Metabolic changes during brief periods of ewe–lamb separation at different agesP. Mora-Medina A , A. Orihuela-Trujillo B , P. Roldan-Santiago C , E. Arch-Tirado D , C. Vázquez-Cruz E and D. Mota-Rojas C F
A PhD Program in Biological Sciences and Health, Universidad Autónoma Metropolitana Xochimilco–Iztapalapa–Cuajimalpa, México, DF Calzada del Hueso, 1100, Colonia. Villa Quietud, Delegation Coyoacán, 04960, México.
B Faculty of Agriculture and Livestock Sciences, Universidad Autónoma del Estado of Morelos, México, Avenida. Universidad 1001, Colonia. Chamilpa, Cuernavaca, Morelos, 62209, México.
C Stress Physiology and Farm Animal Welfare, Department of Animal Production and Agriculture, Universidad Autónoma Metropolitana, México, DF Calzada del Hueso 1100, Colonia. Villa Quietud, Delegation Coyoacán, 04960, México.
D Laboratory of Bioacoustics, Instituto Nacional de Rehabilitation, México, DF, Calzada., México Xochimilco No. 289, Colonia. Arenal de Guadalupe, 14389, México.
E Universidad Nacional Autónoma de México, Facultad de Estudios Superiores Cuautitlán, Cuautitlán Izcalli, Estado de México, 54714, México.
Animal Production Science - https://doi.org/10.1071/AN16221
Submitted: 11 April 2016 Accepted: 18 November 2016 Published online: 23 February 2017
The present study evaluated metabolic changes in lambs during three brief periods of ewe–lamb separation, namely 1 min (T1), 10 min (T10) and 60 min (T60). The lambs were divided by age into the following three groups: 15 days (G1 = 40 lambs), 30 days (G2 = 40 lambs) and 60 days (G3 = 40 lambs). The hypothesis to be tested was that breaking the ewe–lamb bond at different ages and for these brief time periods will cause significant metabolic changes in the lambs. To this end, blood samples were taken from the three test groups 24 h before separation to establish reference values (RVs), and again at the end of the three separation times. The following blood variables were analysed for all three study groups: glucose (mg/dL), lactate (mg/dL), calcium (Ca2+, mmol/L), sodium (Na+, mmol/L), potassium (K+, mmol/L), haematocrit (HTC, %), pCO2 (mmHg), pO2 (mmHg), HCO3– (mmol/L) and pH. Results showed that the G1 lambs suffered the greatest metabolic changes for the variables pO2, pCO2, glucose, lactate, pH, HCO3–, Ca2+, Na+, K+ and HCT. With respect to time, the first 10 min of separation from the mother induced marked metabolic changes in the 15-, 30- and 60-day-old lambs, but, at 60 min, the G2 and G3 lambs tended to recover their physiological RVs, while the G1 lambs did not. These findings showed that breaking the ewe–lamb bond immediately generated metabolic changes in the lambs even though they remained in a familiar, habitual environment. They also indicated that the age of the lambs at separation was a significant factor, as the older animals tended to re-establish their RVs after the metabolic changes, likely because their physiological compensating mechanisms are more efficient, or perhaps because the intensity of attachment to the mother decreases with greater age.
Additional keywords: animal welfare, blood profle, physiological response, stress, weaning.
ReferencesAlonso-Spilsbury M, Mota-Rojas D, Villanueva-García D, Martínez-Burnes J, Orozco H, Ramírez-Necoechea R, López-Mayagoitia A, Trujillo-Ortega ME (2005) Perinatal asphyxia pathophysiology in pig and human: a review. Animal Reproduction Science 90, 1–30.
| Perinatal asphyxia pathophysiology in pig and human: a review.CrossRef |
Arch-Tirado E, Collado-Corona MA (2002) Análisis de vocalizaciones en cobayos recién nacidos, normoyentes y con sordera provocada en períodos de soledad. Cirugia y Cirujanos 70, 442–448.
