1887

Abstract

Antimicrobial-resistant , particularly those resistant to critically important antimicrobials, are increasingly reported in wildlife. The dissemination of antimicrobial-resistant bacteria to wildlife indicates the far-reaching impact of selective pressures imposed by humans on bacteria through misuse of antimicrobials. The grey-headed flying fox (GHFF; ), a fruit bat endemic to eastern Australia, commonly inhabits urban environments and encounters human microbial pollution. To determine if GHFF have acquired human-associated bacteria, faecal samples from wild GHFF (287) and captive GHFF undergoing rehabilitation following illness or injury (31) were cultured to detect beta-lactam-resistant . Antimicrobial susceptibility testing, PCR and whole genome sequencing were used to determine phenotypic and genotypic antimicrobial resistance profiles, strain type and virulence factor profiles. Overall, 3.8 % of GHFF carried amoxicillin-resistant (wild 3.5 % and captive 6.5 %), with 38.5 % of the 13 GHFF isolates exhibiting multidrug resistance. Carbapenem ( ) and fluoroquinolone resistance were detected in one isolate, and two isolates were resistant to third-generation cephalosporins ( and ). Resistance to tetracycline and trimethoprim plus sulfamethoxazole were detected in 69.2% and 30.8 % of isolates respectively. Class 1 integrons, a genetic determinant of resistance, were detected in 38.5 % of isolates. Nine of the GHFF isolates (69.2 %) harboured extraintestinal virulence factors. Phylogenetic analysis placed the 13 GHFF isolates in lineages associated with humans and/or domestic animals. Three isolates were human-associated extraintestinal pathogenic (ST10 O89:H9, ST73 and ST394) and seven isolates belonged to lineages associated with extraintestinal disease in both humans and domestic animals (ST88, ST117, ST131, ST155 complex, ST398 and ST1850). This study provides evidence of anthropogenic multidrug-resistant and pathogenic transmission to wildlife, further demonstrating the necessity for incorporating wildlife surveillance within the One Health approach to managing antimicrobial resistance.

Funding
This study was supported by the:
  • Lake Macquarie City Council (Award Environmental Research Grant)
    • Principle Award Recipient: MichellePower
  • Holsworth Wildlife Research Endowment (Award to Fiona McDougall)
    • Principle Award Recipient: FionaMcDougall
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2024-12-08
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References

  1. Manges AR, Johnson JR, Foxman B, O'Bryan TT, Fullerton KE et al. Widespread distribution of urinary tract infections caused by a multidrug-resistant Escherichia coli clonal group. New Engl J Med 2001; 345:1007–1013
    [Google Scholar]
  2. Petty NK, Zakour NLB, Stanton-Cook M, Skippington E, Totsika M et al. Global dissemination of a multidrug resistant Escherichia coli clone. Proc Natl Acad Sci 2014; 111:5694–5699
    [Google Scholar]
  3. WHO 2019; Critically important antimicrobials for human medicine, 6th revision 2018. World health organisation (WHO). https://apps.who.int/iris/bitstream/handle/10665/312266/9789241515528-eng.pdf?ua=1.30 September 2020
  4. OIE 2018; OIE list of antimicrobial agents of veterinary importance. the world organisation for animal health (OIE). https://www.oie.int/fileadmin/Home/eng/Our_scientific_expertise/docs/pdf/AMR/A_OIE_List_antimicrobials_July2019.pdf30 September 2020
  5. Partridge SR, Kwong SM, Firth N, Jensen SO. Mobile genetic elements associated with antimicrobial resistance. Clin Microbiol Rev 2018; 31:
    [Google Scholar]
  6. Stokes HW, Gillings MR. Gene flow, mobile genetic elements and the recruitment of antibiotic resistance genes into gram-negative pathogens. FEMS Microbiol Rev 2011; 35:790–819
