Livestock Research for Rural Development 28 (7) 2016 Guide for preparation of papers LRRD Newsletter

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Nulliparous Anglo-Nubian goats submitted to male effect under contrasting climatic conditions

L R Oliveira, M T Moura1, J C Ferreira-Silva1, P S Nascimento1, J M Almeida-Irmão2, L M F Neto1, P F Lima1 and M A L Oliveira1

Universidade Federal Rural da Amazônia, Campus Parauapebas, 68515-000, Parauapebas - PA.
1 Universidade Federal Rural de Pernambuco (UFRPE), Departamento de Medicina Veterinária, Laboratório de Biotécnicas Aplicadas à Reprodução, Recife, PE, Brasil.
2 Instituto Federal de Educação, Ciência e Tecnologia (IFECT), Barreiros, PE, Brasil.


Male effect approach induces and synchronizes estrous in small ruminants, but several factors may affect its potential usage. The objective was to test the effect of contrasting climatic conditions upon the reproductive behavior of nulliparous Anglo-Nubian goats subjected to male effect approach. Females (n = 80) were pre-selected on their body score condition and evaluated for their reproductive status (progesterone level). Females were further isolated from bucks of proven fertility during 60 days and submitted to breeding seasons (BS) of 45 days during the dry period (DP) and rainy period (RP).

Progesterone concentration during the DP was lower 0.54 ± 0.53 ηg/mL than the RP 1.12 ± 1.00 ηg/mL. During the DP, 85.0% females exhibited estrus behavior while 95.0% during the RP. Most estrus were detected between days 11 and 15 on both periods. During the DP, mean values for the first estrus varied between cycling and anestrus females (15.0±0.00 and 12.6±2.31 days), respectively. During the RP, the mean values for the first estrus of cycling and anestrus females were 11.9±2.57 days and 11.2±2.39 days, respectively. Same comparison for cycling females during both periods differed (15.0±0.00 vs 11.9±2.57 days), but not anestrus females (12.6±2.31 vs 11.2±2.39 days). The interval between estrus during the DP was 10.7±6.35 days and during the RP was 21.0±1.40 days. Overall pregnancy rate was higher for RP (85.0%) than DP (65.0%), but pregnancy rate in anestrus females was similar between groups. Nulliparous does are efficiently prone to estrus synchronization by male effect usage and display efficient reproductive performance, irrespectively of luteal state and climatic conditions.

Keywords: buck effect, Capra hircus, caprine, fertility


Semiarid regions are commonly destined for small ruminant production, particularly in developing countries. These regions are characterized by limited forage availability, where most production systems lack modern management practices (Gwasdauskas et al 1972; Silva and Araújo 2000) suggesting that adoption of these methods would increase overall productivity and profitability (Maia and Costa 1997; Leal et al 1999; Bandeira et al 2004).

Male effect approach is a technique that induces a neuroendocrine response in females that synchronizes estrus and ovulation (Lima et al 2000; Horta and Gonçalves 2006; Hawken and Martin 2012; Lopez-Sebastian et al 2014). Moreover, it is an attractive approach by ethical and public standards, since it dispenses use of exogenous hormones (Delgadillo et al 2009). The application of male effect allows breeding season and kidding periods planning under favorable conditions under shorter time periods, rationalizing management practices (Valle et al 2000). Despite growing evidence of applicability of male effect approach using pluriparous females, limited information is available for nulliparous females.

The reduction of age of first delivery is a major goal for modern goat production systems (Bandeira et al 2004), however, it is necessary to understand reproductive behavior of nulliparous does. The first estrous in goats varies according to factors such as breed (Simplício et al 1990; Salmito-Vanderley 1999; Mellado et al 2000; Mellado et al 2004) and period of the year born (Delgadillo and Malpaux 1996), while fertility of nulliparous does is associated with live weight, body condition score, sanitary management and nutritional status (Gonzalez-Stagnaro 1993). Due to the limited understanding of nulliparous reproduction under semiarid conditions (Bandeira et al 2004), the work was aimed to evaluate several reproductive behavior parameters of nulliparous Anglo-Nubian does submitted to male effect under contrasting climatic periods under semiarid conditions.

