FREE SHIPPING over $40
OVER 10000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Ecology and evolution2023; 13(5); e10079; doi: 10.1002/ece3.10079

Out of the stable: Social disruption and concurrent shifts in the feral mare (Equus caballus) fecal microbiota.

Abstract: The disruption of animals' symbiotic bacterial communities (their microbiota) has been associated with myriad factors including changes to the diet, hormone levels, and various stressors. The maintenance of healthy bacterial communities may be especially challenging for social species as their microbiotas are also affected by group membership, social relationships, microbial transfer between individuals, and social stressors such as increased competition and rank maintenance. We investigated the effects of increased social instability, as determined by the number of group changes made by females, on the microbiota in free-living, feral horses () on Shackleford Banks, a barrier island off the North Carolina coast. Females leaving their groups to join new ones had fecal microbial communities that were similarly diverse but compositionally different than those of females that did not change groups. Changing groups was also associated with the increased abundance of a several bacterial genera and families. These changes may be significant as horses are heavily dependent upon their microbial communities for nutrient absorption. Though we cannot identify the particular mechanism(s) driving these changes, to the best of our knowledge, ours is the first study to demonstrate an association between acute social perturbations and the microbiota in a free-ranging mammal.
© 2023 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.
Get Full Text
Publication Date: 2023-05-11 PubMed ID: 37187967PubMed Central: PMC10175550DOI: 10.1002/ece3.10079Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
LinkedInCopy
  • Journal Article

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.

This research studied how social upheavals can affect the microbial diversity in the gut of wild horses. It discovered that female horses that changed their group affiliations had different microbial makeups compared to those that didn’t change groups, though the diversity remained about the same.

Intro and research objectives

  • The research begins by exploring the idea that the microbiota, the symbiotic bacterial communities that exist within animals, can be influenced by a variety of factors, including changes in diet, hormonal changes, and the presence of stress.
  • For social animals, the microbiota is also said to be influenced by group membership, interpersonal relationships, microbial transfers between individuals, and social stressors such as competition and the struggle to maintain a certain rank within the social structure.
  • The objective of this study was to understand how increased social instability, as evidenced by a number of group changes by females, affects the microbiota in wild horses living in Shackleford Banks, North Carolina.

Research findings

  • Females who left their groups and joined other groups showed comparably diverse but compositionally different fecal microbial communities from females who did not change groups.
  • Transitioning from one group to another was associated with an increased presence of several bacterial genera and families.
  • These changes could be significant because horses heavily rely on their microbial communities for nutrient absorption.
  • The researchers however could not identify the specific mechanisms behind these changes.
  • This study is unique in that it is the first to demonstrate a link between acute social disturbances and changes in the microbiota in a free-ranging mammal.

Significance and implications

  • Understanding that social changes can have effects on the microbiota of animals adds to our understanding of the complex and multi-layered interactions between animal behaviour, social structures, and health.
  • This discovery could inform future research into the impact social interactions have on the health and well-being of not only wild horses, but potentially other social animal species as well.
  • Understanding these microbial changes can give insight to veterinary and wildlife practices, potentially providing the tools for enhancing the health and survival of wild populations.

Cite This Article

APA
Vaziri GJ, Jones MM, Carr HA, Nuñez CMV. (2023). Out of the stable: Social disruption and concurrent shifts in the feral mare (Equus caballus) fecal microbiota. Ecol Evol, 13(5), e10079. https://doi.org/10.1002/ece3.10079

Publication

Ecology and evolution
ISSN: 2045-7758
NlmUniqueID: 101566408
Country: England
Language: English
Volume: 13
Issue: 5
Pages: e10079
PII: e10079

Researcher Affiliations

Vaziri, Grace J
  • Ecology and Evolutionary Biology University of Connecticut Mansfield Connecticut USA.
Jones, Maggie M
  • Department of Natural Resource Ecology and Management Iowa State University Ames, Iowa USA.
  • Present address: School of Natural Resources and Environment University of Florida Gainesville Florida USA.
Carr, Haley A
  • Department of Natural Resource Ecology and Management Iowa State University Ames, Iowa USA.
Nuñez, Cassandra M V
  • Department of Natural Resource Ecology and Management Iowa State University Ames, Iowa USA.
  • Department of Biological Sciences The University of Memphis Memphis Tennessee USA.

