Effect of Dorper Rams’ Social-Sexual Hierarchy on Their Sexual Behavior and Capacity to Induce Estrus in Ewes

Abstract

This study aimed to assess the influence of the social rank of rams and quality of stimuli to ewes between dominant and subordinate Dorper rams joined to anestrus ewes. Social rank was evaluated for two days (ESR; n = 36); rams were exposed to estrogenized ewes in a competitive test. According to the reproductive response, anovulatory ewes (n = 76) were divided into two groups: LHRe (n = 38; ewes exposed to four low hierarchy rams (LHR)) and HHRe (n = 38; ewes exposed to four high hierarchy rams (HHR)). Regarding aggressive behaviors, HHR showed a higher (p < 0.05) proportion of rams showing threatening, knocking, and blocking behaviors than LHR. Appetitive behavior was higher (p < 0.05) in HHR than LHR rams (3576 ± 0.7 vs. 3054 ± 0.7 number of events). Consummatory sexual behavior was higher (p < 0.05) in HHR than LHR (499 ± 0.3 vs. 205 ± 0.1 number of events). Indicators of sexual inactivity (SRI) were similar between HHR and LHR (499 ± 0.3 vs. 433 ± 0.1; p > 0.05). The estrus response (>80%; p > 0.05) and ovarian response (70%, p > 0.05) were similar for both groups of ewes. It was concluded that LHR are equally effective as HHR in inducing sexual activity in ewes showing postpartum anestrus.

1. Introduction

The ram effect induces estrus in non-cycling ewes [1] and increases luteinizing hormone (LH) secretion advancing the LH surge in cycling ewes [2]. Nevertheless, the response of ewes to the introduction of rams can fluctuate due to several factors, such as the quality of the stimulus from the male, the intensity of the smell, vocalizations, and the male sexual behavior [3,4]. In addition, the response may also differ due to other factors related to ewes, such as body energy reserves and hierarchy [5,6].

In most ungulates, male reproductive success increases with increasing social rank [7]. Social status refers to the relative position of an individual animal within a dominant hierarchy established in a group [8,9]. In sheep, hierarchy is established at a young age (i.e., lambs), and it determines the behavioral and morphological development of rams [10]. Hierarchical links among rams determine unequal access to food and ewes in estrus; higher-ranked rams have more mounts and offspring than lower-ranked rams [11,12]. On the other hand, high social-ranked ewes subjected to the “male effect” ovulate and get pregnant earlier than ewes with low social status [13]. Dominant ewes, in addition to having a larger body weight or body energy reserves, have a greater interaction time (i.e., stimulus) which seems to make them more sensitive to socio-sexual cues emitted by rams. Such physiological and behavioral scenarios favor sexual bio-stimulation, which triggers an early reproductive activity [13,14].

During the reproductive season, high-ranked rams present higher blood testosterone concentrations, a greater volume of ejaculate, and higher sperm concentrations than subordinate rams [15]. Besides, dominant rams have more successful copulations than low social-ranked rams. Moreover, high-ranked rams restrict the reproductive activity of lower-ranked rams [15]. In general, individuals of high social rank have greater reproductive success than those of lower social ranks [5,15,16]. In addition, the highest number of mounts occurs during the day than at night, with peaks of behaviors between 08:00 to 14:00 and 18:00 to 20:00 h [17], being of interest to analyze the sexual behaviors presented during the twilight hours, when many ungulate species are more active [18].

Thus, when rams and ewes interact freely, dominant rams perform a greater number of copulations. However, it has been recently proposed that when the activity of both dominant and subordinate rams is restricted (i.e., distributed in different pens), estrus ewes tend to be mounted and impregnated by rams of lower socio-sexual hierarchy [11]. Based on the above findings, we hypothesize that, in absence of high-ranking rams, low-ranking rams show a high quality of sexual behaviors that stimulate estrus response and a high pregnancy rate in anestrus ewes. This study had two objectives; to compare estrus response and pregnancy rate of anovulatory well-fed Dorper ewes joined to either low social or high social-ranked rams, and also to determine various sexual behavior responses of low social and high social-ranked rams.

