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Human–animal interaction, stress, and embryo production in Bos indicus embryo donors under tropical conditions

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Abstract

This study investigated the effect of human–animal interaction (HAI) and the stress response on the quality of embryo production in superovulated Nelore (Bos indicus) cattle, under tropical conditions. Thirty-two females underwent a superovulation protocol for 5 days. Cortisol concentrations were determined in blood plasma collected on days 0, 4, and 5. Artificial insemination was performed on days 4 and 5, and nonsurgical embryo flushing on day 11. Embryo production and viability were determined. Human stimulation, animal behaviors, accidents, and handling time were recorded to assess HAI. Cattle age was negatively correlated with accidents, frequency of aversive behaviors, and negative stimuli by stockperson during transit through corral compartments to receive superovulation treatments. The factor analysis revealed two distinct groups. The first group was called stressed and had higher cortisol concentration than the nonstressed group, 16.0 ± 2.1 and 12.5 ± 1.0 ng/mL, respectively. Comparisons between these groups showed that the frequency of voice emissions by the stockperson and the number of accidents were higher in the stressed group, and also, the mean handling time was longer in the stressed group than for the nonstressed. As a result, viability rate of the embryos was 19% lower in the stressed group (P < 0.05). This indicates that intensive negative HAI is likely related to stress, which affects embryo production in a superovulation program.

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References

  • Alam, M.G.S. and Dobson, H., 1986. Effect of various veterinary procedures on plasma concentrations of cortisol, luteinizing hormone and prostaglandin E2 metabolite in the cow, Veterinary Research, 118, 7–10.

    CAS  Google Scholar 

  • Albright, J. L., 1987. Dairy Animal Welfare: Current and Needed Research, Journal of Dairy Science, 70, 2711–2731.

    Article  CAS  PubMed  Google Scholar 

  • Andrade, O., Orihuela, A., Solano, J. and Galina, C.S., 2001. Some effects of repeated handling and the use of a mask on stress responses in zebu cattle during restraint, Applied Animal Behaviour Science, 71, 175–181.

    Article  PubMed  Google Scholar 

  • Aoyama, M., Negishi, A., Abe, A., Maejima, Y. and Sugita, S., 2003. Sex differences in stress responses to transportation in goats: effects of gonadal hormones, Animal Science Journal, 74, 511–519.

    Article  CAS  Google Scholar 

  • Blackshaw, J.K., 1986. Notes on some topics in applied animal behaviour. 1. ed. University of Queensland, Queensland, Australia.

    Google Scholar 

  • Breen, K.M. and Karsch, F.J., 2004. Does cortisol inhibits pulsatile luteinizing hormone secretion at the hypothalamic or pituitary level?, Endocrinology, 145, 692–698.

    Article  CAS  PubMed  Google Scholar 

  • Breen, K.M., Billings, H.J., Wagenmaker, E.R., Wessinger, E.W. and Karsch, F.J., 2005. Endocrine basis for disruptive effects of cortisol on preovulatory events, Endocrinology, 156, 2107–2115.

    Article  Google Scholar 

  • Broom, D.M., 1991. Animal welfare: concepts and measurement, Journal of Animal Science, 69, 4167–4175.

    CAS  PubMed  Google Scholar 

  • Burns, K., 2008. A meeting of minds on the welfare of beef cattle, Journal of the American Veterinary Medical Association, 233, 202–205.

    Article  PubMed  Google Scholar 

  • Cafe, L.M., Robinson, D.L., Ferguson, D.M., Mclntyre, B.L., Geesink, G.H. and Greenwod, P.L., 2010. Cattle temperament: persistence of assessments and associations with productivity, efficiency, carcass and meat quality traits, Journal of Animal Science. doi:10.2527/jas.2010-3304.

  • Costa e Silva, E.V., Katayama, K.A., Macedo, G.G., Rueda, P.M., Abreu, U.G.P. and Zúccari, C.E.S.N., 2010. Efeito do manejo e de variáveis bioclimáticas sobre a taxa de gestação em vacas receptoras de embriões, Ciência Animal Brasileira, 11, 280–291.

    Article  Google Scholar 

  • Dobson, H. and Smith, R.F., 2000. What is stress, and how does it affect reproduction?, Animal Reproduction Science, 60–61, 743–752.

    Article  PubMed  Google Scholar 

  • Dobson, H., Ribadu, A.Y., Noble, K.M., Tebble, J.E. and Ward, W.R., 2000. Ultrasonography and hormone profiles of adrenocorticotrophic hormone (ACTH)-induced persistent ovarian follicles (cysts) in cattle, Journal of Reproduction and Fertility, 120, 405–410.

    Article  CAS  PubMed  Google Scholar 

  • Dobson, H., Tebble, J.E., Smith, R.F. and Ward, W.R., 2001. Is stress really all that important?, Theriogenology, 55, 65–73.

