Articles | Volume 26, issue 2
https://doi.org/10.5194/we-26-223-2026
© Author(s) 2026. This work is distributed under
the Creative Commons Attribution 4.0 License.
the Creative Commons Attribution 4.0 License.
https://doi.org/10.5194/we-26-223-2026
© Author(s) 2026. This work is distributed under
the Creative Commons Attribution 4.0 License.
the Creative Commons Attribution 4.0 License.
Gut microbiomes of the little free-tailed bat (Mops pumilus) show high prevalence of potential bacterial pathogens but limited responses to land cover
Julie Teresa Shapiro
CORRESPONDING AUTHOR
School of Natural Resources and Environment, University of Florida, Gainesville, Florida 32611, USA
present address: University of Lyon – French Agency for Food, Environmental and Occupational Health and Safety (ANSES), Epidemiology and Surveillance Support Unit, Lyon 69007, France
Christopher Barnes
Centre for Evolutionary Hologenomics, The Globe Institute, Faculty of Health, University of Copenhagen, Kobenhavn (Copenhagen), Denmark
Department of Agroecology, Faculty of Technical Sciences, Aarhus University, Slagelse 4200, Denmark
Ida Broman Nielsen
Section for GeoGenetics, Globe Institute, University of Copenhagen, Kobenhavn (Copenhagen) 1350, Denmark
Linett Rasmussen
Centre for Evolutionary Hologenomics, The Globe Institute, Faculty of Health, University of Copenhagen, Kobenhavn (Copenhagen), Denmark
present address: Copenhagen Zoo, Frederiksberg 2000, Denmark
Ara Monadjem
Department of Zoology & Entomology, University of Pretoria, Pretoria 0002, South Africa
Department of Biological Sciences, University of Eswatini, Kwaluseni M201, Eswatini
Robert A. McCleery
School of Natural Resources and Environment, University of Florida, Gainesville, Florida 32611, USA
Anders J. Hansen
Section for GeoGenetics, Globe Institute, University of Copenhagen, Kobenhavn (Copenhagen) 1350, Denmark
Cited articles
Adesiyun, A. A., Stewart-Johnson, A., and Thompson, N. N.: Isolation of enteric pathogens from bats in Trinidad, J. Wildlife Dis., 45, 952–961, https://doi.org/10.7589/0090-3558-45.4.952, 2009.
Aladejana, O. M., Oluduro, A. O., Ogunlade, A. O., Babatunde, S. K., and Sanni, O. T.: Isolation, molecular identification and antibiotics susceptibility of Salmonella serotypes isolates from bats in Osun State, Nigeria, Vegetos, 38, 668–675, https://doi.org/10.1007/s42535-023-00791-2, 2025.
Aleman, J. C., Blarquez, O., and Staver, C. A.: Land-use change outweighs projected effects of changing rainfall on tree cover in sub-Saharan Africa, Glob. Change Biol., 22, 3013–3025, https://doi.org/10.1111/gcb.13299, 2016.
Alpízar, P., Risely, A., Tschapka, M., and Sommer, S.: Agricultural fast food: Bats feeding in banana monocultures are heavier but have less diverse gut microbiota, Front. Ecol. Evol., 9, https://doi.org/10.3389/fevo.2021.746783, 2021.
Amato, K. R., Yeoman, C. J., Kent, A., Righini, N., Carbonero, F., Estrada, A., Gaskins, H. R., Stumpf, R. M., Yildirim, S., Torralba, M., Gillis, M., Wilson, B. A., Nelson, K. E., White, B. A., and Leigh, S. R.: Habitat degradation impacts black howler monkey (Alouatta pigra) gastrointestinal microbiomes, ISME J., 7, 1344–1353, https://doi.org/10.1038/ismej.2013.16, 2013.
Arellano-Hernández, H. D., Montes-Carreto, L. M., Guerrero, J. A., and Martinez-Romero, E.: The fecal microbiota of the mouse-eared bat (Myotis velifer) with new records of microbial taxa for bats, PLoS One, 19, e0314847, https://doi.org/10.1371/journal.pone.0314847, 2024.
Bäckhed, F., Ding, H., Wang, T., Hooper, L. V., Koh, G. Y., Nagy, A., Semenkovich, C. F., and Gordon, J. I.: The gut microbiota as an environmental factor that regulates fat storage, P. Natl. Acad. Sci. USA, 101, 15718–15723, https://doi.org/10.1073/pnas.0407076101, 2004.
Bailey, K. M., McCleery, R. A., Binford, M. W., and Zweig, C.: Land-cover change within and around protected areas in a biodiversity hotspot, J. Land Use Sci., 1–23, https://doi.org/10.1080/1747423X.2015.1086905, 2015.
Banskar, S., Mourya, D. T., and Shouche, Y. S.: Bacterial diversity indicates dietary overlap among bats of different feeding habits, Microbiol. Res., 182, 99–108, https://doi.org/10.1016/j.micres.2015.10.006, 2016.
Barelli, C., Albanese, D., Donati, C., Pindo, M., Dallago, C., Rovero, F., Cavalieri, D., Tuohy, K. M., Hauffe, H. C., and De Filippo, C.: Habitat fragmentation is associated to gut microbiota diversity of an endangered primate: implications for conservation, Sci. Rep., 5, 14862, https://doi.org/10.1038/srep14862, 2015.
Barnes, C. J., Rasmussen, L., Asplund, M., Knudsen, S. W., Clausen, M.-L., Agner, T., and Hansen, A. J.: Comparing DADA2 and OTU clustering approaches in studying the bacterial communities of atopic dermatitis, J. Med. Microbiol., 69, 1293–1302, https://doi.org/10.1099/jmm.0.001256, 2020.
Barton, K.: MuMIn: Multi-model inference. R package version 1.40.0, https://CRAN.R-project.org/package=MuMIn (last access: 28 December 2025), 2017.
Bates, D., Mächler, M., Bolker, B., and Walker, S.: Fitting linear mixed-effects models using lme4, J. Stat. Softw., 67, 1–48, https://doi.org/10.18637/jss.v067.i01, 2015.
Becker, D. J., Dyer, K. E., Lock, L. R., Olbrys, B. L., Pladas, S. A., Sukhadia, A. A., Demory, B., Nunes Batista, J. M., Pineda, M., Simmons, N. B., Adams, A. M., Frick, W. F., O'Mara, M. T., and Volokhov, D. V.: Geographically widespread and novel hemotropic mycoplasmas and bartonellae in Mexican free-tailed bats and sympatric North American bat species, mSphere, 10, e00116-24, https://doi.org/10.1128/msphere.00116-24, 2024.
Beisele, M., Shen, Z., Parry, N., Mobley, M., Taylor, N. S., Buckley, E., Abedin, M. Z., Dewhirst, F. E., and Fox, J. G.: Helicobactermarmotae and novel Helicobacter and Campylobacter species isolated from the livers and intestines of prairie dogs, J. Med. Microbiol., 60, 1366–1374, https://doi.org/10.1099/jmm.0.032144-0, 2011.
Bennett, A. J., Suski, C. D., and O'Keefe, J. M.: Molecular epidemiology of Eimeria spp. parasites and the faecal microbiome of Indiana bats (Myotis sodalis): A non-invasive, multiplex metabarcode survey of an endangered species, Microb. Genom., 11, 001358, https://doi.org/10.1099/mgen.0.001358, 2025.
Bernardo-Cravo, A. P., Schmeller, D. S., Chatzinotas, A., Vredenburg, V. T., and Loyau, A.: Environmental factors and host microbiomes shape host–pathogen dynamics, Trends Parasitol., 36, 616–633, https://doi.org/10.1016/j.pt.2020.04.010, 2020.
Bernardo Reyes, A. W., Rovira, H. G., Masangkay, J. S., Ramirez, T. J., Yoshikawa, Y., and Baticados, W. N.: Polymerase Chain Reaction assay and conventional isolation of Salmonella spp. from Philippine bats, Acta Sci. Vet., 39, 1, https://www.redalyc.org/pdf/2890/289022244008.pdf (last access: 18 September 2026), 2011.
Biagi, E., Franceschi, C., Rampelli, S., Severgnini, M., Ostan, R., Turroni, S., Consolandi, C., Quercia, S., Scurti, M., Monti, D., Capri, M., Brigidi, P., and Candela, M.: Gut microbiota and extreme longevity, Curr. Biol., 26, 1480–1485, https://doi.org/10.1016/j.cub.2016.04.016, 2016.
