Analyze Diet
Animals : an open access journal from MDPI2022; 12(20); doi: 10.3390/ani12202874

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.

Abstract: Intestinal microbiota play an important role in the survival of the host. However, no study to date has elucidated the adjustment of intestinal microbiota of the host during rewilding. Thus, this study aims to describe the intestinal bacterial community of reintroduced Przewalski’s horse (RPH) after being released into their original habitat for approximately 20 years in comparison with that of captive Przewalski’s horse (CPH), sympatric domestic horse (DH) and Mongolian wild ass (MWA) by sequencing the 16S rRNA gene. The results showed that the prevalent bacterial communities were different among CPHs, RPHs, DHs and MWAs at the family level. NMDS and ANOSIM analysis showed that the pattern of bacterial community composition in captive equines was distinct from that in the wild groups. It is shown that some bacteria had significant differences among different taxa (p < 0.001), such as Firmicutes, Bacteroidetes, Armatimonadetes, Clostrida, Bacteroidia, Clostridiales, Bacteroidales, Rikenellaceae and Bacteroidales_UCG-001. These bacteria were associated with the transition from in captive to in the wild (CPH and RPH), which reflected the change of environmental conditions. Meanwhile, Proteobacteria, Clostridia, Bacilli, Negativicutes, Gammaproteobacteria, Clostridiales, Bacillales, Selenomonadales, Pseudomonadales and Planococcaceae were the changed groups among RPHs, MWAs and DHs, which are related to feeding habits and diseases. Our results clearly showed the differences between intestinal microbiota in reintroduced animals and wild animals and led us to understand the survival state of reintroduced animals in the wild.
Publication Date: 2022-10-21 PubMed ID: 36290262PubMed Central: PMC9598124DOI: 10.3390/ani12202874Google 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.
  • 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.

The research aimed to understand how the gut bacteria of reintroduced Przewalski’s horses changes when they return to the wild, by comparing them with captive Przewalski’s horses, domestic horses, and Mongolian wild asses. The outcomes showed significant differences in their gut bacterial communities, thereby providing insight into the survival and adjustment of reintroduced animals in their natural habitats.

Objective and Approach

  • The study was driven by the need to explore how the intestinal microbiota (the community of microorganisms) of a host animal adapts during the process of reintroducing those animals from captivity to their respective wild environments.
  • Researchers conducted this study by comparing the intestinal bacterial communities of reintroduced Przewalski’s horses (RPHs), captive Przewalski’s horses (CPHs), domestic horses (DHs), and Mongolian wild asses (MWAs).
  • The comparative analysis was primarily based on sequencing the 16S rRNA gene, a crucial method used in examining bacterial profiles).

Findings

  • The findings demonstrated significant differences in prevalent bacterial communities among animals from the four different groups.
  • Specific indices (NMDS and ANOSIM) indicated that the pattern of bacterial community composition in captive animals differed substantially from those in the wild.
  • Certain groups of bacteria displayed considerable disparities among the different taxa like Firmicutes, Bacteroidetes, Armatimonadetes, and others. These bacteria are associated with environmental change as animals transition from captivity to the wild.
  • Other groups like Proteobacteria, Clostridia, Bacilli, etc., differed among RPHs, MWAs, and DHs, indicating differing feeding habits and susceptibility to diseases.

Implications

  • This research provides comprehensive evidence on how the intestinal microbiota of reintroduced Przewalski’s horses adapts to life back in the wild.
  • The shift in microbial communities can indicate changes in diet, lifestyle, and susceptibility to diseases in these reintroduced animals.
  • The results can aid in understanding the survival and adaptation mechanisms of reintroduced animals, thereby helping conservationists in making well-informed decisions for future reintroductions.

Cite This Article

APA
Hu D, Wang C, Ente M, Zhang K, Zhang D, Li X, Li K, Chu H. (2022). 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), 12(20). https://doi.org/10.3390/ani12202874

Publication

ISSN: 2076-2615
NlmUniqueID: 101635614
Country: Switzerland
Language: English
Volume: 12
Issue: 20

