Abstract
Translocation and isolation of threatened wildlife in new environments may have unforeseen consequences on pathogen transmission and evolution in host populations. Disease threats associated with intensive conservation management of wildlife remain speculative without gaining an understanding of pathogen dynamics in meta-populations and how location attributes may determine pathogen prevalence. We determined the prevalence and population structure of an opportunistic pathogen, Salmonella, in geographically isolated translocated sub-populations of an endangered New Zealand flightless bird, the takahe (Porphyrio hochstetteri). Out of the nine sub-populations tested, Salmonella was only isolated from takahe living on one private island. The apparent prevalence of Salmonella in takahe on the private island was 32% (95% CI 13–57%), with two serotypes, Salmonella Mississippi and Salmonella houtenae 40:gt-, identified. Epidemiological investigation of reservoirs on the private island and another island occupied by takahe identified environmental and reptile sources of S. Mississippi and S. houtenae 40:gt- on the private island. Single nucleotide polymorphism analysis of core genomes revealed low-level diversity among isolates belonging to the same serotype and little differentiation according to host and environmental source. The pattern observed may be representative of transmission between sympatric hosts and environmental sources, the presence of a common unsampled source, and/or evidence of a recent introduction into the ecosystem. This study highlights how genomic epidemiology can be used to ascertain and understand disease dynamics to inform the management of disease threats in endangered wildlife populations.
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References
Thompson RC, Lymbery AJ, Smith A (2010) Parasites, emerging disease and wildlife conservation. Int. J. Parasitol. 40:1163–1170. doi:10.1016/j.ijpara.2010.04.009
Sainsbury AW, Vaughan-Higgins RJ (2012) Analyzing disease risks associated with translocations. Conserv. Biol. 26:442–452. doi:10.1111/j.1523-1739.2012.01839.x
Archie EA, Luikart G, Ezenwa VO (2009) Infecting epidemiology with genetics: a new frontier in disease ecology. Trends Ecol. Evol. 24:21–30. doi:10.1016/j.tree.2008.08.008
VanderWaal KL, Atwill ER, Isbell LA, McCowan B (2014) Quantifying microbe transmission networks for wild and domestic ungulates in Kenya. Biol. Conserv. 169:136–146. doi:10.1016/j.biocon.2013.11.008
VanderWaal KL, Atwill ER, Isbell LA, McCowan B (2013) Linking social and pathogen transmission networks using microbial genetics in giraffe (Giraffa camelopardalis). J. Anim. Ecol. 83:406–414. doi:10.1111/1365-2656.12137
Bull CM, Godfrey SS, Gordon DM (2012) Social networks and the spread of Salmonella in a sleepy lizard population. Mol. Ecol. 21:4386–4392. doi:10.1111/j.1365-294X.2012.05653.x
Gardy JL, Johnston JC, Sui SJH, Cook VJ, Shah L, Brodkin E, Rempel S, Moore R, Zhao Y, Holt R (2011) Whole genome sequencing and social network analysis of a tuberculosis outbreak. N. Engl. J. Med. 364:730–739
Didelot X, Bowden R, Wilson DJ, Peto TE, Crook DW (2012) Transforming clinical microbiology with bacterial genome sequencing. Nat. Rev. Genet. 13:601–612. doi:10.1038/nrg3226
Benton CH, Delahay RJ, Trewby H, Hodgson DJ (2015) What has molecular epidemiology ever done for wildlife disease research? Past contributions and future directions. Eur. J. Wildl. Res. 61:1–16. doi:10.1007/s10344-014-0882-4
Grange ZL, Gartrell BD, Biggs PJ, Nelson NJ, Anderson M, French NP (2016) Microbial genomics of a host-associated commensal bacterium in fragmented populations of endangered Takahe. Microb. Ecol. 71:1020–1029. doi:10.1007/s00248-015-0721-5
BirdLife International (2013) Porphyrio hochstetteri. http://www.iucnredlist.org/. Accessed 24 Feb 2014
