FREE SHIPPING over $40
OVER 9000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Home / Equine Research Bank / Front Microbiol / Gut Microbiomes of Endangered Przewalski’s Horse Popul...
Frontiers in microbiology2020; 11; 363; doi: 10.3389/fmicb.2020.00363

Gut Microbiomes of Endangered Przewalski’s Horse Populations in Short- and Long-Term Captivity: Implication for Species Reintroduction Based on the Soft-Release Strategy.

Abstract: Captivity maybe the only choice for survival of many endangered vertebrates, and understanding its broad effects is important for animal management and conservation, including breeding endangered species for subsequent release. Extreme environmental changes during captivity may influence survival ability in the wild. Captivity decreases gut bacterial diversity in a wide range of animals. However, most studies directly compare animals living in captivity with those in the wild, and there is a lack of understanding of effects of gradient shift in lifestyle during species reintroduction based on the soft-release strategy, which involves a confinement period in a field enclosure. Here, we used 16S rRNA amplicon sequencing to analyze gut microbiomes of 11 captive and 12 semi-wild Przewalski's horses (PH; ) under the same captivity environment, using fecal samples. A subset of samples with abundant extracted DNA (including 3 captive and 3 semi-wild individuals) was selected for whole-genome shotgun sequencing. We found that community diversity did not differ between the semi-wild PH and captive PH, but the semi-wild PH had significantly higher bacterial richness than those in captivity. Relative abundances of all dominant phyla were similar across the semi-wild or captive horses, while those of the non-dominant phyla Tenericutes and Proteobacteria were significantly higher in semi-wild PH than in captive PH. Beta diversity results indicated that bacterial communities of captives and semi-wild horses were clearly separated distinct when considering only composition. Functional profiling of the microbiomes revealed that the semi-wild and captive gut microbiomes were largely similar. However, semi-wild horse microbiomes had higher abundance of bacterial genes related to core metabolic processes, such as carbohydrates, amino acids, and nucleic acid metabolism. The study revealed that semi-wild PH could retain specific non-dominant bacteria and harbor a more diverse microbiome than the captive counterpart, and thus have higher metabolic potential to utilize the complex plants efficiently. These results indicate that change in host lifestyle may play a role in microbiome differentiation in the process of reintroduction, suggesting that a short period of time in captivity is acceptable for PH from the perspective of maintaining the richness of intestinal bacterial flora to some extent.
Copyright © 2020 Tang, Li, Srivathsan, Gao, Li, Hu and Zhang.
Get Full Text
Publication Date: 2020-03-12 PubMed ID: 32226419PubMed Central: PMC7081077DOI: 10.3389/fmicb.2020.00363Google 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 study analyses the differences in gut bacteria between captive and semi-wild Przewalski’s horses, finding that the semi-wild horses have a significantly richer and more diverse gut microbiome. This suggests that a period of captivity, as part of a soft-release strategy for species reintroduction, can maintain a degree of intestinal bacterial richness.

Research Goals and Methodology

  • This research aimed to improve our understanding of the impacts of captivity on endangered species, specifically focusing on the gut microbiomes of Przewalski’s horses.
  • Previous studies have indicated a decrease in gut bacterial diversity in animals in captivity. This study, however, targeted to analyze the gradient shift in lifestyle during species reintroduction based on a soft-release strategy, which involves confinement in a field.
  • Using 16S rRNA amplicon sequencing, the team analyzed gut microbiomes of 11 captive and 12 semi-wild Przewalski’s horses.
  • Selected samples with abundant DNA were also subject to whole-genome sequencing for further analysis.

Findings

  • There was no significant difference in community diversity between semi-wild and captive Przewalski’s horses, but the semi-wild horses had significantly more bacterial richness.
  • The relative abundances of dominant phyla were similar across both types of horses, but the non-dominant phyla Tenericutes and Proteobacteria were more prevalent in semi-wild horses.
  • Analysis of beta diversity indicated distinct bacterial communities in captive and semi-wild horses when considering only composition.
  • Functional profiling of the gut microbiomes revealed similarities between the two types, but the semi-wild horse microbiomes had a higher abundance of bacterial genes related to core metabolic processes like carbohydrates, amino acids, and nucleic acid metabolism.