Researcher Affiliations

Hu, Dini
  • School of Ecology and Nature Conservation, Beijing Forestry University, Qinghua East Road No.35, Beijing 100083, China.
Wang, Chen
  • Xinjiang Kalamaili Ungulate Nature Reserve Management Center, Changji 831100, China.
Ente, Make
  • Xinjiang Research Centre for Breeding Przewalski's Horse, Urumqi 831700, China.
Zhang, Ke
  • School of Ecology and Nature Conservation, Beijing Forestry University, Qinghua East Road No.35, Beijing 100083, China.
Zhang, Dong
  • School of Ecology and Nature Conservation, Beijing Forestry University, Qinghua East Road No.35, Beijing 100083, China.
Li, Xuefeng
  • Xinjiang Research Centre for Breeding Przewalski's Horse, Urumqi 831700, China.
Li, Kai
  • School of Ecology and Nature Conservation, Beijing Forestry University, Qinghua East Road No.35, Beijing 100083, China.
Chu, Hongjun
  • Institute of Forest Ecology, Xinjiang Academy of Forestry, Urumqi 830063, China.

Grant Funding

  • 2020TQ0047 / China Postdoctoral Science Foundation
  • 31670538 / National Natural Science Foundation of China
  • 02210823 / the Forestry Fund of LiBin

Conflict of Interest Statement

The authors declare no conflict of interest.

