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A Comparison of the Intestinal Fungal Community in Wild and Captive Himalayan Vultures (Gyps himalayensis) Cover

A Comparison of the Intestinal Fungal Community in Wild and Captive Himalayan Vultures (Gyps himalayensis)

Open Access
|Sep 2025

References

  1. Abarenkov K, Nilsson RH, Larsson KH, Taylor AFS, May TW, Frøslev TG, Pawlowska J, Lindahl B, Põldmaa K, Truong C, et al. The UNITE database for molecular identification and taxonomic communication of fungi and other eukaryotes: Sequences, taxa and classifications reconsidered. Nucleic Acids Res. 2024 Jan;52(D1):D791–D797. https://doi.org/10.1093/nar/gkad1039
  2. Atiwesh G, Parrish CC, Banoub J, Le TT. Lignin degradation by microorganisms: A review. Biotechnol Prog. 2022 Mar;38(2):e3226. https://doi.org/10.1002/btpr.3226
  3. Berlow M, Wada H, Derryberry EP. Experimental exposure to noise alters gut microbiota in a captive songbird. Microb Ecol. 2022 Nov;84(4):1264–1277. https://doi.org/10.1007/s00248-021-01924-3
  4. Blumstein DT, Rangchi TN, Briggs T, De Andrade FS, Natterson-Horowitz B. A systematic review of carrion eaters’ adaptations to avoid sickness. J Wildl Dis. 2017 Jul;53(3):577–581. https://doi.org/10.7589/2016-07-162
  5. Bodawatta KH, Hird SM, Grond K, Poulsen M, Jønsson KA. Avian gut microbiomes taking flight. Trends Microbiol. 2022 Mar;30(3):268–280. https://doi.org/10.1016/j.tim.2021.07.003
  6. Bornbusch SL, Greene LK, Rahobilalaina S, Calkins S, Rothman RS, Clarke TA, LaFleur M, Drea CM. Gut microbiota of ring-tailed lemurs (Lemur catta) vary across natural and captive populations and correlate with environmental microbiota. Anim Microbiome. 2022 Apr;4(1):29. https://doi.org/10.1186/s42523-022-00176-x
  7. Borruso L, Checcucci A, Torti V, Correa F, Sandri C, Luise D, Cavani L, Modesto M, Spiezio C, Mimmo T, et al. I like the way you eat it: Lemur (Indri indri) gut mycobiome and geophagy. Microb Ecol. 2021 Jul;82(1):215–223. https://doi.org/10.1007/s00248-020-01677-5
  8. Buechley ER, Şekercioğlu ÇH. The avian scavenger crisis: Looming extinctions, trophic cascades, and loss of critical ecosystem functions. Biological Conservation. 2016 Jun;198:220 –228. https://doi.org/10.1016/j.biocon.2016.04.001
  9. Campbell TP, Sun X, Patel VH, Sanz C, Morgan D, Dantas G. The microbiome and resistome of chimpanzees, gorillas, and humans across host lifestyle and geography. ISME J. 2020 Jun;14(6):1584– 1599. https://doi.org/10.1038/s41396-020-0634-2
  10. Chen C, Li M, Li F, Liang X, Zhang H, Gu Y, Guo G. Dynamic alterations of the intestinal microbiota of fifth-instar silkworms (Bombyx mori) fed an artificial diet or mulberry leaves. Insects. 2024 Dec;15(12):970. https://doi.org/10.3390/insects15120970
  11. Chen S, Zhou Y, Chen Y, Gu J. fastp: An ultra-fast all-in-one FASTQ preprocessor. Bioinformatics. 2018 Sep;34(17):i884–i890. https://doi.org/10.1093/bioinformatics/bty560
  12. Dallas JW, Warne RW. Captivity and animal microbiomes: Potential roles of microbiota for influencing animal conservation. Microb Ecol. 2023 Apr;85(3):820–838. https://doi.org/10.1007/s00248-022-01991-0
  13. Edgar RC. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods. 2013 Oct;10(10):996–998. https://doi.org/10.1038/nmeth.2604
  14. García-Jiménez R, Pérez-García JM, Margalida A, Morales-Reyes Z. Avian scavengers’ contributions to people: The cultural dimension of wildlife-based tourism. Sci Total Environ. 2022 Feb;806(Pt_1):150419. https://doi.org/10.1016/j.scito-tenv.2021.150419
  15. Glushakova АМ, Kachalkin АV. Yeast community succession in cow dung composting process. Fungal Biol. 2023 Jun;127(6):1075– 1083. https://doi.org/10.1016/j.funbio.2023.06.001
  16. Guo W, Mishra S, Wang C, Zhang H, Ning R, Kong F, Zeng B, Zhao J, Li Y. Comparative study of gut microbiota in wild and captive giant pandas (Ailuropoda melanoleuca). Genes. 2019 Oct;10(10):827. https://doi.org/10.3390/genes10100827
  17. Hagberg AA, Schult DA, Swart PJ. Exploring network structure, dynamics, and function using NetworkX. In: Varoquaux G, Vaught T, Millman J, editors. Proceedings of the 7th Python in Science Conference (SciPy2008). Pasadena (USA); 2008. p. 11–15.