2. Materials and Methods

2.1. General

The procedures used for this study were approved by the Autonomous Agrarian University Antonio Narro Ethics Committee (38111-425501002-2870).

2.2. Location and Environmental Conditions

The study was carried out during the natural anestrus season (March–May) in the semi-desert of northern Mexico (25°32′40″ N, 103°26′33″ W). The area is characterized by an arid climate, with an annual average temperature of 23.1 °C and an average annual rainfall of 230 mm. The relative humidity ranges from 26 to 61%; the photoperiod ranges from 13 h 41 min during the spring solstice (June) to 10 h 19 min during the winter solstice (December).

2.3. Experimental Animals and Their Management

Dorper adult rams were included in the study (n = 36, 3-yr-old, average live weight (LW) 77.4 ± 3.3 kg, and body condition score (BCS) of 3.9 ± 0.1 units), the BCS was determined by a well-trained technician using a 1–5 scale with 0.5 increments with 1 being emaciated and 5 being extremely fat [19], along with multiparous Dorper ewes (n = 76, 2–3 lambings, LW = 40.2 ± 3.3 kg, and BCS = 2.5 ± 0.4 units). All animals were fed twice a day (10:00 and 18:00 h) with a mixed ration (17% CP and 1.5 Mcal ME/kg DM), having free access to mineral salts and water. All animals received fat-soluble vitamins and were dewormed three weeks before the study. The main management practices and experimental activities are shown in Figure 1.

2.4. Determination of Socio-Sexual Ram Hierarchy (Ram Sexual Index)

A competition test was performed for the evaluation of the social rank (ESR) during two days (n = 36). These tests were performed using estrogenized ewes (n = 10, treated with 2 mg of estradiol cypionate every 48 h for 7 d) as the stimulus. Ram dyads were exposed to an ewe for 5 min in individual 2.5 × 2.5 m pens to elicit competitions. New pairs of rams were formed until each ram competed against the remaining rams recording agonistic behaviors such as aggression (AG); headbutting (HB); knocking (KN); blocking (BL); thrusting (TU); and avoidance (AD), also sexual behaviors such as approaches (AP); flehmen (FL); mounting (MO); sniffing (SN); and disinterested behaviors such as peripheral activity (PE) and eating (EA) were recorded.

The rams’ social rank was determined calculating the success index (SI) formula [13,20], where the performance of each individual is calculated considering all the dyads contested, thus determining three social ranks in the evaluated rams: low (LSR; SI = 0 to 0.33); medium (MSR; SI = 0.34 to 0.66); and high (HSR; SI = 0.67 to 1.0):

$$\mathrm{Succes} \mathrm{index}=\frac{\mathrm{won} \mathrm{events}}{\mathrm{won} \mathrm{events}+\mathrm{lost} \mathrm{events}}$$

An event was considered as “won” when the male was able to displace the contestant and as “lost” when the male was displaced.

2.5. The “Male Effect”: Sexual Behavior of Rams

Once the socio-sexual rank was determined, two experimental groups were formed based on such test: randomly selecting 4 low hierarchy rams (LHR; 0.283 ± 0.03) and 4 high hierarchy rams (HHR; 0.576 ± 0.06), then, their ability to induce the reproductive response of anovulatory ewes through the “male effect” was assessed. The timeline of actions is depicted in Figure 1.

Response variables indicative of appetitive sexual behavior (ASB) were: flehmen; anogenital sniffing; approaches; pawing; vocalization; penis extrusion. Consummatory sexual behavior (CSB) included mount attempts and successful mounts. Indicators of sexual inactivity (ISR) were isolation-standing; isolation-lying down; attempt to escape; aggressions; evasions; and external distractions [21].

