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How Does Sphagnum Growing Affect Testate Amoeba Communities and Corresponding Protozoic Si Pools? Results from Field Analyses in SW China

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Abstract

The policy and practice of ecological restoration and conservation in China obtained some remarkable results. For example, Sphagnum moss growing on abandoned farmland, which was peatland before agricultural use, has rapidly expanded the wetland area in SW China. Microorganisms such as testate amoebae are sensitive to environmental change and thus have been widely used as ecological indicators in various habitats. We analyzed differently aged Sphagnum growing plots on a Sphagnum growing farmland and natural Sphagnum plots in SW China to examine how Sphagnum-dwelling testate amoeba communities and corresponding protozoic silicon (Si) pools respond to ecological restoration practice. We found that abundance, taxon richness, and diversity of testate amoebae were higher in Sphagnum growing farmland plots compared to natural Sphagnum plots. Protozoic Si pools showed an increase with Sphagnum growing time representing increased Si accumulation by idiosomic testate amoeba shells. However, protozoic Si pools were negatively correlated with taxon richness and diversity of testate amoebae. Our results showed that (i) natural Sphagnum plots were not characterized by the expected higher biodiversity of testate amoebae compared to Sphagnum growing plots and (ii) consequently protozoic Si pool quantity in natural Sphagnum plots was less driven by biodiversity of testate amoebae than expected. We concluded our results to underline the value of (i) environmental restoration policy in general and (ii) testate amoeba communities and corresponding protozoic Si pools for Si cycling in restoration areas of peatlands in particular. Based on our results, we recommend a sustainable cultivation of Sphagnum moss and an additional establishment of protected areas, where no Sphagnum harvesting occurs. These protected Sphagnum areas might represent hot spots of undisturbed testate amoeba communities and corresponding protozoic Si pools and thus of microbial Si cycling.

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References

  1. Struyf E, Conley DJ (2009) Silica: an essential nutrient in wetland biogeochemistry. Front Ecol Env 7:88–94. https://doi.org/10.2307/25595061

    Article  Google Scholar 

  2. Struyf E, Mörth CM, Humborg C, Conley DJ (2010) An enormous amorphous silica stock in boreal wetlands. J. Geophys. Res. Biogeosci. 115:G04008. https://doi.org/10.1029/2010JG001324

    Article  CAS  Google Scholar 

  3. Carey JC, Fulweiler RW (2012) The terrestrial silica pump. PLoS One 7:e52932. https://doi.org/10.1371/journal.pone.0052932

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Holden J, Wallage ZE, Lane SN, McDonald AT (2011) Water table dynamics in undisturbed, drained and restored blanket peat. J. Hydrol. 402:103–114. https://doi.org/10.1016/j.jhydrol.2011.03.010

    Article  Google Scholar 

  5. Hooijer A, Page S, Jauhiainen J, Lee WA, Lu XX, Idris A, Anshari G (2012) Subsidence and carbon loss in drained tropical peatlands. Biogeosciences 9:1053–1071. https://doi.org/10.5194/bg-9-1053-2012

    Article  CAS  Google Scholar 

  6. Jauhiainen S (2002) Testacean amoebae in different types of mire following drainage and subsequent restoration. Eur. Protistol 38:59–72. https://doi.org/10.1078/0932-4739-00748

    Article  Google Scholar 

  7. Koenig I, Mulot M, Mitchell EAD (2017) Taxonomic and functional traits responses of Sphagnum peatland testate amoebae to experimentally manipulated water table. Acta Protozool. 56:191–210. https://doi.org/10.1016/j.ecolind.2017.10.017

    Article  CAS  Google Scholar 

  8. Lamentowicz M, Mitchell EA (2005) The ecology of testate amoebae (Protists) in Sphagnum in north-western Poland in relation to peatland ecology. Microb. Ecol. 50:48–63. https://doi.org/10.1007/s00248-004-0105-8

    Article  PubMed  Google Scholar 

  9. Payne RJ, Babeshko KV, van Bellen S, Jeffrey J, Blackford JJ, Booth RK, Charman DJ, Ellershaw MR, Gilbert D, Hughes PM, Jassey VEJ, Lamentowicz Ł, Lamentowicz M, Malysheva EA, Mauquoy D, Mazei Y, Mitchell EAD, Swindles GT, Tsyganov AN, Turner TE, Telford RJ (2016) Significance testing testate amoeba water table reconstructions. Quaternary Sci Rev 138:131–135. https://doi.org/10.1016/j.quascirev.2016.01.030