  18. Henriques M, Buij R, Monteiro H, Sá J, Wambar F, Tavares JP, Botha A, Citegetse G, Lecoq M, Catry P, et al. Deliberate poisoning of Africa’s vultures. Science. 2020 Oct;370(6514):304. https://doi.org/10.1126/science.abd1862
  19. Hill JH, Bell R, Barrios L, Baird H, Ost K, Greenewood M, Monts JK, Tracy E, Meili CH, Chiaro TR, et al. Neonatal fungi promote lifelong metabolic health through macrophage-dependent β cell development. Science. 2025 Mar;387(6738):eadn0953. https://doi.org/10.1126/science.adn0953
  20. Hill JH, Round JL. Intestinal fungal-host interactions in promoting and maintaining health. Cell Host Microbe. 2024 Oct;32(10):1668– 1680. https://doi.org/10.1016/j.chom.2024.09.010
  21. Ives AM, Brenn-White M, Buckley JY, Kendall CJ, Wilton S, Deem SL. A global review of causes of morbidity and mortality in free-living vultures. Ecohealth. 2022 Mar;19(1):40–54. https://doi.org/10.1007/s10393-021-01573-5
  22. Ji P, Rhoads WJ, Edwards MA, Pruden A. Impact of water heater temperature setting and water use frequency on the building plumbing microbiome. ISME J. 2017 Jun;11(6):1318–1330. https://doi.org/10.1038/ismej.2017.14
  23. Li F, Gao Y, Cheng W, Su X, Yang R. Gut fungal mycobiome: A significant factor of tumor occurrence and development. Cancer Lett. 2023 Aug;569:216302. https://doi.org/10.1016/j.canlet.2023.216302
  24. Li J, Chen D, Yu B, He J, Huang Z, Zheng P, Mao X, Li H, Yu J, Luo J, et al. Batch and sampling time exert a larger influence on the fungal community than gastrointestinal location in model animals: A meaningful case study. Front Nutr. 2022 Nov;9:1021215. https://doi.org/10.3389/fnut.2022.1021215
  25. Li Z, Zhao W, Jiang Y, Wen Y, Li M, Liu L, Zou K. New insights into biologic interpretation of bioinformatic pipelines for fish eDNA metabarcoding: A case study in Pearl River estuary. J Environ Manage. 2024 Sep;368:122136. https://doi.org/10.1016/j.jenvman.2024.122136
  26. Liu HY, Li S, Ogamune KJ, Ahmed AA, Kim IH, Zhang Y, Cai D. Fungi in the gut microbiota: Interactions, homeostasis, and host physiology. Microorganisms. 2025 Jan;13(1):70. https://doi.org/10.3390/microorganisms13010070
  27. Liu T, Asif IM, Chen Y, Zhang M, Li B, Wang L. The Relationship between diet, gut mycobiome, and functional gastrointestinal disorders: Evidence, doubts, and prospects. Mol Nutr Food Res. 2024a May;68(9):e2300382. https://doi.org/10.1002/mnfr.202300382
  28. Liu X, Yu J, Huan Z, Xu M, Song T, Yang R, Zhu W, Jiang J. Comparing the gut microbiota of Sichuan golden monkeys across multiple captive and wild settings: Roles of anthropogenic activities and host factors. BMC Genomics. 2024b Feb;25(1):148. https://doi.org/10.1186/s12864-024-10041-7
  29. Lu X, Ke D, Zeng X, Gong G, Ci R. Status, ecology, and conservation of the Himalayan griffon Gyps himalayensis (Aves, Accipitridae) in the Tibetan plateau. Ambio. 2009 May;38(3):166–173. https://doi.org/10.1579/0044-7447-38.3.166
  30. Lu Z, Wang Z, Jia H, Meng D, Wu D. Captivity reduces diversity and shifts composition of the great bustard (Otis tarda dybowskii) microbiome. Ecol Evol. 2025 Jan;15(1):e70836. https://doi.org/10.1002/ece3.70836
  31. Magoč T, Salzberg SL. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics. 2011 Nov;27(21):2957–2963. https://doi.org/10.1093/bioinformatics/btr507