References

This article includes 85 references
  1. Altmann J. Observational study of behavior: sampling methods.. Behaviour 1974;49(3):227-67.
    pubmed: 4597405doi: 10.1163/156853974x00534google scholar: lookup
  2. Amato KR, Yeoman CJ, Kent A, Righini N, Carbonero F, Estrada A, Gaskins HR, Stumpf RM, Yildirim S, Torralba M, Gillis M, Wilson BA, Nelson KE, White BA, Leigh SR. Habitat degradation impacts black howler monkey (Alouatta pigra) gastrointestinal microbiomes.. ISME J 2013 Jul;7(7):1344-53.
    pmc: PMC3695285pubmed: 23486247doi: 10.1038/ismej.2013.16google scholar: lookup
  3. Antwis RE, Lea JMD, Unwin B, Shultz S. Gut microbiome composition is associated with spatial structuring and social interactions in semi-feral Welsh Mountain ponies.. Microbiome 2018 Nov 22;6(1):207.
    pmc: PMC6251106pubmed: 30466491doi: 10.1186/s40168-018-0593-2google scholar: lookup
  4. Bailey MT. The contributing role of the intestinal microbiota in stressor-induced increases in susceptibility to enteric infection and systemic immunomodulation.. Horm Behav 2012 Aug;62(3):286-94.
    pubmed: 22366706doi: 10.1016/j.yhbeh.2012.02.006google scholar: lookup
  5. Bailey MT, Coe CL. Maternal separation disrupts the integrity of the intestinal microflora in infant rhesus monkeys.. Dev Psychobiol 1999 Sep;35(2):146-55.
    pubmed: 10461128
  6. 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.
    pmc: PMC3039072pubmed: 21040780doi: 10.1016/j.bbi.2010.10.023google scholar: lookup
  7. Bailey MT, Dowd SE, Parry NM, Galley JD, Schauer DB, Lyte M. Stressor exposure disrupts commensal microbial populations in the intestines and leads to increased colonization by Citrobacter rodentium.. Infect Immun 2010 Apr;78(4):1509-19.
    pmc: PMC2849416pubmed: 20145094doi: 10.1128/iai.00862-09google scholar: lookup
  8. Berger J. Organizational systems and dominance in feral horses in Grand Canyon. Behavioral Ecology and Sociobiology 2, 131–146.
  9. Bertschinger HJ, Delsink A, Van Altena J, Kirkpatrick JF. Porcine zona pellucida vaccine immunocontraception of African elephant (Loxodonta africana) cows: A review of 22 years of research. Bothalia‐African Biodiversity & Conservation 48, 1–8.
  10. Biddle AS, Tomb JF, Fan Z. Microbiome and Blood Analyte Differences Point to Community and Metabolic Signatures in Lean and Obese Horses.. Front Vet Sci 2018;5:225.
    pmc: PMC6158370pubmed: 30294603doi: 10.3389/fvets.2018.00225google scholar: lookup
  11. 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.
    pmc: PMC5956843pubmed: 29773078doi: 10.1186/s40168-018-0470-zgoogle scholar: lookup
  12. Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F, Bai Y, Bisanz JE, Bittinger K, Brejnrod A, Brislawn CJ, Brown CT, Callahan BJ, Caraballo-Rodríguez AM, Chase J, Cope EK, Da Silva R, Diener C, Dorrestein PC, Douglas GM, Durall DM, Duvallet C, Edwardson CF, Ernst M, Estaki M, Fouquier J, Gauglitz JM, Gibbons SM, Gibson DL, Gonzalez A, Gorlick K, Guo J, Hillmann B, Holmes S, Holste H, Huttenhower C, Huttley GA, Janssen S, Jarmusch AK, Jiang L, Kaehler BD, Kang KB, Keefe CR, Keim P, Kelley ST, Knights D, Koester I, Kosciolek T, Kreps J, Langille MGI, Lee J, Ley R, Liu YX, Loftfield E, Lozupone C, Maher M, Marotz C, Martin BD, McDonald D, McIver LJ, Melnik AV, Metcalf JL, Morgan SC, Morton JT, Naimey AT, Navas-Molina JA, Nothias LF, Orchanian SB, Pearson T, Peoples SL, Petras D, Preuss ML, Pruesse E, Rasmussen LB, Rivers A, Robeson MS 2nd, Rosenthal P, Segata N, Shaffer M, Shiffer A, Sinha R, Song SJ, Spear JR, Swafford AD, Thompson LR, Torres PJ, Trinh P, Tripathi A, Turnbaugh PJ, Ul-Hasan S, van der Hooft JJJ, Vargas F, Vázquez-Baeza Y, Vogtmann E, von Hippel M, Walters W, Wan Y, Wang M, Warren J, Weber KC, Williamson CHD, Willis AD, Xu ZZ, Zaneveld JR, Zhang Y, Zhu Q, Knight R, Caporaso JG. