 |
| Figure 1. Lambing season of traditionally (T group) and rationally managed (R group) ewes |
| Livestock Research for Rural Development 26 (12) 2014 | Guide for preparation of papers | LRRD Newsletter | Citation of this paper |
The relationship of seasonal variation in body condition and helminthic anaemia status with the onset of postpartum ovarian activity was studied in 27 Ouled Djellal ewes under traditional (T ; n = 13) and rational (R ; n = 14) breeding system in 2 farms located, respectively, in a Mediterranean humid (El Tarf) and a semi arid (Constantine) provinces in north eastern Algeria. The resumption of postpartum luteal activity was assessed via radioimmunoassay of plasmatic progesterone during the first 2 months postpartum at 5 to 6 days interval. The peripartum nutritional and helminthic anaemia status of ewes were subjectively monitored using body condition and anaemia scoring (BCS and FAMACHA© system, respectively).
An extended anovulatory period beyond 2 months postpartum, observed following autumn and spring lambing in traditionally managed ewes, appeared to be significantly related to farm management (r = 0.85, P<0.01 ). Ewes of the R group resumed luteal activity 11 ± 1.2 days after lambing. Traditional management under humid climate may affect the onset of luteal activity through food availability and exposure to helminthes infection, mediated by peripartum moderate BCS (lower than 3 or 2 in antepartum or in early postpartum, respectively) and deteriorated FAMACHA© score (higher than 3). The use of these effective indicators proved to be an interesting tool to monitor periparturient ewes and their rebreeding interval.
Key words: anestrus, helminthosis, luteal activity, nutrition, peripartum
In Algeria sheep rearing represents 80% of all domestic food born animals. The “Ouled Djellal” is the main breed representing the so called white Arab breeds in Algeria. There are around 18 millions heads living mainly in a vast area called steppe in a nomadic system characterized by a semi arid climate (Nedjraoui 2006), but a considerable number of them is raised in a sedentary system, on the coastal Mediterranean strip (area called Tell) where the climate is of humid type and agriculture mainly dependant on rainfall. In this area sheep are housed during winter and very often mixed with goats. Flocks are of small sizes; usually from 10 to 20 heads (Nedjraoui 2006).
In Mediterranean and semi-arid areas small ruminant husbandry is characterized by phases of under- and over-nutrition. Nutrient supply and individual body condition vary widely within flocks and throughout the months of the year, which affects both separately and conjointly reproduction in small ruminants (Landau and Molle 1997). Reproduction failure, due to postpartum delayed ovarian activity resumption, has been related to extending lambing intervals (Dunn and Kaltenbach 1980; Chiezey et al 2008). It was reported, in extensive management systems of semi-arid region of Algeria, that body condition could have an effect on reproduction of anoestrous “Ouled Djellal” ewes (Madani et al 2009).
In humid Mediterranean areas and under traditional breeding systems, sheep production has been reported to be limited if infection with gastro intestinal strongyles occurs (Akkari et al 2012). Infection with these internal parasites was reported in the semi arid area of Algeria in “Ouled Djellal” sheep (Boulkaboul and Moulay 2006). The effect of natural and traditional parasitological infection on ewe’s reproduction efficiency was studied in a sub humid area of Nigeria. This effect has been mediated through effects on body condition which ultimately affects re-breeding intervals (Chiezey et al 2008). These internal parasites had been controlled with success in tropical and Mediterranean areas (Bouilhol et al 2009) and in semi arid area of eastern Algeria (Bentounsi et al 2012) via FAMACHA© system for scoring helminthic anaemia (Van Wyk and Bath 2002).
In the present study, the use of subjective indicators (BCS and FAMACHA©) to monitor the effect of nutrition and helminthosis on resumption of postpartum ovarian activity has been assessed by a comparative study in “Ouled Djellal” ewes under traditional and rational breeding management, respectively in 2 biotopes, a Mediterranean humid and a semi arid fields.
The study was conducted in the north east of Algeria from October 2010 to June 2011. Twenty seven ewes aged 2.5 to 5 years, from 2 semi-extensive farms chosen according to their breeding management (traditional or rational) and to the conditions of internal parasites development (climate and anthelminthics prophylaxis), were included in this study.
In the traditionally managed farm the study concerned (T group), all ewes (n = 13, 1 ewe died on the 5th week postpartum) it counted; it was located in a Mediterranean humid (annual rainfall of 699 mm in 2011) province, El-Tarf (latitude 36°45'08.5"N and longitude 7°55'41.9"E).