2.6. The “Male Effect”: Response of the Anovulatory Ewes Exposed to High and Low Hierarchy Rams

To quantify the possible reproductive response of anovulatory Dorper ewes (n = 76; homogeneous regarding age, BW and BCS) to the socio-sexual cues exerted by the LHR and HHR, ewes were divided into two groups: LHRe (n = 38; four groups of ewes exposed to one LHR each) and HHRe (n = 38; four groups of ewes exposed to one HHR). Rams within rank groups were randomly assigned to each experimental group, placed in pens 100 mts apart and rotated between groups every 12 h, before behavioral and estrus evaluations. Before breeding, ewes underwent two ultrasound scans (d -15 and d -7) to determine the absence of corpora lutea to confirm anestrus. In addition, ewes of both groups received an intramuscular dose of 25 mg progesterone 24 h before exposure to rams in order to prevent short estrus cycles [22]. Then, on d 0, the first day of the male-to-female interaction and up to 15 days later, the rams remained with the ewes.

Ewes in estrus were recorded during ram exposure to detect the onset of estrus; evaluations were made every 12 h for 15 d, twice a day (07:00 and 19:00) for 15 min each time. Then, the rams were removed from the ewes’ pen. The latency to estrus was the interval between the first contact with rams and estrus activity. Ewe immobilization was considered a sign of receptivity to rams [23]. The percentage of ovulating ewes was determined as ewes ovulating/ewes exposed, considering the presence of corpora lutea [24] during the ten days after the introduction of rams. Ovaries were scanned with a transrectal ultrasound (Aloka SSD 500, Tokyo, Japan) connected to a 7.5-MHz linear probe. The same equipment was used for pregnancy diagnosis at 45 d after the introduction of rams. Ultrasound scanning was performed by the same skilled operator.

2.7. Statistical Analyses

Rams within each socio-sexual rank and ewes exposed to rams were the experimental units. Since the percentages of aggressive behaviors, sexual behaviors, disinterested behaviors and sexual-success index had non-normal distribution according to the PROC UNIVARIATE procedure of SAS (SAS Institute, Cary, NC, USA), these data were subjected to logarithmic transformation (log (X + 1)); later on, data were analyzed using the PROC GLM procedure of SAS to assess the effects of hierarchical status (low or high) upon such variables. The PROC GENMOD procedure of SAS was used to determine the effect of ram social rank (two levels), time of day (a.m. and p.m.), and totals per day on appetitive and consummatory behaviors. The distribution of counting variables (i.e., estrus induction, inter-estrus interval, estrus duration, ovulation percentage, gestation, and ovulation rate) among main effects were compared using the SAS CATMOD procedure to determine the possible effect of hierarchical status (low or high) on the reproductive response of ewes in anestrus. This procedure was used for evaluating the social rank effect upon the reproductive performance of anestrus ewes (i.e., estrus induction; estrus interval; estrus duration; ovulation percentage; gestation; and ovulation rate). Differences were considered significant at p < 0.05. Values are presented as means ± standard deviations.

3. Results

3.1. Evaluation of Social Rank

Table 1. Confrontational behaviors of well-fed adult Dorper rams recorded during the competition test used to measure the Success Index.

	Low Rank (n = 14)	High Rank (n = 6)
Confrontational behaviors
Aggressions (AG; %-n)	1.5 (4/253) b	4.7 (17/355) a
Headbutting (HB; %-n)	16.2 (41/253) a	21.1 (43/355) a
Knocking (KN; %-n)	22.1 (56/253) b	15.2 (54/355) a
Blocking (BL; %-n)	39.1 (99/253) b	53.1 (185/355) a
Thrusting (TU; %-n)	19.7 (50/253) a	15.2 (54/355) a
Avoidance (AD; %-n)	1.1 (3/253) a	0.5 (2/355) a
Rank index
Events won (%)	28.2 (95/336) b	57.6(83/144) a
Events lost (%)	71.7 (241/336) a	42.3 (61/144) a
Success index	0.283 ± 0.03 b	0.576 ± 0.06 a

^a,b Values in the same column with different superscript differ (p < 0.05).

presents the variables for determining the social rank index of rams in the present study. HHR showed a higher (p < 0.05) proportion of animals showing threatening, knocking, and blocking behaviors than LHR regarding aggressive behaviors.