References

This article includes 58 references
  1. King S.R.B., Boyd L., Zimmermann W., Kendall B. IUCN 2016. IUCN Red List of Threatened Species; Cambridg, UK: 2015. [(accessed on 16 October 2022)]. Equus ferus ssp. Przewalskii. Available online: https://www.iucnredlist.org/
  2. Mohr E.. The Asiatic Wild Horse. J. A. Ellen & Co. Ltd.; London, UK: 1972. pp. 1–124.
  3. Zhang H., Sun L., Cao J.. The Breeding Status of Captive Przewalskii horse in Xinjiang. Chin. J. Zool. 2002:70–72.
  4. Chu H., Jiang Z.G., Lan W., Wang C., Tao Y.S., Jiang F.. Dietary overlap among Kulan Equus hemionus, Goitered gazelle Gazella subgutturosa and livestock. Acta. Zool. Sin. 2008;54:941–954.
  5. Cao J., Hu D., Chen J., Zhang H.. A preliminary observation on the behavioral changes of released Prezwalski’s horses in rewilding process. J. Xinjiang Norm. Univ. Nat. Sci. Ed. 2007;4:69–73.
  6. Chen J.. Utilization of Food, Water and Space by Released Przewalski horse (Equus przewalski) with Reference to Survival Strategies Analysis. J. Beijing For. Univ. 2008.
  7. Wang J., Hu D., Li K., Chen J.. Study on the behavior and activity budgets of reintroduced female Przewalski horse in lactation period. J. Xinjiang Norm. Univ. Nat. Sci. Ed. 2009;28:13–17.
  8. Zhang F., Hu D., Li K., Cao J., Chen J., Waltrau Z.. The agonistic behavior and hierarchical formation of the Equus przewalskii herd in the individual coalition and initial releasing period. Chin. J. Zool. 2009;44:58–63.
  9. Yu X., Hu D., Tang Y., Ji S., Zhang Y., Liu G.. Physiological response of behavior and stress in breeding group of Przewalskii horse during releasing process. China Anim. Husb. Vet. Med. 2011;38:561–580.
  10. Huang X., Ji S., Zhang Y., Cao J., Chu H., Li K., Hu D.. Change of released Equus przewalskii family and the implication to their management in initial period. Sichuan J. Zool. 2012;31:488–491+496.
  11. Meng Y., Hu D., He D., Chen J., Zhang F.. The breeding status of the released Przewalski horses in Xinjiang, China. Bull. Biol. 2009;44:5.
  12. Huang H., Chu H., Cao J., Bu L., Hu D., Zhang D., Li K.. Distribution of Gasterophilus (Diptera, Gasterophilidae) myiasis foci in arid desert steppe: A case study of Kalamaili Mountain Ungulate Nature Reserve. Scien. Silva. Sin. 2017;53:142–149.
  13. Liu G., Shafer A.B., Zimmermann W., Hu D., Wang W.T., Chu H.J., Cao J., Zhao C.X.. Evaluating the reintroduction project of Przewalski’s horse in China using genetic and pedigree data. Biol. Conserv. 2014;171:288–298.
  14. Hu D., Chao Y., Zhang B., Wang C., Qi Y., Ente M., Zhang D., Li K., Mok K.M.. Effects of Gasterophilus pecorum infestation on the intestinal microbiota of the rewilded Przewalski’s horses in China. PLoS ONE 2021;16:e025151.
    pmc: PMC8112688pubmed: 33974667
  15. Berry D., Kuzyk O., Rauch I., Heider S., Schwab C., Hainzl E., Decker T., Müller M., Strobl B., Schleper C.. Intestinal microbiota signatures associated with inflammation history in mice experiencing recurring colitis. Front. Microbiol. 2015;6:1408.
    doi: 10.3389/fmicb.2015.01408pmc: PMC4678223pubmed: 26697002google scholar: lookup
  16. Xiong J., Wang K., Wu J., Qiuqian L., Yang K., Qian Y., Zhang D.. Changes in intestinal bacterial communities are closely associated with shrimp disease severity. Appl. Microbiol. Biot. 2015;99:6911–6919.
    doi: 10.1007/s00253-015-6632-zpubmed: 25947250google scholar: lookup
  17. Sadet-Bourgeteau S., Julliand V.. The diversity of the microbial ecosystem in the equine digestive tract. INRA. Prod. Anim. 2012;25:407–418.
  18. Sadet-Bourgeteau S., Julliand V.. Equine microbial gastro-intestinal health. EAAP Sci. Ser. 2010;128:161–182.
  19. van Leeuwen P., Mykytczuk N., Mastromonaco G.F., Schulte-Hostedde A.. Effects of captivity, diet, and relocation on the gut bacterial communities of white-footed mice. Ecol. Evol. 2020;94:4677–4690.
    doi: 10.1002/ece3.6221pmc: PMC7297780pubmed: 32551052google scholar: lookup
  20. Sjögren Y.M., Tomicic S., Lundberg A., Böttcher M.F., Björkstén B., Sverremark-Ekström E., Jenmalm M.C.. Influence of early gut microbiota on the maturation of childhood mucosal and systemic immune responses: Gut microbiota and immune responses. Clini. Exp. Allergy 2009;39:1842–1851.
  21. El Aidy S., Van Den Bogert B., Kleerebezem M.. The small intestine microbiota, nutritional modulation and relevance for health. Curr. Opin. Biotech. 2015;32:14–20.
