Effects of cortisol levels on reproductive success in cattle of different temperaments during fixed-time artificial insemination (FTAI)

Nuna Faria; José Pacheco-Lima; Maria Helena Moreira da Silva; A. Borba; Joaquim Fernando Moreira da Silva

doi:10.31893/jabb.2024002

Keywords:

Abstract

The present study was designed to assess the effect of stress on the reproductive performance of cattle. For this purpose, a total of 137 cows were divided into two groups: 65 belonging to the Azores Lydia breed and 72 crossing Aberdeen-Angus with Limousine, free of IBR, Chlamydia and BVD diseases and with a body condition score ranging from 2.75 to 4.0. Eight days before starting the experimental procedures, animals passed through the containment sleeve every other day for routine and human presence. For the synchronization protocol, a progesterone-impregnated controlled internal drug release (CIDR®) insert was placed intravaginally, and an injection of GnRH was given. After 7 days, PGF2α was administered, and the CIDR® was removed. Sixty hours after removal, cows were inseminated once after another injection of GnRH to induce ovulation, and pregnancy diagnosis was performed by ultrasonography 30 days after artificial insemination. Peripheral blood was collected in 5 ml tubes with a Z Serum Sep Clot Activator, and cortisol was measured using the IMMULITE 2000 Immunoassay System ®. Our results indicated significant differences (p≤0.05) in the cortisol levels among both groups (beef crossbred cows vs Azores Lydia) of 4.3±0.3 ng/dl and 5.8±0.4 ng/dl, respectively. The pregnancy results were also significantly different: 63.7% vs 45.6%, respectively, for beef crossbred and "Azores Lydia" cows. The present study clearly demonstrated a negative correlation between cortisol levels and pregnancy rates after fixed-time artificial insemination. The low levels of cortisol observed in the animals and particularly in the Azores Lydia breed, when compared to other studies carried out on these animals, must be due to the passage of the animals in the sleeve, allowing them to habituate to a routine, as well as to human presence.
References
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6. Cooke RF, Bohnert DW, Cappellozza BI, Mueller CJ, Delcurto T (2012) Effects of temperament and acclimation to handling on reproductive performance of Bos taurus beef females. Journal of Animal Science 90:3547–3555. https://doi.org/10.2527/jas.2011-4768
7. Correia P, Baron E, Moreira da Silva F, Cortés O (2017) Mitochondrial and Y chromosome genetic diversity in the Portuguese Lidia bovine breed. Revista Brasileira de Zootecnia 46:99-104. https://doi.org/10.1590/S1806-92902017000200003
8. Dobson H, Smith R (2000) What is stress, and how does it affect reproduction? Animal Reproduction Science 60-61:743-752. https://doi.org/10.1016/S0378-4320(00)00080-4
9. Dobson H, Fergani C, Routly JE, Smith RF (2012) Effects of stress on reproduction in ewes. Animal Reproduction Science 130:135–140. https://doi.org/10.1016/j.anireprosci.2012.01.006
10. Drost M, Thatcher WW (1987) Heat stress in dairy cows. Its effect on reproduction. Veterinary Clinics of North America: Food Animal Practice 3:609–618. https://doi.org/10.1016/S0749-0720(15)31133-6
11. Duong TH, Pitrowska KK, Bah MM, Sinderewicz E, Majewska M, Jankowska K, Okuda K, Skarzynski DJ (2012) Effects of cortisol on pregnancy rate and corpus luteum function in heifers: an in vivo study. Journal of Reproduction and Development 58:223–230. https://doi.org/10.1262/jrd.11-122T
