Effects of Ouled Djellal ewes’ body condition scores on their blood metabolic profile, productive and reproductive performances

A Boudebza, MC Abdeldjelil, N Arzour-Lakhel and N Lakhdara¹

PADESCA, Research Laboratory, Institut desSciences Vetérinaires, University of Constantine 1, Mentouri Brothers, Algeria (25100)
¹ Department of Animal Production, Institut des Sciences Vetérinaires, University of Constantine 1, Mentouri Brothers, Algeria (25100)
assia.boudebza77@gmail.com

Abstract

This experiment aimed to evaluate the effect of body condition score (BCS) of Ouled Djellal ewes on their metabolic profile and productive (litter weight) and reproductive (gestation rate and litter size) performances.The experiment was carried out on 137 clinically healthy Ouled Djellel ewes (2-5 years old) with an average live weight of 51.3 ± 7.7 kg reared in a semi extensive system in the Northeast of Algeria. An average body condition score was assigned to each ewe at different physiological stages (weaning period, mating period, early gestation, mid gestation, late gestation, early lactation and mid lactation). For the data analysis, the ewes were classified in three groups according to their body condition scores (BCS < 2.5 ; 2.5 ≤ BCS < 3 ;BCS ≥ 3) for the thin, middle and fat ewes respectively. Weightings were also carried out on newborn lambs. Blood samples were performed in 83 dry or empty ewes. Plasma concentrations of glucose, cholesterol, triglycerides, creatinine, total protein, albumin, urea, ASAT, ALAT, and macro-minerals (Ca, P, Mg, Na, K, Cl) were determined.

The thin ewes had lower plasma concentrations of triglycerides, albumin and macro-minerals compared to fat ewes. A positive correlation between BCS and cholesterolemia, creatinemia, albuminemia and plasma concentrations of macro-minerals was recorded. However, a negative correlation between BCS and uremia was observed. Ewes BCS varied significantly according to physiological stages. The fertility (gestation rate) improved significantly with the increase in the body condition score (BCS≥3) at mating. A positive correlation between litter size and ewes’ BCS at mating and in mid gestation was recorded. While a positive correlation between litter weight and ewes’ BCS in the mid and late gestation was obtained. It is concluded that BCS had a significant effect on certain metabolic indicators as well as on fertility, prolificacy and litter weight. Maintaining the mean body condition score of the flock above the score of 3 at mating and gestation time could improve productivity of Ouled Djellal ewes.

Keywords: gestation rate, litter size, litter weight, reproduction

Introduction

The satisfaction of food needs throughout the year is not guaranteed whatever the production system is. Indeed, according to Pottier et al (2006) the coverage of needs at any time is limited by physiological (limited ingestion capacity) or economic (food costs) reasons. The body reserves are of great importance in relation to meeting the food needs of ruminants. Classically, the body reserves are mobilized in periods of high metabolic requirements (end of pregnancy, lactation) or of very low feed availability (dry seasons), then reconstituted as soon as the amount and quality of feed increases (rainy season) or when requirements decrease (Gonzalez-Garcia et al 2014).

An animal’s total body nutrient reserves are difficult to measure or assess. The reserves located in the abdominal cavity, such as glycogen in the liver and intra-abdominal fat cannot be assessed easily on live animals without a specific equipment. However, the subcutaneous and muscle reserves along the backbone can be assessed using the body condition scoring (BCS) technique (Kenyon et al 2014). This is a method of estimating in living animals the amount of subcutaneous fat by the palpation of specific parts of the body of animals such as small ruminants. This method involves assigning a score to the animals in relation to the amount of tissue reserves present in particular anatomical regions with specific prominences (Russel et al 1969).

The body condition score (BCS) and its evolution over time makes it possible to estimate the impact of nutrition and different farming practices on health, as well as on the reproduction performance of flock. It is considered as a tool of choice for scientists and breeders regarding its low cost and ease of implementation, this well-mastered technique allows a reliable estimate of the fattening state (Morgan-Davies et al 2008). Its interpretation is less questionable than that of weighing, much more difficult due to the variations in the weight of the digestive and uterine reservoirs. However, the effective use of the body condition score is only possible after the determination of the references of a breed (Dedieu 1984). For the establishment of the state referential, several major questions are therefore asked around the place of these body reserves, their evolution during a campaign, and their relationship with the reproductive performance of animals.

