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Captivity and Animal Microbiomes: Potential Roles of Microbiota for Influencing Animal Conservation

  • Host Microbe Interactions
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Abstract

During the ongoing biodiversity crisis, captive conservation and breeding programs offer a refuge for species to persist and provide source populations for reintroduction efforts. Unfortunately, captive animals are at a higher disease risk and reintroduction efforts remain largely unsuccessful. One potential factor in these outcomes is the host microbiota which includes a large diversity and abundance of bacteria, fungi, and viruses that play an essential role in host physiology. Relative to wild populations, the generalized pattern of gut and skin microbiomes in captivity are reduced alpha diversity and they exhibit a significant shift in community composition and/or structure which often correlates with various physiological maladies. Many conditions of captivity (antibiotic exposure, altered diet composition, homogenous environment, increased stress, and altered intraspecific interactions) likely lead to changes in the host-associated microbiome. To minimize the problems arising from captivity, efforts can be taken to manipulate microbial diversity and composition to be comparable with wild populations through methods such as increasing dietary diversity, exposure to natural environmental reservoirs, or probiotics. For individuals destined for reintroduction, these strategies can prime the microbiota to buffer against novel pathogens and changes in diet and improve reintroduction success. The microbiome is a critical component of animal physiology and its role in species conservation should be expanded and included in the repertoire of future management practices.

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References

  1. IUCN (2021) The IUCN Red List of Threatened Species. Version 2021-1. https://www.iucnredlist.org

  2. Keulartz J (2015) Captivity for conservation? Zoos at a crossroads. J Agric Environ Ethics 28:335–351. https://doi.org/10.1007/s10806-015-9537-z

    Article  Google Scholar 

  3. Bowkett AE (2009) Recent captive-breeding proposals and the return of the ark concept to global species conservation. Conserv Biol 23:773–776. https://doi.org/10.1111/j.1523-1739.2008.01157.x

    Article  PubMed  Google Scholar 

  4. Harley D, Mawson PR, Olds L, McFadden M, Hogg C (2018) The contribution of captive breeding in zoos to the conservation of Australia’s threatened fauna. In: Garnett S, Woinarski J, Lindenmayer D, Latch P (eds) Recovering Australian Threatened Species: A Book of Hope. CSIRO Publishing, Australia, pp 281–294

    Google Scholar 

  5. Conde DA, Flesness N, Colchero F, Jones OR, Scheuerlein A (2011) An emerging role of zoos to conserve biodiversity. Science 331:1390–1391

    Article  CAS  PubMed  Google Scholar 

  6. Mason GJ (2010) Species differences in responses to captivity: Stress, welfare and the comparative method. Trends Ecol Evol 25:713–721. https://doi.org/10.1016/j.tree.2010.08.011

    Article  PubMed  Google Scholar 

  7. Hartley M (2016) Assessing risk factors for reproductive failure and associated welfare impacts in elephants in European zoos. J Zoo Aquar Res 4:1–12

    Google Scholar 

  8. McFall-Ngai M, Hadfield MG, Bosch TCG, Carey HV, Domazet-Lošo T, Douglas AE, Dubilier N, Eberl G, Fukami T, Gilbert SF, Hentschel U, King N, Kjelleberg S, Knoll AH, Kremer N, Mazmanian SK, Metcalf JL, Nealson K, Pierce NE, Rawls JF, Reid A, Ruby EG, Rumpho M, Sanders JG, Tautz D, Wernegreen JJ (2013) Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci 110:3229–3236. https://doi.org/10.1073/pnas.1218525110

    Article  PubMed  PubMed Central  Google Scholar 

  9. Antwis RE, Edwards KL, Unwin B, Walker SL, Shultz S (2019) Rare gut microbiota associated with breeding success, hormone metabolites and ovarian cycle phase in the critically endangered eastern black rhino. Microbiome 7:27. https://doi.org/10.1186/s40168-019-0639-0

    Article  PubMed  PubMed Central  Google Scholar 

  10. Harris RN, Brucker RM, Walke JB, Becker MH, Schwantes CR, Flaherty DC, Lam BA, Woodhams DC, Briggs CJ, Vredenburg VT (2009) Skin microbes on frogs prevent morbidity and mortality caused by a lethal skin fungus. ISME J 3:818

    Article  CAS  PubMed  Google Scholar 

  11. Yan J, Herzog JW, Tsang K, Brennan CA, Bower MA, Garrett WS, Sartor BR, Aliprantis AO, Charles JF (2016) Gut microbiota induce IGF-1 and promote bone formation and growth. Proc Natl Acad Sci U S A 113:E7554–E7563. https://doi.org/10.1073/pnas.1607235113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Comizzoli P, Power ML, Bornbusch SL, Muletz-Wolz CR (2021) Interactions between reproductive biology and microbiomes in wild animal species. Anim Microbiome 3:87. https://doi.org/10.1186/s42523-021-00156-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Warne RW, Dallas JW (2022) Microbiome mediation of animal life histories via metabolites and insulin-like signalling. Biol Rev. https://doi.org/10.1111/brv.12833

    Article  PubMed  Google Scholar 

  14. Ley RE, Lozupone CA, Hamady M, Knight R, Gordon JI (2008) Worlds within worlds: evolution of the vertebrate gut microbiota. Nat Rev Microbiol 6:776–788. https://doi.org/10.1038/nrmicro1978

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR, Bircher JS, Schlegel ML, Tucker TA, Schrenzel MD, Knight R, Gordon JI (2008) Evolution of mammals and their gut microbes. Science 320:1647–1651. https://doi.org/10.1126/science.1155725

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Cerf-Bensussan N, Gaboriau-Routhiau V (2010) The immune system and the gut microbiota: friends or foes? Nat Rev Immunol 10:735–744. https://doi.org/10.1038/nri2850

    Article  CAS  PubMed  Google Scholar 

  17. DiGiulio DB, Callahan BJ, McMurdie PJ, Costello EK, Lyell DJ, Robaczewska A, Sun CL, Goltsman DS, Wong RJ, Shaw G, Stevenson DK, Holmes SP, Relman DA (2015) Temporal and spatial variation of the human microbiota during pregnancy. Proc Natl Acad Sci U S A 112:11060–11065. https://doi.org/10.1073/pnas.1502875112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Karl JP, Hatch AM, Arcidiacono SM, Pearce SC, Pantoja-Feliciano IG, Doherty LA, Soares JW (2018) Effects of psychological, environmental and physical stressors on the gut microbiota. Front Microbiol 9:2013. https://doi.org/10.3389/fmicb.2018.02013

    Article  PubMed  PubMed Central  Google Scholar 

  19. Harrison XA, Price SJ, Hopkins K, Leung WTM, Sergeant C, Garner TWJ (2019) Diversity-stability dynamics of the amphibian skin microbiome and susceptibility to a lethal viral pathogen. Front Microbiol 10:2883. https://doi.org/10.3389/fmicb.2019.02883

    Article  PubMed  PubMed Central  Google Scholar 

  20. McKenney EA, Koelle K, Dunn RR, Yoder AD (2018) The ecosystem services of animal microbiomes. Mol Ecol 27:2164–2172. https://doi.org/10.1111/mec.14532

    Article  CAS  PubMed  Google Scholar 

  21. Louca S, Polz MF, Mazel F, Albright MBN, Huber JA, O’Connor MI, Ackermann M, Hahn AS, Srivastava DS, Crowe SA, Doebeli M, Parfrey LW (2018) Function and functional redundancy in microbial systems. Nat Ecol Evol 2:936–943. https://doi.org/10.1038/s41559-018-0519-1

    Article  PubMed  Google Scholar 

  22. Hammer TJ, Janzen DH, Hallwachs W, Jaffe SP, Fierer N (2017) Caterpillars lack a resident gut microbiome. Proc Natl Acad Sci U S A 114:9641–9646. https://doi.org/10.1073/pnas.1707186114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Levy M, Kolodziejczyk AA, Thaiss CA, Elinav E (2017) Dysbiosis and the immune system. Nat Rev Immunol 17:219–232. https://doi.org/10.1038/nri.2017.7

    Article  CAS  PubMed  Google Scholar 

  24. Trevelline BK, Fontaine SS, Hartup BK, Kohl KD (2019) Conservation biology needs a microbial renaissance: a call for the consideration of host-associated microbiota in wildlife management practices. Proc Biol Sci 286:20182448. https://doi.org/10.1098/rspb.2018.2448

    Article  PubMed  PubMed Central  Google Scholar 

  25. West AG, Waite DW, Deines P, Bourne DG, Digby A, McKenzie VJ, Taylor MW (2019) The microbiome in threatened species conservation. Biol Conserv 229:85–98. https://doi.org/10.1016/j.biocon.2018.11.016

    Article  Google Scholar 

  26. Bestion E, Jacob S, Zinger L, Di Gesu L, Richard M, White J, Cote J (2017) Climate warming reduces gut microbiota diversity in a vertebrate ectotherm. Nat Ecol Evol 1:161. https://doi.org/10.1038/s41559-017-0161

    Article  PubMed  Google Scholar 

  27. Fontaine SS, Novarro AJ, Kohl KD (2018) Environmental temperature alters the digestive performance and gut microbiota of a terrestrial amphibian. J ExpBiol 221https://doi.org/10.1242/jeb.187559

  28. Neuman C, Hatje E, Zarkasi KZ, Smullen R, Bowman JP, Katouli M (2016) The effect of diet and environmental temperature on the faecal microbiota of farmed Tasmanian Atlantic Salmon (Salmo salar L.). Aquacult Res 47:660–672. https://doi.org/10.1111/are.12522

    Article  CAS  Google Scholar 

  29. Kikuchi Y, Tada A, Musolin DL, Hari N, Hosokawa T, Fujisaki K, Fukatsu T (2016) Collapse of Insect Gut Symbiosis under Simulated Climate Change. MBio 7https://doi.org/10.1128/mBio.01578-16

  30. Horváthová T, Babik W, Kozłowski J, Bauchinger U (2019) Vanishing benefits - The loss of actinobacterial symbionts at elevated temperatures. J Therm Biol 82:222–228. https://doi.org/10.1016/j.jtherbio.2019.04.015

    Article  PubMed  Google Scholar 

  31. Jin Y, Wu S, Zeng Z, Fu Z (2017) Effects of environmental pollutants on gut microbiota. Environ Pollut 222:1–9

    Article  CAS  PubMed  Google Scholar 

  32. Fackelmann G, Sommer S (2019) Microplastics and the gut microbiome: How chronically exposed species may suffer from gut dysbiosis. Mar Pollut Bull 143:193–203. https://doi.org/10.1016/j.marpolbul.2019.04.030