    Article  Google Scholar 

  10. Swindles GT, Morris PJ, Mullan DJ, Payne RJ, Roland TP, Amesbury MJ, Lamentowicz M, Turner TE, Gallego-Sala A, Sim T, Barr ID, Blaauw M, Blundell A, Chambers FM, Charman DJ, Feurdean A, Galloway JM, Galka M, Green SM, Kajukalo K, Karofeld E, Korhola A, Lamentowicz L, Langdon P, Marcisz K, Mauquoy D, Mazei YA, Mckeown MM, Mitchell EAD, Plunkett G, Roe HM, Schoning K, Sillasoo U, Tsyganov AN, Van der Linden M, Väliranta M, Wanner B (2019) Widespread drying of European peatlands in recent centuries. Nat. Geosci. 12:922–928. https://doi.org/10.1038/s41561-019-0462-z

    Article  CAS  Google Scholar 

  11. Burki F, Roger AJ, Brown MW, Simpson AG (2020) The new tree of eukaryotes. Trends Ecol. Evol. 35:43–55. https://doi.org/10.1016/j.tree.2019.08.008

    Article  PubMed  Google Scholar 

  12. Adl SM, Simpson AGB, Lane CE, Lukeš J, Bass D, Bowser SS, Brown MW, Burki F, Dunthorn M, Hampl V, Heiss A, Hoppenrath M, Lara E, le Gall L, Lynn DH, McManus H, Mitchell EAD, Mozley-Stanridge SE, Parfrey LW, Pawlowski J, Rueckert S, Shadwick L, Schoch CL, Smirnov A, Spiegel FW (2012) The revised classification of eukaryotes. J. Eukaryot. Microbiol. 59:429–493. https://doi.org/10.1111/j.1550-7408.2012.00644.x

    Article  PubMed  PubMed Central  Google Scholar 

  13. Adl SM, Bass D, Lane CE, Lukeš J, Schoch CL. Smirnov A, Agatha S, Berney C, Brow, MW, Burki F, Cárdenas P, Čepička I, Chistyakova L, del Campo J, Dunthorn M, Edvardsen B, Eglit Y, Guillou L, Hampl V, Heiss AA, Hoppenrath M, James TY, Karpov S, Kim E, Kolisko M, Kudryavtsev A, Lahr DJG, Lara E, Le Gall L, Lynn DH, Mann DG, Massana i Molera R, Mitchell EAD, Morrow C, Park JS, Pawlowski JW, Powell MJ, Richter DJ, Rueckert S, Shadwick L, Shimano S, Spiegel FW, Torruella i Cortes G, Youssef N, Zlatogursky V, Zhang Q, Zhang Q (2019) Revisions to the classification, nomenclature, and diversity of eukaryotes. J. Eukaryot. Microbiol. 66: 4–119. https://doi.org/10.1111/jeu.12691

  14. Meisterfeld R (2002a) Testate amoebae with filopodia. In: Lee JJ, Leedale GF, Bradbury P (eds) The illustrated guide to the protozoa. Society of Protozoologists, Lawrence, KS, USA, pp 1054–1084

    Google Scholar 

  15. Wanner M, Seidl-Lampa B, Höhn A, Puppe D, Meisterfeld R, Sommer M (2016) Culture growth of testate amoebae under different silicon concentrations. Eur. J. Protistol. 56:171–179. https://doi.org/10.1016/j.ejop.2016.08.008

    Article  PubMed  Google Scholar 

  16. Puppe D (2020) Review on protozoic silica and its role in silicon cycling. Geoderma 365:114224

    Article  CAS  Google Scholar 

  17. Epstein E (1999) Silicon. Annu. Rev. Plant Biol. 50:641–664

    CAS  Google Scholar 

  18. Ma JF (2004) Role of silicon in enhancing the resistance of plants to biotic and abiotic stresses. Soil Sci. Plant Nutr 50: 11–18. https://doi.org/10.1080/00380768.2004.10408447

  19. Puppe D, Sommer M (2018) Experiments, uptake mechanisms, and functioning of silicon foliar fertilization – a review focusing on maize, rice, and wheat. Adv. Agron. 152:1–49. https://doi.org/10.1016/bs.agron.2018.07.003

    Article  Google Scholar 

  20. Haynes RJ (2014) A contemporary overview of silicon availability in agricultural soils. J. Plant Nutr. Soil Sci. 177:831–844. https://doi.org/10.1002/jpln.201400202

    Article  CAS  Google Scholar 

  21. Haynes RJ (2017) The nature of biogenic Si and its potential role in Si supply in agricultural soils. Agric. Ecosyst. Environ. 245:100–111. https://doi.org/10.1016/j.agee.2017.04.021

