Onset of puberty in Rembi ram lambs; "Clinical and biochemical follow-up"

O Bousta, A Noui and A Boucif

Institute of Veterinary Sciences, Ibn Khaldoun University, BP 78, 14000, Tiaret, Algeria. Laboratory of farm animal reproduction
aboucif30@yahoo.fr

Abstract

The aim of this study was to determine the age of puberty in Rembi lambs using weekly bodily and testicular measurements followed by the testosterone assay at the time of first mating with ejaculation. The study was carried out at the Haider farm (Tiaret, altitude 1 086 m) on 18 lambs of the Rembi breed from 3 months after birth (weaning at 84 days) and raised in a semi-intensive mode.

The puberty (first mating with ejaculation) settled at a mean age of 224 ± 7 days with a mean weight of 36.3 ± 3.0 kg (43% of male adult weight) and a mean scrotal circumference of 24.3 ± 0.5 cm corresponding to a mean testosterone concentration of 3.5 ± 0.4 ng /ml. Highly significant correlations (p <0.001) were observed on one hand between body weight and scrotal circumference and on the other hand between the testicular measurements, the body weight and the age of puberty.So, the age of puberty varies from one breed to another according to the genotype or living conditions of each breed. However the selection of breeders based only on scrotal and testicular measurements is not sufficient; further studies are needed.

Keywords: Algeria, body weight, Rembi breed, scrotal circumference, sexual behavior, sheep, testis, testosterone

Introduction

In Algeria, sheep farming accounts for more than 80% of the total national ruminants’ population. It constitutes a real wealth that can be appreciated by its high number, which exceeds 26 million heads and by the diversity of its breeds of which the Rembi breed is one of the three main sheep breeds representing 12% of the total national sheep population (Lakhdari et al 2015).

One of the greatest advantages offered by sheep is its high capacity to reproduce and increase animal production (meat, milk, wool and skins). However, its performance is still insufficient to cover the animal protein deficit in human nutrition (Dekhili and Aggoun 2007).

During the last years, only the female of the Rembi breed has been studied in particular for its description and its zootechnical performances (Laoun et al 2015, Benchohra et al 2014, Khiati et al 2012). However, few studies have been carried out in the male of this breed focusing only on some physiological or pathological investigations (Boucif et al 2011, Boucif et al 2008).

In addition, there is no data to our knowledge on the advent of puberty in male lambs of this breed. The aim of this study is to determine the body and testicular measurements of Rembi lambs and the testosterone dosage at the time of onset of the first ejaculation, a sign of clinical puberty (Benia et al 2013, Delgadillo et al 2007).

Materials and methods

Location

The study took place at the pilot farm "Haidar" located 13 km to the south-west of the administrative center of Tiaret (Algeria) at an altitude of 1 086 m, a latitude of 35° 15'N and a longitude from 1°26 'E.

The sheep flock of this farm belongs to the Rembi breed whose native district is in the region of Tiaret, place of the present study.

Experimental animals

The animals were raised in semi-intensive mode and subjected to natural photoperiod. Eighteen (18) Rembi lambs born in January 2015 were selected when they were 12 weeks old with an average body weight of 26.1 ± 2.6 kg at the start of the study.

The experiment lasted for period of 5 months from April to September 2015 representing by 22 weeks. A general condition examination followed by a special genital examination was performed on all the lambs used in the study.

The prophylaxis consisted of internal and external deworming, vaccination against enterotoxaemia and administration of vitamins.

Data recorded

Body weight (BW) and scrotal circumference (SC)

This study focuses on three important aspects that characterize the clinical reproductive performances of lambs of the local Rembi breed. Weekly weighing and measurement of SC were performed on eight ten (18) lambs from weaning to the onset of puberty (time of first mating with ejaculation).

The lambs were weighed using an electronic scale (Zenati® model) with a minimum capacity of 50 g and a maximum capacity of 300 kg. Each lamb was weighed twice for more accuracy. The SC of the lambs was measured using a flexible metric tape. These measurements were made by the same operator from the beginning of the end of the study.

Sexual behavior and plasma concentration of testosterone

In our study, the determination of the onset of sexual activity in the lambs used was the time of appearance of the first mating followed by ejaculation (Belibasaki and Kouimtzis 2000).

Once the lambs become interested in females, weekly 30-minute observations were made for each lamb in the presence of an estrogen-treated adult female of the same breed to detect different signs of its sexual behavior.

