Gut microbiota resilience in horse athletes following holidays out to pasture.
Abstract: Elite horse athletes that live in individual boxes and train and compete for hours experience long-term physical and mental stress that compromises animal welfare and alters the gut microbiota. We therefore assessed if a temporary period out to pasture with conspecifics could improve animal welfare and in turn, favorably affect intestinal microbiota composition. A total of 27 athletes were monitored before and after a period of 1.5 months out to pasture, and their fecal microbiota and behavior profiles were compared to those of 18 horses kept in individual boxes. The overall diversity and microbiota composition of pasture and control individuals were temporally similar, suggesting resilience to environmental challenges. However, pasture exposure induced an increase in Ruminococcus and Coprococcus that lasted 1-month after the return to individual boxes, which may have promoted beneficial effects on health and welfare. Associations between the gut microbiota composition and behavior indicating poor welfare were established. Furthermore, withdrawn behavior was associated with the relative abundances of Lachnospiraceae AC2044 group and Clostridiales family XIII. Both accommodate a large part of butyrate-producing bacterial genera. While we cannot infer causality within this study, arguably, these findings suggest that management practices maintained over a longer period of time may moderate the behavior link to the gut ecosystem beyond its resilience potential.
Publication Date: 2021-03-03 PubMed ID: 33658551PubMed Central: PMC7930273DOI: 10.1038/s41598-021-84497-yGoogle Scholar: Lookup
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- Journal Article
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Summary
This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.
The research examines the impact of a break from rigorous training on the gut microbiota in athletic horses and how this could influence their welfare. The study also explores the relationship between certain behaviors indicating poor welfare and the composition of the gut microbiota.
Research Methodology
- The study observed 27 horse athletes before and after a period of 1.5 months in the pasture with their peers. This break from their usual routine of long hours of training and competition was considered as a form of respite from physical and mental stress.
- The study also had a control group of 18 horses which were kept in individual boxes. This control group did not receive any breaks and continued with their usual routine.
- Fecal microbiota analysis and behavior profiles of the horses were studied and compared.
Findings
- The results demonstrated that the overall diversity and composition of the gut microbiota among horses at pasture and control horses were temporally similar, thus, suggesting resilience to changes in the environment.
- A temporary period in the pasture led to an increase in bacteria, specifically Ruminococcus and Coprococcus, that lasted for a month even after the horses returned to individual boxes. The presence of these bacteria may have positive effects on horse health and welfare.
- The study was able to establish links between the composition of gut microbiota and poor welfare-indicating behavior. Withdrawn behavior was associated with increased relative abundance of certain types of bacteria such as Lachnospiraceae AC2044 group and Clostridiales family XIII, which accommodate a large part of butyrate-producing bacterial genera. Butyrate-producing bacteria are known to contribute to gut health.
Implications and Conclusions
- The findings may imply that extended periods of intensive management practices can potentially impact horse behavior and the gut microbiota. While the gut microbiota showed resilience to short-term changes, long-term changes in management practices could have a more profound effect.
- However, the study did not establish a causal link between gut microbiota diversity and horse behavior, only an association, thus more research is needed to investigate this relationship further.
Cite This Article
APA
Mach N, Lansade L, Bars-Cortina D, Dhorne-Pollet S, Foury A, Moisan MP, Ruet A.
(2021).
Gut microbiota resilience in horse athletes following holidays out to pasture.
Sci Rep, 11(1), 5007.
https://doi.org/10.1038/s41598-021-84497-y Publication
Researcher Affiliations
- Animal Genetic and Integrative Biology, University of Paris-Saclay, INRAE, AGroParisTech, 78350, Jouy-en-Josas, France. nuria.mach@inrae.fr.
- PRC, INRAE, CNRS, IFCE, University of Tours, 37380, Nouzilly, France.
- Medicine Department, University of Lleida, 25198, Lleida, Spain.
- Animal Genetic and Integrative Biology, University of Paris-Saclay, INRAE, AGroParisTech, 78350, Jouy-en-Josas, France.
- University of Bordeaux, INRAE, NutriNeuro UMR 1286, 33076, Bordeaux, France.