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2.. Nat Biotechnol 2019 Aug;37(8):852-857.
    pmc: PMC7015180pubmed: 31341288doi: 10.1038/s41587-019-0209-9google scholar: lookup
  13. Burnham KP, Anderson DR. Model selection and multimodel inference: A practical information‐theoretic approach (2nd ed.). .
  14. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M, Gormley N, Gilbert JA, Smith G, Knight R. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms.. ISME J 2012 Aug;6(8):1621-4.
    pmc: PMC3400413pubmed: 22402401doi: 10.1038/ismej.2012.8google scholar: lookup
  15. Comizzoli P, Power ML, Bornbusch SL, Muletz-Wolz CR. Interactions between reproductive biology and microbiomes in wild animal species.. Anim Microbiome 2021 Dec 23;3(1):87.
    pmc: PMC8697499pubmed: 34949226doi: 10.1186/s42523-021-00156-7google scholar: lookup
  16. Costa MC, Arroyo LG, Allen-Vercoe E, Stämpfli HR, Kim PT, Sturgeon A, Weese JS. Comparison of the fecal microbiota of healthy horses and horses with colitis by high throughput sequencing of the V3-V5 region of the 16S rRNA gene.. PLoS One 2012;7(7):e41484.
    pmc: PMC3409227pubmed: 22859989doi: 10.1371/journal.pone.0041484google scholar: lookup
  17. Crowley PH. Dispersal and the stability of predator‐prey interactions. The American Naturalist 118, 673–701.
  18. Feist JD, McCullough DR. Behavior patterns and communication in feral horses.. Z Tierpsychol 1976 Aug;41(4):337-71.
    pubmed: 983427doi: 10.1111/j.1439-0310.1976.tb00947.xgoogle scholar: lookup
  19. Garber A, Hastie P, Murray JA. Factors Influencing Equine Gut Microbiota: Current Knowledge.. J Equine Vet Sci 2020 May;88:102943.
    pubmed: 32303307doi: 10.1016/j.jevs.2020.102943google scholar: lookup
  20. Grieneisen LE, Livermore J, Alberts S, Tung J, Archie EA. Group Living and Male Dispersal Predict the Core Gut Microbiome in Wild Baboons.. Integr Comp Biol 2017 Oct 1;57(4):770-785.
    pmc: PMC5886331pubmed: 29048537doi: 10.1093/icb/icx046google scholar: lookup
  21. Heilmann TJ, Garrott RA, Cadwell LL, Tiller BL. Behavioral response of free‐ranging elk treated with an immunocontraceptive vaccine. Journal of Wildlife Management 62, 243–250.
  22. Jones MM, Nuñez CMV. Laissez-Faire Stallions? Males' Fecal Cortisol Metabolite Concentrations Do Not Vary with Increased Female Turnover in Feral Horses (Equus caballus).. Animals (Basel) 2023 Jan 3;13(1).
    pmc: PMC9817692pubmed: 36611784doi: 10.3390/ani13010176google scholar: lookup
  23. Jones MM, Nuñez CMV. Decreased female fidelity alters male behavior in a feral horse population managed with immunocontraception. Applied Animal Behaviour Science 214, 34–41.
  24. Jones MM, Proops L, Nuñez CMV. Rising up to the challenge of their rivals: Mare infidelity intensifies stallion response to playback of aggressive conspecific vocalizations. Applied Animal Behaviour Science 225, 104949.
