Scrotal thermography to assess the seminal quality in Nelore and Girolando bulls
DOI:
https://doi.org/10.5433/1679-0359.2020v41n1p131Keywords:
Infrared thermography, Testicular thermoregulation, Semen freezing, Bovine bulls.Abstract
Bull selection by andrological examination aims to estimate the reproductive capacity of the male. Bulls of zebu origin adapt better to high temperatures than bulls of taurine origin, which may influence scrotum temperature and seminal quality due to the imbalance of testicular thermoregulation. The objective of this study was to investigate the relationship between bioclimatic variables, the temperature of body and scrotal areas, assessed with infrared thermography, and the quality of fresh and post-thawed semen in zebu Nelore bulls (Bos taurus indicus) and Girolando bulls (Bos taurus taurus x Bos taurus indicus). Bulls were kept in pickets with access to water, mineral mix and a diet supplemented with concentrate. Infrared thermographs of the scrotum, orbital globe and muzzle were performed twice a week with a Flir E40 thermal imager. For scrotal thermograms, we analyzed the temperatures of the spermatic cord, proximal and distal portion of the testes and tail of the epididymis using the Flir Tools software. Samples were collected using an artificial vagina and the ejaculates were processed and frozen in liquid nitrogen until further analyses. Data were analyzed with the Tukey test or the Kruskall-Wallis test, depending on their normal distribution. Our results showed differences (p < 0.05) between the two breeds regarding the temperature in the ocular globe, spermatic cord and proximal portion of the scrotum. Nelore bulls presented lower temperature in the body and in certain regions of the scrotum compared to Girolando bulls. Seminal characteristics varied between breeds, with the Nelore breed presenting better semen. Positive correlations were observed between minor sperm defects and ventral regions of the testes and tails of the epididymis in Girolando bulls. Nelore bulls were less influenced by climatic variables and presented lower temperature in skin surface areas in the infrared thermography examination compared to Girolando bulls. Nelore bulls presented superior semen quality in both fresh and thawed samples than Girolando bulls.References
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Brito, L. F. C., Silva, A. E. D., Barbosa, R. T. & Kastelic, J. P. (2004). Testicular thermoregulation in Bos indicus, crossbred and Bos taurus bulls: relationship with scrotal, testicular vascular cone and testicular morphology, and effects on semen quality and sperm production. Theriogenology, 61(2-3), 511-528. doi: 10.1016/S0093-691X(03)00231-0
Carvalhal, M. V. L., & Costa, F. O. (2018). Principais aspectos sobre bem-estar de touros mantidos em centrais de coleta de sêmen. Revista Brasileira de Zoociências, 19(2), 249-264.
Chacur, M. G. M., Miyasaki, A. A., Oba, E., Souza, C. D., & Gabriel, L. R. A., F°. (2017). Body and testicular development and serum testosterone concentrations in Brahman males. Semina: Ciências Agrárias, 38(4), 2561-2579. doi: 10.5433/1679-0359.2017v38n4Supl1p2561
Chacur, M. G. M., Souza, C. D., Andrade, I. B., Pepino, G., Bastos, F. L. G. D., Souza, M. G. R., & Marques, A. D. P., Jr. (2016). Aplicações da termografia por infravermelho na reprodução animal e bem-estar em animais domésticos e silvestres. Revista Brasileira de Reprodução Animal, 40(3), 88-94.
Chacur, M. G. M., Aurélio, P. T. F., Oba, E., Laposy, C. B., Scalon, O., Jr., Inague, L., & Kronka, S. N. (2010). Influency of one nutraceutic on semen, testosterone, cortisol, eritrogram and body weight in young bulls Bos taurus indicus. Semina: Ciências Agrárias, 31(2), 439-450. doi: 10.5433/1679-0359.2010v31n2p439
Chacur, M. G. M., Machado, N. B., Neto, & Cristancho, D. R. (2006). Winter-springer and Summer influence upon seminal plasma proteins in bulls. Animal Reproduction, 3(2), 251-260.
Colégio Brasileiro de Reprodução Animal [CBRA]. (2013). Procedimentos para exame andrológico e avaliação de sêmen animal. Belo Horizonte: CBRA.
Coulter, G. H., Serenger, P. L., & Bailey, D. R. C. (1988). Relationship of scrotal surface temperature measured by infrared thermography to subcutaneous and deep testicular temperature in the ram. Journal of Reproduction and Fertility, 84(2), 417-423.
