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Ecosystems

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Natural and Regenerated Saltmarshes Exhibit Similar Soil and Belowground Organic Carbon Stocks, Root Production and Soil Respiration

  • Nadia S. SantiniEmail author
  • Catherine E. Lovelock
  • Quan Hua
  • Atun Zawadzki
  • Debashish Mazumder
  • Tim R. Mercer
  • Miriam Muñoz-Rojas
  • Simon A. Hardwick
  • Bindu Swapna Madala
  • William Cornwell
  • Torsten Thomas
  • Ezequiel M. Marzinelli
  • Paul Adam
  • Swapan Paul
  • Adriana Vergés
Article

Abstract

Saltmarshes provide many valuable ecosystem services including storage of a large amount of ‘blue carbon’ within their soils. To date, up to 50% of the world’s saltmarshes have been lost or severely degraded primarily due to a variety of anthropogenic pressures. Previous efforts have aimed to restore saltmarshes and their ecosystem functions, but the success of these efforts is rarely evaluated. To fill this gap, we used a range of metrics, including organic carbon stocks, root production, soil respiration and microbial communities to compare natural and a 20-year restoration effort in saltmarsh habitats within the Sydney Olympic Park in New South Wales, Australia. We addressed four main questions: (1) Have above- and belowground plant biomass recovered to natural levels? (2) Have organic carbon stocks of soils recovered? (3) Are microbial communities similar between natural and regenerated saltmarshes? and (4) Are microbial communities at both habitats associated to ecosystem characteristics? For both soil organic carbon stocks and belowground biomass, we found no significant differences between natural and regenerated habitats (F(1,14) = 0.47, p = 0.5; F(1,42) = 0.08, p = 0.76). Aboveground biomass was higher in the natural habitat compared to the regenerated habitat (F(1,20) = 27.3, p < 0.0001), which may result from a site-specific effect: protection from erosion offered by a fringing mangrove forest in the natural habitat but not the regenerated habitat. Our microbial community assessment indicated that restored and natural saltmarsh habitats were similar at a phylum level, with the exception of a higher proportion of Proteobacteria in the rhizosphere of saltmarshes from the regenerated habitat (p < 0.01). Abundance of both Desulfuromonas and Geobacter was associated with high carbon and nitrogen densities in soils indicating that these genera may be key for the recovery of ecosystem characteristics in saltmarshes. Our restored and natural saltmarsh soils store at 30 cm depth similar levels of organic carbon: 47.9 Mg OC ha−1 to 64.6 Mg OC ha−1. Conservation of urban saltmarshes could be important for ‘blue carbon’ programmes aimed at mitigating atmospheric carbon dioxide.

Keywords

Sarcocornia quinqueflora blue carbon carbon sequestration rehabilitation Sydney Olympic Park 210Pb dating microbial communities 

Notes

Acknowledgements

We would like to thank the following people for technical support: Brodie Cutmore, Patricia Gadd, Daniela Fierro, Barbora Gallagher and Jennifer Van Holst from the Australian Nuclear Science and Technology Organisation; Sophie Baxter, Caitlan Baxter, Delphine Coste, Len Martin, Scott Mooney and Crystal Vargas from the University of New South Wales; Brownwen van Jaarsveld and Bryony Horton from the Office of Environment and Heritage, New South Wales; Daniel Piñero from the Instituto de Ecología at the National Autonomous University of Mexico (UNAM) and Edgar J Gonzalez from the Faculty of Science, UNAM. We also thank the editors and two anonymous reviewers as their revisions substantially improved this manuscript.

Funding

This project was funded by the National Council for Science and Technology (CONACYT, Mexico, Grants 263728 and 277411) and by two research portal grants from the Australian Nuclear Science and Technology Organisation (ANSTO, Australia, Grants 10006 and 11081). We acknowledge the financial support from the Australian Government for the Centre for Accelerator Science at ANSTO through the National Collaborative Research Infrastructure Strategy (NCRIS). This work was performed under a National Parks and Wildlife Act 1974 scientific licence (SL101748).