  25. Kaseda Y, Khalil AM, Ogawa H. Harem stability and reproductive success of Misaki feral mares.. Equine Vet J 1995 Sep;27(5):368-72.
    pubmed: 8654352doi: 10.1111/j.2042-3306.1995.tb04072.xgoogle scholar: lookup
  26. Katoh K, Misawa K, Kuma K, Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform.. Nucleic Acids Res 2002 Jul 15;30(14):3059-66.
    pmc: PMC135756pubmed: 12136088doi: 10.1093/nar/gkf436google scholar: lookup
  27. Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO. Picante: R tools for integrating phylogenies and ecology.. Bioinformatics 2010 Jun 1;26(11):1463-4.
    pubmed: 20395285doi: 10.1093/bioinformatics/btq166google scholar: lookup
  28. Kerekes V, Sándor I, Nagy D, Ozogány K, Göczi L, Ibler B, Széles L, Barta Z. Trends in demography, genetics, and social structure of Przewalski's horses in the Hortobagy National Park, Hungary over the last 22 years. Global Ecology and Conservation 25, e01407.
  29. Klingel H. Social organization and reproduction in equids.. J Reprod Fertil Suppl 1975 Oct;(23):7-11.
    pubmed: 1060868
  30. Koch H, Schmid-Hempel P. Socially transmitted gut microbiota protect bumble bees against an intestinal parasite.. Proc Natl Acad Sci U S A 2011 Nov 29;108(48):19288-92.
    pmc: PMC3228419pubmed: 22084077doi: 10.1073/pnas.1110474108google scholar: lookup
  31. Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR, Bircher JS, Schlegel ML, Tucker TA, Schrenzel MD, Knight R, Gordon JI. Evolution of mammals and their gut microbes.. Science 2008 Jun 20;320(5883):1647-51.
    pmc: PMC2649005pubmed: 18497261doi: 10.1126/science.1155725google scholar: lookup
  32. Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: human gut microbes associated with obesity.. Nature 2006 Dec 21;444(7122):1022-3.
    pubmed: 17183309doi: 10.1038/4441022agoogle scholar: lookup
  33. Lin H, Peddada SD. Analysis of compositions of microbiomes with bias correction.. Nat Commun 2020 Jul 14;11(1):3514.
    pmc: PMC7360769pubmed: 32665548doi: 10.1038/s41467-020-17041-7google scholar: lookup
  34. Linklater WL, Cameron EZ. Tests for cooperative behaviour between stallions.. Anim Behav 2000 Dec;60(6):731-743.
    pubmed: 11124871doi: 10.1006/anbe.2000.1525google scholar: lookup
  35. Linklater WL, Cameron EZ, Minot EO, Stafford KJ. Stallion harassment and the mating system of horses.. Anim Behav 1999 Aug;58(2):295-306.
    pubmed: 10458881doi: 10.1006/anbe.1999.1155google scholar: lookup
  36. Linklater WL, Cameron EZ, Stafford KJ, Veltman CJ. Social and spatial structure and range use by Kaimanawa wild horses (Equus caballus: Equidae). New Zealand Journal of Ecology 24, 139–152.
  37. Liu X, Mao B, Gu J, Wu J, Cui S, Wang G, Zhao J, Zhang H, Chen W. Blautia-a new functional genus with potential probiotic properties?. Gut Microbes 2021 Jan-Dec;13(1):1-21.
    pmc: PMC7872077pubmed: 33525961doi: 10.1080/19490976.2021.1875796google scholar: lookup
  38. Lozupone CA, Hamady M, Kelley ST, Knight R. Quantitative and qualitative beta diversity measures lead to different insights into factors that structure microbial communities.. Appl Environ Microbiol 2007 Mar;73(5):1576-85.
    pmc: PMC1828774pubmed: 17220268doi: 10.1128/aem.01996-06google scholar: lookup
  39. 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.
    pmc: PMC5524898pubmed: 28790932doi: 10.3389/fphys.2017.00535google scholar: lookup
