PLANT BIOLOGY
ANIMAL BIOLOGY
SUBSCRIPTION
E-SUBSCRIPTION
 
MAP
MAIN PAGE

 

 

 

 

Abilov A.I., Gudilina A.A., Kombarova N.A., Turbina V.V., Korneenko-Zhilyaev Yu.A. Cortisol as a marker of physiological stress in Bos taurus sires. Sel'skokhozyaistvennaya Biologiya [Agricultural Biology], 2024, Vol. 59, № 2, p. 301-315.
(how to cite this article)

doi: 10.15389/agrobiology.2024.2.301eng

UDC: 636.2:636.082:577.175.534

 

CORTISOL AS A MARKER OF PHYSIOLOGICAL STRESS IN Bos taurus SIRES

A.I. Abilov1, A.A. Gudilina1, N.A. Kombarova2 ✉, V.V. Turbina1,
Yu.A. Korneenko-Zhilyaev1

1Ernst Federal Research Center for Animal Husbandry, 60, pos. Dubrovitsy, Podolsk District, Moscow Province, 142132 Russia, e-mail ahmed.abilov@mail.ru, v.turbina@oaohcr.ru, serafima_venera@mtu-net.ru, info@vij.ru;
2Head Center for Reproduction of Farm Animals AO, 3, ul. Tsentralnaya, pos. Bykovo, Podolsk Region, Moscow Province, 142143 Russia, e-mail komnina@list.ru (✉ corresponding author), csio-secr@yandex.ru

ORCID:
Abilov A.I. orcid.org/0000-0001-6236-8634
Turbina V.V. orcid.org/0000-0003-1039-0375
Kombarova N.A. orcid.org/0000-0003-3861-4465
Kornienko-Zhilyaev Yu.A. orcid.org/0000-0003-3554-2240
Gudilina A.A. orcid.org/0000-0002-7962-5315

Final revision received October 5, 2023  
Accepted November 3, 2023

 

The endocrine mechanism in animal stress has not yet been fully elucidated. Social stress due to hierarchy in the herd increases the production of cortisol, catecholamines, can affect sexual behavior and fertility, and reduce productivity. Despite the enormous importance of the problem for breeding enterprises involved in the production and cryopreservation of sperm of farm animals for commercial and scientific purposes, there are no special studies to investigate the connection of the qualitative and quantitative parameters of the ejaculate and its fertilizing ability with the post-ejaculatory cortisol level. In the presented work, we revealed for the first time that the effectiveness of artificial insemination is directly proportional to the concentration of blood cortisol in stud bulls after ejaculation. In young stud bulls, stress associated with blood sampling dominated; in adult bulls, sexual arousal suppressed stress caused by this veterinary manipulation. For the first time, we find out the dependence of the fertilizing capability of the bull sperm on the post-ejaculation blood cortisol level. We assessed the pattern of post-ejaculation cortisol concentration in 11 Holstein bulls of foreign selection aged 29-71 months (holding JSC GCV, a subsidiary breeding enterprise of JSC Uralplemtsentr, Sverdlovsk region, 2018-2021) which are exploited according to approved technology and determined the fertilizing rate of the cryopreserved resulting sperm as influenced by the blood cortisol level. In both young and adult animals, there was a significant positive dynamics of cortisol in response to blood sampling. The average blood cortisol concentration in young sires (n = 6) under stress from this regular manipulation increased evenly and reached 70.8; 91.1 and 144.7 nmol/l on the days of three consecutive doublet collections of semen after 4-5-day intervals. In bulls (n = 5) older than 4 years, the peak concentration of cortisol (172.5 nmol/l) occurred in the second semen collection, and by the third collection, there was a slight decrease in the cortisol level, by 5 %. As post-ejaculation blood cortisol increases, the number of spermatozoa per ejaculate increases. In young bulls, after three consecutive double collections of semen at 4-5 day intervals, 4.0, 5.5 and 6.2 billion spermatozoa per ejaculation were obtained, in sires over 4-year old, 6.6, 7.3 and 7.5 billion sperm. The sperm from sires with the highest post-ejaculation levels of cortisol released into the bloodstream (162-216 nmol/l) exhibited the best fertilizing rate, 59-60 % (p < 0.001).

Keywords: sires, cortisol, ejaculation, sperm production, stress, artificial insemination.

