| Livestock Research for Rural Development 34 (5) 2022 | LRRD Search | LRRD Misssion | Guide for preparation of papers | LRRD Newsletter | Citation of this paper |
Breed and season have been reported to affect semen production and quality in rams; however, related studies under tropical conditions are scanty. The aim of this study was to determine the effect of season of the year on body weight, scrotal circumference, sexual behavior, semen characteristics and testosterone concentration. Six mature Pelibuey rams were evaluated for one year, under sub-humid tropical climate at Mexico under a constant good feeding regime: hot-dry (March to June), hot-humid (July to October) and fresh-humid (November to February). Once a week the rams were subjected to a serving capacity test (10 min) and to a semen evaluation. Body weight, scrotal circumference and testosterone concentration were measured monthly. Data were analyzed using general linear model procedures. The season did not affect body weight or scrotal circumference (p>0.05); however, it significantly affected the number of matings, semen characteristics and testosterone concentration (p<0.05). The number of matings was higher in the hot-dry season (2.92 matings). Semen volume was higher in the hot-humid (0.58 ml) and hot-dry seasons (0.55 ml), but sperm concentration was higher in the fresh-humid (257 x 107 sperm/ml) and hot-dry seasons (255 x 107 sperm/ml). Total sperm per ejaculate (145 ± 6 x 107 sperm), mass motility (4.71 points) and progressive sperm motility (87.1 %) were higher in the hot-dry season, but sperm abnormalities were lower in the hot-dry season (5.88 %). The plasma testosterone concentration was higher in the hot-humid season (8.12 ng/ml). The season had effect on sexual behavior, semen characteristics and testosterone concentration; in most cases, rams performed better in the hot-dry season.
Keywords: hair-sheep, scrotal circumference, semen, sexual behavior, testosterone
Sexual behavior and semen characteristics of the ram can vary throughout the year because of various factors, such as age, breed, hormonal influence, nutritional status, environment conditions, etc. (Karagianidis et al 2000; Tajangookeh et al 2007; Zamiri et al 2010; Aller et al 2012). The magnitude of the effect of those factors will affect the reproductive performance of the ram within a flock.
A factor known to influence the reproductive capacity of rams is the environmental conditions (daylight, length, temperature, and humidity) that occur during the seasons of the year. Several studies indicate that sheep are seasonal polyestrous animals of short photoperiod (Kaya et al 2002; Rosa et al 2003). However, it is reported that under tropical conditions at México, hair sheep such as Pelibuey, show reproductive activity most of the year, although it decreases from February to May (Arroyo et al 2007; Arroyo et al 2011). This fact has been associated to the increase of the photoperiod and the environmental temperature.
In relation to the reproductive activity of the rams, in general, it is notified that they are fertile all year round. However, several studies report that the sperm quality of the rams tends to be higher during summer and autumn, than during winter and spring (Oberst et al 2011; Aller et al 2012). It is also known that the scrotal circumference is higher in summer and autumn than at other seasons of the year (Zamiri et al 2010; Aller et al 2012). However, with respect to sexual behavior, the literature provides contradictory results. Some authors (Oberst et al 2011) reported more services in winter than in autumn, whereas others (Aller et al 2012) observed more services in autumn than in winter.
Under tropical conditions and in hair sheep rams, information is still scarce, and the studies carried out do not clearly show the influence of season on semen characteristics and sexual behavior (Aguirre et al 2007a; Cárdenas-Gallegos et al 2012; Cárdenas-Gallegos et al 2015). On the other hand, under tropical conditions the environmental changes (temperature and humidity) are different from those observed in temperate regions. Under these conditions, spring is a time of high temperatures (28.6°C, average) and low humidity; summer is characterized by a slight decrease in temperature (28°C, average) and high humidity (due to summer rains); autumn and winter are characterized by low temperatures (24-25°C, average), and humidity remains high. These variations in temperature and humidity could affect the reproductive capacity; therefore, some researchers have evaluated the effect of environmental conditions, dividing the year into two or three seasons (Aguirre et al 2007a; Cárdenas-Gallegos et al 2012).