Supplementary material

10021_2019_373_MOESM1_ESM.docx (703 kb)
Supplementary material 1 (DOCX 703 kb)

References

  1. Adam P. 2002. Saltmarshes in a time of change. Environ Conserv 29:39–61.CrossRefGoogle Scholar
  2. Adame MF, Wright SF, Grinham A, Lobb K, Reymond CE, Lovelock CE. 2012. Terrestrial-marine connectivity: Patterns of terrestrial soil carbon deposition in coastal sediments determined by analysis of glomalin related soil protein. Limnol Oceanogr 57:1492–502.CrossRefGoogle Scholar
  3. Adame MF, Teutli C, Santini NS, Caamal JP, Zaldívar-Jiménez A, Hernández R, Herrera-Silveira JA. 2014. Root biomass and production of mangroves surrounding a karstic oligotrophic coastal lagoon. Wetlands 34:479–88.CrossRefGoogle Scholar
  4. Alongi D. 2009. The energetics of mangrove forests. Dordrecht: Springer.Google Scholar
  5. Appleby PG. 2001. Chronostratigraphic techniques in recent sediments. In: Last WM, Smol JP, Eds. Tracking environmental change using lake sediments. Developments in paleoenvironmental research, Vol. 1. Dordrecht: Springer. p 171–203.CrossRefGoogle Scholar
  6. Atahan P, Heijnis H, Dodson J, Grice K, Le Metayer P, Taffs K, Hembrow S, Woltering M, Zawadzki A. 2014. Glacial and Holocene terrestrial temperature variability in subtropical east Australia as inferred from branched GDGT distributions in a sediment core from Lake McKenzie. Quat Res 82:132–45.CrossRefGoogle Scholar
  7. Australian Bureau of Meteorology. 2018. Australian Bureau of Meteorology home page. Commonwealth of Australia: Canberra. http://www.bom.gov.au. Accessed 14 Feb 2018.
  8. Bronk RC. 2009. Bayesian analysis of radiocarbon dates. Radiocarbon 51:337–60.CrossRefGoogle Scholar
  9. Burchett MD, Allen C, Pulkownik AA, Macfarlane G. 1998. Rehabilitation of saline wetland, Olympics 2000 Site, Sydney (Australia)-II: saltmarsh transplantation trials and application. Mar Pollut Bull 37:526–34.CrossRefGoogle Scholar
  10. Burden A, Garbutt RA, Evans CD, Jones DL, Cooper DM. 2013. Carbon sequestration and biogeochemical cycling in a saltmarsh subject to coastal managed realignment. Estuar Coast Shelf Sci 120:12–20.CrossRefGoogle Scholar
  11. Calderoni PA, Collavino MM, Kraemer FB, Morrás HJ, Aguilar OM. 2017. Analysis of nifH-RNA reveals phylotypes related to geobacter and cyanobacteria as important functional components of the N2-fixing community depending on depth and agricultural use of soil. Microbiol Open 6:e502.Google Scholar
  12. Card SM, Quideau SA, Se-Woung O. 2010. Carbon characteristics in restored and reference riparian soils. Soil Sci Soc Am J 74:1834–43.CrossRefGoogle Scholar
  13. Chmura GL, Anisfeld SC, Cahoon DR, Lynch JC. 2003. Global carbon sequestration in tidal, saline wetland soils. Glob Biogeochem Cycles 17:7–12.CrossRefGoogle Scholar
  14. Church JA, White NJ. 2006. A 20th century acceleration in global sea level rise. Geophys Res Lett 33:L01602.CrossRefGoogle Scholar
  15. Clarke PJ, Jacoby CA. 1994. Biomass and above-ground productivity of salt-marsh plants in south-eastern Australia. Aust J Mar Freshw Res 45:1521–8.CrossRefGoogle Scholar
  16. Connolly R. 2009. Fish on Australian saltmarshes. In: Saintilan N, Ed. Australian Saltmarsh ecology. Victoria: CSIRO Publishing. p 131–48.Google Scholar
  17. Craft C, Reader J, Sacco JN, Broome SW. 1999. Twenty-five years of ecosystem development of constructed Spartina alterniflora (Loisel) marshes. Ecol Appl 9:1405–19.CrossRefGoogle Scholar
