Hostname: page-component-78c5997874-4rdpn Total loading time: 0 Render date: 2024-11-04T16:44:54.677Z Has data issue: false hasContentIssue false
  • English
  • Français

The continuous presence of ewes in estrus in spring influences testicular volume, testicular echogenicity and testosterone concentration, but not LH pulsatility in rams

Published online by Cambridge University Press:  16 June 2020

J. A. Abecia Open the ORCID record for J. A. Abecia [Opens in a new window] ,
M. Carvajal-Serna ,
A. Casao ,
C. Palacios ,
L. Pulinas ,
M. Keller ,
P. Chemineau  and
J. A. Delgadillo
J. A. Abecia*
Affiliation:
IUCA, Departamento de Producción Animal y Ciencia de los Alimentos, Universidad de Zaragoza, Miguel Servet, 177, 50013Zaragoza, Spain
M. Carvajal-Serna
Affiliation:
IUCA, Departamento de Producción Animal y Ciencia de los Alimentos, Universidad de Zaragoza, Miguel Servet, 177, 50013Zaragoza, Spain
A. Casao
Affiliation:
IUCA, Departamento de Producción Animal y Ciencia de los Alimentos, Universidad de Zaragoza, Miguel Servet, 177, 50013Zaragoza, Spain
C. Palacios
Affiliation:
Departamento de Construcción y Agronomía, Facultad de Ciencias Agrarias y Ambientales, Avenida Filiberto Villalobos, 119, 37007Salamanca, Spain
L. Pulinas
Affiliation:
Department of Veterinary Medicine, University of Sassari, Via Vienna 2, 07100Sassari, Italy
M. Keller
Affiliation:
Physiologie de la Reproduction et des Comportements, UMR INRA, CNRS, Université de Tours, IFCE, Agreenium, 37380Nouzilly, France
P. Chemineau
Affiliation:
Physiologie de la Reproduction et des Comportements, UMR INRA, CNRS, Université de Tours, IFCE, Agreenium, 37380Nouzilly, France
J. A. Delgadillo
Affiliation:
Centro de Investigación en Reproducción Caprina, Universidad Autónoma Agraria Antonio Narro, Periférico Raúl López Sánchez y Carretera a Santa Fe, C.P. 27054, Torreón, Coahuila, Mexico
*
†E-mail: alf@unizar.es
Get access

Abstract

The continuous presence of active male small ruminants prevents seasonal anestrus in females, but evidence of the same mechanism operating from the females to the males is scarce. This study assessed the effects of the continuous presence of ewes in estrus in spring on ram sexual activity, testicular size and echogenicity, and LH and testosterone concentrations. On 1 March, 20 rams were assigned to two groups (n = 10 each): isolated (ISO) from other sheep, or stimulated (STI) by 12 ewes, which were separated from the rams by an openwork metal barrier, allowing contact between sexes. Each week, four ewes were induced into estrus by intravaginal sponges. Live weight, scrotal circumference, testicular width (TW) and length (TL) were recorded at the beginning and at the end of the experiment, and testicular volume (TV) was calculated; at the same time, testicular ultrasonography and color Doppler scanning were performed. Blood samples (March to May) were collected once per week for testosterone determinations, and at the end of the experiment, blood samples were collected for 6 h at 20-min intervals for LH analysis. Rams were exposed to four estrous ewes in a serving-capacity test. Scrotal circumference, TW and TL were higher in the STI than in the ISO rams (P < 0.05) in May, and TV was higher (P < 0.05) in the STI (391 ± 17 cm3) than in the ISO rams (354 ± 24 cm3). In ISO rams, the number of white pixels was higher (P < 0.01) in May (348 ± 74) than in March (94 ± 21) and differed significantly (P < 0.01) from that of the STI rams in May (160 ± 33). In ISO rams, the number of grey pixels was higher (P < 0.05) in May (107 ± 3) than it was in March (99 ± 1). Stimulated and ISO rams did not differ significantly in mean LH plasma concentrations (0.8 ± 0.5 v. 0.9 ± 0.4 ng/ml), LH pulses (2.1 ± 0.5 v. 2.2 ± 0.2) and amplitude (2.0 ± 0.4 v. 3.2 ± 0.7 ng/ml, respectively). Stimulated rams had significantly higher testosterone concentrations than ISO rams from April to the end of the experiment. Stimulated rams performed more (P < 0.05) mountings with intromission (3.0 ± 0.4) than did ISO rams (1.5 ± 0.5). In conclusion, after 3 months in the continuous presence of ewes in estrus in spring, rams had higher TV and some testicular echogenic parameters were modified than isolated rams. Although exposed rams also had higher levels of testosterone after 2 months in the presence of estrous ewes, their LH pulsatility at the end of the study was not modified.