    Article  CAS  PubMed  Google Scholar 

  33. Kohl KD, Cary TL, Karasov WH, Dearing MD (2015) Larval exposure to polychlorinated biphenyl 126 (PCB-126) causes persistent alteration of the amphibian gut microbiota. Environ Toxicol Chem 34:1113–1118. https://doi.org/10.1002/etc.2905

    Article  CAS  PubMed  Google Scholar 

  34. 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 (2013) Habitat degradation impacts black howler monkey (Alouatta pigra) gastrointestinal microbiomes. ISME J 7:1344–1353. https://doi.org/10.1038/ismej.2013.16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Teyssier A, Rouffaer LO, Saleh Hudin N, Strubbe D, Matthysen E, Lens L, White J (2018) Inside the guts of the city: Urban-induced alterations of the gut microbiota in a wild passerine. Sci Total Environ 612:1276–1286. https://doi.org/10.1016/j.scitotenv.2017.09.035

    Article  CAS  PubMed  Google Scholar 

  36. Knutie SA, Chaves JA, Gotanda KM (2019) Human activity can influence the gut microbiota of Darwin’s finches in the Galapagos Islands. Mol Ecol 28:2441–2450. https://doi.org/10.1111/mec.15088

    Article  PubMed  Google Scholar 

  37. Mills JG, Brookes JD, Gellie NJC, Liddicoat C, Lowe AJ, Sydnor HR, Thomas T, Weinstein P, Weyrich LS, Breed MF (2019) Relating Urban Biodiversity to Human Health With the “Holobiont” Concept. Front Microbiol 10:550. https://doi.org/10.3389/fmicb.2019.00550

    Article  PubMed  PubMed Central  Google Scholar 

  38. Harding G, Griffiths RA, Pavajeau L (2016) Developments in amphibian captive breeding and reintroduction programs. Conserv Biol 30:340–349

    Article  PubMed  Google Scholar 

  39. Fischer J, Lindenmayer DB (2000) An assessment of the published results of animal relocations. Biol Conserv 96:1–11

    Article  Google Scholar 

  40. Seddon PJ, Griffiths CJ, Soorae PS, Armstrong DP (2014) Reversing defaunation: Restoring species in a changing world. Science 345:406–412

    Article  CAS  PubMed  Google Scholar 

  41. Clauss M, Wilkins T, Hartley A, Hatt JM (2009) Diet composition, food intake, body condition, and fecal consistency in captive tapirs (Tapirus spp.) in UK collections. Zoo Biol 28:279–291

    Article  CAS  PubMed  Google Scholar 

  42. Erickson GM, Lappin AK, Parker T, Vliet KA (2004) Comparison of bite-force performance between long-term captive and wild American alligators (Alligator mississippiensis). J Zool 262:21–28. https://doi.org/10.1017/s0952836903004400

    Article  Google Scholar 

  43. Goodchild S, Schwitzer C (2008) The problem of obesity in captive lemurs. Int Zoo News 55:353–357

    Google Scholar 

  44. Warwick C, Frye FL, Murphy JB (2013) Health and welfare of captive reptiles. Springer, Netherlands

    Google Scholar 

  45. Ballou JD (1993) Assessing the risks of infectious diseases in captive breeding and reintroduction programs. J Zoo Wildl Med 24:327–335

    Google Scholar 

  46. Cunningham AA (1996) Disease risks of wildlife translocations. Conserv Biol 10:349–353

    Article  Google Scholar 

  47. Ewen JG, Sainsbury AW, Jackson B, Canessa S (2015) Disease risk management in reintroduction. In: Armstrong D, Hayward M, Moro D, Seddon P (eds) Advances in reintroduction biology of Australian and New Zealand fauna. Csiro Publishing, Clayton, Australia, pp 43–57

    Google Scholar 

  48. Viggers K, Lindenmayer D, Spratt D (1993) The importance of disease in reintroduction programmes. Wildl Res 20:687–698

    Article  Google Scholar 

  49. Rideout BA, Gause GE, Benirschke K, Lasley BL (1985) Stress-induced adrenal changes and their relation to reproductive failure in captive nine-banded armadillos (Dasypus novemcinctus). Zoo Biol 4:129–137

    Article  Google Scholar 

  50. Swaisgood RR, Dickman DM, White AM (2006) A captive population in crisis: Testing hypotheses for reproductive failure in captive-born southern white rhinoceros females. Biol Conserv 129:468–476. https://doi.org/10.1016/j.biocon.2005.11.015

    Article  Google Scholar 

  51. Dickens MJ, Bentley GE (2014) Stress, captivity, and reproduction in a wild bird species. Horm Behav 66:685–693. https://doi.org/10.1016/j.yhbeh.2014.09.011

    Article  CAS  PubMed  Google Scholar 

  52. Kedia S, Ghosh TS, Jain S, Desigamani A, Kumar A, Gupta V, Bopanna S, Yadav DP, Goyal S, Makharia G (2021) Gut microbiome diversity in acute severe colitis is distinct from mild to moderate ulcerative colitis. J Gastroenterol Hepatol 36:731–739

    Article  PubMed  Google Scholar 

  53. Kostic AD, Gevers D, Siljander H, Vatanen T, Hyotylainen T, Hamalainen AM, Peet A, Tillmann V, Poho P, Mattila I, Lahdesmaki H, Franzosa EA, Vaarala O, de Goffau M, Harmsen H, Ilonen J, Virtanen SM, Clish CB, Oresic M, Huttenhower C, Knip M, Group DS, Xavier RJ (2015) The dynamics of the human infant gut microbiome in development and in progression toward type 1 diabetes. Cell Host Microbe 17:260–273.https://doi.org/10.1016/j.chom.2015.01.001

  54. Haahtela T (2019) A biodiversity hypothesis. Allergy 74:1445–1456. https://doi.org/10.1111/all.13763

    Article  PubMed  Google Scholar 

  55. Ley RE (2010) Obesity and the human microbiome. Curr Opin Gastroenterol 26:5–11

    Article  PubMed  Google Scholar 

  56. Vallianou N, Stratigou T, Christodoulatos GS, Dalamaga M (2019) Understanding the role of the gut microbiome and microbial metabolites in obesity and obesity-associated metabolic disorders: current evidence and perspectives. Curr Obes Rep 8:317–332

    Article  PubMed  Google Scholar 

  57. Mosca A, Leclerc M, Hugot JP (2016) Gut microbiota diversity and human diseases: should we reintroduce key predators in our ecosystem? Front Microbiol 7:455

    Article  PubMed  PubMed Central  Google Scholar 

  58. Patsch D, van Vliet S, Marcantini LG, Johnson DR (2018) Generality of associations between biological richness and the rates of metabolic processes across microbial communities. Environ Microbiol 20:4356–4368. https://doi.org/10.1111/1462-2920.14352

    Article  CAS  PubMed  Google Scholar 

  59. Tap J, Furet JP, Bensaada M, Philippe C, Roth H, Rabot S, Lakhdari O, Lombard V, Henrissat B, Corthier G, Fontaine E, Dore J, Leclerc M (2015) Gut microbiota richness promotes its stability upon increased dietary fibre intake in healthy adults. Environ Microbiol 17:4954–4964. https://doi.org/10.1111/1462-2920.13006

    Article  CAS  PubMed  Google Scholar 

  60. Alberdi A, Martin G, Aizpurua O (2021) Captivity systematically alters the composition yet not the diversity of vertebrate gut microbiomes. Sci Rep 11:1–10. https://doi.org/10.21203/rs.3.rs-226149/v1

    Article  Google Scholar 

  61. 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 (2017) The effects of captivity on the mammalian gut microbiome. Integr Comp Biol 57:690–704. https://doi.org/10.1093/icb/icx090

    Article  PubMed  PubMed Central  Google Scholar 

  62. Becker MH, Richards-Zawacki CL, Gratwicke B, Belden LK (2014) The effect of captivity on the cutaneous bacterial community of the critically endangered Panamanian golden frog (Atelopus zeteki). Biol Conserv 176:199–206. https://doi.org/10.1016/j.biocon.2014.05.029

    Article  Google Scholar 

  63. Hernández-Gómez O, Briggler JT, Williams RN (2019) Captivity-induced changes in the skin microbial communities of hellbenders (Cryptobranchus alleganiensis). Microb Ecol 77:782–793

    Article  PubMed  Google Scholar 

  64. Ren T, Kahrl AF, Wu M, Cox RM (2016) Does adaptive radiation of a host lineage promote ecological diversity of its bacterial communities? A test using gut microbiota of Anolis lizards. Mol Ecol 25:4793–4804. https://doi.org/10.1111/mec.13796

    Article  CAS  PubMed  Google Scholar 

  65. Gibson KM, Nguyen BN, Neumann LM, Miller M, Buss P, Daniels S, Ahn MJ, Crandall KA, Pukazhenthi B (2019) Gut microbiome differences between wild and captive black rhinoceros - implications for rhino health. Sci Rep 9:7570. https://doi.org/10.1038/s41598-019-43875-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Li Y, Zhang K, Liu Y, Li K, Hu D, Wronski T (2019) Community composition and diversity of intestinal microbiota in captive and reintroduced Przewalski’s horse (Equus ferus przewalskii). Front Microbiol 10https://doi.org/10.3389/fmicb.2019.01821

  67. Edenborough KM, Mu A, Muhldorfer K, Lechner J, Lander A, Bokelmann M, Couacy-Hymann E, Radonic A, Kurth A (2020) Microbiomes in the insectivorous bat species Mops condylurus rapidly converge in captivity. PLoS One 15:e0223629. https://doi.org/10.1371/journal.pone.0223629

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. 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 (2017) Evaluating the impact of domestication and captivity on the horse gut microbiome. Sci Rep 7:15497. https://doi.org/10.1038/s41598-017-15375-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. 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 (2016) Captivity humanizes the primate microbiome. Proc Natl Acad Sci U S A 113:10376–10381. https://doi.org/10.1073/pnas.1521835113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Loudon AH, Woodhams DC, Parfrey LW, Archer H, Knight R, McKenzie V, Harris RN (2014) Microbial community dynamics and effect of environmental microbial reservoirs on red-backed salamanders (Plethodon cinereus). ISME J 8:830–840. https://doi.org/10.1038/ismej.2013.200

    Article  CAS  PubMed  Google Scholar 

  71. Yao R, Xu L, Hu T, Chen H, Qi D, Gu X, Yang X, Yang Z, Zhu L (2019) The “wildness” of the giant panda gut microbiome and its relevance to effective translocation. Glob Ecol Conserv 18:e00644