    doi: 10.1016/j.copbio.2014.09.005pubmed: 25308830google scholar: lookup
  22. Michail S., Lin M., Frey M.R., Fanter R., Wai D., Cleary J.G., Hilbush B.. Altered gut microbial energy and metabolism in children with non-alcoholic fatty liver disease. Fems. Microbiol. Ecol. 2015;91:1.
    doi: 10.1093/femsec/fiu002pmc: PMC4358749pubmed: 25764541google scholar: lookup
  23. Murphy E.A., Velazquez K.T., Herbert K.M.. Influence of high-fat-diet on gut microbiota: A driving force for chronic disease risk. Curr. Opin. Clin. Nutr. Metab. Care 2015;18:515.
  24. Boulangé C.L., Neves A.L., Chilloux J., Nicholson J.K., Dumass M.E.. Impact of the gut microbiota on inflammation, obesity, and metabolic disease. Genome. Med. 2016;8:42.
    doi: 10.1186/s13073-016-0303-2pmc: PMC4839080pubmed: 27098727google scholar: lookup
  25. Li X., Watanabe K., Kimura I.. Gut microbiota dysbiosis drives and implies novel therapeutic strategies for diabetes mellitus and related metabolic diseases. Front. Immunol. 2017;8:1882.
    doi: 10.3389/fimmu.2017.01882pmc: PMC5742320pubmed: 29326727google scholar: lookup
  26. Sun M.F., Shen Y.Q.. Dysbiosis of gut microbiota and microbial metabolites in Parkinson’s Disease. Ageing. Res. Rev. 2018;45:53–61.
    doi: 10.1016/j.arr.2018.04.004pubmed: 29705121google scholar: lookup
  27. Quiroga-González C., Cardenas L.A.C., Ramírez M., Reyes A., González C., Stevenson P.R.. Monitoring the variation in the gut microbiota of captive woolly monkeys related to changes in diet during a reintroduction process. Sci. Rep. 2021;11:6522.
    doi: 10.1038/s41598-021-85990-0pmc: PMC7985493pubmed: 33753830google scholar: lookup
  28. Russell W.M.S., Burch R.. The Principles of Humane Experimental Technique. Methuen; London, UK: 1959.
  29. Wu H., Chu H., Wang Y., Ma J., Ge Y.. Monitoring activity rhythms of Equus hemionus at watering holes by camera traps in Mount Kalamaili Ungulate Nature Reserve, Xinjiang. Biodivers. Sci. 2014;22:752–757.
  30. Sen Z., Qing C., Keremu A., Liu S., Zhang Y., Hu D.. Food patch particularity and forging strategy of reintroduced Przewalski’s horse in North Xinjiang, China. Turk. J. Zool. 2017;41:924–930.
    doi: 10.3906/zoo-1509-9google scholar: lookup
  31. Meng Y., Hu D., Chen J.. Study on feeding source plants and strategy of wild Przewalskii horse. Proceedings of the Fourth National Symposium on Wildlife Ecology and Resource Conservation 2007; Xining, China. 2–5 December 2007; (In Chinese).
  32. Ge Y., Liu C., Chu H., Tao Y.. Present situation of the Equus hemionus resources in the Karamori Mountain Nature Reserve, Xinjiang. Arid Zone Res. 2003;20:32–34, 66.
  33. Ji S.. Non-Invasive Study of the Behavioral and Physiological Ecology Adaptation in Captive Przewalski’s horse (Equus ferus przewalskii). Ph.D. Thesis. Beijing Forestry University; Beijing, China: 2013.
  34. Chen J., Hu D., Li K., Cao J., Meng Y., Cui Y.Y.. The diurnal feeding behavior comparison between the realeased and captive adult female Przewalski’s horse (Equus przewalskii) in summer. Acta. Ecol. Sin. 2008;28:1104–1108.
  35. Riquelme J., Cazanga V., Jeldres J., Pérez R.. Pharmacokinetics of ivermectin in sheep following pretreatment with Escherichia coli endotoxin. J. Vet. Pharmacol. Ther. 2018;41:755–759.
    doi: 10.1111/jvp.12665pubmed: 29889311google scholar: lookup
  36. Yu M., Jia H., Zhou C., Yang Y., Zhao Y., Yang M., Zou Z.. Variations in gut microbiota and fecal metabolic phenotype associated with depression by 16S rRNA gene sequencing and LC/MS-based metabolomics. J. Pharmaceut. Biomed. 2017;138:231–239.
    doi: 10.1016/j.jpba.2017.02.008pubmed: 28219800google scholar: lookup
  37. Quast C., Pruesse E., Yilmaz P., Gerken J., Schweer T., Yarza P., Peplies J., Glockner F.O.. The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic. Acids. Res. 2012;41:590–596.
    doi: 10.1093/nar/gks1219pmc: PMC3531112pubmed: 23193283google scholar: lookup
  38. Salem S.E., Maddox T.W., Berg A., Antczak P., Ketley J.M., Williams N.J., Archer D.C.. Variation in faecal microbiota in a group of horses managed at pasture over a 12-month period. Sci. Rep. 2018;8:8510.
    doi: 10.1038/s41598-018-26930-3pmc: PMC5981443pubmed: 29855517google scholar: lookup
  39. Lin H., Peddada S.D.. Analysis of microbial compositions: A review of normalization and differential abundance analysis. NPJ. Biofilms. Microbi. 2020;6:60.