Despopoulos, A. (2003). Completely revised and expanded. Color Atlas of Physiology (5th ed.). Stuttgart: Thieme.
Instituto Brasileiro de Geografia e Estatística [IBGE]. (2015). PPM 2014: rebanho bovino alcança 212,3 milhões de cabeças. Recuperado de http://saladeimprensa.ibge.gov.br/noticias.html?view=noticia&id =1&idnoticia=3006&busca=1&t=ppm-2014-rebanho-bovino-alcanca-212-3-milhoes-cabecas
Kastelic, J. P. (2014). Understanding and evaluating bovine testes. Theriogenology, 81(1), 18-23. doi: 10.1016/j.theriogenology.2013.09.001
Kastelic, J. P., Wilde, R. E., Rizzoto, G., & Thundathil, J. C. (2017). Hyperthermia and not hypoxia may reduce sperm motility and morphology following testicular hyperthermia. Veterinarni Medicina, 62, 437-442. doi: 10.17221/124/2016-VETMED
Knizkova, I., Kunc, P., Gurdil, G. A. K., Pinar, Y., & Selvi, K. C. (2007). Applications of infrared thermography in animal production. Journal of Faculty of Agriculture, 22(3), 329-336.
Köppen, W., & Geiger, R. (1928). Klimate der Erde. Gotha: Verlag Justus Perthes. [Wall-map 150cmx200cm].
Levine, D. M., Berenson, M. L., & Stephan, D. (2012). Estatística: teoria e aplicações (6th ed.). Rio de Janeiro: LTC.
Losano, J. D. A, Angrinami, D. S. R., Dalmazzo, A., Rocha, C. C., Brito, M. M., Perez, E. G. A.,... Nichi, M. (2018). Efect of Vitamin E and polyunsaturated fatty acids on cryopreserved sperm quality in Bos taurus bulls under testicular heat stress. Animal biotechnology, 39(2), 100-109. doi: 10.1080/10495398.2017.1322973
Marai, I. F. M., El-Darawany, A. A., Fadiel, A., & Abdel-Hafez, M. A. M. (2008) Reproductive performance traits as affected by heat stress and its alleviation in sheep. Tropical and Subtropical Agroecosystems, 8, 209-234.
Menegassi, S. R. O., Barcellos, J. O. J., Lampert, V. N., Borges, J. B. S., & Peripolli, V. (2011). Bioeconomic impact of bull breeding soundness examination in cow-calf systems. Revista Brasileira de Zootecnia, 40(2), 441-447. doi: 10.1590/S1516-35982011000200028
Moreira, G. M. (2016). Primeiro estudo do uso de termografia escrotal em touros Girolando e sua relação com a classificação andrológica por pontos. Dissertação de Mestrado, Universidade Federal de Lavras, Lavras, Brasil.
Nogueira, F. R. B., Souza, B. B., Carvalho, M. G. X., Garino, F. Jr., Marques A. V. M. S., & Leite, R. F. (2013). Termografia infravermelha: uma ferramenta para auxiliar no diagnóstico e prognóstico de mastite em ovelha. Revista Brasileira de Medicina Veterinária, 35(3), 289-297.
Paul, C., Teng, S., & Saunders, P. T. K. (2009). A single, mild, transient scrotal heat stress causes hypoxia and oxidative stress in mouse testes, which induces germ cell death. Biology of Reproduction, 80(5), 913-919. doi: 10.1095/biolreprod.108.071779
Perotto, D., Kroetz, I. A., & Rocha, J. L. (2010). Milk production of crossbred Holstein × Zebu cows in the northeastern of Paraná State. Revista Brasileira de Zootecnia, 39(4), 758-764. doi: 10.1590/S1516-35982010000400009
Renaudeau, D., Collin, A., Yahav, S., Basilio, V., Gourdine, J. L., & Collier, R. J. (2012). Adaptation to hot climate and strategies to alleviate heat stress. Livestock Production Animal, 6(5), 707-728. doi: 10.1017/S1751731111002448
Rhoads, M. L., Rhoads, R. P., Baale, M. J., Collier, R. J., Sanders, S. R., Weber, W. J.,… Baumgard, L. H. (2009). Effects of heat stress and plane of nutrition on lactating Holstein cows: I. Production, metabolism, and aspects of circulating somatotropin. Journal of Dairy Science, 92(5), 1986-1997. doi: 10.3168/jds.2008-1641
Ruediger, F. R., Chacur, M. G. M., Alves, F. C. P. E., Oba, E., & Ramos, A. A. (2016). Digital infrared thermography of the scrotum, semen quality, serum testosterone levels in Nellore bulls (Bos taurus indicus) and their correlation with climatic factors. Semina: Ciências Agrárias, 37(1), 221-232. doi: 10.5433/1679-0359.2016v37n1p221
Ruediger, F. R., Yamada, P. H., Barbosa, L. G. B., Chacur, M. G. M., Ferreira, J. C. P., Carvalho, N. A. T., & Oba, E. (2018). Effect of estrous cycle phase on vulvar, orbital area and muzzle surface temperatures as determined using digital infrared thermography in Murrah buffalo. Animal Reproduction Science, 197, 154-161. doi: 10.1016/j.anireprosci.2018.08.023
Statistical Analysis System (SAS). (2011). SAS/STAT user’s guide: statistics. v.9.3. Cary, NC: Statistical Analysis System.