The reproductive function is generally associated with alterations in energy and endocrine system. The blood parameters, along with the BCS, are good indicators of the nutritional and health status of animals. They could serve as reliable predictors that help in preventing a decline in production and reproductive performance, as well as health status of the animals (Sitaresmi et al 2020).

According to Kenyon et al (2014), it is unlikely that a single BCS could be termed optimal from either a biological or economic perspective. The BCS that is associated with the highest productivity varies depending on physiological state, the number of offspring that the ewe is bearing and rearing, the age of the animal, its sex, its breed (genotype), the production system and the level and quality of the feed on offered. Thus, the objective of this study was to follow the evolution of the Ouled Djellal ewes’ BCS during the different physiological stages and to assess its relation with metabolic profile, production (litter weight) and reproductive (gestation rate and litter size) performances.

Materials and methods

Husbandry and feeding

The study was conducted on a productive herd consisting of Ouled Djellal ewes- Hodna variety- belonging to a state holding, located in Ibn Ziad region, Northwest of Constantine (Eastern Algeria) at an altitude of 468m. The average rainfall in the commune of Ibn-Ziad ranges from 350 to 450mm. This region is subject to the influence of the Mediterranean climate characterized by irregular rainfall, and a long period of summer drought. Its climate is a cool semi-arid type, characterized by two periods: a dry and hot period in summer of 133 days (May to September) and a wet and cold period in winter of 197 days (October to April).

The preparation for breeding is done in parks with supplementation according to the body condition scoring of the ewes (flushing 3-4 weeks before the mating). All animals received the same diet based on pasture, hay and concentrate during pregnancy and lactation (Table 1). Fresh water was offered ad libitum. The ewes were also provided with “salt bricks” for licking.

Animals

The study focused on 137 clinically healthy Ouled Djellal ewes, between 2 and 5 years old, with an average live weight of 51.3 ± 7.7kg. The ewes were managed under semi-extensive conditions and naturally mated with fertile Ouled Djellal rams after synchronization (progesterone vaginal sponge, PMSG) of estrus. A pregnancy diagnosis by ultrasound was made two months after the mating. The lambings took place mainly in the middle of autumn, but started in September.

Body condition scoring

The scoring method used was that of lumbar palpation by two operators who attributed the scores in a concerted manner according to a scoring grid ranging from 0 to 5, from the most "emaciated" to the most "fat" (Russell et al 1969). In the end, an average score was assigned to each ewe at different physiological stages (Table2). The ewes were then classified into three groups according to their body condition: G1: (BCS≤2.5); G2: (2.5 <BCS <3); G3: (BCS≥3). The newborn lambs were weighed immediately after birth.

Blood sampling

The samples were taken from 83 clinically healthy dry or empty Ouled Djellal ewes at the morning prior to feeding. The blood samples were withdrawn from jugular vein into heparinizedvacuum tubes Venoject®. The plasma was immediately separated by centrifugation at 3000 rpm/15min, divided into two aliquots and stored at -20°C until analyzed.

The assays were carried out by two automated systems: the ADVIA®1800 Chemistry System (Siemens Healthcare, Frankfurt am Main Germany) and the corresponding commercially available kits for the biological constants: Glucose, Cholesterol, Triglycerides, Creatinine, Total Proteins, Albumin, Urea, ASAT, ALAT, Calcium (Ca), Phosphorus (P) and Magnesium (Mg); the Dimension RxL Max Integrated Chemistry System (Germany, 2007) for Potassium (K), Sodium (Na) and Chlorine (Cl). The blood parameters were analyzed at the Biochemical Laboratory of Constantine, Hospital-University Center.

Statistical analysis

The results were statistically evaluated by Statistica 10 software (evaluation version). According to the data, three statistics tests were used: the Student's t test, the one-way ANOVA analysis and the significance test of Pearson correlation coefficients. The comparisons were considered significant when the p values ​​were less than 0.05.

Results and discussion

The ewes’ BCS and metabolic profile

The results of metabolic profile according to a ewe’s BCS in dry period are shown in Table 4. The concentrations of blood metabolites for ewes in this study were consistent with the normal range for healthy sheep (Dubreuil et al 2005, Kaneko et al 2008). In the current study, plasma concentrations of triglycerides, albumin and (Na, K, Cl and Mg) varied significantly between the three groups with, in fact, low values in thin ewes (group1).

