermophysiological responses of two gazelle species (Idmi, Gazella gazelles; and Rhim, Gazella leptoceros) normally inhabiting the Arabian Peninsula. A study dealing with this aspect may very well show some of their remarkable adaptive thermoregulatory mechanisms applied to endure such harsh bioclimate.
MATERIALS AND METHODS
Animals and management
Twenty four healthy gazelles of different
genders belonging to Idmi (Gazella gazelles) and Rhim (Gazella leptoceros) species with an average live body weight of 15 - 20 kg and age of 3 - 4 years were used in this study during both summer and winter seasons. In each season, the study was conducted for 3 months comprising of preliminary and experimental periods.
The preliminary period lasted for three weeks and served as an acclimation period during which animals were allowed to adapt to study conditions. On the other hand, climatic data, thermophysiological measurements, and blood samples were collected weekly during the experimental period.
Throughout the study all animals were kept under semi-free environment similar to their natural habitat at the King Khalid Wildlife Research Centre, Riyadh, Saudi Arabia. They were fed on alfalfa hay ad libitum, and had free access to clean tap water. We did not observe any apparent discomfort during handling the animals. Study design was approved by the Faculty Research Ethics Committee at the King Saud University.
Ambient temperature (Ta) and relative humidity (RH) were obtained from the Presidency of Metrology and Environment (PME), Riyadh, Saudi Arabia. To estimate the environmental
severity on the animals, both collected Ta and RH data were used to calculate temperature-humidity index (THI) using the following formula adopted from Kelly and Bond (1971): [THI = Ta [?] (0.55 [?]
0.55 x RH) x (Ta [?] 58)], where Ta is the ambient temperature in oF, and RH is the relative humidity as a fraction of the unit.
On the other hand, rectal (Tr) and skin (Tsk) temperatures were measured at middle of the day (12:00-13:00). A calibrated digital rectal thermometer measure to the nearest 0.10 oC was used to determine Tr, while an infrared thermometer (Traceable Mini IR(tm) Thermometer,
Friendswood, Texas, USA) was used to measure Tsk at 4 shaved regions.
According to Richards (1973), the following formulas: [Tr-Tsk], [Tsk-Ta], and [Tr- Ta] were employed thereafter to estimate the internal (physiological), the external (physical), and the total thermal gradients, respectively.
Blood samples (approximately 10 ml) were collected weekly from all animals via jugular venipuncture into EDTA tubes (for hematological analysis) and plain tubes (for serological analysis).
Collected samples were placed inside an ice box and immediately transferred to the laboratory for analysis.
Within 1 h after collection, a complete heamogram of whole blood was performed using the coulter counter (Coulter Electronics, Luton, Bedfordshire, UK), while sera were separated by centrifugation of plain tubes at 1500 g for 10 min, and then stored at -20oC until analysis.
The colorimetric method was applied to spectrophotometrically quantify serum total protein (g/dL), albumin (g/dL), glucose (mg/dL) and haptoglobin (mg/dL) concentrations using commercial kits (United Diagnostics Industry, Dammam, KSA). Serum globulin (g/dL) concentration was calculated as the difference between measured total protein and albumin concentrations.
The obtained data were analyzed as a full factorial design in three factors (season, species, and gender) each at two levels using the PROC FACTEX procedure of statistical analysis system (SAS Inst., Inc., Cary, NC). Data were subjected to ANOVA using alpha = 0.05.
Means showing significant differences in ANOVA were tested using the PDIFF option. The probability value denoting statistical significance was PLess than0.05. Unless otherwise indicated, means and their pooled SEM are presented.
The obtained data showed that gazelles were exposed to a higher (PLess than0.05) Ta and a lower (P
Less than0.05) RH during summer season compared to
winter season (Table I).
To incorporate the effects
of both Ta and RH, THI is commonly used to quantify the degree of heat stress on animals (Bohmanova et al., 2007; Vitali et al., 2009). In the present study, the THI pattern mirrored the Ta pattern. Calculated average THI values prevailed during the winter season ranged from 55 - 63 with an average of 58.57+-1.09, while higher (PLess than0.05) THI values were observed during the summer season that ranged from 76 - 80 with an average of
77.86+-0.39 (Table I).
Table I.- Bioclimatic measurements throughout the study.
Mean +- SE 14.98+-0.99 35.41 +- 0.54 Less than0.0001
Range 12.1018.70 33.30 38.20
Mean 44.67+-5.04 13.38 +- 0.98 Less than0.0001
Range 29.0064.10 10.10 19.00
Mean 58.57+-1.09 77.86+- 0.39 Less than0.0001
Range 54.6062.70 75.80 80.10
No differences (PGreater than0.05) were generally observed in the measured parameters as influenced by the species (Idmi vs. Rhim) and gender (Male vs. female) factors; thus, data were averaged and jointly analyzed and presented.
