Abstract
The aim was to compare some stress responses to electroejaculation (EE), and the quality of fresh semen, when ram semen is collected at dawn (06:00 h), noon (12:00 h), or evening (18:00 h). Twelve Corriedale rams were used, and semen was collected from four rams at each study time on three different days, with a Latin-square design. The time required for EE, the number of vocalizations emitted, heart rate, and rectal temperature were recorded, and fresh semen was evaluated. The time required for EE was shorter at evening than at dawn and noon (399.3 s, 480.6 s, and 460.2 s respectively; pooled SEM = 72.1; P = 0.03). The percentage of sperm with progressive motility was greater at noon than dawn (59.7% and 50.3%; pooled SEM = 5.8; P = 0.05). Curvilinear velocity was greater at dawn than evening (117.0 µm/s and 95.5 µm/s; pooled SEM = 7.1; P = 0.04), slow linear velocity was greater at evening than at dawn and noon (13.1 µm/s, 9.3 µm/s, and 8.5 µm/s respectively; pooled SEM = 1.7, P = 0.05), and the slow average path velocity was greater at evening than dawn and noon (16.2 µm/s, 11.7 µm/s, and 10.8 µm/s respectively; pooled SEM = 1.9, P = 0.05). In conclusion, the collection time modified the time required for electroejaculation and had only slight effects on the quality of fresh semen. Overall, the time of the day appears to have only slight effects on semen collection and quality.
Similar content being viewed by others
Data availability
The datasets generated and/or analyzed during the current study are available from the corresponding author at reasonable request.
References
Abril-Sánchez, S., Freitas-de-Melo, A., Damián, J.P., Giriboni, J., Villagrá-García, A., Ungerfeld, R., 2017. Ejaculation does not contribute to the stress response to electroejaculation in sheep. Reproduction in Domestic Animals, 52, 403-408. https://doi.org/10.1111/rda.12922
Abril-Sánchez, S., Freitas-de-Melo, A., Giriboni, J., Santiago-Moreno, J., Ungerfeld, R., 2019. Sperm collection by electroejaculation in small ruminants: A review on welfare problems and alternative techniques. Animal Reproduction Science, 205, 1-9. https://doi.org/10.1016/j.anireprosci.2019.03.023
Aquila, S., Middea, E., Catalano, S., Marsico, S., Lanzino, M., Casaburi, I., 2007. Human sperm express a functional androgen receptor: effects on PI3K/AKT pathway. Human Reproduction, 22, 2594– 2605. https://doi.org/10.1093/humrep/dem243
Arthur, G.H., 2001. Veterinary Reproduction and Obstetrics. 8th edition. London: Saunders.
Austin, J., Hupp, E., Murphree, R., 1961. Comparison of quality of bull semen collected in the artificial vagina and by electroejaculation. Journal Dairy Science, 44, 2292-2297.
Ax, R.L., Dally, M.R., Didion, B.A., Lenz, R.W., Love, C.C., Varner, D.D., Hafez, B., Bellin, M.E., 2000. Semen Evaluation. In: Hafez ESE and B. Hafez Editor. Reproduction in Farm Animal. 7th ed. USA: Lippincot Wiliams and Wilkins.
Bath, G., 1998. Management of pain in production animals. Applied Animal Behavior Science, 59, 147–156. https://doi.org/10.1016/s0168-1591(98)00129-4
Bribiescas, R.G., Hill, K.R., 2010. Circadian Variation in Salivary Testosterone Across Age Classes in Ache Amerindian Males of Paraguay. American Journal of Human Biology. 22, 216–220. https://doi.org/10.1002/ajhb.21012
Damián, J.P., Beracochea, F., Hötzel, M.J., Banchero, G., Ungerfeld, R., 2015. Reproductive and sexual behaviour development of dam or artificially reared male lambs. Physiology. Behavior. 147, 47–53. https://doi.org/10.1016/j.physbeh.2015.04.004
Dawood, T., Williams, M.R., Fullerton, M.J., Myles, K., Schuijers, J., Funder, J.W., Krishnankutty, S., Komesaroff, P.A., 2005. Glucocorticoid responses to stress in castrate and testosterone–replaced rams. Regulatory Peptides, 125, 47–53. https://doi.org/10.1016/j.regpep.2004.07.030
De, K., Kumar, D., Saxena, V.K., Naqvi, S.M.K., 2017. Study of circadian rhythmicity of physiological response and skin temperature of sheep during summer and winter in semi-arid tropical environment. Physiology and Behavior, 169, 16–21. https://doi.org/10.1016/j.physbeh.2016.11.010
Evans, G., Maxwell, W.M.C., 1987. Salamon’s Artificial Insemination of Sheep and Goats. No. 2a ed. Butterworths, Sydney: Australia.