  18. Crooks S, Herr D, Tamelander J, Laffoley D, Vandever J. 2011. Mitigating climate change through restoration and management of coastal wetlands and near shore marine ecosystems: challenges and opportunities. Environment department papers. 121. Marine Ecosystem Series. World Bank, Washington DC.Google Scholar
  19. Day JW, Christian RR, Boesch DM, Yáñez-Arancibia A, Morris J, Twilley RR, Naylor L, Schaffner L, Stevenson C. 2008. Consequences of climate change on the ecogeomorphology of coastal wetlands. Estuar Coasts 31:477–91.CrossRefGoogle Scholar
  20. Dhanjal-Adams KL, Hanson JO, Murray NJ, Phinn SR, Wingate VR, Mustin K, Lee JR, Allan JR, Cappadonna JL, Studds CE, Clemens RS, Roelfsema CM, Fuller RA. 2016. The distribution and protection of intertidal habitats in Australia. Emu 116:208–14.CrossRefGoogle Scholar
  21. Duarte CM, Dennison WC, Orth RJW, Carruthers TJB. 2008. The charisma of coastal ecosystems: addressing the imbalance. Estuar Coasts 31:233–8.CrossRefGoogle Scholar
  22. Duarte CM, Losada IJ, Hendriks IE, Mazarrasa I, Marbà N. 2013. The role of coastal communities for climate change mitigation and adaptation. Nat Clim Change 3:961–8.CrossRefGoogle Scholar
  23. Fierer N, Bradford MA, Jackson RB. 2007. Toward an ecological classification of soil bacteria. Ecology 88:1354–64.CrossRefGoogle Scholar
  24. Fierer N, Lauber CL, Ramirez KS, Zaneveld J, Bradford MA, Knight R. 2012. Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients. Int Soc Microb Ecol 6:1007–17.Google Scholar
  25. Fink D, Hotchkis M, Hua Q, Jacobsen G, Smith AM, Zoppi U, Child D, Mifsud C, van der Gaast H, Williams A, Williams M. 2004. The antares AMS facility at ANSTO. Nucl Instrum Methods Phys Res B Beam Interact Mater Atoms 223–224:109–15.CrossRefGoogle Scholar
  26. Gedan KB, Silliman BR, Bertness MD. 2009. Centuries of human-driven change in saltmarsh ecosystems. Annu Rev Mar Sci 1:117–41.CrossRefGoogle Scholar
  27. Gellie NJC, Mills JG, Breed MF, Lowe AJ. 2017. Revegetation rewilds the soil bacterial microbiome of an old field. Mol Ecol 26:2895–904.CrossRefGoogle Scholar
  28. Haney RL, Brinton WF, Evans E. 2008. Soil CO2 respiration: comparison of chemical titration, CO2 IRGA analysis and the Solvita gel system. Renew Agrice Food Syst 23:171–6.Google Scholar
  29. Hardwick SA, Chen WY, Wong T, Kanakamedala BS, Deveson IW, Ongley SE, Santini NS, Marcellin E, Smith MA, Nielsen LK, Lovelock CE, Nielan BA, Mercer TR. 2018. Synthetic microbe communities provide internal reference standards for metagenome sequencing and analysis. Nat Commun 9:1–10.CrossRefGoogle Scholar
  30. Hogg AG, Hua Q, Blackwell PG, Niu M, Buck CE, Guilderson TP, Heaton TJ, Palmer JG, Reimer PJ, Reimer RW, Turney CSM, Zimmerman SRH. 2013. SHCal13 Southern hemisphere calibration, 0–50,000 years Cal BP. Radiocarbon 55:1889–903.CrossRefGoogle Scholar
  31. Howard J, Hoyt S, Isensee K, Pidgeon E, Telszewski M, Eds. 2014. Coastal blue carbon: methods for assessing carbon stocks and emissions factors in mangroves, tidal salt marshes, and seagrass meadows. Conservation International, Intergovernmental Oceanographic Commission of UNESCO, International Union for Conservation of Nature. Arlington, Virginia, USA.Google Scholar
  32. Hua Q, Jacobsen GE, Zoppi U, Lawson EM, Williams AA, Smith AM, McGann MJ. 2001. Progress in radiocarbon target preparation at the ANTARES AMS Centre. Radiocarbon 43:275–82.CrossRefGoogle Scholar
