Hostname: page-component-8448b6f56d-42gr6 Total loading time: 0 Render date: 2024-04-19T23:25:04.828Z Has data issue: false hasContentIssue false

Seasonal effects on plasma cortisol concentrations in the Bedouin buck: circadian studies and response to ACTH

Published online by Cambridge University Press:  11 August 2016

N. Chergui*
Affiliation:
Laboratoire de Recherches sur les Zones Arides (LRZA), Faculty of Biology, Houari Boumediene University of Sciences and Technology (USTHB), PB 39, El Alia, Algiers, 16110, Algeria
P. Mormede
Affiliation:
Nutrition et Neurobiologie Intégrée (NutriNeuro), Institut National de la Recherche Agronomique (INRA), F-33076 Bordeaux, France
A. Foury
Affiliation:
Nutrition et Neurobiologie Intégrée (NutriNeuro), Institut National de la Recherche Agronomique (INRA), F-33076 Bordeaux, France
F. Khammar
Affiliation:
Laboratoire de Recherches sur les Zones Arides (LRZA), Faculty of Biology, Houari Boumediene University of Sciences and Technology (USTHB), PB 39, El Alia, Algiers, 16110, Algeria
Z. Amirat
Affiliation:
Laboratoire de Recherches sur les Zones Arides (LRZA), Faculty of Biology, Houari Boumediene University of Sciences and Technology (USTHB), PB 39, El Alia, Algiers, 16110, Algeria
*
Get access

Abstract

Our work aims at the exploration of cortisol secretion in the Bedouin goat, native to the Algerian Sahara desert, to understand the mechanisms of adaptation to extreme hot climates. In the present study, diurnal and seasonal variations of cortisol concentrations were measured in basal conditions, as well as the response to ACTH stimulation tests across seasons in bucks. The plasma concentrations of cortisol showed no diurnal cycle but a large variation across seasons. The highest levels occurred in summer and winter when the environmental conditions are at their extreme levels. The rectal temperature showed nychthemeral and seasonal variations, and BW was also different across seasons with highest values in summer and lowest in winter. The results obtained after administration of two doses (2 or 10 μg/kg BW) of synthetic ACTH to three different age groups (kids, adults and elderly animals) showed a strong increase in plasma cortisol concentrations under all conditions with maximum levels achieved between 15 and 120 min. The analysis of the area under the cortisol curve showed no significant difference between the responses to the two doses of ACTH and between age groups, but showed seasonal variations with the lowest response in autumn than in other seasons. We conclude that season significantly affects secretion of cortisol in both basal state and under ACTH stimulation. However, the variation of adrenal reactivity to ACTH is not sufficient to explain seasonal differences, and in particular the summer peak in basal circulating cortisol concentrations. Further research should focus on the respective contribution of environmental factors (such as day length, temperature, humidity) and the mechanisms involved in cortisol regulation.

Type
Research Article
Copyright
© The Animal Consortium 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

a Present address: Génétique, Physiologie et Systèmes d’Elevage (GenPhySE), INRA, F-31326 Castanet-Tolosan, France.