In the rationally managed farm (R group), 14 randomly selected ewes were studied; it was situated in Constantine province (latitude 36°24'36.5"N and longitude 6°28'48.0"E), characterized by a semi-arid climate (annual rainfall of 511 mm in 2011).
In the “T” group, the ewes were allowed to suckle their lambs and to run with rams continuously. Grazing natural pasture, sometimes complemented with concentrate and straw during rainy days, made up the essential of feeding. Food stock shortages were frequent. The use of anthelmintic was occasional and did not obey to any planning.
In “R” group, the ewes were isolated continuously from the rams. Mating took place after hormonal synchronization (progesterone vaginal sponge, PMSG) of estrus, once per year (April or spring mating). Suckling was intermittently practiced (lambs were separated and kept in the farm during rainy days while their mothers were at range). Concentrate feeds, produced on the farm, were distributed and supplied consistently by hay grass, straw and natural pasture. Increasing nutrient intake and body condition prior to and during breeding (flushing) were used. The use of anthelminthics obeyed to veterinary instructions.
During peripartum, the nutritional status of ewes in both farms was monitored once in the last 3 weeks antepartum (AP) and 10 times in postpartum on day 5, 11, 17, 23, 28, 34, 40, 46, 52 and 58 using 2 subjective indicators (BCS and FAMACHA©).
The scoring of body condition (1 for emaciated to 5 obese) was done according to the method described by Suiter (1994). The difference between antepartum score and the lowest score observed in the 3 first weeks postpartum was considered as the degree of BCS loss in transition period.
The evaluation of anaemia caused by hematophage parasites and observed by the discoloration of the ocular mucosa using FAMACHA© system on a scale of 1 (optimal) to 5 (fatal) was performed. In sheep, an anemia score lower than 3 is usually recommended (Van Wyk and Bath 2002).
Blood sampling was done at 5 to 6 days interval during the first 2 months postpartum.
Blood samples, from the jugular vein, were collected in heparinised tubes at 7:30 am and stored on ice until they were centrifuged at 4000 rpm for 10 minutes. The collected plasma was stored at -20 °C until assay. Concentrations of plasmatic progesterone (P4) were determined using the radioimmunological competitive analysis commercial kits (Immunotech Sa, Beckman Coulter Company, Marseille Cedex, France).
The resumption of postpartum ovarian activity is defined as the time of the first P4 rate increase over 1 ng/ml, maintained for at least 2 successive samples (Thimonier 2000). This step was used to classify the females in 2 groups: the first (AN group) comprises anovulatory ewes (P4 < 1 ng/ml) and the second (LA group) those who resumed postpartum luteal activity.
Analysis of variance (ANOVA) was performed by using SPSS Statistics 17.0 for Windows Statistical Software. The "t" test of Student and Pearson correlation “r” were calculated. In this latter test, luteal activity resumption (LR), BCS loss, farm management (manage) and lambing season (season) were treated as variables.
In both investigated farms, one lambing per ewe per year was recorded. Lambing, in the traditionally managed farm, was distributed over 2 seasons (autumn and spring) with a greater pick in spring (61.5%) following autumn fertile mating which is considered as the natural breeding season (decreasing day length). In the rational managed system, lambing occurred only once per year during autumn but after heat hormonal synchronization (Figure 1).
|
| Figure 1. Lambing season of traditionally (T group) and rationally managed (R group) ewes |
The commencement of postpartum luteal activity was only observed following lambing autumn around 31.5 ± 10.5 days postpartum in 2 over 4 traditionally managed ewes and around 11 ± 11.18 days postpartum in all ewes of “R” group whereas it was delayed beyond the 2 first postpartum months in all spring lambing ewes of “T” group (n = 8).
Data recorded in this study showed that ewes with luteal activity (LA group) and those from the rationally managed farm (R group) were significantly different (P<0.05) as to BCS (> 3) and FAMACHA© (< 3) scores from those of “AN” (Table 1) and “T” (Table 2) groups, respectively.
During the transition period, from antepartum to postpartum, the body condition of ewes decreased in all groups. In the “AN” and “T” groups, the lowest postpartum BCS did not reach the optimum score (2.5) which had been recorded as the lowest obtained postpartum scores in “LA” (Table 1) and “R” (Table 2) groups. The weight recovery occurred similarly at the second week of postpartum in all groups (Table 1).