The results of the correlation between BCS and metabolic profile are shown in Table 4. A significant positive correlation was recorded between ewes BCS and cholesterolemia, creatinemia, albuminemia and plasma concentrations of Ca, Na, K, Cl and Mg. However, a significant negative correlation between ewes BCS and uremia was demonstrated.

Based on our results, each level of body condition (groups) corresponded to a different metabolic status. Indeed an obvious under nutrition with BCS ≤2.5 (1.97 ± 0.45) was illustrated by low plasma concentrations of cholesterol, triglycerides, albumin, Ca, Na, K, CL and Mg and by a high uremia.

In the current study, the glucose level was not affected by the ewes’ BCS. Similar results were found in previous studies (Jalilian and Moeini 2013, Yagoubi and Atti 2020). However, Caldeira et al (2007a)and Mazur et al (2009) showed lower values for plasma glucose and triglycerides for thin and undernourished ewes. Caldeira and Portugal (1991) reported that the plasma cholesterol concentration increased with BCS, which corroborates our results which indicate a positive and significant correlation of cholesterolemia with BCS.

The triglyceridemia recorded in this study was significantly higher in ewes with a body score ≥ 3, which is in agreement with the observations of Caldeira et al (2007b) who indicated an elevated plasma triglyceride level in ewes with BCS = 4 comparingto those with scores of 2 and 3 and attribute this increase to the increased synthesis of triglycerides in the intestinal mucosa due to the wide availability of substrates. Pesántez-Pacheco et al (2019) also reported that sheep with a higher BCS during gestation and postpartum had a higher triglyceride concentration than sheep with a lower BCS.

The plasma level of total proteins varied in the same direction as the evolution of the body condition. It was lower in ewes with a low BCS than in animals with a high BCS, results also observed by Caldeira et al (2007a). The nutritional level and particularly the protein consumption were closely related to the BCS. Thus, a fall in BCS following dietary restriction was accompanied by a fall in proteinemia (Caldeira et al 2007a, b). It is also important to emphasize the effect of energy nutrition on the level of circulating proteins, where low energy levels lead to a reduction in protein levels, due to the close relationship between energy metabolisms and protein.

Albuminemia in ewes is very sensitive to severe protein deficits and its decrease might be observed under low protein status with a resulting reduction in hepatic synthesis albumin (Lynch and Jackson 1983). In the present study, a positive and significant correlation (r = 0.48 p <0.0001) between the plasma concentration of albumin and the BCS was highlighted, which is in agreement with the observations of Caldeira et al (2007a, b), who noted positive correlations between BCS and albuminemia.

The uremia in a healthy animal is an indicator of the balance between the nitrogen and energy intake of the ration (Vagneur, 1992). This study revealed a significant negative correlation (r = -0.27 p<0.02) between plasma urea and BCS, with higher uremia (0.40 ± 0.08 g / l) in ewes whose BCS≤2.5 compared to other groups. Caldeira et al (2007b) indicate in their work that uremia is higher in ewes with a low and high body condition score (1 and 4) than in those with a median score (2 and 3). The reason of the increase in uremia is twofolds: either during overfeeding (high BCS) as a result of ammonia production in the rumen and an excess of exogenous N compounds to be absorbed from the intestine and that could in parallel not be stored. Either under severe undernourishment (low BCS), where the origin of urea would come from the mobilization of reserves and the catabolism of proteins in order to compensate the energy deficit (Richards et al 1989, Caldeira et al 2007a, b). This last point could explain the results of the current study.

The creatinine level was not affected by the ewes’ BCS. Similar results were found by Yagoubi and Atti (2020) in Barbarine ewes. While Caldeira et al (2007a) reported higher creatininemia in ewes whose BCS was 2 and 4, and explained that, when the BCS = 2, the increase in the plasma concentration of creatinine is probably linked to significant proteolysis; and when the BCS = 4, serum creatinemia is rather related to the importance of muscle mass.

Most of the minerals assayed during this experiment, except phosphorus, were significantly and positively correlated with BCS. In fact, their plasma concentrations were found to be lower in thin ewes. These results confirm that the ewes whose BCS≤ 2.5 were in a state of under nutrition.