  32. Marneweck CJ, Katzner TE, Jachowski DS. Predicted climate-induced reductions in scavenging in eastern North America. Glob Chang Biol. 2021 Jul;27(14):3383–3394. https://doi.org/10.1111/gcb.15653
  33. Martínez-Mota R, Kohl KD, Orr TJ, Denise Dearing M. Natural diets promote retention of the native gut microbiota in captive rodents. ISME J. 2020 Jan;14(1):67–78. https://doi.org/10.1038/s41396-019-0497-6
  34. Meng X, Lu S, Wang Y, Lai XH, Wen Y, Jin D, Yang J, Bai X, Zhang G, Pu J, Lan R, Xu J. Actinomyces vulturis sp. nov., isolated from Gyps himalayensis. Int J Syst Evol Microbiol. 2017a Jun;67(6):1720- 1726. https://doi.org/10.1099/ijsem.0.001851
  35. Meng X, Lu S, Yang J, Jin D, Wang X, Bai X, Wen Y, Wang Y, Niu L, Ye C, et al. Metataxonomics reveal vultures as a reservoir for Clostridium perfringens. Emerg Microbes Infect. 2017b Feb 22;6(2):e9. https://doi.org/10.1038/emi.2016.137
  36. Mohamed TM, Sun W, Bumbie GZ, Elokil AA, Mohammed KAF, Zebin R, Hu P, Wu L, Tang Z. Feeding Bacillus subtilis ATCC19659 to broiler chickens enhances growth performance and immune function by modulating intestinal morphology and cecum microbiota. Front Microbiol. 2022 Feb;12:798350. https://doi.org/10.3389/fmicb.2021.798350
  37. Moreno-Opo R, Carapeto R, Casimiro R, Rubio C, Muñoz B, Moreno I, Aymerich M. The veterinary use of diclofenac and vulture conservation in Spain: Updated evidence and socio-ecological implications. Sci Total Environ. 2021 Nov;796:148851. https://doi.org/10.1016/j.scitotenv.2021.148851
  38. Nguyen NH, Song Z, Bates ST, Branco, S, Tedersoo L, Menke J, Schilling JS, Kennedy PG. FUNGuild: An open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol. 2016;20:241–248. https://doi.org/10.1016/j.funeco.2015.06.006
  39. Paudel K, Amano T, Acharya R, Chaudhary A, Baral HS, Bhusal KP, Chaudhary IP, Green RE, Green RE, Alligan TH. Population trends in Himalayan griffon in upper mustang, Nepal, before and after the ban on diclofenac. Bird Conserv int. 2016 Sep;26:286–292. https://doi.org/10.1017/S0959270915000192
  40. Plaza PI, Lambertucci SA. What do we know about lead contamination in wild vultures and condors? A review of decades of research. Sci Total Environ. 2019 Mar;654:409–417. https://doi.org/10.1016/j.scitotenv.2018.11.099
  41. Plaza PI, Martínez-López E, Lambertucci SA. The perfect threat: Pesticides and vultures. Sci Total Environ. 2019 Oct;687:1207– 1218. https://doi.org/10.1016/j.scitotenv.2019.06.160
  42. Plaza PI, Wiemeyer GM, Lambertucci SA. Veterinary pharmaceuticals as a threat to endangered taxa: Mitigation action for vulture conservation. Sci Total Environ. 2022 Apr;817:152884. https://doi.org/10.1016/j.scitotenv.2021.152884
  43. R Core Team. A language and environment for statistical computing. Vienna (Austria): R Foundation for Statistical Computing; 2014 [cited 2025 Apr 28]. Available from https://www.r-project.org
  44. Robinson K, Yang Q, Stewart S, Whitmore MA, Zhang G. Biogeography, succession, and origin of the chicken intestinal mycobiome. Microbiome. 2022 Apr;10(1):55. https://doi.org/10.1186/s40168-022-01252-9
  45. Sakda P, Xiang X, Wu Y, Zhang X, Xu W, Zhou L. Gut fungal communities are influenced by seasonality in captive Baikal teal (Sibirionetta formosa) and common teal (Anas crecca). Animals (Basel). 2023 Sep;13(18):2948. https://doi.org/10.3390/ani13182948