 

REFERENCES

  1. Collier R.J., Renquist B.J., Xiao Y. A 100-year review: stress physiology including heat stress. J. Dairy Sci., 2017, 100(12): 10367-10380 CrossRef
  2. Lynch E.M. Characterisation of Physiological and immune-related biomarkers of weaning stress in beef cattle. Ph.D. Thesis. National University of Ireland, Maynooth, Ireland, 2010.
  3. Brown E.J., Vosloo A. The involvement of the hypothalamopituitary-adrenocortical axis in stress physiology and its significance in the assessment of animal welfare in cattle. Onderstepoort J. Vet. Res., 2017, 84(1): e1-e9 CrossRef
  4. Yukomzan E.V. E-Scio, 2022, 1(64): 309-324 (in Russ.).
  5. Kosyachenko N.M., Konovalov A.V., Il’ina A.V., Kononov D.V. Ispol’zovanie stressoustoychivosti i povedencheskikh funktsiy krupnogo rogatogo skota pri sovremennykh tekhnologiyakh proizvodstva moloka: monografiya [Use of stress resistance and behavioral functions of cattle under modern milk production technologies: а monograph]. Yaroslavl’, 2013 (in Russ.).
  6. Collier R.J., Gebremedhin K.G. Thermal biology of domestic animals. Annu. Rev. Anim. Biosci., 2015, 3(1): 513-532 CrossRef
  7. Etim N.N., Williams M.E., Evans E.I., Offiong E.E. Physiological and Behavioural Responses of Farm Animals to Stress: Implications to Animal Productivity American Journal of Advanced Agricultural Research (AJAAR), 2013, 1(2): 53-61.
  8. Bova T.L., Chiavaccini L., Cline G.F., Hart C.G., Matheny K., Muth A.M., Voelz B.E., Kesler D., Memili E. Environmental stressors influencing hormones and systems physiology in cattle. Reprod. Biol. Endocrinol., 2014, 12: 58 CrossRef
  9. Kolesnikova L.R., Makarova O.A., Natyaganova L.V., Dolgikh M.I., Korytov L.I. Acta Biomedica Scientifica, 2018, 3(6): 15-22 CrossRef (in Russ.).
  10. Shchuko A.G., Veselov A.A., Yur’eva T.N., Volkova N.V., Shabanov G.A., Rybchenko A.A., Pochtarenko T.V. Sibirskiy nauchnyy meditsinskiy zhurnal, 2017, 37(4): 26-36 (in Russ.).
  11. Chu B., Marwaha K., Sanvictores T., Ayers D. Physiology, stress reaction. StatPearls Publishing, 2019.
  12. Sharypova N.V., Sveshnikov A.A. Polovaya funktsiya u muzhchin i sostoyanie menstrual’nogo tsikla u zhenshchin pri khronicheskom deystvii stress-faktorov chrezvychaynoy intensivnosti: monografiya [Sexual function in men and the state of the menstrual cycle in women under chronic stress factors of extreme intensity: monograph]. Izdatel’skiy dom «Akademiya Estestvoznaniya», Penza, 2013 (in Russ.).
  13. Sapolsky R.M. The influence of social hierarchy on primate health. Science, 2005, 308(5722): 648-652 CrossRef
  14. Val-Laillet D., de Passille A.M., Rushen J., von Keyserlingk M.A.G. The concept of social dominance and the social distribution of feeding-related displacements between cows. Applied Animal Behaviour Science, 2008, 111(1): 158-172. CrossRef
  15. Sel’e G. Ocherki ob adaptatsionnom sindrome [Essays on adaptation syndrome]. Moscow, 1960 (in Russ.).
  16. Ernst L.K., Dzhaparidze T.G., Varnavskiy A.N. Molochnoe i myasnoe skotovodstvo, 2008, 4: 5-8 (in Russ.).
  17. Lenzi A., Lombardo F., Salacone P., Gandini L., Jannini E.A. Stress, sexual dysfunctions, and male infertility. J. Endocrinol. Invest., 2003, 26(3 Suppl): 72-76.
  18. Abilov A.I., Eskin G.V., Kombarova N.A. Blood estradiol level in bull sires influences sperm count and effectiveness of artificial insemination. Sel'skokhozyaistvennaya biologiya [Agricultural Biology], 2016, 51(6): 830-836 CrossRef 