The ewes’ BCS and physiological stages

The descriptive statistics for ewes’ BCS at different physiological stages are reported in Table 5. A significant variation in body condition depending on physiological stage was demonstrated in this study. In fact, between weaning and the period of mating, the BCS significantly increased to reach an average of 2.98 ± 0.49, results also reported by Staykova et al (2013) and Gonzalez-Garcia et al (2014). However, this score remains below the recommendations of Bocquier et al (1988) and Everett-Hincks and Dodds (2005) (3-3.5).

The middle of gestation corresponds to the second period of reconstitution of the body reserves. During this period the ingestion capacity of the ewes is still high and the daily fetal growth remains low,whereas the corresponding needs are negligible. This explains the increase in the ewes’ BCS mean (3.01 ± 0.46) which is within the limits recommended by Bocquier et al (1988) (3-3.5).

In late gestation, the ewes presented a significant fall (p <0.003) from the mean of the BCS (2.61 ± 0.63). These results were also observed by Gonzalez-Garcia et al (2014), which reported a significant mobilization of body reserves in late gestation associated with high plasma levels of AGNE and β-OHB, direct consequence of increased lipolysis (Chilliard 1999). The BCS of ewes a month before lambing should be between 2.5 and 3 according to Fthenakis et al (2012) and between 3 and 3.5 according to Rook (2000). This phase of the reproductive cycle is the most delicate because the needs of the ewe increase very quickly while its capacity to ingest decreases. The female must therefore draw on her energy reserves, but in a moderate way because too much undernourishment risks leading to a reduction in the weight of lambs at birth (Bocquier et al 1988) or to causing pregnancy toxemia (Bocquier et al 1988, Rook 2000, Karagiannis et al 2014). Thus, to limit health disorders of the peripartum, Karagiannis et al (2014), recommend that a strategic rationing plan should be established 30 days before lambing, based on the estimate of BCS and serum β-OHB concentration. These same authors stated that health problems in the ewes were less when their BCSs were between 2.75 and 3.5 and higher when the serum concentration of β-OHB increased.

Even with the distribution of the concentrate during lactation, the average ewes’ BCS declined to reach a value of 2.39 ± 0.60 at the end of the trial period (8 weeks of lactation). This could be explained by the mobilization of the body reserves, because even with the rapid increase in ingestion capacity during this period, the ewe is in a negative energy balance (Everett-Hincks et al 2005, Staykova et al 2013), and cannot, in most cases, ingest enough food to meet the significant increase in these needs (Bocquier et al 1988).

Gonzalez-Garcia et al (2014) reported that the BCS of Romane ewes after lambing does not improve despite an increase in body weight. This increase in the weight of the ewes associated with the high plasma levels of the NEFAs observed during this period suggests that a combination of anabolism and catabolism occurs from lambing until the middle of lactation (Bocquier et al 1990, Rook 2000). These same authors explain these variations by the hypothesis that a reconstitution of protein reserves takes place at the same time as a mobilization of lipid reserves to support milk production.

Relationship between BCS and productive and reproductive performances

Gestation rate

In the present study, fertility (gestation rate) improved significantly with increasing body condition score (BSC) at mating (Table 6). Several studies have reported that fertility and prolificacy are affected by BCS and the live weight of ewes during the mating period (Torre et al 1991, Mellado et al 1994, Zoukekang 2007, Madani et al 2009). Atti et al (2001), observed high fertility in Barbarine ewes whose BCS was > 1.5 and live weight > 35 kg at the beginnig of the mating period. In Sardinian ewes, Molle et al (2001) reported that an increase in BCS (between 2.75 and 3), due to food flushing, leaded to an increase in fertility. However, higher values ​​can cause a decline in fertility (Gunn et al 1984, Rhind et al 1985). For Gunn et al (1972), body condition at mating had a significant ( p<0.01) and positive effect on the incidence of estrus in Scottish Blackface ewes. Whereas a weak body condition during the mating (score of 1.50 points) induced silent heat and a delay in the manifestations of estrus (Rhind et al 1985). Several studies have reported a direct and proportional relationship between the fat reserves of ewes and the ovulation rate (Forcada et al 1990, Barth and Neumann 1991, Molle 2001). Vinoles et al (2005) found that ewes with an elevated BCS had a higher ovulation rate, accompanied by high in FSH and low in estradiol during the follicular phase, high in FSH and low in estradiol during the follicular phase.

Litter size and weight

A positive and significant correlation between litter size and ewes’ BCS at mating and in mid gestation was recorded on the one hand (Table7). In the other hand a relatively stronger positive and significant correlation between litter weight and ewes’ BCS in the mid and late gestation was recorded (Table 8).