The female used in the experiment received an injection of 5 mg of estradiol benzoate the day before to boost it show the heat the next day (Taherti et al 2014). Testosterone was measured for each lamb that made its first ejaculation.

Blood samples obtained from the external jugular vein on heparin tube (Lithium Heparin) were centrifuged 3 000 rpm for 15 minutes (Mona Al-damegh 2012). The serum was decanted and stored at -20°C until plasma testosterone levels were assayed. The concentration of testosterone was measured according to the technique ELISA (Testosterone kit). The testosterone plasmatic concentrations are expressed in nanograms per milliliter of blood (ng/ml).

Statistical analysis

The results obtained in this study were treated by the software "R" version 3.3.0 .2016-05-03.

The correlations between body weight, scrotal circumference and age of lambs were verified by the Pearson Correlation Coefficient Test (p-value) (R version 3.3.0.2016-05-03). Correlations with significance threshold (p<0.05) were considered significant.

The results were expressed as mean ± standard error.

Results

Evolution of body weight and scrotal circumference

BW and SC were monitored from weaning at 84 days to the onset of puberty.

The BW of the lambs increased gradually over the study period (Figure 1) from 26.1 ± 2.6 kg at weaning (84 days) to 36.0 ± 2.8 kg at puberty (224 ± 7 days). At the time of onset of puberty there was an increase of 10.7 kg which is representing an increase of 41.2% (Table 1).

The SC also progressively evolved during the age range between weaning and puberty (Figure 1) from 16.6 ± 0.6 cm to 24.8 ± 0.8 cm representing an increase of 49.7% between weaning and the end of the study an increase of 8.2 ​​cm (Table 1).

Figure 1. Evolution of the scrotal circumference (CS) versus the body weight (BW) (n=18)

There was a highly significant correlation (p <0.0001) among all study parameters from weaning to puberty (Table 2). The testicular growth of the lambs regularly monitored body growth throughout the study period, thus demonstrating a very highly significant (p<0.0001) correlation between the two parameters (r=0.98).

There were strong, highly significant positive correlations (p <0.0001) between age, body weight (r=0.92) and scrotal circumference (r=0.94) respectively.

Evolution of sexual behavior

It was noted that from the 18th week of experimentation after weaning corresponding at the 29th week after birth the lambs started to express their sexual behavior (n=4) by the signs of scent and flehmen (Figure 2).

The first mating was observed from the 20st week in six lambs of which only one (01) finished the mating by an ejaculation (pelvic thrust) at the 31th week after birth that corresponded to the 217th day with a body weight of 35.5 kg and a scrotal circumference of 23.3 ± 0.3 cm.

However, from the 21st week, corresponding to the 32nd week after birth, all the other lambs (n=16) presented mating (Figure 2) of which only 14 lambs ejaculated (n=14). Subsequently, the lambs showed all the signs of sexual behavior completed by ejaculation (n=18) only at the 22nd week of the experiment (Figure 2) which corresponds to the 33rd week of age at an average age of 224 ± 7 days.

Plasma testosterone level

The average testosterone values calculated at the time of puberty based on the onset of first ejaculation for all lambs were 3.5 ± 0.4 ng/ml. The mean values of the various parameters studied and recorded at the time of weaning and puberty are given in Table-1.

Figure 2. Behavioral manifestations expressed in Rembi prepubertal lambs (n =18)

Discussion

Several authors reported that there are different definitions of puberty including the presence of fully developed genitalia, libido and a minimum concentration of sperm in ejaculate (Moulla et al 2018). They reported that the differences observed in terms of puberty onset are attributed to several factors including breed, climate, nutrition management, the methods of estimating puberty and semen collection method employed.

In the current work, the evolution of body weight (BW), the scrotal circumference (SC), the plasma testosterone level and the sexual behavior were considered to investigate the puberty onset.

To our knowledge, no study has focused on the characterization of the advent of puberty in male Rembi lambs in Algeria.

The weaning in the study farm was performed early (84 days) which is similar to the studies of Belibasaki and Kouimtzis (2000) and Tekin et al (2000) at 60 days and 75 days respectively.

In contrast, the weaning of Ouled Djellal lambs (123 days) was delayed which may influence the subsequent growth of lambs (Boussena et al 2016). In Rembi sheep, males expressed puberty at 31 to 33 weeks of age which appeared similar to that reported in Tazegzawt sheep Moulla et al 2018: 33±5 weeks) and in Ouled Djellal sheep (Boussena et al 2016: 31.5-32.5 weeks).