Similarly to the BCS profile, the FAMACHA© scores appear to be lower than the threshold value (3) in “LA” (Table 1) and “R” (Table 2) groups. The traditionally managed ewes, in ante and postpartum, as well as anovulatory ewes, in postpartum, showed a bad score (≥ 3). Ewes in each latter groups, “AN” (Table 1) and “T” (Table 2), showed a sensitive improvement of their anemia status from the second half (day 46) of the 2nd postpartum month.
| Table 1. Comparison of body condition and FAMACHA© scores between groups (t “test”) according to resumption of luteal activity (results are expressed as mean ± SD and probability “P”). | |||||||||||
|
BCS |
|||||||||||
|
Days |
AP |
5 |
11 |
17 |
23 |
28 |
34 |
40 |
46 |
52 |
58 |
|
AN |
2.18 ± 0.47 |
1.83 ± 0.46 |
1.85 ± 0.34 |
2.05 ± 0.48 |
2.18 ± 0.46 |
2.10 ± 0.47 |
2.05 ± 0.45 |
2.20 ± 0.37 |
2.28 ± 0.43 |
2.45 ± 0.50 |
2.39 ± 0.40 |
|
LA |
3.22 ± 0.68 |
2.69 ± 0.64 |
2.52 ± 0.72 |
2.55 ± 0.63 |
2.64 ± 0.52 |
2.52 ± 0.56 |
2.63 ± 0.58 |
2.50 ± 0.47 |
2.61 ± 0.60 |
2.60 ± 0.71 |
2.45 ± 0.51 |
|
P |
0.00 |
0.001 |
0.01 |
0.04 |
0.03 |
0.06 |
0.01 |
0.09 |
0.13 |
0.56 |
0.78 |
|
FAMACHA© |
|||||||||||
|
Days |
AP |
5 |
11 |
17 |
23 |
28 |
34 |
40 |
46 |
52 |
58 |
|
AN |
2.93 ± 0.72 |
2.88 ± 0.78 |
3.33 ± 0.58 |
3.33 ± 0.71 |
3.20 ± 0.59 |
3.13 ± 0.73 |
3.10 ± 0.70 |
3.00 ± 0.66 |
2.83 ± 0.66 |
2.70 ± 0.69 |
2.64 ± 0.45 |
|
LA |
2.17 ± 0.84 |
2.38 ± 0.78 |
2.33 ± 0.82 |
2.42 ± 0.74 |
2.00 ± 0.72 |
2.34 ± 0.77 |
2.28 ± 0.74 |
2.34 ± 0.70 |
2.22 ± 0.69 |
2.45 ± 0.73 |
2.41 ± 0.74 |
|
P |
0.051 |
0.12 |
0.003 |
0.005 |
0.00 |
0.02 |
0.01 |
0.03 |
0.04 |
0.39 |
0.41 |
|
Table 2. Comparison of body condition and FAMACHA© scores between groups (t “test”) according to farm management (results are expressed as mean ± SD and probability “P”). |
|||||||||||
|
BCS |
|||||||||||
|
Days |
AP |
5 |
11 |
17 |
23 |
28 |
34 |
40 |
46 |
52 |
58 |
|
T |
2.10 ± 0.47 |
1.79 ± 0.42 |
1.77 ± 0.36 |
1.96 ± 0.49 |
2.08 ± 0.47 |
2.02 ± 0.47 |
2.00 ± 0.44 |
2.15 ± 0.36 |
2.19 ± 0.44 |
2.33 ± 0.53 |
2.27 ± 0.45 |
|
R |
3.43 ± 0.37 |
2.84 ± 0.52 |
2.68 ± 0.60 |
2.70 ± 0.52 |
2.79 ± 0.37 |
2.64 ± 0.47 |
2.75 ± 0.49 |
2.59 ± 0.42 |
2.73 ± 0.53 |
2.73 ± 0.67 |
2.56 ± 0.44 |
|
P |
0.00 |
0.00 |
0.00 |
0.001 |
0.00 |
0.003 |
0.00 |
0.009 |
0.01 |
0.11 |
0.13 |
|
FAMACHA© |
|||||||||||
|
Days |
AP |
5 |
11 |
17 |
23 |
28 |
34 |
40 |
46 |
52 |
58 |
|
T |
3.11 ± 0.73 |
3.02 ± 0.79 |
3.42 ± 0.57 |
3.40 ± 0.66 |
3.29 ± 0.57 |
3.21 ± 0.69 |
3.21 ± 0.68 |
3.06 ± 0.61 |
2.96 ± 0.67 |
2.85 ± 0.72 |
2.80 ± 0.53 |
|
R |
1.95 ± 0.61 |
2.18 ± 0.60 |
2.11 ± 0.59 |
2.23 ± 0.57 |
1.75 ± 0.26 |
2.13 ± 0.60 |
2.07 ± 0.50 |
2.20 ± 0.61 |
2.02 ± 0.45 |
2.27 ± 0.59 |
2.23 ± 0.63 |
|
P |
0.00 |
0.005 |
0.00 |
0.00 |
0.00 |
0.00 |
0.00 |
0.001 |
0.00 |
0.036 |
0.03 |
An important and very significant negative relation (P<0.01) was observed during periods of follow-up between body condition and anaemia scores in different groups (Table 3). BCS in the transition period (from AP to the 2nd week of postpartum) appeared to have an effect on the resumption of postpartum ovarian activity. This was showed by a significant positive correlation between this indicator and LR.