Material and methods

The research was conducted in Sertânia, Pernambuco, Brazil. The geographic coordinates are 9.107.002 Km N and 691.005 Km E, altitude of 736 m, hot semiarid weather, mean annual temperature of 25ºC, mean annual rainfall 431.0 mm3 with rainy period from February until June, but most rainfall occurs during March and April.

Two bucks with age varying from 24 to 48 months old, and 80 nulliparous Anglo-Nubian females, with age ranging from 9 to 12 months were used in the experiment. Females were raised under semi-intensive conditions, with free access to native pastures (Cynodia vulgaris, L., Mimosa nigra, Hub., Cordia leucocephala, Moric., Bauhinia cheilanta, Steud., Pithecolobium diversiffolium, Benth.) and cultivated pastures (Cenchrus ciliaris, L.). Moreover, animals were fed with hay silage (Pennisetum purpureum, Schum.) during the afternoon during the dry period (DP). All animals had free access to mineral salt and water throughout the experiment.

Females were weighted and identified by numbered ear tags on the day before the experiment onset. Females were initially pre-selected based upon body condition score of 3, in an 1-5 scale (Almeida-Irmão et al 2009; Caldas et al 2015) and were evaluated for their reproductive condition by ultrasonography and vaginoscopy exams (Santos et al 2004; Grunert et al 2005). Progesterone blood concentration was used to determine cyclicity status, where females were considered cycling when P4 concentration was 1 ηg/mL or higher (Morales et al 2003; Almeida-Irmão et al 2009; Caldas et al 2015). Blood samples were collected by jugular vein puncture and serum was stored at -20 °C until further analysis by chimioluminescence.

Bucks were kept apart at a 300 m distance from females during 60 day period. These conditions did not allow any physical, visual, olfactive or auditive contact between genders. Bucks were of proven fertility, but were submitted to an andrology exam the day before breeding season onset (Almeida-Irmão et al 2009; Caldas et al 2015). When introduced in the female herd for 45 day breeding season (BS), bucks were marked with a mixture of grease and ink (4:1) around the sternum bone region in order to facilitate the identification of cycling females. Bucks were re-marked with ink of different color every 10 days for distinguishing different estrus events within the same female.

Information regarding estrus and mating events were collected by trained personnel twice a day (6:00 and 16:00 hours) during both BS. Pregnancy diagnosis was performed by ultrasonography 60 days after the last observed estrus (mating event) (Almeida-Irmão et al 2009; Caldas et al 2015).

The statistical analysis was performed with analysis of variance and means were compared by unpaired t Test and chi-square test for comparisons for binomial data. Differences with probability of P < 0.05 were considered significant.


Progesterone (P4) blood concentration was used to determine the cyclicity status of females before experiment onset (Table 1). P4 concentration was higher in females during the RP. Within cycling females, P4 concentration was similar during both periods; however, anestrus females had higher P4 concentration during the RP. Mean female body weight during the BS of the DP was 26.8±2.36, while during the RP was 25.7 ± 0.67.

Table 1. Progesterone levels in nulliparous goats in breeding seasons of 45 days under contrasting climatic conditions.


Rainy Period

Dry Period


Cycling Females

2.15 ± 0.16

1.70 ± 0.73


Anestrus Females

0.43 ± 0.28

0.33 ± 0.14



1.12 ± 1.00

0.54 ± 0.53





Females showed estrus behavior throughout both BS (Figure 1), but most estrus were detected between days 11 and 15. Estrus detection was also analyzed considering animals that were cycling or anestrus based upon progesterone level before BS onset (Table 1). Estrus incidence differed between cycling and anestrus females during the DP. Remarkably, first estrus within cycling females in the DP was detected on day 15 of the BS. However, estrus were observed at earlier time points for females during both DP and RP, both cycling and anestrus females.