The body weight at puberty in Rembi ram lambs (36.3 ± 3.0 kg) is similar to that recorded in the Najdi breed (38.6 ± 0.6 kg: Swelum et al 2016) and in the Malpura tropical breed (36.7 ± 1.4 kg: Kumar et al 2010). it appeared to be lower than those reported in Ouled Djellal breed (40.4 ± 1.2 kg: Boussena et al 2016), subtropical breed Awassi (42.3 ± 1.7 kg: Kridli and Al-yakoub 2006), in Greek breeds (44.5 ± 3.9 kg at 50.2 ± 2.6 kg: Belibasaki and Kouimtzis 2000) and in Tazegzawt sheep (43.1±5.4 kg: Moulla et al 2018).

However this value is closer to those and much higher than that reported by Wheaton and Godfrey (2003) in the St.Croix breed (25.5 ± 1.1 kg) and by Chafri et al (2008) in the prolific D'man breed (24 kg). Several authors indicate a quite considerable variation in age and body weight at puberty between and within breeds (Moulla et al 2018).

According to Hassan et al (2009), hybrid lambs are heavier at puberty compared to purebreds. Nevertheless, according to Kridli and Al-yakoub (2006), this difference is not significant. But according to Belibasaki and Kouimtzis (2000) and Villasmil-Onteveros et al (2011), the difference in weight at puberty is related to the difference in genotype and birth season. However, Alves et al (2006) reported that the birth season has no influence on pubertal weight.

In our study, the recorded weight corresponds to a percentage of 43% compared to the weight of an adult male of the same breed (Laoun et al 2015: 84.3 ± 1.8 kg). This percentage is similar to that reported in Rambouillet sheep (46.5%; Jiminez-severiano et al 2010) as it is closer to the value reported in the prolific Greek breed Friesland (50%: Belibasaki and Kouimtzis 2000). On the contrary, it is lower than that recorded in lambs of the less prolific Greek breeds such as Karagouniki and Serres (65 to 67%) of adult body weight (Belibasaki and Kouimtzis 2000).

For the scrotal circumference, this percentage is more or less higher (40%) than that reported for Ouled Djellal lambs Boussena et al (2016). Scrotal circumference measured at the time of puberty in our study (24.3 ± 0.5 cm) is similar to that reported in Tazegzawt sheep (25.8 ± 3.7 cm ; Moulla et al 2018), Ouled Djellal breed (Boussena et al 2016: 21.8 ± 0.8 cm), St. Croix lambs (Wheaton and Godfrey (2003: 23.5 ± 0.7 cm), D’man and Timahdite breed Derquaoui et al (2009): 21.4 ± 2.0 cm).

This value is lower than those reported in lambs of Greek breeds raised at high altitudes (Belibasaki and Kouimtzis 2000). According to Bilgin et al (2004), the measurement of the scrotal circumference is a useful test for determining the age of puberty of lambs and the reproductive potential of the rams, but this parameter has some limitations particularly in case of testicular and scrotal affections (Alves et al 2006).

SC varies according to the genetic characteristics of each breed where it is higher in crossbred lambs than in purebred ones (Kridli and Al-yakoub 2006, Soderquist and Hulten 2006). It is also a function of age, whose scrotal growth rate is particularly high around puberty. However, age does not seem to influence testicular development which will be slowed down once growth is completed at two or three years of age (Colas et al 1986).

SC is also a function of the season (Villasmil Onveros et al 2011). Nevertheless, the season does not have great effects in Rembi rams breed where males are sexually active throughout the year (Benia et al 2018). However, all dimensions used for estimating testicular size are much more dependent on body weight and diet than on actual age of males before and after puberty (Ghorbankhania et al 2015, Martinez et al 2012, Mauraya et al 2010).

Dietary restriction in the D'man lambs decreased body and testicular growths and delayed the onset of puberty (Mahouachi et al 2011). The effect of feeding on testicular growth during prepuberty period also affected circulating concentrations of metabolic hormones such as leptin, growth hormone and insulin (Brito et al 2007, Swelum et al 2016).

The strong correlation between body weight and scrotal circumference recorded in our study is in accordance with those reported in previous studies (Chafri et al 2008, Hassan et al 2009, Kumar et al 2010). Similarly, the strong correlation observed between body weight and age is consistent with the findings of other authors (Boussena et al 2016, Elmaz 2007, Jafariahangari et al 2012).