  40. Macpherson AJ, Yilmaz B, Limenitakis JP, Ganal-Vonarburg SC. IgA Function in Relation to the Intestinal Microbiota.. Annu Rev Immunol 2018 Apr 26;36:359-381.
    pubmed: 29400985doi: 10.1146/annurev-immunol-042617-053238google scholar: lookup
  41. Madosky JM. Factors that affect harem stability in a feral horse (Equus caballus) population on Shackleford Banks Island, NC. .
  42. Madosky JM, Rubenstein DI, Howard JJ, Stuska S. The effects of immunocontraception on harem fidelity in a feral horse (Equus caballus) population. Applied Animal Behaviour Science 128, 50–56.
  43. Mallick H, Rahnavard A, McIver LJ, Ma S, Zhang Y, Nguyen LH, Tickle TL, Weingart G, Ren B, Schwager EH, Chatterjee S, Thompson KN, Wilkinson JE, Subramanian A, Lu Y, Waldron L, Paulson JN, Franzosa EA, Bravo HC, Huttenhower C. Multivariable association discovery in population-scale meta-omics studies.. PLoS Comput Biol 2021 Nov;17(11):e1009442.
    pmc: PMC8714082pubmed: 34784344doi: 10.1371/journal.pcbi.1009442google scholar: lookup
  44. Marr AB. Territoriality in Shackleford Island feral horses (Equus caballus). [Unpublished thesis].
  45. McKenzie VJ, Song SJ, Delsuc F, Prest TL, Oliverio AM, Korpita TM, Alexiev A, Amato KR, Metcalf JL, Kowalewski M, Avenant NL, Link A, Di Fiore A, Seguin-Orlando A, Feh C, Orlando L, Mendelson JR, Sanders J, Knight R. The Effects of Captivity on the Mammalian Gut Microbiome.. Integr Comp Biol 2017 Oct 1;57(4):690-704.
    pmc: PMC5978021pubmed: 28985326doi: 10.1093/icb/icx090google scholar: lookup
  46. McMurdie PJ, Holmes S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data.. PLoS One 2013;8(4):e61217.
    pmc: PMC3632530pubmed: 23630581doi: 10.1371/journal.pone.0061217google scholar: lookup
  47. McShea WJ, Monfort SL, Hakim S, Kirkpatrick J, Liu I, Turner JW, Chassy L, Munson L. The effect of immunocontraception on the behavior and reproduction of white‐tailed deer. Journal of Wildlife Management 61, 560–569.
  48. Möstl E, Palme R. Hormones as indicators of stress.. Domest Anim Endocrinol 2002 Jul;23(1-2):67-74.
    pubmed: 12142227doi: 10.1016/s0739-7240(02)00146-7google scholar: lookup
  49. nNational Climate Data Centern(2022). http://www.ncdc.noaa.gov/oa/climate/climatedata.html#monthlyn
  50. National Research Council. Guide for the care and use of laboratory animals (8th ed.). .
    pubmed: 21595115
  51. Nearing JT, Douglas GM, Hayes MG, MacDonald J, Desai DK, Allward N, Jones CMA, Wright RJ, Dhanani AS, Comeau AM, Langille MGI. Microbiome differential abundance methods produce different results across 38 datasets.. Nat Commun 2022 Jan 17;13(1):342.
    pmc: PMC8763921pubmed: 35039521doi: 10.1038/s41467-022-28034-zgoogle scholar: lookup
  52. Noguera JC, Aira M, Pérez-Losada M, Domínguez J, Velando A. Glucocorticoids modulate gastrointestinal microbiome in a wild bird.. R Soc Open Sci 2018 Apr;5(4):171743.
    pmc: PMC5936907pubmed: 29765642doi: 10.1098/rsos.171743google scholar: lookup
  53. Nuñez CMV. Mother‐young relationships in feral horses (Equus caballus): Implications for the function of development in mammals. .
  54. Nuñez CMV, Adelman JS, Carr HA, Alvarez CM, Rubenstein DI. Lingering effects of contraception management on feral mare (Equus caballus) fertility and social behavior.. Conserv Physiol 2017;5(1):cox018.
    pmc: PMC6007543pubmed: 29977561doi: 10.1093/conphys/cox018google scholar: lookup