Stewart, M. (2008). Non-invasive measurement of stress and pain in cattle using infrared thermography. Tesis, Animal Science, Massey University, Palmerston North, New Zealand.
Silva, R. G. D., & Pocay, P. L. B. (2001). Transmissão de radiação ultravioleta através do pelame e da epiderme de bovinos. Revista Brasileira de Zootecnia, 30(6), 1939-1947.
Sirchia, F. P. (2008). Relação entre circunferência escrotal, libido, hormônios e características do sêmen em touros Brangus e Pardo suíço. Dissertação de Mestrado, Universidade do Oeste Paulista, Presidente Prudente, SP, Brasil.
Souza, C. D., Chacur, M. G. M., Ruediger, F. R., Cartocci, J. S., Andrade, I. B., Bastos, G. P.,... Ramos, A. A. (2014). Termorregulação escrotal em touros Nelore (Bos taurus indicus). Colloquium Agrariae, 10, 101-106. doi: 10.5747/ca.2014.v10.nesp.000143
Swenson, M. J., Reece, W. O., & Dukes. (1996) Fisiologia dos animais domésticos. São Paulo: Guanabara Koogan.
Thom, E. C. (1959). The discomfort index. Weatherwise, 12(1), 57-60.
Weschenfelder, A. V., Saucier, L., Maldague, X., Rocha, L. M., Schaefer, A. L., & Faucitano, L. (2013). Use of infrared ocular thermography to assess physiological conditions of pigs prior to slaughter and predict pork quality variation. Meat Science, 95(3), 616-620. doi: 10.1016/j.meatsci.2013.06.003
Wheelock, J. B., Rhoads, R. P., Baale, M. J., Sanders, S. R., & Baumgard, L. H. (2010). Effects of heat stress on energetic metabolism in lactating Holstein cows. Journal of Dairy Science, 93(2), 644-655. doi: 10.3168/jds.2009-2295
Brito, L. F. C., Silva, A. E. D., Barbosa, R. T. & Kastelic, J. P. (2004). Testicular thermoregulation in Bos indicus, crossbred and Bos taurus bulls: relationship with scrotal, testicular vascular cone and testicular morphology, and effects on semen quality and sperm production. Theriogenology, 61(2-3), 511-528. doi: 10.1016/S0093-691X(03)00231-0
Carvalhal, M. V. L., & Costa, F. O. (2018). Principais aspectos sobre bem-estar de touros mantidos em centrais de coleta de sêmen. Revista Brasileira de Zoociências, 19(2), 249-264.
Chacur, M. G. M., Miyasaki, A. A., Oba, E., Souza, C. D., & Gabriel, L. R. A., F°. (2017). Body and testicular development and serum testosterone concentrations in Brahman males. Semina: Ciências Agrárias, 38(4), 2561-2579. doi: 10.5433/1679-0359.2017v38n4Supl1p2561
Chacur, M. G. M., Souza, C. D., Andrade, I. B., Pepino, G., Bastos, F. L. G. D., Souza, M. G. R., & Marques, A. D. P., Jr. (2016). Aplicações da termografia por infravermelho na reprodução animal e bem-estar em animais domésticos e silvestres. Revista Brasileira de Reprodução Animal, 40(3), 88-94.
