Introduction

Dromedary camels (Camelus dromedarius) are commonly considered as animals which have successfully adapted to the harsh envi- ronments especially in the Middle East (No- aman, 2018), sub-Saharan Africa (Legesse et al., 2018) and India (Narnaware et al., 2015). Camels are usually reared on poor pastures under extensive production systems and pro- duce high-quality meat and milk. Hence, their rearing and production costs are rela- tively low. Furthermore, camels were large- ly utilized for transportation, while pastoral lifestyle in the tropics was also a remarkable reason of seasonal immigration. Therefore, camel plays a key role for immigrants es- pecially in less-developed areas. In addition to transportation, camels  are considered as  a portable source of food for their owners (Kashongwe et al., 2017). Such situations during many centuries resulted in domesti- cation of an animal with unique endurance that is able to survive in harsh environments (Mohandesan et al., 2017). Furthermore, due to vast deserts and far distances between cit- ies and villages, most of the camel breeds are naturally adapted for long-distance marching with inadequate rest.

In Iran, especially in the south east of the country, camel raising is considered as an important occupation and different breeds of indigenous and exotic one-humped camels have often been reared for their meat, milk and/or wool production. However, during the last decades using camels for transportation has been limited in Iran through facilitated transportation by roads development  even  in deserts, and people’s changing lifestyle. Among different indigenous breeds, “Balou- chi” breed seems to be one of the dual-pur- pose camels which are widely spread over Afghanistan and Pakistan and south-east Iran

(Salehi and Gharahdaghi, 2013). This breed is generally known for its moderate hump, good marching ability and appropriate meat and milk production. Actually, Balouchi camels move steadily over long distances. Besides Balouchi breeds, almost all of the dromedary camel breeds in Iran have been kept for meat, milk or both, and to a lesser extent, for wool. Nevertheless, a very limited population of dromedary camels in Iran have been selected for short-distance fast-run- ning, so-called racing camels. Iranian racing camels have a relatively lighter weight than other breed types so are not slaughtered for meat. While camel population is decreasing globally, consideration of the racing camels due to their economic importance has be- come more important than before. Recently, considerable attention has been paid to Ira- nian racing camel, “Jammaz” breed, due to their introduction in several annual national and international race competitions. Hence, in the local  market,  Jammaz  breed  is 4 to  6 times more expensive than other breeds. However, this breed makes up a very lim- ited proportion of the national camel popu- lation (Salehi and Gharahdaghi, 2013), and the breed is at risk due to uncontrolled mat- ing with other breeds.

During the last decades, uncontrolled mat- ing has been occurred between different in- digenous and/or exotic one-humped camel breeds in Iran. Over thousands of years, each breed was formed based on its geographical distribution and human needs, hence uncon- trolled mating is not acceptable based on the genetic diversity point of view (Cherifi et al., 2017). Essentially, crossbred camels with un- known genetic make-up and indefinite con- tribution of basic animals is not admissible (Chuluunbat et al., 2014). Uncontrolled mat-

ing also results in difficulties to find out pure breeds. In the case of camels, registration of individuals and pedigree formation under extensive production systems to identify pa- rental lineage may be impossible. As an al- ternative way, while anatomical (body type traits) and physiological (especially blood biochemical parameters) characteristics of each breed seem to be specified, identifica- tion of phenotypic and intrinsic characteris- tics of each breed would be a practical way to ensure breed purity. Accordingly, pure Iranian adult Jammaz and Balouchi breeds were considered to compare their body type traits and blood biochemical parameters as the aim of this study.

