Effects of heat stress on in vivo and in vitro ruminal metabolism in fat-tailed ewes
A. Amini A , R. Pirmohammadi , H. Khalilvandi-Behroozyar * and R. Mazaheri-KhamenehA Animal Science Department, Faculty of Agriculture, Urmia University, Urmia, Iran.
B Surgery and Diagnostic Imaging Department, Faculty of Veterinary Medicine, Urmia University, Urmia, Iran.
Animal Production Science 62(9) 860-869 https://doi.org/10.1071/AN20625
Submitted: 21 November 2020 Accepted: 24 March 2022 Published: 17 May 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Context: Interest in studying heat stress (HS) has increased significantly due to the problems associated with increasing global warming. Heat stress has very destructive effects on the health and performance of livestock.
Aims: Our objective was to investigate the effects of heat stress on in vivo and in vitro ruminal metabolism in fat-tailed Iranian sheep.
Methods: Fourteen intact non-lactating and non-pregnant mature fat-tailed Makoei ewes (67.5 ± 2.5 kg BW) were kept indoors for 24 h/day and randomly assigned to HS (33.0–41.0°C and a temperature–humidity index (THI) of ≥83 for 24 h/day) or thermoneutral (TN; 24.5 ± 2.3°C and a THI of 66.1 ± 2.5) condition in two consecutive experimental periods. At the end of first experimental period, the animals in each group were exchanged with another group. The ewes were fed a total mixed ration two times a day, composed of lucerne hay (33%) and corn silage (1:2) to meet their maintenance metabolisable energy and protein requirements.
Key results: HS ewes had lower dry-matter (DM) intake than did TN ewes (P < 0.05). HS increased the in vivo DM, organic matter (OM) and neutral detergent fiber digestibility (P < 0.05), but crude protein digestibility was not affected. Total volatile fatty acid concentration and pH were not affected by HS. However, propionate molar percentage was increased and N-NH3 concentration was decreased by HS. In vitro gas production of three different tested feeds was lower in rumen fluid collected from HS than that from TN group, but DM and OM digestibility and methane emission were decreased only in the case of Orchard grass (P < 0.05).
Conclusions and implications: In general, HS had detrimental effects on DM intake and in vitro nutrient digestibility but increased in vivo nutrient digestibility, and changed microbial population.
Keywords: fat tailed ewes, feed intake, forage digestion, heat stress, microbial community, methane emission, nutrient digestibility, ruminal metabolism.
References
Albright JL, Alliston CW (1971) Effects of varying the environment upon the performance of dairy cattle. Journal of Animal Science 32, 566–577.| Effects of varying the environment upon the performance of dairy cattle.Crossref | GoogleScholarGoogle Scholar |
Ankom (1998) Procedures for fibre and in vitro analysis. Available at http://www.ankom.com.
AOAC (2000) ‘Official methods of analysis.’ Vol. I. 17th edn. (AOAC: Arlington, VA, USA)
Baumgard LH, Rhoads RP (2013) Effects of heat stress on postabsorptive metabolism and energetics. Annual Review of Animal Biosciences 1, 311–337.
| Effects of heat stress on postabsorptive metabolism and energetics.Crossref | GoogleScholarGoogle Scholar | 25387022PubMed |
Baumgard LH, Rhoads RP, Rhoads ML, Gabler NK, Ross JW, Keating AF, Boddicker RL, Lenka S, Sejian V (2012) Impact of climate change on livestock production. In ‘Environmental stress and amelioration in livestock production’. (Eds V Sejian, SMK Naqvi, T Ezeji, J Lakritz, R Lal) pp. 413–468. (Springer)
| Crossref |
Bernabucci U (2012) Impact of hot environment on nutrient requirements. In ‘Environmental physiology of livestock’. (Eds RJ Collier, JL Collier) pp. 101–128. (John Wiley & Sons, Inc.)