    [Google Scholar]
  7. Hall RM, Collis CM. Mobile gene cassettes and integrons: capture and spread of genes by site‐specific recombination. Mol Microbiol 1995; 15:593–600
    [Google Scholar]
  8. Kaper JB, Nataro JP, Mobley HL. Pathogenic Escherichia coli. Nat Rev Microbiol 2004; 2:123–140
    [Google Scholar]
  9. Köhler C-D, Dobrindt U. What defines extraintestinal pathogenic Escherichia coli?. Int J Med Microbiol 2011; 301:642–647
    [Google Scholar]
  10. Wirth T, Falush D, Lan R, Colles F, Mensa P et al. Sex and virulence in Escherichia coli: an evolutionary perspective. Mol Microbiol 2006; 60:1136–1151
    [Google Scholar]
  11. Riley L. Pandemic lineages of extraintestinal pathogenic Escherichia coli. Clin Microbiol Infect 2014; 20:380–390
    [Google Scholar]
  12. Skjøt-Rasmussen L, Olsen S, Jakobsen L, Ejrnaes K, Scheutz F et al. Escherichia coli clonal group A causing bacteraemia of urinary tract origin. Clin Microbiol Infect 2013; 19:656–661
    [Google Scholar]
  13. Nicolas-Chanoine M-H, Bertrand X, Madec J-Y. Escherichia coli ST131, an intriguing clonal group. Clin Microbiol Rev 2014; 27:543–574
    [Google Scholar]
  14. Alhashash F, Wang X, Paszkiewicz K, Diggle M, Zong Z et al. Increase in bacteraemia cases in the East Midlands region of the UK due to MDR Escherichia coli ST73: high levels of genomic and plasmid diversity in causative isolates. J Antimicrob Chemother 2016; 71:339–343
    [Google Scholar]
  15. P-L H, Lo W-U LEL, Law PY, Leung SM, Wang Y. Clonal diversity of CTX-M-producing, multidrug-resistant Escherichia coli from rodents. J Med Microbiol 2015; 64:185–190
    [Google Scholar]
  16. Hasan B, Olsen B, Alam A, Akter L, Å M. Dissemination of the multidrug-resistant extended-spectrum β-lactamase-producing Escherichia coli O25b-ST131 clone and the role of house crow (Corvus splendens) foraging on hospital waste in Bangladesh. Clin Microbiol Infect 2015; 21:1000. e1–e4
    [Google Scholar]
  17. Mora A, García-Peña FJ, Alonso MP, Pedraza-Diaz S, Ortega-Mora LM et al. Impact of human-associated Escherichia coli clonal groups in Antarctic pinnipeds: presence of ST73, ST95, ST141 and ST131. Sci Rep 2018; 8:1–11
    [Google Scholar]
  18. Mukerji S, Stegger M, Truswell AV, Laird T, Jordan D et al. Resistance to critically important antimicrobials in Australian silver gulls (Chroicocephalus novaehollandiae) and evidence of anthropogenic origins. J Antimicrob Chemother 2019; 74:2566–2574
    [Google Scholar]
  19. Guenther S, Ewers C, Wieler LH. Extended-spectrum beta-lactamases producing E. coli in wildlife yet another form of environmental pollution?. Front Microbiol 2011; 2:
    [Google Scholar]
  20. Dolejska M, Masarikova M, Dobiasova H, Jamborova I, Karpiskova R et al. High prevalence of Salmonella and IMP-4-producing Enterobacteriaceae in the silver gull on Five Islands, Australia. J Antimicrob Chemother 2016; 71:63–70
    [Google Scholar]
  21. Skurnik D, Ruimy R, Andremont A, Amorin C, Rouquet P et al. Effect of human vicinity on antimicrobial resistance and integrons in animal faecal Escherichia coli. J Antimicrob Chemother 2006; 57:1215–1219
    [Google Scholar]
  22. Kinjo T, Minamoto N, Sugiyama M, Sugiyama Y. Comparison of antimicrobial resistant Escherichia coli in wild and captive Japanese serows. J Vet Med Sci 1992; 54:821–827
    [Google Scholar]
  23. Blyton MD, Pi H, Vangchhia B, Abraham S, Trott DJ et al. Genetic structure and antimicrobial resistance of Escherichia coli and cryptic clades in birds with diverse human associations. Appl Environ Microbiol 2015; 81:5123–5133
    [Google Scholar]
  24. SS M, Urdahl AM, Madslien K, Sunde M, Nesse LL et al. What does the Fox say? monitoring antimicrobial resistance in the environment using wild red foxes as an indicator. PLoS One. 2018; 13:
    [Google Scholar]
  25. Wang J, Ma Z-B ZZ-L, Yang X-W, Huang Y, Liu J-H. The role of wildlife (wild birds) in the global transmission of antimicrobial resistance genes. Zool Res 2017; 38:55
    [Google Scholar]
  26. Cooper LN, Cretekos CJ, Sears KE. The evolution and development of mammalian flight. Wiley Interdiscip Rev Dev Biol 2012; 1:773–779
    [Google Scholar]
  27. Tidemann CR, Nelson JE. Long-distance movements of the grey-headed flying fox (Pteropus poliocephalus). J Zool 2004; 263:141–146
    [Google Scholar]
  28. Welbergen JA, Meade J, Field HE, Edson D, McMichael L et al. Extreme mobility of the world’s largest flying mammals creates key challenges for management and conservation. BMC Biol 2020; 18:1–13
    [Google Scholar]
  29. Burgin CJ, Colella JP, Kahn PL, Upham NS. How many species of mammals are there?. J Mammal 2018; 99:1–14
    [Google Scholar]
  30. Teeling EC, Springer MS, Madsen O, Bates P, O'brien SJ et al. A molecular phylogeny for bats illuminates biogeography and the fossil record. Science 2005; 307:580–584
    [Google Scholar]
  31. Iovine RD, Dejuste C, Miranda F, Filoni C, Bueno MG et al. Isolation of Escherichia coli and Salmonella spp. from free-ranging wild animals. Braz J Microbiol 2015; 46:1257–1263
    [Google Scholar]
  32. Pinus M, Müller H. Enterobacteria of bats (Chiroptera). Zentralbl Bakteriol A 1980; 247:315–322
    [Google Scholar]
  33. Nowak K, Fahr J, Weber N, Lübke-Becker A, Semmler T et al. Highly diverse and antimicrobial susceptible Escherichia coli display a naïve bacterial population in fruit bats from the Republic of Congo. PLoS One 2017; 12:e0178146
    [Google Scholar]
  34. Klite P. Intestinal bacterial flora and transit time of three Neotropical bat species. J Bacteriol 1965; 90:375–379
    [Google Scholar]
  35. Moreno G, Lopes C, Seabra E, Pavan C, Correa A. Bacteriological study of the intestinal flora of bats (Desmodus rotundus). Arq Inst Biol 1975; 42:229–232
    [Google Scholar]
  36. Heard DJ, De Young JL, Goodyear B, Ellis GA. Comparative rectal bacterial flora of four species of flying fox (Pteropus sp. J Zoo Wildl Med 1997; 28:471–475
    [Google Scholar]
  37. Benavides J, Shiva C, Virhuez M, Tello C, Appelgren A et al. Extended‐spectrum beta‐lactamase‐producing Escherichia coli in common vampire bats Desmodus rotundus and livestock in Peru. Zoonoses Publ Health 2018
    [Google Scholar]
  38. Nowakiewicz A, Zięba P, Gnat S, Trościańczyk A, Osińska M et al. Bats as a reservoir of resistant Escherichia coli: A methodical view. Can we fully estimate the scale of resistance in the reservoirs of free-living animals? Res Vet Sci 2020; 128:49–58
    [Google Scholar]
  39. Garcês A, Correia S, Amorim F, Pereira JE, Igrejas G et al. First report on extended-spectrum beta-lactamase (ESBL) producing Escherichia coli from European free-tailed bats (Tadarida teniotis) in Portugal: A one-health approach of a hidden contamination problem. J Hazard Mater 2019; 370:219–224
    [Google Scholar]
  40. Nguema M, Philippe P, Onanga R, Atome N, Roger G et al. Characterization of ESBL-producing enterobacteria from fruit bats in an unprotected area of Makokou, Gabon. Microorg 2020; 8:138
    [Google Scholar]
  41. Oluduro AO. Antibiotic-resistant commensal Escherichia coli in faecal droplets from bats and poultry in Nigeria. Vet Ital 2012; 48:297–308
    [Google Scholar]
  42. Graves S, Kennelly-Merrit S, Tidemann C, Rawlinson P, Harvey K et al. Antibiotic-Resistance patterns of enteric bacteria of wild mammals on the Krakatau islands and West Java, Indonesia. Philos Trans R Soc Lond B Biol Sci 1988; 322:339–353
    [Google Scholar]
  43. Parry‐Jones K, Augee M. Factors affecting the occupation of a colony site in Sydney, New South Wales by the Grey‐headed Flying‐fox Pteropus poliocephalus (Pteropodidae). Austral Ecol 2001; 26:47–55