Exposure of gazelles to hot summer conditions resulted in pronounced (PLess than0.05) elevations of their overall means of Tr by 1.20+-0.20oC and Tsk by 10.80+-0.60oC compared to the winter season (Fig. 1).
Additionally, body thermal gradients had exhibited noticeable (PLess than0.05) seasonal alterations. Under the summer condition, gazelles showed marked reductions (PLess than0.05) in internal [Tr-Tsk], external [Tsk-Ta], as well as total [Tr-Ta] thermal gradients compared to the winter condition (Fig. 2).
As presented in Table II, exposure of gazelles to hot environmental conditions during the summer season elicited clear (PLess than0.05) reductions in red blood cells count (RBCs), mean corpuscular haemoglobin content (MCH), haemoglobin concentration (Hb), and mean corpuscular haemoglobin concentration (MCHC) compared to the winter season.
Meanwhile, mean corpuscular volume (MCV), total leucocytes (WBCs) count, and heterophil/lymphocyte (H/L) ratio were all exhibited increases (PLess than0.05) during the summer season compared to the winter season.
However, no seasonal influence (PGreater than0.05) was observed on the packed cell volume (Table II).
Table II.- Changes of blood haematological indices of gazelles during winter and summer seasons
Parameters1 SEM P value
RBCs (106/L) 11.89 10.71 0.09 Less than0.0001
WBCs (103/L) 5.18 7.77 0.29 Less than0.0001
PCV (%) 48.99 48.33 0.37 0.225
Hb (g/dL) 15.13 12.53 0.33 Less than0.0001
MCV (fL) 41.45 45.63 0.43 Less than0.0001
MCH (pg) 12.76 11.79 0.28 0.022
MCHC (%) 30.87 26.10 0.73 Less than0.0001
N/L ratio 2.76 3.68 0.14 Less than0.0001
On the other hand, overall means of serum albumin, glucose and haptoglobin concentrations showed (PGreater than0.05) higher values during the summer season over the winter season (Table III), while serum total protein and globulin concentrations were reduced (PLess than0.05) during the summer season compared to the winter season (Table III).
Table III.- Changes of blood biochemical parameters of gazelles during winter and summer seasons.
Parameters SEM P value
6.93 6.04 0.12 Less than0.0001
Albumin (g/dL) 4.49 5.04 0.06 Less than0.0001
Globulin (g/dL) 2.44 1.00 0.13 Less than0.0001
Glucose (mg/dL) 123.71 157.85 9.56 0.015
0.94 1.03 0.01 Less than0.0001
The bioclimate of Arabian Peninsula during the summer season is characterized by extended periods of high Ta (where it usually reaches 45oC and soil surface temperatures regularly exceed 60oC) with erratic precipitation and brief eruption of forages.
In fact, simulation of the biometeorological changes in Saudi Arabia predict that daily Ta will increase by 3-5oC while rainfall pattern will remains the same by the end of the 21st century (Chowdhury and Al-Zahrani, 2013), which will further accentuate heat stress-related problems in animals.
Because of the recognition that most gazelles inhabiting Saudi Arabia are not migrating, these animals are therefore particularly threatened unless they applies remarkable adaptive thermoregulatory mechanisms in order to survive.
The present study examined the seasonal variations on some thermophysiological responses of two gazelle species (Idmi, Gazella gazelles; and Rhim, Gazella leptoceros) normally inhabiting the Arabian Peninsula.
As expected, the results of the present study indicated that gazelles were under heat stress during the summer season, based on the findings that calculated average THI values prevailed during summer season surpass the THI threshold above which most animals enter a state of severe heat stress (Silanikove, 2000; Marai et al., 2007).
Under such supra-neutral conditions, gazelles are expected to gain heat from the environment and subsequently may challenge their survivability. According to Richards (1973), the internal [Tr-Tsk] and external [Tsk-Ta] body thermal gradients under TNZ conditions drive the heat flux from the body to the environment, while under heat stress conditions heat flows from the external environment to the animal body.
In the present study, it was clearly evident that body thermal gradients of gazelles exhibited noticeable reductions during the summer season compared to the winter season, which attesting that gazelles tried to constrict the thermal gradient between their bodies and the surrounding environment in order to regulate their body temperatures. This came in agreement with our previous reports on camels and goats (Abdoun et al., 2012; Samara et al., 2012; Al-Haidary et al., 2013).