    Article  CAS  Google Scholar 

  22. Qin Y, Puppe D, Payne R, Li L, Li J, Zhang Z, Xie S (2020) Land-use change effects on protozoic silicon pools in the Dajiuhu National Wetland Park, China. Geoderma 368:114305. https://doi.org/10.1016/j.geoderma.2020.114305

    Article  CAS  Google Scholar 

  23. Keller C, Guntzer F, Barboni D, Labreuche J, Meunier JD (2012) Impact of agriculture on the Si biogeochemical cycle: input from phytolith studies. Compt. Rendus Geosci 344: 739–746. https://doi.org/10.1016/j.crte.2012.10.004

  24. Meunier JD, Guntzer F, Kirman S, Keller C (2008) Terrestrial plant-Si and environmental changes. Mineral. Mag. 72:263–267. https://doi.org/10.1180/minmag.2008.072.1.263

    Article  CAS  Google Scholar 

  25. Vandevenne F, Struyf E, Clymans W, Meire P (2012) Agricultural silica harvest: have humans created a new loop in the global silica cycle? Front. Ecol. Environ. 10:243–248. https://doi.org/10.1890/110046

    Article  Google Scholar 

  26. Puppe D, Kaczorek D, Wanner M, Sommer M (2014) Dynamics and drivers of the protozoic Si pool along a 10-year chronosequence of initial ecosystem states. Ecol. Eng. 70:477–482. https://doi.org/10.1016/j.ecoleng.2014.06.011

    Article  Google Scholar 

  27. Puppe D, Höhn A, Kaczorek D, Wanner M, Sommer M (2016) As time goes by – spatiotemporal changes of biogenic Si pools in initial soils of an artificial catchment in NE Germany. Appl. Soil Ecol 105: 9–16. https://doi.org/10.1016/j.apsoil.2016.01.020

  28. Puppe D, Höhn A, Kaczorek D, Wanner M, Wehrhan M, Sommer M (2017) How big is the influence of biogenic silicon pools on short-term changes in water-soluble silicon in soils? Implications from a study of a 10-year-old soil–plant system. Biogeosciences 14:5239–5252. https://doi.org/10.5194/bg-14-5239-2017

    Article  CAS  Google Scholar 

  29. Creevy AL, Fisher J, Puppe D, Wilkinson DM (2016) Protist diversity on a nature reserve in NW England — with particular reference to their role in soil biogenic silicon pools. Pedobiologia 59:51–59. https://doi.org/10.1016/j.pedobi.2016.02.001

    Article  Google Scholar 

  30. Cui Y, Jiang C (2018) Growing Sphagnum, transform herbs into treasure. Rural Baishitong, 16: 13. https://doi.org/10.19433/j.cnki.1006-9119.2018.16.004(In Chinese)

  31. Xie S, Evershed RP, Huang X, Zhu Z, Pancost RD, Meyers PA, Gong L, Hu C, Huang J, Zhang S, Gu Y, Zhu J (2013) Concordant monsoon-driven postglacial hydrological changes in peat and stalagmite records and their impacts on prehistoric cultures in central China. Geology 41:827–830. https://doi.org/10.1130/G34318.1

    Article  Google Scholar 

  32. Qin Y, Mitchell EAD, Lamentowicz M, Payne RJ, Lara E, Gu Y, Huang X, Wang H (2013) Ecology of testate amoebae in peatlands of central China and development of a transfer function for paleohydrological reconstruction. J. Paleolimnol. 50:319–330. https://doi.org/10.1007/s10933-013-9726-6

    Article  Google Scholar 

  33. Booth RK (2001) Ecology of testate amoebae (protozoa) in two Lake Superior coastal wetlands: implications for palaeoecology and environmental monitoring. Wetlands 21:564–576. https://doi.org/10.1672/0277-5212(2001)021[0564:eotapi]2.0.co;2

    Article  Google Scholar 

  34. Payne R, Charman DJ, Matthews S, Eastwood W (2008) Testate amoebae as palaeoclimate proxies in sürmene ağaçbaşi Yaylasi peatland (Northeast Turkey). Wetlands 28:311–323. https://doi.org/10.1672/07-42.1

    Article  Google Scholar 

  35. Mazei Y, Chernyshov V, Tsyganov AN, Payne RJ (2015) Testing the effect of refrigerated storage on testate amoeba samples. Microb. Ecol. 70:861–864. https://doi.org/10.1007/s00248-015-0628-1

    Article  PubMed  Google Scholar 

  36. Payne RJ, Mitchell EAD (2009) How many is enough? Determining optimal count totals for ecological and palaeoecological studies of testate amoebae. J. Paleolimnol. 42:483–495. https://doi.org/10.1007/s10933-008-9299-y