Figure 1. Estrus distribution in nulliparous does submitted to male effect during breeding
seasons of 45 days under contrasting climatic conditions.

The Table 2 contains data regarding the percentage of females that cycled during both climatic conditions. The percentage of cycling females with estrous detected during the DP was lower than RP, but no difference was observed within anestrus females. There was a difference when the percentages of estrous of cycling and anestrus females were compared on DP, however, no difference was observed during RP. A total of 85.0% females cycled during the DP and 95.0% during the RP.

Table 2. Estrous percentage in nulliparous goats during breeding seasons of 45 days under contrasting climatic conditions.

Reproductive status

Dry Season
Estrous / Females (%)

Rainy Season
Estrous / Females (%)


Cycling Females

02/06 (33.3)

16/16 (100)


Anestrous Females

32/34 (94.1)

22/24 (91.6)


34/40 (85.0)

38/40 (95.0)





The timing between estrous in the DP varied from 7 to 18 days (mean value of 10.7±6.35 days) and during the RP from 20 to 22 days (mean of 21.0±1.40 days), with no difference between periods (Table 3). During the DP, 13/20 (65.0%) females cycled once and within those that cycles twice, 2/20 (10.0%) had a short cycle and 1/20 (5.0%) from an estrous cycle with a normal duration. During the RP, 17/20 (85.0%) females cycled once and within those that repeated, 2/20 (10.0%) had a normal estrous cycle, and no short estrous cycles were observed.

Table 3. Mean, standard deviation and range in days for first estrous in cycling and anestrous nulliparous does during breeding seasons of 45 days under contrasting climatic conditions.

Reproductive status

Dry Period

Rainy Period



Mean ± s


Mean ± s

Cycling females


15.0 ± 0.00


11.9 ± 2.57


Anestrous females


12.6 ± 2.31


11.2 ± 2.39





Pregnancy rates were determined after both BS in order to better estimate the viability of estrus induced by the male effect (Table 4). However, no difference was observed between periods while accounting for anestrous females. In contrast, comparison between cycling females pregnancy rates was not made, since no pregnancy was established during the DP from cycling females.

Table 4. Pregnancy rates of nulliparous goats during breeding seasons of 45 days under contrasting climatic conditions.

Reproductive status

Dry Period
Pregnant / Females (%)

Rainy Period
Pregnant / Females (%)


Cycling Females

0/6 (0.0)

14/16 (87.5)


Anestrus Females

26/34 (76.5)

20/24 (83.5)



26/40 (65.0)

34/40 (85.0)






Male effect was not sufficient to synchronize estrous within initial five days of the BS, as previously described for pluriparous females (Chemineau 1983; Lima et al 2000; Almeida-Irmão et al 2009; Lopez-Sebastian et al 2014). The absence of cyclicity response within initial five days of the BS is probably be due to the lack of sexual experience of nulliparous females (Gelez and Fabre-Nys 2004). However, the great majority of detected estrous were concentrated within the 11th and 15th days of the BS is attributable to the male effect, favoring kidding period planning under favorable conditions and under shorter periods of time, while reducing the time and effort for assisting females under delivery (Valle et al 2000).

The complete isolation of genders, with complete avoidance of physical, visual, olfactive and auditive contact for a period of 60 days and sudden introduction of male into females flocks induced estrus at high rates. These findings are supported by extensive literature on pluriparous and nulliparous females (Pearce and Oldham 1988; Lima et al 2000; Chemineau et al 2006; Luna-Orozco et al 2008). The low percentage of estrus in cycling females cannot be credited to the BS during the DP or any reproductive inability of bucks or does, but rather to the small number of animals that were found under cycling conditions (P4 levels).

