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Reproductive Performance of Holstein Dairy Cows Grazing in Dry-summer Subtropical Climatic Conditions: Effect of Heat Stress and Heat Shock on Meiotic Competence and In vitro Fertilization

  • Pavani, Krishna (Department of Agrarian Sciences, CITA-A (Research Centre for Agricultural and Environmental Sciences and Technology of the Azores), Animal Reproduction, University of the Azores) ;
  • Carvalhais, Isabel (Department of Agrarian Sciences, CITA-A (Research Centre for Agricultural and Environmental Sciences and Technology of the Azores), Animal Reproduction, University of the Azores) ;
  • Faheem, Marwa (Department of Animal Production Science, Faculty of Agriculture, Cairo University) ;
  • Chaveiro, Antonio (Department of Agrarian Sciences, CITA-A (Research Centre for Agricultural and Environmental Sciences and Technology of the Azores), Animal Reproduction, University of the Azores) ;
  • Reis, Francisco Vieira (Centre of Climate, Meteorology and Global Change of the University of the Azores) ;
  • da Silva, Fernando Moreira (Department of Agrarian Sciences, CITA-A (Research Centre for Agricultural and Environmental Sciences and Technology of the Azores), Animal Reproduction, University of the Azores)
  • Received : 2014.07.02
  • Accepted : 2014.11.02
  • Published : 2015.03.01

Abstract

The present study was designed to evaluate how environmental factors in a dry-summer subtropical climate in Terceira-Azores (situated in the North Atlantic Ocean: $38^{\circ}43^{\prime}N27^{\circ}12^{\prime}W$) can affect dairy cow (Holstein) fertility, as well as seasonal influence on in vitro oocytes maturation and embryos development. Impact of heat shock (HS) effects on in vitro oocyte's maturation and further embryo development after in vitro fertilization (IVF) was also evaluated. For such purpose the result of the first artificial insemination (AI) performed 60 to 90 days after calving of 6,300 cows were recorded for one year. In parallel, climatic data was obtained at different elevation points (n = 5) from 0 to 1,000 m and grazing points from 0 to 500 m, in Terceira island, and the temperature humidity index (THI) was calculated. For in vitro experiments, oocytes (n = 706) were collected weekly during all year, for meiotic maturation and IVF. Further, to evaluate HS effect, 891 oocytes were collected in the cold moths (December, January, February and March) and divided in three groups treated to HS for 24 h during in vitro maturation at: C (Control = $38.5^{\circ}C$), HS1 ($39.5^{\circ}C$) and HS2 ($40.5^{\circ}C$). Oocytes from each group were used for meiotic assessment and IVF. Cleavage, morula and blastocyst development were evaluated respectively on day 2, 6, and 9 after IVF. A negative correlation between cow's conception rate (CR) and THI in grazing points (-91.3%; p<0.001) was observed. Mean THI in warmer months (June, July, August and September) was $71.7{\pm}0.7$ and the CR ($40.2{\pm}1.5%$) while in cold months THI was $62.8{\pm}0.2$ and CR was $63.8{\pm}0.4%$. A similar impact was obtained with in vitro results in which nuclear maturation rate (NMR) ranged from 78.4% (${\pm}8.0$) to 44.3% (${\pm}8.1$), while embryos development ranged from 53.8% (${\pm}5.8$) to 36.3% (${\pm}3.3$) in cold and warmer months respectively. In vitro HS results showed a significant decline (p<0.05) on NMR of oocytes for every $1^{\circ}C$ rising temperature ($78.4{\pm}8.0$, $21.7{\pm}3.1$ and $8.9{\pm}2.2$, respectively for C, HS1, and HS2). Similar results were observed in cleavage rate and embryo development, showing a clear correlation (96.9 p<0.05) between NMR and embryo development with respect to temperatures. Results clearly demonstrated that, up to a THI of 70.6, a decrease in the CR occurs in first AI after calving; this impairment was confirmed with in vitro results.