Materials and Methods

Animals

This study was conducted following the general ethical guidelines of Animal Care and Use Committee (ACUC), Faculty of Veterinary Medicine, University of Zabol, Zabol, Iran. To support the aim of the cur-  rent study, many camel herds were evaluat- ed based on available historical information of the herds, the local veterinary inspectors’ judgment, experience of vaccination techni- cians, and consultation with the herd owners to identify pure Iranian Jammaz and Balou- chi camel breeds. Eventually, 32 Jammaz

and 42 Balouchi pure breeds were identified at southern Sistan and Baluchistan province in November 2017. Camels were from dif- ferent herds but all of them were reared on low-quality pastures under extensive pro- duction system. Camels were between 6 and 10 years old. None of the camels were preg- nant. Lactating animals were  not  included in the study. Immediately, before body mea- surement and blood sample collection con- ventional veterinary practices were made to ensure the health status of the animals.

Body type traits

In the current study body type traits re- lated to the camel marching/running ability were taken into account. Body measure- ments (cm) were body length (BL), neck length (NL), chest girth (CG), barrel girth (BG), hump circumference (HC), fore limb length (FLL), hind limb length (HLL), height at hump (HH), fore limbs interval (FLI), hind limbs interval (HLI), fore hoof circumference (FHC), hind hoof circum- ference (HHC), abdominal circumference (AC), shank circumference (SC) and leg circumference (LC) which were accord-  ing to definitions described by Legesse et al. (2018). Body type traits (body measurements) description and abbreviations are shown in Table 1. Moreover, descriptive statistics of body type traits are shown in Table 2.

Table 1. Description of body measurements (type traits) and abbreviations

Table 2. Descriptive statistics of body type traits in Iranian Jammaz (rac- ing camel) and Balouchi (dual-purpose camel) breeds (n = 74)

Plasma biochemical parameters

Blood samples (5 ml) were collected from the jugular vein of each individual in vacuum tubes with anticoagulant (EDTA) between 09:00 and 11:00 AM. Animals did not have

physical activity during the 24 h before blood sampling. All blood samples were placed on ice immediately after collection, then transported to the laboratory. Plasma was separated by centrifugation (3000 rpm,

25 min and 8 °C). Collected plasma were frozen at −80 °C until biochemical anal- yses. Plasma concentration of Glucose, blood urea nitrogen (BUN), creatinine, cholesterol, total bilirubin (Bili-T), direct bilirubin (Bili-D), calcium (Ca), phospho- rus (P), magnesium (Mg), aspartate ami- notransferase (AST), creatine kinase (CK), lactate dehydrogenase (LDH), total protein (TP), albumin (Alb), triiodothyronine (T3) and thyroxine (T4) were measured with

commercial biochemical kits (DiaSys Di- agnostic Systems GmbH, Germany) using Selectra proM (ELITech Group, France) autoanalyzer. Globulin (Glo) concentra- tions was calculated through total TP minus Alb concentrations. Then, Alb to Glo ratio (Alb:Glo) calculated through Alb concen- tration was divided by Glo concentration. Descriptive statistics of blood biochemical parameters of camels in the current study are shown in Table 3.

Table 3. Descriptive statistics of blood biochemical parameters in Iranian Jam- maz (racing camel) and Balouchi (dual-purpose camel) breeds (n = 74)

BUN: Blood Urea Nitrogen; Bili-T: Total Bilirubin; Bili-D: Direct Bilirubin; Ca: Calcium; P: Phosphorous; Mg: Magnesium; AST: Aspartate Ami- notransferase; CK: Creatine Kinase; LDH: Lactate Dehydrogenase; TP: Total Protein; Alb: Albumin; Glo: Globulin: Alb:Glo: Albumin to Globulin ratio; T3: Triiodothyronine; T4: Thyroxine

Statistical Analysis

Statistical significance of  differences be- tween body type traits and plasma biochemi- cal parameters of Iranian racing (Jammaz) and dual-purpose (Balouchi) camels was compared through the non-paired Student’s t-test in SAS (SAS Institute Inc., 2008).( P < 0.05) was con- sidered significant.

