Microbial Ecology

, Volume 77, Issue 4, pp 1014–1024 | Cite as

Small-scale Variation of Testate Amoeba Assemblages: the Effect of Site Heterogeneity and Empty Shell Inclusion

  • Zuzana LizoňováEmail author
  • Marie Zhai
  • Jindřiška Bojková
  • Michal Horsák
Soil Microbiology


Studies on testate amoeba species distribution at small scales (i.e., single peatland sites) are rare and mostly focus on bogs or mineral-poor Sphagnum fens, leaving spatial patterns within mineral-rich fens completely unexplored. In this study, two mineral-rich fen sites of contrasting groundwater chemistry and moss layer composition were selected for the analysis of testate amoeba compositional variance within a single site. At each study site, samples from 20 randomly chosen moss-dominated plots were collected with several environmental variables being measured at each sampling spot. We also distinguished between empty shells and living individuals to evaluate the effect of empty shell inclusion on recorded species distribution. At the heterogeneous-rich Sphagnum-fen, a clear composition turnover in testate amoebae between Sphagnum-dominated and brown moss-dominated samples was closely related to water pH, temperature and redox potential. We also found notable species composition variance within the homogeneous calcareous fen, yet it was not as high as for the former site and the likely drivers of community assembly remained unidentified. The exclusion of empty shells provided more accurate data on species distribution as well as their relationship with some environmental variables, particularly moisture. Small-scale variability in species composition of communities seems to be a worthwhile aspect in testate amoeba research and should be considered in future sampling strategies along with a possible empty shell bias for more precise understanding of testate amoeba ecology and paleoecology.


Testate amoebae Fens Peatlands Empty shells Small-scale variability 



Special thanks goes to Eva Kristová for her help with the field and laboratory work as well as the moss identification, to Anna Šímová for her help with testate amoeba taxonomy, and to Ondřej Hájek for his help with GIS and the study site map. For technical and laboratory support, we would like to thank Marcela Růžičková and Zuzana Formánková. Also, we would like to thank the reviewers for their comments and suggestions that helped to improve the manuscript.

Funding Information

This study was supported by the institutional support for Ph.D. students at the Masaryk University and the Czech Science Foundation (project no. P505/16-03881S).

Supplementary material

248_2018_1292_MOESM1_ESM.docx (21 kb)
ESM 1 (DOCX 20 kb)