  55. Nuñez CMV, Adelman JS, Mason C, Rubenstein DI. Immunocontraception decreases group fidelity in a feral horse population during the non‐breeding season. Applied Animal Behaviour Science 117, 74–83.
  56. Nuñez CM, Adelman JS, Smith J, Gesquiere LR, Rubenstein DI. Linking social environment and stress physiology in feral mares (Equus caballus): group transfers elevate fecal cortisol levels.. Gen Comp Endocrinol 2014 Jan 15;196:26-33.
    pubmed: 24275609doi: 10.1016/j.ygcen.2013.11.012google scholar: lookup
  57. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H. Vegan: Community ecology package. R package version 2.3‐5.
  58. Ozato N, Saito S, Yamaguchi T, Katashima M, Tokuda I, Sawada K, Katsuragi Y, Kakuta M, Imoto S, Ihara K, Nakaji S. Blautia genus associated with visceral fat accumulation in adults 20-76 years of age.. NPJ Biofilms Microbiomes 2019;5(1):28.
    pmc: PMC6778088pubmed: 31602309doi: 10.1038/s41522-019-0101-xgoogle scholar: lookup
  59. Pollock J. Behavioural ecology and body condition changes in New Forest ponies. Scientific Publications of the RSPCA 6, 1–118.
  60. Price MN, Dehal PS, Arkin AP. FastTree 2--approximately maximum-likelihood trees for large alignments.. PLoS One 2010 Mar 10;5(3):e9490.
    pmc: PMC2835736pubmed: 20224823doi: 10.1371/journal.pone.0009490google scholar: lookup
  61. R Core Team. R: A language and environment for statistical computing. .
  62. Ransom JI, Cade BS, Hobbs NT. Influences of immunocontraception on time budgets, social behavior, and body condition in feral horses. Applied Animal Behaviour Science 124, 51–60.
  63. Rubenstein DI. Behavioural ecology of island feral horses. Equine Veterinary Journal 13, 27–34.
  64. Rubenstein DI. Ecology and sociality in horses and zebras. In Rubenstein DI & Wrangham RW (Eds.), Ecological aspects of social evolution, birds and mammals (pp. 282–302).
  65. Rubenstein DI. The ecology of female social behavior in horses, zebras, and asses. In Jarman PJ & Rossiter A (Eds.), Animal societies: Individuals, interactions, and organization (pp. 13–28).
  66. Rubenstein DI, Feinstein LH. Bothersome flies: How free‐ranging horses reduce harm while maintaining nutrition. Frontiers in Ecology and Evolution 9, 659570.
  67. Rubenstein DI, Nuñez CMV. Sociality and reproductive skew in horses and zebras. In Hager R & Jones CB (Eds.), Reproductive skew in vertebrates: Proximate and ultimate causes (pp. 196–226).
  68. Rutberg AT. Intergroup transfer in Assateague pony mares. Animal Behaviour 40, 945–952.
  69. Sacco AG. Antigenic cross-reactivity between human and pig zona pellucida.. Biol Reprod 1977 Mar;16(2):164-73.
    pubmed: 401654doi: 10.1095/biolreprod16.2.164google scholar: lookup
  70. Schoster A, Mosing M, Jalali M, Staempfli HR, Weese JS. Effects of transport, fasting and anaesthesia on the faecal microbiota of healthy adult horses.. Equine Vet J 2016 Sep;48(5):595-602.
    pubmed: 26122549doi: 10.1111/evj.12479google scholar: lookup
  71. Stothart MR, Bobbie CB, Schulte-Hostedde AI, Boonstra R, Palme R, Mykytczuk NC, Newman AE. Stress and the microbiome: linking glucocorticoids to bacterial community dynamics in wild red squirrels.. Biol Lett 2016 Jan;12(1):20150875.
    pmc: PMC4785925pubmed: 26740566doi: 10.1098/rsbl.2015.0875google scholar: lookup