Fisher, R. A., 1925. Statistical Methods for Research Workers. First Edition. Edinburgh: Oliver and Boyd.
Fritz, W., Sena, L., Becker, S., Katz, L., 2019. Differential effects of androgens, estrogens and socio-sexual context on sexual behaviors in the castrated male goat. Hormones and Behavior, 109, 10-17. https://doi.org/10.1016/j.yhbeh.2019.01.008
Goeritz, F., Quest, M., Wagener, A., Fassbender, M., Broich, A., Hildebrandt, T., Hofmann, R., Blottner, S., 2003. Seasonal timing of sperm production in roe deer: interrelationship among changes in ejaculate parameters, morphology and function of testis and accessory glands. Theriogenology, 59, 1487-1502. https://doi.org/10.1016/s0093-691x(2)01201-3
Hatazoe, T., Kubota, C., Fujiki, M., Misumi, K., 2012. Mating behavior increases workload of the heart in Thoroughbred stallions. Journal of Veterinary Medical Science, 74, 423–428. https://doi.org/10.1292/jvms.11-0360
Hulet, C., Foote, W., Blackwell, R., 1964. Effects of natural and electrical ejaculation on predicting fertility in the ram. Journal Animal Science, 23, 418-424. https://doi.org/10.2527/jas1964.232418x
Jeyendran, R.S., Van der Ven, H.H., Perez-Pelaez, M., Crabo, B.G., Zaneveld, L.J.D., 1984. Development of an assay to assess the functional integrity of the human sperm membrane and its relationship to other semen characteristics. Journals of Reproduction & Fertility, 70, 219–228. https://doi.org/10.1530/jrf.0.0700219
Kasimanickam, V.R., Kasimanickam, R.K., Kastelic, J.P., Stevenson, J.S., 2013. Associations of adiponectin and fertility estimates in Holstein bulls. Theriogenology, 79, 766-777. https://doi.org/10.1016/j.theriogenology.2012.12.001
Kishk, W., 2008. Interrelationship between ram plasma testosterone level and some semen characteristics. Slovak Journal Animal Science, 41, 67-71.
Lacerda, L.D., Kowarski, A., Johanson, A.J., Athanasiou, R., Migeon, C.J., 1973. Integrated Concentration and Circadian Variation of Plasma Testosterone in Normal Men. The Journal of Clinical Endocrinology and Metabolism, 37, 366–371. https://doi.org/10.1210/jcem-37-3-366
Ledesma, A., 2018. Mejoramiento cualitativo de espermatozoides ovinos criopreservados a partir de la utilización de moléculas diferenciales del plasma seminal obtenidas por dos métodos de colecta seminal: electroeyaculador y vagina artificial. Tesis de doctorado. Universidad Nacional de Mar del Plata. Balcarce, Argentina.