  1. 1.
    Mitchell EAD, Borcard D, Buttler AJ, Grosvernier P, Gilbert D, Gobat J (2000) Horizontal distribution patterns of testate amoebae (Protozoa) in a Sphagnum magellanicum carpet. Microb Ecol 39:290–300PubMedGoogle Scholar
  2. 2.
    Booth RK, Zygmunt JR (2005) Biogeography and comparative ecology of testate amoebae inhabiting Sphagnum-dominated peatlands in the Great Lakes and Rocky Mountain regions of North America. Divers Distrib 11:577–590. CrossRefGoogle Scholar
  3. 3.
    Bobrov AA, Charman DJ, Warner BG (1999) Ecology of testate amoebae (Protozoa : Rhizopoda) on peatlands in western Russia with special attention to niche separation in closely related taxa. Protist 150:125–136CrossRefPubMedGoogle Scholar
  4. 4.
    Jassey VEJ, Lamentowicz L, Robroek BJM, Gąbka M, Rusińska A, Lamentowicz M (2014) Plant functional diversity drives niche-size-structure of dominant microbial consumers along a poor to extremely rich fen gradient. J Ecol 102:1150–1162. CrossRefGoogle Scholar
  5. 5.
    Lamentowicz L, Gabka M, Rusinska A et al (2011) Testate amoeba (Arcellinida, Euglyphida) ecology along a poor-rich gradient in fens of western Poland. Int Rev Hydrobiol 96:356–380. CrossRefGoogle Scholar
  6. 6.
    Lamentowicz M, Lamentowicz L, van der Knaap WO, Gąbka M, Mitchell EAD (2010) Contrasting species-environment relationships in communities of testate amoebae, bryophytes and vascular plants along the fen-bog gradient. Microb Ecol 59:499–510. CrossRefPubMedGoogle Scholar
  7. 7.
    Lamentowicz M, Mitchell EAD (2005) The ecology of testate amoebae (protists) in Sphagnum in North-Western Poland in relation to peatland ecology. Microb Ecol 50:48–63. CrossRefPubMedGoogle Scholar
  8. 8.
    Opravilová V, Hájek M (2006) The variation of testacean assemblages (Rhizopoda) along the complete base-richness gradient in fens: a case study from the Western Carpathians. Acta Protozool 45:191–204Google Scholar
  9. 9.
    Kishaba K, Mitchell EAD (2005) Changes in testate amoebae (Protists) communities in a small raised bog. A 40-year study. Acta Protozool 44:1–12Google Scholar
  10. 10.
    Niedźwiecki M, Mieczan T, Adamczuk M (2016) Ecology of testate amoebae (Protists) in a Sphagnum-dominated peat bog and the relationship between species assemblages and environmental parameters. Oceanol Hydrobiol Stud 45(344).
  11. 11.
    Marcisz K, Lamentowicz L, Slowinska S et al (2014) Seasonal changes in Sphagnum peatland testate amoeba communities along a hydrological gradient. Eur J Protistol 50:445–455. CrossRefPubMedGoogle Scholar
  12. 12.
    Jassey VEJ, Chiapusio G, Mitchell EAD, Binet P, Toussaint ML, Gilbert D (2011) Fine-scale horizontal and vertical micro-distribution patterns of testate amoebae along a narrow fen/bog gradient. Microb Ecol 61:374–385. CrossRefPubMedGoogle Scholar
  13. 13.
    Hájek M, Horsák M, Hájková P, Dítě D (2006) Habitat diversity of central European fens in relation to environmental gradients and an effort to standardise fen terminology in ecological studies. Perspect Plant Ecol Evol Syst 8:97–114. CrossRefGoogle Scholar
  14. 14.
    Křoupalová V, Opravilová V, Bojková J, Horsák M (2013) Diversity and assemblage patterns of microorganisms structured by the groundwater chemistry gradient in spring fens. Ann Limnol Int J Limnol 49:207–223. CrossRefGoogle Scholar
  15. 15.
    Lamers LPM, Vile MA, Grootjans AP, Acreman MC, van Diggelen R, Evans MG, Richardson CJ, Rochefort L, Kooijman AM, Roelofs JGM, Smolders AJP (2015) Ecological restoration of rich fens in Europe and North America: from trial and error to an evidence-based approach. Biol Rev 90:182–203. CrossRefPubMedGoogle Scholar
  16. 16.
    Peterka T, Hájek M, Jiroušek M, Jiménez-Alfaro B, Aunina L, Bergamini A, Dítě D, Felbaba-Klushyna L, Graf U, Hájková P, Hettenbergerová E, Ivchenko TG, Jansen F, Koroleva NE, Lapshina ED, Lazarević PM, Moen A, Napreenko MG, Pawlikowski P, Plesková Z, Sekulová L, Smagin VA, Tahvanainen T, Thiele A, Biţǎ-Nicolae C, Biurrun I, Brisse H, Ćušterevska R, de Bie E, Ewald J, FitzPatrick Ú, Font X, Jandt U, Kącki Z, Kuzemko A, Landucci F, Moeslund JE, Pérez-Haase A, Rašomavičius V, Rodwell JS, Schaminée JHJ, Šilc U, Stančić Z, Chytrý M (2017) Formalized classification of European fen vegetation at the alliance level. Appl Veg Sci 20:124–142. CrossRefGoogle Scholar
  17. 17.