    Article  CAS  PubMed  Google Scholar 

  • Dobson, H., Walker, S.L., Morris, M.J., Routly, J.E. and Smith, R.F., 2008. Why is it getting more difficult to successfully artificially inseminate dairy cows?, Animal, 2, 1104–1111.

    Article  PubMed  Google Scholar 

  • Edwards, L.M., Rahe, C.H. and Griffin, J.L., 1987. Effect of transportation stress on ovarian function in superovulated Hereford heifers, Theriogenology, 28, 291–299.

    Article  CAS  PubMed  Google Scholar 

  • FAO, 2008. Food and Agriculture Organization. Available at: http://www.fao.org/. Accessed 17 June 2010.

  • Grandin, T., 1997. Assessment of stress during handling and transport, Journal of Animal Science, 75, 249–257.

    CAS  PubMed  Google Scholar 

  • Grandin, T. and Deesing, M.J., 1998. Behavioral genetics and animal science. Article. http://www.grandin.com/references/genetics.html. Accessed 13 June 2010.

  • Hemsworth, P.H. and Coleman, G.J., 1998. Human-livestock interactions: the stockperson and the productivity and welfare of intensively farmed animal, Wallingford: Cab International.

    Google Scholar 

  • Hemsworth, P.H., Coleman, G.J., Barnett, J.L. and Borg, S., 2000. Relationships between human-animal interactions and productivity of commercial dairy cows, Journal of Animal Science, 78, 2821–2831.

    CAS  PubMed  Google Scholar 

  • IBGE, 2008. Instituto Brasileiro de Geografia e Estatística. Avaliable at: http://www.ibge.gov.br/english/. Accessed 17 June 2008.

  • Johnson, R.A. and Wichern, D.W., 1999. Applied multivariate statistical analysis, 2 ed, (Upper Saddle River, NJ: Prentice-Hall Inc.).

    Google Scholar 

  • Lay, D.C., Friend, T.H.Jr., Bowers, C.L., Grissom, K.K. and Jenkins, O.C., 1992. A comparative physiological and behavioral study of freeze and hot-iron branding using dairy cows, Journal of Animal Science, 70, 1121–1125.

    PubMed  Google Scholar 

  • Lindner, G.M. and Wright, J.R.W., 1983. Bovine embryo morphology and evaluation, Theriogenology, 20, 407–416.

    Article  CAS  PubMed  Google Scholar 

  • Mihm, M., Baguisi, A., Boland, M.P. and Roche, J.F., 1994. Association between the duration of dominance of the ovulatory follicle and pregnancy rate in beef heifers, Journal of Reproduction and Fertilitly, 102, 123–130.

    Article  CAS  Google Scholar 

  • Minton, J.E., 1994. Function of the hypothalamic-pituitary-adrenal axis and the sympathetic nervous system in models of acute stress in domestic farm animals, Journal of Animal Science, 72, 1891–1898.

    CAS  PubMed  Google Scholar 

  • Moberg, G.P., 1987. A model for assessing the impact of behavioral stress on domestic animals, Journal of Animal Science, 7, 1228–1235.

    Google Scholar 

  • Morris, M.J., Walker, S.L., Jones, D.N., Routly, J.E., Smith, R.F and Dobson, H., 2009. Influence of somatic cell count, body condition and lameness on follicular growth and ovulation in dairy cows, Theriogenology, 71, 801–806.

    Article  CAS  PubMed  Google Scholar 

  • Negrão, J.A. and Marnet, P.G., 2006. Milk yield, residual milk, oxytocin and cortisol release during machine milking in Gir, Gir × Holstein and Holstein cows, Reproduction Nutrition and Development, 46, 77–85

    Article  Google Scholar 

  • Nogueira, M.F.G., Fragnito, P.S., Trinca, L.A. and Barros, C.M., 2007. The effect of type of vaginal insert and dose of pLH on embryo production, following fixed-time AI in a progestin-based superstimulatory protocol in Nelore cattle, Theriogenology, 67, 655–660.

    Article  CAS  PubMed  Google Scholar 

  • Pajor, E.A., Rushen, J. and de Passillé, A.M.B., 2000. Aversion learning techniques to evaluate dairy cattle handling practices, Applied Animal Behavior Science, 69, 89–102.

    Article  Google Scholar 

  • Peixoto, M.G.C.D., Fonseca, C.G., Penna, V.M. and Alvim, M.T.T., 2002. Análise multivariada de resultados da ovulação múltipla seguida de transferência de embriões de doadoras zebuínas, Brazilian Journal of Veterinary and Animal Science, 54, 492–500.

    Google Scholar 

  • Peixoto, M.G.C.D., Bergmann, J.A.G., Fonseca, C.G., Penna, V.M. and Pereira, C.S., 2006. Effects of environmental factors on multiple ovulation of zebu donors. Brazilian Journal of Veterinary and Animal Science, 58, 567–574.