    doi: 10.1038/s41522-020-00160-wpmc: PMC7710733pubmed: 33268781google scholar: lookup
  40. Caporaso J.G., Kuczynski J., Stombaugh J., Bittinger K., Bushman F.D., Costello E.K., Fierer N., Peña A.G., Goodrich J.K., Gordon J.I.. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 2010;7:335.
    doi: 10.1038/nmeth.f.303pmc: PMC3156573pubmed: 20383131google scholar: lookup
  41. Ihaka R., Gentleman R.. R: A language for data analysis and graphics. J. Comput. Graph. Stat. 1996;5:299–314.
  42. Deng G., Zha Y., Zhang G., Wang Y., Li Y., Peng X., Zhou H., Liu Y.. Comparison of human and animal fecal microbiota with Illumina sequencing of 16S rRNA tags. Ecologic. Sci. 2014;33:851–857.
  43. 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
  44. Tang L., Li Y., Srivathsan A., Guo Y., Li K., Hu D., Zhang D.. 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. 2020;11:363.
    doi: 10.3389/fmicb.2020.00363pmc: PMC7081077pubmed: 32226419google scholar: lookup
  45. Chen J., Hu D., Cao J., Lv Q., Men Y.. A preliminary report on the summer water resources used by Equus przewalskii. J. Xinjiang Norm. Univ. Nat. Sci. Ed. 2008;27:76–79.
  46. Liu R., Shi J., Shultz S., Guo D., Liu D.. Fecal bacterial community of allopatric Przewalski’s gazelles and their sympatric relatives. Front. Microbiol. 2021;12:737042.
    doi: 10.3389/fmicb.2021.737042pmc: PMC8499116pubmed: 34630362google scholar: lookup
  47. Zhao Y., Li B., Bai D., Huang J., Shiraigo W., Yang L., Zhao Q., Ren X., Wu J., Bao W.. Comparison of fecal microbiota of Mongolian and thoroughbred horses by high-throughput sequencing of the V4 Region of the 16S rRNA gene. Asian–Austral. J. Anim. Sci. 2016;29:1345.
    doi: 10.5713/ajas.15.0587pmc: PMC5003997pubmed: 26954132google scholar: lookup
  48. 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;7:212.
    doi: 10.1186/s13568-017-0517-8pmc: PMC5700909pubmed: 29170893google scholar: lookup
  49. Zhang M., Shi M., Fan M., Xu S., Li Y., Zhang T., Cha M., Liu Y., Guo X., Chen Q.. Comparative analysis of gut microbiota changes in Père David’s deer populations in Beijing Milu Park and Shishou, Hubei province in China. Front. Microbiol. 2018;9:1258.
    doi: 10.3389/fmicb.2018.01258pmc: PMC6005820pubmed: 29946310google scholar: lookup
  50. Xu J., Bjursell M.K., Himrod J., Deng S., Carmichael L.K., Chiang H.C., Hooper L.V., Gordon J.I.. A genomic view of the human-Bacteroides thetaiotaomicron symbiosis. Science 2003;299:2074–2076.
    doi: 10.1126/science.1080029pubmed: 12663928google scholar: lookup
  51. Bäckhed F., Ley R.E., Sonnenburg J.L., Peterson D.A., Gordon J.I.. Host-bacterial mutualism in the human intestine. Science 2005;307:1915–1920.
    doi: 10.1126/science.1104816pubmed: 15790844google scholar: lookup
  52. Chen S., Cheng H., Wyckoff K.N., He Q.. Linkages of Firmicutes and Bacteroidetes populations to methanogenic process performance. J Ind. Microbiol. Biot. 2016;43:771–781.
    doi: 10.1007/s10295-016-1760-8pubmed: 27021844google scholar: lookup
  53. Biddle A., Tomb J.F., Fan Z.. Microbiome and blood analyte differences point to community and metabolic signatures in lean and obese horses. Front. Vet. Sci. 2018;5:225.
    doi: 10.3389/fvets.2018.00225pmc: PMC6158370pubmed: 30294603google scholar: lookup
  54. Schwab C., Cristescu B., Northrup J.M., Stenhouse G.B., Ganzle M.. Diet and environment shape fecal bacterial microbiota composition and enteric pathogen load of grizzly bears. PLoS ONE 2011;6:e27905.
  55. Navarrete P., Magne F., Araneda C., Fuentes P., Barros L., Opazo R., Espejo R., Romero J.. PCR-TTGE analysis of 16S rRNA from rainbow trout (Oncorhynchus mykiss) gut microbiota reveals host-specific communities of active bacteria. PLoS ONE 2012;7:e31335.
  56. Shin N.R., Whon T.W., Bae J.W.. Proteobacteria: Microbial signature of dysbiosis in gut microbiota. Trends. Biotechnol. 2015;33:496–503.
    doi: 10.1016/j.tibtech.2015.06.011pubmed: 26210164google scholar: lookup
  57. Huang H., Zhang B., Chu H., Zhang D., Li K.. Gasterophilus (Diptera, Gasterophilidae) infestation of equids in the Kalamaili nature Reserve, China. Parasite 2016;23:36.
    doi: 10.1051/parasite/2016036pmc: PMC5018932pubmed: 27593434google scholar: lookup
  58. Xu W., Yang W., Qiao J.. Food habits of Kulan (Equus hemionus) in Kalamaili Mountain Nature Reserve, Xinjiang, China. Acta Theriologica Sin. 2009;29:427–431.