This ovarian function was not affected by the FAMACHA© scores in antepartum in the 1st week postpartum but was negatively and significantly (P<0.01) dependent of anemia score (Table 3). Correlation test showed that body condition and anaemia status of ewes were significantly (P<0.0) more related to farm management than season of lambing (Table 3).
|
Table 3 . Correlation (Pearson) of BCS and FAMACHA© with different variables. |
|||||||
|
BCS/variables |
FAMACHA©/variables |
BCS/FAMACHA© |
|||||
|
LR |
Manage |
season |
LR |
Manage |
season |
||
|
Day AP |
0.66** |
0.85** |
-0.49* |
-0.41 |
-0.67** |
0.09 |
-0.68** |
|
Day 5 |
0.60** |
0.75** |
-0.43* |
-0.31 |
-0.53** |
0.05 |
-0.69** |
|
Day 11 |
0.49* |
0.68** |
-0.36 |
-0.57** |
-0.76** |
0.42* |
-0.64** |
|
Day 17 |
0.40* |
0.60** |
-0.25 |
-0.53** |
-0.70** |
0.41* |
-0.72** |
|
Day 23 |
0.43* |
0.66** |
-0.23 |
-0.67** |
-0.88** |
0.48* |
-0.81** |
|
Day 28 |
0.37 |
0.57** |
-0.21 |
-0.47* |
-0.66** |
0.29 |
-0.68** |
|
Day 34 |
0.48* |
0.64** |
-0.32 |
-0.50** |
-0.71** |
0.34 |
-0.73** |
|
Day 40 |
0.33 |
0.50** |
-0.20 |
-0.44* |
-0.59** |
0.28 |
-0.69** |
|
Day 46 |
0.30 |
0.50** |
-0.13 |
-0.41* |
-0.65** |
0.19 |
-0.50** |
|
Day 52 |
0.12 |
0.32 |
0.06 |
-0.18 |
-0.42* |
-0.05 |
-0.59** |
|
Day 58 |
0.06 |
0.32 |
0.16 |
-0.18 |
-0.45* |
-0.04 |
-0.42* |
|
*: P<0.05; **: P<0.01 |
|||||||
These related factors, management and lambing season, had a great impact on the commencement of postpartum ovarian activity such as presented in Table 4 via a strong significant correlation (P<0.01) between variables and LA. This resumption appeared to be not related to BCS loss and somehow dependent on farm management (r = 0.44, p<0.05).
|
Table 4 . Correlation (Pearson) of luteal activity resumption with farm management and lambing season. |
||||
|
LR |
BCS LOSS |
Manage |
Season |
|
|
LR |
1 |
0.85** |
-0.84** |
|
|
BCS LOSS |
0.34 |
1 |
0.44* |
-0.30 |
|
Manage |
0.85** |
0.44* |
1 |
-0.72** |
|
Season |
-0.84** |
-0.30 |
-0.72** |
1 |
|
**: P<0.01; *: P<0.05 |
||||
In the traditionally managed farm, occurrence of lambing over 2 seasons (October-November and March) is comparable to what has been described in Algerian semi-arid area (Madani et al 2009). It was observed that the difference between groups (Tables 1 and 2) has shown the effect of BCS and FAMACHA© on resumption of postpartum ovarian activity which was only observed following autumn lambing.