  46. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol. 2009 Dec;75(23):7537– 7541. https://doi.org/10.1128/aem.01541-09
  47. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T. Cytoscape: A software environment for integrated models of biomolecular interaction networks. Genome Res. 2003 Nov;13(11):2498–2504. https://doi.org/10.1101/gr.1239303
  48. Shekarabi A, Qureishy I, Puglisi CH, Dalseth M, Vuong HE. Host-microbe interactions: communication in the microbiota-gut-brain axis. Curr Opin Microbiol. 2024 Aug;80:102494. https://doi.org/10.1016/j.mib.2024.102494
  49. Sherub S, Bohrer G, Wikelski M, Weinzierl R. Behavioural adaptations to flight into thin air. Biol Lett. 2016 Oct;12(10):20160432. https://doi.org/10.1098/rsbl.2016.0432
  50. Sherub S, Fiedler W, Duriez O, Wikelski M. Bio-logging, new technologies to study conservation physiology on the move: a case study on annual survival of Himalayan vultures. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2017 Jul;203(6–7):531–542. https://doi.org/10.1007/s00359-017-1180-x
  51. Sun Y, Liu X, Sun L, Men M, Wang B, Deng L, Zhao L, Han Y, Jong C, Bi Ret al. Microecological insight to fungal structure and key fungal communities regulating nitrogen transformation based on spatial heterogeneity during cow manure composting by multi-angle and multi-aspect analyses. Waste Manag. 2022 Apr;142:132–142. https://doi.org/10.1016/j.wasman.2022.02.013
  52. Tilg H, Zmora N, Adolph TE, Elinav E. The intestinal microbiota fuelling metabolic inflammation. Nat Rev Immunol. 2020 Jan;20(1):40–54. https://doi.org/10.1038/s41577-019-0198-4
  53. Wang Q, Cole JR. Updated RDP taxonomy and RDP Classifier for more accurate taxonomic classification. Microbiol Resour Announc. 2024 Apr;13(4):e0106323. https://doi.org/10.1128/mra.01063-23
  54. Wang Y, Zhai J, Tang B, Dong Y, Sun S, He S, Zhao W, Lancuo Z, Jia Q, Wang W. Metagenomic comparison of gut communities between wild and captive Himalayan griffons. Front Vet Sci. 2024 May;11:1403932. https://doi.org/10.3389/fvets.2024.1403932
  55. Wu H, Wu FT, Zhou QH, Zhao DP. Comparative analysis of gut microbiota in captive and wild oriental white storks: Implications for conservation biology. Front Microbiol. 2021 Mar;12:649466. https://doi.org/10.3389/fmicb.2021.649466
  56. Wu Y, Li Z, Zhao J, Chen Z, Xiang X. Significant differences in intestinal fungal community of hooded cranes along the wintering periods. Front Microbiol. 2022 Sep;13:991998. https://doi.org/10.3389/fmicb.2022.991998
  57. Xiao Y, Xiao G, Liu H, Zhao X, Sun C, Tan X, Sun K, Liu S, Feng J. Captivity causes taxonomic and functional convergence of gut microbial communities in bats. PeerJ. 2019 Apr;7:e6844. https://doi.org/10.7717/peerj.6844
  58. Xie G, Kong X, Kang J, Su N, Fei J, Luo G. Fungal community succession contributes to product maturity during the co-composting of chicken manure and crop residues. Bioresour Technol. 2021 May;328:124845. https://doi.org/10.1016/j.biortech.2021.124845
  59. Xie Y, Xia P, Wang H, Yu H, Giesy JP, Zhang Y, Mora MA, Zhang X. Effects of captivity and artificial breeding on microbiota in feces of the red-crowned crane (Grus japonensis). Sci Rep. 2016 Sep;6:33350. https://doi.org/10.1038/srep33350