    [Google Scholar]
  44. Currey K, Kendal D, Van der Ree R, Lentini PE. Land manager perspectives on conflict mitigation strategies for urban flying-fox camps. Divers 2018; 10:39
    [Google Scholar]
  45. McDougall F, Boardman W, Gillings M, Power M. Bats as reservoirs of antibiotic resistance determinants: A survey of class 1 integrons in Grey-headed Flying Foxes (Pteropus poliocephalus). Infect Genet Evol 2019; 70:107–113
    [Google Scholar]
  46. Matuschek E, Brown DF, Kahlmeter G. Development of the EUCAST disk diffusion antimicrobial susceptibility testing method and its implementation in routine microbiology laboratories. Clin Microbiol Infect 2014; 20:O255–O66
    [Google Scholar]
  47. Magiorakos AP, Srinivasan A, Carey R, Carmeli Y, Falagas M et al. Multidrug‐resistant, extensively drug‐resistant and pandrug‐resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect 2012; 18:268–281
    [Google Scholar]
  48. Dawes FE, Kuzevski A, Bettelheim KA, Hornitzky MA, Djordjevic SP et al. Distribution of class 1 integrons with IS26-mediated deletions in their 3′-conserved segments in Escherichia coli of human and animal origin. PLoS One 2010; 5:e12754
    [Google Scholar]
  49. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477
    [Google Scholar]
  50. Zankari E, Hasman H, Cosentino S, Vestergaard M, Rasmussen S et al. Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother 2012; 67:2640–2644
    [Google Scholar]
  51. Beghain J, Bridier-Nahmias A, Le Nagard H, Denamur E, Clermont O. ClermonTyping: an easy-to-use and accurate in silico method for Escherichia genus strain phylotyping. Microb Genomics 2018; 4:
    [Google Scholar]
  52. Roer L, Tchesnokova V, Allesøe R, Muradova M, Chattopadhyay S et al. Development of a web tool for Escherichia coli subtyping based on fimH alleles. J Clin Microbiol 2017; 55:2538–2543
    [Google Scholar]
  53. Zhou Z, Alikhan N-F, Mohamed K, Fan Y, Achtman M et al. The EnteroBase user’s guide, with case studies on Salmonella transmissions, Yersinia pestis phylogeny, and Escherichia core genomic diversity. Genome Res 2020; 30:138–152
    [Google Scholar]
  54. Joensen KG, Scheutz F, Lund O, Hasman H, Kaas RS et al. Real-time whole-genome sequencing for routine typing, surveillance, and outbreak detection of verotoxigenic Escherichia coli. J Clin Microbiol 2014; 52:1501–1510
    [Google Scholar]
  55. Chen L, Zheng D, Liu B, Yang J, VFDB JQ. 2016: hierarchical and refined dataset for big data analysis—10 years on. Nucleic Acids Res 2016; 44:D694–D7
    [Google Scholar]
  56. Johnson JR, Kuskowski MA, Owens K, Gajewski A, Winokur PL. Phylogenetic origin and virulence genotype in relation to resistance to fluoroquinolones and/or extended-spectrum cephalosporins and cephamycins among Escherichia coli isolates from animals and humans. J Infect Dis 2003; 188:759–768
    [Google Scholar]
  57. Pitout J. Extraintestinal pathogenic Escherichia coli: a combination of virulence with antibiotic resistance. Front Microbiol 2012; 3:9
    [Google Scholar]
  58. Zakour NLB, Alsheikh-Hussain AS, Ashcroft MM, NTK N, Roberts LW et al. Sequential acquisition of virulence and fluoroquinolone resistance has shaped the evolution of Escherichia coli ST131. MBio 2016; 7:
    [Google Scholar]
  59. Carattoli A, Zankari E, García-Fernández A, Larsen MV, Lund O et al. In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob Agents Chemother 2014; 58:3895–3903
    [Google Scholar]
  60. Zhou Z, Alikhan N-F, Sergeant MJ, Luhmann N, Vaz C et al. GrapeTree: visualization of core genomic relationships among 100,000 bacterial pathogens. Genome Res 2018; 28:1395–1404
    [Google Scholar]