  19. Abilov A.I., Mityashova O.S., Mymrin S.V., Gudilina A.A., Pyzhova E.A., Kombarova N.A., Levina G.N. Endogenous hormone level in bull sires in relation to age, autoimmune status, and production performance of maternal ancestors. Sel'skokhozyaistvennaya biologiya [Agricultural Biology], 2018, 53(4): 743-752 CrossRef
  20. Silva W.C., Silva J.A.R., Camargo-Júnior R.N.C., Silva É.B.R., Santos M.R.P., Viana R.B., Silva A.G.M., Silva C.M.G., Lourenço-Júnior J.B. Animal welfare and effects of per-female stress on male and cattle reproduction — a review. Front. Vet. Sci., 2023, 10: 1083469 CrossRef  
  21. Gusakova E.A., Gorodetskaya I.V. Vestnik VGMU, 2020, 19(1): 24-35 CrossRef (in Russ.).
  22. Kovyazina N.A., Alkhutova N.A. Klinicheskaya laboratornaya diagnostika, 2019, 64(3): 140-144 CrossRef (in Russ.).
  23. Xiong X., Wu Q., Zhang L., Gao S., Li R., Han L., Fan M., Wang M., Liu L., Wang X., Zhang C., Xin Y., Li Z., Huang C., Yang J. Chronic stress inhibits testosterone synthesis in Leydig cells through mitochondrial damage via Atp5a1. Journal of Cellular and Molecular Medicine, 2022, 26(2): 354-363 CrossRef
  24. Al’-Shukri S.Kh., Borovets S.Yu., Toropov V.A. Urologicheskie vedomosti, 2016. VI(1): 21-28 CrossRef (in Russ.).
  25. Abilov A.I., Kombarova N.A., Amerkhanov Kh.A., Shemetyuk S.A., Shamshidin A.S., Mymrin S.V., Pyzhova E.A., Bogolyubova N.V., Gudilina A.A., Abilova S.F., Kombarov P.G., Mityashova O.S. Metabolic profiles and sperm production in imported holstein bull sires under different climatic and geochemical conditions of Russia and Kazakhstan. Sel'skokhozyaistvennaya biologiya [Agricultural Biology], 2021, 56(4): 730-751 CrossRef
  26. Ermakova I.V. Novye issledovaniya, 2014, 4(41: 77-86 (in Russ.).
  27. Malenka R.C., Nestler E.J., Hyman S.E. Molecular neuropharmacology: a foundation for clinical neuroscience (2nd ed.). McGraw-Hill Medical, New York, 2009: 246-259.
  28. Mormède P., Andanson S., Aupérin B., Beerda V., Guémené D., Malmkvist J., Manteca X., Manteuffel G., Prunet P., van Reenen C.G., Richard S., Veissier I. Exploration of the hypothalamic—pituitary—adrenal function as a tool to evaluate animal welfare. Physiology & Behavior, 2007, 92(3): 317-339 CrossRef
  29. Chen Y., Arsenault R., Napper S., Griebel P. Models and methods to investigate acute stress responses in cattle. Animals, 2015, 5(4): 1268-1295 CrossRef
  30. Ramamoorthy S., Cidlowski J.A. Corticosteroids: mechanisms of action in health and disease. Rheumatic Diseases Clinics of North America, 2016, 42(1): 15-31 CrossRef
  31. Binsiya T., Sejian V., Bagath M., Krishnan G., Hyder I., Manimaran A., Lees A., Gaughan J., Bhatta R. Significance of hypothalamic—pituitary—adrenal axis to adapt to climate change in livestock.International Research Journal of Agricultural and Food Sciences, 2017, 2(1): 1-20.
  32. Kholl Dzh. E. Meditsinskaya fiziologiya po Gaytonu i Khollu [Medical physiology by Guyton and Hall]. 2-e izd. Moscow, 2018 (in Russ.).
  33. Caldwell J.D., Jirikowski G.F. Sex hormone binding globulin and corticosteroid binding globulin as major effectors of steroid action. Steroids, 2014, 81: 13-16 CrossRef
  34. Burdick N.C., Randel R.D., Carroll J.A., Welsh T.H. Interactions between temperament, stress, and immune function in cattle. International Journal of Zoology, 2011, 2011: Article ID 373197 CrossRef
