Advertisement

Microbial Ecology

, Volume 79, Issue 1, pp 123–133 | Cite as

Soil Testate Amoebae and Diatoms as Bioindicators of an Old Heavy Metal Contaminated Floodplain in Japan

  • Manfred WannerEmail author
  • Klaus Birkhofer
  • Thomas Fischer
  • Miki Shimizu
  • Satoshi Shimano
  • Daniel Puppe
Soil Microbiology

Abstract

Soil protists are rarely included in ecotoxicological investigations, despite their fundamental role in ecological processes. Moreover, testate amoebae and diatoms contribute considerably to silicon fluxes in soils. We investigated the effects of heavy metals on testate amoebae (species and individual densities) and diatoms (individual densities) in aged soils of a floodplain (Watarase retarding basin, Japan) taking soil samples from two unpolluted reference sites and two polluted sites. The total concentrations of Cu, Pb, and Zn in soil were higher at the polluted sites as compared with the reference sites. The available concentrations of Co, Cu, and Zn in CaCl2 extracts were higher at the polluted sites but available Pb was not detectable. Testate amoeba taxonomic richness was higher in the reference sites (45/38 taxa) than in the polluted sites (36/27 taxa). The reference sites had higher diatom and amoeba densities than the polluted sites. There was a significant negative correlation between total testate amoeba density and heavy metal concentration (available Co), while significant negative correlations were found between diatom density and Co, Cu, and Zn (available and total concentration). Densities of Cyclopyxis kahli cyclostoma, Centropyxis spp., and Trinema complanatum were negatively correlated to concentrations of available heavy metals. The observed decrease in individual numbers due to heavy metal pollution resulted in a considerable decline in protozoic (testate amoebae) and protophytic (pennate diatoms) silicon pools. Our data suggest that heavy metal pollution affects biogeochemical cycling in this system.

Keywords

Soil protists Heavy metals Silicon Aged soils Floodplain 

Notes

Acknowledgements

We greatly thank Dr. Takafumi Kamitani (Shizuoka Institute of Environment and Hygiene) and Prof. Nobuhiro Kaneko (Faculty of Food and Agricultural Sciences, Fukushima University) for coordinates of Watarase sites and local authorities for soil sampling permission. We thank for permission from the Tonegawa Upstream Office of River, Kanto Regional Development Bureau, Ministry of Land, Infrastructure, Transport and Tourism and support by Mr. Takashi Yamada of the office. The laboratory team of the Dept. Soil Protection and Recultivation, BTU Cottbus-Senftenberg, kindly conducted the heavy metal analyses.

Funding Information

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). This study was supported by The Japan Society for the Promotion of Science (JSPS, grant number S16738, MW) and by the JSPS KAKENHI (15H02858, SS).