Billeter, S. A., Hayman, D. T. S., Peel, A. J., Baker, K., Wood, J. L. N., Cunningham, A., Suu-Ire, R., Dittmar, K., and Kosoy, M. Y.: Bartonella species in bat flies (Diptera: Nycteribiidae) from western Africa, Parasitology, 139, 324–329, https://doi.org/10.1017/S0031182011002113, 2012.
Blanchet, F. G., Legendre, P., and Borcard, D.: Forward selection of explanatory variables, Ecology, 89, 2623–2632, https://doi.org/10.1890/07-0986.1, 2008.
Bodenhofer, U., Bonatesta, E., Horejš-Kainrath, C., and Hochreiter, S.: msa: an R package for multiple sequence alignment, Bioinformatics, 31, 3997–3999, https://doi.org/10.1093/bioinformatics/btv494, 2015.
Bohmann, K., Monadjem, A., Noer, C. L., Rasmussen, M., Zeale, M. R. K., Clare, E., Jones, G., Willerslev, E., and Gilbert, M. T. P.: Molecular diet analysis of two African free-tailed bats (Molossidae) using high throughput sequencing, PLoS One, 6, e21441, https://doi.org/10.1371/journal.pone.0021441, 2011.
Borcard, D., Legendre, P., and Drapeau, P.: Partialling out the spatial component of ecological variation, Ecology, 73, 1045–1055, https://doi.org/10.2307/1940179, 1992.
Bouchard, S.: Chaerephon pumilus, Mamm. Species, 574, 1–6, 1998.
Brook, C. E., Bai, Y., Dobson, A. P., Osikowicz, L. M., Ranaivoson, H. C., Zhu, Q., Kosoy, M. Y., and Dittmar, K.: Bartonella spp. in fruit bats and blood-feeding ectoparasites in Madagascar, PLoS Neglect. Trop. D., 9, e0003532, https://doi.org/10.1371/journal.pntd.0003532, 2015.
Burgin, C. J., Zijlstra, J. S., Becker, M. A., Handika, H., Alston, J. M., Widness, J., Liphardt, S., Huckaby, D. G., and Upham, N. S.: How many mammal species are there now? Updates and trends in taxonomic, nomenclatural, and geographic knowledge, J. Mammal., 106, 1082–1117, https://doi.org/10.1093/jmammal/gyaf047, 2025.
Burnham, K. P. and Anderson, D. R.: Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach, Springer-Verlag, New York, 488 pp., https://doi.org/10.1007/b97636, 2002.
Bustin, S. A., Benes, V., Garson, J. A., Hellemans, J., Huggett, J., Kubista, M., Mueller, R., Nolan, T., Pfaffl, M. W., Shipley, G. L., Vandesompele, J., and Wittwer, C. T.: The MIQE guidelines: Minimum information for publication of quantitative real-time PCR experiments, Clin. Chem., 55, 611–622, https://doi.org/10.1373/clinchem.2008.112797, 2009.
Callahan, B. J., McMurdie, P. J., Rosen, M. J., Han, A. W., Johnson, A. J. A., and Holmes, S. P.: DADA2: High-resolution sample inference from Illumina amplicon data, Nat. Methods, 13, 581–583, https://doi.org/10.1038/nmeth.3869, 2016.
Carmody, R. N., Gerber, G. K., Luevano, J. M., Gatti, D. M., Somes, L., Svenson, K. L., and Turnbaugh, P. J.: Diet dominates host genotype in shaping the murine gut microbiota, Cell Host Microbe, 17, 72–84, https://doi.org/10.1016/J.CHOM.2014.11.010, 2015.
Carrillo-Araujo, M., Taş, N., Alcántara-Hernández, R. J., Gaona, O., Schondube, J. E., Medellín, R. A., Jansson, J. K., and Falcón, L. I.: Phyllostomid bat microbiome composition is associated to host phylogeny and feeding strategies, Front. Microbiol., 6, 447, https://doi.org/10.3389/fmicb.2015.00447, 2015.
Chambers, C. L., Cushman, S. A., Medina-Fitoria, A., Martínez-Fonseca, J., and Chávez-Velásquez, M.: Influences of scale on bat habitat relationships in a forested landscape in Nicaragua, Landscape Ecol., 31, 1299–1318, https://doi.org/10.1007/s10980-016-0343-4, 2016.
Chang, C.-W., Huang, B.-H., Lin, S.-M., Huang, C.-L., and Liao, P.-C.: Changes of diet and dominant intestinal microbes in farmland frogs, BMC Microbiol., 16, 33, https://doi.org/10.1186/s12866-016-0660-4, 2016.
Chao, A.: Estimating the population size for capture-recapture data with unequal catchability, Biometrics, 43, 783–791, 1987.
Charif, D. and Lobry, J.: SeqinR 1.0-2: a contributed package to the R project for statistical computing devoted to biological sequences retrieval and analysis, in: Structural approaches to sequence evolution: Molecules, networks, populations, series Biological and Medical Physics, Biomedical Engineering, edited by: Bastolla, U., Porto, M., Roman, H., and Vendruscolo, M., Springer Verlag, New York, 207–232, ISBN 978-3-540-35305-8, 2007.
Cicuttin, G. L., De Salvo, M. N., La Rosa, I., and Dohmen, F. E. G.: Neorickettsia risticii, Rickettsia sp. and Bartonella sp. in Tadarida brasiliensis bats from Buenos Aires, Argentina, Comp. Immunol. Microb., 52, 1–5, https://doi.org/10.1016/j.cimid.2017.04.004, 2017.
Claesson, M. J., Jeffery, I. B., Conde, S., Power, S. E., O'Connor, E. M., Cusack, S., Harris, H. M. B., Coakley, M., Lakshminarayanan, B., O'Sullivan, O., Fitzgerald, G. F., Deane, J., O'Connor, M., Harnedy, N., O'Connor, K., O'Mahony, D., Van Sinderen, D., Wallace, M., Brennan, L., Stanton, C., Marchesi, J. R., Fitzgerald, A. P., Shanahan, F., Hill, C., Ross, R. P., and O'Toole, P. W.: Gut microbiota composition correlates with diet and health in the elderly, Nature, 488, 178–185, https://doi.org/10.1038/nature11319, 2012.
Coburn, B., Grassl, G. A., and Finlay, B. B.: Salmonella, the host and disease: A brief review, Immunol. Cell Biol., 85, 112–118, https://doi.org/10.1038/sj.icb.7100007, 2007.
Daszak, P., Cunningham, A. A. A., and Hyatt, A. D. D.: Anthropogenic environmental change and the emergence of infectious diseases in wildlife, Acta Trop., 78, 103–116, https://doi.org/10.1016/s0001-706x(00)00179-0, 2001.
Dawood, A., Algharib, S. A., Zhao, G., Zhu, T., Qi, M., Delai, K., Hao, Z., Marawan, M. A., Shirani, I., and Guo, A.: Mycoplasmas as host pantropic and specific pathogens: Clinical implications, gene transfer, virulence factors, and future perspectives, Front. Cell. Infect. Mi., 12, 855731, https://doi.org/10.3389/fcimb.2022.855731, 2022.
Descloux, E., Mediannikov, O., Gourinat, A.-C., Colot, J., Chauvet, M., Mermoud, I., Desoutter, D., Cazorla, C., Klement-Frutos, E., Antonini, L., Levasseur, A., Bossi, V., Davoust, B., Merlet, A., Goujart, M.-A., Oedin, M., Brescia, F., Laumond, S., Fournier, P.-E., and Raoult, D.: Flying fox hemolytic fever, description of a new zoonosis caused by Candidatus Mycoplasma haemohominis, Clin. Infect. Dis., 73, e1445–e1453, https://doi.org/10.1093/cid/ciaa1648, 2021.
Di Cataldo, S., Kamani, J., Cevidanes, A., Msheliza, E. G., and Millán, J.: Hemotropic mycoplasmas in bats captured near human settlements in Nigeria, Comp. Immunol. Microb., 70, 101448, https://doi.org/10.1016/j.cimid.2020.101448, 2020.
Dietrich, M., Tjale, M. A., Weyer, J., Kearney, T., Seamark, E. C. J., Nel, L. H., Monadjem, A., and Markotter, W.: Diversity of Bartonella and Rickettsia spp. in bats and their blood-feeding ectoparasites from South Africa and Swaziland, PLoS One, 11, e0152077, https://doi.org/10.1371/journal.pone.0152077, 2016.
