Relationship between udder morphology traits , alveolar and cisternal milk compartments and machine milking performances of dairy camels ( Camelus dromedarius )

A total of 22 dairy dromedary camels under intensive conditions in late lactation (275 ± 24 days) were used to study the relationship between external and internal udder morphology and machine milking performances. Measurements of udder and teat morphology were obtained immediately before milking and in duplicate. Individual milk yield, lag time and total milking time were recorded during milking, and milk samples were collected and analyzed for milk composition thereafter. Cisternal and alveolar milk volumes and composition were evaluated at 9 h milking interval. Results revealed that dairy camels had well developed udders and milk veins, with medium sized teats. On average, milk yield as well as milk fat and protein contents were 4.80 ± 0.50 L d, 2.61 ± 0.16% and 3.08 ± 0.05%, respectively. The low fat values observed indicated incomplete milk letdown during machine milking. Lag time, and total milking time were 3.0 ± 0.3, and 120.0 ± 8.9s, on average, respectively. Positive correlations (p < 0.05) were observed between milk yield and udder depth (r = 0.37), distance between teats (r = 0.57) and milk vein diameter (r = 0.28), while a negative correlation was found with udder height (r = –0.25, p < 0.05). Cisternal milk accounted for 11% of the total udder milk. Positive correlations were observed between total milk yield and volume of alveolar milk (r = 0.98; p < 0.001) as well as with volume of cisternal milk (r = 0.63, p < 0.05). Despite the low udder milk storage capacity observed in dairy camels, our study concluded that the evaluated dromedary sample had adequate udder morphology for machine milking. Finally, positive relationships were detected between milk yield and udder morphology traits of dairy camels. Additional key words: dromedary camel; milk production; udder traits; cisternal milk; intensive system. * Corresponding author: mayadi@ksu.edu.sa Received: 05-02-13. Accepted: 22-07-13. Abbreviations used: BW (body weight); CMT (California mastitis test); EC (electrical conductivity); LSD (least significant difference); SCC (somatic cell count). Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA) Spanish Journal of Agricultural Research 2013 11(3): 790-797 Available online at www.inia.es/sjar ISSN: 1695-971-X http://dx.doi.org/10.5424/sjar/2013113-4060 eISSN: 2171-9292


Introduction
Dromedary camels (Camelus dromedarius) population in Saudi Arabia is estimated at 830,000 heads (Agriculture Statistical Year Book, 2010) distributed in different parts of the country.Camels are one of the largest terrestrial mammals that inhabit areas where diurnal ambient temperatures exceed that of their body temperatures (Al-Haidary, 2006).Despite the severe conditions confronted in their natural environmental habitat, dairy camels are capable -in comparison to other farm animals-of taking the advantages of the Relationship between udder morphology traits, alveolar and cisternal milk compartments and machine milking performances of dairy camels (Camelus dromedarius) limited resources to produce a daily milk yield ranging between 4 to 18 L per head (Saoud et al., 1988;Gaili et al., 2000;Aljumaah et al., 2011).
Milking management can be regarded as a key step in the milk production chain.Despite the considerable number of studies that have been conducted on milking management of dairy cattle, sheep and goats, little information is available on lactation biology of dairy camels.Hand milking is the predominant milking system in camels.Nevertheless, as a result of the market demand, machine milking have recently been adopted in intensive camel dairy farms for commercial milk production (Wernery et al., 2004;Faye, 2005;Hammadi et al., 2010).
Exploring the external as well as the internal morphology traits of the udder was proven useful for improving milk yield and milking ability in dairy animals (Labussiere, 1988).Zayeed et al. (1991) reported high variations (attributed to several factors such as breed, lactation stage, parity number and disease) in the size and length of udders and teats in dairy camels.Similarly, Abdallah & Faye (2012) observed a clear variability in teats and udder length in 12 breeds of camels in Saudi Arabia, while some of the udder morphometric measurements of Lahween dromedary camel in Sudan have proved to possess an impact on their milk yield (Eisa et al., 2010).Additionally, dairy camels are characterized by the development of the udder and milk veins (Wardeh & Al-Mustafa, 1990).
The secreted milk is stored in two anatomical compartments as alveolar and cisternal milk.Animals that store large amounts of milk in the gland cistern generally produce more milk, and tolerate extended milking intervals (Knight & Dewhurst, 1994;Ayadi et al., 2003).Therefore, studying the pattern of milk accumulation and storage in the udder can help improving the techniques and routines for machine milking in camels.
As far as we know, there is a paucity of data studying the relationship between udder morphology traits and milk yield of dairy dromedary camels.Therefore, the aim of this study was to evaluate the external (morphological) and internal (milk compartments) udder traits and machine milking performances in lactating dromedaries managed under intensive conditions in Saudi Arabia.