It is very important to know the effect that environmental variations have on the reproductive ability of rams throughout the year, because it could be a factor to consider in the management of the animals in a herd. In that sense, various researchers have mentioned that the differences in the flock fertility may reflect differences of sexual behavior expression and the semen characteristics of rams (Stellflug et al 2007; Ungerfeld et al 2008; Alexander et al 2012).
The objective pursued here was to determine the effect of the season of the year on body weight, scrotal circumference, sexual behavior, semen characteristics and testosterone concentration in Pelibuey rams under tropical conditions.
This study was carried out at the Faculty of Veterinary and Animal Science (FVAS) of the “Universidad Autónoma de Yucatán”, México (20° 51′ 43′′ N and 89° 37′ 30′′ W), located at an altitude of 10 m above sea level. The region had sub-humid tropical climate (Aw0), with temperature and rainfall means of 26.3 °C and 890 mm, respectively.
Based on climatological information of the region (temperature and relative humidity) from 1996-2010 (CONAGUA 2014), three seasons were established: hot-dry (March to June), hot-humid (July to October) and fresh-humid (November to February). The hot-dry season had a temperature of 27.9 °C and 69.5% relative humidity (RH); the means for the hot-humid season were 27.7 °C and 80.0% RH, and the fresh-humid season had 24.0 °C and 75.8% RH (CONAGUA 2014). The information on the climatic conditions during the study year shown in Figure 1 was obtained from the meteorological station of the National Water Commission (CONAGUA) of the city of Mérida, Yucatán, México, located 15 km from the study site.
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| Figure 1. Climatological information during the year of study | |
Six Pelibuey rams (3.1 ± 0.5 years old) with a mean body condition score of 3.5 points in scale 1-5 (Russel 1984), and mean body weight of 57.5 kg were used. The males were kept under natural photoperiod and were housed individually in shaded pens. Rams grazed (6 hours/day) in paddocks of African Star grass (Cynodon plectostachius) with irrigation, plus 400 g/day/animal of a commercial feed with 14% crude protein and free access to water and mineral supplement. All rams had been previously bred to ewes, and semen was collected using an artificial vagina.
During one year (January to December 2011), once a week in the morning (08:00 to 10:00 hours), each ram was tested for service capacity. The test lasted 10 min., and each ram was exposed to an ewe kept in a breeding crate in a 3 m x 3 m pen. During each test the sexual behavior (flehmen, anogenital sniffing, foreleg kicks, mounts), the number of matings (mounts with ejaculation) and the duration of each event were recorded. The data were used to estimate the time to first mating (reaction time), the refractory period between the first and second mating (latency-1), and between the second and third mating (latency-2). Rams were not allowed to copulate the exposed ewes. Mating was defined when rams mounted, penetrated and ejaculated into an artificial vagina (Stellflug and Berardinelli 2002; Cárdenas-Gallegos et al 2015). During the serving capacity tests, the semen was collected weekly with an artificial vagina. The semen collected was quickly taken to the FVAS laboratory, placed in a water bath (37°C) and evaluated.
Volume: determined by direct observation of the graduated scale of the collecting tube and expressed in ml. Spermatic mass motility (MM): a drop of semen was evaluated under a microscope using a 0 to 5 points scale; where 0 indicated no waves and spermatozoa moving and 5 the presence of dense and fast waves. Progressive sperm motility (IM): evaluated in a drop of semen, diluted in sodium citrate at 2.9%, at 37 ºC and scored on a 0 to 100% scale. Sperm concentration (SPC): measured in a Neubauer chamber with the semen diluted (1:400) in physiological saline solution, buffered with 1% formaldehyde and methylene blue; it was registered in millions of sperms per ml. Total sperm per ejaculate (TSE): calculated by multiplying sperm concentration and ejaculate volume. Sperm abnormalities (SA): determinated in a diluted drop of semen with 1% formaldehyde, and then counting 100 sperm cells per ejaculate, using a contrast phase microscope, and it was expressed from 0 to 100% (Evans and Maxwell 1990; Aké-López et al 2017).
Rams were weighed monthly in the morning (8:00 - 9:00 a.m.) using an electronic scale with ± 0.5 kg precision (SmartScale 300, Gallagher Group Ltd, Hamilton, Hamilton, New Zealand). The scrotal circumference was measured with the help of a tape band (testimeter), moving the testicles to the lowest part of the scrotal sac; the tape was placed in the widest part of the testicles (Ake-López et al 2017).