In lamb production systems, the total number and the weight of lambs weaned have a significant impact on profitability (Morel and Kenyon 2006, Young et al 2010). The energy balance of a ewe is an important factor in determining the number and weight of lambs weaned. Therefore, it might be expected that ewes of lower BCS will display reduced reproductive performance in comparison with those of greater BCS (Kenyon et al 2014).

A significant effect of body condition during mating on litter size was demonstrated in this study (Table 6). Similar results were previously reported for the same breed (Meredef and Madani 2015). In other breeds, Kleemann et al (2006), Newton et al (1980) and Saul et al (2011) all reported that BCS at breeding and/or mid-pregnancy was positively correlated with the number of lambs weaned per ewe exposed to the ram. Similarly Zoukekang (2007) noted a significant influence of the BCS at the end of the mating on prolificacy. Scaramuzzi et al (2006) reported the existence of a direct relationship between the body condition score and the ovulation rate which determines the prolificacy rate.

The relationship between ewe’s BCS at different physiological stages and a litter weight are shown in Table 7. The obtained results of present study indicated that the heaviest lambs were those from ewes whose BCS was greater than or equal to 3 in mid and late gestation, which agreed with the results of Aliyari et al (2012) and Jalilian and Moeini (2013). For Zoukekang (2007), fat ewes at the end of the third month of gestation gived significantly heavier lambs (p <0.01) than thin ewes. On the Vendéen and Western Red sheep, Seegers (1984) observed that the highest average birth weights were found in flocks where the body condition of the sheep at around 4 months of gestation was greater than 3points.

Conclusion

• This study demonstrated a significant correlation between ewes’ BSC and their metabolic profile, in particular cholesterol, creatinine, albumin and urea as well as those of major-minerals (Ca, Na, K, Cl and Mg).
  
  
• These results confirm that the BCS is a reflection of the nutritional status of the ewes and that it is the best indicator of their body reserves.
  
  
• This study also demonstrated that a BCS ≥3 during breeding period could significantly improve the fertility and prolificacy of Ouled Djellal ewes, while in mid and late gestation; it could be related to an increase in litter weight.

References

Aliyari D, Moeini M M, Shahir M H and Sirjani M A 2012 Effect of Body Condition Score, Live Weight and Age on Reproductive Performance of Afshari Ewes. Asian Journal of Animal and Veterinary Advances, 7, 904-909.

Atti N, Theriez M and Abdennebi L 2001 Relationship between ewe body condition at mating and reproductive performance in the fat-tailed Barbarine breed. Animal Research, 50,135-144. https://doi.org/10.1051/animres:2001121

Barth K and Neumann D 1991 Body condition score is superior to body weight data. The effects of body weight and body condition score on fertility in ewes. Tierzucht, 45, 224-225.

Bocquier F, Theriez M, Prache S and Brelurut A 1988 Alimentation des ovins, in: Alimentation des Bovins, Ovins et Caprins, INRA Ed., France, 249-281.

Caldeira R M, Belo A T, Santos C C, Vazques M I and Portugal A V 2007a The effect of body condition score on blood metabolites and hormonal profiles in ewes. Small Ruminant Research, Volume 68, Issue 3, 233-241.

Caldeira R M, Belo A T, Santos C C, Vazques M I and Portugal A V 2007b The effect of long-term feed restriction and over-nutrition on body condition score, blood metabolites and hormonal profiles in ewes. Small Ruminant Research, 68, 242-255.

Caldeira R M and Portugal A V 1991 Interrelationship between body condition and metabolic status in ewes. Small Ruminant Research, 6, 15-24.

Chilliard Y 1999 Metabolic adaptations and nutrient partitioning in the lactating animal. In: Martinet J, Houdebine LM, Head HH, editors. Biology of lactation. France, Paris, Inserm/INRA, 503-552.

Dedieu B 1984 L’élevage ovin sur parcours méditerranéen : adaptations et mutations des systèmes de production en Cévennes Gardoises. Thèse de docteur ingénieur INAG-PG Paris, 311 p.

Dubreuil P, Arsenault J and Belanger D 2005 Biochemical reference ranges for groups of ewes of different ages. Veterinary Record, 156, 636-638.