Dietrich, M., Kearney, T., Seamark, E. C. J., and Markotter, W.: The excreted microbiota of bats: Evidence of niche specialisation based on multiple body habitats, FEMS Microbiol. Lett., 364, fnw284, https://doi.org/10.1093/femsle/fnw284, 2017.
Dietrich, M., Kearney, T., Seamark, E. C. J., Paweska, J. T., and Markotter, W.: Synchronized shift of oral, faecal and urinary microbiotas in bats and natural infection dynamics during seasonal reproduction, Roy. Soc. Open Sci., 5, 180041, https://doi.org/10.1098/rsos.180041, 2018.
do Amaral, R. B., Lourenço, E. C., Famadas, K. M., Garcia, A. B., Machado, R. Z., and André, M. R.: Molecular detection of Bartonella spp. and Rickettsia spp. in bat ectoparasites in Brazil, PLoS One, 13, e0198629, https://doi.org/10.1371/journal.pone.0198629, 2018.
Dutta, P., Uddin, Md. H., Islam, S., Islam, M., Hossain, M. S., Sagor, M. S., Rumi, M. A., Rahman, M. K., FLora, M. S., Samad, M. A., Forwood, J. K., Epstein, J. H., Chowdhury, S., and Islam, A.: Epidemiology and ecology of multidrug resistance (MDR) Salmonella in fruit bats in Bangladesh, The 20th International Bat Research Conference (IBRC) 2025, 171–171, https://researchoutput.csu.edu.au/en/publications/epidemiology-and-ecology-of-multidrug-resistance-mdr-salmonella-i/ (last access: 18 September 2026), 2025.
Edgar, R. C.: UNBIAS: An attempt to correct abundance bias in 16S sequencing, with limited success, bioRxiv [preprint], https://doi.org/10.1101/124149, 2017.
Elbrecht, V. and Leese, F.: Can DNA-based ecosystem assessments quantify species abundance? Testing primer bias and biomass–sequence relationships with an innovative metabarcoding protocol, PLoS One 10, e0130324, https://doi.org/10.1371/journal.pone.0130324, 2015.
Ethier, K. and Fahrig, L.: Positive effects of forest fragmentation, independent of forest amount, on bat abundance in eastern Ontario, Canada, Landscape Ecol., 26, 865–876, https://doi.org/10.1007/s10980-011-9614-2, 2011.
Evans, N. J., Bown, K. J., Timofte, D., Simpson, V. R., and Birtles, R. J.: Fatal borreliosis in bat caused by relapsing fever spirochete, United Kingdom, Emerg. Infect. Dis., 15, 1331–1333, https://doi.org/10.3201/eid1508.090475, 2009.
Fackelmann, G., Gillingham, M. A. F., Schmid, J., Heni, A. C., Wilhem, K., Schwensow, N., and Sommer, S.: Human encroachment into wildlife gut microbiomes, Commun. Biol., 4, 800, https://doi.org/10.1038/s42003-021-02315-7, 2021.
Fahrig, L.: Effects of habitat fragmentation on biodiversity, Annu. Rev. Ecol. Evol. S., 34, 487–515, https://doi.org/10.1146/annurev.ecolsys.34.011802.132419, 2003.
Faith, D. P.: Conservation evaluation and phylogenetic diversity, Biol. Conserv., 61, 1–10, https://doi.org/10.1016/0006-3207(92)91201-3, 1992.
Feddema, J. J., Oleson, K. W., Bonan, G. B., Mearns, L. O., Buja, L. E., Meehl, G. A., and Washington, W. M.: The importance of land-cover change in simulating future climates, Science, 310, 1674–1678, https://doi.org/10.1126/science.1118160, 2005.
Ferreira, A. C. R., Vieira, T. M., da Costa Custódio, D. A., Melo, M. N., Gontijo, C. M. F., Lage, A. P., and Dorneles, E. M. S.: Cross-sectional study on Brucella spp., Leptospira spp. and Salmonella spp. in bats from Montes Claros, Minas Gerais, Brazil, Comp. Immunol. Microb., 78, 101692, https://doi.org/10.1016/j.cimid.2021.101692, 2021.
Ferreira, A. C. R., Colocho, R. A. B., Pereira, C. R., Veira, T. M., Gregorin, R., Lage, A. P., and Dorneles, E. M. S.: Zoonotic bacterial pathogens in bats samples around the world: A scoping review, Prev. Vet. Med., 225, 106135, https://doi.org/10.1016/j.prevetmed.2024.106135, 2024.
Ficetola, G. F., Pansu, J., Elie Bonin, A., Coissac, E., Giguet-Covex, C., De Barba, M., Gielly, L., Lopes, C. M., and Boyer, E. E.: Replication levels, false presences and the estimation of the presence/absence from eDNA metabarcoding data, Mol. Ecol. Resour., 15, 543–556, https://doi.org/10.1111/1755-0998.12338, 2015.
Fischer, J. and Lindenmayer, D. B.: Beyond fragmentation: The continuum model for fauna research and conservation in human-modified landscapes, Oikos, 112, 473–480, https://doi.org/10.1111/j.0030-1299.2006.14148.x, 2006.
Fleischer, R., Jones, C., Ledezma-Campos, P., Czirják, G. Á., Sommer, S., Gillespie, T. R., and Vicente-Santos, A.: Gut microbial shifts in vampire bats linked to immunity due to changed diet in human disturbed landscapes, Sci. Total Environ., 907, 167815, https://doi.org/10.1016/j.scitotenv.2023.167815, 2024.
Frick, W. F., Kingston, T., and Flanders, J.: A review of the major threats and challenges to global bat conservation, Ann. NY Acad. Sci., 1469, 5–25, https://doi.org/10.1111/nyas.14045, 2020.
Frøslev, T. G., Kjøller, R., Bruun, H. H., Ejrnæs, R., Brunbjerg, A. K., Pietroni, C., and Hansen, A. J.: Algorithm for post-clustering curation of DNA amplicon data yields reliable biodiversity estimates, Nat. Commun., 8, 1188, https://doi.org/10.1038/s41467-017-01312-x, 2017.
Gaona, O., Gómez-Acata, E. S., Cerqueda-García, D., Neri-Barrios, C. X., and Falcón, L. I.: Fecal microbiota of different reproductive stages of the central population of the lesser-long nosed bat, Leptonycteris yerbabuenae, PLoS One, 14, e0219982, https://doi.org/10.1371/journal.pone.0219982, 2019.
Ge, X., Li, Y., Yang, X., Zhang, H., Zhou, P., Zhang, Y., and Shi, Z.: Metagenomic analysis of viruses from bat fecal samples reveals many novel viruses in insectivorous bats in China, J. Virol., 86, 4620–4630, https://doi.org/10.1128/jvi.06671-11, 2012.
Geldenhuys, M., Mortlock, M., Weyer, J., Bezuidt, O., Seamark, E. C. J., Kearney, T., Gleasner, C., Erkkila, T. H., Cui, H., and Markotter, W.: A metagenomic viral discovery approach identifies potential zoonotic and novel mammalian viruses in Neoromicia bats within South Africa, PLoS One, 13, e0194527, https://doi.org/10.1371/journal.pone.0194527, 2018.
Gerbáčová, K., Maliničová, L., Kisková, J., Maslišová, V., Uhrin, M., and Pristaš, P.: The faecal microbiome of building-dwelling insectivorous bats (Myotis myotis and Rhinolophus hipposideros) also Contains antibiotic-resistant bacterial representatives, Curr. Microbiol., 77, 2333–2344, https://doi.org/10.1007/s00284-020-02095-z, 2020.
Goldman, C. G., Matteo, M. J., Loureiro, J. D., Almuzara, M., Barberis, C., Vay, C., Catalano, M., Heredia, S. R., Mantero, P., Boccio, J. R., Zubillaga, M. B., Cremaschi, G. A., Solnick, J. V., Perez-Perez, G. I., and Blaser, M. J.: Novel gastric helicobacters and oral campylobacters are present in captive and wild cetaceans, Vet. Microbiol., 152, 138–145, https://doi.org/10.1016/j.vetmic.2011.04.023, 2011.
Goodrich, J. K., Waters, J. L., Poole, A. C., Sutter, J. L., Koren, O., Blekhman, R., Beaumont, M., Van Treuren, W., Knight, R., Bell, J. T., Spector, T. D., Clark, A. G., and Ley, R. E.: Human genetics shape the gut microbiome, Cell, 159, 789–799, https://doi.org/10.1016/J.CELL.2014.09.053, 2014.