Results

Body type traits

Comparisons of body type traits of Irani-  an racing (Jammaz breed) and dual-purpose camel (Balouchi breed) are shown in Table 4. In general, it seems that body size of Balouchi breed is greater than Jammaz breed. There- fore, BL in Balouchi breed is almost 5% taller than Jammaz breed, while this difference was

not statistically significant (P < 0.05). About a 5% longer neck in Jammaz breed (105.36 cm) than Balouchi breed (100.93 cm) was sta- tistically significant (P ≥ 0.05). According to the approximately larger feature and es- timated heavier weight of Balouchi cam- els, wider CG in this breed was expected, but this trait between two breeds was not significantly different (P ≥ 0.05). Expect- edly, BG in Balouchi breed was almost 20 cm wider than Jammaz breed (P < 0.05). In spite of developed CG in Jammaz camels, AC in this breed was almost 8% thinner than Balouchi breed (P < 0.05). Compari- son of two breeds for their HC showed no statistically significant differences (103.79 vs. 108.07 for Jammaz and Baluchi breeds, respectively) Table 4.

Table 4. Comparison of body type traits of Iranian Jammaz and Balouchi camels

* Means with different letters are significantly different from each other.

Height of Jammaz camels at hump (HH) was on average only 4.64 cm taller than Ba- louchi breed, though, difference of breeds for this trait was significant (P < 0.05). In addition, FLL and HLL were approximate- ly 5 and 6 cm more in Jammaz breed than Balouchi breed (P < 0.05). Comparisons showed no differences for FLI between two breeds, although HLI in Balouchi breed  was almost 16.5% more than Jammaz breed which obviously indicate bigger AC and probably wider pelvic region in Balouchi breed. In the case of Jammaz camels, FHC and HHC were 5.72 and 5.29 cm smaller than Balouchi breed, respectively, which

were statistically significant (P < 0.05). Shank and leg circumferences (SL and LC, respectively) in Balouchi breed were also thicker than Jammaz breed (19.93 vs. 21.00 cm and 17371 vs. 18. 79 cm, respectively).

Plasma biochemical parameters

Based on Table 5, blood glucose level in Jammaz camels was almost 20% more than in Balouchi breed (96.60 vs. 80.56 mg/100 ml) which was considerably different (P < 0.05). In our study, cholesterol concentra- tion in Jammaz camels (27.53 mg/ 100 ml) was higher than in Balouchi breed (25.67 mg/100 ml), although the differences were not significant (P ≥ 0.05).

Table 5. Comparison of plasma biochemical parameters of Iranian Jammaz and Balouchi camels

.Means with different letters are significantly different from each other*

.Ca: Calcium; P: Phosphorous; Mg: Magnesium**

According to our results, mineral concen- trations between studied breeds did not show statistical significance except for plasma P (P < 0.05), which was higher in Balouchi breed (6.25 mg/100 ml) than in Jammaz

breed (5.57 mg/100 ml). In the current study, plasma level of Ca in Jammaz breed (7.39 mg/100 ml) is higher than in Balouchi breed (7.22 mg/100 ml) but it is not significantly different between two breeds (P ≥ 0.05).

Table 6. Comparison of liver enzymes, nitrogen parameters and plasma proteins of Iranian Jammaz and Balouchi camels

*AST: Aspartate Aminotransferase; CK: Creatine Kinase; LDH: Lactate Dehydrogenase; Bili-T: Total Bilirubin; Bili-D: Direct Bilirubin; BUN: Blood Urea Nitrogen; TP: Total Protein; Alb: Albumin; Glo: Globulin: Alb:Glo: Albumin to Globulin ratio.