Implications

  • The findings suggest that semi-wild Przewalski’s horses retain certain non-dominant bacteria and maintain a more diverse microbiome than their captive counterparts.
  • This higher diversity correlates with a higher metabolic potential for efficiently utilizing complex plants.
  • From the perspective of the gut microbiome, these results imply that a short period of captivity can still maintain a certain extent of intestinal bacterial richness in these horses, thus could be useful in species reintroduction strategies.

Cite This Article

APA
Tang L, Li Y, Srivathsan A, Gao Y, Li K, Hu D, Zhang D. (2020). Gut Microbiomes of Endangered Przewalski’s Horse Populations in Short- and Long-Term Captivity: Implication for Species Reintroduction Based on the Soft-Release Strategy. Front Microbiol, 11, 363. https://doi.org/10.3389/fmicb.2020.00363

Publication

Frontiers in microbiology
ISSN: 1664-302X
NlmUniqueID: 101548977
Country: Switzerland
Language: English
Volume: 11
Pages: 363
PII: 363

Researcher Affiliations

Tang, Liping
  • School of Nature Conservation, Beijing Forestry University, Beijing, China.
Li, Yimeng
  • School of Nature Conservation, Beijing Forestry University, Beijing, China.
Srivathsan, Amrita
  • Department of Biological Sciences, National University of Singapore, Singapore, Singapore.
Gao, Yunyun
  • School of Nature Conservation, Beijing Forestry University, Beijing, China.
Li, Kai
  • School of Nature Conservation, Beijing Forestry University, Beijing, China.
Hu, Defu
  • School of Nature Conservation, Beijing Forestry University, Beijing, China.
Zhang, Dong
  • School of Nature Conservation, Beijing Forestry University, Beijing, China.