Chacur, M. G. M., Aurélio, P. T. F., Oba, E., Laposy, C. B., Scalon, O., Jr., Inague, L., & Kronka, S. N. (2010). Influency of one nutraceutic on semen, testosterone, cortisol, eritrogram and body weight in young bulls Bos taurus indicus. Semina: Ciências Agrárias, 31(2), 439-450. doi: 10.5433/1679-0359.2010v31n2p439
Chacur, M. G. M., Machado, N. B., Neto, & Cristancho, D. R. (2006). Winter-springer and Summer influence upon seminal plasma proteins in bulls. Animal Reproduction, 3(2), 251-260.
Colégio Brasileiro de Reprodução Animal [CBRA]. (2013). Procedimentos para exame andrológico e avaliação de sêmen animal. Belo Horizonte: CBRA.
Coulter, G. H., Serenger, P. L., & Bailey, D. R. C. (1988). Relationship of scrotal surface temperature measured by infrared thermography to subcutaneous and deep testicular temperature in the ram. Journal of Reproduction and Fertility, 84(2), 417-423.
Despopoulos, A. (2003). Completely revised and expanded. Color Atlas of Physiology (5th ed.). Stuttgart: Thieme.
Instituto Brasileiro de Geografia e Estatística [IBGE]. (2015). PPM 2014: rebanho bovino alcança 212,3 milhões de cabeças. Recuperado de http://saladeimprensa.ibge.gov.br/noticias.html?view=noticia&id =1&idnoticia=3006&busca=1&t=ppm-2014-rebanho-bovino-alcanca-212-3-milhoes-cabecas
Kastelic, J. P. (2014). Understanding and evaluating bovine testes. Theriogenology, 81(1), 18-23. doi: 10.1016/j.theriogenology.2013.09.001
Kastelic, J. P., Wilde, R. E., Rizzoto, G., & Thundathil, J. C. (2017). Hyperthermia and not hypoxia may reduce sperm motility and morphology following testicular hyperthermia. Veterinarni Medicina, 62, 437-442. doi: 10.17221/124/2016-VETMED
Knizkova, I., Kunc, P., Gurdil, G. A. K., Pinar, Y., & Selvi, K. C. (2007). Applications of infrared thermography in animal production. Journal of Faculty of Agriculture, 22(3), 329-336.
Köppen, W., & Geiger, R. (1928). Klimate der Erde. Gotha: Verlag Justus Perthes. [Wall-map 150cmx200cm].
Levine, D. M., Berenson, M. L., & Stephan, D. (2012). Estatística: teoria e aplicações (6th ed.). Rio de Janeiro: LTC.
Losano, J. D. A, Angrinami, D. S. R., Dalmazzo, A., Rocha, C. C., Brito, M. M., Perez, E. G. A.,... Nichi, M. (2018). Efect of Vitamin E and polyunsaturated fatty acids on cryopreserved sperm quality in Bos taurus bulls under testicular heat stress. Animal biotechnology, 39(2), 100-109. doi: 10.1080/10495398.2017.1322973
Marai, I. F. M., El-Darawany, A. A., Fadiel, A., & Abdel-Hafez, M. A. M. (2008) Reproductive performance traits as affected by heat stress and its alleviation in sheep. Tropical and Subtropical Agroecosystems, 8, 209-234.
Menegassi, S. R. O., Barcellos, J. O. J., Lampert, V. N., Borges, J. B. S., & Peripolli, V. (2011). Bioeconomic impact of bull breeding soundness examination in cow-calf systems. Revista Brasileira de Zootecnia, 40(2), 441-447. doi: 10.1590/S1516-35982011000200028
Moreira, G. M. (2016). Primeiro estudo do uso de termografia escrotal em touros Girolando e sua relação com a classificação andrológica por pontos. Dissertação de Mestrado, Universidade Federal de Lavras, Lavras, Brasil.
Nogueira, F. R. B., Souza, B. B., Carvalho, M. G. X., Garino, F. Jr., Marques A. V. M. S., & Leite, R. F. (2013). Termografia infravermelha: uma ferramenta para auxiliar no diagnóstico e prognóstico de mastite em ovelha. Revista Brasileira de Medicina Veterinária, 35(3), 289-297.