**Means with different letters are significantly different from each other.

As shown in Table 6, liver enzymes in Jam- maz breed were higher than Balouchi breed. Nevertheless, while AST (13.58 %) and CK (11.92%) both in Jammaz breed were higher than Balouchi breed, just the difference for LDH was significant (P < 0.05). In fact, plas- ma levels of LDH in Jammaz camels was al- most two times higher than Balouchi breed (1015.40 U/l in Balouchi breed vs. 609.56 U/l in Jammaz breed). Differences in both Bili-T and Bili-D in two breeds in our study were strongly significant (P < 0.05 for Bili-T and Bili-D), while there were no consider- able differences between values in  Balou- chi and Jammaz breeds (0.03 and 0.02 mg/l for Bili-T and Bili-D, respectively). Plas-  ma concentration of BUN and creatinine in Jammaz breed was higher than in Balouchi breed (43.5% and 31%, respectively), which resulted in a statistically significant differ- ence for both parameters (P < 0.05). While plasma levels of Alb in two breeds were very

similar (3.34 vs. 3.38 gr/dl in Jammaz and Balouchi breeds, respectively), however, TP concentration in Balouchi breed was almost 9.87% lower than Jammaz breed. Accord- ingly, Glo concentration in Jammaz breed was also 0.65 gr/dl higher than Balouchi breed (P < 0.05). The lower amounts of Glo concentration in Balouchi breed resulted in higher amount for Alb:Glo in this breed than in Jammaz breed which was strongly signif- icant (P < 0.05) Table 7.

Comparing plasma concentrations of hor- mones (Cortisol, T3, and T4) between Iranian racing and dual-purpose camels (Table 7), all of the values for Jammaz breed were higher than Balouchi breed, while the difference for T3 between two breeds was  not  significant (P ≥ 0.05). For Balouchi breed, cortisol, and T4 concentrations were lower than Jammaz breed, 0.42 and 3.89 ng/ml, respectively, while comparison of T3 concentrations be- tween two breeds was almost equal.

Table 7 Comparison of plasma hormones of Iranian Jammaz and Balouchi camels

.Means with different letters are significantly different from each other*

.T3: Triiodothyronine; T4: Thyroxine**

Discussion

Body type traits

Mean of body lengths in 8 breeds of Ethi- opian camels was calculated as 148.7 cm, while separate BL for each breed was not re- ported (Legesse et al., 2018). Their reports for BL were similar to the BL of Iranian rac- ing and dual-purpose camel breeds, while Iranian camels have slightly longer bodies. Feed quality and quantity in particular at ear- lier stage of life influenced positively on BL (Saini et al., 2014), therefore, shorter body length in Jammaz breed may be due to con- trolled feeding during the  growing  period  of the camels. Camels naturally lower their heads during running, therefore, longer neck in Jammaz camels helps them maintain bal- ance, whereas, neck movements during run- ning result in balanced locomotion. The NL for Ethiopian camels was reported as 106.67 cm (Legesse et al., 2018). No significant dif- ference of CG indicates developed respirato- ry system and larger lungs in Jammaz breed than Balouchi breed. Accordingly, short-dis- tance fast running activity needs rapid res- piration and Jammaz breed is well adapted for this purpose. Since camel weighing is not always possible, some body type traits, espe- cially CG, height at withers and hump girth are usually taken into account for estimation of body weight in camels (Boujenane, 2018). Chest girth measurement of Iranian camels in the current study was lower than that of Legesse et al. (2018), which reported 207 cm for this trait.

Larger size of BG in Balouchi breed is related to both its larger body and its hump size. It should be considered that in Jammaz breed to keep running ability, higher weight is assumed as an unfavorable characteristic. Therefore, Jammaz breed owners usually give limited feed to the camels to control

bodyweight. Consequently, fat and protein storage in hump of Jammaz camels is lim- ited. Legesse et al. (2018) reported 244.89 cm for BG in average on 535 individuals of different Ethiopian camel breeds, which was approximately in the middle of our values for Iranian racing (232.79 cm) and dual-pur- pose (252.71 cm) breeds.