References

This article includes 63 references
  1. Amato KR, Leigh SR, Kent A, Mackie RI, Yeoman CJ, Stumpf RM, Wilson BA, Nelson KE, White BA, Garber PA. The gut microbiota appears to compensate for seasonal diet variation in the wild black howler monkey (Alouatta pigra).. Microb Ecol 2015 Feb;69(2):434-43.
    doi: 10.1007/s00248-014-0554-7pubmed: 25524570google scholar: lookup
  2. Barnosky AD, Matzke N, Tomiya S, Wogan GO, Swartz B, Quental TB, Marshall C, McGuire JL, Lindsey EL, Maguire KC, Mersey B, Ferrer EA. Has the Earth's sixth mass extinction already arrived?. Nature 2011 Mar 3;471(7336):51-7.
    doi: 10.1038/nature09678pubmed: 21368823google scholar: lookup
  3. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Statist. Soc. B 57 289–300.
    doi: 10.1111/j.2517-6161.1995.tb02031.xgoogle scholar: lookup
  4. Bowyer RCE, Jackson MA, Pallister T, Skinner J, Spector TD, Welch AA, Steves CJ. Use of dietary indices to control for diet in human gut microbiota studies.. Microbiome 2018 Apr 25;6(1):77.
    doi: 10.1186/s40168-018-0455-ypmc: PMC5918560pubmed: 29695307google scholar: lookup
  5. Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND.. Nat Methods 2015 Jan;12(1):59-60.
    doi: 10.1038/nmeth.3176pubmed: 25402007google scholar: lookup
  6. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R. QIIME allows analysis of high-throughput community sequencing data.. Nat Methods 2010 May;7(5):335-6.
    pmc: PMC3156573pubmed: 20383131doi: 10.1038/nmeth.f.303google scholar: lookup
  7. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample.. Proc Natl Acad Sci U S A 2011 Mar 15;108 Suppl 1(Suppl 1):4516-22.
    doi: 10.1073/pnas.1000080107pmc: PMC3063599pubmed: 20534432google scholar: lookup
  8. Carmody RN, Gerber GK, Luevano JM Jr, Gatti DM, Somes L, Svenson KL, Turnbaugh PJ. Diet dominates host genotype in shaping the murine gut microbiota.. Cell Host Microbe 2015 Jan 14;17(1):72-84.
    doi: 10.1016/j.chom.2014.11.010pmc: PMC4297240pubmed: 25532804google scholar: lookup
  9. Chen J, Weng Q, Chao J, Hu D, Taya K. Reproduction and Development of the Released Przewalski's Horses (Equus przewalskii) in Xinjiang, China.. J Equine Sci 2008;19(1):1-7.
    doi: 10.1294/jes.19.1pmc: PMC4019202pubmed: 24833949google scholar: lookup
  10. Chen J, Zhang H, Wu X, Shang S, Yan J, Chen Y, Zhang H, Tang X. Characterization of the gut microbiota in the golden takin (Budorcas taxicolor bedfordi).. AMB Express 2017 Dec;7(1):81.
    doi: 10.1186/s13568-017-0374-5pmc: PMC5392452pubmed: 28413853google scholar: lookup
  11. Chen S, Zhou Y, Chen Y, Gu J. fastp: an ultra-fast all-in-one FASTQ preprocessor.. Bioinformatics 2018 Sep 1;34(17):i884-i890.
    doi: 10.1093/bioinformatics/bty560pmc: PMC6129281pubmed: 30423086google scholar: lookup
  12. Christiansen G, Birkelund S. Transmission electron microscopy and immunogold staining of mollicute surface antigens.. Methods Mol Biol 1998;104:309-18.
    doi: 10.1385/0-89603-525-5:309pubmed: 9711666google scholar: lookup
  13. Clarke R H, Boulton R L, Clarke M F. Translocation of the socially complex Black-eared Miner Manorina melanotis: a trial using hard and soft release techniques. Pac. Conserv. Biol. 8 223–234.
    doi: 10.1071/PC030223google scholar: lookup