Animals and management
Twenty two multiparous lactating dromedary camels (590 ± 40 kg BW) in late lactation (275 ± 24 days) with apparent healthy udders and maintained at the farm of Camel and Range Research Center (Skaka, Al-Jouf, Saudi Arabia) were used in the present study.All camels were identified by electronic ceramic boluses (Rumitag, Esplugues de Llobregat, Barcelona, Spain) according to Salama et al. (2012).The boluses contained a 32 × 3.8 mm radiofrequency transponder (Ri-Trp-RR2B-06, Tiris, Almelo, the Netherlands) working at a low frequency (134.2 kHz).
Lactating camels suckled their calves freely during the 1 st month of lactation.Then, the dams were introduced to twice daily (08:00 and 17:00 h) machine milking being the calves from their dams and allowed to suckle for striping after milking.Calves were weaned at 12 th month of age.
The milking routine included: milk let-down by calves; udder preparation, machine milking, and final stripping by the calf.Camels were milked using a portable machine milking (Kurstsan Milking Machine, type SSM, Istambul, Turkey).The milking clusters had a claw and four individual teats cups with rubber liners and stainless steel cups.The weight of the milking cluster and the diameter of the lines were 2.6 kg and 23 mm, respectively.The milking machine was set at 45 kPa, 60 pulses min -1 , and 60:40 pulsation ratio, and equipped with recording jars and a low milk pipeline.
Daily ration per animal consisted of alfalfa hay adlibitum supplemented with 3 kg d -1 of barley grain and 1 kg d -1 of wheat bran.Camel had free access to clean tap water.

Udder morphology measurements
Measurements of udders and teats were taken in duplicate in the evening (17:00) just before the p.m. milking.Measurements (cm) were the following (Fig. 1); udder depth (UD, distance between the rear udder attachment and the base of teat), udder height (UH, distance from the ground to the base of the teats), udder length (UL, distance between the front and rear attachments of the udder), teat length (TL, distance from the teat insertion base to the teat orifice), teat diameter (TD, measured in the middle of the teat using a Vernier caliper; ASAHIT, Hamburg, Germany), teat separation (TS, distance between front and rear teat ends), teat-end to floor (TEF, vertical distance between the teat-end and the floor), and milk veins diameter (MVD) measured approximately at 20 cm from the udder with the same Vernier caliper.
Udder traits and milk yield in machine milking dromedary camels

Milk yield and milking characteristics
Individual milk yield, lag time (time from cup attachment to the first drops of milk being observed) and milking time (time to obtain all machine milk fractions) were recorded during milking.Milk samples were collected and analyzed for fat, protein, lactose and total solids using an automatic milk analyzer device (Lactoscan MCC, Milkotronic Ltd, Stara Zagora, Bulgaria) previously calibrated for camel milk.

Cisternal and alveolar udder compartments
To study the milk partitioning between cisternal and alveolar udder compartments, a subset of 10 late lactating camels (255 ± 45 days) were used 9 h after milking.Dams were separated from their calves and moved to a restraining pen (unfamiliar surroundings) to reach a stressful situation for preventing spontaneous milk letdown during udder manipulation according to Bruckmaier et al. (1993).At first, cisternal milk volume was evacuated by machine milking.Thereafter, dams received intramuscular injection of oxytocin (20 IU/camel; Biocytocine, Laboratoires Biové, Arques, France) to induce milk letdown.Alveolar milk was obtained by machine milking and then volume was recorded.Milk samples of each fraction were collected and analyzed for; fat, protein, lactose, and solids-not-fat using the Lactoscan.

Statistical analysis
Data were analyzed for least squares means using the proc GLM of Statistical Analysis System (SAS version 9.2, SAS Inst.Inc., Cary, NC, USA).Significant differences between means were determined by Fischer's least significant difference (LSD).The overall level for statistical significance was set at p < 0.05.The degree of association between measurements was analyzed using the Proc CORR of SAS, where the correlation coefficients (r) of Pearson were computed.