References

Aboul-Naga, A, Osman, MA, Alary, V, Hassan, F, Daoud, I and Tourrand, JF 2014. Raising goats as adaptation process to long drought incidence at the Coastal Zone of Western Desert in Egypt. Small Ruminant Research 121, 106110.Google Scholar
Al-Busaidi, R, Johnson, EH and Mahgoub, O 2008. Seasonal variations of phagocytic response, immunoglobulin G (IgG) and plasma cortisol levels in Dhofari goats. Small Ruminant Research 79, 118123.Google Scholar
Alila-Johansson, A, Eriksson, L, Soveri, T and Laakso, M-L 2003. Serum cortisol levels in goats exhibit seasonal but not daily rhythmicity. Chronobiology International 20, 6579.Google Scholar
Alila-Johansson, A, Eriksson, L, Soveri, T and Laakso, M-L 2006. The daily rhythms of melatonin and free fatty acids in goats under varying photoperiods and constant darkness. Chronobiology International 23, 565581.Google Scholar
Al-Samawi, KA, Al-Hassan, MJ and Swelum, AA 2014. Thermoregulation of female Aardi goats exposed to environmental heat stress in Saudi Arabia. Indian Journal of Animal Research 48, 344349.CrossRefGoogle Scholar
Amirat, Z, Khammar, F and Brudieux, R 1980. Seasonal changes in plasma and adrenal concentrations of cortisol, corticosterone, aldosterone, and electrolytes in the adult male sand rat (Psammomys obesus). General and Comparative Endocrinology 40, 3643.Google Scholar
Amirat, Z, Lakdari, Y and Khammar, F 2001. Cycle saisonnier de I’activité sexuelle chez le bouc de race Bédouine (Seasonal cycle of sexual activity in male Bedouin goat). Rencontres Autour des Recherches sur les Ruminants 8, 373.Google Scholar
Barenton, B, Ravault, J-P, Chabanet, C, Daveau, A, Pelletier, J and Ortavant, R 1988. Photoperiodic control of growth hormone secretion and body weight in rams. Domestic Animal Endocrinology 5, 247255.Google Scholar
Blum, ID, Lamont, EW and Abizaid, A 2012. Competing clocks: metabolic status moderates signals from the master circadian pacemaker. Neuroscience and Biobehavioral Reviews 36, 254270.Google Scholar
Cahill, S, Tuplin, E and Holahan, MR 2013. Circannual changes in stress and feeding hormones and their effect on food-seeking behaviors. Frontiers in Neuroscience 7, 140.CrossRefGoogle ScholarPubMed
Campos, PHRF, Noblet, J, Jaguelin-Peyraud, Y, Gilbert, H, Mormede, P, Donzele RFM de, O, Donzele, JL and Renaudeau, D 2014. Thermoregulatory responses during thermal acclimation in pigs divergently selected for residual feed intake. International Journal of Biometeorology 58, 15451557.Google Scholar
Carcangiu, V, Giannetto, C, Luridiana, S, Fazio, F, Mura, MC, Parmeggiani, A and Piccione, G 2015. Seasons induce changes in the daily rhythm of plasma melatonin in goats (Capra hircus). Animal Biology 65, 1320.Google Scholar
Choshniak, I, Ben-Kohav, N, Taylor, CR, Robertshaw, D, Barnes, RJ, Dobson, A, Belkin, V and Shkolnik, A 1995. Metabolic adaptations for desert survival in the Bedouin goat. American Journal of Physiology 268, R1101R1110.Google Scholar
Dangi, SS, Gupta, M, Maurya, D, Yadav, VP, Panda, RP, Singh, G, Mohan, NH, Nitai, H, Bhure, SK, Das, BC, Bag, S, Mahapatra, R, Taru Sharma, G and Sarkar, M 2012. Expression profile of HSP genes during different seasons in goats (Capra hircus). Tropical Animal Health and Production 44, 19051912.Google Scholar
Desautes, C, Bidanel, JP and Mormede, P 1997. Genetic study of behavioral and pituitary-adrenocortical reactivity in response to an environmental challenge in pigs. Physiology and Behavior 62, 337345.Google Scholar
Dickmeis, T, Weger, BD and Weger, M 2013. The circadian clock and glucocorticoids – interactions across many time scales. Molecular and Cellular Endocrinology 380, 215.Google Scholar
Ebling, FJP 2015. Hypothalamic control of seasonal changes in food intake and body weight. Frontiers in Neuroendocrinology 37, 97107.Google Scholar