  14. Clayton JB, Vangay P, Huang H, Ward T, Hillmann BM, Al-Ghalith GA, Travis DA, Long HT, Tuan BV, Minh VV, Cabana F, Nadler T, Toddes B, Murphy T, Glander KE, Johnson TJ, Knights D. Captivity humanizes the primate microbiome.. Proc Natl Acad Sci U S A 2016 Sep 13;113(37):10376-81.
    doi: 10.1073/pnas.1521835113pmc: PMC5027417pubmed: 27573830google scholar: lookup
  15. Conde DA, Flesness N, Colchero F, Jones OR, Scheuerlein A. Conservation. An emerging role of zoos to conserve biodiversity.. Science 2011 Mar 18;331(6023):1390-1.
    doi: 10.1126/science.1200674pubmed: 21415339google scholar: lookup
  16. Conway WG. Buying time for wild animals with zoos.. Zoo Biol 2011 Jan-Feb;30(1):1-8.
    doi: 10.1002/zoo.20352pubmed: 20938970google scholar: lookup
  17. 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.
    doi: 10.1017/S0007114511003825pubmed: 21816118google scholar: lookup
  18. Dhanasiri AK, Brunvold L, Brinchmann MF, Korsnes K, Bergh Ø, Kiron V. Changes in the intestinal microbiota of wild Atlantic cod Gadus morhua L. upon captive rearing.. Microb Ecol 2011 Jan;61(1):20-30.
    doi: 10.1007/s00248-010-9673-ypubmed: 20424834google scholar: lookup
  19. Dougal K, de la Fuente G, Harris PA, Girdwood SE, Pinloche E, Geor RJ, Nielsen BD, Schott HC 2nd, Elzinga S, Newbold CJ. Characterisation of the faecal bacterial community in adult and elderly horses fed a high fibre, high oil or high starch diet using 454 pyrosequencing.. PLoS One 2014;9(2):e87424.
    doi: 10.1371/journal.pone.0087424pmc: PMC3913607pubmed: 24504261google scholar: lookup
  20. Edgar RC. Search and clustering orders of magnitude faster than BLAST.. Bioinformatics 2010 Oct 1;26(19):2460-1.
    doi: 10.1093/bioinformatics/btq461pubmed: 20709691google scholar: lookup
  21. Fernando SC, Purvis HT 2nd, Najar FZ, Sukharnikov LO, Krehbiel CR, Nagaraja TG, Roe BA, Desilva U. Rumen microbial population dynamics during adaptation to a high-grain diet.. Appl Environ Microbiol 2010 Nov;76(22):7482-90.
    doi: 10.1128/AEM.00388-10pmc: PMC2976194pubmed: 20851965google scholar: lookup
  22. Fu L, Niu B, Zhu Z, Wu S, Li W. CD-HIT: accelerated for clustering the next-generation sequencing data.. Bioinformatics 2012 Dec 1;28(23):3150-2.
    doi: 10.1093/bioinformatics/bts565pmc: PMC3516142pubmed: 23060610google scholar: lookup
  23. Gaunitz C, Fages A, Hanghøj K, Albrechtsen A, Khan N, Schubert M, Seguin-Orlando A, Owens IJ, Felkel S, Bignon-Lau O, de Barros Damgaard P, Mittnik A, Mohaseb AF, Davoudi H, Alquraishi S, Alfarhan AH, Al-Rasheid KAS, Crubézy E, Benecke N, Olsen S, Brown D, Anthony D, Massy K, Pitulko V, Kasparov A, Brem G, Hofreiter M, Mukhtarova G, Baimukhanov N, Lõugas L, Onar V, Stockhammer PW, Krause J, Boldgiv B, Undrakhbold S, Erdenebaatar D, Lepetz S, Mashkour M, Ludwig A, Wallner B, Merz V, Merz I, Zaibert V, Willerslev E, Librado P, Outram AK, Orlando L. Ancient genomes revisit the ancestry of domestic and Przewalski's horses.. Science 2018 Apr 6;360(6384):111-114.
    doi: 10.1126/science.aao3297pubmed: 29472442google scholar: lookup
  24. Guan Y, Yang H, Han S, Feng L, Wang T, Ge J. Comparison of the gut microbiota composition between wild and captive sika deer (Cervus nippon hortulorum) from feces by high-throughput sequencing.. AMB Express 2017 Nov 23;7(1):212.
    doi: 10.1186/s13568-017-0517-8pmc: PMC5700909pubmed: 29170893google scholar: lookup
  25. Halbedel S, Hames C, Stülke J. Regulation of carbon metabolism in the mollicutes and its relation to virulence.. J Mol Microbiol Biotechnol 2007;12(1-2):147-54.