Handy, R. D., Clark, N. J., Hutt, L. P., and Bescós, R.: The microbiomes of wildlife and chemical pollution: Status, knowledge gaps and challenges, Current Opinion in Toxicology, 36, 100428, https://doi.org/10.1016/j.cotox.2023.100428, 2023.
Hansen, C. H. F., Krych, L., Nielsen, D. S., Vogensen, F. K., Hansen, L. H., Sørensen, S. J., Buschard, K., and Hansen, A. K.: Early life treatment with vancomycin propagates Akkermansia muciniphila and reduces diabetes incidence in the NOD mouse, Diabetologia, 55, 2285–2294, https://doi.org/10.1007/s00125-012-2564-7, 2012.
Harrell Jr., F. E.: Hmisc: Harrell Miscellaneous. R package version 3.0-12, https://cran.r-project.org/web/packages/Hmisc/index.html (last access: 28 December 2025), 2006.
Hartup, B. K., Bickal, J. M., Dhondt, A. A., Ley, D. H., and Kollias, G. V.: Dynamics of conjunctivitis and Mycoplasma gallisepticum infections in house Finches, Auk, 118, 327–333, https://doi.org/10.1093/auk/118.2.327, 2001.
Hatta, Y., Omatsu, T., Tsuchiaka, S., Katayama, Y., Taniguchi, S., Masangkay, J. S., Puentespina Jr., R., Eres, E., Cosico, E., Une, Y., Yoshikawa, Y., Maeda, K., Kyuwa, S., and Mizutani, T.: Detection of Campylobacter jejuni in rectal swab samples from Rousettus amplexicaudatus in the Philippines, J. Vet. Med. Sci., 78, 1347–1350, https://doi.org/10.1292/jvms.15-0621, 2016.
Hayman, D. T. S.: Bats as viral reservoirs, Ann. Rev. Virol., 3, 77–99, https://doi.org/10.1146/annurev-virology-110615-042203, 2016.
Hazeleger, W. C., Jacobs-Reitsma, W. F., Lina, P. H. C., de Boer, A. G., Bosch, T., van Hoek, A. H. A. M., and Beumer, R. R.: Wild, insectivorous bats might be carriers of Campylobacter spp., PLoS One, 13, e0190647, https://doi.org/10.1371/journal.pone.0190647, 2018.
Hijmans, R. J.: geosphere: Spherical trigonometry, https://cran.r-project.org/web/packages/geosphere/index.html (last access: 18 September 2026), 2017.
Hornok, S., Szőke, K., Meli, M. L., Sándor, A. D., Görföl, T., Estók, P., Wang, Y., Tu, V. T., Kováts, D., Boldogh, S. A., Corduneanu, A., Sulyok, K. M., Gyuranecz, M., Kontschán, J., Takács, N., Halajian, A., Epis, S., and Hofmann-Lehmann, R.: Molecular detection of vector-borne bacteria in bat ticks (Acari: Ixodidae, Argasidae) from eight countries of the Old and New Worlds, Parasit. Vector., 12, 50, https://doi.org/10.1186/s13071-019-3303-4, 2019.
Hughes, G. M., Leech, J., Puechmaille, S. J., Lopez, J. V., and Teeling, E. C.: Is there a link between aging and microbiome diversity in exceptional mammalian longevity?, PeerJ, 6, e4174, https://doi.org/10.7717/peerj.4174, 2018.
Imnadze, T., Natradze, I., Zhgenti, E., Malania, L., Abazashvili, N., Sidamonidze, K., Khmaladze, E., Zakalashvili, M., Imnadze, P., Arner, R. J., Motin, V., and Kosoy, M.: Identification of a novel Yersinia enterocolitica strain from bats in association with a bat die-off that occurred in Georgia (Caucasus), Microorganisms, 8, 1000, https://doi.org/10.3390/microorganisms8071000, 2020.
Ingala, M. R., Simmons, N. B., Wultsch, C., Krampis, K., Speer, K. A., and Perkins, S. L.: Comparing microbiome sampling methods in a wild mammal: Fecal and intestinal samples record different signals of host ecology, evolution, Front. Microbiol., 9, 803, https://doi.org/10.3389/fmicb.2018.00803, 2018.
Ingala, M. R., Becker, D. J., Bak Holm, J., Kristiansen, K., and Simmons, N. B.: Habitat fragmentation is associated with dietary shifts and microbiota variability in common vampire bats, Ecol. Evol., 9, 6508–6523, https://doi.org/10.1002/ece3.5228, 2019.
Islam, A., Mikolon, A., Mikoleit, M., Ahmed, D., Khan, S. U., Sharker, M. A. Y., Hossain, M. J., Islam, A., Epstein, J. H., Zeidner, N., and Luby, S. P.: Isolation of Salmonella Virchow from a fruit bat (Pteropus giganteus), EcoHealth, 10, 348–351, https://doi.org/10.1007/s10393-013-0866-y, 2013.
Jiménez, R. R. and Sommer, S.: 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, 2017.
Johnson J. S., Reeder, D. M., McMichael III, J. W., Meierhofer, M. B., Stern, D. W. F., Lumadue, S. S., Sigler, L. E., Winters, H. D., Vodzak, M. E., Kurta, A., Kath, J. A., and Field, K. A.: Host, pathogen, and environmental characteristics predict White-Nose Syndrome mortality in captive little brown myotis (Myotis lucifugus), PLoS One, 9, e112502, https://doi.org/10.1371/journal.pone.0112502, 2014.
Kamani, J., Baneth, G., Mitchell, M., Mumcuoglu, K. Y., Gutiérrez, R., and Harrus, S.: Bartonella species in bats (Chiroptera) and bat flies (Nycteribiidae) from Nigeria, West Africa, Vector-Borne Zoonot., 14, 625–32, https://doi.org/10.1089/vbz.2013.1541, 2014.
Kembel, S. W., Cowan, P. D., Helmus, M. R., Cornwell, W. K., Morlon, H., Ackerly, D. D., Blomberg, S. P., and Webb, C. O.: Picante: R tools for integrating phylogenies and ecology, Bioinformatics, 26, 1463–1464, https://doi.org/10.1093/bioinformatics/btq166, 2010.
Kolodny, O., Weinberg, M., Reshef, L., Harten, L., Hefetz, A., Gophna, U., Feldman, M. W., and Yovel, Y.: Coordinated change at the colony level in fruit bat fur microbiomes through time, Nat. Ecol. Evol., 3, 116–124, https://doi.org/10.1038/s41559-018-0731-z, 2019.
Kosoy, M., Hayman, D. T. S., and Chan, K.-S.: Bartonella bacteria in nature: Where does population variability end and a species start?, Infect. Genet. Evol., 12, 894–904, https://doi.org/10.1016/j.meegid.2012.03.005, 2012.
Kunz, T. H. and Anthony, E. L. P.: Age estimation and post-natal growth in the bat Myotis lucifugus, J. Mammal., 63, 23–32, 1982.
Kuznetsova, A., Brockhoff, P. B., and Christensen, R. H. B.: lmerTest Package: Tests in Linear Mixed Effects Models. J. Stat. Softw., 82, 1–26, https://doi.org/10.18637/jss.v082.i13, 2017.
Lambin, E. F., Tran, A., Vanwambeke, S. O., Linard, C., and Soti, V.: Pathogenic landscapes: Interactions between land, people, disease vectors, and their animal hosts, Int. J. Health Geogr., 9, 54, https://doi.org/10.1186/1476-072X-9-54, 2010.
Laurance, W. F., Sayer, J., and Cassman, K. G.: Agricultural expansion and its impacts on tropical nature, Trends Ecol. Evol., 29, 107–116, https://doi.org/10.1016/J.TREE.2013.12.001, 2014.
Law, B. S.: Residency and site fidelity of marked populations of the Common Blossom Bat Syconycteris australis in relation to the availability of Banksia inflorescences in New South Wales, Australia, Oikos, 77, 447–458, https://doi.org/10.2307/3545934, 1996.
Lebeuf-Taylor, E., Cosby, A., Webber, Q., and Cottenie, K.: Social structuring of the gut microbiome in communally roosting bats, PLoS One, 20, e0325710, https://doi.org/10.1371/journal.pone.0325710, 2025.
Leemans, R. and Zuidema, G.: Evaluating changes in land cover and their importance for global change, Trends Ecol. Evol., 10, 76–81, https://doi.org/10.1016/S0169-5347(00)88981-8, 1995.