Keywords

sheepsocio-sexual signalsanestrushormonestesticle
Type
Research Article
Information
animal , Volume 14 , Issue 12 , December 2020 , pp. 2554 - 2561
Copyright
© The Author(s), 2020. Published by Cambridge University Press on behalf of The Animal Consortium

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abecia, JA, Forcada, F and Zuñiga, O 2002. A note on the effect of individual housing conditions on LH secretion in ewes after exposure to a ram. Applied Animal Behaviour Science 75, 347–352.Google Scholar
Abecia, JA, Chemineau, P, Flores, JA, Keller, M, Duarte, G, Forcada, F and Delgadillo, JA 2015. Continuous exposure to sexually active rams extends estrous activity in ewes in spring. Theriogenology 84, 1549–1555.CrossRefGoogle ScholarPubMed
Abecia, JA, Chemineau, P, Gómez, A, Palacios, C, Keller, M and Delgadillo, JA 2017. Exposure to photoperiod-melatonin-induced, sexually-activated rams after weaning advances the resumption of sexual activity in post-partum Mediterranean ewes lambing in January. Veterinary Science 4, 4.CrossRefGoogle ScholarPubMed
Abecia, JA, Araya, J, Chemineau, P, Palacios, C, Keller, M and Delgadillo, JA 2018. Photoperiod-melatonin-induced, sexually-activated rams increase pregnancy rate and number of lambs per ewe in a ram effect. Large Animal Review 24, 31–35.Google Scholar
Abecia, JA, Gave, M, García, AI, Casao, A, Carvajal-Serna, M, Palacios, C, Keller, M, Chemineau, P and Delgadillo, JA 2019a. Long days in winter or the presence of adult sexually active rams did not influence the timing of puberty of autumn-born Rasa Aragonesa ram lambs. Biological Rhythm Research. doi: 10.1080/09291016.2019.1613321.CrossRefGoogle Scholar
Abecia, JA, Keller, M, Palacios, C, Chemineau, P and Delgadillo, JA 2019b. Light-induced sexually active rams prevent the seasonal inhibition of luteinizing-hormone in ovariectomized estradiol-implanted ewes. Theriogenology 136, 43–46.CrossRefGoogle ScholarPubMed
Batissaco, L, Celeghini, ECC, Pinafei, FLV, Oliveria, BMM, Andrade, AFC, Recalde, ECS and Fernandes, CBF 2013. Correlations between testicular hemodynamic and sperm characteristics in rams. Brazilian Journal of Veterinary Research and Animal Science 50, 384–395.CrossRefGoogle Scholar
Calderón-Leyva, G, Meza-Herrera, CA, Martinez-Rodriguez, R, Angel-García, O, Rivas-Muñoz, R, Delgado-Bermejo, JV and Véliz-Deras, FG 2018. Influence of sexual behavior of Dorper rams treated with glutamate and/or testosterone on reproductive performance of anovulatory ewes. Theriogenology 106, 79–86.CrossRefGoogle ScholarPubMed
Carvajal-Serna, M, Santorroman, M, Barale, J, Cardozo, J, Cebrian-Perez, JA, Muiño-Blanco, T, Abecia, JA, Perez-Pe, R and Casao, A 2019. Monthly changes in testicular ultrasonography and their association with ram sperm quality. Reproduction in Domestic Animals 54, 1–149.Google Scholar
Damián, JP, Beracochea, F, Hötzel, MJ, Banchero, G and Ungerfeld, R 2015. Reproductive and sexual behaviour development of dam or artificially reared male lambs. Physiology & Behavior 147, 47–53.CrossRefGoogle ScholarPubMed
Delgadillo, JA, Flores, JA, Hernández, H, Poindron, P, Keller, M, Fitz-Rodríguez, G, Duarte, G, Vielma, J, Fernández, IG and Chemineau, P 2015. Sexually active males prevent the display of seasonal anestrus in female goats. Hormones and Behavior 69, 8–15.Google ScholarPubMed