  61. Argimón S, Masim MA, Gayeta JM, Lagrada ML, Macaranas PK et al. Integrating whole-genome sequencing within the National antimicrobial resistance surveillance program in the Philippines. Nature Comm 2020; 11:1–15
    [Google Scholar]
  62. WHO 2017; Global priority list of antibiotic-resistant bacteria to guide research, discovery, and developmentof new antibiotics. World health organisation (who). https://www.who.int/medicines/publications/WHO-PPL-Short_Summary_25Feb-ET_NM_WHO.pdf?ua=130 September 2020
  63. Sherley M, Gordon DM, Collignon PJ. Variations in antibiotic resistance profile in Enterobacteriaceae isolated from wild Australian mammals. Environ Microbiol 2000; 2:620–631
    [Google Scholar]
  64. Abraham S, Jordan D, Wong HS, Johnson JR, Toleman MA et al. First detection of extended-spectrum cephalosporin-and fluoroquinolone-resistant Escherichia coli in Australian food-producing animals. J Glob Antimicrob Resist 2015; 3:273–277
    [Google Scholar]
  65. Kidsley AK, Abraham S, Bell JM, O'Dea M, Laird TJ et al. Antimicrobial susceptibility of Escherichia coli and Salmonella spp. isolates from healthy pigs in Australia: results of a pilot national survey. Front Microbiol 2018; 9:1207
    [Google Scholar]
  66. Hornsey M, Phee L, Wareham DW. A novel variant, NDM-5, of the New Delhi metallo-β-lactamase in a multidrug-resistant Escherichia coli ST648 isolate recovered from a patient in the United Kingdom. Antimicrob Agents Chemother 2011; 55:5952–5954
    [Google Scholar]
  67. Wailan AM, Paterson DL, Kennedy K, Ingram PR, Bursle E et al. Genomic characteristics of NDM-producing Enterobacteriaceae isolates in Australia and their blaNDM genetic contexts. Antimicrob Agents Chemother 2016; 60:136–141
    [Google Scholar]
  68. Yaici L, Haenni M, Saras E, Boudehouche W, Touati A et al. blaNDM-5-carrying IncX3 plasmid in Escherichia coli ST1284 isolated from raw milk collected in a dairy farm in Algeria. J Antimicrob Chemother 2016; 71:2671–2672
    [Google Scholar]
  69. Yousfi M, Mairi A, Bakour S, Touati A, Hassissen L et al. First report of NDM-5-producing Escherichia coli ST1284 isolated from dog in Bejaia, Algeria. New Microbes New Infect 2015; 8:17
    [Google Scholar]
  70. Hong JS, Song W, Park H-M, J-Y O, Chae J-C et al. First detection of New Delhi metallo-β-Lactamase-5-producing Escherichia coli from companion animals in Korea. Microb Drug Resist 2019; 25:344–349
    [Google Scholar]
  71. Saputra S, Jordan D, Mitchell T, San Wong H, Abraham RJ et al. Antimicrobial resistance in clinical Escherichia coli isolated from companion animals in Australia. Vet Microbiol 2017; 211:43–50
    [Google Scholar]
  72. Kidsley AK, White RT, Beatson SA, Saputra S, Schembri MA et al. Companion animals are spillover hosts of the multidrug-resistant human extraintestinal Escherichia coli pandemic clones ST131 and ST1193. Front Microbiol 2020; 11:1968
    [Google Scholar]
  73. Rusdi B, Laird T, Abraham R, Ash A, Robertson ID et al. Carriage of critically important antimicrobial resistant bacteria and zoonotic parasites amongst cAMP dogs in remote Western Australian Indigenous communities. Sci Rep 2018; 8:1–8
    [Google Scholar]
  74. Gharout-Sait A, Touati A, Ahmim M, Brasme L, Guillard T et al. Occurrence of carbapenemase-producing Klebsiella pneumoniae in bat guano. Microb Drug Resist 2019; 25:1057–1062
    [Google Scholar]
  75. Hastak P, Cummins ML, Gottlieb T, Cheong E, Merlino J et al. Genomic profiling of Escherichia coli isolates from bacteraemia patients: a 3-year cohort study of isolates collected at a Sydney teaching hospital. Microb Genomics 2020; 6:e000371
    [Google Scholar]
  76. Reid CJ, Wyrsch ER, Chowdhury PR, Zingali T, Liu M et al. Porcine commensal Escherichia coli: a reservoir for class 1 integrons associated with IS26. Microb Genomics 2017; 3:
    [Google Scholar]