Legendre, P. and Anderson, M. J.: Distance-based redundancy analysis: Testing multispecies responses in multifactorial ecological experiments, Ecol. Monogr., 69, 1–24, https://doi.org/10.1890/0012-9615(1999)069[0001:DBRATM]2.0.CO;2, 1999.
Leonard, A., Abalos, J., Adhola, T., et al.: A global initiative for ecological and evolutionary hologenomics, Trends Ecol. Evol., 39, 616–620, https://doi.org/10.1016/j.tree.2024.03.005, 2024.
Leulmi, H., Aouadi, A., Bitam, I., Bessas, A., Benakhla, A., Raoult, D., and Parola, P.: Detection of Bartonella tamiae, Coxiella burnetii and rickettsiae in arthropods and tissues from wild and domestic animals in northeastern Algeria, Parasit. Vector., 9, 27, https://doi.org/10.1186/s13071-016-1316-9, 2016.
Ley, R. E., Turnbaugh, P. J., Klein, S., and Gordon, J. I.: Microbial ecology: Human gut microbes associated with obesity, Nature, 444, 1022–1023, https://doi.org/10.1038/4441022a, 2006.
Ley, R. E., Hamady, M., Lozupone, C., Turnbaugh, P. J., Ramey, R. R., Bircher, J. S., Schlegel, M. L., Tucker, T. A., Schrenzel, M. D., Knight, R., and Gordon, J. I.: Evolution of mammals and their gut microbes, Science, 320, 1647–1651, https://doi.org/10.1126/science.1155725, 2008a.
Ley, R. E., Lozupone, C. A., Hamady, M., Knight, R., and Gordon, J. I.: Worlds within worlds: Evolution of the vertebrate gut microbiota, Nat. Rev. Microbiol., 6, 776–788, https://doi.org/10.1038/nrmicro1978, 2008b.
Li, J., Li, L., Jiang, H., Yuan, L., Zhang, L., Ma, J., Zhang, X., Cheng, M., and Chen, J.: Fecal bacteriome and mycobiome in bats with diverse diets in South China, Curr. Microbiol., 75, 1352–1361, https://doi.org/10.1007/s00284-018-1530-0, 2018.
Linard, C., Gilbert, M., Snow, R. W., Noor, A. M., and Tatem, A. J.: Population distribution, settlement patterns and accessibility across Africa in 2010, PLoS One, 7, e31743, https://doi.org/10.1371/journal.pone.0031743, 2012.
Lobato-Bailón, L., García-Ulloa, M., Santos, A., Guixé, D., Camprodon, J., Florensa-Rius, X., Molleda, R., Manzano, R., P. Ribas, M., Espunyes, J., Dias-Alves, A., Marco, I., Migura-Garcia, L., Martínez-Urtaza, J., and Cabezón, O.: The fecal bacterial microbiome of the Kuhl's pipistrelle bat (Pipistrellus kuhlii) reflects landscape anthropogenic pressure, Anim. Microbiome, 5, 7, https://doi.org/10.1186/s42523-023-00229-9, 2023.
Lutz, H. L., Jackson, E. W., Webala, P. W., Babyesiza, W. S., Kerbis Peterhans, J. C., Demos, T. C., Patterson, B. D., and Gilbert, J. A.: Ecology and host identity outweigh evolutionary history in shaping the bat microbiome, mSystems, 4, 10.1128/msystems.00511-19, https://doi.org/10.1128/msystems.00511-19, 2019.
Lutz, H. L., Gilbert, J. A., and Dick, C. W.: Associations between Afrotropical bats, eukaryotic parasites, and microbial symbionts, Mol. Ecol., 31, 1939–1950, https://doi.org/10.1111/mec.16044, 2022.
Man, S. M.: The clinical importance of emerging Campylobacter species, Nat. Rev. Gastro. Hepat., 8, 669–685, https://doi.org/10.1038/nrgastro.2011.191, 2011.
Martin, M.: Cutadapt removes adapter sequences from high-throughput sequencing reads, EMBnet.journal, 17, 10, https://doi.org/10.14806/ej.17.1.200, 2011.
Mascarelli, P. E., Keel, M. K., Yabsley, M., Last, L. A., Breitschwerdt, E. B., and Maggi, R. G.: Hemotropic mycoplasmas in little brown bats (Myotis lucifugus), Parasit. Vector., 7, 117, https://doi.org/10.1186/1756-3305-7-117, 2014.
McMurdie, P. J. and Holmes, S.: phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data, PLoS One, 8, e61217, https://doi.org/10.1371/journal.pone.0061217, 2013.
Mcwilliam, A. N.: Polyoestry and postpartum oestrus in Tadarida (Chaerephon) pumila (Chiroptera: Molossidae) in northern Ghana, West Africa, J. Zool., 213, 735–739, https://doi.org/10.1111/j.1469-7998.1987.tb03738.x, 1987.
Melville, D. W., Meyer, M., Risely, A., Wilhelm, K., Baldwin, H. J., Badu, E. K., Nkrumah, E. E., Oppong, S. K., Schwensow, N., Tschapka, M., Vallo, P., Corman, V. M., Drosten, C., and Sommer, S.: Hibecovirus (genus Betacoronavirus) infection linked to gut microbial dysbiosis in bats, ISME Comm., 5, ycae154, https://doi.org/10.1093/ismeco/ycae154, 2025.
Mendes, P., With, K. A., Signorelli, L., and De Marco, P.: The relative importance of local versus landscape variables on site occupancy in bats of the Brazilian Cerrado, Landscape Ecol., 32, 745–762, https://doi.org/10.1007/s10980-016-0483-6, 2017.
Mettenleiter, T. C., Markotter, W., Charron, D. F., Adisasmito, W. B., Almuhairi, S., Behravesh, C. B., Bilivogui, P., Bukachi, S. A., Casas, N., Becerra, N. C., Chaudhary, A., Zanella, J. R. C., Cunningham, A. A., Dar, O., Debnath, N., Dungu, B., Farag, E., Gao, G. F., Hayman, D. T. S., Khaitsa, M., Koopmans, M. P. G., Machalaba, C., Mackenzie, J. S., Morand, S., Smolenskiy, V., and Zhou, L.: The One Health High-Level Expert Panel (OHHLEP), One Health Outlook, 5, 18, https://doi.org/10.1186/s42522-023-00085-2, 2023.
Millán, J., López-Roig, M., Delicado, V., Serra-Cobo, J., and Esperón, F.: Widespread infection with hemotropic mycoplasmas in bats in Spain, including a hemoplasma closely related to “Candidatus Mycoplasma hemohominis,” Comp. Immunol. Microb., 39, 9–12, https://doi.org/10.1016/j.cimid.2015.01.002, 2015.
Mistrick, J., Kipp, E. J., Weinberg, S. I., Adams, C. C., Larsen, P. A., and Craft, M. E.: Microbiome diversity and zoonotic bacterial pathogen prevalence in Peromyscus mice from agricultural landscapes and synanthropic habitat, Mol. Ecol., 33, e17309, https://doi.org/10.1111/mec.17309, 2024.
Monadjem, A. and Reside, A.: The influence of riparian vegetation on the distribution and abundance of bats in an African savanna, Acta Chiropterol., 10, 339–348, https://doi.org/10.3161/150811008x414917, 2008.
Monadjem, A., Boycott, R. C., Parker, V., and Culverwell, J.: Threatened vertebrates of Swaziland, in: Swaziland red data book: fishes, amphibians, reptiles, birds and mammals, Ministry of Tourism, Environment and Communications, Mbabane, Eswatini, 2003.
Monadjem, A., Taylor, P. J., Cotterill, F. P. D., and Schoeman, M. C.: Bats of Southern and Central Africa: A Biogeographic and Taxonomic Synthesis, Wits University Press, Johannesburg, https://doi.org/10.18772/22020085829, 2020.
Monadjem, A., Simelane, F., Shapiro, J. T., Gumbi, B. C., Mamba, M. L., Sibiya, M. D., Lukhele, S. M., and Mahlaba, T. A. M.: Using species distribution models to gauge the completeness of the bat checklist of Eswatini, Eur. J. Wildlife Res., 67, 1–10, https://doi.org/10.1007/s10344-021-01463-9, 2021.
Mpenyana-Monyatsi, L., Onyango, M. S., and Benteke Momba, M. N.: Groundwater quality in a South African rural community: A possible threat to public health, Pol. J. Environ. Stud., 21, 1349–1358, 2012.