Results
No subclinical mastitis was detected in any of the udders during the experimental period as indicated by the CMT (< 1), SCC, and EC.On average, milk yield as well as milk fat and protein contents were 4.80 ± 0.50 L d -1 , 2.61 ± 0.16% and 3.08 ± 0.05%, respectively (Table 1).Low fat:protein ratio (< 1.0) was observed.Average values of lag time and milking time were 3.0 ± 0.3 s and 120.0±8.9 s, respectively (Table 1), for the milk yield obtained at the evening milking (1.99 ± 0.39 L).No differences were detected between right and left teats measurements (Table 2); therefore, values were averaged and jointly discussed.Results revealed that dairy camels had a developed udder and milk vein, with medium size teats (Table 2).
Positive correlations were observed between udder height and both teat-end floor distances (r = 0.75 to 0.87, p < 0.05) as well as between teat length and diameter (r = 0.38 to 0.75, p < 0.05), while negative correlation was obtained between teats diameter and distance between teats (r = -0.23,p = 0.09) (Table 3).Furthermore, milk yield was correlated positively (p < 0.05) with udder depth (r = 0.37), distance between teats (r = 0.57) and milk vein diameter (r = 0.28), while a negative correlation was found with udder height (r = -0.25)(Table 3).Positive correlations were observed between milking time and milk yield (r = 0.61; p < 0.01) as well as distance between teats (r = 0.42, p = 0.06).However, lag time was not correlated with milk yield and all udder measurements.
No difference was detected between right and left cisternal milk; therefore, values were averaged and jointly discussed.Cisternal milk accounted for only 11% of the total udder milk (Table 4).Volume of cisternal milk did not correlate (r = 0.46; p = 0.21) with alveolar milk.However, positive correlations were observed between milk yield and volume of alveolar (r = 0.98; p < 0.001) as well as volume of cisternal milk (r = 0.63, p < 0.05).Fat content in alveolar milk was greater (21%; p < 0.05) than in cisternal milk (Table 4).However, protein, lactose and solids-not-fat contents did not differ between cisternal and alveolar milk fractions (Table 4).The SCC   averaged 355 ± 104 (×1,000 cells mL -1 ), and did not change significantly between cisternal and alveolar milk fractions, although it was numerically greater in cisternal milk compared to alveolar milk (Table 4).