Keywords

References

  1. Aman, R. R and J. E. Parks. 1994. Effects of cooling and rewarming on the meiotic spindle and chromosomes of in vitro-matured bovine oocytes. Biol. Reprod. 50:103-110. https://doi.org/10.1095/biolreprod50.1.103
  2. Alexander, V. S. 2010. Effect of two types of stress (heat shock/high temperature and malnutrition/serum deprivation) on porcine ovarian cell functions and their response to hormones. J. Exp. Biol. 213:2125-2130. https://doi.org/10.1242/jeb.040626
  3. Azevedo, E. B. 1996. Modelling of Insular Climate at Local Scale. Model CIELO Applied to Terceira. Ph.D. Thesis, Universidade dos Acores, Angra do Heroismo, Portugal.
  4. Badinga, L., R. J. Collier, W. W. Thatcher, and C. J. Wilcox. 1985. Effects of climatic and management factors on conception rate of dairy cattle in subtropical environment. J. Dairy Sci. 68:78-85. https://doi.org/10.3168/jds.S0022-0302(85)80800-6
  5. Badinga, L., W. W. Thatcher, T. Diaz, M. Drost, and D. Wolfenson. 1993. Effect of environmental heat stress on follicular development and steroidogenesis in lactating Holstein cows. Theriogenology 39:797-810. https://doi.org/10.1016/0093-691X(93)90419-6
  6. Baumgartner, A. P and C. L. Chrisman. 1987. Embryonic mortality caused by maternal heat stress during mouse oocyte maturation. Anim. Reprod. Sci. 14:309-316. https://doi.org/10.1016/0378-4320(87)90021-2
  7. Britt, J. H. 1994. Follicular development and fertility: Potential impacts of negative energy balance. In: Proc. Nat. Reprod. Symp. 103-112.
  8. Biggers, B. G., R. D. Geisert, R. P. Wetteman, and D. S. Buchanan. 1987. Effect of heat stress on early embryonic development in the beef cow. J. Anim. Sci. 64:1512-1518.
  9. Collier, R. J., G. E. Dahl, and M. J. Van-Baale. 2006. Major advances associated with environmental effects on dairy cattle. J. Dairy Sci. 89:1244-1253. https://doi.org/10.3168/jds.S0022-0302(06)72193-2
  10. De Rensis, F. and R. J. Scaramuzzi. 2003. Heat stress and seasonal effects on reproduction in the dairy cow-A review. Theriogenology 60:1139-1151. https://doi.org/10.1016/S0093-691X(03)00126-2
  11. Ducibella, T. and J. Buetow. 1994. Competence to undergo normal, fertilization-induced cortical activation develops after metaphase I of meiosis in mouse oocytes. Dev. Biol. 165:95-104. https://doi.org/10.1006/dbio.1994.1237
  12. Edwards, J. L. and P. J. Hansen. 1997. Differential responses of bovine oocytes and preimplantation embryos to heat shock. Mol. Reprod. Dev. 46:138-145. https://doi.org/10.1002/(SICI)1098-2795(199702)46:2<138::AID-MRD4>3.0.CO;2-R
  13. Edwards, J. L., A. M. Saxton, J. L. Lawrence, R. R. Payton, and J. R. Dunlap. 2005. Exposure to a physiologically relevant elevated temperature hastens in vitro maturation in bovine oocytes. J. Dairy Sci. 88:4326-4333. https://doi.org/10.3168/jds.S0022-0302(05)73119-2
  14. Ealy, A. D., M. Drost, and P. J. Hansen. 1993. Developmental changes in embryonic resistance to adverse effects of maternal heat stress in cows. J. Dairy Sci. 76:2899-2905. https://doi.org/10.3168/jds.S0022-0302(93)77629-8
  15. El-Sayed, A. M., F. Hoelker, D. Rings, D. Slilew, E. Jennen, M. A. Tholen, K. Sirard, and D. Schellander Tesfaye. 2006. Largescale transcriptional analysis of bovine embryos biopsies in relation to pregnancy success after transfer to recipients. Physiol. Genomics 28:84-96. https://doi.org/10.1152/physiolgenomics.00111.2006