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13. Grandin T (1997) Assessment of stress during handling and transport. Journal of Animal Science 75:249-257. https://doi.org/10.2527/1997.751249x
14. Güldenpfennig J, Schmicke M, Hoedemaker M, Siebert U, Keuling O (2021) An approach to assess stress in response to drive hunts using cortisol levels of wild boar (Sus scrofa) Scientific Reports 11:16381. https://doi.org/10.1038/s41598-021-95927-2
15. Hall NL, Buchanan DS, Anderson V L, Ilse B R, Carlin KR, Berg, EP (2011) Working chute behavior of feedlot cattle can be an indication of cattle temperament and beef carcass composition and quality. Meat Science, 89:52–57. https://doi.org/10.1016/j.meatsci.2011.03.020
16. Hughes HD, Carroll JA, Burdick Sanchez NCB, Richeson JT (2014) Natural variations in the stress and acute phase responses of cattle. Innate immunity 20:888–896. https://doi.org/10.1177/1753425913508993
17. Jeffus J, Reuter R, Wagner K, Goodman L, Parker T (2021) 5 Effects of Virtual Fencing on Cortisol Concentrations and Behavior of Beef Cattle. Journal of Animal Science 99:1-2. https://doi.org/10.1093/jas/skab235.001
18. Kalin NH, Shelton SE, Turner JG (1992) Effects of !b-carboline on fear-related behavioral and neurohormonal responses in infant rhesus monkeys. Biological Psychiatry 31:1008–1019. https://doi.org/10.1016/0006-3223(92)90094-G
19. Kim WS, Lee JS, Jeon SW, Peng DQ, Kim YS, Bae MH, Jo YH, Lee HG (2018) Correlation between blood, physiological and behavioral parameters in beef calves under heat stress. Asian-Australasian Journal of Animal sciences 31: 919–925. https://doi.org/10.5713/ajas.17.0545
20. Korchia J, Freeman KP (2021) Validation study of canine urine cortisol measurement with the Immulite 2000 Xpi cortisol immunoassay. Journal of Veterinary Diagnostic Investigation 33:1051-1068.
21. Lee C, Colditz IG, Campbell DLM (2018) A Framework to Assess the Impact of New Animal Management Technologies on Welfare: A Case Study of Virtual Fencing. Frontiers In Veterinary Science 21:187.
22. Ley SJ, Waterman AE, Livingston A (1996) Measurement of mechanical thresholds, plasma cortisol and catecholamines in control and lame cattle: A preliminary study. Research in Veterinary Science 61:172-173. https://doi.org/10.1016/S0034-5288(96)90096-X
23. Lowman BG, Scott NA, Somerville SH (1976) Condition Scoring of Cattle. Bull. 6. East of Scotland College of Agriculture 6:31. Edinburgh, UK. https://pasture.io/farm-animal-health/body-condition-scoring (accessed on 5 September, 2023)
24. McEwen BS, Stellar E (1993) Stress and the individual. Mechanisms leading to disease. Archives of Internal Medicine 153:2093–2101.
25. Miranda-de la Lama GC, Sepúlveda WS, Villarroel M, & María GA (2011) Livestock vehicle accidents in Spain: causes, consequences, and effects on animal welfare. Journal of Applied Animal Welfare Science 14:109–123. https://doi.org/10.1080/10888705.2011.551622
26. Molony V, Kent J, Robertson I (1993) Behavioural responses of lambs of three ages in the first three hours after three methods of castration and tail docking. Research in Veterinary Science 55:236-245. https://doi.org/10.1016/0034-5288(93)90087-V
27. Wrangham RW, Muller MN (2004) Dominance, cortisol and stress in wild chimpanzees (Pan troglodytes schweinfurthii) Behavioral Ecology and Sociobiology 55:332-340. http://dx.doi.org/10.1007/s00265-003-0713-1