  35. Kim L.U., D’Orsogna M.R., Chou T. Onset, timing, and exposure therapy of stress disorders: mechanistic insight from a mathematical model of oscillating neuroendocrine dynamics. Biology Direct, 2016, 11: article number 13 CrossRef
  36. Artemova E.V. Ozhirenie i metabolizm, 2017, 2017, 14(2): 48-52 CrossRef (in Russ.).
  37. Lishmanov Yu.B., Maslov L.N., Naryzhnaya N.V., Pey Zhan-ming, Kolar F., Zhang I., Portnichenko A.G., Vang Kh. Vestnik RAMN, 2012, 6: 73-92 CrossRef (in Russ.).
  38. Tkachuk V.A., Vorotnikov A.V. Sakharnyy diabet, 2014, 2: 29-34 CrossRef (in Russ.).
  39. Viru A., Viru M. Cortisol — essential adaptation hormone in exercise. Int. J, Sports Med., 2004, 25(6): 461-464 CrossRef
  40. Encyclopedia of human behavior (2nd ed.). V.S. Ramachandran (ed.). Academic Press, 2012.
  41. Morozov V.N., Khadartsev A.A. Vestnik novykh meditsinskikh tekhnologiy, 2010, XVII(1): 5-17 (in Russ.).
  42. Suarez-Trujillo A., Hoang N., Robinson L., McCabe C.J., Conklin D., Minor R.C., Townsend J., Plaut K., George U.Z., Boerman J., Casey T.M. Effect of circadian system disruption on the concentration and daily oscillations of cortisol, progesterone, melatonin, serotonin, growth hormone, and core body temperature in periparturient dairy cattle. J. Dairy Sci., 2022, 105(3): 2651-2668 CrossRef
  43. Fatima N., Rana S. Metabolic implications of circadian disruption. Pflugers Archiv: European Journal of Physiology, 2020, 472(5): 513–526 CrossRef
  44. Amstislavskaya T.G. Psikhofarmakologiya i biologicheskaya narkologiya, 2008, 8(1-2/1): 2271-2279 (in Russ.).
  45. Thüer S., Mellema S., Doherr M.G., Wechsler B., Nuss K., Steiner A. Effect of local anaesthesia on short- and long-term pain induced by two bloodless castration methods in calves. Vet. J., 2007, 173: 333-342 CrossRef
  46. Huszenicza G., Jánosi S., Gáspárdy A., Kulcsár M. Endocrine aspects in pathogenesis of mastitis in postpartum dairy cows. Anim. Reprod. Sci., 2004, 82-83: 389-400 CrossRef
  47. Almeida P.E., Weber P.S., Burton JL., Zanella A.J. Depressed DHEA and increased sickness response behaviors in lame dairy cows with inflammatory foot lesions. Domestic Animal Endocrinology, 2008, 34(1): 89-99 CrossRef
  48. Forslund K.B., Ljungvall O.A., Jones B.V. Low cortisol levels in blood from dairy cows with ketosis: a field study. Acta Vet. Scand., 2010 ,52(1): 31 CrossRef
  49. Ciobotaru E. Spontaneous diabetes mellitus in animals. In: Diabetes mellitus — insights and perspectives. O.O. Oguntibeju (ed.). Intech, 2013: 271-296 CrossRef
  50. Beerda B., Kornalijnslijper J.E., van der Werf J.T., Noordhuizen-Stassen E.N., Hopster H. Effects of milk production capacity and metabolic status on HPA function in early postpartum dairy cows. J. Dairy Sci., 2004, 87(7): 2094-2102 CrossRef
  51. de Boer G., Trenkle A., Young J.W. Glucagon, insulin, growth hormone, and some blood metabolites during energy restriction ketonemia of lactating cows. J. Dairy Sci., 1985, 68(2): 326-337 CrossRef
  52. Veterinary medicine: a textbook of the diseases of cattle, horses, sheep, pigs and goats. 10th Edition. Elsevier Saunders, London, 2007.
  53. Moyes K.M., Drackley J.K., Salak-Johnson J.L, Morin D.E., Hope J.C., Loor J.J. Dietary-induced negative energy balance has minimal effects on innate immunity during a Streptococcus uberis mastitis challenge in dairy cows during midlactation. J. Dairy Sci., 2009, 92: 4301-4316 CrossRef
  54. Dzhaparov E.K., Derkho M.A. Uchenye zapiski KGAVM im. N.E. Baumana, 2019, 3: 110-117 CrossRef (in Russ.).