Testosterone concentration (ng/ml) was measured in two sheep blood samples (8:00 and 8:30 am) taken every thirty days from January to December. The samples were collected into heparinized vacuum tubes by jugular puncture and then placed in a refrigerator (4-5 °C) until processing. The tubes were centrifuged (3000 X g per 10 min), and the plasma recovered was stored in the freezer at -20 °C, until analysis (more or less 15 min.). The plasma testosterone concentration (ng/ml) was measured using a commercial RIA kit (Siemens, Coat-a-Count, Los Angeles, CA, USA), with a within-assay coefficient of variation of 5 to 18% and an inter-assay coefficient of 6 to 12%. Specificity for 19-Nortestosterone was 20%, for 5α dihydrotestosterone 3.3%, for androstenedione 0.5% and for estradiol 0.02%.
The data corresponding to body weight, scrotal circumference, sexual behavior (number of matings performed, reaction time, latencies, anogenital sniffing, flehmen, foreleg kicks, mounts), semen characteristics (semen volume, SPC, TSE, MM, IM, SA), as well as the testosterone concentration were evaluated using repeated measure models. The mathematical model fitted the fixed effects of season of the year and time when the measure was taken; whereas, ram was taken as random effect. A compound symmetry (co)variance matrix to adjust for correlation of repeated measures was used. Original data for plasma testosterone concentration were transformed to logarithms, and percentage data transformed using arcsine-square root functions, and back transformed after statistical analysis. Mean differences between seasons were performed at a 5% significance level, using ram within season as the experimental error. All statistical analyses were performed using the SAS software (SAS 2012).
No season effect (p>0.05) was found on scrotal circumference (32.5 ± 0.1 cm), nor on body weight (59.0 ± 0.9 kg). The scrotal circumference varied from 32.2 cm to 32.8 cm and the body weight from 57.1 to 61.8 kg.
The sexual behavior activities of rams are shown in Table 1. The number of matings was higher in the hot-dry season (2.92 ± 0.03) than in fresh-humid season (2.76 ± 0.03; p<0.05). Lack of statistical differences were observed between seasons in the other sexual behavioral activities (flehmen, anogenital sniffing, foreleg kicks, mounts).
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Table 1. Sexual behaviour characteristics by season of the year in Pelibuey rams under tropical conditions (means ± SEM). |
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Parameters |
Hot-dry |
Hot-humid |
Fresh-humid |
Average |
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Matings |
2.92 ± 0.03 a |
2.82 ± 0.03 ab |
2.76 ± 0.03b |
2.84 ± 0.02 |
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Anogenital sniffings |
4.18 ± 0.28a |
4.09 ± 0.27a |
4.42 ± 0.28a |
4.23 ± 0.16 |
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Flehmen |
1.65 ± 0.15a |
1.73 ± 0.14a |
1.85 ± 0.15a |
1.74 ± 0.09 |
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Foreleg kicks |
1.75 ±0.28a |
1.99 ± 0.27a |
2.61 ± 0.28a |
2.12 ± 0.16 |
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Mounts |
0.95 ± 0.15a |
0.79 ± 0.15a |
1.27 ± 0.15a |
1.00 ± 0.09 |
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a,b Values with different superscripts between seasons, indicate statistical difference (p < 0.05). |
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No significant differences (p > 0.05) were found between seasons of the year for reaction time, latency-1 and latency-2 (Table 2). The average time to perform the first service (reaction time) was 28.9 ± 2.0 s, the average for the time between the first and second service (latency-1) was 89.8 ± 4.6 s, and the average time between the second and third services (latency-2) was 149 ± 7 s.