28. Ortiga-Carvalho TM, Chiamolera MI, Pazos-Moura CC, Wondisford FE (2016) Hypothalamus-Pituitary-Thyroid Axis. Comprehensive Physiology 6:1387–1428. https://doi.org/10.1002/cphy.c150027
29. Pacheco-Lima J, Moreira da Silva J (2019a) Reproductive Characterization of The Bovine Lidia Called “Brava Dos Açores”. Biomedical Journal of Scientific and Technical Research 15:1. https://doi:10.26717/BJSTR.2019.15.002632
30. Pacheco-Lima J, Silva H, Campillo Beneitez JP, Fernandes da Silva D, Moreira da Silva F (2019b) Effect of Vaccination Against Ibr/Bvd on The Reproductive Performances of Brava Dos Açores -A Bovine Lidia Breed. American Journal of Biomedical Science and Research 6:266-272.
31. Parent J, Chapdelaine P, Sirois J, Fortier MA (2002) Expression of microsomal prostaglandin E synthase in bovine endometrium: coexpression with cyclooxygenase type 2 and regulation by interferon-tau. Endocrinology 143(8):2936-2943. https://doi.org/10.1210/endo.143.8.8969
32. Rausch, WD, Hofer A, Gemeiner M, Möstl E (1989) Catecholamine and cortisol concentrations in plasma from cattle at parturition]. Zentralblatt fur Veterinarmedizin 36(3): 218–224.
33. Richeson JT, Hughes HD, Broadway PR, Carroll JA (2019) Vaccination Management of Beef Cattle: Delayed Vaccination and Endotoxin Stacking. Veterinary Clinics of North America Food Animal Practice 35:575–592. https://doi.org/10.1016/j.cvfa.2019.07.003
34. Rizzo A, Minoia G, Trisolini C, Manca R, Sciorsci RL (2007) Concentrations of free radicals and beta-endorphins in repeat breeder cows. Animal Reproduction Science 100: 257–263.
35. Roth Z (2018) Symposium review: Reduction in oocyte developmental competence by stress is associated with alterations in mitochondrial function. Journal of Dairy Science 101(4): 3642–3654. https://doi.org/10.3168/jds.2017-13389
36. Sánchez J, Castro M, Alonso M, Gaudioso (1996) Adaptive metabolic responses in females of the fighting breed submitted to different sequences of stress stimuli. Physiology and Behavior 60(4): 1047-1052. https://doi.org/10.1016/0031-9384(96)00160-6
37. Seth S, Lewis AJ, Galbally M (2016) Perinatal maternal depression and cortisol function in pregnancy and the postpartum period: a systematic literature review. BMC Pregnancy and Childbirth 16(1): 124. https://doi.org/10.1186/s12884-016-0915-y
38. Shenavai S, Preissing S, Hoffmann B, Dilly M, Pfarrer C, Özalp GR, Caliskan C, Seyrek-Intas K, Schuler G (2012) Investigations into the mechanisms controlling parturition in cattle. Reproduction (Cambridge, England), 144(2), 279–292. https://doi.org/10.1530/REP-11-0471
39. Souza JMG, Batista R, Melo LM, Freitas VJ (2011) Reproductive biotechnologies applied to the conservation of endangered ruminant - past, present, and future. Revista Portuguesa de Ciências Agrárias 106: 31-38.
40. Stilwell, G. (2012) Scientific Opinion on the welfare of cattle kept for beef production and the welfare in intensive calf farming systems. EFSA Journal 10(5): 2669. http://dx.doi.org/10.2903/j.efsa.2012.2669
41. Tucker CB, Coetzee JF, Stookey JM, Thomson DU, Grandin T, Schwartzkopf-Genswein SK (2015) Beef cattle welfare in the USA: identification of priorities for future research. Animal Health Research Reviews 16(2) 107-124. https://doi.org/10.1017/S1466252315000171
42. Vale S, Selinger L, Martins JM, Gomes AC, Bicho M, Carmo I, Escera C (2014) The relationship between dehydroepiandrosterone (DHEA), working memory and distraction – A behavioral and electrophysiological approach. PloS One 9(8) e104869. https://doi.org/10.1371/journal.pone.0104869