- University of Bordeaux, INRAE, NutriNeuro UMR 1286, 33076, Bordeaux, France.
- PRC, INRAE, CNRS, IFCE, University of Tours, 37380, Nouzilly, France.
MeSH Terms
- Adaptation, Physiological
- Animal Welfare / ethics
- Animals
- Bacteroidetes / classification
- Bacteroidetes / genetics
- Bacteroidetes / isolation & purification
- Biodiversity
- Butyrates / metabolism
- Clostridiales / classification
- Clostridiales / genetics
- Clostridiales / isolation & purification
- Competitive Behavior / physiology
- Feces / microbiology
- Female
- Fibrobacteres / classification
- Fibrobacteres / genetics
- Fibrobacteres / isolation & purification
- Firmicutes / classification
- Firmicutes / genetics
- Firmicutes / isolation & purification
- Gastrointestinal Microbiome / genetics
- Horses / microbiology
- Horses / physiology
- Horses / psychology
- Male
- RNA, Ribosomal, 16S / genetics
- Spirochaetales / classification
- Spirochaetales / genetics
- Spirochaetales / isolation & purification
- Sports
- Stress, Physiological
Conflict of Interest Statement
The authors declare no competing interests.
References
This article includes 74 references
- Sommer F, Anderson JM, Bharti R, Raes J, Rosenstiel P. The resilience of the intestinal microbiota influences health and disease.. Nat Rev Microbiol 2017 Oct;15(10):630-638.
- Mach N, Clark A. Micronutrient Deficiencies and the Human Gut Microbiota.. Trends Microbiol 2017 Aug;25(8):607-610.
- Ruet A, Lemarchand J, Parias C, Mach N, Moisan MP, Foury A, Briant C, Lansade L. Housing Horses in Individual Boxes Is a Challenge with Regard to Welfare.. Animals (Basel) 2019 Aug 28;9(9).
- Farm Animal Welfare Committee. FAWC updates the five freedoms. Vet. Rec. 17, 357 (1992).
- Mormede P. Animal welfare: Context, definition, evaluation. INRA Prod. Anim. 2018;31:145–162.
- Wong BBM, Candolin U. Behavioral responses to changing environments. Behav. Ecol. 2015;26:665–673.
- Dellmeier GR. Motivation in relation to the welfare of enclosed livestock. Appl. Anim. Behav. Sci. 1989;22:129–138.
- Mach N, Ruet A, Clark A, Bars-Cortina D, Ramayo-Caldas Y, Crisci E, Pennarun S, Dhorne-Pollet S, Foury A, Moisan MP, Lansade L. Priming for welfare: gut microbiota is associated with equitation conditions and behavior in horse athletes.. Sci Rep 2020 May 20;10(1):8311.
- Rhee SH, Pothoulakis C, Mayer EA. Principles and clinical implications of the brain-gut-enteric microbiota axis.. Nat Rev Gastroenterol Hepatol 2009 May;6(5):306-14.
- Johnson KV, Foster KR. Why does the microbiome affect behaviour?. Nat Rev Microbiol 2018 Oct;16(10):647-655.
- Destrez A, Grimm P, Julliand V. Dietary-induced modulation of the hindgut microbiota is related to behavioral responses during stressful events in horses.. Physiol Behav 2019 Apr 1;202:94-100.
- Bulmer LS, Murray JA, Burns NM, Garber A, Wemelsfelder F, McEwan NR, Hastie PM. High-starch diets alter equine faecal microbiota and increase behavioural reactivity.. Sci Rep 2019 Dec 9;9(1):18621.
- Perry E, Cross TL, Francis JM, Holscher HD, Clark SD, Swanson KS. Effect of Road Transport on the Equine Cecal Microbiota.. J Equine Vet Sci 2018 Sep;68:12-20.
- Jiang H, Ling Z, Zhang Y, Mao H, Ma Z, Yin Y, Wang W, Tang W, Tan Z, Shi J, Li L, Ruan B. Altered fecal microbiota composition in patients with major depressive disorder.. Brain Behav Immun 2015 Aug;48:186-94.