The strongly correlated relationship between scrotal circumference and age is consistent with other studies (Boussena et al 2016, Mandiki et al 2011, Rege et al 2000) and in contrast to results obtained by Hassan et al (2009). The role of testosterone in the sexual behavior of the male results in changes in seasonal testosterone levels by the effect of castration and the effect of hormone replacement therapy as well as "sexual awakening" during puberty (Fabre-Nys 2000).

The plasma testosterone level recorded in our study (3.5 ± 0.4 ng / ml) falls well within the range reported in the literature (2.0 ng/ml to 6.25 ng/ml; Mona Al-Damegh 2012, NazariI-Zenouz et al 2016). This rate is similar to that found in the Najdi breed (3.4 ± 1.4 ng / ml), whereas it is lower than that reported in the Noemi breed (6.25 ± 1.2 ng / ml) in Saudi Arabia (Mona Al-Damegh 2012). However, this rate is higher than reported in lambs of the Iranian Ghezel breed (2 ng/ml; NazariI-Zenouz et al 2016). The effect of the race on the testosterone levels has been demonstrated by several authors where a significant increase has been reported between Outaouais lambs (5.1± 0.7 ng / ml) compared to lambs of the Suffolk breed (2.2 ± 0.3 ng / ml: Fallah-Rad and Connor 1999) and between the two Saudi breeds (Noemi and Najdi; Mona Al-Damegh, 2012).

The onset of puberty generally coincides with an increase in the number of Leydig cells and their nuclear diameter during the prepubertal period, which leads to a substantial increase in testosterone (NazariI-Zenouz et al 2016, Okpe and Ezfasor 2016). Our study did not check the time when the testosterone level began higher than 1 ng/ml.

However, other studies have indicated that the htesighest concentrations of testosterone occurred after the age of puberty (Langford et al 1998). Other factors may also influence plasma testosterone levels with photoperiod fat level and leptin acting negatively on testosterone levels (Picard-Hagen et al 1996; Swelum et al 2016).

The age is one of the factors contributing to the modulation of the expression of sexual behavior resulting in an increase in sexual activity with age. The experience has little effect on the consumption phase of sexual behavior, but it can greatly influence the ability to identify the partner and engage in court behavior (Coltman 2002, Kridli and Said 1999, Simitzis et al 2006).

It is possible that the lambs' lack of interest for the estrogenized females at the beginning of the study period was due to the lack of experience where the lambs become more interested in these females over time. Most articles do not separate the effect the age from the effect of experience (Stellfug and Lewis 2000) but the effect of experience is felt only during the first and/or second exposure (Price et al 1991)

According to Borja dos Santos (2011) the pre-pubescent lambs take a longer time compared to adult rams to show the first lateral approach and first-time females. This finding is confirmed in the present study. On the other hand, the latency to perform the first ejaculation does not differ between young and adult animals (Price 1991).

The difference of the expression of sexual behavior cannot be attributed to the age because the lambs tested in our study were of the same age. However, other factors may influence the results, which differ according to the number and size of ewes exposed to the males, the condition of the ewe (attached or free) and its breed (Belibasaki and Kouimtzis 2000, Borja dos Santos 2011). This is why the performance of young rams should not be evaluated by the number of ejaculations, especially if the female stimuli used are larger than the rams but rather by the number of side approaches and the number of matings (Borja dos Santos 2011).

Conclusion

• A good control of the age of reproduction in males begins with the knowledge of the age at puberty which is not only conditioned by the body growth but also by that of the testes.
  
  
• This study is a contribution to  the morphological and clinical onset of puberty in Rembi lambs, one of the main sheep breeds in Algeria. It confirms the importance of all the morphological, clinical and hormonal measures used to determine the age of puberty in sheep.
  
  
• Rembi lambs reached puberty at an average age of 224 ± 7 days corresponding to a weight of 36.3 ± 3.0 kg (43% of adult weight) and a scrotal circumference of 24.3 ± 0.4 cm.
  
  
• This study helps to understand some reproductive performances in males of the Rembi breed raised in its cradle. It remains now to assess their reproductive potential and identify the factors of variation in their sexual activity throughout the year.

Acknowledgments

The authors thank Professor Daniel Tainturier, Head of the Department of Reproductive Pathology, ONIRIS (France) for his collaboration in the improvement of this manuscript. The authors would also like to thank all the staff of the pilot farm "Haidar" for their help and cooperation in carrying out this work.

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Received 22 February 2020; Accepted 29 April 2020; Published 1 June 2020

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