Barth E, Albuszies G, Baumgart K, Matejovic M, Wachter U, Vogt J, Radermacher P, Calzia E (2007) Glucose metabolism and catecholamines. Critical Care Medicine 35, S508–S518.
| Glucose metabolism and catecholamines.CrossRef | 1:CAS:528:DC%2BD2sXptlKgs74%3D&md5=5970a0d68a206b4819f0af96a3cb3508CAS |
Becerril-Herrera M, Alonso-Spilsbury M, Lemus-Flores C, Guerrero-Legarreta I, Olmos-Hernández A, Ramírez-Necoechea R, Mota-Rojas D (2009) CO2 stunning may compromise swine welfare compared with electrical stunning. Meat Science 81, 233–237.
| CO2 stunning may compromise swine welfare compared with electrical stunning.CrossRef | 1:CAS:528:DC%2BD1cXht1eisrvO&md5=7d873cbe87a1b96e848891e3644c510aCAS |
Bergamasco L, Macchi E, Facello C, Badino P, Odore R, Pagliasso S, Bellino C, Osella M, Re G (2005) Effects of brief maternal separation in kids on neurohormonal an electroencephalographic parameters. Applied Animal Behaviour Science 93, 39–52.
| Effects of brief maternal separation in kids on neurohormonal an electroencephalographic parameters.CrossRef |
Bessho T, Taira S, Koyama K (1997) Effect of respiratory acidosis on body movements in the chronically instrumented fetal lamb. Acta Obstetricia et Gynecologica Scandinavica 76, 200–204.
| Effect of respiratory acidosis on body movements in the chronically instrumented fetal lamb.CrossRef | 1:STN:280:DyaK2s3ks12rtA%3D%3D&md5=52d933afd2d30da73de58241476f8d21CAS |
Bockenhauer D, Zieg J (2014) Electrolyte disorders. Clinics in Perinatology 41, 575–590.
| Electrolyte disorders.CrossRef |
Coulon M, Hild S, Schroeer A, Janczak AM, Zanella AJ (2011) Gentle vs. aversive handling of pregnant ewes: II. Physiology and behavior of the lambs. Physiology & Behavior 103, 575–584.
| Gentle vs. aversive handling of pregnant ewes: II. Physiology and behavior of the lambs.CrossRef | 1:CAS:528:DC%2BC3MXntFWitLk%3D&md5=58210a0f875159e2570aa240f37ad7feCAS |
Desborough JP (2000) The stress response to trauma ans surgery. British Journal of Anaesthesia 85, 109–117.
| The stress response to trauma ans surgery.CrossRef | 1:STN:280:DC%2BD3czptFSltw%3D%3D&md5=11e04949abee382cb87ea36eff60a542CAS |
DiBartola SP (2012) Disorders of sodium and water: hypernatremia and hyponatremia. In ‘Fluid, electrolyte, and acid-base disorders in small animal practice’. (Ed. SP DiBartola) pp. 45–79. (WB Saunders: Saint Louis, MI)
Fazio F, Casella S, Giudice E, Giannetto C, Piccione G (2015) Evaluation of secondary stress biomarkers during road transport in rabbit. Livestock Science 173, 106–110.
| Evaluation of secondary stress biomarkers during road transport in rabbit.CrossRef |
Fazio F, Arfuso F, Giudice E, Giannetto C, Piccione G (2016) Physiological differences between twin and single-born lambs and kids during the first month of life. Archives Animal Breeding 59, 201–207.
| Physiological differences between twin and single-born lambs and kids during the first month of life.CrossRef |
Freitas-de-Melo A, Ungerfeld R (2016) Artificial weaning in sheep: stress response and animal welfare. Revista Mexicana de Ciencias Pecuarias 7, 361–375. [Review]
Galeana L, Orihuela A, Aguirre V, Vázquez R (2007) Mother–young spatial association and its relation with proximity to a fence separating ewes and lambs during enforced weaning in hair sheep (Ovis aries). Applied Animal Behaviour Science 108, 81–88.
| Mother–young spatial association and its relation with proximity to a fence separating ewes and lambs during enforced weaning in hair sheep (Ovis aries).CrossRef |
Gladden L (2004) Lactate metabolism: a new paradigm for the third millennium. The Journal of Physiology 558, 5–30.
| Lactate metabolism: a new paradigm for the third millennium.CrossRef | 1:CAS:528:DC%2BD2cXmtFWhsLg%3D&md5=b1960db967d2434e2589a89d96603db0CAS |
Hinch GN, Lynch JJ, Elwin RL, Green GC (1990) Long-term associations between Merino ewes and their offspring. Applied Animal Behaviour Science 27, 93–103.
| Long-term associations between Merino ewes and their offspring.CrossRef |
Houpt RT (1984) Water, electrolytes, and acid-base balance. In ‘Duke’s physiology of domestic animals’. (Ed. MJ Swenson) pp. 486–506. (Cornell University Press: Ithaca, NY)
Ježek J, Klopčič M, Klinkon M (2006) Influence of age on biochemical parameters in calves. Bulletin of the Veterinary Institute in Pulawy 50, 211–214.