  33. Hua Q. 2009. Radiocarbon: a chronological tool for the recent past. QuatGeochronol 4:378–90.Google Scholar
  34. Kelleway JJ, Saintilan N, Macreadie PI, Baldock JA, Heijnis H, Zawadzki A, Gadd P, Jacobsen G, Ralph PJ. 2016. Geochemical analyses reveal the importance of environmental history for blue carbon sequestration. J Geophys Res Biogeosci 122:1789–805.CrossRefGoogle Scholar
  35. Kirwan ML, Megonigal JP. 2013. Tidal wetland stability in the face of human impacts and sea-level rise. Nature 504:53–60.CrossRefGoogle Scholar
  36. Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–9.  https://doi.org/10.1038/nmeth.1923.CrossRefGoogle Scholar
  37. Leslie C, Hancock GJ. 2008. Estimating the date corresponding to the horizon of the first detection of 137Cs and 239+240Pu in sediment cores. J Environ Radioact 99:483–90.CrossRefGoogle Scholar
  38. Levin LA, Talley TS. 2002. Natural and manipulated sources of heterogeneity controlling early faunal development of a salt marsh. Ecol Appl 12:1785–802.CrossRefGoogle Scholar
  39. Lovelock C, Ellison J. 2007. Vulnerability of mangroves and tidal wetlands of the Great Barrier Reef to climate change. In: Johnson JE, Marshall PA, Eds. Climate change and the Great Barrier Reef: a vulnerability assessment. Townsville: Great Barrier Reef Marine Park Authority and Australian Greenhouse Office. p 237–69.Google Scholar
  40. Lovelock CE, Adame MF, Bennion V, Hayes M, O’Mara J, Reef R, Santini NS. 2014. Contemporary rates of carbon sequestration through vertical accretion of sediments in mangrove forests and saltmarshes of South East Queensland, Australia. Estuar Coasts 37:763–71.CrossRefGoogle Scholar
  41. Lovelock CE, Adame MF, Bennion V, Hayes M, Reef R, Santini N, Cahoon DR. 2015a. Sea level and turbidity controls on mangrove soil surface elevation change. Estuar Coast Shelf Sci 153:1–9.CrossRefGoogle Scholar
  42. Lovelock CE, Cahoon DR, Friess DA, Guntenspergen GR, Krauss KW, Reef R, Rogers K, Saunders ML, Sidik F, Swales A, Saintilan N, Thuyen LX, Triet T. 2015b. The vulnerability of Indo-Pacific Mangrove forests to sea-level rise. Nature 526:559–63.CrossRefGoogle Scholar
  43. Macreadie PI, Ollivier QR, Kelleway JJ, Serrano O, Carnell PE, Ewers Lewis CJ, Atwood TB, Sanderman J, Baldock J, Connolly RM, Duarte CM, Lavery PS, Steven A, Lovelock CE. 2017. Carbon sequestration by Australian tidal marshes. Sci Rep 7:44071.CrossRefGoogle Scholar
  44. Mazumder D, Saintilan N, Williams RJ. 2006. Trophic relationships between itinerant fish and crab larvae in a temperate Australian saltmarsh. Mar Freshw Res 57:193–9.CrossRefGoogle Scholar
  45. McKee KL. 2001. Root proliferation in decaying roots and old root channels: a nutrient conservation mechanism in oligotrophic mangrove forest? J Ecol 89:876–87.CrossRefGoogle Scholar
  46. McLeod E, Chmura GL, Bouillon S, Salm R, Björk M, Duarte CM, Lovelock CE, Schlesinger WH, Silliman BR. 2011. A blueprint for blue carbon: toward an improved understanding of the role of vegetated coastal habitats in sequestering CO2. Front Ecol Environ 9:552–60.CrossRefGoogle Scholar
  47. Meyer F, Paarmann D, D’Souza M, Olson R, Glass EM, Kubal M, Paczian T, Rodriguez A, Stevens R, Wilke A, Wilkening J, Edwards RA. 2008. The metagenomics RAST server—a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinform 9:1–8.CrossRefGoogle Scholar