  72. Stothart MR, Greuel RJ, Gavriliuc S, Henry A, Wilson AJ, McLoughlin PD, Poissant J. Bacterial dispersal and drift drive microbiome diversity patterns within a population of feral hindgut fermenters.. Mol Ecol 2021 Jan;30(2):555-571.
    pubmed: 33231332doi: 10.1111/mec.15747google scholar: lookup
  73. Tung J, Barreiro LB, Burns MB, Grenier JC, Lynch J, Grieneisen LE, Altmann J, Alberts SC, Blekhman R, Archie EA. Social networks predict gut microbiome composition in wild baboons.. Elife 2015 Mar 16;4.
    pmc: PMC4379495pubmed: 25774601doi: 10.7554/elife.05224google scholar: lookup
  74. Turnbaugh PJ, Ridaura VK, Faith JJ, Rey FE, Knight R, Gordon JI. The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice.. Sci Transl Med 2009 Nov 11;1(6):6ra14.
    pmc: PMC2894525pubmed: 20368178doi: 10.1126/scitranslmed.3000322google scholar: lookup
  75. Turner JW Jr, Liu IKM, Flanagan DR, Rutberg AT, Kirkpatrick JF. Immunocontraception in wild horses: One inoculation provides two years of infertility. The Journal of Wildlife Management 71, 662–667.
  76. Vaziri GJ, Jones MM, Carr HA, Nuñez CMV. vaziri et al_metadata_20201231. Open Science Framework .
  77. Ward A, Webster M. Sociality: The behaviour of group‐living animals. .
  78. Wasser SK, Hunt KE, Brown JL, Cooper K, Crockett CM, Bechert U, Millspaugh JJ, Larson S, Monfort SL. A generalized fecal glucocorticoid assay for use in a diverse array of nondomestic mammalian and avian species.. Gen Comp Endocrinol 2000 Dec;120(3):260-75.
    pubmed: 11121291doi: 10.1006/gcen.2000.7557google scholar: lookup
  79. Wickham H. ggplot2: Elegant graphics for data analysis. .
  80. Willis P. Equine immunoconcentraception using porcine zona‐pellucida – A new method for remote delivery and characterization of the immune‐response. Journal of Equine Veterinary Science 14, 429.
  81. Wu GD, Chen J, Hoffmann C, Bittinger K, Chen YY, Keilbaugh SA, Bewtra M, Knights D, Walters WA, Knight R, Sinha R, Gilroy E, Gupta K, Baldassano R, Nessel L, Li H, Bushman FD, Lewis JD. Linking long-term dietary patterns with gut microbial enterotypes.. Science 2011 Oct 7;334(6052):105-8.
    pmc: PMC3368382pubmed: 21885731doi: 10.1126/science.1208344google scholar: lookup
  82. Yildirim S, Yeoman CJ, Sipos M, Torralba M, Wilson BA, Goldberg TL, Stumpf RM, Leigh SR, White BA, Nelson KE. Characterization of the fecal microbiome from non-human wild primates reveals species specific microbial communities.. PLoS One 2010 Nov 12;5(11):e13963.
    pmc: PMC2980488pubmed: 21103066doi: 10.1371/journal.pone.0013963google scholar: lookup
  83. Zaiss MM, Harris NL. Interactions between the intestinal microbiome and helminth parasites.. Parasite Immunol 2016 Jan;38(1):5-11.
    pmc: PMC5019230pubmed: 26345715doi: 10.1111/pim.12274google scholar: lookup
  84. Zaneveld JR, Burkepile DE, Shantz AA, Pritchard CE, McMinds R, Payet JP, Welsh R, Correa AM, Lemoine NP, Rosales S, Fuchs C, Maynard JA, Thurber RV. Overfishing and nutrient pollution interact with temperature to disrupt coral reefs down to microbial scales.. Nat Commun 2016 Jun 7;7:11833.
    pmc: PMC4899628pubmed: 27270557doi: 10.1038/ncomms11833google scholar: lookup
  85. 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.
    pubmed: 28836573doi: 10.1038/nmicrobiol.2017.121google scholar: lookup

Citations

This article has been cited 0 times.
Subscribe to our newsletter
Join 99,850 horse owners like you who receive our email updates on horse health and nutrition.