Kohari D, Namikawa S, Tanaka M (2014) How do visual and auditory cues influence calf stress reactions at weaning? Animal Science Journal 85, 336–341.
| How do visual and auditory cues influence calf stress reactions at weaning?CrossRef |
Lefcourt AM, Elsasser TH (1995) Adrenal responses of Angus × Hereford cattle to the stress of weaning. Journal of Animal Science 73, 2669–2676.
| Adrenal responses of Angus × Hereford cattle to the stress of weaning.CrossRef | 1:CAS:528:DyaK2MXotFWqurk%3D&md5=9e69624b2c9db5923a5bc931ca76ea17CAS |
Maldonado A, Orihuela A, Aguirre V, Vázquez R, Flores-Pérez I (2015) Changes in mother-offspring relationships with the increasing age of the lamb in hair sheep (Ovis aries). Journal of Veterinary Behavior 10, 166–170.
| Changes in mother-offspring relationships with the increasing age of the lamb in hair sheep (Ovis aries).CrossRef |
Manning AM (2001) Electrolyte disorders. The Veterinary Clinics of North America. Small Animal Practice 31, 1289–1321.
| Electrolyte disorders.CrossRef | 1:STN:280:DC%2BD3MnotF2ntQ%3D%3D&md5=832eec954ebc728e15208c3e403a680aCAS |
Marchant-Forde JN, Marchant-Forde RM, Weary DM (2002) Responses of dairy cows and calves to each other’s vocalisations after early separation. Applied Animal Behaviour Science 78, 19–28.
| Responses of dairy cows and calves to each other’s vocalisations after early separation.CrossRef |
Martínez-Rodríguez R, Roldan-Santiago P, Orozco-Gregorio H, Trujillo-Ortega M, Mora-Medina P, González-Lozano M, Sánchez-Hernández M, Bonilla-Jaime H, García-Herrera R, Hernández-Trujillo ME, Mota-Rojas D (2015) Physiological responses and blood gas exchange following long-distance transport of piglets weaned at different ages over unpaved or paved roads. Livestock Science 172, 69–78.
| Physiological responses and blood gas exchange following long-distance transport of piglets weaned at different ages over unpaved or paved roads.CrossRef |
Mears GJ, Brown FA (1997) Cortisol and b-endorphin responses to physical and psychological stressors in lambs. Canadian Journal of Animal Science 77, 689–694.
| Cortisol and b-endorphin responses to physical and psychological stressors in lambs.CrossRef | 1:CAS:528:DyaK1cXitlajsb4%3D&md5=f021e3bde4e555e07b57b9194e82e732CAS |
Mendoza-Lara M, Orozco-Gregorio H, Ramírez-Necoechea R, Caballero-Chacón S, Hernández-Gonzalez R, Becerril-Herrera M, Mora-Medina P, Mota-Rojas D (2012) Physiometabolic profile of Belgian Malinois shepherd and Dutch shepherd dogs in response to a training session for French ring. Archivos de Medicina Veterinaria 44, 137–144.
| Physiometabolic profile of Belgian Malinois shepherd and Dutch shepherd dogs in response to a training session for French ring.CrossRef | 1:CAS:528:DC%2BC38XhsFags7%2FK&md5=90a3a3c5c01b0caa6d61bdbcad208efbCAS |
Minton JE (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.
Moberg GP (2000) Biological response to stress: implications for animal welfare. In ‘The biology of animal stress: basic principles and implications for animal welfare’. (Eds GP Moberg, JA Mench) pp. 1–21. (CABI publishing: New York, NY)
Mora-Medina P, Mota-Rojas D, Arch-Tirado E, Orozco-Gregorio H (2015) Animal welfare in lambs: ewe-lamb separation. Large Animal Review 21, 39–44.