Mtsetfwa, F., McCleery, R. A., and Monadjem, A.: Changes in bat community composition and activity patterns across a conservation-agriculture boundary, Afr. Zool., 53, 99–106, https://doi.org/10.1080/15627020.2018.1531726, 2018.
Muegge, B. D., Kuczynski, J., Knights, D., Clemente, J. C., González, A., Fontana, L., Henrissat, B., Knight, R., and Gordon, J. I.: Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans, Science, 332, 970–974, https://doi.org/10.1126/science.1198719, 2011.
Mühldorfer, K.: Bats and bacterial pathogens: A review, Zoonoses Public Hlth., 60, 93–103, https://doi.org/10.1111/j.1863-2378.2012.01536.x, 2013.
Muhummed, A. M., Lanker, K. C., Yersin, S., Zinsstag, J., and Vonaesch, P.: One Health, One Microbiome, Microbiome, 13, 216, https://doi.org/10.1186/s40168-025-02231-6, 2025.
Müller, J., Mehr, M., Bässler, C., Fenton, M. B., Hothorn, T., Pretzsch, H., Klemmt, H.-J., and Brandl, R.: Aggregative response in bats: Prey abundance versus habitat, Oecologia, 169, 673–684, https://doi.org/10.1007/s00442-011-2247-y, 2012.
Nishida, A. H. and Ochman, H.: Rates of gut microbiome divergence in mammals, Mol. Ecol., 27, 1884–1897, https://doi.org/10.1111/mec.14473, 2018.
Noer, C. L., Dabelsteen, T., Bohmann, K., Monadjem, A., and Monadiem, A.: Molossid bats in an African agro-ecosystem select sugarcane fields as foraging habitat, Afr. Zool., 47, 1–11, https://doi.org/10.3377/004.047.0120, 2012.
Núñez-Montero, K., Santos, A., Quezada-Solís, D., Martínez-Urtaza, J., Lisón, F., and Barrientos, L.: Bacterial communities in fecal samples of Myotis chiloensis from southern Chile, Int. J. Morphol., 39, 57–63, https://doi.org/10.4067/S0717-95022021000100057, 2021.
Oksanen, J., Kindt, R., Legendre, P., O'Hara, B., Henry, M., and Stevens, H.: The vegan package, https://doi.org/10.32614/CRAN.package.vegan, 2007.
Olkkola, S., Rossi, M., Jaakkonen, A., Simola, M., Tikkanen, J., Hakkinen, M., Tuominen, P., Huitu, O., Niemimaa, J., Henttonen, H., and Kivistö, R.: Host-dependent clustering of Campylobacter strains from small mammals in Finland, Front. Microbiol., 11, https://doi.org/10.3389/fmicb.2020.621490, 2021.
Paradis, E., Claude, J., and Strimmer, K.: APE: Analyses of Phylogenetics and Evolution in R language, Bioinformatics, 20, 289–290, https://doi.org/10.1093/bioinformatics/btg412, 2004.
Pekin, B. K. and Pijanowski, B. C.: Global land use intensity and the endangerment status of mammal species, Divers. Distrib., 18, 909–918, https://doi.org/10.1111/j.1472-4642.2012.00928.x, 2012.
Phelps, K. and Kingston, T.: Environmental and biological context modulates the physiological stress response of bats to human disturbance, Oecologia, 188, 41–52, https://doi.org/10.1007/s00442-018-4179-2, 2018.
Phillips, C. D., Phelan, G., Dowd, S. E., McDonough, M. M., Ferguson, A. W., Hanson, J. D., Siles, L., Ordonez-Garza, N., San Francisco, M., and Baker, R. J.: Microbiome analysis among bats describes influences of host phylogeny, life history, physiology and geography, Mol. Ecol., 21, 2617–2627, https://doi.org/10.1111/j.1365-294X.2012.05568.x, 2012.
Popov, I. V., Popov, I. V., Krikunova, A. A., Lipilkina, T. A., Derezina, T. N., Chikindas, M. L., Venema, K., and Ermakov, A. M.: Gut microbiota composition of insectivorous synanthropic and fructivorous zoo bats: A direct metagenomic comparison, Int. J. Mol. Sci., 24, 17301, https://doi.org/10.3390/ijms242417301, 2023.
Prestele, R., Alexander, P., Rounsevell, M. D. A., Arneth, A., Calvin, K., Doelman, J., Eitelberg, D. A., Engström, K., Fujimori, S., Hasegawa, T., Havlik, P., Humpenöder, F., Jain, A. K., Krisztin, T., Kyle, P., Meiyappan, P., Popp, A., Sands, R. D., Schaldach, R., Schüngel, J., Stehfest, E., Tabeau, A., Van Meijl, H., Van Vliet, J., and Verburg, P. H.: Hotspots of uncertainty in land-use and land-cover change projections: a global-scale model comparison., Glob. Change Biol., 22, 3967–3983, https://doi.org/10.1111/gcb.13337, 2016.
Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J., and Glöckner, F. O.: The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools, Nucleic Acids Res., 41, D590–D596, https://doi.org/10.1093/nar/gks1219, 2012.
R Core Team: R: A language and environment for statistical computing, R Foundation for Statistical Computing, Vienna, Austria, https://www.R-project.org/ (last access: 18 September 2026), 2013.
Racey, P. A.: Ageing and assessment of reproductive status of Pipistrelle bats, Pipistrellus pipistrellus, J. Zool., 173, 264–271, https://doi.org/10.1111/j.1469-7998.1974.tb03136.x, 1974.
Racey, P. A.: The ecology of reproduction, in: The ecology of bats, edited by: Kunz, T. H., Plenum Press, New York, 57–104, https://doi.org/10.1007/978-1-4613-3421-7, 1982.
Raulo, A., Bürkner, P. C., Finerty, G. E., Dale, J., Hanski, E., English, H. M., Lamberth, C., Firth, J. A., Coulson, T., and Knowles, S. C. L.: Social and environmental transmission spread different sets of gut microbes in wild mice, Nat. Ecol. Evol. 8, 972–985, https://doi.org/10.1038/s41559-024-02381-0, 2024.
Reeves, W. K., Rogers, T. E., Durden, L. A., and Dasch, G. A.: Association of Bartonella with the fleas (Siphonaptera) of rodents and bats using molecular techniques, J. Vector Ecol., 32, 118–122, https://doi.org/10.3376/1081-1710(2007)32[118:AOBWTF]2.0.CO;2, 2007.
Riopelle, J. C., Shamsaddini, A., Holbrook, M. G., Bohrnsen, E., Zhang, Y., Lovaglio, J., Cordova, K., Hanley, P., Kendall, L. V., Bosio, C. M., Schountz, T., Schwarz, B., Munster, V. J., and Port, J. R.: Sex differences and individual variability in the captive Jamaican fruit bat (Artibeus jamaicensis) intestinal microbiome and metabolome, Sci. Rep.-UK, 14, 3381, https://doi.org/10.1038/s41598-024-53645-5, 2024.
Rothschild, D., Weissbrod, O., Barkan, E., Kurilshikov, A., Korem, T., Zeevi, D., Costea, P. I., Godneva, A., Kalka, I. N., Bar, N., Shilo, S., Lador, D., Vila, A. V., Zmora, N., Pevsner-Fischer, M., Israeli, D., Kosower, N., Malka, G., Wolf, B. C., Avnit-Sagi, T., Lotan-Pompan, M., Weinberger, A., Halpern, Z., Carmi, S., Fu, J., Wijmenga, C., Zhernakova, A., Elinav, E., and Segal, E.: Environment dominates over host genetics in shaping human gut microbiota, Nature, 555, 210–215, https://doi.org/10.1038/nature25973, 2018.
Ruxton, G. D.: The unequal variance t-test is an underused alternative to Student's t-test and the Mann–Whitney U test, Behav. Ecol., 17, 688–690, https://doi.org/10.1093/beheco/ark016, 2006.
Saitou, N. and Nei, M.: The neighbor-joining method: a new method for reconstructing phylogenetic trees, Mol. Biol. Evol., 406–425, https://doi.org/10.1093/oxfordjournals.molbev.a040454, 1987.
Sanders, J. G., Powell, S., Kronauer, D. J. C., Vasconcelos, H. L., Frederickson, M. E., and Pierce, N. E.: Stability and phylogenetic correlation in gut microbiota: Lessons from ants and apes, Mol. Ecol., 23, 1268–1283, https://doi.org/10.1111/mec.12611, 2014.