D’Occhio, MJ and Brooks, DE 1982. Threshold of plasma testosterone required for normal mating activity in male sheep. Hormones and Behavior 16, 383–394.CrossRefGoogle ScholarPubMed
El-Zelaky, OA, Khalifa, EI, Mohamed, AH, Bahera, KM and Hussein, AM 2011. Productive and reproductive performance of Rahmani male lambs fed rations containing Jatropha cake. Egyptian Journal of Sheep and Goats Sciences 6, 15–24.Google Scholar
Faure, MO, Nicol, L, Fabre, S, Fauntaine, J, Mohoric, N, McNeilly, A and Taragnat, C 2005. BMP-4 inhibits follicle-stimulating hormone secretion in Ewe pituitary. Journal of Endocrinology 186, 109e21.CrossRefGoogle ScholarPubMed
Giriboni, J, Lacuesta, L and Ungerfeld, R 2017. Continuous contact with females in estrus throughout the year enhances testicular activity and improves seminal traits of male goats. Theriogenology 87, 284–289.CrossRefGoogle ScholarPubMed
González, R, Levy, F, Orgeur, P, Poindron, P and Signoret, JP 1991a. Female effect in sheep: II. Role of volatile substances from the sexually receptive female; implication of the sense of smell. Reproduction, Nutrition and Development 31, 103–109.CrossRefGoogle ScholarPubMed
González, R, Orgeur, P and Signoret, JP 1988. Luteinizing hormone, testosterone and cortisol responses in rams upon presentation of estrous females in the nonbreeding season. Theriogenology 30, 1075–1086.CrossRefGoogle ScholarPubMed
González, R, Orgeur, P, Poindron, P and Signoret, JP 1991b. Female effect in sheep: I. The effects of sexual receptivity of females and the sexual experience of rams. Reproduction, Nutrition and Development 31, 97–102.CrossRefGoogle ScholarPubMed
Hawken, PAR and Martin, GB 2012. Sociosexual stimuli and gonadotropin-releasing hormone/luteinizing hormone secretion in sheep and goats. Domestic Animal Endocrinology 43, 85–94.Google ScholarPubMed
Hedia, MG, El-Belely, MS, Ismail, ST and Abo El-Maaty, AM 2019. Monthly changes in testicular blood flow dynamics and their association with testicular volume, plasma steroid hormones profile and semen characteristics in rams. Theriogenology 123, 68–73.CrossRefGoogle ScholarPubMed
Hochereau-de Reviers, MT, Copin, M, Seck, M, Monet-Kuntz, M, Cornu, C, Fontaine, C, Perreau, C, Elsen, JM and Boomarov, O 1990. Stimulation of testosterone production by PMSG injection in the ovine male: effect of breed and age and application to males carrying or not carrying the F Booroola gene. Animal Reproduction Science 23, 21–32.CrossRefGoogle Scholar
Kilgour, RJ and Whale, RG 1980. The relation between mating activity of rams in pens and subsequent flock mating performance. Australian Journal of Experimental Agriculture 20, 5–8.CrossRefGoogle Scholar
Knight, TW and Lynch, PR 1980. Source of ram pheromones that stimulate ovulation in the ewe. Animal Reproduction Science 3, 133–136.CrossRefGoogle Scholar
María, G, Valares, JA, Forcada, F and Abecia, JA 2015. Sheep as an experimental model: individual housing allowing visual, auditory, olfactory and tactile contact is not an obstacle for studies involving hormonal interrelationships. Scavian Journal of Laboratory Animal Science 41, 1–9.Google Scholar
Martin, G, Oldham, C, Cognie, Y and Pearce, D 1986. The physiological responses of anovulatory ewes to the introduction of rams: a review. Livestock Production Science 15, 219–247.CrossRefGoogle Scholar
