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
Struyf E, Conley DJ (2009) Silica: an essential nutrient in wetland biogeochemistry. Front Ecol Env 7:88–94. https://doi.org/10.2307/25595061
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
Carey JC, Fulweiler RW (2012) The terrestrial silica pump. PLoS One 7:e52932. https://doi.org/10.1371/journal.pone.0052932
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
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
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
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
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
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
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
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
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
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
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
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
Puppe D (2020) Review on protozoic silica and its role in silicon cycling. Geoderma 365:114224
Epstein E (1999) Silicon. Annu. Rev. Plant Biol. 50:641–664
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
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
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
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
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
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
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
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
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
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
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
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
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)
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
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
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
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
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
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
Charman DJ, Hendon D, Woodland WA (2000) The identification of testate amoebae (Protozoa: Rhizopoda) in peats: quaternary research association
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
Mazei Y, Tsyganov AN (2006) Freshwater testate amoebae. Moscow, KMK
Shannon CE, Weaver W (1949) The mathematical theory of communication. University of Illinois Press, Urbana
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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We are grateful to three anonymous reviewers for their constructive comments, which improved the quality of this paper.
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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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DOI: https://doi.org/10.1007/s00248-020-01668-6