    doi: 10.1159/000096470pubmed: 17183222google scholar: lookup
  26. Hale VL, Tan CL, Niu K, Yang Y, Zhang Q, Knight R, Amato KR. Gut microbiota in wild and captive Guizhou snub-nosed monkeys, Rhinopithecus brelichi.. Am J Primatol 2019 Oct;81(10-11):e22989.
    doi: 10.1002/ajp.22989pubmed: 31106872google scholar: lookup
  27. Hamady M, Lozupone C, Knight R. Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data.. ISME J 2010 Jan;4(1):17-27.
    doi: 10.1038/ismej.2009.97pmc: PMC2797552pubmed: 19710709google scholar: lookup
  28. Hardman B, Moro D. Optimising reintroduction success by delayed dispersal: is the release protocol important for hare-wallabies?. Biol. Conserv. 128 403–411.
    doi: 10.1016/j.biocon.2005.10.006google scholar: lookup
  29. Hyde ER, Navas-Molina JA, Song SJ, Kueneman JG, Ackermann G, Cardona C, Humphrey G, Boyer D, Weaver T, Mendelson JR 3rd, McKenzie VJ, Gilbert JA, Knight R. The Oral and Skin Microbiomes of Captive Komodo Dragons Are Significantly Shared with Their Habitat.. mSystems 2016 Jul-Aug;1(4).
    doi: 10.1128/mSystems.00046-16pmc: PMC5069958pubmed: 27822543google scholar: lookup
  30. Kaczensky P, Ganbataar O, Altansukh N, Enkhsaikhan N, Stauffer C, Walzer C. The danger of having all your eggs in one basket--winter crash of the re-introduced Przewalski's horses in the Mongolian Gobi.. PLoS One 2011;6(12):e28057.
    doi: 10.1371/journal.pone.0028057pmc: PMC3247207pubmed: 22216089google scholar: lookup
  31. Kanehisa M, Goto S. KEGG: kyoto encyclopedia of genes and genomes.. Nucleic Acids Res 2000 Jan 1;28(1):27-30.
    pmc: PMC102409pubmed: 10592173doi: 10.1093/nar/28.1.27google scholar: lookup
  32. King S R B, Boyd L, Zimmermann W, Kendall B. Equus Ferus ssp. Przewalskii. IUCN2016 2016 IUCN Red List of Threatened Species.
  33. Knowles SCL, Eccles RM, Baltrūnaitė L. Species identity dominates over environment in shaping the microbiota of small mammals.. Ecol Lett 2019 May;22(5):826-837.
    doi: 10.1111/ele.13240pubmed: 30868708google scholar: lookup
  34. Kohl KD, Dearing MD. Wild-caught rodents retain a majority of their natural gut microbiota upon entrance into captivity.. Environ Microbiol Rep 2014 Apr;6(2):191-5.
    doi: 10.1111/1758-2229.12118pubmed: 24596293google scholar: lookup
  35. Lavoie C, Courcelle M, Redivo B, Derome N. Structural and compositional mismatch between captive and wild Atlantic salmon (Salmo salar) parrs' gut microbiota highlights the relevance of integrating molecular ecology for management and conservation methods.. Evol Appl 2018 Oct;11(9):1671-1685.
    doi: 10.1111/eva.12658pmc: PMC6183451pubmed: 30344635google scholar: lookup
  36. Li D, Liu CM, Luo R, Sadakane K, Lam TW. MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph.. Bioinformatics 2015 May 15;31(10):1674-6.
    doi: 10.1093/bioinformatics/btv033pubmed: 25609793google scholar: lookup
  37. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform.. Bioinformatics 2009 Jul 15;25(14):1754-60.
    doi: 10.1093/bioinformatics/btp324pmc: PMC2705234pubmed: 19451168google scholar: lookup
  38. Li R, Yu C, Li Y, Lam TW, Yiu SM, Kristiansen K, Wang J. SOAP2: an improved ultrafast tool for short read alignment.. Bioinformatics 2009 Aug 1;25(15):1966-7.
    doi: 10.1093/bioinformatics/btp336pubmed: 19497933google scholar: lookup