    Lamentowicz M, Bragazza L, Buttler A, Jassey VEJ, Mitchell EAD (2013) Seasonal patterns of testate amoeba diversity, community structure and species-environment relationships in four Sphagnum-dominated peatlands along a 1300 m altitudinal gradient in Switzerland. Soil Biol Biochem 67:1–11. CrossRefGoogle Scholar
  18. 18.
    Lahr DJG, Parfrey LW, Mitchell EAD, Katz LA, Lara E (2011) The chastity of amoebae: re-evaluating evidence for sex in amoeboid organisms. Proc R Soc B Biol Sci 278:2081–2090. CrossRefGoogle Scholar
  19. 19.
    Mazei YA, Tsyganov AN (2006) Freshwater testate amoebae. KMK, MoscowGoogle Scholar
  20. 20.
    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. CrossRefGoogle Scholar
  21. 21.
    Wilkinson DM, Koumoutsaris S, Mitchell EAD, Bey I (2012) Modelling the effect of size on the aerial dispersal of microorganisms. J Biogeogr 39:89–97. CrossRefGoogle Scholar
  22. 22.
    Wilkinson DM (2010) Have we underestimated the importance of humans in the biogeography of free-living terrestrial microorganisms? J Biogeogr 37:393–397. CrossRefGoogle Scholar
  23. 23.
    Fournier B, Coffey EED, van der Knaap WO, Fernández LD, Bobrov A, Mitchell EAD (2016) A legacy of human-induced ecosystem changes: spatial processes drive the taxonomic and functional diversities of testate amoebae in Sphagnum peatlands of the Galápagos. J Biogeogr 43:533–543. CrossRefGoogle Scholar
  24. 24.
    Mitchell EAD, Buttler A, Grosvernier P et al (2000) Relationships among testate amoebae (Protozoa), vegetation and water chemistry in five Sphagnum-dominated peatlands in Europe. New Phytol 145:95–106. CrossRefGoogle Scholar
  25. 25.
    Sullivan ME, Booth RK (2011) The potential influence of short-term environmental variability on the composition of testate amoeba communities in Sphagnum peatlands. Microb Ecol 62:80–93. CrossRefPubMedGoogle Scholar
  26. 26.
    Jassey VEJ, Gilbert D, Binet P, Toussaint ML, Chiapusio G (2011) Effect of a temperature gradient on Sphagnum fallax and its associated living microbial communities: a study under controlled conditions. Can J Microbiol 57:226–235. CrossRefPubMedGoogle Scholar
  27. 27.
    Krashevska V, Sandmann D, Maraun M, Scheu S (2014) Moderate changes in nutrient input alter tropical microbial and protist communities and belowground linkages. ISME J 8:1126–1134CrossRefPubMedGoogle Scholar
  28. 28.
    Marcisz K, Fournier B, Gilbert D, Lamentowicz M, Mitchell EAD (2014) Response of Sphagnum peatland testate amoebae to a 1-year transplantation experiment along an artificial hydrological gradient. Microb Ecol 67:810–818. CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Payne R, Gauci V, Charman DJ (2010) The impact of simulated sulfate deposition on peatland testate amoebae. Microb Ecol 59:76–83. CrossRefPubMedGoogle Scholar
  30. 30.
    Song L, Li H, Wang K, Yan X, Wu D (2018) Seasonal dynamics in the community structure and trophic structure of testate amoebae inhabiting the Sanjiang peatlands, Northeast China. Eur J Protistol 63:51–61. CrossRefPubMedGoogle Scholar
  31. 31.
    Swindles GT, Green SM, Brown L, Holden J, Raby CL, Turner TE, Smart R, Peacock M, Baird AJ (2016) Evaluating the use of dominant microbial consumers (testate amoebae) as indicators of blanket peatland restoration. Ecol Indic 69:318–330. CrossRefGoogle Scholar
  32. 32.
    Schönfeld J, Alve E, Geslin E, Jorissen F, Korsun S, Spezzaferri S (2012) The FOBIMO (FOraminiferal BIo-MOnitoring) initiative - towards a standardised protocol for soft-bottom benthic foraminiferal monitoring studies. Mar Micropaleontol 94–95:1–13. CrossRefGoogle Scholar
  33. 33.
    Decloitre L (1962) Le genre Euglypha Dujardin. Arch Protistenkd 106:51–100Google Scholar
  34. 34.
    Mitchell EAD (2002) The identification of Centropyxis, Cyclopyxis, Trigonopyxis and similar Phryganella species living in Sphagnum. International Society for Testate Amoeba Research (ISTAR). Accessed May 2012
  35. 35.
    Mitchell EAD (2002) The identification of Heleopera species living in Sphagnum. International Society for Testate Amoeba Research (ISTAR). Accessed May 2012
  36. 36.
    Mitchell EAD (2003) The identification of Nebela and similar species with indications on their ecology and distribution. International Society for Testate Amoeba Research (ISTAR). Accessed May 2012
  37. 37.
    Ogden CG (1983) Observations on the systematics of the genus Difflugia in Britain (Rhizopoda, Protozoa). Bull Br Mus Nat Hist (Zool) 44:1–73Google Scholar
  38. 38.
