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The Effect of Early Life Nutrition on Rumen Microbial Community Development and Impact on Lifetime Performance in Ruminants

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Copyright is owned by the Author of the thesis. Permission is given for a copy to be downloaded by an individual for the purpose of research and private study only. The thesis may not be reproduced elsewhere without the permission of the Author. THE EFFECT OF EARLY LIFE NUTRITION ON RUMEN MICROBIAL COMMUNITY DEVELOPMENT AND IMPACT ON LIFETIME PERFORMANCE IN RUMINANTS A thesis presented in partial fulfilment of the requirements for the degree of Doctor of Philosophy In Veterinary Sciences At Massey University Palmerston North New Zealand Omar Cristobal Carballo 2019 Abstract Manipulation of the rumen microbiota in adult ruminants has been intended to improve animal performance and decrease greenhouse gas emissions, but results have only shown a short- or non-lasting effect after intervention. Changes in the ruminal microbiota during rumen development have recently shown promising results in the short-term. Therefore, the purpose of the present body of work was to determine how dietary management and chemical interventions, during rumen development, modify the ruminal microbial community composition, and whether these changes affect rumen fermentation and development, and consequently, performance in the young ruminants. The objectives of this thesis were to: (i) evaluate the impact of early weaning on rumen development and function in artificially-reared lambs; (ii) characterize the impact of early weaning in lambs on the rumen microbiota in the first 16 weeks of life and examine the relationships between rumen microbiota composition and rumen fermentation profiles, rumen development and blood metabolites; (iii) assess whether contrasting feeding regimes in the first 7 months of life lead to an imprint in the rumen microbial community structure, fermentation profiles and methane emissions in the rumen of calves; (iv) and evaluate the effect of methane inhibitors on the rumen microbial community composition, fermentation pathways, and gas emissions in calves. A series of three experiments were carried out in young ruminants separated from their mothers after colostrum intake, to address the objectives of this thesis. In experiment one, 3-5-day-old lambs were euthanized at weeks 0, 4 and 16 of rearing to investigate objectives (i) and (ii). Early weaning of lambs increased plasma - hydroxybutyrate at week 4 of rearing, while dry matter intake, fermentation profiles and rumen morphology were similar between groups. Papillae morphology and muscular thickness differed between ruminal sites at 4 and 16 weeks of rearing, but not between treatments. Diversity and relative abundance of ruminal bacteria was affected by feeding management, whilst the archaea community showed few changes. Changes in the proportions of abundant bacteria genera from Bacteroidetes and Firmicutes were associated with fermentation profiles, rumen morphology and blood metabolites; however, further investigations are required to explain these associations. In experiment two, ~1- week-old calves were reared with two divergent feeding systems and different post- weaning forage quality with a common pasture diet after 7 months of age to investigate objective (iii). Consumption of pre-weaning concentrate compared to forage produced I | P a g e lower methane yields and greater total short chain fatty acids (SCFA) concentrations and propionate proportions; whist ruminal microbes showed greater proportions of saccharolitic bacteria and Methanobrevibacter boviskoreani, but lower hemicellulolytic and cellulolytic bacteria, and Mbb. gottschalkii. Post-weaning, high-quality forage produced greater total SCFA concentration and propionate proportions than low-quality forages, while methane yield was similar. Hemicellulolytic bacteria and Methanosphaera spp. were greater in high-quality forages, while cellulolytic bacteria and Methanomassiliicoccales spp. were greater in low-quality forages. No pre-weaning effect was observed. Finally, the consumption of a common diet after 7 months of age resulted in similar methane emissions, fermentation profiles and microbial communities. In experiment three, ~1-week-old calves fed either concentrate starter diets or starter diets plus methane inhibitors were tested to evaluate objective (iv). Inhibitor intake decreased methane yield, but increased hydrogen yield and the proportion of propionate and had no effect on dry matter intake, total SCFA concentrations or animal growth. Within the abundant bacteria, the proportions of hydrogen utilizing and producing bacteria increased and decreased, respectively. Archaea diversity and proportions were affected during the period of methane inhibitor intake. However, similar gas emissions, fermentation profiles, and microbial communities were observed between groups at 24 and 49 weeks of age. Collectively, these results showed that reducing the age at weaning and introducing the solid feed to lambs at ~1 week of life accelerated some aspects of rumen morphology and function. Dietary management and methanogen inhibitor interventions affected the composition of the ruminal microbiota and fermentation profiles during treatment, however, no permanent changes in the microbial community and resulting ruminal fermentation were observed post-treatment in young ruminants. II | P a g e List of Publications Abstracts O. Cristobal-Carballo, F.W. Knol, S. Muetzel, M.A. Khan, D. Stevens and S.A. McCoard. 