  72. Wang W, Zheng S, Sharshov K, Sun H, Yang F, Wang X, Li L, Xiao Z (2017) Metagenomic profiling of gut microbial communities in both wild and artificially reared Bar-headed goose (Anser indicus). Microbiologyopen 6https://doi.org/10.1002/mbo3.429

  73. Clayton JB, Al-Ghalith GA, Long HT, Tuan BV, Cabana F, Huang H, Vangay P, Ward T, Minh VV, Tam NA, Dat NT, Travis DA, Murtaugh MP, Covert H, Glander KE, Nadler T, Toddes B, Sha JCM, Singer R, Knights D, Johnson TJ (2018) Associations between nutrition, gut microbiome, and health in a novel nonhuman primate model. Sci Rep 8:11159. https://doi.org/10.1038/s41598-018-29277-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Roth TL, Switzer A, Watanabe-Chailland M, Bik EM, Relman DA, Romick-Rosendale LE, Ollberding NJ (2019) Reduced gut microbiome diversity and metabolome differences in rhinoceros species at risk for iron overload disorder. Front Microbiol 10:2291. https://doi.org/10.3389/fmicb.2019.02291

    Article  PubMed  PubMed Central  Google Scholar 

  75. Menke S, Melzheimer J, Thalwitzer S, Heinrich S, Wachter B, Sommer S (2017) Gut microbiomes of free-ranging and captive Namibian cheetahs: Diversity, putative functions and occurrence of potential pathogens. Mol Ecol 26:5515–5527

    Article  PubMed  Google Scholar 

  76. Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R (2012) Diversity, stability and resilience of the human gut microbiota. Nature 489:220–230. https://doi.org/10.1038/nature11550

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. De Filippo C, Cavalieri D, Di Paola M, Ramazzotti M, Poullet JB, Massart S, Collini S, Pieraccini G, Lionetti P (2010) Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci U S A 107:14691–14696. https://doi.org/10.1073/pnas.1005963107

    Article  PubMed  PubMed Central  Google Scholar 

  78. Chiarello M, Auguet JC, Bettarel Y, Bouvier C, Claverie T, Graham NAJ, Rieuvilleneuve F, Sucre E, Bouvier T, Villeger S (2018) Skin microbiome of coral reef fish is highly variable and driven by host phylogeny and diet. Microbiome 6:147. https://doi.org/10.1186/s40168-018-0530-4

    Article  PubMed  PubMed Central  Google Scholar 

  79. Greene LK, McKenney EA, O’Connell TM, Drea CM (2018) The critical role of dietary foliage in maintaining the gut microbiome and metabolome of folivorous sifakas. Sci Rep 8:14482. https://doi.org/10.1038/s41598-018-32759-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Barraza-Guerrero SI, Meza-Herrera CA, Garcia-De la Pena C, Avila-Rodriguez V, Vaca-Paniagua F, Diaz-Velasquez CE, Pacheco-Torres I, Valdez-Solana MA, Siller-Rodriguez QK, Valenzuela-Nunez LM, Herrera-Salazar JC (2021) Unveiling the fecal microbiota in two captive Mexican wolf (Canis lupus baileyi) populations receiving different type of diets. Biology (Basel) 10https://doi.org/10.3390/biology10070637

  81. Sun B, Xia Y, Garber PA, Amato KR, Gomez A, Xu X, Li W, Huang M, Xia D, Wang X, Li J (2021) Captivity is associated with gut mycobiome composition in Tibetan macaques (Macaca thibetana). Front Microbiol 12:665853. https://doi.org/10.3389/fmicb.2021.665853

    Article  PubMed  PubMed Central  Google Scholar 

  82. Eigeland K (2012) Bacterial community structure in the hindgut of wild and captive dugongs (Dugong dugon). Aquat Mamm 38:402–411. https://doi.org/10.1578/am.38.4.2012.402

    Article  Google Scholar 

  83. Jiang HY, Ma JE, Li J, Zhang XJ, Li LM, He N, Liu HY, Luo SY, Wu ZJ, Han RC, Chen JP (2017) Diets alter the gut microbiome of crocodile lizards. Front Microbiol 8:2073. https://doi.org/10.3389/fmicb.2017.02073

    Article  PubMed  PubMed Central  Google Scholar 

  84. Jia T, Zhao S, Knott K, Li X, Liu Y, Li Y, Chen Y, Yang M, Lu Y, Wu J, Zhang C (2018) The gastrointestinal tract microbiota of northern white-cheeked gibbons (Nomascus leucogenys) varies with age and captive condition. Sci Rep 8:3214. https://doi.org/10.1038/s41598-018-21117-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Kohl KD, Skopec MM, Dearing MD (2014) Captivity results in disparate loss of gut microbial diversity in closely related hosts. Conserv Physiol 2:cou009 https://doi.org/10.1093/conphys/cou009

  86. Oliveira BCM, Murray M, Tseng F, Widmer G (2020) The fecal microbiota of wild and captive raptors. Anim Microbiome 2https://doi.org/10.1186/s42523-020-00035-7

  87. Milton K, McBee RH (1983) Rates of fermentative digestion in the howler monkey, Alouatta palliata (primates: ceboidea). Comp Biochem Physiol A Physiol 74:29–31

    Article  CAS  Google Scholar 

  88. Foley W, Bouskila A, Shkolnik A, Choshniak I (1992) Microbial digestion in the herbivorous lizard Uromastyx aegyptius (Agamidae). J Zool 226:387–398

    Article  Google Scholar 

  89. Heinritz SN, Weiss E, Eklund M, Aumiller T, Louis S, Rings A, Messner S, Camarinha-Silva A, Seifert J, Bischoff SC, Mosenthin R (2016) Intestinal microbiota and microbial metabolites are changed in a pig model fed a high-fat/low-fiber or a low-fat/high-fiber diet. PLoS One 11:e0154329. https://doi.org/10.1371/journal.pone.0154329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. de Andrade Carneiro L, Moreno TB, Fernandes BD, Souza CMM, Bastos TS, Felix AP, da Rocha C (2021) Effects of two dietary fiber levels on nutrient digestibility and intestinal fermentation products in captive brown howler monkeys (Alouatta guariba). Am J Primatol 83:e23238. https://doi.org/10.1002/ajp.23238

    Article  CAS  Google Scholar 

  91. Vester BM, Beloshapka AN, Middelbos IS, Burke SL, Dikeman CL, Simmons LG, Swanson KS (2010) Evaluation of nutrient digestibility and fecal characteristics of exotic felids fed horse- or beef-based diets: use of the domestic cat as a model for exotic felids. Zoo Biol 29:432–448. https://doi.org/10.1002/zoo.20275

    Article  PubMed  Google Scholar 

  92. Kišidayová S, Váradyová Z, Pristaš P, Piknová M, Nigutová K, Petrželková KJ, Profousová I, Schovancová K, Kamler J, Modrý D (2009) Effects of high-and low-fiber diets on fecal fermentation and fecal microbial populations of captive chimpanzees. Am J Primatol 71:548–557

    Article  PubMed  Google Scholar 

  93. Sonnenburg ED, Smits SA, Tikhonov M, Higginbottom SK, Wingreen NS, Sonnenburg JL (2016) Diet-induced extinctions in the gut microbiota compound over generations. Nature 529:212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Kohl KD, Brun A, Magallanes M, Brinkerhoff J, Laspiur A, Acosta JC, Caviedes-Vidal E, Bordenstein SR (2017) Gut microbial ecology of lizards: Insights into diversity in the wild, effects of captivity, variation across gut regions and transmission. Mol Ecol 26:1175–1189. https://doi.org/10.1111/mec.13921

    Article  PubMed  Google Scholar 

  95. Becker A, Harrison SWR, Whitehouse-Tedd G, Budd JA, Whitehouse-Tedd KM (2020) Integrating gut bacterial diversity and captive husbandry to optimize vulture conservation. Front Microbiol 11:1025. https://doi.org/10.3389/fmicb.2020.01025

    Article  PubMed  PubMed Central  Google Scholar 

  96. Bird AK, Prado-Irwin SR, Vredenburg VT, Zink AG (2018) Skin microbiomes of California terrestrial salamanders are influenced by habitat more than host phylogeny. Front Microbiol 9:442. https://doi.org/10.3389/fmicb.2018.00442

    Article  PubMed  PubMed Central  Google Scholar 

  97. Walker DM, Leys JE, Grisnik M, Grajal-Puche A, Murray CM, Allender MC (2019) Variability in snake skin microbial assemblages across spatial scales and disease states. ISME J 13:2209–2222

    Article  PubMed  PubMed Central  Google Scholar 

  98. Sentenac H, Loyau A, Leflaive J, Schmeller DS (2021) The significance of biofilms to human, animal, plant and ecosystem health. Funct Ecol. https://doi.org/10.1111/1365-2435.13947

    Article  Google Scholar 

  99. Avena CV, Parfrey LW, Leff JW, Archer HM, Frick WF, Langwig KE, Kilpatrick AM, Powers KE, Foster JT, McKenzie VJ (2016) Deconstructing the bat skin microbiome: Influences of the host and the environment. Front Microbiol 7:1753. https://doi.org/10.3389/fmicb.2016.01753

    Article  PubMed  PubMed Central  Google Scholar 

  100. Walke JB, Becker MH, Loftus SC, House LL, Cormier G, Jensen RV, Belden LK (2014) Amphibian skin may select for rare environmental microbes. ISME J 8:2207–2217. https://doi.org/10.1038/ismej.2014.77

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Muletz Wolz CR, Yarwood SA, Campbell Grant EH, Fleischer RC, Lips KR (2018) Effects of host species and environment on the skin microbiome of Plethodontid salamanders. J Anim Ecol 87: 341-353.