| Crossref |
Bernabucci U, Lacetera N, Danieli PP, Bani P, Nardone A, Ronchi B (2009) Influence of different periods of exposure to hot environment on rumen function and diet digestibility in sheep. International Journal of Biometeorology 53, 387–395.
| Influence of different periods of exposure to hot environment on rumen function and diet digestibility in sheep.Crossref | GoogleScholarGoogle Scholar | 19370363PubMed |
Bernabucci U, Lacetera N, Baumgard LH, Rhoads RP, Ronchi B, Nardone A (2010) Metabolic and hormonal acclimation to heat stress in domesticated ruminants. Animal 4, 1167–1183.
| Metabolic and hormonal acclimation to heat stress in domesticated ruminants.Crossref | GoogleScholarGoogle Scholar | 22444615PubMed |
Broderick GA, Kang JH (1980) Automated simultaneous determination of ammonia and total amino acids in ruminal fluid and in vitro media. Journal of Dairy Science 63, 64–75.
| Automated simultaneous determination of ammonia and total amino acids in ruminal fluid and in vitro media.Crossref | GoogleScholarGoogle Scholar | 7372898PubMed |
Buffington DE, Collazo-Arocho A, Canton GH, Pitt D, Thatcher WW, Collier RJ (1981) Black globe-humidity index (BGHI) as comfort equation for dairy cows. Transactions of the ASAE 24, 0711–0714.
| Black globe-humidity index (BGHI) as comfort equation for dairy cows.Crossref | GoogleScholarGoogle Scholar |
Cardoso CC, Peripolli V, Amador SA, et al. (2015) Physiological and thermographic response to heat stress in zebu cattle. Livestock Science 182, 83–92.
| Physiological and thermographic response to heat stress in zebu cattle.Crossref | GoogleScholarGoogle Scholar |
Chaidanya K, Soren NM, Sejian V, Bagath M, Gundallahalli BM, Kurien EK, Varma G, Bhatta R (2017) Impact of heat stress, nutritional stress and combined (heat and nutritional) stresses on rumen associated fermentation characteristics, histopathology and HSP70 gene expression in goats. Journal of Animal Behaviour and Biometeorology 5, 36–48.
| Impact of heat stress, nutritional stress and combined (heat and nutritional) stresses on rumen associated fermentation characteristics, histopathology and HSP70 gene expression in goats.Crossref | GoogleScholarGoogle Scholar |
Christopherson R (1985) The thermal environment and the ruminant digestive system. In ‘Stress physiology in livestock. Vol. 1. Basic principles’. (Ed. MK Yousef) pp. 163–187. (CRC Press: Boca Raton, FL, USA)
Conte G, Ciampolini R, Cassandro M, Lasagna E, Calamari L, Bernabucci U, Abeni F (2018) Feeding and nutrition management of heat-stressed dairy ruminants. Italian Journal of Animal Science 17, 604–620.
| Feeding and nutrition management of heat-stressed dairy ruminants.Crossref | GoogleScholarGoogle Scholar |
Czerkawski JW (2013) ‘An introduction to rumen studies.’ (Elsevier)
Denman SE, McSweeney CS (2006) Development of a real-time PCR assay for monitoring anaerobic fungal and cellulolytic bacterial populations within the rumen. FEMS Microbiology Ecology 58, 572–582.
| Development of a real-time PCR assay for monitoring anaerobic fungal and cellulolytic bacterial populations within the rumen.Crossref | GoogleScholarGoogle Scholar | 17117998PubMed |
Dixon RM, Thomas R, Holmes JHG (1999) Interactions between heat stress and nutrition in sheep fed roughage diets. The Journal of Agricultural Science 132, 351–359.
| Interactions between heat stress and nutrition in sheep fed roughage diets.Crossref | GoogleScholarGoogle Scholar |
Fievez V, Babayemi O, Demeyer D (2005) Estimation of direct and indirect gas production in syringes: A tool to estimate short chain fatty acid production that requires minimal laboratory facilities. Animal Feed Science and Technology 123, 197–210.