  39. Li Y, Hu X, Yang S, Zhou J, Zhang T, Qi L, Sun X, Fan M, Xu S, Cha M, Zhang M, Lin S, Liu S, Hu D. Comparative Analysis of the Gut Microbiota Composition between Captive and Wild Forest Musk Deer.. Front Microbiol 2017;8:1705.
    doi: 10.3389/fmicb.2017.01705pmc: PMC5591822pubmed: 28928728google scholar: lookup
  40. Li Y, Zhang K, Liu Y, Li K, Hu D, Wronski T. Community Composition and Diversity of Intestinal Microbiota in Captive and Reintroduced Przewalski's Horse (Equus ferus przewalskii).. Front Microbiol 2019;10:1821.
    doi: 10.3389/fmicb.2019.01821pmc: PMC6693443pubmed: 31440229google scholar: lookup
  41. Li ZP, Liu HL, Li GY, Bao K, Wang KY, Xu C, Yang YF, Yang FH, Wright AD. Molecular diversity of rumen bacterial communities from tannin-rich and fiber-rich forage fed domestic Sika deer (Cervus nippon) in China.. BMC Microbiol 2013 Jul 8;13:151.
    doi: 10.1186/1471-2180-13-151pmc: PMC3723558pubmed: 23834656google scholar: lookup
  42. Magoč T, Salzberg SL. FLASH: fast length adjustment of short reads to improve genome assemblies.. Bioinformatics 2011 Nov 1;27(21):2957-63.
    doi: 10.1093/bioinformatics/btr507pmc: PMC3198573pubmed: 21903629google scholar: lookup
  43. 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.
    doi: 10.1093/icb/icx090pmc: PMC5978021pubmed: 28985326google scholar: lookup
  44. Meng Y. Research on Feeding Plants, Feeding Habits and Feeding Strategies of Przewalski Horse. Beijing: Beijing Forestry University.
  45. Metcalf JL, Song SJ, Morton JT, Weiss S, Seguin-Orlando A, Joly F, Feh C, Taberlet P, Coissac E, Amir A, Willerslev E, Knight R, McKenzie V, Orlando L. Evaluating the impact of domestication and captivity on the horse gut microbiome.. Sci Rep 2017 Nov 14;7(1):15497.
    doi: 10.1038/s41598-017-15375-9pmc: PMC5686199pubmed: 29138485google scholar: lookup
  46. Moschen AR, Wieser V, Tilg H. Dietary Factors: Major Regulators of the Gut's Microbiota.. Gut Liver 2012 Oct;6(4):411-6.
    doi: 10.5009/gnl.2012.6.4.411pmc: PMC3493718pubmed: 23170142google scholar: lookup
  47. Muegge BD, Kuczynski J, Knights D, Clemente JC, González A, Fontana L, Henrissat B, Knight R, Gordon JI. Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans.. Science 2011 May 20;332(6032):970-4.
    doi: 10.1126/science.1198719pmc: PMC3303602pubmed: 21596990google scholar: lookup
  48. Oakenfull E A, Lim H N, Ryder O A. A survey of equid mitochondrial DNA: implications for the evolution, genetic diversity and conservation of Equus. Conserv. Genet. 1 341–355.
    doi: 10.1023/A:1011559200897google scholar: lookup
  49. Pan X, Xue F, Nan X, Tang Z, Wang K, Beckers Y, Jiang L, Xiong B. Illumina Sequencing Approach to Characterize Thiamine Metabolism Related Bacteria and the Impacts of Thiamine Supplementation on Ruminal Microbiota in Dairy Cows Fed High-Grain Diets.. Front Microbiol 2017;8:1818.
    doi: 10.3389/fmicb.2017.01818pmc: PMC5611408pubmed: 28979254google scholar: lookup
  50. Parks DH, Tyson GW, Hugenholtz P, Beiko RG. STAMP: statistical analysis of taxonomic and functional profiles.. Bioinformatics 2014 Nov 1;30(21):3123-4.
    doi: 10.1093/bioinformatics/btu494pmc: PMC4609014pubmed: 25061070google scholar: lookup
  51. Pryde SE, Duncan SH, Hold GL, Stewart CS, Flint HJ. The microbiology of butyrate formation in the human colon.. FEMS Microbiol Lett 2002 Dec 17;217(2):133-9.
