Microbial Ecology

, Volume 71, Issue 3, pp 725–734 | Cite as

Testate Amoebae Like It Hot: Species Richness Decreases Along a Subalpine-Alpine Altitudinal Gradient in Both Natural Calluna vulgaris Litter and Transplanted Minuartia sedoides Cushions

  • T. J. Heger
  • N. Derungs
  • J .P. Theurillat
  • E. A. D. Mitchell
Soil Microbiology

Abstract

Most groups of higher organisms show a decrease in species richness toward high altitude, but the existence of such a pattern is debated for micro-eukaryotes. Existing data are scarce and mostly confounded with the diversity of habitats that also decreases with elevation. In order to disentangle these two factors, one approach is to consider only similar types of habitats occurring across an elevational gradient. We assessed the diversity and community structure of testate amoebae in two specific habitats: (1) natural Calluna vulgaris litter and (2) Minuartia sedoides cushions 7 years after their transplantation along a vertical transect from 1770 to 2430 m in the subalpine and alpine zones of the Swiss Alps. Analyses of co-variance and variance showed that testate amoeba species richness, equitability, and diversity declined with elevation and were significantly correlated to habitat type. In a redundancy analysis, the variation in the relative abundance of the testate amoeba taxa in Calluna vulgaris litter was equally explained by elevation and litter pH. This is the first study documenting a monotonic decrease of protist diversity in similar habitats across an elevational gradient.

Keywords

Biodiversity patterns Elevational gradient Micro-eukaryotes Pot experiment Protists Soil 

Notes

Acknowledgments

This work was supported by the Swiss National Science Foundation (projects no. 205321-109709/1). T.J. Heger is currently supported by the Swiss National Science Foundation (project no. PA00P3_145374). We thank Alexandre Buttler, François Gillet, Jean-Michel Gobat, Claire Guenat, Julia Gustavsen, Michael De la Harpe, Marcie Kamerzin, Tanja Schwander, Aurélie Thébault, and Jean-David Teuscher for constructive discussion, laboratory assistance, help with statistical analyses, collection and transplantation of Minuartia sedoides, and/or comments on the manuscripts. We thank two referees for insightful comments that helped in improving several aspects of this paper.

Supplementary material

248_2015_687_MOESM1_ESM.docx (185 kb)
ESM 1 (DOCX 185 kb)
248_2015_687_MOESM2_ESM.doc (237 kb)
ESM 2 (DOC 237 kb)
248_2015_687_MOESM3_ESM.doc (94 kb)
ESM 3 (DOC 94 kb)