  48. Moreno-Mateos D, Power ME, Comín FA, Yockteng R. 2012. Structural and functional loss in restored wetland ecosystems. PLoS Biol 10:e1001247.  https://doi.org/10.1371/journal.pbio.1001247.CrossRefGoogle Scholar
  49. Muñoz-Rojas M, Erickson TE, Dixon KW, Merritt DJ. 2016. Soil quality indicators to assess functionality of restored soils in degraded semiarid ecosystems. Restor Ecol 24:S43–52.  https://doi.org/10.1111/rec.12368.CrossRefGoogle Scholar
  50. Muyzer G, Stams AJM. 2008. The ecology and biotechnology of sulphate-reducing bacteria. Nat Rev Microbiol 6:441–54.CrossRefGoogle Scholar
  51. Neubauer SC. 2008. Contributions of mineral and organic components to tidal freshwater marsh accretion. Estuar Coast Shelf Sci 78:78–88.CrossRefGoogle Scholar
  52. Oksanen JF, Blanchet G, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Henry M, Stevens H, Szoecs E, Wagner H. 2018. Vegan: community ecology package. R package version 2.5 – 1. https://CRAN.R-project.org/package=vegan. Accessed 12 June 2018.
  53. Osland MJ, Spivak AC, Nestlerode JA, Lessman JM, Almario AE, Heimuller PT, Rusell MJ, Krauss KW, Alvarez F, Dantin DD, Harvey JE, From AS, Cormier N, Stagg CL. 2013. Ecosystem development after mangrove wetland creation: plant-soil change across a 20-year chronosequence. Ecosystems 15:848–66.CrossRefGoogle Scholar
  54. Pi N, Tam NFY, Wu Y, Wong MH. 2009. Root anatomy and spatial pattern of radial oxygen loss of eight true mangrove species. Aquat Bot 90:222–30.CrossRefGoogle Scholar
  55. R Core Team. 2018. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. Accessed 25 December 2018.
  56. Reef R, Feller IC, Lovelock CE. 2010. Nutrition of mangroves. Tree Physiol 30:1148–60.CrossRefGoogle Scholar
  57. Rogers K, Boon PI, Branigan S et al. 2016. The state of legislation and policy protecting Australia’s mangrove and salt marsh and their ecosystem services. Mar Policy 72:139–55.CrossRefGoogle Scholar
  58. Rogers K, Saintilan N, Heijnis H. 2005. Mangrove encroachment of salt marsh in Western Port Bay, Victoria: the role of sedimentation, subsidence, and sea level rise. Estuaries 28:551–9.CrossRefGoogle Scholar
  59. Rogers K, Saintilan N, Howe AJ, Rodriguez JF. 2013. Sedimentation, elevation and marsh evolution in a southeastern Australian estuary during changing climatic conditions. Estuar Coast Shelf Sci 133:172-81.  https://doi.org/10.1016/j.ecss.2013.08.025.CrossRefGoogle Scholar
  60. Saintilan N, Rogers K, Mazumder D, Woodroffe CD. 2013. Allochthonous and autochthonous contributions to carbon accumulation and carbon store in south-eastern Australian coastal wetlands. Estuar Coast Shelf Sci 128:84–92.CrossRefGoogle Scholar
  61. Schmidt M, Torn MS, Abiven S, Dittmar T, Guggenberger G, Janssens IA, Kleber M, Kogel-Knabner I, Lehmann J, Manning DAC, Nannipieri P, Rasse DP, Weiner S, Trumbore SE. 2011. Persistence of soil organic matter as an ecosystem property. Nature 478:49–56.CrossRefGoogle Scholar
  62. Segers R, Leffelaar PA. 2001. Modeling methane fluxes in wetlands with gas-transporting plants 3. Plot scale. J Geophys Res 106:3541–58.CrossRefGoogle Scholar
  63. Shrestha PM, Kube M, Reinhardt R, Liesack W. 2009. Transcriptional activity of paddy soil bacterial communities. Environ Microbiol 11:960–70.CrossRefGoogle Scholar
  64. Stuiver M, Polach HA. 1977. Reporting of 14C data. Radiocarbon 19:353–63.CrossRefGoogle Scholar