Table 2. Sexual and non-sexual behaviors of LHR and HHR shown in the competition tests during the non-breeding season.

	Low Rank (n = 14)	High Rank (n = 6)
Sexual behaviors
Approaches (AP; %-n)	26.3 (159/604) a	23.0 (108/469) a
Flehmen (FL; %-n)	6.7 (41/604) a	4.6 (22/469) a
Mounting (MO; %-n)	19.0 (115/604) b	28.5 (134/469) a
Sniffing (SN; %-n)	47.8 (289/604) a	43.7 (205/469) b
No sexual behaviors
Peripheral behavior (PE; %-n)	78.1 (111/142) a	70.0 (28/40) a
Eating (EA; %-n)	21.8 (31/142) a	30.0 (12/40) a

^a,b Values in the same column with different superscript differ (p < 0.05).

presents sexual behaviors shown by LHR and HHR towards ewes during the competition test, HHR had the highest number of mounting and sniffing behaviors (p < 0.05).

3.2. Sexual Behaviors of LHR and HHR during the “Male Effect”

The general result of the appetitive sexual behavior, consummatory sexual behavior and sexual inactivity, aggressions, and escapes of the rams (low and high social rank) are shown in

Table 3. Appetitive and consummatory sexual behaviors and sexual inactivity, aggressions, and escape behaviors of adult low or high hierarchy Dorper rams (ASB; n = 8) during the morning or afternoon during the non-breeding season.

	Low Rank (n = 4)	High Rank (n = 4)
Appetitive sexual behavior (ASB; n)
Morning	1747 ± 1.2 aB	2107 ± 1.2 aA
Afternoon	1347 ± 1.2 bB	1599 ± 1.2 bA
Whole day	3094 ± 0.7 B	3706 ± 0.7 A
%	45.5	54.5
Consummatory sexual behavior (CSB; n)
Morning	90 ± 0.1 aB	298 ± 0.5 aA
Afternoon	120 ± 0.3 aB	201 ± 0.5 bA
Whole day	210 ± 0.1 B	499 ± 0.3 A
%	33.3	66.6
Indicators for sexual inactivity, aggressions, and escapes (SRI; n)
Morning	193 ± 0.1 aA	205 ± 0.5 aA
Afternoon	240 ± 0.2 aA	201 ± 0.5 bA
Whole day	433 ± 0.1 A	499 ± 0.3 A
%	53	47

^A,B Values in the same row, with different superscript differ (p < 0.05), ^a,b Values in the same column, with different superscript differ (p < 0.05).

. In general, in the appetitive behavior, there was a more significant number in the HHR vs. LHR (3576 ± 0.7 vs. 3054 ± 0.7, respectively; p < 0.05). There were more of these behaviors during the morning regardless of social rank (p < 0.05). The number of consummatory sexual behaviors was greater in HHR than in LHR rams (p < 0.05). Finally, the SRI did not differ between HHR and LHR (p > 0.05).

Appetitive sexual behaviors of the rams (low or high rank) are shown in

Table 4. Appetitive sexual behavior of adult Dorper rams (ASB) classified as low (LHR) or high hierarchy rams (HHR) during the morning and afternoon.