- Rogers GB, Keating DJ, Young RL, Wong ML, Licinio J, Wesselingh S. From gut dysbiosis to altered brain function and mental illness: mechanisms and pathways.. Mol Psychiatry 2016 Jun;21(6):738-48.
- Du Y, Gao XR, Peng L, Ge JF. Crosstalk between the microbiota-gut-brain axis and depression.. Heliyon 2020 Jun;6(6):e04097.
- Valles-Colomer M, Falony G, Darzi Y, Tigchelaar EF, Wang J, Tito RY, Schiweck C, Kurilshikov A, Joossens M, Wijmenga C, Claes S, Van Oudenhove L, Zhernakova A, Vieira-Silva S, Raes J. The neuroactive potential of the human gut microbiota in quality of life and depression.. Nat Microbiol 2019 Apr;4(4):623-632.
- Bercik P, Park AJ, Sinclair D, Khoshdel A, Lu J, Huang X, Deng Y, Blennerhassett PA, Fahnestock M, Moine D, Berger B, Huizinga JD, Kunze W, McLean PG, Bergonzelli GE, Collins SM, Verdu EF. The anxiolytic effect of Bifidobacterium longum NCC3001 involves vagal pathways for gut-brain communication.. Neurogastroenterol Motil 2011 Dec;23(12):1132-9.
- Ruet A. Effects of a temporary period on pasture on the welfare state of horses housed in individual boxes. Appl. Anim. Behav. Sci. 2020;228:105027.
- Lesimple C. Indicators of Horse Welfare: State-of-the-Art.. Animals (Basel) 2020 Feb 13;10(2).
- Ruet A, Biau S, Arnould C, Galloux P, Destrez A, Pycik E, Boichot L, Lansade L. Horses Could Perceive Riding Differently Depending on the Way They Express Poor Welfare in the Stable.. J Equine Vet Sci 2020 Nov;94:103206.
- Costa MC, Stämpfli HR, Arroyo LG, Allen-Vercoe E, Gomes RG, Weese JS. Changes in the equine fecal microbiota associated with the use of systemic antimicrobial drugs.. BMC Vet Res 2015 Feb 3;11:19.
- Ilhan ZE, Marcus AK, Kang DW, Rittmann BE, Krajmalnik-Brown R. pH-Mediated Microbial and Metabolic Interactions in Fecal Enrichment Cultures.. mSphere 2017 May-Jun;2(3).
- Blikslager AT. Colic Prevention to Avoid Colic Surgery: A Surgeon's Perspective.. J Equine Vet Sci 2019 May;76:1-5.
- Van den Berg M, Hoskin SO, Rogers CW, Grinberg A. Fecal pH and microbial populations in thoroughbred horses during transition from pasture to concentrate feeding. J. Equine Vet. Sci. 2013;33:215–222.
- Fleming I, Defazio J, Zaborina O, Alverdy JC. Critical illness and intestinal microflora: Ph as a surrogate marker. Diet Nutr. Crit. Care. 2015;1:1–9.
- Wittebolle L, Marzorati M, Clement L, Balloi A, Daffonchio D, Heylen K, De Vos P, Verstraete W, Boon N. Initial community evenness favours functionality under selective stress.. Nature 2009 Apr 2;458(7238):623-6.
- Kostic AD, Xavier RJ, Gevers D. The microbiome in inflammatory bowel disease: current status and the future ahead.. Gastroenterology 2014 May;146(6):1489-99.
- Dalile B, Van Oudenhove L, Vervliet B, Verbeke K. The role of short-chain fatty acids in microbiota-gut-brain communication.. Nat Rev Gastroenterol Hepatol 2019 Aug;16(8):461-478.
- Dinan TG, Cryan JF. Microbes, Immunity, and Behavior: Psychoneuroimmunology Meets the Microbiome.. Neuropsychopharmacology 2017 Jan;42(1):178-192.