Ebling, FJP and Lincoln, GA 1987. Beta-endorphin secretion in rams related to season and photoperiod. Endocrinology 120, 809818.Google Scholar
El-Husseini, M and Haggag, G 1974. Antidiuretic hormone and water conservation in desert rodents. Comparative Biochemistry and Physiology Part A: Physiology 47, 347350.Google Scholar
Fulkerson, WJ and Tang, BY 1979. Ultradian and circadian rhythms in the plasma concentration of cortisol in sheep. Journal of Endocrinology 81, 135141.Google Scholar
Haggag, G and El-Husseini, M 1974. The adrenal cortex and water conservation in desert rodents. Comparative Biochemistry and Physiology Part A: Physiology 47, 351359.CrossRefGoogle ScholarPubMed
Johnson, HD and Vanjonack, WJ 1976. Effects of environmental and other stressors on blood hormone patterns in lactating animals. Journal of Dairy Science 59, 16031617.Google Scholar
Katoh, K, Yoshida, M, Kobayashi, Y, Onodera, M, Kogusa, K and Obara, Y 2005. Responses induced by arginine-vasopressin injection in the plasma concentrations of adrenocorticotropic hormone, cortisol, growth hormone and metabolites around weaning time in goats. Journal of Endocrinology 187, 249256.Google Scholar
Kokkonen, U, Riskila, P, Roihankorpi, M and Soveri, T 2001. Circadian variation of plasma atrial natriuretic peptide, cortisol and fluid balance in the goat. Acta Physiologica Scandinavica 171, 18.Google Scholar
Kumar, R, Pramod, RK, Kumar, R, Negi, M, Singh, SP, Singh, R and Mitra, A 2014. Testicular biometry and seasonal variations in semen parameters of Black Bengal goats. Indian Journal of Animal Science 84, 635639.Google Scholar
Larzul, C, Terenina, E, Foury, A, Billon, Y, Louveau, I, Merlot, E and Mormede, P 2015. The cortisol response to ACTH in pigs, heritability and influence of corticosteroid-binding globulin. Animal 9, 19291934.Google Scholar
Lee, JA, Roussel, JD and Beatty, JF 1976. Effect of temperature-season on bovine adrenal cortical function, blood cell profile, and milk production. Journal of Dairy Science 59, 104108.Google Scholar
Malpaux, B, Migaud, M, Tricoire, H and Chemineau, P 2001. Biology of mammalian photoperiodism and the critical role of the pineal gland and melatonin. Journal of Biological Rhythms 16, 336347.Google Scholar
Maltz, E, Silanikove, N and Shkolnik, A 2009. Energy cost and water requirement of black Bedouin goats at different levels of production. Journal of Agricultural Science 98, 499504.Google Scholar
Marple, DN, Aberle, ED, Forrest, JC, Blake, WH and Judge, MD 1972. Effects of humidity and temperature on porcine plasma adrenal corticoids, ACTH and growth hormone levels. Journal of Animal Science 34, 809812.Google Scholar
Mesbah, S and Brudieux, R 1982. Diurnal variation of plasma concentrations of cortisol, aldosterone and electrolytes in the ram. Hormone and Metabolic Research 14, 320323.Google Scholar
Meza-Herrera, CA, Bocanegra, JA, Banuelos, R, Arechiga, CF, Rincon, RM, Ochoa-Cordero, MA, Juarez-Reyes, AS, Cerrillo-Soto, MA and Salinas, H 2007. Circannual fluctuations in serum cortisol and glucose concentrations and hair coat growth in goats. Journal of Applied Animal Research 31, 7982.Google Scholar
Minka, NS and Ayo, JO 2012. Assessment of thermal load on transported goats administered with ascorbic acid during the hot-dry conditions. International Journal of Biometeorology 56, 333341.Google Scholar
Mormede, P, Andanson, S, Auperin, B, Beerda, B, Guemene, D, Malmkvist, J, Manteca, X, Manteuffel, G, Prunet, P, van Reenen, CG, Richard, S and Veissier, I 2007. Exploration of the hypothalamic-pituitary-adrenal function as a tool to evaluate animal welfare. Physiology and Behavior 92, 317339.Google Scholar