References

  1. 1.
    Cachada A, Rocha-Santos T, Duarte AC (2018) Soil and pollution: an introduction to the main issues. In: Cachada A, Rocha-Santos T, Duarte AC (eds) Soil pollution. From monitoring to remediation. London, San Diego, Cambridge, Oxford, Elsevier, pp 1–28Google Scholar
  2. 2.
    Smolders E, Oorts K, Van Sprang P, Schoeters I, Janssen CR, McGrath SP, McLaughlin MJ (2009) Toxicity of trace metals in soil as affected by soil type and aging after contamination: using calibrated bioavailability models to set ecological soil standards. Environ Toxicol Chem 28:1633–1642PubMedGoogle Scholar
  3. 3.
    Haimi J (2000) Decomposer animals and bioremediation of soils. Environ Pollut 107:233–238PubMedGoogle Scholar
  4. 4.
    Kamitani T, Oba H, Kaneko N (2006) Microbial biomass and tolerance of microbial community of an aged heavy metal polluted floodplain in Japan. Water Air Soil Pollut 172:185–200Google Scholar
  5. 5.
    Geisen S, Mitchell EAD, Adl S, Bonkowski M, Dunthorn M, Ekelund F, Fernández LD, Jousset A, Krashevska V, Singer D, Spiegel FW, Walochnik J, Lara E (2018) Soil protists: a fertile frontier in soil biology research. FEMS Microbiol Rev 42:293–323PubMedGoogle Scholar
  6. 6.
    Foissner W (1987) Soil protozoa: fundamental problems, ecological significance, adaptations in ciliates and testaceans, bioindicators, and guide to the literature. In: Corliss JO, Patterson DJ (eds) Progress in Protistology, vol 2. Biopress, Bristol, pp 69–212Google Scholar
  7. 7.
    Ehrmann O, Puppe D, Wanner M, Kaczorek D, Sommer M (2012) Testate amoebae in 31 mature forest ecosystems — densities and micro-distribution in soils. Eur J Protistol 48:161–168PubMedGoogle Scholar
  8. 8.
    Szelecz I, Fournier B, Seppey CVW, Amendt J, Mitchell EAD (2014) Can soil testate amoebae be used for estimating the time since death? A field experiment in a deciduous forest. Forensic Sci Int 236:90–98PubMedGoogle Scholar
  9. 9.
    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, pp 1054–1084Google Scholar
  10. 10.
    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, pp 827–860Google Scholar
  11. 11.
    Adl SM, Bass D, Lane CE, Lukeš J, Schoch CL, Smirnov A, Agatha S, Berney C, Brown 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, Karnkowska A, Karpov S, Kim E, Kolisko M, Kudryavtsev A, Lahr DJG, Lara E, le Gall L, Lynn DH, Mann DG, Massana R, Mitchell EAD, Morrow C, Park JS, Pawlowski JW, Powell MJ, Richter DJ, Rueckert S, Shadwick L, Shimano S, Spiegel FW, Torruella G, Youssef N, Zlatogursky V, Zhang Q (2019) Revisions to the classification, nomenclature, and diversity of eukaryotes. J Eukaryot Microbiol 66:4–119PubMedPubMedCentralGoogle Scholar
  12. 12.
    Gomaa F, Mitchell EAD, Lara E (2013) Amphitremida (Poche, 1913) is a new major, ubiquitous labyrinthulomycete clade. PLoS One 8:e53046PubMedPubMedCentralGoogle Scholar
  13. 13.
    Patterson RT, Barker T, Burbidge SM (1996) Arcellaceans (Thecamoebians) as proxies of arsenic and mercury contamination in northeastern Ontario lakes. J Foraminiferal Res 26:172–183Google Scholar
  14. 14.
    Reinhardt EG, Dalby AP, Kumar A, Patterson RT (1998) Arcellaceans as pollution indicators in mine tailing contaminated lakes near Cobalt, Ontario, Canada. Micropaleontology 44:131–148Google Scholar
  15. 15.
    Kihlman S, Kauppila T (2009) Mine water-induced gradients in sediment metals and arcellacean assemblages in a boreal freshwater bay (Petkellahti, Finland). J Paleolimnol 42:533–550Google Scholar
  16. 16.
    Nguyen-Viet H, Bernard N, Mitchell EAD, Cortet J, Badot P-M, Gilbert D (2007) Relationship between testate amoeba (protist) communities and atmospheric heavy metals accumulated in Barbula indica (Bryophyta) in Vietnam. Microb Ecol 53:53–65PubMedGoogle Scholar
  17. 17.
    Nguyen-Viet H, Bernard N, Mitchell EAD, Badot P-M, Gilbert D (2008) Effect of lead pollution on testate amoebae communities living in Sphagnum fallax: an experimental study. Ecotoxicol Environ Saf 69:130–138PubMedGoogle Scholar
  18. 18.
    Qin Y, Payne R, Yang X, Yao M, Xue J, Gu Y, Xie S (2016) Testate amoebae as indicators of water quality and contamination in shallow lakes of the Middle and Lower Yangtze Plain. Environ Earth Sci 75:627Google Scholar
  19. 19.
    Balik V (1991) The effect of the road traffic pollution on the communities of testate amoebae (Rhizopoda, Testacea) in Warsaw (Poland). Acta Protozool 30:5–11 (German with English summary)Google Scholar
  20. 20.
    Amacker N, Mitchell EAD, Ferrari BJD, Chèvre N (2018) Development of a new ecotoxicological assay using the testate amoeba Euglypha rotunda (Rhizaria; Euglyphida) and assessment of the impact of the herbicide S-metolachlor. Chemosphere 201:351–360PubMedGoogle Scholar
  21. 21.
    Wanner M, Betker E, Shimano S, Krawczynski R (2018) Are soil testate amoebae and diatoms useful for forensics? Forensic Sci Int 289:223–231PubMedGoogle Scholar
  22. 22.
    Fernández MR, Martín G, Corzo J, de la Linde A, García E, López M, Sousa M (2018) Design and testing of a new diatom-based index for heavy metal pollution. Arch Environ Contam Toxicol 74:170–192PubMedGoogle Scholar