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How to cite

Faria, N., Pacheco-Lima, J., Moreira da Silva, M. H., Borba, A., & Moreira da Silva, J. F. (2023). Effects of cortisol levels on reproductive success in cattle of different temperaments during fixed-time artificial insemination (FTAI). Journal of Animal Behaviour and Biometeorology, 12(1), 2024002. https://doi.org/10.31893/jabb.2024002

[1] Aluru N, Vijayan MM (2009) Stress transcriptomics in fish: A role for genomic cortisol. General Comparative Endocrinology 164:142–50. https://doi.org/10.1016/j.ygcen.2009.03.020

[2] Brandão A, Cooke R (2021) Effects of Temperament on the Reproduction of Beef Cattle. Animals 11:3325. https://doi.org/10.3390/ani11113325

[3] Cabrera F (2012) Variables neuroendocrinas y su relación con el comportamiento durante la lidia del toro bravo, (Bos taurus L.) (PhD Thesis) Facultad de Veterinaria- Universidad Complutense de Madrid. https://hdl.handle.net/20.500.14352/37148 (accessed on: July 18, 2023)

[4] Colditz GI, Hine, BC (2016) Resilience in farm animals: biology, management, breeding, and implications for animal welfare. Animal Production Science 56:1961-1983. https://doi.org/10.1071/AN15297

[5] Cooke RF, Arthington JD, Austin BR, Yelich, JV (2009) Effects of acclimation to handling on performance, reproductive, and physiological responses of Brahman-crossbred heifers. Journal of Animal Science 87:3403–3412. https://doi.org/10.2527/jas.2009-1910

[6] Cooke RF, Bohnert DW, Cappellozza BI, Mueller CJ, Delcurto T (2012) Effects of temperament and acclimation to handling on reproductive performance of Bos taurus beef females. Journal of Animal Science 90:3547–3555. https://doi.org/10.2527/jas.2011-4768

[7] Correia P, Baron E, Moreira da Silva F, Cortés O (2017) Mitochondrial and Y chromosome genetic diversity in the Portuguese Lidia bovine breed. Revista Brasileira de Zootecnia 46:99-104. https://doi.org/10.1590/S1806-92902017000200003

[8] Dobson H, Smith R (2000) What is stress, and how does it affect reproduction? Animal Reproduction Science 60-61:743-752. https://doi.org/10.1016/S0378-4320(00)00080-4

[9] Dobson H, Fergani C, Routly JE, Smith RF (2012) Effects of stress on reproduction in ewes. Animal Reproduction Science 130:135–140. https://doi.org/10.1016/j.anireprosci.2012.01.006

[10] Drost M, Thatcher WW (1987) Heat stress in dairy cows. Its effect on reproduction. Veterinary Clinics of North America: Food Animal Practice 3:609–618. https://doi.org/10.1016/S0749-0720(15)31133-6

[11] Duong TH, Pitrowska KK, Bah MM, Sinderewicz E, Majewska M, Jankowska K, Okuda K, Skarzynski DJ (2012) Effects of cortisol on pregnancy rate and corpus luteum function in heifers: an in vivo study. Journal of Reproduction and Development 58:223–230. https://doi.org/10.1262/jrd.11-122T

[12] Fisher AD, Crowe MA, Alonso de la Varga ME, Enright WJ (1996) Effect of castration method and the provision of local anaesthesia on plasma cortisol, scrotal circumference, growth, and feed intake of bull calves. Journal of Animal Science 74:2336-2343. https://doi.org/10.2527/1996.74102336x

[13] Grandin T (1997) Assessment of stress during handling and transport. Journal of Animal Science 75:249-257. https://doi.org/10.2527/1997.751249x

[14] Güldenpfennig J, Schmicke M, Hoedemaker M, Siebert U, Keuling O (2021) An approach to assess stress in response to drive hunts using cortisol levels of wild boar (Sus scrofa) Scientific Reports 11:16381. https://doi.org/10.1038/s41598-021-95927-2