Everett-Hincks J M, Blair H T, Stafford K J, Lopez-Villalobos N, Kenyon PR and Morris S T 2005 The effect of pasture allowance during pregnancy on maternal behavior and lamb rearing performance in highly fecund ewes. Livestock Production Science, 97, 253-266.

Forcada F, Abecia J A and Sierra I 1990 Effect of body condition on reproduction in Aragon ewes. Informacion Tecnica Economica Agraria, 2, 123-132.

Fthenakis G C, Arsenos G, Brozos C, Fragkou I A, Giadinis ND, Giannenas I, Mavrogianni V S, Papodopoulos E and Valasi I 2012 Health management of ewes during pregnancy. Animal Reproduction Science, 130, 198-212.

Gonzalez-Garcia E, Gozzo D E, Figuereido V, Foulquie D, Jousserand E, Autran P, Camous S, Tesniere A, Bocquier F and Jouven M 2014 Circannual body reserve dynamics and metabolic profile changes in Romane ewes grazing on rangelands. Domestic Animal Endocrinology, 46, 37-48.

Gunn R G, Doney J M and Russel A J F 1972 Embryo mortality in Scottish Blackface ewes as influenced by body condition at mating and by post mating nutrition. Journal of Agricultural Science, Cambridge, 79, 19-25.

Gunn R G, Russel A J F and Smith W F 1984 The effect of level of premating nutrition on ovulation rate in Scottish Blackface ewes in different body conditions at mating. Animal Production, 39, 99-105.

Jalilian M T and Moeini M M 2013 The effect of body condition score and body weight of Sanjabi ewes on immune system, productive and reproductive performance. Acta Agriculturae Slovenica, 102, 99-106.

Kaneko J J, Harvey J W and Bruss M L 2008 Clinical Biochemistry of Domestic Animals, 6th ed. Elsevier/Academic Press, Amsterdam, 904p.

Karagiannis L, Panousis N, Kiossis E, Tsakmakidis L, Lafi S, Arsenos G, Boscos C and Broscos C H 2014 Associations of pre-lambing body condition score and serum β-hydroxybutyric acid and non-esterified fatty acids concentrations with periparturient health of Chios dairy ewes. Small Ruminant Research, 120, 164-173.

Kenyon P R, Maloney SK and Blache D 2014 Review of sheep body condition score in relation to production characteristics. New Zealand Journal of Agricultural Research, 57, 38-64. https://doi.org/10.1080/00288233.2013.857698

Kleemann D O, Grosser T I and Walker SK 2006 Fertility in South Australian commercial Merino flocks: aspects of management. Theriogenology, 65, 1649- 1665.

Lynch G P and Jackson J R C 1983 Metabolic responses of ewes to different protein intake during late gestation. Canadian Journal of Animal Science, 63, 595-601.

Madani T, Chouia F and Abbas K 2009 Effect of oestrus synchronization and body condition on reproduction of anoestrus Ouled Djellal ewes. Asian Journal of Animal and Veterinary Advances, 4, 34-40. https://scialert.net/abstract/?doi=ajava.2009.34.40

Mazur A, Ozgo M and Rayssiguier Y 2009 Altered plasma triglyceride-rich lipoproteins and triglyceride secretion in feedrestricted pregnant ewes. Veterinarni Medicina, 54, 412-418. https://doi.org/10.17221/77/2009-VETMED

Mellado M, Vera A and Loera H 1994 Reproductive performance of crossbred goats in good or poor body condition exposed to bucks before breeding. Small Rumant Research, 14, 45-48. https://doi.org/10.1016/0921-4488(94)90008-6

Meredef A and Madani T 2015 Dynamique des réserves corporelles de la brebis Ouled Djellal en zone semi-aride. Livestock Research for Rural Development. Volume 27, Article #69. Retrieved July 29, 2020, from http://www.lrrd.org/lrrd27/4/mere27069.html

Molle G, Sana S R, Ligios S, Branca A, Oppia P, Caria A, Corda A R, Demuru G, Fressura G and Ruiu G 2001 The effect of nutrition on the reproductive performance of Sardinian sheep. Informatore Agrario, 57, 75-81.

Morel P C H and Kenyon P R 2006 Sensitivity analysis of weaner lamb production in New Zealand. Proceedings of the New Zealand Society of Animal Production, 66, 377-381.

Morgan-Davies C, Waterhouse A, Pollock M L and Milner J M 2008 Body condition score as an indicator of ewe survival under extensive conditions. Universities Federation for Animal Welfare, 17, 71-77.