- Vital M, Howe A, Bergeron N, Krauss RM, Jansson JK, Tiedje JM. Metagenomic Insights into the Degradation of Resistant Starch by Human Gut Microbiota.. Appl Environ Microbiol 2018 Dec 1;84(23).
- Bailey MT, Dowd SE, Galley JD, Hufnagle AR, Allen RG, Lyte M. Exposure to a social stressor alters the structure of the intestinal microbiota: implications for stressor-induced immunomodulation.. Brain Behav Immun 2011 Mar;25(3):397-407.
- Louis P, Flint HJ. Diversity, metabolism and microbial ecology of butyrate-producing bacteria from the human large intestine.. FEMS Microbiol Lett 2009 May;294(1):1-8.
- Xie X, Yang C, Guan LL, Wang J, Xue M, Liu JX. Persistence of Cellulolytic Bacteria Fibrobacter and Treponema After Short-Term Corn Stover-Based Dietary Intervention Reveals the Potential to Improve Rumen Fibrolytic Function.. Front Microbiol 2018;9:1363.
- Burokas A, Arboleya S, Moloney RD, Peterson VL, Murphy K, Clarke G, Stanton C, Dinan TG, Cryan JF. Targeting the Microbiota-Gut-Brain Axis: Prebiotics Have Anxiolytic and Antidepressant-like Effects and Reverse the Impact of Chronic Stress in Mice.. Biol Psychiatry 2017 Oct 1;82(7):472-487.
- van de Wouw M, Boehme M, Lyte JM, Wiley N, Strain C, O'Sullivan O, Clarke G, Stanton C, Dinan TG, Cryan JF. Short-chain fatty acids: microbial metabolites that alleviate stress-induced brain-gut axis alterations.. J Physiol 2018 Oct;596(20):4923-4944.
- Lukić I, Getselter D, Ziv O, Oron O, Reuveni E, Koren O, Elliott E. Antidepressants affect gut microbiota and Ruminococcus flavefaciens is able to abolish their effects on depressive-like behavior.. Transl Psychiatry 2019 Apr 9;9(1):133.
- Julliand V, de Vaux A, Millet L, Fonty G. Identification of Ruminococcus flavefaciens as the predominant cellulolytic bacterial species of the equine cecum.. Appl Environ Microbiol 1999 Aug;65(8):3738-41.
- Flauger B, Krueger K. Aggression level and enclosure size in horses ( Equus caballus ). Pferdeheilkunde 2013;29:495–504.
- Zaneveld JR, McMinds R, Vega Thurber R. Stress and stability: applying the Anna Karenina principle to animal microbiomes.. Nat Microbiol 2017 Aug 24;2:17121.
- Martin-Rosset W, Vermorel M, Doreau M, Tisserand JL, Andrieu J. The French horse feed evaluation systems and recommended allowances for energy and protein. Livest. Prod. Sci. 1994;40:37–56.
- Smith BL, Jones JH, Hornof WJ, Miles JA, Longworth KE, Willits NH. Effects of road transport on indices of stress in horses.. Equine Vet J 1996 Nov;28(6):446-54.
- Padalino B, Raidal SL, Hall E, Knight P, Celi P, Jeffcott L, Muscatello G. Risk factors in equine transport-related health problems: A survey of the Australian equine industry.. Equine Vet J 2017 Jul;49(4):507-511.
- Massacci FR, Clark A, Ruet A, Lansade L, Costa M, Mach N. Inter-breed diversity and temporal dynamics of the faecal microbiota in healthy horses.. J Anim Breed Genet 2020 Jan;137(1):103-120.
- Plancade S, Clark A, Philippe C, Helbling JC, Moisan MP, Esquerré D, Le Moyec L, Robert C, Barrey E, Mach N. Unraveling the effects of the gut microbiota composition and function on horse endurance physiology.. Sci Rep 2019 Jul 3;9(1):9620.
- Destrez A, Grimm P, Cézilly F, Julliand V. Changes of the hindgut microbiota due to high-starch diet can be associated with behavioral stress response in horses.. Physiol Behav 2015 Oct 1;149:159-64.