Appetitive Sexual Behavior (ASB; n)	LHR	HHR	LHR	HHR
Approaches			Flehmen
			After directly smelling the female
Morning	258 ± 3.8 aA	213 ± 2.3 aA	80 ± 0.9 aA	92 ± 0.8 aA
Afternoon	194 ± 2.0 bA	145 ± 2.0 bA	67 ± 0.7 aA	41 ± 0.4 bA
Whole day	452 ± 2.1 A	358 ± 1.5 B	147 ± 0.5 A	133 ± 0.5 A
%	62	44.8	42.6	44
Pawing			Without smelling the female
Morning	143 ± 1.6 aB	256 ± 3.7 aA	12 ± 0.3 aA	22 ± 0.3 aA
Afternoon	133 ± 1.6 aB	185 ± 2.4 bA	22 ± 0.3 aA	20 ± 0.4 aA
Whole day	276 ± 1.1 B	441 ± 2.2 A	34 ± 0.2 A	42 ± 0.2 A
%	38	55.2	9.8	13.9
Penis extrusion			After smelling the ewe’s urine
Morning	24 ± 0.4 aB	92 ± 1.6 aA	84 ± 0.7 aA	66 ± 0.9 aA
Afternoon	16 ± 0.3 aB	38 ± 0.5 bA	80 ± 0.8 aA	61 ± 0.6 aA
Whole day	40 ± 0.3 B	130 ± 0.5 A	164 ± 0.5 A	127 ± 0.6 A
%	24	76	47.5	42
Total	40 ± 0.2 B	130 ± 0.8 A	345 ± 0.3 A	302 ± 0.2 A
Vocalizations			Sniffing
	Low		Anogenital
Morning	46 ± 0.8 aB	128 ± 3.1 aA	818 ± 5.1 aA	913 ± 5.1 aA
Afternoon	50 ± 0.7 aA	61 ± 0.9 bA	596 ± 3.5 bA	633 ± 3.2 bA
Whole day	96 ± 0.5 B	189 ± 1.6 A	1414 ± 3.2 A	1546 ± 3.1 A
%	66.6	53.3	76.9	72.8
	High		Body
Morning	21 ± 0.4 aB	84 ± 1.5 aA	261 ± 2.8 aA	241 ± 2.2 bA
Afternoon	27 ± 0.7 aB	81 ± 1.8 aA	162 ± 1.8 bB	334 ± 3.0 aA
Whole day	48 ± 0.4 B	165 ± 1.2 A	423 ± 0.7 B	575 ± 1.9 A
%	33.3	46.6	23	27.1
Total	144 ± 0.3 B	354 ± 1.0 A	1837 ± 2.2 B	2121 ± 2.2 A

^A,B Values in the same row, with different superscript, differ (p < 0.05), ^a,b Values in the same column, with different superscript differ (p < 0.05).

. The percentages of behaviors were higher in the HHR (p < 0.05), except for approaches where the LHR was higher (p < 0.05). Therefore, it is believed that, regardless of social rank, there is a behavioral distribution of the flehmen. That is, ASU and ASF behaviors have priority relative to WSF, regardless of rams’ social rank. Regarding the number of ‘sniffings’ (AGS), HHR and LHR did not differ (p > 0.05). However, in terms of vocalizations, approaches, pawing, and penis extrusion, the HHR showed a greater number (p < 0.05) of these behaviors than LHR.

The appetitive behaviors are shown in

Table 5. Consummatory sexual behavior in Dorper rams (CSB; n = 8) of low (LHR) or high social hierarchy (HHR) during the morning and afternoon, during the non-breeding season.

Consummatory Sexual Behavior		LHR	HHR	LHR	HHR
		Mounting attempts		Mounting with penetration
	Morning	37 ± 0.6 bB	86 ± 1.7 aA	24 ± 0.5 aA	42 ± 0.6 aA
	Afternoon	73 ± 1.3 aA	67 ± 1.5 aA	11 ± 0.2 aB	31 ± 0.5 aA
	Whole day	110 ± 0.7 a	153 ± 0.9 a	35 ± 0.3 b	73 ± 0.4 a
	%	52.3	41.4	16.6	19.8
		Mounting with penis unsheathed		Mounting with ejaculation
	Morning	19 ± 0.3 aB	65 ± 1.4 aA	10 ± 0.2 aA	13 ± 0.5 aA
	Afternoon	23 ± 0.5 aA	43 ± 0.7 aA	13 ± 0.3 aA	22 ± 0.5 aA
	Whole day	42 ± 0.3 b	108 ± 0.8 a	23 ± 0.2 a	35 ± 0.3 a
	%	20	29.2	11	9.5

^a,b Values in the same line, with different superscript, differ (p < 0.05); ^A,B Values in the same column, with different superscript, differ (p < 0.05).