References

  1. 1.
    Gaston KJ (2000) Global patterns in biodiversity. Nature 405:220–227CrossRefPubMedGoogle Scholar
  2. 2.
    Rahbek C (1995) The elevational gradient of species richness—a uniform pattern. Ecography 18:200–205. doi: 10.1111/j.1600-0587.1995.tb00341.x CrossRefGoogle Scholar
  3. 3.
    Rahbek C (2005) The role of spatial scale and the perception of large-scale species-richness patterns. Ecol Lett 8:224–239. doi: 10.1111/j.1461-0248.2004.00701.x CrossRefGoogle Scholar
  4. 4.
    Nogues-Bravo D, Araujo MB, Romdal T, Rahbek C (2008) Scale effects and human impact on the elevational species richness gradients. Nature 453:216–U218. doi: 10.1038/nature06812 CrossRefPubMedGoogle Scholar
  5. 5.
    Bodelier PLE (2011) Toward understanding, managing, and protecting microbial ecosystems. Front in Microbiol 2. doi:  10.3389/fmicb.2011.00080
  6. 6.
    Wall DH, Bardgett RD, Behan-Pelletier V, Herrick JE, Jones H, Ritz K, Six J, Strong DR, van der Putten WH (2012) Soil ecology and ecosystem services. OxfordGoogle Scholar
  7. 7.
    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. doi: 10.1111/j.1550-7408.2012.00644.x CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Gremmen NJM, Van De Vijver B, Frenot Y, Lebouvier M (2007) Distribution of moss-inhabiting diatoms along an altitudinal gradient at sub-Antarctic Iles Kerguelen. Antarct Sci 19:17–24. doi: 10.1017/s0954102007000041 CrossRefGoogle Scholar
  9. 9.
    Todorov M (1998) Observation on the soil and moss testate amoebae (Protozoa: Rhizopoda) from Pirin Mountain (Bulgaria). Acta Zool Bulg 50:19–29Google Scholar
  10. 10.
    Mitchell EAD (2004) Response of testate amoebae (Protozoa) to N and P fertilization in an Arctic wet sedge tundra. Arct Antarct Alp Res 36:77–82CrossRefGoogle Scholar
  11. 11.
    Krashevska V, Bonkowski M, Maraun M, Ruess L, Kandeler E, Scheu S (2008) Microorganisms as driving factors for the community structure of testate amoebae along an altitudinal transect in tropical mountain rain forests. Soil Biol Biochem 40:2427–2433CrossRefGoogle Scholar
  12. 12.
    Krashevska V, Bonkowski M, Maraun M, Scheu S (2007) Testate amoebae (protista) of an elevational gradient in the tropical mountain rain forest of Ecuador. Pedobiologia 51:319–331CrossRefGoogle Scholar
  13. 13.
    Krashevska V, Maraun M, Scheu S (2010) Micro- and macroscale changes in density and diversity of testate amoebae of tropical montane rain forests of southern Ecuador. Acta Protozool 49:17–28Google Scholar
  14. 14.
    Tsyganov AN, Milbau A, Beyens L (2013) Environmental factors influencing soil testate amoebae in herbaceous and shrubby vegetation along an altitudinal gradient in subarctic tundra (Abisko, Sweden). Eur J Protistol 49:238–248. doi: 10.1016/j.ejop.2012.08.004 CrossRefPubMedGoogle Scholar
  15. 15.
    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. doi: 10.1016/j.soilbio.2013.08.002 CrossRefGoogle Scholar
  16. 16.
    Shen C, Liang W, Shi Y, Lin X, Zhang H, Wu X, Xie G, Chain P, Grogan P, Chu H (2014) Contrasting elevational diversity patterns between eukaryotic soil microbes and plants. Ecology 95:3190–3202CrossRefGoogle Scholar
  17. 17.
    Ledeganck P, Nijs I, Beyens L (2003) Plant functional group diversity promotes soil protist diversity. Protist 154:239–249CrossRefPubMedGoogle Scholar
  18. 18.
    Wilkinson DM (2008) Testate amoebae and nutrient cycling: peering into the black box of soil ecology. Trends Ecol Evol 23:596–598CrossRefPubMedGoogle Scholar
  19. 19.
    Jassey VEJ, Chiapusio G, Binet P, Buttler A, Laggoun-Defarge F, Delarue F, Bernard N, Mitchell EAD, Toussaint ML, Francez AJ, Gilbert D (2013) Above- and belowground linkages in Sphagnum peatland: climate warming affects plant-microbial interactions. Glob Chang Biol 19:811–823. doi: 10.1111/gcb.12075 CrossRefPubMedGoogle Scholar
  20. 20.
    Lamentowicz M, Mitchell EAD (2005) The ecology of testate amoebae (Protists) in Sphagnum in north-western Poland in relation to peatland ecology. Microb Ecol 50:48–63CrossRefPubMedGoogle Scholar
  21. 21.
    Charman DJ (1997) Modelling hydrological relationships of testate amoebae (Protozoa: Rhizopoda) on New Zealand peatlands. J R Soc N Z 27:465–483CrossRefGoogle Scholar
  22. 22.
    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. doi: 10.1139/w10-116 CrossRefPubMedGoogle Scholar
  23. 23.
    Mitchell EAD, Payne RJ, Lamentowicz M (2008) Potential implications of differential preservation of testate amoeba shells for paleoenvironmental reconstruction in peatlands. J Paleolimnol 40:603–618. doi: 10.1007/s10933-007-9185-z CrossRefGoogle Scholar
  24. 24.
    Aeschimann D, Lauber K, Moser DM (2004) Theurillat JP. Flora alpina, ParisGoogle Scholar