    doi: 10.1016/s0378-1097(02)01106-0pubmed: 12480096google scholar: lookup
  52. Redford KH, Segre JA, Salafsky N, Martinez del Rio C, McAloose D. Conservation and the microbiome.. Conserv Biol 2012 Apr;26(2):195-7.
    doi: 10.1111/j.1523-1739.2012.01829.xpmc: PMC3513825pubmed: 22443125google scholar: lookup
  53. Samsudin AA, Evans PN, Wright AD, Al Jassim R. Molecular diversity of the foregut bacteria community in the dromedary camel (Camelus dromedarius).. Environ Microbiol 2011 Nov;13(11):3024-35.
    doi: 10.1111/j.1462-2920.2011.02579.xpubmed: 21914099google scholar: lookup
  54. Schulte-Hostedde AI, Mastromonaco GF. Integrating evolution in the management of captive zoo populations.. Evol Appl 2015 Jun;8(5):413-22.
    doi: 10.1111/eva.12258pmc: PMC4430766pubmed: 26029256google scholar: lookup
  55. Shanks OC, Kelty CA, Archibeque S, Jenkins M, Newton RJ, McLellan SL, Huse SM, Sogin ML. Community structures of fecal bacteria in cattle from different animal feeding operations.. Appl Environ Microbiol 2011 May;77(9):2992-3001.
    doi: 10.1128/AEM.02988-10pmc: PMC3126396pubmed: 21378055google scholar: lookup
  56. Sommer F, Bäckhed F. The gut microbiota--masters of host development and physiology.. Nat Rev Microbiol 2013 Apr;11(4):227-38.
    doi: 10.1038/nrmicro2974pubmed: 23435359google scholar: lookup
  57. Song SJ, Lauber C, Costello EK, Lozupone CA, Humphrey G, Berg-Lyons D, Caporaso JG, Knights D, Clemente JC, Nakielny S, Gordon JI, Fierer N, Knight R. Cohabiting family members share microbiota with one another and with their dogs.. Elife 2013 Apr 16;2:e00458.
    doi: 10.7554/eLife.00458pmc: PMC3628085pubmed: 23599893google scholar: lookup
  58. Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, Koonin EV, Krylov DM, Mazumder R, Mekhedov SL, Nikolskaya AN, Rao BS, Smirnov S, Sverdlov AV, Vasudevan S, Wolf YI, Yin JJ, Natale DA. The COG database: an updated version includes eukaryotes.. BMC Bioinformatics 2003 Sep 11;4:41.
    doi: 10.1186/1471-2105-4-41pmc: PMC222959pubmed: 12969510google scholar: lookup
  59. Thoetkiattikul H, Mhuantong W, Laothanachareon T, Tangphatsornruang S, Pattarajinda V, Eurwilaichitr L, Champreda V. Comparative analysis of microbial profiles in cow rumen fed with different dietary fiber by tagged 16S rRNA gene pyrosequencing.. Curr Microbiol 2013 Aug;67(2):130-7.
    doi: 10.1007/s00284-013-0336-3pubmed: 23471692google scholar: lookup
  60. Wang J, Chen L, Zhao N, Xu X, Xu Y, Zhu B. Of genes and microbes: solving the intricacies in host genomes.. Protein Cell 2018 May;9(5):446-461.
    doi: 10.1007/s13238-018-0532-9pmc: PMC5960464pubmed: 29611114google scholar: lookup
  61. 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.
    doi: 10.1126/science.1208344pmc: PMC3368382pubmed: 21885731google scholar: lookup
  62. Xia C, Cao J, Zhang H, Gao X, Yang W, Blank D. Reintroduction of Przewalski’s horse (Equus ferus przewalskii) in Xinjiang, China: the status and experience. Biol. Conserv. 177 142–147.
    doi: 10.1016/j.biocon.2014.06.021google scholar: lookup
  63. Zhang Y, Cao QS, Rubenstein DI, Zang S, Songer M, Leimgruber P, Chu H, Cao J, Li K, Hu D. Water Use Patterns of Sympatric Przewalski's Horse and Khulan: Interspecific Comparison Reveals Niche Differences.. PLoS One 2015;10(7):e0132094.
    doi: 10.1371/journal.pone.0132094pmc: PMC4498657pubmed: 26161909google scholar: lookup