. There was a significant difference between mounts with unsheathing, mounts with penetration, and unsheathing, HHR displayed greater appetitive behaviors than LHR (p < 0.05). Finally,

Table 6. Sexual inactivity, aggressions, and escapes (SRI; n = 8) of low (LHR) or high social ranking (HHR) Dorper rams during the morning and afternoon under natural photoperiod, when joined to anovulatory ewes.

Indicators for Sexual Rest, Aggressions and Escapes (SRI; n)	LHR	HHR	LHR	HHR
Aggressions			Isolation
			Standing isolation
Morning	33 ± 0.3 aA	22 ± 0.1 aA	40 ± 0.3 bA	63 ± 0.7 aA
Afternoon	25 ± 0.2 aA	12 ± 0.4 aA	70 ± 0.8 aA	52 ± 0.7 aA
Whole day	58 ± 0.2 A	34 ± 0.5 A	110 ± 0.5 A	115 ± 0.3 A
%	63	37	62.5	73.2
Scape attempts			Isolation lying down
Morning	3 ± 0.0 aA	1 ± 0.0 aA	33 ± 0.3 aA	17 ± 0.2 aA
Afternoon	5 ± 0.1 aA	7 ± 0.1 aA	25 ± 0.2 aA	25 ± 0.4 aA
Whole day	8 ± 0.5 A	8 ± 0.1 A	58 ± 0.2 A	42 ± 0.2 A
%	50	50	33	26.7
Evasions			Total
Morning	84 ± 0.8 aA	102 ± 1.1 aA	73 ± 0.2 A	95 ± 0.2 A
Afternoon	115 ± 1.0 aA	89 ± 1.0 aA
Whole day	199 ± 0.6 A	191 ± 0.7 A
%	45	55

^a,b Values in the same line, with different superscripts, differ (p < 0.05), ^A,B Values in the same column, with different superscripts, differ (p < 0.05).

shows the behaviors related to sexual disinterest, aggression, and escape. There was no difference in the number of behaviors between the two social ranks (p < 0.05).

3.3. Reproductive Response of Ewes Exposed to LHR and HHR

The reproductive response of anovulatory ewes exposed to LHR or HHR is shown in

Table 7. Reproductive response of anovulatory ewes (LHRe and HHRe) exposed to low (LHR) or high (HHR) hierarchy rams under natural photoperiod during the anestrus season.

	LHRe	HHRe
Estrus induction rate (%, n)	81 (30/37)	89.4 (34/38)
Estrus interval (h)	121 ± 10.9	88.6 ± 8.8
Estrus duration (h)	25.6 ± 2.2	28.2 ± 1.9
Ovulation rate (%, n)	73 (27/37)	89.4 (34/38)
Pregnancy rate (%, n)	64.4 (24/37)	84.2 (32/38)
Ovulation rate (n)	1.22 ± 0.0	1.44 ± 0.0

For all variables no differences (p > 0.05) were detected when comparing high vs. low-ranked rams.

and Figure 2. The estrus response was similar in both groups of ewes (p > 0.05); likewise, the ovarian response was similar (p > 0.05) between groups. However, a shorter interval to estrus was observed in ewes exposed to HHR than LHR (p < 0.05). This difference is observed in Figure 2, where the cumulative percentage of ewes that showed estrus was higher in ewes exposed to HHR after 96 h of joining than ewes in contact with LHR.

4. Discussion

During the success index test, more AG and MO behaviors were observed in HHR than LHR. When comparing these results with the CSB and SRI tests they were similar. These two variables are tangible indicators for both tests. By performing the social rank test, the MO and AG of rams could be determined without the need to run an additional CSB and SRI test. An index of 0.57 is high enough to classify rams as high-ranking animals, which differs from the values of Alvarez et al. [13], who established a high social status above an index of 0.66. However, the present study agrees with the aforementioned author, in that values below 0.33 are low indexes.

HHR had more than 65% consummatory behaviors, which indicates that ewes exposed to HHR had a higher quality–quantity socio-sexual stimulation, generating a rapid response of ewes to these rams. This response partially agrees with previous results where Dorper rams given exogenous testosterone, and presumably with stronger sexual stimuli toward ewes, markedly increased ewes in estrus, the interval from joining to onset of estrus, duration of estrus, and ewes ovulating [25].