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Table 2. Reaction time, latency 1 and latency 2 by season in Pelibuey rams under tropical conditions (means ± SEM). |
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Parameters |
Hot-dry |
Hot-humid |
Fresh-humid |
Average |
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Reaction time (s) |
24.9 ± 3.5a |
32.4 ± 3.4a |
29.0 ± 3.5a |
28.9 ± 2.0 |
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Latency 1 (s) |
76.7 ± 8.0a |
98.2 ± 7.9a |
94.2 ± 8.1a |
89.8 ± 4.6 |
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Latency 2 (s) |
130 ± 12a |
160 ± 12a |
160 ± 12a |
149 ±7 |
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a Values with same superscript between seasons, indicate non statistical difference (P > 0.05). |
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The season of the year significantly affected (p <0.05) all the semen characteristics (Table 3). Semen volume was higher in the hot-humid season (0.58 ± 0.02 ml) and sperm concentration (255 ± 5 x 107 sperm/ml) in the fresh-humid season, TSE (145 ± 6 x 107 sperms), mass motility (4.37 ± 0.03 points) and progressive sperm motility (83.7 ± 0.4%) were higher in the hot-dry season. The highest percentage of sperm abnormalities was found in the hot-humid season (18.0 ± 0.6%; p <0.05).
The concentration of plasma testosterone was also influenced by season of the year (p<0.05; Table 4). The highest concentration of testosterone was found in the hot-humid season (8.12 ± 0.66 ng/ml).
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Table 3. Semen characteristics by season in Pelibuey rams under tropical conditions (Means ± SEM) |
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Parameters |
Hot-dry |
Hot-humid |
Fresh-humid |
Average |
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V (ml) |
0.55 ± 0.02ab |
0.58 ±0.02a |
0.51 ± 0.02b |
0.55 ± 0.01 |
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SPC (x107/ml)
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255 ± 5a
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236 ± 5b
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257 ± 5a
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249 ± 3
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MM (0-5) |
4.71 ± 0.03a |
4.37 ± 0.03c |
4.59 ± 0.04b |
4.56 ± 0.01 |
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IM (%) |
87.1 ± 0.4a |
83.8 ± 0.4b |
86.0 ± 0.4a |
86.0 ± 0.3 |
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SA (%) |
5.88 ± 0.64b |
18.02 ± 0.63a |
5.49 ± 0.66b |
9.95 ± 0.37 |
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V = Volume, SPC = Sperm concentration, TSE = Total sperm
per ejaculate, MM = Mass motility, |
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Table 4. Testosterone concentration by season in Pelibuey rams under tropical conditions (means ± SEM). |
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Parameters |
Hot-Dry |
Hot-humid |
Fresh-humid |
Average |
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Testosterone (ng/ml) |
4.25 ± 0.66b |
8.12 ± 0.66a |
6.41 ± 0.66a |
6.26 ± 0.39 |
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a,b Values with different superscripts between seasons, indicate statistical difference (p < 0.05). |
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Unlike it has been reported in other studies (Tajangookeh et al 2007; Aller et al 2012; Zamiri et al 2005; Tabbaa et al 2016), no effect of season was found here, on body weight and scrotal circumference. This result agrees with that of other authors (Cárdenas-Gallegos et al 2012), who evaluated Pelibuey, Blackbelly, Katahdin and Dorper rams in tropical conditions and did not find season effect (p> 0.05) on the scrotal circumference. The lack of significant difference in the body weight and scrotal circumference of the Pelibuey rams in the present study was probably due to the fact that the rams used were adults and remained under a constant feeding regime throughout the year, so variations in weight and testicular size were minimal.
Several studies reported that sexual behavior was influenced by season of the year (Avdi et al 2004; Kafi et al 2004; Aller et al 2012, Moghaddam et al 2012). Aller et al (2012) reported that the highest average number of matings was found in autumn, and Kafi et al (2004) found that the greatest number of matings was observed in winter. In the present study, no significant effect of the season was found on courtship behaviors (anogenital sniffing, flehmen, foreleg kicks, mounts) of Pelibuey rams. However, season significantly affected the average number of matings, which was higher in the hot-dry and hot-humid seasons. This is a contradictory result, since the highest ambient temperatures (Figure 1) with the lowest (hot-dry) and highest humidity (hot-humid) of the year are observed in those seasons.
In relation to the time to perform the mating (reaction time, latency-1, latency-2), in the present study, no significant differences were found between seasons. These results agree with those from Gündögan (2007), who did not find differences with respect to time to the first service throughout the year (p >0.05). However, our results differ from other authors (Cárdenas-Gallegos et al 2015), using Pelibuey, Blackbelly, Dorper and Katahdin rams, under tropical conditions. They found that the season significantly affected the time at first mating (p < 0.05).