[15] Hall NL, Buchanan DS, Anderson V L, Ilse B R, Carlin KR, Berg, EP (2011) Working chute behavior of feedlot cattle can be an indication of cattle temperament and beef carcass composition and quality. Meat Science, 89:52–57. https://doi.org/10.1016/j.meatsci.2011.03.020

[16] Hughes HD, Carroll JA, Burdick Sanchez NCB, Richeson JT (2014) Natural variations in the stress and acute phase responses of cattle. Innate immunity 20:888–896. https://doi.org/10.1177/1753425913508993

[17] Jeffus J, Reuter R, Wagner K, Goodman L, Parker T (2021) 5 Effects of Virtual Fencing on Cortisol Concentrations and Behavior of Beef Cattle. Journal of Animal Science 99:1-2. https://doi.org/10.1093/jas/skab235.001

[18] Kalin NH, Shelton SE, Turner JG (1992) Effects of !b-carboline on fear-related behavioral and neurohormonal responses in infant rhesus monkeys. Biological Psychiatry 31:1008–1019. https://doi.org/10.1016/0006-3223(92)90094-G

[19] Kim WS, Lee JS, Jeon SW, Peng DQ, Kim YS, Bae MH, Jo YH, Lee HG (2018) Correlation between blood, physiological and behavioral parameters in beef calves under heat stress. Asian-Australasian Journal of Animal sciences 31: 919–925. https://doi.org/10.5713/ajas.17.0545

[20] Korchia J, Freeman KP (2021) Validation study of canine urine cortisol measurement with the Immulite 2000 Xpi cortisol immunoassay. Journal of Veterinary Diagnostic Investigation 33:1051-1068.

[21] Lee C, Colditz IG, Campbell DLM (2018) A Framework to Assess the Impact of New Animal Management Technologies on Welfare: A Case Study of Virtual Fencing. Frontiers In Veterinary Science 21:187.

[22] Ley SJ, Waterman AE, Livingston A (1996) Measurement of mechanical thresholds, plasma cortisol and catecholamines in control and lame cattle: A preliminary study. Research in Veterinary Science 61:172-173. https://doi.org/10.1016/S0034-5288(96)90096-X

[23] Lowman BG, Scott NA, Somerville SH (1976) Condition Scoring of Cattle. Bull. 6. East of Scotland College of Agriculture 6:31. Edinburgh, UK. https://pasture.io/farm-animal-health/body-condition-scoring (accessed on 5 September, 2023)

[24] McEwen BS, Stellar E (1993) Stress and the individual. Mechanisms leading to disease. Archives of Internal Medicine 153:2093–2101.

[25] Miranda-de la Lama GC, Sepúlveda WS, Villarroel M, & María GA (2011) Livestock vehicle accidents in Spain: causes, consequences, and effects on animal welfare. Journal of Applied Animal Welfare Science 14:109–123. https://doi.org/10.1080/10888705.2011.551622

[26] Molony V, Kent J, Robertson I (1993) Behavioural responses of lambs of three ages in the first three hours after three methods of castration and tail docking. Research in Veterinary Science 55:236-245. https://doi.org/10.1016/0034-5288(93)90087-V

[27] Wrangham RW, Muller MN (2004) Dominance, cortisol and stress in wild chimpanzees (Pan troglodytes schweinfurthii) Behavioral Ecology and Sociobiology 55:332-340. http://dx.doi.org/10.1007/s00265-003-0713-1

[28] Ortiga-Carvalho TM, Chiamolera MI, Pazos-Moura CC, Wondisford FE (2016) Hypothalamus-Pituitary-Thyroid Axis. Comprehensive Physiology 6:1387–1428. https://doi.org/10.1002/cphy.c150027

[29] Pacheco-Lima J, Moreira da Silva J (2019a) Reproductive Characterization of The Bovine Lidia Called “Brava Dos Açores”. Biomedical Journal of Scientific and Technical Research 15:1. https://doi:10.26717/BJSTR.2019.15.002632

[30] Pacheco-Lima J, Silva H, Campillo Beneitez JP, Fernandes da Silva D, Moreira da Silva F (2019b) Effect of Vaccination Against Ibr/Bvd on The Reproductive Performances of Brava Dos Açores -A Bovine Lidia Breed. American Journal of Biomedical Science and Research 6:266-272.