| Estimation of direct and indirect gas production in syringes: A tool to estimate short chain fatty acid production that requires minimal laboratory facilities.Crossref | GoogleScholarGoogle Scholar |
Hamzaoui S, Salama AAK, Albanell E, Such X, Caja G (2013) Physiological responses and lactational performances of late-lactation dairy goats under heat stress conditions. Journal of Dairy Science 96, 6355–6365.
| Physiological responses and lactational performances of late-lactation dairy goats under heat stress conditions.Crossref | GoogleScholarGoogle Scholar | 23958010PubMed |
Houseknecht KL, Baile CA, Matteri RL, Spurlock ME (1998) The biology of leptin: a review. Journal of Animal Science 76, 1405–1420.
| The biology of leptin: a review.Crossref | GoogleScholarGoogle Scholar | 9621947PubMed |
Indira D, Srividya G (2012) Reducing the livestock related green house gases emission. Veterinary World 5, 244–247.
| Reducing the livestock related green house gases emission.Crossref | GoogleScholarGoogle Scholar |
Jouany J-P (1996) Effect of rumen protozoa on nitrogen utilization by ruminants. The Journal of Nutrition 126, 1335S–1346S.
| Effect of rumen protozoa on nitrogen utilization by ruminants.Crossref | GoogleScholarGoogle Scholar | 8642481PubMed |
Kadzere CT, Murphy MR, Silanikove N, Maltz E (2002) Heat stress in lactating dairy cows: a review. Livestock Production Science 77, 59–91.
| Heat stress in lactating dairy cows: a review.Crossref | GoogleScholarGoogle Scholar |
Koike S, Kobayashi Y (2001) Development and use of competitive PCR assays for the rumen cellulolytic bacteria: Fibrobacter succinogenes, Ruminococcus albus and Ruminococcus flavefaciens. FEMS Microbiology Letters 204, 361–366.
| Development and use of competitive PCR assays for the rumen cellulolytic bacteria: Fibrobacter succinogenes, Ruminococcus albus and Ruminococcus flavefaciens.Crossref | GoogleScholarGoogle Scholar | 11731149PubMed |
Mahjoubi E, Amanlou H, Hossein Yazdi M, Aghaziarati N, Noori GR, Vahl CI, Bradford BJ, Baumgard LH (2016) A supplement containing multiple types of gluconeogenic substrates alters intake but not productivity of heat-stressed Afshari lambs. Journal of Animal Science 94, 2497–2505.
| A supplement containing multiple types of gluconeogenic substrates alters intake but not productivity of heat-stressed Afshari lambs.Crossref | GoogleScholarGoogle Scholar | 27285926PubMed |
Marai IFM, El-Darawany AA, Fadiel A, Abdel-Hafez MAM (2007) Physiological traits as affected by heat stress in sheep: a review. Small Ruminant Research 71, 1–12.
| Physiological traits as affected by heat stress in sheep: a review.Crossref | GoogleScholarGoogle Scholar |
Menke HH, Steingass H (1988) Estimation of the energetic feed value obtained from chemical analysis and in vitro gas production using rumen fluid. Animal Research and Development 28, 7–55.
Menke KH, Raab L, Salewski A, Steingass H, Fritz D, Schneider W (1979) The estimation of the digestibility and metabolizable energy content of ruminant feedingstuffs from the gas production when they are incubated with rumen liquor in vitro. The Journal of Agricultural Science 93, 217–222.
| The estimation of the digestibility and metabolizable energy content of ruminant feedingstuffs from the gas production when they are incubated with rumen liquor in vitro.Crossref | GoogleScholarGoogle Scholar |
Ngwabie NM, Jeppsson K-H, Gustafsson G, Nimmermark S (2011) Effects of animal activity and air temperature on methane and ammonia emissions from a naturally ventilated building for dairy cows. Atmospheric Environment 45, 6760–6768.