  55. Kubasov R.V. Gormonal’nye izmeneniya v otvet na ekstremal’nye faktory vneshney sredy Vestnik Rossiyskoy akademii meditsinskikh nauk, 2014, 69(9-10): 102-109 CrossRef (in Russ.).
  56. Fernandez-Novo A., Pérez-Garnelo S.S., Villagrá A., Pérez-Villalobos N., Astiz S. The effect of stress on reproduction and reproductive technologies in beef cattle — a review. Animals, 2020, 10(11), 2096 CrossRef
  57. Kuznetsova E.A., Adamchik A.S., Goncharov N.P., Katsiya G.V. Andrologiya i genital’naya khirurgiya, 2016, 17(1): 26-31 CrossRef (in Russ.).
  58. van der Meij L., Demetriou A., Tulin M., Méndez I., Dekker P., Pronk T. Hormones in speed-dating: the role of testosterone and cortisol in attraction. Hormones and Behavior, 2019, 116: 104555 CrossRef
  59. Phoenix C.H., Dixson A.F., Resko J.A. Effects of ejaculation on levels of testosterone, cortisol, and luteinizing hormone in peripheral plasma of rhesus monkeys. Journal of Comparative and Physiological Psychology, 977, 91(1): 120-127 CrossRef
  60. Alomar M., Soukouti A., Alzoabi M.A., Zarkawi M. Testosterone and cortisol patterns and the effects of electro-ejaculation and copulation in Awassi rams. Archives Animal Breeding, 2016, 59(1): 139-144 CrossRef
  61. Veronesi M.C., Tosi U., Villani M., Govoni N., Faustini M., Kindahl H.,  Carluccio A. Oxytocin, vasopressin, prostaglandin F(2a), luteinizing hormone, testosterone, estrone sulfate, and cortisol Theriogenology, 2010, 73(4), 460-467 CrossRef
  62. Veronesi M.C., De Amicis I., Panzani S., Kindahl H., Govoni N., Probo M., Carluccio A. PGF(2a), LH, testosterone, oestrone sulphate, and cortisol plasma concentrations around sexual stimulation in jackass. Theriogenology, 2011, 75(8): 1489-1498 CrossRef
  63. Natsional’naya tekhnologii zamorazhivaniya i ispol’zovanie spermy plemennykh bykov-proizvoditeley /Pod redaktsiey A.I. Abilova, N.M. Reshetnikovoy [National technology of freezing and use of semen of bulls sires. A.I. Abilov, N.M. Reshetnikova (eds.)]. Moscow, 2008 (in Russ.).
  64. Khabarov S.V., Sterlikova N.A. Vestnik novykh meditsinskikh tekhnologiy, 2022, 29(3): 17-31 CrossRef (in Russ.).
  65. Thun R., Eggenberger E., Zerobin K., Lüscher T., Vetter W. Twenty-four-hour secretory pattern of cortisol in the bull: evidence of episodic secretion and circadian rhythm. Endocrinology, 1981, 109(6): 2208-2212 CrossRef
  66. Lee D.Y., Kim E., Choi M.H. Technical and clinical aspects of cortisol as a biochemical marker of chronic stress. BMB Reports, 2015, 48(4): 209-216 CrossRef
  67. Lightman S.L., Birnie M.T., Conway-Campbell B.L. Dynamics of ACTH and cortisol secretion and implications for disease. Endocrine Reviews, 2020, 41(3): bnaa002 CrossRef
  68. Huang Y.M., Chi C.W., Wu P.S., Tai H.C., Chien M.N., Chen Y.J. Adrenal gland irradiation causes fatigue accompanied by reactive changes in cortisol levels. J. Clin. Med., 2022, 11(5): 1214 CrossRef
  69. Borg K.E., Esbenshade K.L., Johnson B.H. Cortisol, growth hormone, and testosterone concentrations during mating behavior in the bull and boar.Journal of Animal Science, 1991, 69(8): 3230-3240 CrossRef
  70. Bishop J.D., Malven P.V., Singleton W.L., Weesner G.D. Hormonal and behavioural correlates of emotional states in sexually trained boars. Journal of Animal Science, 77(12), 3339-3345 CrossRef

 

back

 


CONTENTS

 

 

Full article PDF (Rus)

Full article PDF (Eng)