Muñoz, AL, Chesneau, D, Hernández, H, Bedos, M, Duarte, G, Vielma, J, Zarazaga, LA, Chemineau, P, Keller, M and Delgadillo, JA 2017. Sexually active bucks counterbalance the seasonal negative feedback of estradiol on LH in ovariectomized goats. Domestic Animal Endocrinology 60, 42–49.CrossRefGoogle ScholarPubMed
Ortavant, R, Pelletier, J, Ravault, JP, Thimonier, J and Volland-Nail, P 1985. Photoperiod: main proximal and distal factor of the circannual cycle of reproduction in farm animals. Oxford Reviews of Reproductive Biology 7, 305–345.Google Scholar
Ortiz-Rodriguez, M, Anel-Lopez, L, Martín-Muñoz, P, Álvarez, M, Gaitskell-Phillips, G, Anel, L, Rodríguez-Medina, P, Peña, J and Ortega Ferrusola, C 2017. Pulse Doppler ultrasound as a tool for the diagnosis of chronic testicular dysfunction in stallions. PLoS ONE 12, e0175878.Google Scholar
Perkins, A and Fitzgerald, JA 1994. The behavioral component of the ram effect: the influence of ram sexual behavior on the induction of estrus in anovulatory ewes. Journal of Animal Science 72, 51–55.Google ScholarPubMed
Ramírez, S, Hernández, H, Mendieta, ES, Nandayapa, E, Keller, M and Delgadillo, JA 2017. La presencia de cabras en estro mejora el comportamiento sexual de los machos cabríos durante el reposo sexual. In Proceedings of the XVII Jornadas sobre Producción Animal, 30–31 May 2017, Zaragoza, Spain, pp. 356–358.Google Scholar
Ramírez, S, Chesneau, D, Grimaldo-Viesca, G, Vielma, J, Hernández, H, Santiago-Moreno, J, Chemineau, P, Keller, M and Delgadillo, JA 2019. Continuous presence of females in estrus does not prevent seasonal inhibition of LH and androgen concentrations in bucks. Domestic Animal Endocrinology 69, 68–74.CrossRefGoogle Scholar
Rodríguez Iglesias, RM, Ciccioli, NH, Irazoqui, H and Rodríguez, BT 1991. Importance of behavioural stimuli in ram-induced ovulation in seasonally anovular Corriedale ewes. Applied Animal Behaviour Science 30, 323–332.CrossRefGoogle Scholar
Samir, H, Nyametease, P, Nagaoka, K and Watanabe, G 2018. Effect of seasonality on testicular blood flow as determined by color Doppler ultrasonography and hormonal profiles in Shiba goats. Animal Reproduction Science 197, 185–192.CrossRefGoogle ScholarPubMed
Schanbacher, BD, Orgeur, P, Pelletier, J and Signoret, JP 1987. Behavioural and hormonal responses of sexually-experienced Ile-de-France rams to oestrous females. Animal Reproduction Science 14, 293–300.Google Scholar
Ungerfeld, R and Silva, L 2004. Ewe effect: endocrine and testicular changes in experienced adult and inexperienced young Corriedale rams used for the ram effect. Animal Reproduction Science 80, 251–259.Google ScholarPubMed
Ungerfeld, R and Fila, D 2011. Testicular fluid content and scrotal surface temperature increase with rams’ sexual activity. Reproduction in Domestic Animals 47, e56–8.CrossRefGoogle ScholarPubMed
Vidal, A, Zhang, Q, Médigue, C, Fabre, S and Clément, F 2012. DynPeak: an algorithm for pulse detection and frequency analysis in hormonal time series. PLoS ONE 7, e39001.Google ScholarPubMed
Yeates, NTM 1949. The breeding season of the sheep with particular reference to its modification by artificial means using light. Journal of Agricultural Science 39, 1–43.CrossRefGoogle Scholar