Lincoln, G.A., Peet, M.J., 1977. Photoperiodic control of gonadotrophin secretion in the ram: a detailed study of the temporal changes in plasma levels of follicle-stimulating hormone, luteinizing hormone and testosterone following an abrupt switch from long to short days. Journal of Endocrinology, 74, 355-367. https://doi.org/10.1677/joe.0.0740355
Lincoln, G.A., Peet, M.J., Cunningham. R.A., 1977. Seasonal and circadian changes in the episodic release of follicle-stimulating hormone, luteinizing hormone and testosterone in rams exposed to artificial photoperiods. Journal of Endocrinology, 72, 337-349. https://doi.org/10.1677/joe.0.0720337
Liu, K., Meng, T., Chen, Q., Hou, G., Wang, X., Hu, S., Gu, X., Li, H., Li, Y., Xiong, C., Cao, J., 2022. Diurnal rhythm of human semen quality: analysis of large-scale human sperm bank data and timing-controlled laboratory study. Human Reproduction, 37, 1727-1738. https://doi.org/10.1093/humrep/deac135
Maxwell, W.M.C., Long, C.R., Johnson, L.A., Dobrinsky, J.R., Welch, G.R., 1998. The relationship between membrane status and fertility of boar spermatozoa after flow cytometric sorting in the presence or absence of seminal plasma. Reproduction, Fertility & Development, 10, 433-440. https://doi.org/10.1071/RD98102
Maxwell, W.M.C., De Graaf, S.P., El-Hajj Ghaoui, R., Evans, G., 2007. Seminal plasma effects on sperm handling and female fertility. Society for Reproduction and Fertility Supplement, 64, 13-38. https://doi.org/10.5661/rdr-vi-13
Morelli, A., Filippi, S., Mancina, R., Luconi, M., Vignozzi, L., Marini, M., Orlando, C., Vannelli, G.B., Aversa, A., Natali, A., Forti, G., Giorgi, M., Jannini, E.A., Ledda, F., Maggi, M., 2004. Androgens regulate phosphodiesterase type 5 expression and functional activity in corpora cavernosa. Endocrinology, 145, 2253–2263. https://doi.org/10.1210/en.2003-1699
Orihuela, A., Omaña, J.C., and Ungerfeld, R., 2016. Heart rate patterns during courtship and mating in rams and in estrous and nonestrous ewes (Ovis aries). Journal of Animal Science, 94, 556–562. https://doi.org/10.2527/jas2015-9425
Ortavant, R., Daveau, A., Garnier, D.H., Pelletier, J., De Reviers, M.M., Terqui, M., 1982. Diurnal variation in release of LH and testosterone in the ram. Journals of Reproduction & Fertility, 64, 347-353. https://doi.org/10.1530/jrf.0.0640347
Palmer, C.W., 2005. Welfare aspects of theriogenology: Investigating alternatives to electroejaculation of bulls. Theriogenology, 64, 469–479. https://doi.org/10.1016/j.theriogenology.2005.05.032
Pasing, S., Von Lewinski, M., Wulf, M., Erber, R., Aurich, C., 2013. Influence of semen collection on salivary cortisol release, heart rate, and heart rate variability in stallions. Theriogenology. 80, 256–261. https://doi.org/10.1016/j.theriogenology.2013.04.003
Perumal, P., De, A.K., Alyethodi, R.R., Savino, N., Khate, K., Vupru, K., Khan, M.H., 2021. Daily and seasonal rhythmic secretary pattern of endocrinological profiles in Mithun bull. Theriogenology, 166, 46-54. https://doi.org/10.1016/j.theriogenology.2021.02.017
Piccione, G., Caola, G., Refinetti, R., 2002. Circadian modulation of starvation-induced hypothermia in sheep and goats. Chronobiology International, 19, 531-541. https://doi.org/10.1081/CBI-120004225
Pinto-Santini, L., Ungerfeld, R., 2019. The phase of the estrous cycle modifies the endocrine, metabolic and behavior rhythms in ewes. Physiology and Behavior, 204, 324-335. https://doi.org/10.1016/j.physbeh.2019.03.011
Pinto-Santini, L., Pérez-Clariget, R., Ungerfeld, R., 2022. Does the metabolic and behavior daily variation pattern on rams differ in summer and winter? Biological Rhythm Research, https://doi.org/10.1080/09291016.2022.2129541
Reiter, E., McNamara, M., Closset, J., Hennen, G., 1995. Expression and functionality of luteinizing hormone/chorionic gonadotropin receptor in the rat prostate. Endocrinology, 136, 917–923. https://doi.org/10.1210/endo.136.3.7867600
Santolaria, P., Vicente-Fiel, S., Palacín, I., Fantova, E., Blasco, M.E., Silvestre, M.A., Yániz, J.L. 2015. Predictive capacity of sperm quality parameters and sperm subpopulations on field fertility after artificial insemination in sheep. Animal Reproduction Science, 163, 82–88. https://doi.org/10.1016/j.anireprosci.2015.10.001
Solakidi, S., Psarra, A.M., Nikolaropoulos, S., Sekeris, C.E., 2005. Estrogen receptors alpha and beta (ERalpha and ERbeta) and androgen receptor (AR) in human sperm: localization of ERbeta and AR in mitochondria of the midpiece. Human Reproduction, 20, 3481– 3487. https://doi.org/10.1093/humrep/dei267