  65. Tripathee R, Schafer KVR. 2015. Above- and belowground biomass allocation in four dominant salt marsh species of the Eastern United States. Wetlands 35:21–30.CrossRefGoogle Scholar
  66. Waisel Y, Eshel A, Kafkafi U. 1996. Plant roots: the hidden half. New York: Marcel Dekker Inc.Google Scholar
  67. White NJ, Haigh ID, Church JA, Koen T, Watson CS, Pritchard TR, Watson PJ, Burgette RJ, McInnes K, You Z, Zhang X, Tregoning P. 2014. Australian sea levels-trends, regional variability and influencing factors. Earth Sci Rev 136:155–74.CrossRefGoogle Scholar
  68. Williams RJ, Allen CB, Kelleway J. 2011. Saltmarsh of the Parramatta River—Sydney Harbour: determination of cover and species composition including comparison of API and pedestrian survey. Cunninghamia 12:29–44.Google Scholar
  69. Winning G, Saintilan N. 2010. Vegetation changes in Hexham Swamp, Hunter River, New South Wales, since the construction of floodgates in 1971. Cunninghamia 11:185–94.Google Scholar
  70. Xie T, Cui B, Li S. 2015. Analysing how plants in coastal wetlands respond to varying tidal regimens throughout their life cycles. Mar Pollut Bull 123:113–21.CrossRefGoogle Scholar
  71. Yamamoto M, Takai K. 2011. Sulfur metabolisms in epsilon- and gamma- Proteobacteria in deep-sea hydrothermal fields. Front Microb 2:1–8.CrossRefGoogle Scholar
  72. Zedler JB. 2000. Progress in wetland restoration ecology. Trends Ecol Evol 15:402–7.CrossRefGoogle Scholar
  73. Zedler JB. 2007. Success: an unclear, subjective descriptor of restoration outcomes. Ecol Restor 25:162–8.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Nadia S. Santini
    • 1
    • 2
    Email author
  • Catherine E. Lovelock
    • 3
  • Quan Hua
    • 4
  • Atun Zawadzki
    • 4
  • Debashish Mazumder
    • 4
  • Tim R. Mercer
    • 5
    • 6
    • 7
  • Miriam Muñoz-Rojas
    • 2
    • 8
    • 9
  • Simon A. Hardwick
    • 5
  • Bindu Swapna Madala
    • 5
  • William Cornwell
    • 2
  • Torsten Thomas
    • 2
    • 10
  • Ezequiel M. Marzinelli
    • 10
    • 11
    • 12
  • Paul Adam
    • 2
  • Swapan Paul
    • 13
  • Adriana Vergés
    • 2
    • 10
  1. 1.Cátedra CONACYT- Instituto de EcologíaUniversidad Nacional Autónoma de México, Ciudad UniversitariaMexico CityMexico
  2. 2.School of Biological, Earth and Environmental SciencesUniversity of New South WalesSydney, KensingtonAustralia
  3. 3.School of Biological SciencesThe University of QueenslandBrisbane, St. LuciaAustralia
  4. 4.Australian Nuclear Science and Technology OrganisationSydney, Lucas HeightsAustralia
  5. 5.Genomics and Epigenetics DivisionGarvan Institute of Medical ResearchSydney, DarlinghurstAustralia
  6. 6.Altius Institute for Biomedical SciencesSeattleUSA
  7. 7.St. Vincent’s Clinical School, Faculty of MedicineUniversity of New South Wales SydneyKensingtonAustralia
  8. 8.School of Biological SciencesThe University of Western AustraliaCrawley, PerthAustralia
  9. 9.Department of Biodiversity, Conservation and AttractionsKings Park ScienceKings Park, PerthAustralia
  10. 10.Centre for Marine Bio-InnovationUniversity of New South WalesSydney, KensingtonAustralia
  11. 11.School of Life and Environmental SciencesThe University of SydneySydney, DarlingtonAustralia
  12. 12.Singapore Centre for Environmental Life Sciences EngineeringNanyang Technological UniversitySingaporeSingapore
  13. 13.Sydney Olympic Park AuthoritySydney, Sydney Olympic ParkAustralia

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