Wider CG and thinner AC in racing ani- mals have also been seen in some breeds of racing dogs such as Greyhound breed. Thin- ner AC in Jammaz camels helps them to run more easily and allows the hind limbs to move effortlessly. Considering HC in stud- ied breeds suggests that Jammaz camels also can initially store substantial amounts of fat while due to the aim of rearing (racing abil- ity) they are fed ad libitum and their HC is more limited. Considering taller FLL and HLL in Jammaz breed, it is concluded that higher HH in this breed is due to its longer limbs. Longer limbs in Jammaz camels help them to jump higher and therefore run faster. Average HLL in Ethiopian camels (148.34 cm) (Legesse et al., 2018) was very similar to Iranian racing camels (148.71 cm) and they are taller than Balouchi breed (142.07 cm). Hoof style plays a key role in running/ marching performance of camels. Moreover, circumference of this organ is associated with the animal’s weight. Smaller FHC and HHC in Jammaz camels is rooted in their evolutionary history. Smaller hoofs result in lesser friction with the ground, which helps them to run faster.

Plasma biochemical parameters

The normal range for plasma glucose in camel is reported as 60–140 mg/100 ml, while except for camels, basal plasma glu- cose in mono-gastric animals is considerably higher than adult ruminants such as sheep (Faye and Bengoumi, 2018). Camels are ru-

minants, therefore fermentation of glucose occurs in their rumen. However, they are ex- ceptional with regard to their carbohydrate metabolism, while plasma glucose levels in camels are in the range of single stomach animals or even higher (Abdel-Fattah et al., 1999). Plasma level of glucose is widely in- fluenced by feeding time, season, age, rut- ting season, physical activity reviewed by (Faye and Bengoumi, 2018). Considering rapid running and needs for available energy sources for muscular function, it seems that higher amounts of blood glucose in Jammaz camels is reasonable. Cholesterol is an essen- tial lipid with structural role (both integrity and fluidity) in cell membranes. Basal plas- ma concentration of cholesterol in camels are very variable (18–150 mg/100 ml), nev- ertheless, plasma cholesterol concentration  in one-humped camels is lower than other animals reviewed by (Faye and Bengoumi, 2018). According to the data of the litera- ture, extremely broad variation in plasma concentration of cholesterol in camels could be because of breed and climate differences which are often not taken into account. Con- sequently, all of the one-humped camels are compared together without considering the effect of breed.

Higher values of P in Balouchi breed than Jammaz breed (12.38%), might to be due to intrinsic characteristics of this breed. The concentration of P in Hijin racing camel was

5.02 mg/100 ml (Mohamed and Hussein, 1999), which was lower than Iranian Balou- chi and Jammaz camels. Normal ranges for Ca, P and Mg in camel for different breeds are reported as 8.4–12.4, 3.8–8.4 and 1.8–2.8 mg/100 ml, respectively (Faye and Bengou- mi, 2018). Therefore, our measurements were in the range of other breeds, except for Mg which were lower in both Jammaz  (1.45

mg/100 ml) and Balouchi (1.50 mg/100 ml) breeds. Like Ca, P is also an essential mac- ro-mineral for animals and occurred and various biological pathways. Plasma levels of Ca, P and Mg are related to multiple fac- tors such as age, ovarian activity, pregnancy stage and even mineral content of feedstuffs available for animals. Ca is proposed as the main macro-mineral in animal body, which plays an essential role in various biological systems. For example, Ca is necessary for muscular contraction.

The AST basal levels in different  breeds of one-humped camels were reported from 37 to 131 U/l (Faye and Bengoumi, 2018). The AST is an index for liver health status, and in the current study, the AST level for both breeds was in the normal range. The enzymatic activity of CK in the muscle fibers is important for the production of energy. Therefore, relatively higher values for CK are expected in Jammaz camels (19.91 U/l) in comparison with Balouchi breed. Lac-  tate dehydrogenase is an enzyme that works mainly in muscles and erythrocytes and cat- alyzes the reversible conversion  of  lactate to pyruvate. Plasma levels of LDH increase after anaerobic catabolism of glucose during intense physical activities such as marathon running (Knechtle and Nikolaidis, 2018). Higher levels for LDH in Jammaz breed obviously reflect the need of this breed to provide pyruvate from lactate after racing. Therefore, according to LDH level, it is sug- gested that Jammaz camels ran faster than other breeds.