Wickes C, Crouchley D, Maxwell JM (2009) Takahe (Porphorio hochstetteri) recovery plan 2007–2012. In: Department of Conservation (ed.), Wellington, NZ
Grange ZL, Van Andel M, French NP, Gartrell BD (2014) Network analysis of translocated Takahe populations to identify disease surveillance targets. Conserv. Biol. 28:518–528. doi:10.1111/cobi.12178
Acevedo-Whitehouse K, Gulland F, Greig D, Amos W (2003) Inbreeding: disease susceptibility in California sea lions. Nature 422:35–35
Smith KF, Acevedo-Whitehouse K, Pedersen AB (2009) The role of infectious diseases in biological conservation. Anim. Conserv. 12:1–12. doi:10.1111/j.1469-1795.2008.00228.x
Cunningham AA (1996) Disease risks of wildlife translocations. Conserv. Biol. 10:349–353. doi:10.1046/j.1523-1739.1996.10020349.x
McInnes K, Cromarty P, Ombler J (2004) Standard operating procedure for the health management of terrestrial vertebrate species protected under the wildlife act. Department of Conservation, Wellington, NZ
Ewen JG, Thorogood R, Nicol C, Armstrong DP, Alley M (2007) Salmonella typhimurium in hihi, New Zealand. Emerg. Infect. Dis. 13:788–790
Alley MR, Connolly JH, Fenwick SG, Mackereth GF, Leyland MJ, Rogers LE, Haycock M, Nicol C, Reed CEM (2002) An epidemic of salmonellosis caused by Salmonella Typhimurium DT160 in wild birds and humans in New Zealand. N. Z. Vet. J. 50:170–176
Lawson B, Howard T, Kirkwood JK, Macgregor SK, Perkins M, Robinson RA, Ward LR, Cunningham AA (2010) Epidemiology of salmonellosis in garden birds in England and Wales, 1993 to 2003. EcoHealth 7:294–306. doi:10.1007/s10393-010-0349-3
Hall AJ, Saito EK (2008) Avian wildlife mortality events due to salmonellosis in the United States, 1985-2004. J. Wildl. Dis. 44:585–593
Winfield MD, Groisman EA (2003) Role of nonhost environments in the lifestyles of Salmonella and Escherichia coli. Appl. Environ. Microbiol. 69:3687–3694. doi:10.1128/Aem.69.7.3687-3694.2003
Stevenson M (2014) epiR: an R package for the analysis of epidemiological data
Core Team R (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Jolley KA, Maiden MC (2010) BIGSdb: scalable analysis of bacterial genome variation at the population level. BMC bioinformatics 11:595. doi:10.1186/1471-2105-11-595
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792–1797. doi:10.1093/nar/gkh340
Drummond A, Ashton B, Cheung M, Heled J, Kearse M, Moir R (2013) Geneious Pro In: Biomatters (ed.)
Gardner SN, Hall BG (2013) When whole-genome alignments just won't work: kSNP v2 software for alignment-free SNP discovery and phylogenetics of hundreds of microbial genomes. PLoS ONE 8. doi: 10.1371/journal.pone.0081760
Ewen JG, Armstrong DP, Empson R, Jack S, Makan T, McInnes K, Parker KA, Richardson K, Alley M (2012) Parasite management in translocations: lessons from a threatened New Zealand bird. Oryx 46:446–456. doi:10.1017/s0030605311001281
Leighton FA (2002) Health risk assessment of the translocation of wild animals. Revue Scientifique et Technique-Office International des Epizooties 21:187–216
Jakob-Hoff R, MacDiarmid SC, Lees C, Miller PS, Travis D, Kock RA (2014), International Office of Epizootics., International Union for Conservation of Nature. Manual of procedures for wildlife disease risk analysis. World Organisation for Animal Health, pp. ix, 149 pages
Haydon DT, Cleaveland S, Taylor LH, Laurenson MK (2002) Identifying reservoirs of infection: a conceptual and practical challenge. Emerg. Infect. Dis. 8:1468–1473
Viana M, Mancy R, Biek R, Cleaveland S, Cross PC, Lloyd-Smith JO, Haydon DT (2014) Assembling evidence for identifying reservoirs of infection. Trends Ecol. Evol. 29:270–279. doi:10.1016/j.tree.2014.03.002
Orr M (1997) Salmonella Brandenburg in a takahe. In: NZVA, WSo (ed.) Kokako, vol. 4, pp. 14
McLelland JM, Gartrell BD, Roe WD (2011) A retrospective study of post-mortem examination findings in takahe (Porphyrio hochstetteri). N. Z. Vet. J. 59:160–165. doi:10.1080/00480169.2011.579243