These results indicate that, under tropical conditions, the sexual behavior of Pelibuey rams does not change significantly during the year, which could be used in breeding programs, any time of the year; an aspect that has been suggested in other studies (Aller et al 2012; Kafi et al 2004; Cárdenas-Gallegos et al 2015; Aguirre et al 2007a).
In the present study, all semen characteristics showed significant differences by season. Semen volume was higher in the hot-humid season (summer and early autumn) than in the fresh-humid season (late autumn and winter). These results differ from what was found by other authors, who reported that semen volume increased in autumn (Kafi et al 2004; Aller et al 2012; Gündögan 2007), which is considered the reproductive period of the sheep. However, studies conducted with Pelibuey rams under tropical conditions show contradictory results. Some authors (Cárdenas-Gallegos et al 2012) reported that the season of the year does not affect semen volume, whereas others (Aguirre et al 2007a) indicated that the volume of semen increases in the period of short days, period that corresponds to the autumn season.
Sperm concentration per ml, in the present study, was significantly higher in the fresh-humid and the hot-dry seasons (middle of autumn, winter and spring). These results agree partially with others (Tajangookeh et al 2007; Zamiri et al 2010) that showed higher sperm concentration in autumn (September-October), and lower concentration from February to June (late winter-spring). However, agree with what was reported in Pelibuey rams (Cárdenas-Gallegos et al 2012), who found higher sperm concentration (p < 0.05) from March to June (spring) and lower concentration from July to October (mid-summer to early autumn). As for total sperms per ejaculate, a higher value was observed in the hot-dry and hot-humid seasons; this probably associated with the greater seminal volume in those two seasons. Nevertheless, the higher number of spermatozoa per ejaculate found in those seasons differs partially with what was found by other authors (Karagianidis et al 2000; Kafi et al 2004) who reported higher sperm concentrations per ejaculate in summer-autumn and autumn-winter. Despite the statistical differences between seasons, a high sperm concentration was observed throughout the year, which suggest that the season does not affect sperm production. The same situation has been reported in other studies (Aguirre et al 2007b; Tajangookeh et al 2007; Aller et al 2012).
The lowest values of spermatic mass and progressive sperm motility were found in the hot-humid season (summer and early autumn). This result is consistent with reports in the literature that indicate that the best sperm motility in rams was found in autumn (Karagianidis et al 2000; Kafi et al 2004; Tajangookeh et al 2007; Gündögan 2006; Gündögan 2007). Despite of the differences between seasons, the spermatic mass and progressive sperm motility were adequate throughout the year, similar to what was observed for sperm concentration.
The highest average of sperm abnormalities observed in the hot–humid season (18.0%) confirm previous results that indicate that sperm abnormalities increased in summer (Karagianidis et al 2000; Gündögan 2006; Gündögan 2007); this probably was due to the increase in environmental and/or testicular temperature (Manco et al 2000; Marai et al 2008).
The concentration of testosterone of the Pelibuey rams in the present study showed seasonal effect, being the highest in the hot–humid season (mid-summer and early autumn) and fresh-humid season (late autumn and winter), which agrees with the decrease of the photoperiod in the region (Figure 1). These results agree with different reports, which indicated that the testosterone concentration increased towards the autumn when there is a decrease in the photoperiod, and decreased in the months with more light time (Tajangookeh et al 2007; Casao et al 2010; Hamidi et al 2012; Hedia et al 2019). However, the increase in the concentration of testosterone in Pelibuey rams was not reflected in the characteristics here studied, since scrotal circumference remained practically constant throughout the year. Sexual behavior, except for number of matings, did not seem to be affected in a significantly way, and semen characteristics tended to be better in the hot-dry season, when the testosterone concentration was the lowest.
Scholarship for the second author by the “Consejo Nacional de Ciencia y Tecnología (CONACYT)” is acknowledged (grant number 337470).
The procedures here used were conducted according to the Mexican Official Standard NOM-062-ZOO-1999 for the care, production and use of experimental animals.
The authors declare that there is not conflict of interest in the publication of the article.
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