In vertebrates, bilirubin is the normal yellow pigment that occurs in the catabolic pathway during breakdown of the red blood cells (Lam et al., 2017). Therefore, this me- tabolite is greatly influenced by the longevity of erythrocytes. According to the review of

Faye and Bengoumi, (2018) basal bilirubin concentrations in different breeds of camels normally range between 0.5 and 8.6 mg/l, which suggests a variety of factors influence on blood bilirubin concentration  (Gao  et  al., 2018; Chen et al., 2018). Measurements for BUN and creatinine were in the normal range, as according to Faye and Bengoumi, (2018) range of BUN and creatinine for dif- ferent breeds of camels are 8–30 mg/100 ml and 0.8–2 mg/100 ml, respectively. During protein digestion and turn over (amino acids catabolism), urea as the main non-protein nitrogen is produced through urea cycle in the kidneys and mainly in the liver. Actually, waste ammonia in the form of urea  carries in the blood and excretes from the animals’ body through urine.  Although  blood  urea  in camels (as a ruminant) returns to rumen through the rumen wall or saliva. It has been demonstrated that urea excretion via urine in camels rarely occures (Schmidt-Nielsen et al., 1957). Specifically, while diet with poor nitrogen content is available, camels have a very efficient mechanism that allows them to reuse blood urea by means of microbial po- tential to protein synthesis (Emmanuel et al., 1976). While, BUN is an indicator of renal or even liver health, some other factors such as diet protein content or increased protein catabolism may influence on BUN concen- tration. According to different sources and variation in BUN, difference between Jam- maz and Balouchi the breeds is not clear, while camels of both  breeds  were  healthy at the time of sampling. Afterward, Jam- maz camels have, to some extent, access to green herbage, Balouchi breed is reared on poor roughage. Therefore, higher content of protein in the Jammaz camels diet could be the reason of this difference. Besides BUN, creatinine is typically considered as a bio-

chemical indicator of kidney function. One- humped camels are usually known for their water resistance, therefore the creatinine dosage is an indicator for the normal kidney function.

The animal dehydration status and feed nitrogen content are the main factors in- fluencing blood total protein (Bouaouda et al., 2014). While Alb and Glo are the main fractions of the blood proteins, factors in- fluencing these two parts directly influence blood protein concentration. For instance, infectious disease results in enhanced plas- ma Glo concentrations. Differences between Glo concentrations in Jammaz and Balouchi breeds may not be due to infection, while health status of the camels was approved before blood sampling. According to Faye and Bengoumi, (2018)  normal  values  of  TP and Glo are 6.3–8.3 gr/100 ml and 2–5 gr/100 ml, respectively. Therefore, our mea- surements did not exceed the standard range. TP concentration in a former report to Irani- an dromedary camel (unknown breed) was

6.8 gr/100 ml (Ghodsian et al., 1978), which was very similar to TP in Jammaz camels (6.79 g/100 ml). The Alb:Glo  ratio  would be a useful parameter to evaluate proportion of plasma protein fractions. In the case of camels, the normal value for this parameter is recommended as 1.03 (Jassim Ram and Shahsavari, 2015).

Cortisol releases in plasma response to stress and/or low blood glucose concen- tration in all of the mammalian species. In camels, different sources of stress result in higher secretion of cortisol, too  (Saeb  et  al., 2010; Sid-Ahmed et al., 2013). Plasma concentrations of cortisol in Jammaz breed was almost 25% higher than Balouchi breed. Higher levels of cortisol lead to immune sys- tem suppression (Philip and Vijayan, 2015).