An interesting finding was that flehmen behavior is similar in ASF and ASU, which are greater than WSF behaviors regardless of social rank. This can be attributed to the fact that for ASU and ASF, there was physical contact with the ewes, which may stimulate the expression of flehmen because sheep urine is a source of chemical information that conveys sexual receptivity clues to rams [26]. Flehmen behavior is associated with incentives of pheromones from the urine, wherein by the act of smelling the perianal region or urine, the flehmen response is triggered [27]. In addition to confirming the ewe’s sexual responsiveness, this behavior enhances the male’s libido to perform other sexual activities during courtship and copulation [28]

A greater number of ASB behaviors were observed during the morning regardless of social rank, and a greater number of CSB behaviors only in the HHR. These findings are in line with previous studies where Hair rams were more sexually active during daytime [29]. This is probably due to a variation in testosterone production as this hormone exhibits a circadian rhythm. For example, Bremner et al. [30] mention that young men show a circadian rhythm in serum testosterone, with levels higher around 08:00 h and lower levels in the late afternoon, which would explain this difference in rams in the present study. High hierarchy rams have higher plasma testosterone concentrations [31], which is responsible for rams’ sexual drive and smell, essential to generate a more potent stimulus to induce estrus in anestrus ewes [32].

Rams with stronger sexual behavior stimulate more anestrus ewes to become in estrus, accelerating this response [21]. On the other hand, HHR during the reproductive season present higher blood testosterone concentrations than subordinate mates [15]. Thus, in sheep, dominant rams have more successful mounts than LHR [33]. Usually, estrus females will mate with the dominant males but subordinate males are not excluded from reproduction [34]; however, it has been suggested that ewes express greater interest or spend more time near to LHR when the HHR rams’ behavior is restricted, because HHR tend to show more aggressive behaviors [11].

The sexual response of ewes to the introduction of rams was similar in both groups, indicating that stimulus from HHR and LHR was adequate to induce sexual activity in anestrus ewes. Indeed, more than 80% of ewes in both groups showed estrus during the first 10 days of stimulus. In addition, estrus of those ewes exposed to the ram stimulus was accompanied by ovulation, with more than 60% of ewes becoming pregnant. Nonetheless, there was a strong tendency towards a higher response from females exposed to HHR, this could be explained by the higher amount of CSB showed by this group. The CSB are more important for inducing estrus and ovulation in ewes due to a faster increase in LH and FSH, which in order elicits faster follicular waves that, in line, increases ovulation rate and enhances embryo survival [17,35]. In this regard, it is important to note that the Dorper breed has a mild sexual seasonality. Therefore, at any time of the year, rams of this breed have an adequate sexual behavior for inducing ovulation in anestrus ewes [36]. In fact, in sheep breeds with low reproductive seasonality, the male effect is efficient at any time of the year, as long as ewes are not cycling [37,38], as was the case of ewes in the present study.

The level of sexual behavior expressed by LHR was probably because these animals have always been in an intensive system where they do not experience undernutrition, which can significantly influence weight gain. Indeed, nutrition plays an essential role in the secretion of reproductive hormones; for example, when feeding is increased, plasma leptin concentrations increase, and these are correlated with an increase in the frequency of LH pulses [39]. However, although the sexual response was adequate in both groups of ewes, it is important to note that sheep exposed to low-ranking rams had a slower sexual response. A suboptimal quality could generate this delay in the estrus response in the sexual stimulation of the rams. However, it is worth mentioning that LHR rams have been more effective than HHR rams when mating ewes in estrus without competition [40].

5. Conclusions

Low-ranked rams did not differ from high-ranked rams to stimulate sexual activity in non-estrual ewes; however, ewes exposed to low-ranked rams showed a slower sexual response. Likewise, low-ranked rams were equally effective in inducing ovulation and impregnating ewes as high-ranked rams did. Regardless of socio-sexual hierarchy, appetitive behavior was greater in the mornings than in the afternoon.