Mora-Medina P, Orihuela A, Arch-Tirado E, Roldan-Santiago P, Terrazas A, Mota-Rojas D (2016) Sensory factors involved in mother-young bonding in sheep: a review. Veterinarni Medicina 61, 595–611.
| Sensory factors involved in mother-young bonding in sheep: a review.CrossRef |
Mota-Rojas D, Orozco-Gregorio H, Villanueva-Garcia D, Bonilla-Jaime H, Suárez-Bonilla X, Hernandez-Gonzalez R, Roldan-Santiago P, Trujillo-Ortega ME (2011) Foetal and neonatal energy metabolism in pigs and humans: a review. Veterinarni Medicina 56, 215–225.
Mota-Rojas D, Becerril-Herrera M, Roldan-Santiago P, Alonso-Spilsbury M, Flores-Peinado S, Ramírez-Necoechea R, Ramírez-Telles JA, Mora-Medina P, Pérez M, Molina E, Soní E, Trujillo-Ortega ME (2012a) Effects of long distance transportation and CO2 stunning on critical blood values in pigs. Meat Science 90, 893–898.
| Effects of long distance transportation and CO2 stunning on critical blood values in pigs.CrossRef | 1:CAS:528:DC%2BC38XosF2lsg%3D%3D&md5=de8a706f6119de32e0021ba6bd324ae3CAS |
Mota-Rojas D, Martínez-Burnes J, Villanueva-Garcia D, Roldan-Santiago P, Trujillo-Ortega ME, Orozco-Gregorio H, Bonilla-Jaime H, Lopez-Mayagoitia A (2012b) Animal welfare in the newborn piglet: a review. Veterinarni Medicina 57, 338–349.
Mota-Rojas D, Villanueva-García D, Hernández-González R, Roldan-Santiago P, Martínez-Rodríguez R, González-Meneses B, Sánchez-Hernández M, Trujillo-Ortega ME (2012c) Assessment of the vitality of the newborn: an overview. Scientific Research and Essays 7, 712–718.
| Assessment of the vitality of the newborn: an overview.CrossRef |
Norouzian MA (2015) Effect of weaning method on lamb behaviour and weight gain. Small Ruminant Research 133, 17–20.
| Effect of weaning method on lamb behaviour and weight gain.CrossRef |
Orgeur P, Bernard S, Naciri M, Nowak R, Schaal B, Levy F (1999) Psychobiological consequences of two different weaning methods in sheep. Reproduction, Nutrition, Development 39, 231–244.
| Psychobiological consequences of two different weaning methods in sheep.CrossRef | 1:STN:280:DyaK1M3lvFCgtw%3D%3D&md5=8df230aad357a3e9db76a4acefb3e1a4CAS |
Orozco-Gregorio H, Mota-Rojas D, Alonso-Spilsbury M, Olmos-Hernández A, Ramírez-Necoechea R, Velázquez-Armenta EY, Nava-Ocampo AA, Hernández-González R, Trujillo-Ortega ME, Villanueva-García D (2008) Short-term neurophysiologic consequences of intrapartum asphyxia in piglets born by spontaneous parturition. The International Journal of Neuroscience 118, 1299–1315.
| Short-term neurophysiologic consequences of intrapartum asphyxia in piglets born by spontaneous parturition.CrossRef | 1:CAS:528:DC%2BD1cXpslKnsL8%3D&md5=7ab72fd212592ac95c0edac15e8be4b1CAS |
Otovic P, Hutchinson E (2015) Limits to using hpa axis activity as an indication of animal welfare. ALTEX 32, 41–50.
Pérez EC, Elie JE, Soulage CO, Soula HA, Mathevon N, Vignal C (2012) The acoustic expression of stress in a songbird: does corticosterone drive isolation-induced modifications of zebra finch calls? Hormones and Behavior 61, 573–581.
| The acoustic expression of stress in a songbird: does corticosterone drive isolation-induced modifications of zebra finch calls?CrossRef |
Piccione G, Costa A, Bertolucci C, Borruso M, Pennisi P, Caola G (2006) Acid–base balance modifications in the lamb and goat kids during the first week of life. Small Ruminant Research 63, 304–308.
| Acid–base balance modifications in the lamb and goat kids during the first week of life.CrossRef |
Piccione G, Borruso M, Fazio F, Giannetto C, Caola G (2007) Physiological parameters in lambs during the first 30 days postpartum. Small Ruminant Research 72, 57–60.
| Physiological parameters in lambs during the first 30 days postpartum.CrossRef |
Piccione G, Arfuso F, Faggio C, Casella S, Zumbo A, Panzera M (2013) Serum proteins profile in Comisana lambs during the first month of life Giuseppe. Archiv fur Tierzucht 56, 742–750.