  16. Faheem, M. S., I. Carvalhais, A. Chaveiro, and F. Moreira da Silva. 2011. In vitro oocyte fertilization and subsequent embryonic development after cryopreservation of bovine tissue, using an effective approach for oocyte collection. Anim. Reprod. Sci. 125:49-55. https://doi.org/10.1016/j.anireprosci.2011.02.011
  17. Ferreira, R. M., H. Ayres, M. R. Chiaratti, M. L. Ferraz, A. B. Araujo, C. A. Rodrigues, Y. F. Watanabe, A. A. Vireque, D. C. Joaquim, L. C. Smith, F. V. Meirelles, and P. S. Baruselli. 2011. The low fertility of repeat-breeder cows during summer heat stress is related to a low oocyte competence to develop into blastocysts. J. Dairy Sci. 94:2383-2392. https://doi.org/10.3168/jds.2010-3904
  18. Garcia Ispierto, I., F. Lopez-Gatius, G. Bech-Sabat, P. Santolaria, J. L. Yaniz, C. Nogareda, F. De Rensis, and M. Lopez-Bejar. 2007. Climate factors affecting conception rate of high producing dairy cows in northeastern spain. Theriogenology 67:1379-1385. https://doi.org/10.1016/j.theriogenology.2007.02.009
  19. Hansen P. J., M. Drost, R. M. Rivera, F. F. Paula-Lopes, Y. M. Al-Katanani, C. E. Krininger, and C. C. Chase. 2001. Adverse impact of heat stress on embryo production: causes and strategies for mitigation. Theriogenology 55:91-103. https://doi.org/10.1016/S0093-691X(00)00448-9
  20. Hosoe, M. and Y. Shioya.1997. Distribution of cortical granules in bovine oocytes classified by cumulus complex. Zygote 5:371-376.
  21. Ju, J. C. 1999. The Effect of Heat Shock on the Developmental Competence and Activation of Bovine Oocytes. Ph.D Thesis. Cornell University, Ithaca, NY, USA.
  22. Leroy, J. L. M. R., T. Vanholder, J. R. Delanghe, G. Opsomer, A. Van Soom, P. E. J. Bols, J. Dewulf, and A. de Kruif. 2004. Metabolic changes in follicular fluid of the dominant follicle in high-yielding dairy cows early postpartum. Theriogenology 62:1131-1143. https://doi.org/10.1016/j.theriogenology.2003.12.017
  23. Lawrence, J. L., R. R. Payton, J. D. Godkin, A. M. Saxton, F. N. Schrick, and J. L. Edwards. 2004. Retinol improves development of bovine oocytes compromised by heat stress during maturation. J. Dairy Sci. 87:2449-2454. https://doi.org/10.3168/jds.S0022-0302(04)73368-8
  24. Maya-Soriano, M. J., F. Lopez-Gatius, C. Andreu-Vazquez, and M. Lopez-Bejar. 2013. Bovine oocytes show a higher tolerance to heat shock in the warm compared with the cold season of the year. Theriogenology 79:299-305. https://doi.org/10.1016/j.theriogenology.2012.08.020
  25. Paula-Lopes, F. F., M. Milazzotto, M. E. O. A. Assumpcao, and J. A. Visintin. 2008. Heat shock-induced damage in bovine oocytes. Reprod. Fertil. Dev. 43:208.
  26. Payton, R. R., R. Romar, P. Coy, A. M. Saxton, J. L. Lawrence, and J. L. Edwards. 2004. Susceptibility of bovine germinal vesicle-stage oocytes from antral follicles to direct effects of heat stress in vitro. Biol. Reprod. 71:1303-1308. https://doi.org/10.1095/biolreprod.104.029892
  27. Pires, M. F. A., A. M. Ferreira, H. M. Saturnino, and R. L. Teodoro. 2002. Pregnancy rate in holstein females confined in free stall, in summer and winter. Arq. Bras. Med. Vet. Zootec. 54:57-63.
  28. Putney, D. J., S. Mullins, W. W. Thatcher, M. Drost, and T. S. Gross. 1989. Embryonic development in superovulated dairy cattle exposed to elevated ambient temperatures between the onset of estrus and insemination. Anim. Reprod. Sci 19:37-51. https://doi.org/10.1016/0378-4320(89)90045-6
  29. Ray, D. E., T. J. Halbach, and D. V. Armstrong. 1992. Season and lactation number effects on milk production and reproduction in dairy cattle in Arizona. J. Dairy Sci. 75:2976-2983. https://doi.org/10.3168/jds.S0022-0302(92)78061-8