    Article  Google Scholar 

  37. Charman DJ, Hendon D, Woodland WA (2000) The identification of testate amoebae (Protozoa: Rhizopoda) in peats: quaternary research association

  38. Meisterfeld R (2002b) Order Arcellinida Kent, 1880. In: Lee JJ, Leedale GF, Bradbury P (eds) The illustrated guide to the Protozoa. Society of Protozoologists, Lawrence, KS, USA, pp 827–860

    Google Scholar 

  39. Mazei Y, Tsyganov AN (2006) Freshwater testate amoebae. Moscow, KMK

    Google Scholar 

  40. Shannon CE, Weaver W (1949) The mathematical theory of communication. University of Illinois Press, Urbana

    Google Scholar 

  41. Aoki Y, Hoshino M, Matsubara T (2007) Silica and testate amoebae in a soil under pine-oak forest. Geoderma 142:29–35. https://doi.org/10.1016/j.geoderma.2007.07.009

    Article  CAS  Google Scholar 

  42. Puppe D, Ehrmann O, Kaczorek D, Wanner M, Somme M (2015) The protozoic Si pool in temperate forest ecosystems – quantification, abiotic controls and interactions with earthworms. Geoderma 243-244:196–204. https://doi.org/10.1016/j.geoderma.2014.12.018

    Article  CAS  Google Scholar 

  43. Lamentowicz M, Obremska M, Mitchell EAD (2008) Autogenic succession, land-use change, and climatic influences on the Holocene development of a kettle-hole mire in northern Poland. Rev. Palaeobot. Palyno 151:21–40. https://doi.org/10.1016/j.revpalbo.2008.01.009

    Article  Google Scholar 

  44. Urbanová B, Bárta J (2020) Recovery of methanogenic community and its activity in long-term drained peatlands after rewetting. Ecol. Eng. 180:105852. https://doi.org/10.1016/j.ecoleng.2020.105852

    Article  Google Scholar 

  45. Qin Y, Man B, Kosakyan A, Lara E, Gu Y, Wang H, Mitchell EAD (2016) Nebela jiuhuensis nov. sp. (Amoebozoa; Arcellinida; Hyalospheniidae): a new member of the Nebela saccifera-equicalceus-ansata group described from Sphagnum peatlands in south-Central China. J. Eukaryot. Microbiol. 63:558–566. https://doi.org/10.1111/jeu.12300

    Article  CAS  PubMed  Google Scholar 

  46. Remm L, Lõhmus A, Leibak E, Kohv M, Salm J, Lõhmus P, Rosenvald R, Runnel K, Vellak K, Ranna R (2019) Restoration dilemmas between future ecosystem and current species values: the concept and a practical approach in Estonian mires. J. Environ. Manag. 250:109439. https://doi.org/10.1016/j.jenvman.2019.109439

    Article  Google Scholar 

  47. Herrmann S, Fox JM (2014) Assessment of rural livelihoods in south-West China based on environmental, economic, and social indicators. Ecol. Indic. 36:746–748. https://doi.org/10.1016/j.ecolind.2013.06.006

    Article  Google Scholar 

  48. Robroek BJM, van Ruijven J, Schouten MGC, Breeuwer A, Crushell PH, Berendse F, Limpens J (2009) Sphagnum re-introduction in degraded peatlands: the effects of aggregation, species identity and water table. Basic Appl Ecol 10:697–706. https://doi.org/10.1016/j.baae.2009.04.005

    Article  Google Scholar 

  49. Pouliot R, Hugron S, Rochefort L (2015) Sphagnum farming: a long-term study on producing peat moss biomass sustainably. Ecol. Eng. 74:135–147. https://doi.org/10.1016/j.ecoleng.2014.10.007

    Article  Google Scholar 

  50. Andersen R, Grasset L, Thormann MN, Rochefort L, Francez A (2010) Changes in microbial community structure and function following Sphagnum peatland restoration. Soil Biol. Biochem. 42:291–301. https://doi.org/10.1016/j.soilbio.2009.11.006

    Article  CAS  Google Scholar 

  51. Putkinen A, Tuittila E, Siljanen HMP, Bodrossy L, Fritze H (2018) Recovery of methane turnover and the associated microbial communities in restored cutover peatlands is strongly linked with increasing Sphagnum abundance. Soil Biol. Biochem. 116:110–119. https://doi.org/10.1016/j.soilbio.2017.10.005