Mormede, P and Terenina, E 2012. Molecular genetics of the adrenocortical axis and breeding for robustness. Domestic Animal Endocrinology 43, 116131.CrossRefGoogle ScholarPubMed
Pevet, P and Challet, E 2011. Melatonin: both master clock output and internal time-giver in the circadian clocks network. Journal of Physiology, Paris 105, 170182.Google Scholar
Pruessner, JC, Kirschbaum, C, Meinlschmid, G and Hellhammer, DH 2003. Two formula for the computation of the area under the curve represent measures of total hormone concentration versus time-dependent change. Psychoneuroendocrinology 28, 916931.Google Scholar
Redondo, E, Franco, A, Garcia, A and Masot, AJ 2010. Changes in concentrations of cortisol and melatonin in plasma, expression of synaptophysin, and ultrastructural properties of pinealocytes in goat kids in situations of stress due to early weaning: the effect of melatonin. New Zealand Veterinary Journal 58, 160167.Google Scholar
Reinberg, A, Touitou, Y, Levi, F and Nicolai, A 1983. Circadian and seasonal changes in ACTH-induced effects in healthy young men. European Journal of Clinical Pharmacology 25, 657665.Google Scholar
Rhind, SM and McMillen, SR 1995. Seasonal changes in systemic hormone profiles and their relationship to patterns of fibre growth and moulting in goats of contrasting genotypes. Australian Journal of Agricultural Research 46, 12731283.Google Scholar
Romero, M 2002. Seasonal changes in plasma glucocorticoid concentrations in free-living vertebrates. General and Comparative Endocrinology 128, 124.Google Scholar
Shamay, A, Mabjeesh, S, Shapiro, F and Silanikove, N 2000. Adrenocorticotrophic hormone and dexamethasone failed to affect milk yield in dairy goats: comparative aspects. Small Ruminant Research 38, 255259.Google Scholar
Sharma, S, Ramesh, K, Hyder, I, Uniyal, S, Yadav, VP, Panda, RP, Maurya, VP, Singh, G, Kumar, P, Mitra, A and Sarkar, M 2013. Effect of melatonin administration on thyroid hormones, cortisol and expression profile of heat shock proteins in goats (Capra hircus) exposed to heat stress. Small Ruminant Research 112, 216223.Google Scholar
Silanikove, N 2000. The physiological basis of adaptation in goats to harsh environments. Small Ruminant Research 35, 181193.CrossRefGoogle Scholar
Silanikove, N, Tagari, H and Shkolnik, A 1993. Comparison of rate of passage, fermentation rate and efficiency of digestion of high fiber diet in desert Bedouin goats compared to Swiss Saanen goats. Small Ruminant Research 12, 4560.Google Scholar
Ssewannyana, E, Lincoln, GA, Linton, EA and Lowry, PJ 1990. Regulation of the seasonal cycle of β-endorphin and ACTH secretion into the peripheral blood of rams. Journal of Endocrinology 124, 443454.Google Scholar
Todini, L, Terzano, GM, Borghese, A, Debenedetti, A and Malfatti, A 2011. Plasma melatonin in domestic female Mediterranean sheep (Comisana breed) and goats (Maltese and Red Syrian). Research in Veterinary Science 90, 3539.CrossRefGoogle ScholarPubMed
Tong, YL 1976. Parameter estimation in studying circadian rhythms. Biometrics 32, 8594.CrossRefGoogle ScholarPubMed
Torres-Farfan, C, Valenzuela, FJ, Mondaca, M, Valenzuela, GJ, Krause, B, Herrera, EA, Riquelme, R, Llanos, AJ and Seron-Ferre, M 2008. Evidence of a role for melatonin in fetal sheep physiology: direct actions of melatonin on fetal cerebral artery, brown adipose tissue and adrenal gland. Journal of Physiology 586, 40174027.Google Scholar
Yagil, R and Etzion, Z 1979. The role of antidiuretic hormone and aldosterone in the dehydrated and rehydrated camel. Comparative Biochemistry and Physiology Part A: Physiology 63, 275278.Google Scholar
Zarazaga, LA, Guzmán, JL, Domínguez, C, Pérez, MC and Prieto, R 2009. Effects of season and feeding level on reproductive activity and semen quality in Payoya buck goats. Theriogenology 71, 13161325.CrossRefGoogle ScholarPubMed