  30. Roth, Z., A. Arav, A. Boar, Y. Zeron, and D. Wolfenson. 2001. Improvement of quality of oocyte collected in the autumn by enhanced removal of impaired follicles from previously heatstressed cows. Reproduction 122:737-744. https://doi.org/10.1530/rep.0.1220737
  31. Roth, Z., R. Meidan, R. Braw-Tal, and D. Wolfenson. 2000. Immediate and delayed effects of heat stress on follicular development and its association with plasma FSH and inhibin concentration in cows. J. Reprod. Fertil. 120:83-90.
  32. Roth, Z. and P. J. Hansen. 2004. Involvement of apoptosis in disruption of developmental competence of bovine oocytes by heat shock during maturation. Biol. Reprod. 71:1898-1906. https://doi.org/10.1095/biolreprod.104.031690
  33. Roth, Z. and P. J. Hansen. 2005. Disruption of nuclear maturation and rearrangement of cytoskeletal elements in bovine oocytes exposed to heat shock during maturation. Reproduction 129: 235-244. https://doi.org/10.1530/rep.1.00394
  34. Sieuve de Menezes, S., A. Chaveiro, and F. Moreira da Silva. 2011. Effect of climatic conditions on reproductive performance of grazing heifers and lactating cows in the Azores, a warm temperate region. Theriogenol. Insight 1:89-97.
  35. Sun, Q. Y., G. M. Wu, L. Lai, K. W. Park, R. Cabot, H. T. Cheong, B. N. Day, R. S. Prather, and H. Schatten. 2001. Translocation of active mitochondria during pig oocyte maturation, fertilization and early embryo development in vitro. Reproduction 122:155-163. https://doi.org/10.1530/rep.0.1220155
  36. Torres-Junior, J. R., M. F. Pires, W. F. Sa, M. A. Ferreira, J. H. M. Viana, L. S. A. Camargo, A. A. Ramos, I. M. Folhadella, J. Polisseni, C. Freitas, C. A. A. Clemente, M. F. Sa Filho, F. F. Paula-Lopes, and P. S. Baruselli. 2008. Effect of maternal heatstress on follicular growth and oocyte competence in Bos indicus cattle. Theriogenology 69:155-166. https://doi.org/10.1016/j.theriogenology.2007.06.023
  37. Tseng, J. K., C. H. Chen, P. C. Chou, S. P. Yeh, and J. C. Ju. 2004. Influences of follicular size on parthenogenetic activation and in vitro heat shock on the cytoskeleton in cattle oocytes. Reprod. Domest. Anim. 39:146-153. https://doi.org/10.1111/j.1439-0531.2004.00493.x
  38. Wang, W., M. Hosoe, R. Li, and Y. Shioya. 1997. Development of the competence of bovine oocytes to release cortical granules and block polyspermy after meiotic maturation. Dev. Growth Differ. 39:607-615. https://doi.org/10.1046/j.1440-169X.1997.t01-4-00008.x
  39. Wang, W. H., L. Meng, R. J. Hackett, R. Odenbourg, and D. L. Keefe. 2001. Limited recovery of meiotic spindles in living human oocytes after cooling-rewarming observed using polarized light microscopy. Hum. Reprod. 16:2374-2378.
  40. White, F. J., R. P. Wettemann, M. L. Looper, T. M. Prado, and G. L. Morgan. 2002. Seasonal effects on estrous behaviour and time of ovulation in non-lactating beef cows. J. Anim. Sci. 80: 3053-3059.
  41. Yaser, M. A., D. W. Webb, and P. J. Hansen. 1999. Factors affecting seasonal variation in 90-Day nonreturn rate to first service in lactating holstein cows in a hot climate. J. Dairy Sci. 82:2611-2616. https://doi.org/10.3168/jds.S0022-0302(99)75516-5
  42. Yousef, M. K. 1985. Stress physiology: definition and terminology. Stress Physiology in livestock. In: Basic principles (Ed. M. K. Yousef) Vol. 1, pp. 3-7. CRC Press, Boca Raton, FL, USA.

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