Discussion
Exploring the udder morphology as well as studying milk accumulation and storage in the udder are necessary aspects for improving milk yield and machine milking ability of dromedary camels.
In the current study, introducing machine milking did not negatively affect the udder health of dromedary camels as indicated by CMT, SCC, and EC.This agrees with previous conclusions of Wernery et al. (2004) and Hammadi et al. (2010) on dromedary milked under intensive conditions.
Daily milk yield as well as protein, lactose, and total solids contents were within the normal ranges reported in literature of dromedary camels under intensive conditions (Konuspayeva et al., 2009;Aljumaah et al., 2012a;Nagy et al., 2013).Meanwhile, milk fat content was lower than those reported by Ayadi et al. (2009) and Hammadi et al. (2010).The low fat values observed in our case resulted in an inverted fat:protein ratio (Table 1), which was a consequence of the incomplete milk letdown during the machine milking (e.g.milk without stimulatory calf suckling or inefficient prestimulation machine milking).Nevertheless, the incidence of low milk fat syndrome as a consequence of low proportion of forage in the diet should not be discarded and would need further research.
Regarding milking characteristics, mean value of lag time (3 s; Table 1) was shorter than observed by Hammadi et al. (2010;36 s) on machine milked dromedary camels, which may be attributed to a direct consequence of using calves for inducing milk letdown in our case.Moreover, the lag time in dairy cows depends on the degree of udder filling which varied with interval between milkings, stage of lactation and udder cistern volume (Bruckmaier, 2005).On the other hand, mean values of total milking time (120 s) determined herein were similar to the results previously reported by Wernery et al. (2004) but shorter than the previously observed by Hammadi et al. (2010).
According to our observations, dromedary camels had a developed udder and milk vein with medium sized teats.Udder height measured in the current study was similar to values reported by Eisa et al. (2010) on dromedary camels.However, udder length and depth values were greater than the results previously reported by Eisa et al. (2010) and Abdallah & Faye (2012) on dromedary camels, but within the same range reported for cows (Rogers & Spenser, 1991;Alfonso et al., 2011) and buffaloes (Prasad et al., 2010).Furthermore, teat lengths were similar to values reported in different breeds of camel in Saudi Arabia (Abdallah & Faye, 2012), but were greater than values observed in Sudanese Lahween camel (Eisa et al., 2010).Teat diameter values were similar to those reported by Eisa et al. (2010).Meanwhile, the distance between teats was greater than the results previously reported by Eisa et al. (2010) on camel, but within the same range reported by Alfonso et al. (2011)  With regard to the correlation coefficients between udder traits, significant positive correlations were observed between teat length and diameter, which could indicate that longer teats were wider at the mid-point.The high positive correlations among these measurements suggest that only one single teat measurement could be included in the selection schemes.Furthermore, the positive correlations observed between daily milk yield and udder depth, distance between teats as well as milk vein diameter traits agree with Eisa et al. (2010).The well developed milk veins observed in our work may reflect a high yield milk secretion potential in Saudi dromedary camel.Similarly to our results, negative correlations were obtained between daily milk yield and udder height trait in dromedary camels (Eisa et al., 2010) and cows (Rogers & Spenser, 1991).However, no significant correlations were observed between daily milk yield and teat length and diameter as reported by Eisa et al. (2010).Accordingly, dromedary camels showed adequate udder morphology traits to the machine milking, and subsequently can be adopted in breeding programs of dromedary camels in Saudi Arabia.
The cisternal milk fraction varied according to species, breed, lactation stage, parity and milking intervals (Caja et al., 2004;Salama et al., 2004;Castillo et al., 2008).According to Yagil et al. (1999), camels do not have a noticeable mammary cistern which is contradicted by our results.Although the percentage of cisternal milk obtained in our study at 9-h milking interval was lower than that reported by Ayadi et al. (2009) in camels at 24-h milking interval (20 %), Ayadi et al. (2003) in cows at 12-h milking interval (30%), and McKusick et al. (2002) in ewes at 8-h milking interval (38%), our result was greater than reported by Thomas et al. (2004) in buffaloes at 12-h milking interval (5%).Animals that store large amounts of milk in the gland cistern generally produce more milk, milked faster and tolerate extended milking intervals (Knight & Dewhurst, 1994;Ayadi et al., 2003).The relatively small cistern size of camels may impair milk secretion and subsequently the total milk yield especially for late lactation and extended milking intervals (Ayadi et al., 2009).Consequently, efficient udder stimulation is recommended in dromedary camels to maximize machine fraction and to minimize stripping fraction during machine milking.Cisternal milk was correlated positively with total milk yield, which might indicate that cisternal size could be used for predicting milk yield in dromedary camels.
In the current study, the parameters of machine milking were set for cows as milking parameters for camel milking are unknown.It is necessary to perform further research work to determine the suitable parameters for machine milking in dairy camels.
Fat content in alveolar milk was greater than in cisternal milk for the 9-h milking interval.This difference can be explained by the viscosity and large size of fat globules which are accumulated in the alveolar compartment.This result agrees with those previously reported in camels (Ayadi et al., 2009), sheep (McKusick et al., 2002) and cows (Davis et al., 1998;Ayadi et al., 2004).On the other hand, no significant difference was observed between milk protein percentage of cisternal and alveolar milk.Protein in milk is primarily found in form of small casein micelles (Cowie & Tindal, 1971) within the aqueous fraction of the milk.Therefore, proteins pass freely from the alveolar to the cistern compartment without being dependent on milk ejection reflex as fat matter.This result agrees with those previously reported in dairy cows (Ayadi et al., 2004), but disagree with results of Ayadi et al. (2009) on camels where alveolar milk protein content was found to be greater than in cisternal milk.The discrepancy between the current and previous results in camels could be explained by the difference in the interval between milking, which was 24-h in the study of Ayadi et al. (2009).Furthermore, SCC did not change between cisternal and alveolar milk fractions.Similar results were obtained in milk fraction of dairy cows (Ontsouka et al., 2003), dairy ewes (McKusick et al., 2002;Castillo et al., 2008) and dairy goats (Salama et al., 2005).
In conclusion, the present study shows that lactating dromedary camels had a developed udder and milk vein with medium size teats, indicating adequate udder morphology for machine-milking.Some udder morphology traits had a positive correlation with milk yield and can be adopted for genetic improving in the breeding programs of dromedary camels in Saudi Arabia.Udder cistern sizes observed in our study were relatively small.This recommends implementing a milking routine with an efficient pre-stimulation before milking to avoid the negative effects of an incomplete milk letdown during machine-milking and to ultimately improve the milk production, milking ability and udder health of dairy camels.Further research is required to confirm these results at early and mid stage of lactation.
Udder traits and milk yield in machine milking dromedary camels

Table 2 .
Least square means (LSM) of udder morphology traits (cm) in dromedary camels measured at late lactation Averaged values for left and right teats are presented.
3Distance between front and rear teats.

Table 3 .
Correlation coefficients between udder traits and milk yield in machine milking dromedary camels

Table 4 .
on cows and Prasad et al. (2010) on buffaloes.Similar results were observed for 794 M. Ayadi et al. / Span J Agric Res (2013) 11(3): 790-797 Cisternal and alveolar milk volumes and their composition at 9 h milking interval in lactating dromedary camel Values with different superscript letters in the same row indicate significant differences at p < 0.05.milk vein diameter trait by Eisa et al. (2010) in camels and Rizzo et al. (2012) in cows.