  102. Lemieux-Labonté V, Tromas N, Shapiro BJ, Lapointe FJ (2016) Environment and host species shape the skin microbiome of captive neotropical bats. PeerJ 4:e2430. https://doi.org/10.7717/peerj.2430

    Article  PubMed  PubMed Central  Google Scholar 

  103. Prest TL, Kimball AK, Kueneman JG, McKenzie VJ (2018) Host-associated bacterial community succession during amphibian development. Mol Ecol 27:1992–2006. https://doi.org/10.1111/mec.14507

    Article  CAS  PubMed  Google Scholar 

  104. Blum WEH, Zechmeister-Boltenstern S, Keiblinger KM (2019) Does soil contribute to the human gut microbiome? Microorganisms 7https://doi.org/10.3390/microorganisms7090287

  105. Tasnim N, Abulizi N, Pither J, Hart MM, Gibson DL (2017) Linking the gut microbial ecosystem with the environment: Does gut health depend on where we live? Front Microbiol 8:1935. https://doi.org/10.3389/fmicb.2017.01935

    Article  PubMed  PubMed Central  Google Scholar 

  106. Mancabelli L, Milani C, Lugli GA, Turroni F, Ferrario C, van Sinderen D, Ventura M (2017) Meta-analysis of the human gut microbiome from urbanized and pre-agricultural populations. Environ Microbiol 19:1379–1390. https://doi.org/10.1111/1462-2920.13692

    Article  PubMed  Google Scholar 

  107. Mills JG, Weinstein P, Gellie NJC, Weyrich LS, Lowe AJ, Breed MF (2017) Urban habitat restoration provides a human health benefit through microbiome rewilding: the Microbiome Rewilding Hypothesis. Restor Ecol 25:866–872. https://doi.org/10.1111/rec.12610

    Article  Google Scholar 

  108. Hanski I, von Hertzen L, Fyhrquist N, Koskinen K, Torppa K, Laatikainen T, Karisola P, Auvinen P, Paulin L, Makela MJ, Vartiainen E, Kosunen TU, Alenius H, Haahtela T (2012) Environmental biodiversity, human microbiota, and allergy are interrelated. Proc Natl Acad Sci U S A 109:8334–8339. https://doi.org/10.1073/pnas.1205624109

    Article  PubMed  PubMed Central  Google Scholar 

  109. Reese AT, Kearney SM (2019) Incorporating functional trade-offs into studies of the gut microbiota. Curr Opin Microbiol 50:20–27. https://doi.org/10.1016/j.mib.2019.09.003

    Article  CAS  PubMed  Google Scholar 

  110. Bataille A, Lee-Cruz L, Tripathi B, Kim H, Waldman B (2016) microbiome variation across amphibian skin regions: Implications for chytridiomycosis mitigation efforts. Microb Ecol 71:221–232. https://doi.org/10.1007/s00248-015-0653-0

    Article  PubMed  Google Scholar 

  111. Nelson TM, Rogers TL, Carlini AR, Brown MV (2013) Diet and phylogeny shape the gut microbiota of Antarctic seals: a comparison of wild and captive animals. Environ Microbiol 15:1132–1145. https://doi.org/10.1111/1462-2920.12022

    Article  CAS  PubMed  Google Scholar 

  112. Zhu L, Zhu W, Zhao T, Chen H, Zhao C, Xu L, Chang Q, Jiang J (2021) Environmental temperatures affect the gastrointestinal microbes of the Chinese giant salamander. Front Microbiol 12:543767. https://doi.org/10.3389/fmicb.2021.543767

    Article  PubMed  PubMed Central  Google Scholar 

  113. Soriano EL, Ramírez DT, Araujo DR, Gómez-Gil B, Castro LI, Sánchez CG (2018) Effect of temperature and dietary lipid proportion on gut microbiota in yellowtail kingfish Seriola lalandi juveniles. Aquaculture 497:269–277. https://doi.org/10.1016/j.aquaculture.2018.07.065

    Article  CAS  Google Scholar 

  114. Wernegreen JJ (2012) Mutualism meltdown in insects: bacteria constrain thermal adaptation. Curr Opin Microbiol 15:255–262. https://doi.org/10.1016/j.mib.2012.02.001

    Article  PubMed  PubMed Central  Google Scholar 

  115. Zhang B, Leonard SP, Li Y, Moran NA (2019) Obligate bacterial endosymbionts limit thermal tolerance of insect host species. Proc Natl Acad Sci U S A 116:24712–24718. https://doi.org/10.1073/pnas.1915307116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Moeller AH, Ivey K, Cornwall MB, Herr K, Rede J, Taylor EN, Gunderson AR (2020) The lizard gut microbiome changes with temperature and is associated with heat tolerance. Appl Environ Microbiol 86:e01181–20

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Chen S, Zheng Y, Zhou Y, Guo W, Tang Q, Rong G, Hu W, Tang J, Luo H (2019) Gut dysbiosis with minimal enteritis induced by high temperature and humidity. Sci Rep 9:18686. https://doi.org/10.1038/s41598-019-55337-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Houtz JL, Sanders JG, Denice A, Moeller AH (2021) Predictable and host-species specific humanization of the gut microbiota in captive primates. Mol Ecol 30:3677–3687. https://doi.org/10.1111/mec.15994

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Nishida AH, Ochman H (2021) Captivity and the co-diversification of great ape microbiomes. Nat Commun 12:5632. https://doi.org/10.1038/s41467-021-25732-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Gogarten JF, Ruhlemann M, Archie E, Tung J, Akoua-Koffi C, Bang C, Deschner T, Muyembe-Tamfun JJ, Robbins MM, Schubert G, Surbeck M, Wittig RM, Zuberbuhler K, Baines JF, Franke A, Leendertz FH, Calvignac-Spencer S (2021) Primate phageomes are structured by superhost phylogeny and environment. Proc Natl Acad Sci U S A 118https://doi.org/10.1073/pnas.2013535118

  121. Tang GS, Liang XX, Yang MY, Wang TT, Chen JP, Du WG, Li H, Sun BJ (2020) Captivity influences gut microbiota in crocodile lizards (Shinisaurus crocodilurus). Front Microbiol 11:550. https://doi.org/10.3389/fmicb.2020.00550

    Article  PubMed  PubMed Central  Google Scholar 

  122. Ley RE, Turnbaugh PJ, Klein S, Gordon JI (2006) Microbial ecology: Human gut microbes associated with obesity. Nature 444:1022

    Article  CAS  PubMed  Google Scholar 

  123. Lax S, Smith DP, Hampton-Marcell J, Owens SM, Handley KM, Scott NM, Gibbons SM, Larsen P, Shogan BD, Weiss S (2014) Longitudinal analysis of microbial interaction between humans and the indoor environment. Science 345:1048–1052

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. 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 (2016) The oral and skin microbiomes of captive Komodo dragons are significantly shared with their habitat. mSystems 1 https://doi.org/10.1128/mSystems.00046-16

  125. Morgan KN, Tromborg CT (2007) Sources of stress in captivity. Appl Anim Behav Sci 102:262–302. https://doi.org/10.1016/j.applanim.2006.05.032

    Article  Google Scholar 

  126. DuRant S, Love AC, Belin B, Tamayo-Sanchez D, Santos Pacheco M, Dickens MJ, Calisi RM (2020) Captivity alters neuroendocrine regulators of stress and reproduction in the hypothalamus in response to acute stress. Gen Comp Endocrinol 295:113519. https://doi.org/10.1016/j.ygcen.2020.113519

    Article  CAS  PubMed  Google Scholar 

  127. Fischer CP, Wright-Lichter J, Romero LM (2018) Chronic stress and the introduction to captivity: How wild house sparrows (Passer domesticus) adjust to laboratory conditions. Gen Comp Endocrinol 259:85–92. https://doi.org/10.1016/j.ygcen.2017.11.007

    Article  CAS  PubMed  Google Scholar 

  128. Love AC, Lovern MB, DuRant SE (2017) Captivity influences immune responses, stress endocrinology, and organ size in house sparrows (Passer domesticus). Gen Comp Endocrinol 252:18–26. https://doi.org/10.1016/j.ygcen.2017.07.014

    Article  CAS  PubMed  Google Scholar 

  129. Romero LM, Wingfield JC (1999) Alterations in hypothalamic–pituitary–adrenal function associated with captivity in Gambel’s white-crowned sparrows (Zonotrichia leucophrys gambelii). Comp Biochem Physiol B Biochem Mol Biol 122:13–20

    Article  CAS  PubMed  Google Scholar 

  130. Wingfield JC, Boonstra R (2013) Ecological processes and the ecology of stress: the impacts of abiotic environmental factors. Funct Ecol 27:37–44. https://doi.org/10.1111/1365-2435.12039

    Article  Google Scholar 

  131. Fischer CP, Romero LM (2019) Chronic captivity stress in wild animals is highly species-specific. Conserv Physiol 7:coz093 https://doi.org/10.1093/conphys/coz093

  132. Stothart MR, Palme R, Newman AEM (2019) It’s what’s on the inside that counts: stress physiology and the bacterial microbiome of a wild urban mammal. Proc Biol Sci 286:20192111. https://doi.org/10.1098/rspb.2019.2111

    Article  PubMed  PubMed Central  Google Scholar 

  133. Azevedo A, Wauters J, Kirschbaum C, Serra R, Rivas A, Jewgenow K (2020) Sex steroids and glucocorticoid ratios in Iberian lynx hair. Conserv Physiol 8:coaa075 https://doi.org/10.1093/conphys/coaa075

  134. Cabezas S, Carrete M, Tella JL, Marchant TA, Bortolotti GR (2013) Differences in acute stress responses between wild-caught and captive-bred birds: A physiological mechanism contributing to current avian invasions? Biol Invasions 15:521–527

    Article  Google Scholar 

  135. Huo R, Zeng B, Zeng L, Cheng K, Li B, Luo Y, Wang H, Zhou C, Fang L, Li W, Niu R, Wei H, Xie P (2017) Microbiota modulate anxiety-like behavior and endocrine abnormalities in hypothalamic-pituitary-adrenal axis. Front Cell Infect Microbiol 7:489. https://doi.org/10.3389/fcimb.2017.00489

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Neuman H, Debelius JW, Knight R, Koren O (2015) Microbial endocrinology: the interplay between the microbiota and the endocrine system. FEMS Microbiol Rev 39:509–521. https://doi.org/10.1093/femsre/fuu010

    Article  PubMed  Google Scholar 

  137. Rooks MG, Garrett WS (2016) Gut microbiota, metabolites and host immunity. Nat Rev Immunol 16:341–352. https://doi.org/10.1038/nri.2016.42

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  138. Stothart MR, Bobbie CB, Schulte-Hostedde AI, Boonstra R, Palme R, Mykytczuk NC, Newman AE (2016) Stress and the microbiome: linking glucocorticoids to bacterial community dynamics in wild red squirrels. Biol Lett 12:20150875. https://doi.org/10.1098/rsbl.2015.0875

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Zhao H, Jiang X, Chu W (2020) Shifts in the gut microbiota of mice in response to dexamethasone administration. Int Microbiol 23:565–573. https://doi.org/10.1007/s10123-020-00129-x

    Article  CAS  PubMed  Google Scholar 

  140. Unsal H, Balkaya M, Unsal C, Biyik H, Basbulbul G, Poyrazoglu E (2008) The short-term effects of different doses of dexamethasone on the numbers of some bacteria in the ileum. Dig Dis Sci 53:1842–1845. https://doi.org/10.1007/s10620-007-0089-6

    Article  CAS  PubMed  Google Scholar 

  141. Hickmott AJ, Boose KJ, Wakefield ML, Brand CM, Snodgrass JJ, Ting N, White FJ (2022) A comparison of fecal glucocorticoid metabolite concentration and gut microbiota diversity in Bonobos (Pan paniscus). bioRxiv.