These observations are attributed to the noticeable elevation of gazelles Tsk during the summer season, which in turn is most likely be due to the heat-stress induced vasodilatation of skin capillary bed with the consequent shifting of blood flow to the skin surface (McManus et al., 2009; Schutz et al., 2011).
This adjustment gradually impairs the dissipation of body heat by the sensible means and shifts it to the insensible evaporative avenue which in turn may enhance body water loss (Spiers, 2012). Heterothermy was proposed to be a key thermophysiological adaptation for some ungulate living in arid bioclimate, where body heat is stored during the hot diurnal time, with a consequent rise in body temperature, to reduce insensible evaporative heat loss.
Then, during the cold nocturnal time, the stored heat can be dissipated using sensible means allowing body temperature to fall (Williams et al., 2001; Fuller et al., 2004). Exposure of gazelles to hot summer conditions in the present study resulted in pronounced elevations of their Tr.
In fact, heterothermal characteristic of body heat storage and the corresponding water conservation were estimated for gazelles during both seasons according to Ostrowski et al. (2003). Notably, the use of heterothermy by gazelles resulted in storage of 109.65 and 31.92 kJ/day/animal in summer and winter, respectively. Dissipation of these amounts of heat by the insensible evaporative avenue would require 45.61 and 13.82 ml H2O/day/animal in summer and winter, respectively.
This shows that elevation of gazelles Tr during summer compared to winter season is an important physiological adaptation. Notably, these findings are consistent with previous reports on gazelle as well as other ungulate such as oryx and eland inhabiting the same bioclimatic conditions (Williams et al., 2001; Ostrowski et al., 2003, 2006; Hetem et al., 2012).
On the contrary in other domestic animals, seasonal high Ta are associated with high Tr, which considered as an indicator of disturbance in their homoeothermic status simply because these animals ineffectively enhanced their body heat loss (Herz and Steinhauf, 1978; Joshi and Tripathy, 1991; Wenz et al., 2011; Ganaie et al., 2013).
Therefore, this bears substantial evidence that heterothermy in gazelles during summer season may served as an ideal ecophysiological adjustment to minimize their body water losses.
The observed elevated body temperatures as well as reduced body thermal gradients under summer conditions were associated with noticeable alterations in the blood profile. In the present study, the reduced levels of erythrocyte indices -with the exception of MCV- observed during the summer season may associate with the decreased oxygen demand to meet the reduced energy requirements during hot conditions (Hellgren et al., 1989), which may suggest another adaptive mechanism applied by gazelles during heat acclimation (Patterson et al., 2004).
Additionally, exposure of gazelles to hot summer conditions resulted in serum hyperalbuminemia indicating an adjustable mechanism to maintain blood volume by inducing water movement into the vascular system (More et al., 1980; Alamer, 2006). This finding is quite relevant since albumin is the major extracellular source of thiols.
Thereby, inducing hyperalbuminemia permitted the utilization of albumin as an antioxidant to scavenge reactive oxygen species which may be produced from the exposure to heat stress during summer season (Halliwel, 1998; Ganaie et al., 2013).
Moreover, serum hyperglycaemia was also observed in gazelles kept under summer conditions, which may collectively relate to stress-induced activation of corticosteroid secretion and the consequent stimulation of liver gluconeogenesis and glycogenolysis pathways as well as inhibition of cellular glucose uptake and utilization (Duncan et al., 1994; Marai et al., 2007).
A similar trend was also observed in previous studies on camels (Al- Haidary, 2005) and goats (El-Nouty et al., 1990; Samara et al., 2012). Furthermore, results revealed that both H/L ratio and haptoglobin concentration, as direct indicators of stress (Davis et al., 2008; Adenkola et al., 2009), had exhibited elevations during the summer season compared to the winter season, which implies that gazelles were actually under heat stress conditions during the summer season.
The present study shed some basic lights upon seasonal variations of some thermophysiological adjustments of gazelle normally inhabiting the Arabian Peninsula. These ungulates were proved to be thermally adapted and can endure such harsh bioclimate.
This conclusion was demonstrated by the findings that gazelles, under summer conditions, were able to 1) adjust their body temperatures, 2) express numerous water economy mechanisms, and 3) exhibit noticeable adaptive changes in their blood profile, which collectively may enabled these animals to tolerate their natural environment. Research dealing with
this aspect will improve our understanding of gazelle's welfare under such harsh bioclimatic conditions.
Our deep gratitude and appreciation are extended to King Khalid Wildlife Research Centre, Saudi Arabia, for providing their animals for this study in addition to their continuous help throughout the study. The authors also extend their appreciation to Deanship of Scientific Research at King Saud University for funding the work through the research group project Nr. RGP-VPP-171.
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