| Effects of animal activity and air temperature on methane and ammonia emissions from a naturally ventilated building for dairy cows.Crossref | GoogleScholarGoogle Scholar |
Nonaka I, Takusari N, Tajima K, Suzuki T, Higuchi K, Kurihara M (2008) Effects of high environmental temperatures on physiological and nutritional status of prepubertal Holstein heifers. Livestock Science 113, 14–23.
| Effects of high environmental temperatures on physiological and nutritional status of prepubertal Holstein heifers.Crossref | GoogleScholarGoogle Scholar |
NRC (2007) ‘Nutrient requirements of small ruminants: sheep, goats, cervids, and new world camelids.’ (NRC)
Ogimoto K, Imai S (1981) ‘Atlas of rumen microbiology.’ (Japan Scientific Societies Press)
Ottenstein DM, Bartley DA (1971) Improved gas chromatography separation of free acids C2–C5 in dilute solution. Analytical Chemistry 43, 952–955.
| Improved gas chromatography separation of free acids C2–C5 in dilute solution.Crossref | GoogleScholarGoogle Scholar |
Potu RB, AbuGhazaleh AA, Hastings D, Jones K, Ibrahim SA (2011) The effect of lipid supplements on ruminal bacteria in continuous culture fermenters varies with the fatty acid composition. The Journal of Microbiology 49, 216–223.
| The effect of lipid supplements on ruminal bacteria in continuous culture fermenters varies with the fatty acid composition.Crossref | GoogleScholarGoogle Scholar | 21538241PubMed |
Rhoads RP, Baumgard LH, Suagee JK, Sanders SR (2013) Nutritional interventions to alleviate the negative consequences of heat stress. Advances in Nutrition 4, 267–276.
| Nutritional interventions to alleviate the negative consequences of heat stress.Crossref | GoogleScholarGoogle Scholar | 23674792PubMed |
Russell JB (1998) The importance of pH in the regulation of ruminal acetate to propionate ratio and methane production in vitro. Journal of Dairy Science 81, 3222–3230.
| The importance of pH in the regulation of ruminal acetate to propionate ratio and methane production in vitro.Crossref | GoogleScholarGoogle Scholar | 9891267PubMed |
Sahebi AM, Pirmohammadi R, Khalilvandi-Behroozyar H, Anassori E (2020) Potential of walnut (Juglans regia) leave ethanolic extract to modify ruminal fermentation, microbial populations and mitigate methane emission. Animal Production Science 60, 1189–1200.
| Potential of walnut (Juglans regia) leave ethanolic extract to modify ruminal fermentation, microbial populations and mitigate methane emission.Crossref | GoogleScholarGoogle Scholar |
Salles MSV, Zanetti MA, Salles FA, Titto EAL, Conti RMC (2010) Changes in ruminal fermentation and mineral serum level in animals kept in high temperature environments. Revista Brasileira de Zootecnia 39, 883–890.
| Changes in ruminal fermentation and mineral serum level in animals kept in high temperature environments.Crossref | GoogleScholarGoogle Scholar |
Shafie MM, Murad HM, El-Bedawy TM, Salem SM (1994) Effect of heat stress on feed intake, rumen fermentation and water turnover in relation to heat tolerance response by sheep. Egyptian Journal of Animal Production 31, 317–327.
| Effect of heat stress on feed intake, rumen fermentation and water turnover in relation to heat tolerance response by sheep.Crossref | GoogleScholarGoogle Scholar |
Soriani N, Panella G, Calamari L (2013) Rumination time during the summer season and its relationships with metabolic conditions and milk production. Journal of Dairy Science 96, 5082–5094.
| Rumination time during the summer season and its relationships with metabolic conditions and milk production.Crossref | GoogleScholarGoogle Scholar | 23791488PubMed |
St-Pierre NR, Cobanov B, Schnitkey G (2003) Economic losses from heat stress by US livestock industries. Journal of Dairy Science 86, E52–E77.