  142. Noguera JC, Aira M, Perez-Losada M, Dominguez J, Velando A (2018) Glucocorticoids modulate gastrointestinal microbiome in a wild bird. R Soc Open Sci 5:171743. https://doi.org/10.1098/rsos.171743

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  143. Berlow M, Wada H, Derryberry EP (2021) Experimental exposure to noise alters gut microbiota in a captive songbird. Microb Ecol. https://doi.org/10.1007/s00248-021-01924-3

    Article  PubMed  Google Scholar 

  144. Knutie SA, Gabor CR, Kohl KD, Rohr JR (2018) Do host-associated gut microbiota mediate the effect of an herbicide on disease risk in frogs? J Anim Ecol 87:489–499. https://doi.org/10.1111/1365-2656.12769

    Article  PubMed  Google Scholar 

  145. Vlčková K, Shutt-Phillips K, Heistermann M, Pafco B, Petrzelkova KJ, Todd A, Modry D, Nelson KE, Wilson BA, Stumpf RM, White BA, Leigh SR, Gomez A (2018) Impact of stress on the gut microbiome of free-ranging western lowland gorillas. Microbiology 164:40–44. https://doi.org/10.1099/mic.0.000587

    Article  CAS  PubMed  Google Scholar 

  146. O’Mahony SM, Marchesi JR, Scully P, Codling C, Ceolho AM, Quigley EM, Cryan JF, Dinan TG (2009) Early life stress alters behavior, immunity, and microbiota in rats: implications for irritable bowel syndrome and psychiatric illnesses. Biol Psychiatry 65:263–267. https://doi.org/10.1016/j.biopsych.2008.06.026

    Article  PubMed  Google Scholar 

  147. Dahlhausen KE, Doroud L, Firl AJ, Polkinghorne A, Eisen JA (2018) Characterization of shifts of koala (Phascolarctos cinereus) intestinal microbial communities associated with antibiotic treatment. PeerJ 6:e4452. https://doi.org/10.7717/peerj.4452

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  148. Vlčková K, Gomez A, Petrželková KJ, Whittier CA, Todd AF, Yeoman CJ, Nelson KE, Wilson BA, Stumpf RM, Modrý D (2016) Effect of antibiotic treatment on the gastrointestinal microbiome of free-ranging western lowland gorillas (Gorilla g. gorilla). Microb Ecol 72:943–954

    Article  PubMed  Google Scholar 

  149. Nobel YR, Cox LM, Kirigin FF, Bokulich NA, Yamanishi S, Teitler I, Chung J, Sohn J, Barber CM, Goldfarb DS (2015) Metabolic and metagenomic outcomes from early-life pulsed antibiotic treatment. Nat Commun 6:7486

    Article  PubMed  Google Scholar 

  150. Feuerbacher O, Bonar SA, Barrett PJ (2016) Enhancing hatch rate and survival in laboratory-reared hybrid devils hole pupfish through application of antibiotics to eggs and larvae. N Am J Aquacult 79:106–114. https://doi.org/10.1080/15222055.2016.1240123

    Article  Google Scholar 

  151. Theriot CM, Koenigsknecht MJ, Carlson PE Jr, Hatton GE, Nelson AM, Li B, Huffnagle GB, Li JZ, Young VB (2014) Antibiotic-induced shifts in the mouse gut microbiome and metabolome increase susceptibility to Clostridium difficile infection. Nat Commun 5:3114

    Article  PubMed  Google Scholar 

  152. Jin C, Luo T, Zhu Z, Pan Z, Yang J, Wang W, Fu Z, Jin Y (2017) Imazalil exposure induces gut microbiota dysbiosis and hepatic metabolism disorder in zebrafish. Comp Biochem Physiol C Toxicol Pharmacol 202:85–93

    Article  CAS  PubMed  Google Scholar 

  153. Blaser MJ (2016) Antibiotic use and its consequences for the normal microbiome. Science 352:544–545. https://doi.org/10.1126/science.aad9358

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  154. Modi SR, Collins JJ, Relman DA (2014) Antibiotics and the gut microbiota. J Clin Investig 124:4212–4218

    Article  PubMed  PubMed Central  Google Scholar 

  155. Raymann K, Shaffer Z, Moran NA (2017) Antibiotic exposure perturbs the gut microbiota and elevates mortality in honeybees. PLoS Biol 15:e2001861. https://doi.org/10.1371/journal.pbio.2001861

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  156. Thomason CA, Mullen N, Belden LK, May M, Hawley DM (2017) Resident microbiome disruption with antibiotics enhances virulence of a colonizing pathogen. Sci Rep 7:16177

    Article  PubMed  PubMed Central  Google Scholar 

  157. Burdet C, Sayah-Jeanne S, Nguyen TT, Hugon P, Sablier-Gallis F, Saint-Lu N, Corbel T, Ferreira S, Pulse M, Weiss W, Andremont A, Mentre F, de Gunzburg J (2018) Antibiotic-induced dysbiosis predicts mortality in an animal model of Clostridium difficile infection. Antimicrob Agents Chemother 62https://doi.org/10.1128/AAC.00925-18

  158. Holden WM, Hanlon SM, Woodhams DC, Chappell TM, Wells HL, Glisson SM, McKenzie VJ, Knight R, Parris MJ, Rollins-Smith LA (2015) Skin bacteria provide early protection for newly metamorphosed southern leopard frogs (Rana sphenocephala) against the frog-killing fungus, Batrachochytrium dendrobatidis. Biol Conserv 187:91–102. https://doi.org/10.1016/j.biocon.2015.04.007

    Article  Google Scholar 

  159. Klein EY, Van Boeckel TP, Martinez EM, Pant S, Gandra S, Levin SA, Goossens H, Laxminarayan R (2018) Global increase and geographic convergence in antibiotic consumption between 2000 and 2015. Proc Natl Acad Sci U S A 115:E3463–E3470. https://doi.org/10.1073/pnas.1717295115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  160. Van Boeckel TP, Brower C, Gilbert M, Grenfell BT, Levin SA, Robinson TP, Teillant A, Laxminarayan R (2015) Global trends in antimicrobial use in food animals. Proc Natl Acad Sci U S A 112:5649–5654. https://doi.org/10.1073/pnas.1503141112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  161. Joosten P, Ceccarelli D, Odent E, Sarrazin S, Graveland H, Van Gompel L, Battisti A, Caprioli A, Franco A, Wagenaar JA, Mevius D, Dewulf J (2020) Antimicrobial usage and resistance in companion animals: A cross-sectional study in three European countries. Antibiotics (Basel) 9https://doi.org/10.3390/antibiotics9020087

  162. McNally KL, Innis CJ, Kennedy A, Bowen JL (2021) Characterization of oral and cloacal microbial communities in cold-stunned Kemp’s ridley sea turtles (Lepidochelys kempii) during the time course of rehabilitation. PLoS One 16:e0252086. https://doi.org/10.1371/journal.pone.0252086

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  163. Bloodgood JCG, Hernandez SM, Isaiah A, Suchodolski JS, Hoopes LA, Thompson PM, Waltzek TB, Norton TM (2020) The effect of diet on the gastrointestinal microbiome of juvenile rehabilitating green turtles (Chelonia mydas). PLoS One 15:e0227060. https://doi.org/10.1371/journal.pone.0227060

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  164. Zaneveld JR, McMinds R, Vega Thurber R (2017) Stress and stability: Applying the Anna Karenina principle to animal microbiomes. Nat Microbiol 2:17121. https://doi.org/10.1038/nmicrobiol.2017.121

    Article  CAS  PubMed  Google Scholar 

  165. Allen HK, Donato J, Wang HH, Cloud-Hansen KA, Davies J, Handelsman J (2010) Call of the wild: antibiotic resistance genes in natural environments. Nat Rev Microbiol 8:251–259. https://doi.org/10.1038/nrmicro2312

    Article  CAS  PubMed  Google Scholar 

  166. Carter DL, Docherty KM, Gill SA, Baker K, Teachout J, Vonhof MJ (2018) Antibiotic resistant bacteria are widespread in songbirds across rural and urban environments. Sci Total Environ 627:1234–1241

    Article  CAS  PubMed  Google Scholar 

  167. Delport TC, Harcourt RG, Beaumont LJ, Webster KN, Power ML (2015) Molecular detection of antibiotic-resistance determinants in Escherichia coli isolated from the endangered Australian sea lion (Neophoca Cinerea). J Wildl Dis 51:555–563. https://doi.org/10.7589/2014-08-200

    Article  CAS  PubMed  Google Scholar 

  168. Power ML, Emery S, Gillings MR (2013) Into the wild: dissemination of antibiotic resistance determinants via a species recovery program. PLoS One 8:e63017. https://doi.org/10.1371/journal.pone.0063017

    Article  PubMed  PubMed Central  Google Scholar 

  169. Stoddard RA, Atwill ER, Conrad PA, Byrne BA, Jang S, Lawrence J, McCowan B, Gulland FM (2009) The effect of rehabilitation of northern elephant seals (Mirounga angustirostris) on antimicrobial resistance of commensal Escherichia coli. Vet Microbiol 133:264–271. https://doi.org/10.1016/j.vetmic.2008.07.022

    Article  CAS  PubMed  Google Scholar 

  170. Ahasan MS, Picard J, Elliott L, Kinobe R, Owens L, Ariel E (2017) Evidence of antibiotic resistance in Enterobacteriales isolated from green sea turtles, Chelonia mydas on the Great Barrier Reef. Mar Pollut Bull 120:18–27

    Article  CAS  PubMed  Google Scholar 

  171. Poole K (2002) Mechanisms of bacterial biocide and antibiotic resistance. J Appl Microbiol 92:55S-64S

    Article  PubMed  Google Scholar 

  172. Russell AD (2003) Biocide use and antibiotic resistance: the relevance of laboratory findings to clinical and environmental situations. Lancet Infect Dis 3:794–803. https://doi.org/10.1016/s1473-3099(03)00833-8