Schmid, D. W., Fackelmann, G., Wasimuddin, Rakotondranary, J., Ratovonamana, Y. R., Montero, B. K., Ganzhorn, J. U., and Sommer, S.: A framework for testing the impact of co-infections on host gut microbiomes, Anim. Microbiome, 4, https://doi.org/10.1186/s42523-022-00198-5, 2022.
Shao, W., Li, Y., Cheng, X., Guo, L., Wei, L.: Hibernation shifts in gut microbiota composition and metabolic function in the Chinese Horseshoe Bat (Rhinolophus sinicus), Ecol Evol., 16, e73087, https://doi.org/10.1002/ece3.73087, 2026.
Shapiro, J. T.: Update to Mops_pumilus_Gut_microbiomes repository v.2.0, Zenodo [data set] and [code], https://doi.org/10.5281/zenodo.18614739, 2026.
Shapiro, J. T. and Monadjem, A.: Two new bat species for Swaziland and a revised list for the country, Mammalia, 80, 353–357, https://doi.org/10.1515/mammalia-2014-0174, 2016.
Shapiro, J. T., Monadjem, A., Röder, T., and McCleery, R. A.: Response of bat activity to land cover and land use in savannas is scale-, season-, and guild-specific, Biol. Conserv., 241, 108245, https://doi.org/10.1016/j.biocon.2019.108245, 2020.
Shapiro, J. T., Mollerup, S., Jensen, R. H., Olofsson, J. K., Nguyen, N. D., Hansen, T. A., Vinner, L., Monadjem, A., McCleery, R. A., and Hansen, A. J.: Metagenomic analysis reveals previously undescribed bat coronavirus strains in Eswatini, EcoHealth, https://doi.org/10.1007/s10393-021-01567-3, 2021.
Shapiro, J. T., Phelps, K., Racey, P., Vicente, A., Viquez-R, L., Walsh, A., Weinberg, M., and Kingston, T.: IUCN SSC BSG guidelines for field hygiene, Zenodo, https://doi.org/10.5281/zenodo.12169384, 2024.
Siddiqui, R., Maciver, S. K., and Khan, N. A.: Gut microbiome–immune system interaction in reptiles, J. Appl. Microbiol., 132, 2558–2571, https://doi.org/10.1111/jam.15438, 2022.
Simmons, N. B. and Cirranello, A. L.: Bat species of the world: A taxonomic and geographic database. (1.9), https://batnames.org (last access: 18 September 2026), 2025.
Song, X.-P., Hansen, M. C., Stehman, S. V., Potapov, P. V., Tyukavina, A., Vermote, E. F., and Townshend, J. R.: Global land change 1982–2016, Nature, 560, 639–643, https://doi.org/10.1038/s41586-018-0411-9, 2018.
Speakman, J. R. and Racey, P. A.: The influence of body condition on sexual development of male Brown long-eared bats (Plecotus auratus) in the wild, J. Zool., 210, 515–525, https://doi.org/10.1111/j.1469-7998.1986.tb03653.x, 1986.
Steenkamp, Y., Van Wyk, B., Victor, J., Hoare, D., Smith, G. F., Dold, T., and Cowling, R. M.: Maputaland-Pondoland-Albany, in: Hotspots Revisited: Earth's biologically richest and most endangered terrestrial ecoregions, edited by: Mittermeier, R. A., Robles Gil, P., Hoffman, M., Pilgrim, J., Brooks, T., Goettsch Mittermeier, C., Lamoreux, J., and Da Fonseca, G. A. B., Chicago, 219–228, ISBN: 968-6397-77-9, 2005.
Storm, M. B., Arfaoui, E. M. R., Simelane, P., Denlinger, J., Dias, C. A., da Conceição, A. G., Monadjem, A., Bohmann, K., Poulsen, M., and Bodawatta, K. H.: Diet components associated with specific bacterial taxa shape overall gut community compositions in omnivorous African viverrids, Ecol. Evol., 14, e11486, https://doi.org/10.1002/ece3.11486, 2024.
Stuckey, M. J., Chomel, B. B., de Fleurieu, E. C., Aguilar-Setién, A., Boulouis, H.-J., and Chang, C.: Bartonella, bats and bugs: A review, Comp. Immunol. Microb., 55, 20–29, https://doi.org/10.1016/j.cimid.2017.09.001, 2017.
Suzuki, T. A.: Links between natural variation in the microbiome and host fitness in wild mammals, Integr. Comp. Biol., 57, 756–769, https://doi.org/10.1093/icb/icx104, 2017.
Swartz, E., Weier, S., Pretorius, M., and Keith, M.: Natural vegetation edges promote bat activity in macadamia orchards in northeastern South Africa, Afr. J. Wildl. Res., 52, https://doi.org/10.3957/056.052.0155, 2022.
Szentivanyi, T., McKee, C., Jones, G., and Foster, J. T.: Trends in bacterial pathogens of bats: Global distribution and knowledge gaps, Transbound. Emerg. Dis., 2023, 9285855, https://doi.org/10.1155/2023/9285855, 2023.
Tanalgo, K. C., Dela Cruz, K. C., and Russo, D.: Susceptibility of bats to ecological and evolutionary traps, Biol. Conserv., 305, 111110, https://doi.org/10.1016/j.biocon.2025.111110, 2025.
Tardy, F., Baranowski, E., Nouvel, L.-X., Mick, V., Manso-Silvàn, L., Thiaucourt, F., Thébault, P., Breton, M., Sirand-Pugnet, P., Blanchard, A., Garnier, A., Gibert, P., Game, Y., Poumarat, F., and Citti, C.: Emergence of atypical Mycoplasma agalactiae strains harboring a new prophage and associated with an alpine wild ungulate mortality episode, Appl. Environ. Microb., 78, 4659–4668, https://doi.org/10.1128/AEM.00332-12, 2012.
Thompson, J. D., Higgins, D. G., and Gibson, T. J.: CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice, Nucleic Acids Res., 22, 4673–4680, https://doi.org/10.1093/nar/22.22.4673, 1994.
Tompa, E., Jaenson, T. G. T., and Wilhelmsson, P.: First records of possibly human pathogenic Rickettsia species in bat ticks, Carios vespertilionis, in Sweden, Microorganisms, 11, 357, https://doi.org/10.3390/microorganisms11020357, 2023.
Trevelline, B. K., Fontaine, S. S., Hartup, B. K., and Kohl, K. D.: Conservation biology needs a microbial renaissance: A call for the consideration of host-associated microbiota in wildlife management practices, Proc. R. Soc. B, 286, 20182448, https://doi.org/10.1098/rspb.2018.2448, 2019.
Tscharntke, T., Tylianakis, J. M., Rand, T. A., Didham, R. K., Fahrig, L., Batáry, P., Bengtsson, J., Clough, Y., Crist, T. O., Dormann, C. F., Ewers, R. M., Fründ, J., Holt, R. D., Holzschuh, A., Klein, A. M., Kleijn, D., Kremen, C., Landis, D. A., Laurance, W., Lindenmayer, D., Scherber, C., Sodhi, N., Steffan-Dewenter, I., Thies, C., Van Der Putten, W. H., and Westphal, C.: Landscape moderation of biodiversity patterns and processes – eight hypotheses, Biol. Rev., 87, 661–685, https://doi.org/10.1111/j.1469-185X.2011.00216.x, 2012.
Turnbaugh, P. J., Ley, R. E., Hamady, M., Fraser-Liggett, C. M., Knight, R., and Gordon, J. I.: The Human Microbiome Project, Nature, 449, 804–810, https://doi.org/10.1038/nature06244, 2007.
VanDerWal, J., Falconi, L., Januchowski, S., Shoo, L., and Storlie, C.: Package “SDMTools,” https://cran.r-project.org/src/contrib/Archive/SDMTools/ (last access: 18 September 2026), 2014.
Vavrek, M. J.: fossil: Palaeoecological and palaeogeographical analysis tools, Palaeontol. Electron., 14, 1T, https://palaeo-electronica.org/2011_1/238/index.html (last access: 18 September 2026), 2011.
Veikkolainen, V., Vesterinen, E. J., Lilley, T. M., and Pulliainen, A. T.: Bats as reservoir hosts of human bacterial pathogen, Bartonella mayotimonensis, Emerg. Infect. Dis., 20, 960–967, https://doi.org/10.3201/eid2006.130956, 2014.