- Willing B, Vörös A, Roos S, Jones C, Jansson A, Lindberg JE. Changes in faecal bacteria associated with concentrate and forage-only diets fed to horses in training.. Equine Vet J 2009 Dec;41(9):908-14.
- Daly K, Proudman CJ, Duncan SH, Flint HJ, Dyer J, Shirazi-Beechey SP. Alterations in microbiota and fermentation products in equine large intestine in response to dietary variation and intestinal disease.. Br J Nutr 2012 Apr;107(7):989-95.
- Hansen NC, Avershina E, Mydland LT, Næsset JA, Austbø D, Moen B, Måge I, Rudi K. High nutrient availability reduces the diversity and stability of the equine caecal microbiota.. Microb Ecol Health Dis 2015;26:27216.
- Salem SE, Maddox TW, Berg A, Antczak P, Ketley JM, Williams NJ, Archer DC. Variation in faecal microbiota in a group of horses managed at pasture over a 12-month period.. Sci Rep 2018 May 31;8(1):8510.
- Harlow BE, Donley TM, Lawrence LM, Flythe MD. Effect of starch source (corn, oats or wheat) and concentration on fermentation by equine faecal microbiota in vitro.. J Appl Microbiol 2015 Nov;119(5):1234-44.
- Respondek F, Goachet AG, Julliand V. Effects of dietary short-chain fructooligosaccharides on the intestinal microflora of horses subjected to a sudden change in diet.. J Anim Sci 2008 Feb;86(2):316-23.
- Goodson J, Tyznik WJ, Cline JH, Dehority BA. Effects of an abrupt diet change from hay to concentrate on microbial numbers and physical environment in the cecum of the pony.. Appl Environ Microbiol 1988 Aug;54(8):1946-50.
- Grimm P, Philippeau C, Julliand V. Faecal parameters as biomarkers of the equine hindgut microbial ecosystem under dietary change.. Animal 2017 Jul;11(7):1136-1145.
- Jensen RB, Austbø D, Blache D, Bach Knudsen KE, Tauson AH. The effect of feeding barley or hay alone or in combination with molassed sugar beet pulp on the metabolic responses in plasma and caecum of horses. Anim. Feed Sci. Technol. 214, 53–65 (2016).
- De Fombelle A, Julliand V, Drogoul C, Jacotot E. Feeding and microbial disorders in horses: 1-effects of an abrupt incorporation of two levels of barley in a hay diet on microbial profile and activities. J. Equine Vet. Sci. 2001;21:439–445.
- Muhonen S, Connysson M, Lindberg JE, Julliand V, Bertilsson J, Jansson A. Effects of crude protein intake from grass silage-only diets on the equine colon ecosystem after an abrupt feed change.. J Anim Sci 2008 Dec;86(12):3465-72.
- Mach N, Foury A, Kittelmann S, Reigner F, Moroldo M, Ballester M, Esquerré D, Rivière J, Sallé G, Gérard P, Moisan MP, Lansade L. The Effects of Weaning Methods on Gut Microbiota Composition and Horse Physiology.. Front Physiol 2017;8:535.
- Clark A, Sallé G, Ballan V, Reigner F, Meynadier A, Cortet J, Koch C, Riou M, Blanchard A, Mach N. Strongyle Infection and Gut Microbiota: Profiling of Resistant and Susceptible Horses Over a Grazing Season.. Front Physiol 2018;9:272.
- Ericsson AC, Johnson PJ, Lopes MA, Perry SC, Lanter HR. A Microbiological Map of the Healthy Equine Gastrointestinal Tract.. PLoS One 2016;11(11):e0166523.
- Reed KJ. Can fecal samples be used to inform about microbial communities of the equine hindgut?. J. Equine Vet. Sci. 2017;52:52–53.
- Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJ, Holmes SP. DADA2: High-resolution sample inference from Illumina amplicon data.. Nat Methods 2016 Jul;13(7):581-3.
- Bokulich NA, Kaehler BD, Rideout JR, Dillon M, Bolyen E, Knight R, Huttley GA, Gregory Caporaso J. Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2's q2-feature-classifier plugin.. Microbiome 2018 May 17;6(1):90.