Citations

This article has been cited 14 times.
  1. Cui X, Zhang Q, Zhang Q, Chen H, Liu G, Zhu L. The putative maintaining mechanism of gut bacterial ecosystem in giant pandas and its potential application in conservation. Evol Appl 2023 Jan;16(1):36-47.
    doi: 10.1111/eva.13494pubmed: 36699119google scholar: lookup
  2. Hu D, Wang C, Ente M, Zhang K, Zhang D, Li X, Li K, Chu H. Assessment of Adaptation Status of Reintroduced Equus Przewalskii Based on Comparative Analysis of Fecal Bacteria with Those of Captive E. Przewalskii, Domestic Horse and Mongolian Wild Ass. Animals (Basel) 2022 Oct 21;12(20).
    doi: 10.3390/ani12202874pubmed: 36290262google scholar: lookup
  3. Ni Q, Dong S, Xing B, Zeng B, Kong F, Xu H, Yao Y, Li D, Zhang M, Fan X, Yang D, Yang M, Xie M. Oral and fecal microbiome of confiscated Bengal slow lorises in response to confinement duration. Front Microbiol 2022;13:941261.
    doi: 10.3389/fmicb.2022.941261pubmed: 36238588google scholar: lookup
  4. Tang L, Gao Y, Yan L, Jia H, Chu H, Ma X, He L, Wang X, Li K, Hu D, Zhang D. Comparative Analysis of Microbiome Metagenomics in Reintroduced Wild Horses and Resident Asiatic Wild Asses in the Gobi Desert Steppe. Microorganisms 2022 Jun 7;10(6).
    doi: 10.3390/microorganisms10061166pubmed: 35744684google scholar: lookup
  5. Hu D, Yang J, Qi Y, Li B, Li K, Mok KM. Metagenomic Analysis of Fecal Archaea, Bacteria, Eukaryota, and Virus in Przewalski's Horses Following Anthelmintic Treatment. Front Vet Sci 2021;8:708512.
    doi: 10.3389/fvets.2021.708512pubmed: 34490397google scholar: lookup
  6. Zhu Y, Wang X, Deng L, Chen S, Zhu C, Li J. Effects of Pasture Grass, Silage, and Hay Diet on Equine Fecal Microbiota. Animals (Basel) 2021 May 7;11(5).
    doi: 10.3390/ani11051330pubmed: 34066969google scholar: lookup
  7. Hu D, Chao Y, Zhang B, Wang C, Qi Y, Ente M, Zhang D, Li K, Mok KM. Effects of Gasterophilus pecorum infestation on the intestinal microbiota of the rewilded Przewalski's horses in China. PLoS One 2021;16(5):e0251512.
    doi: 10.1371/journal.pone.0251512pubmed: 33974667google scholar: lookup
  8. Zheng Y, Zheng C, Sun K, Liu H, Fan H, Wang Y, Nan X, An L, Pan F, Wang X, Xu G, Liu T. Calcium Nitrate Supplementation Improves Meat Quality in Hu Sheep via Microbial and Transcriptomic Regulation. Animals (Basel) 2026 Jan 21;16(2).
    doi: 10.3390/ani16020325pubmed: 41594513google scholar: lookup
  9. Liu H, Xiao L, Liu Z, Deng Y, Zhu J, Yang C, Liu Q, Tian D, Cui X, Peng J. Impacts of Captive Domestication and Geographical Divergence on the Gut Microbiome of Endangered Forest Musk Deer. Animals (Basel) 2025 Jul 2;15(13).
    doi: 10.3390/ani15131954pubmed: 40646853google scholar: lookup
  10. Gao C, Huang Q, Yang X, Cui X, Wen K, Liu Y, Wang C, Dai Q, Xie J, Zhu L. Diet and environment drive the convergence of gut microbiome in wild-released giant pandas and forest musk deer. iScience 2025 Jul 18;28(7):112837.
    doi: 10.1016/j.isci.2025.112837pubmed: 40620903google scholar: lookup
  11. Wang C, Li C, You F, Zhou Y, Tu G, Liu R, Yi P, Wu X, Nie H. Multi-Omics Analysis of Gut Microbiome and Host Metabolism in Different Populations of Chinese Alligators (alligator sinensis) During Various Reintroduction Phases. Ecol Evol 2025 Apr;15(4):e71221.
    doi: 10.1002/ece3.71221pubmed: 40212922google scholar: lookup
  12. van Leeuwen PML, Mastromonaco GF, Mykytczuk N, Schulte-Hostedde AI. Captivity conditions matter for the gut microbiota of an endangered obligate hibernator. Conserv Physiol 2024;12(1):coae072.
    doi: 10.1093/conphys/coae072pubmed: 39464172google scholar: lookup
  13. Subrata SA, Yuda P, Artama WT, de-Garine Wichatitsky M, André A, Michaux J. Rusa deer microbiota: the importance of preliminary data analysis for meaningful diversity comparisons. Int Microbiol 2025 Jan;28(1):37-47.
    doi: 10.1007/s10123-024-00521-xpubmed: 38589705google scholar: lookup
  14. Li J, Huang X, He L, Li C, Jing H, Lin J, Ma C, Li X. Effect of ellagic acid on body weight, nutrient digestibility, fecal microbiota, and urolithin A metabolism in Thoroughbred horses. J Anim Sci 2023 Jan 3;101.
    doi: 10.1093/jas/skad232pubmed: 37422771google scholar: lookup
Subscribe to our newsletter
Join 99,359 horse owners like you who receive our email updates on horse health and nutrition.