The body condition scored in late gestation (2.18) and in the 2 first weeks of postpartum (around 1.84) delayed the resumption of ovarian activity in “AN” ewes of the traditionally managed farm when compared with those of LA group (Table 1), beyond 2 months postpartum.
On the contrary, all ewes of R group (BCS decreasing from 3.43 ± 0.37 in antepartum to 2.68 ± 0.60 on day 11 postpartum) resumed earlier their luteal activity (11 ± 11.18 days); the traditionally managed ewes showed a moderate body condition in peripartum (from 2.10 ± 0.47 in antepartum to 1.77 ± 0.36 on day 11 postpartum) which was outside the recommendation range of Suiter (1994). This author suggested that during periods of feed shortage, such as noted in the studied traditionally managed farm, when feeding for survival or for maintenance of body condition, the livestock should be maintained at a condition score of 2.
The relationship between the antepartum BCS (r = 0.66, P<0.01) and that of the first week postpartum (r = 0.60, P<0.01) with the resumption of luteal activity appeared to be dependent mainly on farm management as shown by the significant positive correlation ("r" varied from 0.85 to 0.68 during pripartum, P<0.01) (Table 3).
An adequate body condition in peripartum has probably led to an earlier resumption of postpartum ovarian activity in the rationally farm as reported by other authors (Mitchell et al 2003; Bocquier et al 1993). This could be due to the direct effect of glucose and metabolic hormones (insulin and leptin) at the ovarian level as it was reported following short-term nutritional supplementation of ewes in low body condition (Viñoles et al 2005).
However, the degree of BCS loss (0.64: mean loss of all ewes) from antepartum to early postpartum signed a degree of body fat mobilization related to an inevitable negative energy balance (Cannas, 2004), did not affect the resumption of luteal activity (Table 4).This body loss, if higher than 1 unit in 6 week (not optimal for all breeds), can affect fertility of ewes (Cannas 2004).
The similarity between the variations of the profile of BCS and FAMACHA© as shown via a strong and significant correlation (P˂0.01) between indicators (Table 3) was expressed through an association between a decrease of BCS peripartum and an increase of anemia score in ewes managed traditionally (Table 2). The kinetic of these indicators reflected probably a strongylosis digestive infestation as it was reported in sheep grazing pasture under similar breeding condition in North West of Tunisia (Akkari et al 2012).
Deterioration of anemia status and body condition around lambing in T group was probably the result of the relaxation of the peripartum immunity, periparturient rise, and the nutritional deficit (Akkari et al 2012; Boulkaboul and Moulay 2006; Leask et al 2013).
The luteal inactivity in AN group ewes appeared to be significantly related to the deterioration of anaemia in the first postpartum month (FAMACHA© score higher than 3 starting from 11 to 40 days postpartum). This impact could be explained by the negative influence of the traditional management in humid area on anaemia status (significant negative correlation at all days of monitoring, Table 3). Furthermore, helminthosis effect on reproductive efficiency in ewes in under nutrition (availability of quantity and quality of feed) could be mediated mainly through effects on body condition which ultimately affects re-breeding intervals (Chiezey et al 2008).
In the traditionally managed flock, the lack of adequate prevention by anthelminthic and presence of favorable climatic condition of parasite development aggravated by the relaxation of the peripartum immunity and by feed shortage frequently observed in this farm could explained the greater relation (r = 0.85, P<0.01) between management and resumption of postpartum luteal activity (Table 4).
The commencement of luteal activity was also greatly related to lambing season (r = 0.84, P<0.01) which was reported to be the major factor that controls the moment of the onset of postpartum ovarian activity independently of breed (Santiago-Moreno et al 2000) but at the opposite of what was reported in another sheep Algerian breed “Tadmït” ewes (Ammar-Khodja and Brudieux 1982) where the luteal activity was reported to be not related to photoperiod. Furthermore, a study in "Ouled Djellal" ewes (Benyounes and Lamrani 2013) has shown the existence of silent ovulations in early, in the middle and at the end, of the seasonal anoestrus whatever body condition was.
In this study, the planned absence of lambing during long days in the rationally managed farm has restricted the comparative scope study on the ovulation postpartum occurrence in ewes of the traditionally managed farm that lambed in spring.
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Received 25 August 2014; Accepted 30 October 2014; Published 1 December 2014