The time interval between estrus in the BS of the DP was reduced due to short estrous cycles, fact that was not observed during the RP. The hypothesis on short estrous cycles are conflicting. These atypical cycles could be due to premature Corpus luteum (CL) regression (Jainudeen and Hafez 2004), or alternatively, due to CL formed from low quality follicles, resulting in small quantities of luteal cells and insufficient P4 secretion (Chemineau et al 2006). Moreover, short cycles could be due to low P4 levels by undefined factors (Lassoued et al 1997). As described here, females were considered non-cycling when displayed P4 concentrations lower than 1ηg/mL as previously described (Morales et al 2003), and in agreement with this fact, a low incidence of short cycles was found.

The period for first estrus detection was not affected by luteal activity and climatic period, which varied from 7 to 16 days after exposure to males, demonstrating that the male effect is stablished at a low pace in nulliparous females. These results are in accordance with previous reports in young ewes, where an adaptation period occurs to odor emanating from males, in order to affect female reproductive behavior (Gelez and Fabre-Nys 2004). It was also noted that most ewes without sexual experience and exposed to males did not readily activate LH secretion, differently from sexually experienced females. Based on these findings, results described here differ from previous reports, where females displayed estrus within 24 hour period onwards (Chemineau 1983; Almeida-Irmão et al 2009; Luna-Orozco et al 2008).

Despite the fact that first estrus events were detected between the 7th and 8th days after male introduction, estrus incidence was not affected by climatic conditions. However, it is interesting to note that numbers found were higher than 66.6% reported for a Norgestomet and eCG synchronization protocol and 16.6% for male effect alone (Mellado et al 2000), and similar to another report (Luna-Orozco et al 2008), that found an incidence rate of 95%. Collectively, these finding demonstrate that male effect can be efficiently adapted to different environmental conditions.

The interval between estrus during the BS varied from 20 to 22 days in the RP and from 7 to 18 days in the DP, with no short estrous cycle in the RP and only 5% during the DP. In contrast, other authors have found higher incidences for short estrous cycles, e.g. 20 to 62% (Chemineau 1983; Lima et al 2000) 20% associating male effect to cloprostenol in pluriparous does (Luna-Orozco et al 2008), while others have observed a rate of 26% in nulliparous females and 62% in seasonal anestrous pluriparous females and another report registered 20% in pluriparous does using male effect in a 1:40 male to female ratio during the dry season (Almeida-Irmão et al 2009).

It was expected a higher percentage of females exhibiting short estrous cycles, a fact that was not observed here, supporting the hypothesis that young females have lower capacity to attract and stimulate males (Rosciszewska 1985; Gelez et al 2003), and that other factors, such as social-sexual interactions, sexual experience and body size could affect reproductive performance (Gelez and Fabre-Nys 2004).

However, short cycles observed in does and ewes during the initial days of the BS are associated with premature CL regression or anovulation (Lassoued et al 1997; Jainudeen and Hafez 2004) outlined by lack of P4 and its effect on estradiol secretion inhibition and on the establishment of oxitocine receptors in endometrium. Moreover, it was not observed any influence of P4 concentration and climatic condition on response to male effect and short cycle incidence, reinforcing the ongoing hypothesis (Rosciszewska 1985; Gelez et al 2003; Gelez and Fabre-Nys 2004).

It is interesting to note that, smaller values of this steroid before mating events were registered in the DP, probably due to low provitamin A levels found in native and cultured pastures available to the animals, in contrast to the increasing demand for this compound be the animals during this period (Andriguetto et al 2004). The interaction between these factors may be responsible for a vitamin deficit in animals, that may lead to, impairment of ovarian activity, such as lower progesterone production (Rakes et al 1985).

In tropical regions such as the area were this research was conducted, there is normally the interference on the hot environment on reproductive performance such as fertilization failure, embryonic death and fetal loss (Gwasdauskas et al 1972; Jainudeen and Hafez 2004). However, this study did not display any impact on pregnancy establishment and maintenance, despite the trend for lower pregnancy rate in the DP.



We would like to acknowledge CAPES and CNPq for their financial support of the study. M.T. Moura is a PNPD/CAPES Fellow.


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Received 1 April 2016; Accepted 7 June 2016; Published 1 July 2016

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