  60. Xuan DD, Li YL, Zhang GN, Ding LW, Cao PP, Jia RJ, Zheng YA, Zhou XJ, Pan LY, Hu SK, et al. [Analysis of intestinal microbial diversity in Leopoldamys edwardsi based on illumina sequencing technique] (in Chinese). Zhonghua Yu Fang Yi Xue Za Zhi. 2022 Apr;56(4):512–518. https://doi.org/10.3760/cma.j.cn112150-20210915-00892
  61. Xun W, Liu Y, Li W, Ren Y, Xiong W, Xu Z, Zhang N, Miao Y, Shen Q, Zhang R. Specialized metabolic functions of keystone taxa sustain soil microbiome stability. Microbiome. 2021 Jan;9(1):35. https://doi.org/10.1186/s40168-020-00985-9
  62. Yang S, Gao X, Meng J, Zhang A, Zhou Y, Long M, Li B, Deng W, Jin L, Zhao S, et al. Metagenomic analysis of bacteria, fungi, bacteriophages, and helminths in the gut of giant pandas. Front Microbiol. 2018 Jul;9:1717. https://doi.org/10.3389/fmicb.2018.01717
  63. Yao H, Zhang Z, Wu N, Wang M, Wu Q, Wu H, Zhao D. Comparative analysis of intestinal flora at different overwintering periods in wild relict gulls (Larus relictus): First evidence from Northern China. Frontiers in Microbiomes. 2023 Oct;2:1218281. https://doi.org/10.3389/frmbi.2023.1218281
  64. Ye J, Joseph SD, Ji M, Nielsen S, Mitchell DRG, Donne S, Horvat J, Wang J, Munroe P, Thomas T. Chemolithotrophic processes in the bacterial communities on the surface of mineral-enriched biochars. ISME J. 2017 May;11(5):1087–1101. https://doi.org/10.1038/ismej.2016.187
  65. Zhai J, Wang Y, Tang B, Zheng S, He S, Zhao W, Chen H, Lin J, Li F, Bao Y, et al. Comparative analysis of gut DNA viromes in wild and captive Himalayan vultures. Front Microbiol. 2023 Aug;14:1120838. https://doi.org/10.3389/fmicb.2023.1120838
  66. Zhang J, Shen C, Shang TH, Liu JL. Difference responses of soil fungal communities to cattle and chicken manure composting application. J Appl Microbiol. 2022a Aug;133(2):323–339. https://doi.org/10.1111/jam.15549
  67. Zhang K, Wang X, Gong X, Sui J. Gut microbiome differences in rescued common kestrels (Falco tinnunculus) before and after captivity. Front Microbiol. 2022b Jun;13:858592. https://doi.org/10.3389/fmicb.2022.858592
  68. Zhang Y, He X, Mo X, Wu H, Zhao D. Similarities and differences: species and diet impact gut microbiota of captive pheasants. PeerJ. 2024 Mar;12:e16979.
  69. Zhang Y, Mahidul Islam Masum M, Gao C, Cheng Y, Guan J. Ozone reduces the fruit decay of postharvest winter jujube by altering the microbial community structure on fruit surface. Microbiol Res. 2022c Sep;262:127110. https://doi.org/10.1016/j.micres.2022.127110
  70. Zhou X, Zhang X, Yu J. Gut mycobiome in metabolic diseases: Mechanisms and clinical implication. Biomed J. 2024 Jun;47(3):100625. https://doi.org/10.1016/j.bj.2023.100625
  71. Zou D, Tian S, Zhang T, Zhuoma N, Wu G, Wang M, Dong L, Rossiter SJ, Zhao H. Vulture genomes reveal molecular adaptations underlying obligate scavenging and low levels of genetic diversity. Mol Biol Evol. 2021 Aug;38(9):3649–3663. https://doi.org/10.1093/molbev/msab130
DOI: https://doi.org/10.33073/pjm-2025-033 | Journal eISSN: 2544-4646 | Journal ISSN: 1733-1331
Language: English
Page range: 385 - 400
Submitted on: May 28, 2025
Accepted on: Aug 12, 2025
Published on: Sep 16, 2025
Published by: Polish Society of Microbiologists
In partnership with: Paradigm Publishing Services
Publication frequency: 4 issues per year

© 2025 FENG LI, QUANCHAO CUI, SITONG FAN, HUIWEN LI, WEN WANG, published by Polish Society of Microbiologists
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