Soleilhavoup, C., Tsikis, G., Labas, V., Harichaux, G., Kohnke, P.L., Dacheux, J.L., Guerin, Y., Gatti, J.L., De Graaf, S.P., Druart, X., 2014. Ram seminal plasma proteome and its impact on liquid preservation of spermatozoa. Journal of proteomics, 109, 245-60. https://doi.org/10.1016/j.jprot.2014.07.007
Stafford, K.J., Spoorenberg, J., West, D.M., Vermunt, J.J., Petrie, N., Lawoko, C.R., 1996. The effect of electro-ejaculation on aversive behavior and plasma cortisol concentration in rams. New Zealand Veterinary Journal, 44, 95–98. https://doi.org/10.1080/00480169.1996.35943
Tao, Y.X., Lei, Z.M., Rao, C.V., 1998. Seminal vesicles are novel sites of luteinizing hormone/human chorionic gonadotropin—receptor gene expression. Journal of Andrology, 19, 343–347. https://doi.org/10.1002/j.1939-4640.1998.tb02014.x
Thun, R., Eggenberger, E., Zerobin, K., Luscher, T., Vetter, W., 1981. Twenty-four-hour secretory pattern of cortisol in the bull: evidence of episodic secretion and circadian rhythm. Endocrinology, 109, 2208-2212. https://doi.org/10.1210/endo-109-6-2208
Ungerfeld, R., González-Pensado, S.P., 2008. Social rank affects reproductive development in male lambs. Animal Reproduction Science 109, 161–171. https://doi.org/10.1016/j.anireprosci.2007.12.006
Ungerfeld, R., 2012. Seasonal reproductive patterns and effectiveness as teasers (ram effect) of Corriedale and Milchschaf rams. Animal Production Science 52, 1036- https://doi.org/10.1071/AN12114
Vandenheede, M., Bouissou, M.F., 1993. Effect of androgen treatment on fear reactions in ewes. Hormones and Behavior, 27, 435–448. 10.1006/ hbeh.1993.1032
Vicente-Fiel, S., Palacín, I., Santolaria, P., Fantova, E., Quintín-Casorrán, F.J., Sevilla-Mur, E., Yániz, J.L., 2014. In vitro assessment of sperm quality from rams of high and low field fertility. Animal Reproduction Science, 146, 15-20. https://doi.org/10.1016/j.anireprosci.2014.02.005
Wilk, M.B., and Kempthorne, O., 1957. Non-Additives in a Latin Square Design. Journal of the American Statistical Association, 52, 218–236. https://doi.org/10.2307/2280847
Xie, M., Utzinger K.S., Blickenstorfer, K., Leeners, B., 2018. Diurnal and seasonal changes in semen quality of men in subfertile partnerships. Chronobiology International. 35, 1375-1384. https://doi.org/10.1080/07420528.2018.1483942
Yarney, T.A., Sanford, L.M., 1983. The reproductive endocrine response of adult rams to sexual encounters with estrual ewes is season dependent. Hormones and Behavior, 17, 169-182. https://doi.org/10.1016/0018-506X(83)90005-3
Acknowledgements
We acknowledge Sofía Rodríguez for helping in the laboratory, Augusto Ryonosuke and Juliana Dantas for helping in the semen collection, and Milton Pintos, Nadia Carballo, and María Pedrozo for the handling of the rams. We acknowledge INIFAP (Mexico), for supporting JC Orihuela studies in Uruguay.
Funding
We acknowledge and state “The research that gives rise to the results presented in this publication received funds from the Agencia Nacional de Investigación e Innovación under the code POS_NAC_D_2020_1_164576”.
Author information
Authors and Affiliations
Contributions
J.C. Orihuela: study design, coordination and development of the experiment, analysis and data interpretation, and writing of the manuscript. L. Pinto-Santini, F. Beracochea, J. Giriboni, and M. Viera: development of the experiment, critical review with important contributions to the manuscript. P. Siveira: sample analysis and review of the manuscript. R. Ungerfeld: study design, development of the experiment, review of data analysis and interpretation, and review and writing of the manuscript.
Corresponding author
Ethics declarations
Ethics approval
This study was performed as part of a PhD project. Approval was granted by the Comisión de Ética en el Uso de Animales (CEUA Ethical Committee) of the Facultad de Veterinaria of the Universidad de la República, Uruguay.
Consent to participate
All authors read and approved the final manuscript.
Consent for publication
All authors have agreed to the publish manuscript.
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Orihuela, J.C., Pinto-Santini, L., Beracochea, F. et al. Time of day modified the time required for semen collection with electroejaculation and slightly affected the quality of fresh semen in rams. Trop Anim Health Prod 55, 144 (2023). https://doi.org/10.1007/s11250-023-03564-w
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11250-023-03564-w