    Article  CAS  Google Scholar 

  52. Creevy A, Payne RJ, Andersen R, Rowson JG (2020) Annual gaseous carbon budgets of forest-to-bog restoration sites are strongly determined by vegetation composition. Sci. Total Environ. 705:135863. https://doi.org/10.1016/j.scitotenv.2019.135863

    Article  CAS  PubMed  Google Scholar 

  53. Gaffney PPJ, Hancock MH, Taggart MA, Andersen R (2018) Measuring restoration progress using pore- and surface-water chemistry across a chronosequence of formerly afforested blanket bogs. J. Environ. Manag. 219:239–251. https://doi.org/10.1016/j.jenvman.2018.04.106

    Article  CAS  Google Scholar 

  54. Creevy AL, Andersen R, Rowson JG, Payne RJ (2018) Testate amoebae as functionally significant bioindicators in forest-to-bog restoration. Ecol. Indic. 84:274–282. https://doi.org/10.1016/j.ecolind.2017.08.062

    Article  Google Scholar 

  55. Markel E, Booth RK, Qin Y (2010) Testate amoebae and 13C of Sphagnum as surface moisture proxies in Alaskan peatlands. Holocene 20:463–475. https://doi.org/10.1177/0959683609354303

    Article  Google Scholar 

  56. Meyer C, Gilbert D, Gillet F, Moskura M, Franchi M, Bernard N (2012) Using “bryophytes and their associated testate amoeba” microsystems as indicators of atmospheric pollution. Ecol. Indic. 13:144–151. https://doi.org/10.1016/j.ecolind.2011.05.020

    Article  CAS  Google Scholar 

  57. Wanner M, Birkhofer K, Fischer T, Shimizu M, Shimano S, Puppe D (2020a) Soil testate amoebae and diatoms as bioindicators of an old heavy metal contaminated floodplain in Japan. Microb. Ecol. 79:123–133. https://doi.org/10.1007/s00248-019-01383-x

    Article  CAS  PubMed  Google Scholar 

  58. Krashevska V, Klarner B, Widyastuti R, Maraun M, Scheu S (2016) Changes in structure and functioning of protist (testate amoebae) communities due to conversion of lowland rainforest into rubber and oil palm plantations. PLoS One 11:e0160179. https://doi.org/10.1371/journal.pone.0160179

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Wanner M, Birkhofer K, Puppe D, Shimano SD, Shimizu M (2020b) Tolerance of testate amoeba species to rising sea levels under laboratory conditions and in the South Pacific. Pedobiologia 79:150610. https://doi.org/10.1016/j.pedobi.2019.150610

    Article  Google Scholar 

  60. Fournier B, Malysheva E, Mazei Y, Moretti M, Mitchell EAD (2012) Toward the use of testate amoeba functional traits as indicator of floodplain restoration success. Eur. J. Soil Biol. 49:85–91. https://doi.org/10.1016/j.ejsobi.2011.05.008

    Article  Google Scholar 

  61. Wanner M, Elmer M, Sommer M, Funk R, Puppe D (2015) Testate amoebae colonizing a newly exposed land surface are of airborne origin. Ecol. Indic. 48:55–62. https://doi.org/10.1016/j.ecolind.2014.07.037

    Article  Google Scholar 

  62. Wanner M, Elmer M, Kazda M, Xylander WE (2008) Community assembly of terrestrial testate amoebae: how is the very first beginning characterized? Microb. Ecol 56: 43–54. https://doi.org/10.1007/s00248-007-9322-2

  63. Kosakyan A, Lahr DJ, Mulot M, Meisterfeld R, Mitchell EA, Lara E (2016) Phylogenetic reconstruction based on COI reshuffles the taxonomy of hyalosphenid shelled (testate) amoebae and reveals the convoluted evolution of shell plate shapes. Cladistics 32:606–623

    Article  Google Scholar 

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Acknowledgments

We are grateful to three anonymous reviewers for their constructive comments, which improved the quality of this paper.

Funding

This work was supported by the National Science Foundation of China (NO. 41502167) and the “111 project” of China (grant No. BP0820004). DP was funded by the Deutsche Forschungsgemeinschaft (DFG) under grant PU 626/2-1 (Biogenic Silicon in Agricultural Landscapes (BiSiAL)–Quantification, Qualitative Characterization, and Importance for Si Balances of Agricultural Biogeosystems).

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Qin, Y., Puppe, D., Zhang, L. et al. How Does Sphagnum Growing Affect Testate Amoeba Communities and Corresponding Protozoic Si Pools? Results from Field Analyses in SW China. Microb Ecol 82, 459–469 (2021). https://doi.org/10.1007/s00248-020-01668-6

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