Paul, C., Teng, S., & Saunders, P. T. K. (2009). A single, mild, transient scrotal heat stress causes hypoxia and oxidative stress in mouse testes, which induces germ cell death. Biology of Reproduction, 80(5), 913-919. doi: 10.1095/biolreprod.108.071779
Perotto, D., Kroetz, I. A., & Rocha, J. L. (2010). Milk production of crossbred Holstein × Zebu cows in the northeastern of Paraná State. Revista Brasileira de Zootecnia, 39(4), 758-764. doi: 10.1590/S1516-35982010000400009
Renaudeau, D., Collin, A., Yahav, S., Basilio, V., Gourdine, J. L., & Collier, R. J. (2012). Adaptation to hot climate and strategies to alleviate heat stress. Livestock Production Animal, 6(5), 707-728. doi: 10.1017/S1751731111002448
Rhoads, M. L., Rhoads, R. P., Baale, M. J., Collier, R. J., Sanders, S. R., Weber, W. J.,… Baumgard, L. H. (2009). Effects of heat stress and plane of nutrition on lactating Holstein cows: I. Production, metabolism, and aspects of circulating somatotropin. Journal of Dairy Science, 92(5), 1986-1997. doi: 10.3168/jds.2008-1641
Ruediger, F. R., Chacur, M. G. M., Alves, F. C. P. E., Oba, E., & Ramos, A. A. (2016). Digital infrared thermography of the scrotum, semen quality, serum testosterone levels in Nellore bulls (Bos taurus indicus) and their correlation with climatic factors. Semina: Ciências Agrárias, 37(1), 221-232. doi: 10.5433/1679-0359.2016v37n1p221
Ruediger, F. R., Yamada, P. H., Barbosa, L. G. B., Chacur, M. G. M., Ferreira, J. C. P., Carvalho, N. A. T., & Oba, E. (2018). Effect of estrous cycle phase on vulvar, orbital area and muzzle surface temperatures as determined using digital infrared thermography in Murrah buffalo. Animal Reproduction Science, 197, 154-161. doi: 10.1016/j.anireprosci.2018.08.023
Statistical Analysis System (SAS). (2011). SAS/STAT user’s guide: statistics. v.9.3. Cary, NC: Statistical Analysis System.
Stewart, M. (2008). Non-invasive measurement of stress and pain in cattle using infrared thermography. Tesis, Animal Science, Massey University, Palmerston North, New Zealand.
Silva, R. G. D., & Pocay, P. L. B. (2001). Transmissão de radiação ultravioleta através do pelame e da epiderme de bovinos. Revista Brasileira de Zootecnia, 30(6), 1939-1947.
Sirchia, F. P. (2008). Relação entre circunferência escrotal, libido, hormônios e características do sêmen em touros Brangus e Pardo suíço. Dissertação de Mestrado, Universidade do Oeste Paulista, Presidente Prudente, SP, Brasil.
Souza, C. D., Chacur, M. G. M., Ruediger, F. R., Cartocci, J. S., Andrade, I. B., Bastos, G. P.,... Ramos, A. A. (2014). Termorregulação escrotal em touros Nelore (Bos taurus indicus). Colloquium Agrariae, 10, 101-106. doi: 10.5747/ca.2014.v10.nesp.000143
Swenson, M. J., Reece, W. O., & Dukes. (1996) Fisiologia dos animais domésticos. São Paulo: Guanabara Koogan.
Thom, E. C. (1959). The discomfort index. Weatherwise, 12(1), 57-60.
Weschenfelder, A. V., Saucier, L., Maldague, X., Rocha, L. M., Schaefer, A. L., & Faucitano, L. (2013). Use of infrared ocular thermography to assess physiological conditions of pigs prior to slaughter and predict pork quality variation. Meat Science, 95(3), 616-620. doi: 10.1016/j.meatsci.2013.06.003
Wheelock, J. B., Rhoads, R. P., Baale, M. J., Sanders, S. R., & Baumgard, L. H. (2010). Effects of heat stress on energetic metabolism in lactating Holstein cows. Journal of Dairy Science, 93(2), 644-655. doi: 10.3168/jds.2009-2295
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2020-01-10
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Redivo Júnior, N., Souza, C. D. de, Martins, E. A. F., Uherara, T. I., Cattini, M. M., Creste, D. O., … Chacur, M. G. M. (2020). Scrotal thermography to assess the seminal quality in Nelore and Girolando bulls. Semina: Ciências Agrárias, 41(1), 131–144. https://doi.org/10.5433/1679-0359.2020v41n1p131
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