Newton J E, Betts J E and Wilde R 1980 The effect of body condition and time of mating on the reproductive performance of Masham ewes. Animal Production, 30, 253-260.

Pesántez-Pacheco J L, Heras-Molina A, Torres-Rovira L, SanzFernández M V, García-Contreras C, Vázquez-Gómez M and Martínez-Ros P 2019 Influence of maternal factors (Weight, Body Condition, Parity, and Pregnancy Rank) on plasma metabolites of dairy ewes and their lambs. Animals, 9, 122-140. https://doi.org/10.3390/ani9040122

Pottier E, Sagot L and Cailleau L M 2006 Conséquences d’une maximisation de la part du pâturage sur les performances techniques d’un troupeau ovin allaitant. Rencontres Recherches Ruminants, 13, 73-77.

Rhind S M, Leslie L D, Gunn R G and Doney J M 1985 Plasma FSH, LH, prolactin and progesterone profiles of Cheviot ewes with different levels of intake before and after mating and associated effects on reproductive performance. Animal Reproduction Science, 8, 301-313.

Richards M W, Wettemann R P and Schoenemann H M 1989 Nutritional anestrus in beef cows: Body weight change, body condition, luteinizing hormone in serum and ovarian activity. J. Anim. Sci. 67, 1520-1526.

Rook J S 2000 Pregnancy toxemia of ewes, does, and beef cows. Veterinary Clinics of North America, Food Animal Practice, 16, 293-317.

Russell A J F, Doney J M and Gunn R G 1969 Subjective assessment of body fat in live sheep. Journal of Agricultural Science, 72, 451-454.

Saul G, Kearney G and Borg D 2011 Pasture systems to improve productivity of sheep in south-western Victoria 2. Animal production from ewes and lambs. Animal Production Science, 51, 982-989.

Scaramuzzi R J, Campbell B K, Downing J A, Kendall N R, Khalid M, Muñoz-Gutierrez M and Somchit A 2006 A review of the effects of supplementary nutrition in the ewe on the concentrations of reproductive and metabolic hormones and the mechanisms that regulate folliculogenesis and ovulation rate. Reproduction Nutrition Development, 46, 339-354. https://doi.org/10.1051/rnd:2006016

Seegers H 1984 Enquête sur la mortalité des agneaux dans les élevages intensifs de l’Ouest. 3. Les facteurs liés aux animaux. Recueil de Médecine Vétérinaire,160, 721-730.

Sitaresmi P I, Widyobroto B P, Bintara S and Widayati D T 2020 Effects of body condition score and estrus phase on blood metabolites and steroid hormones in Saanen goats in the tropics. Veterinary World, 13, 833-839. https://doi.org/10.14202/vetworld.2020.833-839

Staykova G, Penchev P and Stancheva N 2013 Interrelationship between body condition score at different physiological statuses and some economic traits in the Caucasian sheep breed. Bulgarian Journal of Agricultural Science, 19, 1105-1111.

Torre C, Casals R, Caja G, Paramio M T and Ferret A 1991 The effect of body condition score and flushing on the reproductive performance of Ripollesa breed ewes mated in spring. Options Méditerranéennes, Série A, 13, 85-90.

Vagneur M 1992 Biochimie de la vache laitière appliquée à la nutrition. La Dépêche Technique, 28-26.

Viñoles C, Forsberg M, Martin G B, Cajarville C, Repetto J and Meikle A 2005 Short-term nutritional supplementation of ewes in low body condition affects follicle development due to an increase in glucose and metabolic hormones. Reproduction, 129, 299-309. https://doi.org/10.1530/rep.1.00536

Yagoubi Y and Atti N 2020 Effects of the fat-tailed ewes’ body condition scores at lambing on their metabolic profile and offspring growth. Arch. Anim. Breed., 63, 183–191. https://doi.org/10.5194/aab-63-183-2020

Young J M, Thompson A N and Kennedy A J 2010 Bioeconomic modelling to identify the relative importance of a range of critical control points for prime lamb production systems in south-west Victoria. Animal Production Science, 50, 748-756.

Zoukekang E D 2007 Etat corporel de la brebis : relations avec les performances de reproduction et applications pratiques dans un système préalpin pastoral. Mémoire de Master M2, Productions Animales en Régions Chaudes, Montpellier SupAgro, 140 p.