Pörtner HO, Grieshaber MK (1993) Critical pO2(s) in oxyconforming and oxyregulating animals gas exchange, metabolic rate and the mode of energy production. In ‘The vertebrate gas transport cascade adaptations to environment and mode of life’. (Ed. JEPW Bicudo) pp. 330–357. (CRC Press: Boca Raton, FL)
Robinson EN (2009) Función respiratoria. Homeostasia acido-básica. In ‘Fisiología veterinaria’. (Ed. JG Cunningham) pp. 468, 524, 527. (Elsevier: España, Spain)
Roldan-Santiago P, Martínez-Rodríguez R, Yánez-Pizaña A, Trujillo-Ortega ME, Sánchez-Hernández M, Pérez-Pedraza E, Mota-Rojas D (2013) Stressor factors in the transport of weaned piglets: a review. Veterinarni Medicina 58, 241–251.
Roldan-Santiago P, Trujillo-Ortega M, Borderas-Tordesillas F, Martínez-Rodríguez R, Mora-Medina P, Flores-Peinado S, Sánchez-Hernández M, García-Herrera R, González-Lozano M, Mota-Rojas D (2015) Physiometabolic responses to road transport in weaned piglets for a short period and the effects of straw bedding. Animal Science Journal 86, 563–571.
| Physiometabolic responses to road transport in weaned piglets for a short period and the effects of straw bedding.CrossRef |
Ruffin VA, Salameh AI, Boron WF, Parker MD (2014) Intracellular pH regulation by acid–base transporters in mammalian neurons. Frontiers in Physiology 5, 43
| Intracellular pH regulation by acid–base transporters in mammalian neurons.CrossRef |
SAS (2004) ‘SAS version 9.2.’ (SAS Institute, Inc.: Cary, NC)
Soares PC, do Rêgo Leal ML, Satisuki-Mori C, Araripe-Sucupira MC, Lippi-Ortolani E (2012) Blood gas profile of copper-poisoned in sheep treated with ammonium tetrathiomolybdate. Semina. Ciências Agrárias 33, 731–740.
| Blood gas profile of copper-poisoned in sheep treated with ammonium tetrathiomolybdate.CrossRef | 1:CAS:528:DC%2BC38XptFehsL0%3D&md5=f63c5c8eff1cc028bd3d8b49bcf3612eCAS |
Tadich N, Mendez G, Wittwer F, Meyer K (1997) Blood biochemical values of loadcart draught horses in the city of Valdivia (Chile). Archivos de Medicina Veterinaria 29, 45–53.
Trujillo-Ortega ME, Mota-Rojas D, Juárez O, Villanueva-García D, Roldan-Santiago P, Becerril-Herrera M, Hernández-González R, Mora-Medina P, Alonso-Spilsbury M, Rosales AM, Martínez-Rodríguez R, Ramírez-Necoechea R (2011) Porcine neonates failing vitality score: physio-metabolic profile and latency to the first teat contact. Czech Journal of Animal Science 56, 499–508.
Ungerfeld R, Hötzel MJ, Scarsi A, Quintans G (2011) Behavioral and physiological changes in early-weaned multiparous and primiparous beef cows. Animal 5, 1270–1275.
| Behavioral and physiological changes in early-weaned multiparous and primiparous beef cows.CrossRef | 1:STN:280:DC%2BC38vovV2ntw%3D%3D&md5=d2f859b35d7f94f148846ffcc039f1a2CAS |
Vannucchi CI, Rodrigues JA, Silva LCG, Lúcio CF, Veiga GAL (2012) A clinical and hemogasometric survey of neonatal lambs. Small Ruminant Research 108, 107–112.
| A clinical and hemogasometric survey of neonatal lambs.CrossRef |
Vázquez-Galindo G, de Aluja AS, Guerrero-Legarreta I, Orozco-Gregorio H, Borderas-Tordesillas F, Mora-Medina P, Roldan-Santiago P, Flores-Peinado S, Mota-Rojas D (2013) Adaptation of ostriches to transport-induced stress: physiometabolic response. Animal Science Journal 84, 350–358.
| Adaptation of ostriches to transport-induced stress: physiometabolic response.CrossRef |