[31] Parent J, Chapdelaine P, Sirois J, Fortier MA (2002) Expression of microsomal prostaglandin E synthase in bovine endometrium: coexpression with cyclooxygenase type 2 and regulation by interferon-tau. Endocrinology 143(8):2936-2943. https://doi.org/10.1210/endo.143.8.8969

[32] Rausch, WD, Hofer A, Gemeiner M, Möstl E (1989) Catecholamine and cortisol concentrations in plasma from cattle at parturition]. Zentralblatt fur Veterinarmedizin 36(3): 218–224.

[33] Richeson JT, Hughes HD, Broadway PR, Carroll JA (2019) Vaccination Management of Beef Cattle: Delayed Vaccination and Endotoxin Stacking. Veterinary Clinics of North America Food Animal Practice 35:575–592. https://doi.org/10.1016/j.cvfa.2019.07.003

[34] Rizzo A, Minoia G, Trisolini C, Manca R, Sciorsci RL (2007) Concentrations of free radicals and beta-endorphins in repeat breeder cows. Animal Reproduction Science 100: 257–263.

[35] Roth Z (2018) Symposium review: Reduction in oocyte developmental competence by stress is associated with alterations in mitochondrial function. Journal of Dairy Science 101(4): 3642–3654. https://doi.org/10.3168/jds.2017-13389

[36] Sánchez J, Castro M, Alonso M, Gaudioso (1996) Adaptive metabolic responses in females of the fighting breed submitted to different sequences of stress stimuli. Physiology and Behavior 60(4): 1047-1052. https://doi.org/10.1016/0031-9384(96)00160-6

[37] Seth S, Lewis AJ, Galbally M (2016) Perinatal maternal depression and cortisol function in pregnancy and the postpartum period: a systematic literature review. BMC Pregnancy and Childbirth 16(1): 124. https://doi.org/10.1186/s12884-016-0915-y

[38] Shenavai S, Preissing S, Hoffmann B, Dilly M, Pfarrer C, Özalp GR, Caliskan C, Seyrek-Intas K, Schuler G (2012) Investigations into the mechanisms controlling parturition in cattle. Reproduction (Cambridge, England), 144(2), 279–292. https://doi.org/10.1530/REP-11-0471

[39] Souza JMG, Batista R, Melo LM, Freitas VJ (2011) Reproductive biotechnologies applied to the conservation of endangered ruminant - past, present, and future. Revista Portuguesa de Ciências Agrárias 106: 31-38.

[40] Stilwell, G. (2012) Scientific Opinion on the welfare of cattle kept for beef production and the welfare in intensive calf farming systems. EFSA Journal 10(5): 2669. http://dx.doi.org/10.2903/j.efsa.2012.2669

[41] Tucker CB, Coetzee JF, Stookey JM, Thomson DU, Grandin T, Schwartzkopf-Genswein SK (2015) Beef cattle welfare in the USA: identification of priorities for future research. Animal Health Research Reviews 16(2) 107-124. https://doi.org/10.1017/S1466252315000171

[42] Vale S, Selinger L, Martins JM, Gomes AC, Bicho M, Carmo I, Escera C (2014) The relationship between dehydroepiandrosterone (DHEA), working memory and distraction – A behavioral and electrophysiological approach. PloS One 9(8) e104869. https://doi.org/10.1371/journal.pone.0104869

Abstract

References

How to cite