ESR (2010) Public health surveillance: non human Salmonella isolates. Accessed 12 Jun 2014
Jamieson IG, Ryan CJ (2001) Island takahe: closure of the debate over the merits of introducing Fiordland takahe to predator-free islands. In: Jamieson, IG, Lee, WG (eds.) The takahe: fifty years of conservation management and research. Otago University Press, Dunedin, New Zealand, pp. 96–113
Iveson JB, Shellam GR, Bradshaw SD, Smith DW, Mackenzie JS, Mofflin RG (2009) Salmonella infections in Antarctic fauna and island populations of wildlife exposed to human activities in coastal areas of Australia. Epidemiology & Infection 137:858–870. doi:10.1017/S0950268808001222
Middleton DMRL, La Flamme AC, Gartrell BD, Nelson NJ (2014) Reptile reservoirs and seasonal variation in the environmental presence of Salmonella in an island ecosystem, Stephens Island, New Zealand. J. Wildl. Dis. 50:655–659. doi:10.7589/2013-10-277
Parsons SK, Bull CM, Gordon DM (2010) Low prevalence of Salmonella enterica in Australian wildlife. Environ. Microbiol. Rep. 2:657–659. doi:10.1111/j.1758-2229.2010.00152.x
Ashbolt R, Kirk MD (2006) Salmonella Mississippi infections in Tasmania: the role of native Australian animals and untreated drinking water. Epidemiology & Infection 134:1257–1265. doi:10.1017/S0950268806006224
van Andel M, Jackson BH, Midwinter AC, Alley MR, Ewen JG, McInnes K, Hoff RJ, Reynolds AD, French N (2015) Investigation of mortalities associated with Salmonella spp. infection in wildlife on Tiritiri Matangi Island in the Hauraki Gulf of New Zealand. N. Z. Vet. J. 63:235–239. doi:10.1080/00480169.2014.990065
Nunn CL, Thrall PH, Kappeler PM (2014) Shared resources and disease dynamics in spatially structured populations. Ecol. Model. 272:198–207. doi:10.1016/j.ecolmodel.2013.10.004
Hines AM, Ezenwa VO, Cross P, Rogerson JD (2007) Effects of supplemental feeding on gastrointestinal parasite infection in elk (Cervus elaphus): preliminary observations. Vet. Parasitol. 148:350–355
Dhondt AA, Altizer S, Cooch EG, Davis AK, Dobson A, Driscoll MJL, Hartup BK, Hawley DM, Hochachka WM, Hosseini PR, Jennelle CS, Kollias GV, Ley DH, Swarthout ECH, Sydenstricker KV (2005) Dynamics of a novel pathogen in an avian host: mycoplasmal conjunctivitis in house finches. Acta Trop. 94:77–93. doi:10.1016/j.actatropica.2005.01.009
Lawson B, Robinson RA, Colvile KM, Peck KM, Chantrey J, Pennycott TW, Simpson VR, Toms MP, Cunningham AA (2012) The emergence and spread of finch trichomonosis in the British Isles. Philosophical Transactions of the Royal Society B: Biological Sciences 367:2852–2863. doi:10.1098/rstb.2012.0130
Joseph MB, Mihaljevic JR, Arellano AL, Kueneman JG, Preston DL, Cross PC, Johnson PTJ, Morgan E (2013) Taming wildlife disease: bridging the gap between science and management. J. Appl. Ecol. 50:702–712. doi:10.1111/1365-2664.12084
Ryan CJ, Jamieson IG (1998) Estimating the home range and carrying capacity for takahe on predator free offshore islands: implications for future management. N. Z. J. Ecol. 22:17–24
Vigo GB, Leotta GA, Caffer MI, Salve A, Binsztein N, Pichel M (2011) Isolation and characterization of Salmonella enterica from Antarctic wildlife. Polar Biol. 34:675–681. doi:10.1007/s00300-010-0923-8
Biek R, Pybus OG, Lloyd-Smith JO, Didelot X (2015) Measurably evolving pathogens in the genomic era. Trends Ecol. Evol. 30:306–313. doi:10.1016/j.tree.2015.03.009
Didelot X, Bowden R, Street T, Golubchik T, Spencer C, McVean G, Sangal V, Anjum MF, Achtman M, Falush D, Donnelly P (2011) Recombination and population structure in Salmonella enterica. PLoS Genet. 7:e1002191. doi:10.1371/journal.pgen.1002191
Smith NH, Gordon SV, de la Rua-Domenech R, Clifton-Hadley RS, Hewinson RG (2006) Bottlenecks and broomsticks: the molecular evolution of Mycobacterium bovis. Nat. Rev. Microbiol. 4:670–681