    Ogden CG, Hedley RH (1980) An atlas of freshwater testate amoebae. Oxford University Press [for the] British Museum (Natural History), OxfordCrossRefGoogle Scholar
  39. 39.
    Siemensma FJ (2018) Microworld, world of amoeboid organisms. Accessed April 2008
  40. 40.
    Kosakyan A, Lahr DJG, Mulot M, Meisterfeld R, Mitchell EAD, 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. CrossRefGoogle Scholar
  41. 41.
    RCoreTeam (2017) R: a language and environment for statistical computing. R Foundation for statistical computing, ViennaGoogle Scholar
  42. 42.
    Oksanen J, Blanchet FG, Friendly M, et al (2017) Vegan: community ecology package. R package version 2.4–3Google Scholar
  43. 43.
    Dray S, Legendre P, Blanchet G (2013) packfor: Forward Selection with permutation (Canoco p.46). R package version 0.0-8/r109Google Scholar
  44. 44.
    Sjörs H (1950) On the relation between vegetation and electrolytes in north Swedish mire waters. Oikos 2:241–258. CrossRefGoogle Scholar
  45. 45.
    Warner BG, Asada T, Quinn NP (2007) Seasonal influences on the ecology of testate amoebae (Protozoa) in a small Sphagnum peatland in Southern Ontario, Canada. Microb Ecol 54:91–100. CrossRefPubMedGoogle Scholar
  46. 46.
    Hájková P, Bojková J, Fránková M et al (2011) Disentangling the effects of water chemistry and substratum structure on moss-dwelling unicellular and multicellular micro-organisms in spring-fens. J Limnol 70:54–64. CrossRefGoogle Scholar
  47. 47.
    Payne RJ (2011) Can testate amoeba-based palaeohydrology be extended to fens? J Quat Sci 26:15–27. CrossRefGoogle Scholar
  48. 48.
    Lamentowicz L, Gabka M, Lamentowicz M (2007) Species composition of testate amoebae (Protists) and environmental parameters in a Sphagnum peatland. Pol J Ecol 55:749–759Google Scholar
  49. 49.
    Ulanowski TA, Branfireun BA (2013) Small-scale variability in peatland pore-water biogeochemistry, Hudson Bay Lowland, Canada. Sci Total Environ 454:211–218. CrossRefPubMedGoogle Scholar
  50. 50.
    Marcisz K, Colombaroli D, Jassey VEJ, Tinner W, Kołaczek P, Gałka M, Karpińska-Kołaczek M, Słowiński M, Lamentowicz M (2016) A novel testate amoebae trait-based approach to infer environmental disturbance in Sphagnum peatlands. Sci Rep 6:33907CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Jassey VEJ, Signarbieux C, Hättenschwiler S, Bragazza L, Buttler A, Delarue F, Fournier B, Gilbert D, Laggoun-Défarge F, Lara E, T. E. Mills R, Mitchell EAD, Payne RJ, Robroek BJM (2015) An unexpected role for mixotrophs in the response of peatland carbon cycling to climate warming. Sci Rep 5:16931CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Payne RJ (2013) Seven reasons why protists make useful bioindicators. Acta Protozool 52:105–113. CrossRefGoogle Scholar
  53. 53.
    Roe HM, Elliott SM, Patterson RT (2017) Re-assessing the vertical distribution of testate amoeba communities in surface peats: implications for palaeohydrological studies. Eur J Protistol 60:13–27. CrossRefPubMedGoogle Scholar
  54. 54.
    Koenig I, Mulot M, Mitchell EAD (2018) Taxonomic and functional traits responses of Sphagnum peatland testate amoebae to experimentally manipulated water table. Ecol Indic 85:342–351. CrossRefGoogle Scholar
  55. 55.
    Charman DJ (2001) Biostratigraphic and palaeoenvironmental applications of testate amoebae. Quat Sci Rev 20:1753–1764. CrossRefGoogle Scholar
  56. 56.
    Hájková P, Grootjans AB, Lamentowicz M, Rybníčková E, Madaras M, Opravilová V, Michaelis D, Hájek M, Joosten H, Wołejko L (2012) How a Sphagnum fuscum-dominated bog changed into a calcareous fen: the unique Holocene history of a Slovak spring-fed mire. J Quat Sci 27:233–243. CrossRefGoogle Scholar
  57. 57.
    Mitchell EAD, Payne RJ, van der Knaap WO, Lamentowicz Ł, Gąbka M, Lamentowicz M (2013) The performance of single- and multi-proxy transfer functions (testate amoebae, bryophytes, vascular plants) for reconstructing mire surface wetness and pH. Quat Res 79:6–13. CrossRefGoogle Scholar
  58. 58.
    Vitt DH (1990) Growth and production dynamics of boreal mosses over climatic, chemical and topographic gradients. Bot J Linn Soc 104:35–59. CrossRefGoogle Scholar
  59. 59.
    Mitchell EAD, Charman DJ, Warner BG (2008) Testate amoebae analysis in ecological and paleoecological studies of wetlands: past, present and future. Biodivers Conserv 17:2115–2137. CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Botany and Zoology, Faculty of ScienceMasaryk UniversityBrnoCzech Republic

Personalised recommendations