Skip to main content

Advertisement

SpringerLink
Log in

Diversity of nivicolous myxomycetes of the Teberda State Biosphere Reserve (Northwestern Caucasus, Russia)

  • Published:
Fungal Diversity Aims and scope Submit manuscript

Abstract

Nivicolous myxomycete assemblages were surveyed on the northwest of the Greater Caucasian ridge in May-June 2010 and 2011 at a north facing transect between 1,700 and 2,920 m elevation of the summit Malaya Khatipara situated within the Teberda State Biosphere Reserve. Morphological characters of 396 collections representing 45 taxa (39 species, 3 varieties, and 3 forms) of myxomycetes in 8 genera and 5 families were recorded. Many (13) taxa are classified as rare (a species represents <0.5 % of all records). Only seven species were found to be widely distributed (present in 50 % or more of the 17 studied localities). To confirm the assignment of specimens to morphospecies, we obtained independently from determination 145 partial sequences of the 18S SSU rRNA gene from 35 taxa of Lamproderma, Meriderma, Physarum and Diderma, which turned out to represent 58 genotypes. Most of the taxa represented by more than one sequence had several genotypes, with an average of 1.7 genotypes per taxon. Except for three taxonomically difficult groups of species, partial SSU sequences did well correspond with the respective morphospecies and where similar or identical to sequences of specimens from the European Alps, making this marker a good candidate for barcoding in myxomycetes. Species richness and diversity increased from subalpine crooked-stem birch forests (23 species, 2 varieties, H′ = 2.8, E = 0.88, D = 0.08) to alpine dwarf shrub communities (34 species and 2 varieties, 2 forms, H′ = 3.2, E = 0.89, D = 0.05) but decreased again for alpine meadows (27 species and 2 varieties, 2 forms, H′ = 3.1, E = 0.91, D = 0.06). Species richness and alpha-diversity reached maximum values for ground litter, whereas leaves and stems of living shrubs above ground harboured a more depauperate myxomycete assemblage.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figs. 1–3
Figs. 4–11
Figs. 12–29
Figs. 30–52
Figs. 53–74
Figs. 75–99
Figs. 100–117
Fig. 118
Fig. 119
Figs. 120–121
Fig. 122

Similar content being viewed by others

References

  • Anonymous (2012) NBS/ISCC color system. Original and improved 267 color centroids. Washington: Inter-Society Color Council. National Bureau of Standards. http://tx4.us/nbs-iscc.htm. Accessed 28 July 2012

  • Chao A, Chazdon RL, Colwell RK, Shen TJ (2005) A new statistical approach for assessing similarity of species compostion with incidence and abundance data. Ecol Lett 8:148–159

    Article  Google Scholar 

  • Chao A, Chazdon RL, Colwell RK, Shen TJ (2006) Abundance-based similarity indices and their estimation when there are unseen species in samples. Biometrics 62:361–371

    Article  PubMed  Google Scholar 

  • Colwell RK (2009) EstimateS: statistical estimation of species richness and shared species from samples. Version 8.2. User’s guide and application. http://purl.oclc.org/estimates. Accessed 12 April 2012

  • Colwell RK, Chao A, Gotelli NJ, Lin S-Y, Mao CX, Chazdon RL, Longino JT (2012) Models and estimators linking individual-based and sample-based rarefaction, extrapolation and comparison of assemblages. J Plant Ecol 5(1):3–21

    Article  Google Scholar 

  • Elumeeva TG, Salpagarov AD, Onipchenko VG (2007) Dynamics of temperature and precipitation in Karachaevo-Cherkesia during the second part of XX century. Trans Teberda Reserv 27:20–29

    Google Scholar 

  • Fiore-Donno AM, Meyer M, Baldauf SL, Pawlowski J (2008) Evolution of dark-spored myxomycetes (slime-molds): molecules versus morphology. Mol Phylogenet Evol 46(3):878–889

    Article  PubMed  CAS  Google Scholar 

  • Fiore-Donno AM, Novozhilov YK, Meyer M, Schnittler M (2011) Genetic structure of two protist species (Myxogastria, Amoebozoa) suggests asexual reproduction in sexual amoebae. PLoS One 6(8):e22872. doi:22810.21371/journal.pone.0022872

    Article  PubMed  CAS  Google Scholar 

  • Fiore-Donno AM, Kamono A, Meyer M, Schnittler M, Fukui M, Cavalier-Smith T (2012) 18S rDNA Phylogeny of Lamproderma and allied genera (Stemonitales, Myxomycetes, Amoebozoa). PLoS One 7(4):e35359. doi:10.1371/journal.pone.0035359

    Article  PubMed  CAS  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp 41:95–98

    CAS  Google Scholar 

  • Kamono A, Matsumoto J, Kojima H, Fukui M (2009a) Characterization of myxomycete communities in soil by reverse transcription polymerase chain reaction (RT-PCR)-based method. Soil Biol Biochem 41:1324–1330

    Article  CAS  Google Scholar 

  • Kamono A, Kojima H, Matsumoto J, Kawamura K, Fukui M (2009b) Airborne myxomycete spores: detection using molecular techniques. Naturwissenschaften 96(1):147–151

    Article  PubMed  CAS  Google Scholar 

  • Karlsen A (1943) Studies on myxomycetes II. The myxomycete flora of Hardangen. Bergens Museums Naturvitenskapelig Rekke 4:1–34

    Google Scholar 

  • Kirk P (2012) Authors of fungal names. http://wwwindexfungorumorg/authorsoffungalnameshtm. Accessed 15 April 2012

  • Kowalski DT (1971) The genus Lepidoderma. Mycologia 63:490–516

    Article  Google Scholar 

  • Kuhnt A (2011) Lamproderma lycopodiicola und L. nordica (Myxomycetes, Stemonitales), zwei neue nivicole Arten. Z Mykologie 77:71–88