Bager F, Petersen J (1991) Sensitivity and specificity of different methods for the isolation of Salmonella from pigs. Acta Vet. Scand. 32:473–481
Worby CJ, Lipsitch M, Hanage WP (2014) Within-host bacterial diversity hinders accurate reconstruction of transmission networks from genomic distance data. PLoS Comput. Biol. 10:e1003549. doi:10.1371/journal.pcbi.1003549
Benavides JA, Cross PC, Luikart G, Creel S (2014) Limitations to estimating bacterial cross-species transmission using genetic and genomic markers: inferences from simulation modeling. Evol. Appl. 7:774–787. doi:10.1111/Eva.12173
Biek R, O'Hare A, Wright D, Mallon T, McCormick C, Orton RJ, McDowell S, Trewby H, Skuce RA, Kao RR (2012) Whole genome sequencing reveals local transmission patterns of Mycobacterium bovis in sympatric cattle and badger populations. PLoS Pathog. 8:e1003008. doi:10.1371/journal.ppat.1003008
Matthews DT, Schmieder R, Silva GGZ, Busch J, Cassman N, Dutilh BE, Green D, Matlock B, Heffernan B, Olsen GJ, Farris Hanna L, Schifferli DM, Maloy S, Dinsdale EA, Edwards RA (2015) Genomic comparison of the closely-related Salmonella enterica Serovars Enteritidis, Dublin and Gallinarum. PLoS One 10:e0126883. doi:10.1371/journal.pone.0126883
Deng X, Shariat N, Driebe EM, Roe CC, Tolar B, Trees E, Keim P, Zhang W, Dudley EG, Fields PI, Engelthaler DM (2015) Comparative analysis of subtyping methods against a whole-genome-sequencing standard for Salmonella enterica serotype Enteritidis. J. Clin. Microbiol. 53:212–218. doi:10.1128/jcm.02332-14
Grange ZL, Gartrell BD, Biggs PJ, Nelson NJ, Marshall JC, Howe L, Balm GMM, French NP (2015) Using a common commensal bacterium in endangered Takahe, as a model to explore pathogen dynamics in isolated wildlife populations. Conserv. Biol. 29:1327–1336. doi:10.1111/cobi.12521
Jolley KA, Bliss CM, Bennett JS, Bratcher HB, Brehony C, Colles FM, Wimalarathna H, Harrison OB, Sheppard SK, Cody AJ, Maiden MC (2012) Ribosomal multilocus sequence typing: universal characterization of bacteria from domain to strain. Microbiology 158:1005–1015. doi:10.1099/mic.0.055459-0
Acknowledgements
This study was funded by the Allan Wilson Centre as part of the PhD study of Dr. Grange and MSc of S. Rose. We would like to thank Ngai Tahu for their support of this research, T. Burns for field assistance, A. Reynolds for laboratory support, and Dr. Howe for guidance.
Supporting Information
A map of pitfall locations on Maud Island (Appendix S1), the number of lizards captured and sampled (Appendix S2), the list of Salmonella genomes used for 51 gene ribosomal multi-locus sequence comparison (Appendix S3), SNP information for Salmonella Mississippi (Appendix S4) and S. houtenae 40:gt- (Appendix S5) study isolates, and the alignment of rMLST gene sequences (Appendix S6) are available online. The authors are solely responsible for the content and functionality of these materials. Queries (other than absence of the material) should be directed to the corresponding author.
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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted. Reptile capture and sampling was conducted according to a Victoria University of Wellington animal ethics permit 2012R33 and the New Zealand Department of Conservation research permit 37543-FAU. Takahe samples were collected under a Massey University animal ethics permit MUAEC Protocol 11/95. This article does not contain any studies with human participants performed by any of the authors. This study was funded by the Allan Wilson Centre.
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Grange, Z.L., Biggs, P.J., Rose, S.P. et al. Genomic Epidemiology and Management of Salmonella in Island Ecosystems Used for Takahe Conservation. Microb Ecol 74, 735–744 (2017). https://doi.org/10.1007/s00248-017-0959-1
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DOI: https://doi.org/10.1007/s00248-017-0959-1