| Economic losses from heat stress by US livestock industries.Crossref | GoogleScholarGoogle Scholar |
Sylvester JT, Karnati SKR, Yu Z, Morrison M, Firkins JL (2004) Development of an assay to quantify rumen ciliate protozoal biomass in cows using real-time PCR. The Journal of Nutrition 134, 3378–3384.
| Development of an assay to quantify rumen ciliate protozoal biomass in cows using real-time PCR.Crossref | GoogleScholarGoogle Scholar | 15570040PubMed |
Tajima K, Aminov RI, Nagamine T, Matsui H, Nakamura M, Benno Y (2001) Diet-dependent shifts in the bacterial population of the rumen revealed with real-time PCR. Applied and Environmental Microbiology 67, 2766–2774.
| Diet-dependent shifts in the bacterial population of the rumen revealed with real-time PCR.Crossref | GoogleScholarGoogle Scholar | 11375193PubMed |
Tajima K, Nonaka I, Higuchi K, Takusari N, Kurihara M, Takenaka A, Mitsumori M, Kajikawa H, Aminov RI (2007) Influence of high temperature and humidity on rumen bacterial diversity in Holstein heifers. Anaerobe 13, 57–64.
| Influence of high temperature and humidity on rumen bacterial diversity in Holstein heifers.Crossref | GoogleScholarGoogle Scholar | 17317231PubMed |
Tedeschi LO, Cannas A, Fox DG (2010) A nutrition mathematical model to account for dietary supply and requirements of energy and other nutrients for domesticated small ruminants: the development and evaluation of the Small Ruminant Nutrition System. Small Ruminant Research 89, 174–184.
| A nutrition mathematical model to account for dietary supply and requirements of energy and other nutrients for domesticated small ruminants: the development and evaluation of the Small Ruminant Nutrition System.Crossref | GoogleScholarGoogle Scholar |
Uyeno Y, Sekiguchi Y, Tajima K, Takenaka A, Kurihara M, Kamagata Y (2010) An rRNA-based analysis for evaluating the effect of heat stress on the rumen microbial composition of Holstein heifers. Anaerobe 16, 27–33.
| An rRNA-based analysis for evaluating the effect of heat stress on the rumen microbial composition of Holstein heifers.Crossref | GoogleScholarGoogle Scholar | 19446029PubMed |
Van Keulen J, Young BA (1977) Evaluation of acid-insoluble ash as a natural marker in ruminant digestibility studies. Journal of Animal Science 44, 282–287.
| Evaluation of acid-insoluble ash as a natural marker in ruminant digestibility studies.Crossref | GoogleScholarGoogle Scholar |
Van Soest PJ, Robertson JB, Lewis BA (1991) Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. Journal of Dairy Science 74, 3583–3597.
| Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition.Crossref | GoogleScholarGoogle Scholar | 1660498PubMed |
Yadav B, Singh G, Verma AK, Dutta N, Sejian V (2013) Impact of heat stress on rumen functions. Veterinary World 6, 992
| Impact of heat stress on rumen functions.Crossref | GoogleScholarGoogle Scholar |
Yadav B, Singh G, Wankar A, Dutta N, Chaturvedi VB, Verma MR (2016) Effect of simulated heat stress on digestibility, methane emission and metabolic adaptability in crossbred cattle. Asian-Australasian Journal of Animal Sciences 29, 1585
| Effect of simulated heat stress on digestibility, methane emission and metabolic adaptability in crossbred cattle.Crossref | GoogleScholarGoogle Scholar | 26954228PubMed |
Zhou M, Hernandez-Sanabria E, Guan LL (2009) Assessment of the microbial ecology of ruminal methanogens in cattle with different feed efficiencies. Applied and Environmental Microbiology 75, 6524–6533.
| Assessment of the microbial ecology of ruminal methanogens in cattle with different feed efficiencies.Crossref | GoogleScholarGoogle Scholar | 19717632PubMed |