    Google Scholar 

  • Randel, R.D., 1984. Seasonal effects on female reproductive functions in the bovine (Indian breeds). Theriogenology, 21, 170–185.

    Article  CAS  Google Scholar 

  • Rushen, J., de Passillé, A.M.B. and Munksgaard, L., 1999. Fear of people by cows and effects on milk yield, behavior, and heart rate at milking, Journal of Dairy. Science, 82, 720–727.

    Article  CAS  PubMed  Google Scholar 

  • Sapolsky, R.M., Romero, M.L. and Munck, A.U., 2000. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions, Endocrinology, 89, 21–55.

    Google Scholar 

  • Schmied C, Boivin X and Waiblinger S., 2008. Stroking different body regions of dairy cows: effects on avoidance and approach behavior toward humans, Journal of Dairy Science, 91, 596–605.

    Article  CAS  PubMed  Google Scholar 

  • Wagenmaker, E.R., Breen, K.M., Oakley, A.E. and Tilbrook, A.J. and Karsch, F.J., 2009. Psychosocial Stress Inhibits Amplitude of Gonadotropin-Releasing Hormone Pulses Independent of Cortisol Action on the Type II Glucocorticoid Receptor, Endocrinology, 150, 762–769.

    Article  CAS  PubMed  Google Scholar 

  • Waiblinger, S., Menke, C., Korff, J. and Bucher, A., 2004. Previous handling and gentle interactions affect behaviour and heart rate of dairy cows during a veterinary procedure, Applied Animal Behavior Science, 85, 31–42.

    Article  Google Scholar 

  • Waiblinger, S., Boivin, X., Pedersen, V., Tosi, M.V., Janczak, A.M., Visser, E.K. and Jones, R.B., 2006. Assessing the human–animal relationship in farmed species: A critical review, Applied Animal Behavior Science, 101, 185–242.

    Article  Google Scholar 

  • Walker, S.L., Smith, R.F., Routly, J.E., Jones, D.N., Morris, M.J. and H. Dobson, 2008. Lameness, activity time-budgets, and estrus expression in dairy cattle, Journal of Dairy Science, 91, 4552–4559.

    Article  CAS  PubMed  Google Scholar 

  • Walker, S.L., Smith, R.F., Jones, D.N., Routly, J.E., Morris, M.J. and Dobson, H., 2010. The effect of a chronic stressor, lameness, on detailed sexual behavior and hormonal profiles in milk and plasma of dairy cattle, Reproduction in Domestic Animals, 45, 109–117.

    Article  CAS  PubMed  Google Scholar 

  • Waynert, D.F., Stookey, J.M., Schwartzkopf-Genswein, K.S., Watts, J.M. and Waltz, C.S., 1999. The responses of beef cattle to noise during handling. Applied Animal Behaviour, Science, 62, 27–42.

    Article  Google Scholar 

  • Wiltbank, J.N., 1983. Effect of nutrition and other factors on the reproduction heifers. In: Proceedings of the 26th Annual Beef Cattle Short Course, 1983. University of Florida, Gainesville, FI, USA, Gainesville, 1983, 63–68.

  • Zanenga, C.A., Marques, M.O., Santos, I.C.C., Valentin, R. and Baruselli, P.S., 2003 Comparação entre dois protocolos de superovulação com inseminação artificial em tempo fixo em vacas Nelore (Bos taurus indicus), Acta Science Veterinariae, 31, 626–627.

    Google Scholar 

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Acknowledgments

The authors thank Fazenda Sete Estrelas Embriões and Fundação de Apoio ao Desenvolvimento do Ensino, Ciência e Tecnologia—Mato Grosso do Sul for providing cattle, facilities and financial support.

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Authors and Affiliations

  1. Faculty of Veterinary Medicine and Animal Science, Universidade Federal de Mato Grosso do Sul, Campo Grande, 79070-900, Mato Grosso do Sul, Brazil

    Gustavo Guerino Macedo, Carmem Estefânia Serra Neto Zúccari & Eliane Vianna da Costa e Silva

  2. Brazilian Agricultural Research Corporation–EMBRAPA Pantanal, Corumbá, 79320-900, Mato Grosso do Sul, Brazil

    Urbano Gomes Pinto de Abreu

  3. Faculty of Animal Sciences and Food Engineering, Universidade de São Paulo, Pirassununga, 13630-970, São Paulo, Brazil

    João Alberto Negrão

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  1. Gustavo Guerino Macedo
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Correspondence to Eliane Vianna da Costa e Silva.

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Macedo, G.G., Zúccari, C.E.S.N., de Abreu, U.G.P. et al. Human–animal interaction, stress, and embryo production in Bos indicus embryo donors under tropical conditions. Trop Anim Health Prod 43, 1175–1182 (2011). https://doi.org/10.1007/s11250-011-9820-6

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