2016. Impact of early weaning on rumen development and fermentation profiles in artificially-reared lambs. Proceedings of the Annual Meeting of the European Federation of Animal Science, No. 67 p. 368, Belfast UK. Awarded: Best poster O. Cristobal-Carballo, M. A. Khan, F. W. Knol, S. J. Lewis, D. Stevens, S. A. McCoard. 2017. Effect of weaning age on ruminal fermentation profiles of artificially reared lambs. Proceedings of Sheep Milk NZ Conference. Awapuni, NZ. O. Cristobal-Carballo, S. A. McCoard, K. Lowe, S. Ganesh, S. J. Lewis, S. Muetzel. 2019. Rumen microbial composition and fermentation profiles through divergent dietary interventions during early-life in calves. Proceedings of the Congress on Gastrointestinal Function 2019. Chicago, IL. Conference proceedings Cristobal-Carballo, O., M. A. Khan, F. W. Knol, S. J. Lewis, D. R. Stevens, and S. A. McCoard. 2017. Impact of early weaning on rumen fermentation profiles of artificially reared lambs. Proceedings of the New Zealand Society of Animal Production No. 77. p 49- 54, Rotorua NZ. Peer-reviewed O. Cristobal-Carballo, M. A. Khan, F. W. Knol, S. J. Lewis, D. Stevens, R. A. Laven, S. A. McCoard. 2019. Impact of weaning age on rumen development in artificially-reared lambs. Journal of Animal Science (in press). III | P a g e IV | P a g e Acknowledgements I wish to express my sincere thanks to my supervisors Dr Sue McCoard (AgResearch, Grasslands), Dr Stefan Muetzel (AgResearch, Grasslands), Dr Adrian Cookson (AgResearch, Grasslands), and Professor Richard Laven (School of Veterinary Science). This has been an intensive journey, which I would have not completed without your tremendous support, understanding, encouragement and patience. I would like to thank AgResearch’s Strategic Science Investment Fund (SSIF), ANZCO Foods, Ministry of Primary Industries (MPI) through the Sustainable Land Management and Climate Change (SLMACC) program Hydrogen management and MPI as part of the Joint Programming Initiative on Agriculture, Food Security and Climate Change (FACCE-JPI) ‘RumenStability’ program for funding the research projects. A very special thank you to NZAID program, CONACYT-Mexico, Instituto Nacional de Ivestigaciones Forestales, Agricolas y Pecuarias (INIFAP), AgResearch and IVABS funds for their financial support. Thanks to all the people from AgResearch who made me feel part of a great research institution. A special thanks to the Animal Nutrition and Physiology team, to the Rumen Microbiology team and to the Ulyatt Reid Large Animal Facility team in Grasslands people for their help during the animal trials and processing of the samples. Thanks to my friends, Khan and Arjan for the great coffee-times and talk that we share. Also, thanks to all AgResearch PhD students and Massey University PhD students. I am also extremely grateful to John Koolaard and Ganesh Siva (AgResearch, Grasslands). Thanks John for your guidance and always kind support with the statistical analysis, and Ganesh for those long hours and great help with the statistical analysis of those complex models. My time living in New Zealand would have not been as pleasant and easy going without all the amazing people that made me feel like at home. In these years I have met wonderful friends with whom I shared many experiences, thank you for being part of my life. V | P a g e I would especially like to thank to my beloved family, my parents: Gelasia Carballo Suarez and Bernabe Cristobal Calderon, my sister: Viridiana Cristobal Carballo and my girlfriend: Kelly E. Clinton, for all the love and support they have given me, and for encouraging me to pursuit my dreams. VI | P a g e Table of Contents ABSTRACT…….................................................................................................................... I LIST OF PUBLICATIONS ................................................................................................. III ACKNOWLEDGEMENTS ................................................................................................. V TABLE OF CONTENTS ................................................................................................... VII LIST OF FIGURES
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