- McMurdie PJ, Holmes S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data.. PLoS One 2013;8(4):e61217.
- McMurdie PJ, Holmes S. Phyloseq: a bioconductor package for handling and analysis of high-throughput phylogenetic sequence data.. Pac Symp Biocomput 2012;:235-46.
- Dixon P. VEGAN, a package of R functions for community ecology. J. Veg. Sci. 2003;14:927.
- Bates D, Maechler M, Bolker B, Walker S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 2015;67:1–48.
- Shields-Cutler RR, Al-Ghalith GA, Yassour M, Knights D. SplinectomeR Enables Group Comparisons in Longitudinal Microbiome Studies.. Front Microbiol 2018;9:785.
- Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2.. Genome Biol 2014;15(12):550.
- Clarke KR, Ainsworth M. A method of linking multivariate community structure to environmental variables. Mar. Ecol. Prog. Ser. 1993;92:205–219.
- Oksanen J. Package ‘vegan’: a community ecology package. 260 (2013).
- Blanchet FG, Legendre P, Borcard D. Forward selection of explanatory variables.. Ecology 2008 Sep;89(9):2623-32.
- Witten DM, Tibshirani R, Hastie T. A penalized matrix decomposition, with applications to sparse principal components and canonical correlation analysis.. Biostatistics 2009 Jul;10(3):515-34.
- Clark A, Mach N. Exercise-induced stress behavior, gut-microbiota-brain axis and diet: a systematic review for athletes.. J Int Soc Sports Nutr 2016;13:43.
Citations
This article has been cited 9 times.- Foury A, Mach N, Ruet A, Lansade L, Moisan MP. Transcriptomic signature related to poor welfare of sport horses.. Compr Psychoneuroendocrinol 2023 Nov;16:100201.
- Xi L, Wen X, Jia T, Han J, Qin X, Zhang Y, Wang Z. Comparative study of the gut microbiota in three captive Rhinopithecus species.. BMC Genomics 2023 Jul 14;24(1):398.
- Homer B, Judd J, Mohammadi Dehcheshmeh M, Ebrahimie E, Trott DJ. Gut Microbiota and Behavioural Issues in Production, Performance, and Companion Animals: A Systematic Review.. Animals (Basel) 2023 Apr 25;13(9).
- Boisseau M, Dhorne-Pollet S, Bars-Cortina D, Courtot É, Serreau D, Annonay G, Lluch J, Gesbert A, Reigner F, Sallé G, Mach N. Species interactions, stability, and resilience of the gut microbiota - Helminth assemblage in horses.. iScience 2023 Feb 17;26(2):106044.
- Wiącek J, Szurkowska J, Kryściak J, Galecka M, Karolkiewicz J. No changes in the abundance of selected fecal bacteria during increased carbohydrates consumption period associated with the racing season in amateur road cyclists.. PeerJ 2023;11:e14594.
- Li C, Li X, Guo R, Ni W, Liu K, Liu Z, Dai J, Xu Y, Abduriyim S, Wu Z, Zeng Y, Lei B, Zhang Y, Wang Y, Zeng W, Zhang Q, Chen C, Qiao J, Liu C, Hu S. Expanded catalogue of metagenome-assembled genomes reveals resistome characteristics and athletic performance-associated microbes in horse.. Microbiome 2023 Jan 12;11(1):7.
- Mach N, Midoux C, Leclercq S, Pennarun S, Le Moyec L, Rué O, Robert C, Sallé G, Barrey E. Mining the equine gut metagenome: poorly-characterized taxa associated with cardiovascular fitness in endurance athletes.. Commun Biol 2022 Oct 3;5(1):1032.
- Simões J, Batista M, Tilley P. The Immune Mechanisms of Severe Equine Asthma-Current Understanding and What Is Missing.. Animals (Basel) 2022 Mar 16;12(6).
- Mach N, Baranowski E, Nouvel LX, Citti C. The Airway Pathobiome in Complex Respiratory Diseases: A Perspective in Domestic Animals.. Front Cell Infect Microbiol 2021;11:583600.
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