  77. Bogema D, McKinnon J, Liu M, Hitchick N, Miller N et al. Whole-genome analysis of extraintestinal Escherichia coli sequence type 73 from a single hospital over a 2 year period identified different circulating clonal groups. Microb Genomics 2020; 6:e000255
    [Google Scholar]
  78. Wallace-Gadsden F, Johnson JR, Wain J, Okeke IN. Enteroaggregative Escherichia coli related to uropathogenic clonal group A. Emerg Infect Dis 2007; 13:757
    [Google Scholar]
  79. Krieger JN, Thumbikat P. 7 Bacterial prostatitis: bacterial virulence, clinical outcomes, and new directions. In Mulvey MA, Klumpp D, Stapleton AE. (editors) Urinary Tract Infections: Molecular Pathogenesis and Clinical Management Washington (DC): ASM Press; 2017 pp 121–134
    [Google Scholar]
  80. Manges AR, Geum HM, Guo A, Edens TJ, Fibke CD et al. Global extraintestinal pathogenic Escherichia coli (ExPEC) lineages. Clin Microbiol Rev 2019; 32:
    [Google Scholar]
  81. Maluta RP, Logue CM, Casas MRT, Meng T, Guastalli EAL et al. Overlapped sequence types (STs) and serogroups of avian pathogenic (APEC) and human extra-intestinal pathogenic (ExPEC) Escherichia coli isolated in Brazil. PLoS One 2014; 9:e105016
    [Google Scholar]
  82. Manges A. Escherichia coli and urinary tract infections: the role of poultry-meat. Clin Microbiol Infect 2016; 22:122–129
    [Google Scholar]
  83. Manges AR, Harel J, Masson L, Edens TJ, Portt A et al. Multilocus sequence typing and virulence gene profiles associated with Escherichia coli from human and animal sources. Foodborne Pathog Dis 2015; 12:302–310
    [Google Scholar]
  84. Cummins ML, Reid CJ, Chowdhury PR, Bushell RN, Esbert N et al. Whole genome sequence analysis of Australian avian pathogenic Escherichia coli that carry the class 1 integrase gene. Microb Genomics 2019; 5:
    [Google Scholar]
  85. Clermont O, Dixit OV, Vangchhia B, Condamine B, Dion S et al. Characterization and rapid identification of phylogroup G in Escherichia coli, a lineage with high virulence and antibiotic resistance potential. Environ Microbiol 2019; 21:3107–3117
    [Google Scholar]
  86. Arnold KE, Williams NJ, Bennett M. ‘Disperse abroad in the land’: the role of wildlife in the dissemination of antimicrobial resistance. Biol Lett 2016; 12:20160137
    [Google Scholar]
  87. Ahmed AM, Motoi Y, Sato M, Maruyama A, Watanabe H et al. Zoo animals as reservoirs of gram-negative bacteria harboring integrons and antimicrobial resistance genes. Appl Environ Microbiol 2007; 73:6686–6690
    [Google Scholar]
  88. Vittecoq M, Godreuil S, Prugnolle F, Durand P, Brazier L et al. Antimicrobial resistance in wildlife. J Appl Ecol 2016; 53:519–529
    [Google Scholar]
  89. Messenger AM, Barnes AN, Gray GC. Reverse zoonotic disease transmission (zooanthroponosis): a systematic review of seldom-documented human biological threats to animals. PLoS One 2014; 9:e89055
    [Google Scholar]
  90. Mo M, Roache M, Haering R, Kwok A. Using wildlife carer records to identify patterns in flying-fox rescues: a case study in New South Wales, Australia. Pac Conserv Biol. 2020
    [Google Scholar]
  91. Bodley K. Appendix 4. Drug formulary. In Vogelnest L, Portas T. (editors) Current Therapy in Medicine of Australian Mammals Clayton South (VIC): CSIRO Publishing; 2019 pp 702–727
    [Google Scholar]
  92. Scheelings TF, Frith SE. Anthropogenic Factors Are the Major Cause of Hospital Admission of a Threatened Species, the Grey-Headed Flying Fox (Pteropus poliocephalus), in Victoria, Australia. PLoS One 2015; 10:e0133638
    [Google Scholar]
  93. Páez DJ, Restif O, Eby P, Plowright RK. Optimal foraging in seasonal environments: implications for residency of Australian flying foxes in food-subsidized urban landscapes. Phil Trans R Soc B Biol Sci 1745; 2018:20170097
    [Google Scholar]
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