  25. 25.
    Carnelli AL, Theurillat JP, Thinon M, Vadi G, Talon B (2004) Past uppermost tree limit in the Central European Alps (Switzerland) based on soil and soil charcoal. Holocene 14:393–405. doi: 10.1191/0959683604hl715rp CrossRefGoogle Scholar
  26. 26.
    Gobat JM, Fierz M (1996) Modification de l’écocline subalpin/alpin. Unpublished report.Google Scholar
  27. 27.
    Theurillat J-P, Schlüssel A, Geissler P, Guisan A, Velluti C, Wiget L (2003) Vascular plant and bryophyte diversity along elevation gradients in the Alps. In: Grabherr G, Körner C, Thompson DBA (eds) Nagy, L. Alpine biodiversity in Europe Springer, Berlin, pp 185–193Google Scholar
  28. 28.
    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 49:85–91CrossRefGoogle Scholar
  29. 29.
    Quinn GPaMJK (2002) Experimental design and data analysis for biologists. Cambridge University PressGoogle Scholar
  30. 30.
    Legendre P, Gallagher ED (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129:271–280CrossRefGoogle Scholar
  31. 31.
    Blanchet FG, Legendre P, Borcard D (2008) Forward selection of explanatory variables. Ecology 89:2623–2632. doi: 10.1890/07-0986.1 CrossRefPubMedGoogle Scholar
  32. 32.
    Development Core Team R (ed) (2010) R: a language and environment for statistical computing. foundation for statistical computing, Version 2.8.0. R Development Core Team, Vienna, Austria, http://www.R-projectorg Google Scholar
  33. 33.
    Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2013) Vegan: community ecology package. R package version 2Google Scholar
  34. 34.
    Renaud V, Rebetez M (2009) Comparison between open-site and below-canopy climatic conditions in Switzerland during the exceptionally hot summer of 2003. Agric For Meteorol 149:873–880. doi: 10.1016/j.agrformet.2008.11.006 CrossRefGoogle Scholar
  35. 35.
    Morecroft MD, Taylor ME, Oliver HR (1998) Air and soil microclimates of deciduous woodland compared to an open site. Agric For Meteorol 90:141–156. doi: 10.1016/s0168-1923(97)00070-1 CrossRefGoogle Scholar
  36. 36.
    Geisen S, Bandow C, Roembke J, Bonkowski M (2014) Soil water availability strongly alters the community composition of soil protists. Pedobiologia 57:205–213. doi: 10.1016/j.pedobi.2014.10.001 CrossRefGoogle Scholar
  37. 37.
    Woodland WA, Charman DJ, Sims C (1998) Quantitative estimates of water tables and soil moisture in Holocene peatlands from testate amoebae. The Holocene 8:261–273CrossRefGoogle Scholar
  38. 38.
    Nagy L, Grabherr G (2009) The biology of alpine habitats. Oxford University Press, New YorkGoogle Scholar
  39. 39.
    McCain CM, Grytnes JA (2010) Elevational gradients in species richness. In: Encyclopedia of life sciences., pp 1–10Google Scholar
  40. 40.
    Barry RG (2008) Mountain weather and climate. Cambridge University Press, UKCrossRefGoogle Scholar
  41. 41.
    Zech W, Hintermaier-Erhard G (2002) Böden der Welt: ein Bildatlas. Spektrium Heidelberg, BerlinGoogle Scholar
  42. 42.
    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 54:91–100CrossRefPubMedGoogle Scholar
  43. 43.
    Lousier JD (1974) Effects of experimental soil moisture fluctuations on turnover rates of Testacea. Soil Biol Biochem 6:19–26CrossRefGoogle Scholar
  44. 44.
    Lomolino MV (2001) Elevation gradients of species-density: historical and prospective views. Glob Ecol Biogeogr 10:3–13. doi: 10.1046/j.1466-822x.2001.00229.x CrossRefGoogle Scholar
  45. 45.
    Jassey VEJ, Lamentowicz L, Robroek BJM, Gazbka M, Rusinska 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. doi: 10.1111/1365-2745.12288 CrossRefGoogle Scholar
  46. 46.
    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. doi: 10.1016/j.ecolind.2011.05.020 CrossRefGoogle Scholar
  47. 47.
    De Maester L (2011) A metacommunity perspective on the phylo- and biogeography of small organisms. In: Fontaneto, D (ed.) Biogeography of microscopic organisms, is everything small everywhere? Systematics Association & Cambridge University Press, pp. 324–334Google Scholar
  48. 48.
    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 48:55–62CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • T. J. Heger
    • 1
  • N. Derungs
    • 2
  • J .P. Theurillat
    • 3
    • 4
  • E. A. D. Mitchell
    • 2
    • 5
  1. 1.Beaty Biodiversity CenterUniversity of British ColumbiaVancouverCanada
  2. 2.University of NeuchâtelNeuchâtelSwitzerland
  3. 3.Centre Alpien de Phytogéographie, Fondation J.-M. AubertChampexSwitzerland
  4. 4.Laboratoire de Biogéographie, Section de BiologieUniversité de GenèveChambésySwitzerland
  5. 5.Jardin Botanique de NeuchâtelNeuchâtelSwitzerland

Personalised recommendations