    Article  CAS  PubMed  Google Scholar 

  173. Romero JL, Grande Burgos MJ, Perez-Pulido R, Galvez A, Lucas R (2017) Resistance to antibiotics, biocides, preservatives and metals in bacteria isolated from seafoods: Co-selection of strains resistant or tolerant to different classes of compounds. Front Microbiol 8:1650. https://doi.org/10.3389/fmicb.2017.01650

    Article  PubMed  PubMed Central  Google Scholar 

  174. Pal C, Bengtsson-Palme J, Kristiansson E, Larsson DG (2016) The structure and diversity of human, animal and environmental resistomes. Microbiome 4:54. https://doi.org/10.1186/s40168-016-0199-5

    Article  PubMed  PubMed Central  Google Scholar 

  175. Donaghy JA, Jagadeesan B, Goodburn K, Grunwald L, Jensen ON, Jespers AD, Kanagachandran K, Lafforgue H, Seefelder W, Quentin MC (2019) Relationship of sanitizers, disinfectants, and cleaning agents with antimicrobial resistance. J Food Prot 82:889–902. https://doi.org/10.4315/0362-028X.JFP-18-373

    Article  CAS  PubMed  Google Scholar 

  176. Council NR (2011) Guide for the care and use of laboratory animals, 8th edn. The National Academies Press, Washington, DC

    Google Scholar 

  177. Adu-Oppong B, Gasparrini AJ, Dantas G (2017) Genomic and functional techniques to mine the microbiome for novel antimicrobials and antimicrobial resistance genes. Ann N Y Acad Sci 1388:42–58. https://doi.org/10.1111/nyas.13257

    Article  PubMed  Google Scholar 

  178. Walker SF, Bosch J, James TY, Litvintseva AP, Valls JAO, Piña S, García G, Rosa GA, Cunningham AA, Hole S (2008) Invasive pathogens threaten species recovery programs. Curr Biol 18:R853–R854

    Article  CAS  PubMed  Google Scholar 

  179. Troyer K (1984) Microbes, herbivory and the evolution of social behavior. J Theor Biol 106:157–169

    Article  Google Scholar 

  180. Funkhouser LJ, Bordenstein SR (2013) Mom knows best: the universality of maternal microbial transmission. PLoS Biol 11:e1001631. https://doi.org/10.1371/journal.pbio.1001631

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  181. Cox LM, Yamanishi S, Sohn J, Alekseyenko AV, Leung JM, Cho I, Kim SG, Li H, Gao Z, Mahana D, Zarate Rodriguez JG, Rogers AB, Robine N, Loke P, Blaser MJ (2014) Altering the intestinal microbiota during a critical developmental window has lasting metabolic consequences. Cell 158:705–721. https://doi.org/10.1016/j.cell.2014.05.052

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  182. Wang S, Ryan CA, Boyaval P, Dempsey EM, Ross RP, Stanton C (2020) Maternal vertical transmission affecting early-life microbiota development. Trends Microbiol 28:28–45. https://doi.org/10.1016/j.tim.2019.07.010

    Article  CAS  PubMed  Google Scholar 

  183. Baniel A, Petrullo L, Mercer A, Reitsema L, Sams S, Beehner JC, Bergman TJ, Snyder-Mackler N, Lu A (2021) Maternal effects on early-life gut microbiome maturation in a wild nonhuman primate. bioRxiv.

  184. Walke JB, Harris RN, Reinert LK, Rollins-Smith LA, Woodhams DC (2011) Social immunity in amphibians: Evidence for vertical transmission of innate defenses. Biotropica 43:396–400

    Article  Google Scholar 

  185. Warne RW, Kirschman L, Zeglin L (2017) Manipulation of gut microbiota reveals shifting community structure shaped by host developmental windows in amphibian larvae. Integr Comp Biol 57:786–794. https://doi.org/10.1093/icb/icx100

    Article  PubMed  Google Scholar 

  186. Köhler G (2005) Incubation of reptile eggs. Krieger Publishing Company, Malabar

    Google Scholar 

  187. Mohapatra RK, Sahu SK, Das JK, Paul S (2019) Hand rearing of wild mammals in captivity. Nandankanan Biological Park, Forest and Environment Department, Government of Odisha

  188. Troyer K (1984) Behavioral acquisition of the hindgut fermentation system by hatchling Iguana iguana. Behav Ecol Sociobiol 14:189–193

    Article  Google Scholar 

  189. Knol J, Scholtens P, Kafka C, Steenbakkers J, Gro S, Helm K, Klarczyk M, Schöpfer H, Böckler H-M, Wells J (2005) Colon microflora in infants fed formula with galacto-and fructo-oligosaccharides: more like breast-fed infants. J Pediatr Gastroenterol Nutr 40:36–42

    Article  CAS  PubMed  Google Scholar 

  190. Gritz EC, Bhandari V (2015) The human neonatal gut microbiome: A brief review. Front Pediatr 3:17. https://doi.org/10.3389/fped.2015.00017

    Article  PubMed  PubMed Central  Google Scholar 

  191. Antwis RE, Haworth RL, Engelmoer DJ, Ogilvy V, Fidgett AL, Preziosi RF (2014) Ex situ diet influences the bacterial community associated with the skin of red-eyed tree frogs (Agalychnis callidryas). PLoS One 9:e85563. https://doi.org/10.1371/journal.pone.0085563

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  192. Pusceddu MM, El Aidy S, Crispie F, O’Sullivan O, Cotter P, Stanton C, Kelly P, Cryan JF, Dinan TG (2015) N-3 polyunsaturated fatty acids (PUFAs) Reverse the Impact of Early-Life Stress on the Gut Microbiota. PLoS One 10:e0139721. https://doi.org/10.1371/journal.pone.0139721

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  193. Webster TMU, Rodriguez-Barreto D, Castaldo G, Gough P, Consuegra S, de Leaniz CG (2019) Environmental plasticity and colonisation history in the Atlantic salmon microbiome: a translocation experiment. bioRxiv: 564104.

  194. van Leeuwen P, Mykytczuk N, Mastromonaco GF, Schulte-Hostedde AI (2020) Effects of captivity, diet, and relocation on the gut bacterial communities of white-footed mice. Ecology and Evolution 10:4677–4690

    Article  PubMed  PubMed Central  Google Scholar 

  195. Ni Q, Zhang C, Li D, Xu H, Yao Y, Zhang M, Fan X, Zeng B, Yang D, Xie M (2021) Effects of dietary alteration on the gut microbiome and metabolome of the rescued Bengal slow loris. Front Microbiol 12:650991. https://doi.org/10.3389/fmicb.2021.650991

    Article  PubMed  PubMed Central  Google Scholar 

  196. Martínez-Mota R, Kohl KD, Orr TJ, Dearing MD (2020) Natural diets promote retention of the native gut microbiota in captive rodents. ISME J 14:67–78

    Article  PubMed  Google Scholar 

  197. Arrieta MC, Stiemsma LT, Amenyogbe N, Brown EM, Finlay B (2014) The intestinal microbiome in early life: health and disease. Front Immunol 5:427. https://doi.org/10.3389/fimmu.2014.00427

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  198. Bledsoe JW, Peterson BC, Swanson KS, Small BC (2016) Ontogenetic characterization of the intestinal microbiota of channel catfish through 16S rRNA gene sequencing reveals insights on temporal shifts and the influence of environmental microbes. PLoS One 11:e0166379. https://doi.org/10.1371/journal.pone.0166379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  199. Capone KA, Dowd SE, Stamatas GN, Nikolovski J (2011) Diversity of the human skin microbiome early in life. J Invest Dermatol 131:2026–2032. https://doi.org/10.1038/jid.2011.168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  200. Kirschman LJ, Khadjinova A, Ireland K, Milligan-Myhre KC (2020) Early life disruption of the microbiota affects organ development and cytokine gene expression in threespine stickleback. Integr Comp Biol. https://doi.org/10.1093/icb/icaa136

    Article  PubMed  Google Scholar 

  201. Videvall E, Song SJ, Bensch HM, Strandh M, Engelbrecht A, Serfontein N, Hellgren O, Olivier A, Cloete S, Knight R, Cornwallis CK (2019) The development of gut microbiota in ostriches and its association with juvenile growth. Mol Ecol 2019:2653–2667. https://doi.org/10.1101/270017

    Article  CAS  Google Scholar 

  202. Warne RW, Kirschman L, Zeglin L (2019) Manipulation of gut microbiota during critical developmental windows affects host physiological performance and disease susceptibility across ontogeny. J Anim Ecol 88:845–856. https://doi.org/10.1111/1365-2656.12973

    Article  PubMed  Google Scholar 

  203. Ballou AL, Ali RA, Mendoza MA, Ellis JC, Hassan HM, Croom WJ, Koci MD (2016) Development of the Chick Microbiome: How Early Exposure Influences Future Microbial Diversity. Front Vet Sci 3:2. https://doi.org/10.3389/fvets.2016.00002

    Article  PubMed  PubMed Central  Google Scholar 

  204. McKenzie VJ, Bowers RM, Fierer N, Knight R, Lauber CL (2012) Co-habiting amphibian species harbor unique skin bacterial communities in wild populations. ISME J 6:588–596. https://doi.org/10.1038/ismej.2011.129

    Article  CAS  PubMed  Google Scholar 

  205. Hernandez-Gomez O, Hoverman JT, Williams RN (2017) Cutaneous microbial community variation across populations of eastern hellbenders (Cryptobranchus alleganiensis alleganiensis). Front Microbiol 8:1379. https://doi.org/10.3389/fmicb.2017.01379

    Article  PubMed  PubMed Central  Google Scholar 

  206. Kueneman JG, Parfrey LW, Woodhams DC, Archer HM, Knight R, McKenzie VJ (2014) The amphibian skin-associated microbiome across species, space and life history stages. Mol Ecol 23:1238–1250. https://doi.org/10.1111/mec.12510

    Article  PubMed  Google Scholar 

  207. Sanchez E, Bletz MC, Duntsch L, Bhuju S, Geffers R, Jarek M, Dohrmann AB, Tebbe CC, Steinfartz S, Vences M (2017) Cutaneous bacterial communities of a poisonous salamander: A perspective from life stages, body parts and environmental conditions. Microb Ecol 73:455–465. https://doi.org/10.1007/s00248-016-0863-0

    Article  CAS  PubMed  Google Scholar 

  208. Stuart SN, Chanson JS, Cox NA, Young BE, Rodrigues AS, Fischman DL, Waller RW (2004) Status and trends of amphibian declines and extinctions worldwide. Science 306:1783–1786. https://doi.org/10.1126/science.1103538