Vengust, M., Knapic, T., and Weese, J. S.: The fecal bacterial microbiota of bats; Slovenia, PLoS One, 13, e0196728, https://doi.org/10.1371/journal.pone.0196728, 2018.
Vincenty, T.: Direct and inverse solutions of geodesics on the ellipsoid with application of nested equations, Surv. Rev., 23, 88–93, https://doi.org/10.1179/sre.1975.23.176.88, 1975.
Víquez-R, L., Speer, K., Wilhelm, K., Simmons, N., Medellín, R. A., Sommer. S., and Tschapka, M.: A faithful gut: Core features of gastrointestinal microbiota of long-distance migratory bats remain stable despite dietary shifts driving differences in specific bacterial taxa, Microbiol. Spectr., 9, e01525-21, https://doi.org/10.1128/Spectrum.01525-21, 2021.
Volokhov, D. V., Lock, L. R., Dyer, K. E., DeAnglis, I. K., Andrews, B. R., Simonis, M. C., Stockmaier, S., Carter, G. G., Downs, C. J., Fenton, M. B., Simmons, N. B., and Becker, D. J.: Expanded diversity of novel hemoplasmas in rare and undersampled Neotropical bats, One Health, 17, 100633, https://doi.org/10.1016/j.onehlt.2023.100633, 2023.
Wang, R., Li, Z.-M., Peng, Q.-M., Gu, X.-L., Zhou, C.-M., Xiao, X., Han, H.-J., and Yu, X.-J.: High prevalence and genetic diversity of hemoplasmas in bats and bat ectoparasites from China, One Health, 16, 100498, https://doi.org/10.1016/j.onehlt.2023.100498, 2023.
Warne, R. W., Kirschman, L., and Zeglin, L.: 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, 2019.
Wasimuddin, Brändel, S. D., Tschapka, M., Page, R., Rasche, A., Corman, V. M., Drosten, C., and Sommer, S.: Astrovirus infections induce age-dependent dysbiosis in gut microbiomes of bats, ISME J., 12, 2883–2893, https://doi.org/10.1038/s41396-018-0239-1, 2018.
Weier, S. M., Grass, I., Linden, V. M. G., Tscharntke, T., and Taylor, P. J.: Natural vegetation and bug abundance promote insectivorous bat activity in macadamia orchards, South Africa, Biol. Conserv., 226, 16–23, https://doi.org/10.1016/J.BIOCON.2018.07.017, 2018.
Weier, S. M., Linden, V. M. G., Hammer, A., Grass, I., Tscharntke, T., and Taylor, P. J.: Bat guilds respond differently to habitat loss and fragmentation at different scales in macadamia orchards in South Africa, Agr. Ecosyst. Environ., 320, 107588, https://doi.org/10.1016/j.agee.2021.107588, 2021.
Weinberg, M., Mazar, O., Rachum, A., Chen, X., Goutink, S., Lifshitz, N., Winter-Livneh, R., Czirják, G. Á. and Yovel, Y.: Seasonal challenges of tropical bats in temperate zones, Sci. Rep.-UK, 12, 16869, https://doi.org/10.1038/s41598-022-21076-9, 2022.
Weinberg, M., Knazovicka, D., Pelgrims, R., Taskaya, I., Sinkovec, P., Víquez-R, L., Phelps, K., Walsh, A., Racey, PA., Kingston, T., and Shapiro, J. T.: Case report of unusual mortality of Egyptian fruit bat (Rousettus aegyptiacus) in northern Cyprus, bioRxiv [preprint], https://doi.org/10.64898/2026.06.08.730983, 2026.
Weinert, L. A., Werren, J. H., Aebi, A., Stone, G. N., and Jiggins, F. M.: Evolution and diversity of Rickettsia bacteria, BMC Biol., 7, 6, https://doi.org/10.1186/1741-7007-7-6, 2009.
Welch, B. L.: The generalization of “Student's” problem when several different population variances are involved, Biometrika, 34, 28–35, https://doi.org/10.1093/biomet/34.1-2.28, 1947.
Weldon, L., Abolins, S., Lenzi, L., Bourne, C., Riley, E. M., and Viney, M.: The Gut Microbiota of Wild Mice, PLoS One, 10, e0134643, https://doi.org/10.1371/journal.pone.0134643, 2015.
Wickham, H.: ggplot2: Elegant graphics for data analysis, https://ggplot2.tidyverse.org (last access: 18 September 2026), 2016.
Willerslev, E., Davison, J., Moora, M., Zobel, M., Coissac, E., Edwards, M. E., Lorenzen, E. D., Vestergård, M., Gussarova, G., Haile, J., Craine, J., Gielly, L., Boessenkool, S., Epp, L. S., Pearman, P. B., Cheddadi, R., Murray, D., Bråthen, K. A., Yoccoz, N., Binney, H., Cruaud, C., Wincker, P., Goslar, T., Alsos, I. G., Bellemain, E., Brysting, A. K., Elven, R., Sønstebø, J. H., Murton, J., Sher, A., Rasmussen, M., Rønn, R., Mourier, T., Cooper, A., Austin, J., Möller, P., Froese, D., Zazula, G., Pompanon, F., Rioux, D., Niderkorn, V., Tikhonov, A., Savvinov, G., Roberts, R. G., MacPhee, R. D. E., Gilbert, M. T. P., Kjær, K. H., Orlando, L., Brochmann, C., and Taberlet, P.: Fifty thousand years of Arctic vegetation and megafaunal diet, Nature, 506, 47–51, https://doi.org/10.1038/nature12921, 2014.
Williams, C. E., Hammer, T. J., and Williams, C. L.: Diversity alone does not reliably indicate the healthiness of an animal microbiome, ISME J., 18, wrae133, https://doi.org/10.1093/ismejo/wrae133, 2024.
Worsley, S. F., Davies, C. S., Mannarelli, M.-E., Hutchings, M. I., Komdeur, J., Burke, T., Dugdale, H. L., and Richardson, D. S.: Gut microbiome composition, not alpha diversity, is associated with survival in a natural vertebrate population, Anim. Microbiome, 3, 84, https://doi.org/10.1186/s42523-021-00149-6, 2021.
Wu, Z., Yang, L., Ren, X., He, G., Zhang, J., Yang, J., Qian, Z., Dong, J., Sun, L., Zhu, Y., Du, J., Yang, F., Zhang, S., and Jin, Q.: Deciphering the bat virome catalog to better understand the ecological diversity of bat viruses and the bat origin of emerging infectious diseases, ISME J., 10, 609–620, https://doi.org/10.1038/ismej.2015.138, 2016.
Wulder, M. A., Coops, N. C., Roy, D. P., White, J. C., and Hermosilla, T.: Land cover 2.0, Int. J. Remote Sens., 39, 4254–4284, https://doi.org/10.1080/01431161.2018.1452075, 2018.
Xiao, G., Liu, S., Xiao, Y., Zhu, Y., Zhao, H., Li, A., Li, Z., and Feng, J.: Seasonal changes in gut microbiota diversity and composition in the Greater Horseshoe Bat, Front. Microbiol., 10, 2247, https://doi.org/10.3389/fmicb.2019.02247, 2019.
Xiong, R., Li, J., Wang, K., Kong, H., Dai, Z., Wang, Y., and Zheng, R.: Seasonal dietary changes drive adaptive responses in the gut microbiota and function of Myotis chinensis, Ecol. Evol., 16, e73281, https://doi.org/10.1002/ece3.73281, 2026.
Zhao, S., Yang, M., Liu, G., Hornok, S., Zhao, S., Sang, C., Tan, W., and Wang, Y.: Rickettsiae in the common pipistrelle Pipistrellus pipistrellus (Chiroptera: Vespertilionidae) and the bat soft tick Argas vespertilionis (Ixodida: Argasidae), Parasit. Vector., 13, 10, https://doi.org/10.1186/s13071-020-3885-x, 2020.
Zilber-Rosenberg, I. and Rosenberg, E.: Role of microorganisms in the evolution of animals and plants: The hologenome theory of evolution, FEMS Microbiol. Rev., 32, 723–735, https://doi.org/10.1111/j.1574-6976.2008.00123.x, 2008.
Short summary
The gut microbiome (microorganisms in the digestive tract) is important for the health of wildlife but may be impacted by human-caused disturbance, such as land cover change. Using genetic sequences of bacteria, we found that the gut microbiomes of the little free-tail bat (Mops pumilus) in Eswatini were highly individual and may have potential pathogens but did not appear to be influenced by land cover.
The gut microbiome (microorganisms in the digestive tract) is important for the health of...