  23. 23.
    Schröter D, Wolters V, De Ruiter PC (2003) C and N mineralisation in the decomposer food webs of a European forest transect. Oikos 102:294–308Google Scholar
  24. 24.
    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 70:477–482Google Scholar
  25. 25.
    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(7):e0160179.  https://doi.org/10.1371/journal.pone.0160179 CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Puppe D, Ehrmann O, Kaczorek D, Wanner M, Sommer M (2015) The protozoic Si pool in temperate forest ecosystems – quantification, abiotic controls and interactions with earthworms. Geoderma 243–244:196–204Google Scholar
  27. 27.
    Tréguer PJ, De La Rocha CL (2013) The world ocean silica cycle. Annu Rev Mar Sci 5:477–501Google Scholar
  28. 28.
    Clarke J (2003) The occurrence and significance of biogenic opal in the regolith. Earth-Sci Rev 60:175–194Google Scholar
  29. 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 59:51–59Google Scholar
  30. 30.
    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 105:9–16Google Scholar
  31. 31.
    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 14:5239–5252Google Scholar
  32. 32.
    Coûteaux M-M (1978) Quelques thécamoebiens du sol du Japon. Rev Écol Biol Sol 15:119–128Google Scholar
  33. 33.
    Bobrov A, Shimano S, Mazei Y (2012) Two new species of testate amoebae from mountain forest soils of Japan and redescription of the genus Deharvengia Bonnet, 1979. Acta Protozool 51:55–63Google Scholar
  34. 34.
    Shimano S, Bobrov A, Mazei Y (2014) Testate amoebae of the Imperial Palace, Tokyo. Mem Natl Mus Nat Sci, Tokyo 50:21–28Google Scholar
  35. 35.
    Shimano S, Onodera Y, Wanner M (2017) Testate amoebae collected from moss on urban buildings with different age, height and distance to a possible source habitat – are there obvious colonization patterns? Soil Organ 89:151–155Google Scholar
  36. 36.
    Aoki Y, Hoshino M, Matsubara T (2007) Silica and testate amoebae in a soil under pine-oak forest. Geoderma 142:29–35Google Scholar
  37. 37.
    Hurlbert SH (1984) Pseudoreplication and the design of ecological field experiments. Ecol Monogr 54:187–211Google Scholar
  38. 38.
    Oksanen L (2001) Logic of experiments in ecology: is pseudoreplication a pseudoissue? Oikos 94:27–38Google Scholar
  39. 39.
    Alef K (1991) Methodenhandbuch Bodenmikrobiologie. Ecomed, LandsbergGoogle Scholar
  40. 40.
    Schönborn W (1977) Production studies on protozoa. Oecologia 27:171–184PubMedGoogle Scholar
  41. 41.
    Wanner M (1999) A review on the variability of testate amoebae: methodological approaches, environmental influences and taxonomical implications. Acta Protozool 38:15–29Google Scholar
  42. 42.
    Didier C, van der Merwe N, Betournay M, Mainz M, Kotyrba A, Oydan O, Josien J, Song W-K (2008) Mine closure and post-mining management. International state-of-the-art. International commission on mine closure. International Society for Rock Mechanics (ISRM).  https://doi.org/10.13140/2.1.3267.8407
  43. 43.
    Karasek K (2013) Environmenal disaster in Japan. Historical Perspectives: Santa Clara University Undergraduate Journal of History, series II 18(10):84–103Google Scholar
  44. 44.
    Bobrov A, Qin Y, Payne RJ (2018) A new testate amoebae species Planhoogenraadia wuchanica sp. nov. from subtropical forest soils in Wuhan, Central China. Zootaxa  https://doi.org/10.11646/zootaxa.4550.2.9 4550:289–294Google Scholar
  45. 45.
    Bobrov A, Kosakyan A (2015) A new species from mountain forest soils in Japan: Porosia paracarinata sp. nov., and taxonomic concept of the genus Porosia Jung, 1942. Acta Protozool 54:289–294Google Scholar
  46. 46.
    Puppe D, Wanner M, Sommer M (2018) Data on euglyphid testate amoeba densities, corresponding protozoic silicon pools, and selected soil parameters of initial and forested biogeosystems. Data Brief 21:1697–1703PubMedPubMedCentralGoogle Scholar
  47. 47.
    Morin S, Cordonier A, Lavoie I, Arini A, Blanco S, Duong TT, Tornés E, Bonet B, Corcoll N, Faggiano L, Laviale M, Pérès F, Becares E, Coste M, Feurtet-Mazel A, Fortin C, Guasch H, Sabater S (2012) Consistency in diatom response to metal-contaminated environments. In: Guasch H et al (eds) Emerging and priority pollutants in rivers: bringing science into river management plans. Handbook of Environmental Chemistry series, vol 19. Springer, Heidelberg, pp 117–146.  https://doi.org/10.1007/978-3-642-25722-3_5 CrossRefGoogle Scholar
  48. 48.
    Struyf E, Mörth C-M, Humborg C, Conley DJ (2010) An enormous amorphous silica stock in boreal wetlands. J Geophys Res 115:G04008.  https://doi.org/10.1029/2010JG001324 CrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  1. 1.Department EcologyBrandenburg University of Technology Cottbus-SenftenbergCottbusGermany
  2. 2.Central Analytical LaboratoryBrandenburg University of Technology Cottbus-SenftenbergCottbusGermany
  3. 3.Science Research CenterHosei UniversityTokyoJapan
  4. 4.Leibniz Centre for Agricultural Landscape Research (ZALF)MünchebergGermany

Personalised recommendations