    Article  CAS  PubMed  Google Scholar 

  209. Lam BA, Walke JB, Vredenburg VT, Harris RN (2010) Proportion of individuals with anti-Batrachochytrium dendrobatidis skin bacteria is associated with population persistence in the frog Rana muscosa. Biol Conserv 143:529–531. https://doi.org/10.1016/j.biocon.2009.11.015

    Article  Google Scholar 

  210. Becker MH, Brucker RM, Schwantes CR, Harris RN, Minbiole KP (2009) The bacterially produced metabolite violacein is associated with survival of amphibians infected with a lethal fungus. Appl Environ Microbiol 75:6635–6638. https://doi.org/10.1128/AEM.01294-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  211. Jiménez RR, Sommer S (2016) The amphibian microbiome: natural range of variation, pathogenic dysbiosis, and role in conservation. Biodivers Conserv 26:763–786. https://doi.org/10.1007/s10531-016-1272-x

    Article  Google Scholar 

  212. Walke JB, Belden LK (2016) Harnessing the microbiome to prevent fungal infections: Lessons from amphibians. PLoS Pathog 12:e1005796. https://doi.org/10.1371/journal.ppat.1005796

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  213. Kenison EK, Hernandez-Gomez O, Williams RN (2020) A novel bioaugmentation technique effectively increases the skin-associated microbial diversity of captive eastern hellbenders. Conserv Physiol 8:coaa040 https://doi.org/10.1093/conphys/coaa040

  214. Muletz CR, Myers JM, Domangue RJ, Herrick JB, Harris RN (2012) Soil bioaugmentation with amphibian cutaneous bacteria protects amphibian hosts from infection by Batrachochytrium dendrobatidis. Biol Conserv 152:119–126. https://doi.org/10.1016/j.biocon.2012.03.022

    Article  Google Scholar 

  215. Schmidt E, Mykytczuk N, Schulte-Hostedde AI (2019) Effects of the captive and wild environment on diversity of the gut microbiome of deer mice (Peromyscus maniculatus). ISME J 13:1293–1305. https://doi.org/10.1038/s41396-019-0345-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  216. Yeung F, Chen YH, Lin JD, Leung JM, McCauley C, Devlin JC, Hansen C, Cronkite A, Stephens Z, Drake-Dunn C, Fulmer Y, Shopsin B, Ruggles KV, Round JL, Loke P, Graham AL, Cadwell K (2020) Altered immunity of laboratory mice in the natural environment is associated with fungal colonization. Cell Host Microbe 27(809–822):e806. https://doi.org/10.1016/j.chom.2020.02.015

    Article  CAS  Google Scholar 

  217. Greene LK, Bornbusch SL, McKenney EA, Harris RL, Gorvetzian SR, Yoder AD, Drea CM (2019) The importance of scale in comparative microbiome research: New insights from the gut and glands of captive and wild lemurs. Am J Primatol 81:e22974

  218. Chong R, Grueber CE, Fox S, Wise P, Barrs VR, Hogg CJ, Belov K (2019) Looking like the locals - gut microbiome changes post-release in an endangered species. Anim Microbiome 1https://doi.org/10.1186/s42523-019-0012-4

  219. George Kerry R, Patra JK, Gouda S, Park Y, Shin HS, Das G (2018) Benefaction of probiotics for human health: A review. J Food Drug Anal 26:927–939. https://doi.org/10.1016/j.jfda.2018.01.002

    Article  CAS  Google Scholar 

  220. Suez J, Zmora N, Segal E, Elinav E (2019) The pros, cons, and many unknowns of probiotics. Nat Med 25:716–729. https://doi.org/10.1038/s41591-019-0439-x

    Article  CAS  PubMed  Google Scholar 

  221. Gatesoupe FJ (1999) The use of probiotics in aquaculture. Aquaculture 180:147–165

    Article  Google Scholar 

  222. Schmidt V, Gomez-Chiarri M, Roy C, Smith K, Amaral-Zettler L (2017) Subtle microbiome manipulation using probiotics reduces antibiotic-associated mortality in fish. Msystems 2:e00133-00117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  223. Pedroso AA, Batal AB, Lee MD (2015) Effect of in ovo administration of an adult-derived microbiota on establishment of the intestinal microbiome in chickens. Am J Vet Res 77:514–526. https://doi.org/10.2460/ajvr.77.5.514

    Article  Google Scholar 

  224. Collins JW, La Ragione RM, Woodward MJ, Searle LE (2009) Application of prebiotics and probiotics in livestock. In: Charalampopoulos D, Rastall RA (eds) Prebiotics and probiotics science and technology. Springer-Verlag, New York, pp 1123–1192

    Chapter  Google Scholar 

  225. McKenzie VJ, Kueneman JG, Harris RN (2018) Probiotics as a tool for disease mitigation in wildlife: insights from food production and medicine. Ann N Y Acad Sci 1429:18–30. https://doi.org/10.1111/nyas.13617

    Article  PubMed  Google Scholar 

  226. Jin Song S, Woodhams DC, Martino C, Allaband C, Mu A, Javorschi-Miller-Montgomery S, Suchodolski JS, Knight R (2019) Engineering the microbiome for animal health and conservation. Exp Biol Med 244:494–504

    Article  CAS  Google Scholar 

  227. Davis DJ, Doerr HM, Grzelak AK, Busi SB, Jasarevic E, Ericsson AC, Bryda EC (2016) Lactobacillus plantarum attenuates anxiety-related behavior and protects against stress-induced dysbiosis in adult zebrafish. Sci Rep 6:33726. https://doi.org/10.1038/srep33726

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  228. Hoyt JR, Kilpatrick AM, Langwig KE (2021) Ecology and impacts of white-nose syndrome on bats. Nat Rev Microbiol 19:196–210. https://doi.org/10.1038/s41579-020-00493-5

    Article  CAS  PubMed  Google Scholar 

  229. Fisher MC, Garner TW (2020) Chytrid fungi and global amphibian declines. Nat Rev Microbiol 18:332–343

    Article  CAS  PubMed  Google Scholar 

  230. Lorch JM, Knowles S, Lankton JS, Michell K, Edwards JL, Kapfer JM, Staffen RA, Wild ER, Schmidt KZ, Ballmann AE, Blodgett D, Farrell TM, Glorioso BM, Last LA, Price SJ, Schuler KL, Smith CE, Wellehan JF, Jr., Blehert DS (2016) Snake fungal disease: an emerging threat to wild snakes. Philos Trans R Soc Lond B Biol Sci 371https://doi.org/10.1098/rstb.2015.0457

  231. Bletz MC, Loudon AH, Becker MH, Bell SC, Woodhams DC, Minbiole KP, Harris RN (2013) Mitigating amphibian chytridiomycosis with bioaugmentation: characteristics of effective probiotics and strategies for their selection and use. Ecol Lett 16:807–820. https://doi.org/10.1111/ele.12099

    Article  PubMed  Google Scholar 

  232. Hill AJ, Leys JE, Bryan D, Erdman FM, Malone KS, Russell GN, Applegate RD, Fenton H, Niedringhaus K, Miller AN, Allender MC, Walker DM (2018) Common Cutaneous Bacteria Isolated from Snakes Inhibit Growth of Ophidiomyces ophiodiicola. Ecohealth 15:109–120. https://doi.org/10.1007/s10393-017-1289-y

    Article  PubMed  Google Scholar 

  233. Cheng TL, Mayberry H, McGuire LP, Hoyt JR, Langwig KE, Nguyen H, Parise KL, Foster JT, Willis CKR, Kilpatrick AM, Frick WF (2017) Efficacy of a probiotic bacterium to treat bats affected by the disease white-nose syndrome. J Appl Ecol 54:701–708. https://doi.org/10.1111/1365-2664.12757

    Article  Google Scholar 

  234. Kearns PJ, Fischer S, Fernandez-Beaskoetxea S, Gabor CR, Bosch J, Bowen JL, Tlusty MF, Woodhams DC (2017) Fight fungi with fungi: antifungal properties of the amphibian mycobiome. Front Microbiol 8:2494. https://doi.org/10.3389/fmicb.2017.02494

    Article  PubMed  PubMed Central  Google Scholar 

  235. Rawski M, Kieronczyk B, Dlugosz J, Swiatkiewicz S, Jozefiak D (2016) Dietary probiotics affect gastrointestinal microbiota, histological structure and shell mineralization in turtles. PLoS One 11:e0147859https://doi.org/10.1371/journal.pone.0147859

  236. Stanley D, Hughes RJ, Geier MS, Moore RJ (2016) Bacteria within the gastrointestinal tract microbiota correlated with improved growth and feed conversion: challenges presented for the identification of performance enhancing probiotic bacteria. Front Microbiol 7:187

    Article  PubMed  PubMed Central  Google Scholar 

  237. Mohapatra S, Chakraborty T, Prusty A, Das P, Paniprasad K, Mohanta K (2012) Use of different microbial probiotics in the diet of rohu, Labeo rohita fingerlings: Effects on growth, nutrient digestibility and retention, digestive enzyme activities and intestinal microflora. Aquac Nutr 18:1–11

    Article  CAS  Google Scholar 

  238. Yan J, Charles JF (2018) Gut Microbiota and IGF-1. Calcif Tissue Int 102:406–414. https://doi.org/10.1007/s00223-018-0395-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  239. Poinsot P, Schwarzer M, Peretti N, Leulier F (2018) The emerging connections between IGF1, the intestinal microbiome, Lactobacillus strains and bone growth. J Mol Endocrinol 61:T103–T113. https://doi.org/10.1530/JME-17-0292

    Article  CAS  PubMed  Google Scholar 

  240. Carnevali O, de Vivo L, Sulpizio R, Gioacchini G, Olivotto I, Silvi S, Cresci A (2006) Growth improvement by probiotic in European sea bass juveniles (Dicentrarchus labrax, L.), with particular attention to IGF-1, myostatin and cortisol gene expression. Aquaculture 258:430–438. https://doi.org/10.1016/j.aquaculture.2006.04.025

    Article  CAS  Google Scholar 

  241. Krawczyk B, Wityk P, Galecka M, Michalik M (2021) The many faces of Enterococcus spp.-commensal, probiotic and opportunistic pathogen. Microorganisms 9 https://doi.org/10.3390/microorganisms9091900

  242. Kothari D, Patel S, Kim SK (2019) Probiotic supplements might not be universally-effective and safe: A review. Biomed Pharmacother 111:537–547. https://doi.org/10.1016/j.biopha.2018.12.104

    Article  CAS  PubMed  Google Scholar 

  243. Sharifuzzaman S, Austin B (2017) Probiotics for disease control in aquaculture. In: Austin B, Newaj-Fyzul A (eds) Diagnosis and control of diseases of fish and shellfish. John Wiley & Sons, pp 189–222

    Chapter  Google Scholar 

  244. Rebollar EA, Martínez-Ugalde E, Orta AH (2020) The amphibian skin microbiome and its protective role against chytridiomycosis. Herpetologica 76https://doi.org/10.1655/0018-0831-76.2.167

  245. Bojanova DP, Bordenstein SR (2016) Fecal transplants: what is being transferred? PLoS biology 14:e1002503

  246. Borody TJ, Paramsothy S, Agrawal G (2013) Fecal microbiota transplantation: indications, methods, evidence, and future directions. Curr Gastroenterol Rep 15:337. https://doi.org/10.1007/s11894-013-0337-1

    Article  PubMed  PubMed Central  Google Scholar 

  247. Biliński J, Grzesiowski P, Sorensen N, Mądry K, Muszynski J, Robak K, Wróblewska M, Dzieciątkowski T, Dulny G, Dwilewicz-Trojaczek J, Wiktor-Jedrzejczak W, Basak GW (2017) Fecal microbiota transplantation in patients with blood disorders inhibits gut colonization with antibiotic-resistant bacteria: Results of a prospective, single-center study. Clin Infect Dis 65:364–370. https://doi.org/10.1093/cid/cix252

    Article  CAS  PubMed  Google Scholar 

  248. Leung V, Vincent C, Edens TJ, Miller M, Manges AR (2018) Antimicrobial resistance gene acquisition and depletion following fecal microbiota transplantation for recurrent Clostridium difficile infection. Clin Infect Dis 66:456–457. https://doi.org/10.1093/cid/cix821

    Article  CAS  PubMed  Google Scholar 

  249. Ekmekciu I, von Klitzing E, Fiebiger U, Escher U, Neumann C, Bacher P, Scheffold A, Kuhl AA, Bereswill S, Heimesaat MM (2017) Immune responses to broad-spectrum antibiotic treatment and fecal microbiota transplantation in mice. Front Immunol 8:397. https://doi.org/10.3389/fimmu.2017.00397

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  250. Hensley-McBain T, Zevin AS, Manuzak J, Smith E, Gile J, Miller C, Agricola B, Katze M, Reeves RK, Kraft CS, Langevin S, Klatt NR (2016) Effects of fecal microbial transplantation on microbiome and immunity in simian immunodeficiency virus-infected macaques. J Virol 90:4981–4989. https://doi.org/10.1128/JVI.00099-16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  251. Waite DW, Deines P, Taylor MW (2013) Quantifying the impact of storage procedures for faecal bacteriotherapy in the critically endangered New Zealand parrot, the kakapo (Strigops habroptilus). Zoo Biol 32:620–625. https://doi.org/10.1002/zoo.21098

    Article  PubMed  Google Scholar 

  252. Blyton MDJ, Soo RM, Whisson D, Marsh KJ, Pascoe J, Le Pla M, Foley W, Hugenholtz P, Moore BD (2019) Faecal inoculations alter the gastrointestinal microbiome and allow dietary expansion in a wild specialist herbivore, the koala. Animal Microbiome 1https://doi.org/10.1186/s42523-019-0008-0

  253. Miller AW, Oakeson KF, Dale C, Dearing MD (2016) Microbial community transplant results in increased and long-term oxalate degradation. Microb Ecol 72:470–478. https://doi.org/10.1007/s00248-016-0800-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  254. Stapleton TE, Kohl KD, Dearing MD (2022) Plant secondary compound-and antibiotic-induced community disturbances improve the establishment of foreign gut microbiota. FEMS Microbiol Ecol 98:fiac005. https://doi.org/10.1093/femsec/fiac005

  255. Dickens MJ, Delehanty DJ, Michael Romero L (2010) Stress: An inevitable component of animal translocation. Biol Conserv 143:1329–1341. https://doi.org/10.1016/j.biocon.2010.02.032

    Article  Google Scholar 

  256. MacLeod KJ, Kohl KD, Trevelline BK, Langkilde T (2022) Context-dependent effects of glucocorticoids on the lizard gut microbiome. Mol Ecol 31:185–196. https://doi.org/10.1111/mec.16229

    Article  CAS  PubMed  Google Scholar 

  257. Aguilar-Cucurachi MA, Dias PA, Rangel-Negrin A, Chavira R, Boeck L, Canales-Espinosa D (2010) Preliminary evidence of accumulation of stress during translocation in mantled howlers. Am J Primatol 72:805–810. https://doi.org/10.1002/ajp.20841

    Article  PubMed  Google Scholar 

  258. Batson WG, Gordon IJ, Fletcher DB, Portas TJ, Manning AD (2017) The effect of pre-release captivity on the stress physiology of a reintroduced population of wild eastern bettongs. J Zool 303:311–319. https://doi.org/10.1111/jzo.12494

    Article  Google Scholar 

  259. Yang H, Leng X, Du H, Luo J, Wu J, Wei Q (2020) Adjusting the prerelease gut microbial community by diet training to improve the postrelease fitness of captive-bred Acipenser dabryanus. Front Microbiol 11:488. https://doi.org/10.3389/fmicb.2020.00488

    Article  PubMed  PubMed Central  Google Scholar 

  260. Quiroga-Gonzalez C, Cardenas LAC, Ramirez M, Reyes A, Gonzalez C, Stevenson PR (2021) Monitoring the variation in the gut microbiota of captive woolly monkeys related to changes in diet during a reintroduction process. Sci Rep 11:6522. https://doi.org/10.1038/s41598-021-85990-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  261. Eliades SJ, Brown JC, Colston TJ, Fisher RN, Niukula JB, Gray K, Vadada J, Rasalato S, Siler CD (2021) Gut microbial ecology of the Critically Endangered Fijian crested iguana (Brachylophus vitiensis): Effects of captivity status and host reintroduction on endogenous microbiomes. Ecol Evol 11:4731–4743. https://doi.org/10.1002/ece3.7373

    Article  PubMed  PubMed Central  Google Scholar 

  262. Le Bastard Q, Ward T, Sidiropoulos D, Hillmann BM, Chun CL, Sadowsky MJ, Knights D, Montassier E (2018) Fecal microbiota transplantation reverses antibiotic and chemotherapy-induced gut dysbiosis in mice. Sci Rep 8:6219. https://doi.org/10.1038/s41598-018-24342-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  263. Reardon S (2018) Faecal transplants could help preserve vulnerable species. Nature 558:173–175

    Article  CAS  PubMed  Google Scholar 

  264. Xie Y, Xia P, Wang H, Yu H, Giesy JP, Zhang Y, Mora MA, Zhang X (2016) Effects of captivity and artificial breeding on microbiota in feces of the red-crowned crane (Grus japonensis). Sci Rep 6:33350. https://doi.org/10.1038/srep33350

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  265. Ericsson AC, Franklin CL (2015) Manipulating the gut microbiota: Methods and challenges. ILAR J 56:205–217. https://doi.org/10.1093/ilar/ilv021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  266. Madison JD, Austin S, Davis DR, Kerby JL (2018) Bacterial microbiota response in Graptemys pseudogeographica to captivity and Roundup® exposure. Copeia 106:580–588. https://doi.org/10.1643/ch-18-082

    Article  Google Scholar 

  267. Björk JR, Dasari M, Grieneisen L, Archie EA (2019) Primate microbiomes over time: Longitudinal answers to standing questions in microbiome research. Am J Primatol:e22970 https://doi.org/10.1002/ajp.22970

  268. Oh J, Byrd AL, Park M, Program NCS, Kong HH, Segre JA (2016) Temporal stability of the human skin microbiome. Cell 165:854–866. https://doi.org/10.1016/j.cell.2016.04.008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  269. Chong R, Shi M, Grueber CE, Holmes EC, Hogg CJ, Belov K, Barrs VR (2019) Fecal viral diversity of captive and wild Tasmanian devils characterized using virion-enriched metagenomics and metatranscriptomics. J Virol 93https://doi.org/10.1128/JVI.00205-19

  270. Sawaswong V, Fahsbender E, Altan E, Kemthong T, Deng X, Malaivijitnond S, Payungporn S, Delwart E (2019) High diversity and novel enteric viruses in fecal viromes of healthy wild and captive Thai cynomolgus macaques (Macaca fascicularis). Viruses 11https://doi.org/10.3390/v11100971

  271. Bates KA, Shelton JMG, Mercier VL, Hopkins KP, Harrison XA, Petrovan SO, Fisher MC (2019) Captivity and infection by the fungal pathogen Batrachochytrium salamandrivorans perturb the amphibian skin microbiome. Front Microbiol 10:1834. https://doi.org/10.3389/fmicb.2019.01834

    Article  PubMed  PubMed Central  Google Scholar 

  272. Mukhopadhya I, Segal JP, Carding SR, Hart AL, Hold GL (2019) The gut virome: the “missing link” between gut bacteria and host immunity? Therap Adv Gastroenterol 12:1756284819836620. https://doi.org/10.1177/1756284819836620

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  273. Ning Y, Qi J, Dobbins MT, Liang X, Wang J, Chen S, Ma J, Jiang G (2020) Comparative analysis of microbial community structure and function in the gut of wild and captive Amur tiger. Front Microbiol 11:1665. https://doi.org/10.3389/fmicb.2020.01665

    Article  PubMed  PubMed Central  Google Scholar 

  274. Hale VL, Tan CL, Niu K, Yang Y, Zhang Q, Knight R, Amato KR (2019) Gut microbiota in wild and captive Guizhou snub-nosed monkeys, Rhinopithecus brelichi. Am J Primatol 81:e22989. https://doi.org/10.1002/ajp.22989

    Article  CAS  PubMed  Google Scholar 

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    Jason W. Dallas & Robin W. Warne

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Jason Dallas contributed to manuscript conception. The first draft of the manuscript was written by Jason Dallas, and both authors commented on previous versions of the manuscript. Both authors read and approved the final manuscript.

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Dallas, J.W., Warne, R.W. Captivity and Animal Microbiomes: Potential Roles of Microbiota for Influencing Animal Conservation. Microb Ecol 85, 820–838 (2023). https://doi.org/10.1007/s00248-022-01991-0

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  • DOI: https://doi.org/10.1007/s00248-022-01991-0

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