    Google Scholar 

  • Lado C (2004) Nivicolous myxomycetes of the Iberian Peninsula: considerations on species richness and ecological requirements. Syst Geogr Plant 74:143–157

    Google Scholar 

  • Lado C (2005–2012) An on-line nomenclatural information system of Eumycetozoa. http://www.nomen.eumycetozoa.com accessed. Accessed 10 February 2012

  • Lado C, Ronikier A (2008) Nivicolous myxomycetes from the Pyrenees: notes on taxonomy and species diversity. Part 1. Physarales and Trichiales. Nova Hedwigia 87(3–4):337–360

    Article  Google Scholar 

  • Lado C, Ronikier A (2009) Nivicolous myxomycetes from the Pyrenees: notes on the taxonomy and species diversity. Part 2. Stemonitales. Nova Hedwigia 89(1–2):131–145

    Article  Google Scholar 

  • Lado C, Ronikier A, Ronikier M, Drozdowicz A (2005) Nivicolous myxomycetes from the Sierra de Gredos (central Spain). Nova Hedwigia 81(3–4):371–394

    Article  Google Scholar 

  • Magurran AE (2004) Measuring biological diversity. Blackwell Publishing, Malden

    Google Scholar 

  • Makarov MI, Onipchenko VG, Malysheva TI, Salpagarov AD (2007) Temporal dynamics of soil temperature and climatic parameters of alpine ecosystems in the scientific station “Malaya Khatipara”. Trans Teberda Reserve 27:30–41

    Google Scholar 

  • Meylan C (1914) Remarques sur quelques espèces nivales de myxomycètes. Bull Soc Vaud Sci Nat 50(182):237–244

    Google Scholar 

  • Mitchel DH, Chapman SW, Farr ML (1986) Notes on Colorado fungi V: Physarum alpestre, a new species. Mycologia 78:66–69

    Article  Google Scholar 

  • Moreno G, Sanchez A, Castillo A, Singer H, Illana C (2003) Nivicolous myxomycetes from the Sierra Nevada National Park (Spain). Mycotaxon 87:223–242

    Google Scholar 

  • Moreno G, Singer H, Illana C (2004) A taxonomic review on the nivicolous myxomycete species described by Kowalski. II. Physarales and trichiales. Oesterr Z Pilzk 13:61–73

    Google Scholar 

  • Moreno G, Singer H, Sanchez A, Illana C (2005) A critical study of some Stemonitales of North American herbaria and comparison with European nivicolous collections. Bol Soc Micol Madrid 28:21–41

    Google Scholar 

  • Müller H (2002) Beitrag zur Kenntnis und Verbreitung nivicoler Myxomyceten im Thüringer Wald. Z Mykologie 68(2):199–208

    Google Scholar 

  • Novozhilov YK (1986) Nivicolous myxomycetes of the Leningrad region. Novosti Sistematiki Nizshikh Rastenii 23:146–149 (in Russian)

    Google Scholar 

  • Novozhilov YK, Schnittler M (1997) Nivicole myxomycetes of the Khibine mountains (Kola peninsula). Nord J Bot 16:549–561

    Article  Google Scholar 

  • Onipchenko VG (ed) (2004) Alpine ecosystems in the Northwest Caucasus. Kluwer Academic Publishers, Dordrecht, Boston; London

    Google Scholar 

  • Onipchenko VG (2007) Syntaxonomy of alpine vegetation in the Teberda reserve: syntaxa prodromus and diagnostic species. Trans Teberda Reserv 27:75–82

    Google Scholar 

  • Poulain M, Meyer M, Bozonnet J (2011) Les Myxomycètes, vol 1–2. Fédération mycologique et botanique Dauphiné-Savoie

  • Ronikier A, Ronikier M (2009) How ‘alpine’ are nivicolous myxomycetes? A worldwide assessment of altitudinal distribution. Mycologia 101(1):1–16

    Article  PubMed  CAS  Google Scholar 

  • Ronikier A, Ronikier M, Drozdowicz A (2008) Diversity of nivicolous myxomycetes in the Gorce mountains — a low-elevation massif of the western Carpathians. Mycotaxon 103:337–352

    Google Scholar 

  • Ronikier A, Lado C, Meyer M, de Basanta DW (2010) Two new species of nivicolous Lamproderma (myxomycetes) from the mountains of Europe and America. Mycologia 102(3):718–728

    Article  PubMed  Google Scholar 

  • Schnittler M (2001) Ecology of Myxomycetes of a winter-cold desert in western Kazakhstan. Mycologia 93(4):653–669

    Article  Google Scholar 

  • Schnittler M, Novozhilov YK (1999) Lepidoderma crustaceum, a nivicolous myxomycete, found on the island of Crete. Mycotaxon 71:387–392

    Google Scholar 

  • Singer H, Moreno G, Illana C (2005) Mountainous and nivicolous myxomycetes described by Charles Meylan. A SEM-study. Oesterr Z Pilzk 14:11–29

    Google Scholar 

  • Stephenson S (2001) Collecting myxomycetes and fungi in Snowbank habitats of New Zealand. Inoculum Suppl Mycol 52(3):1–2

    Google Scholar 

  • Stephenson SL (2011) From morphological to molecular: studies of myxomycetes since the publication of the Martin and Alexopoulos (1969) monograph. Fungal Divers 50(1):21–34

    Article  Google Scholar 

  • Stephenson SL, Shadwick JDL (2009) Nivicolous myxomycetes from alpine areas of south-eastern Australia. Aust J Bot 57(2):116–122

    Article  Google Scholar 

  • Stephenson SL, Kalyanasundaram I, Lakhanpal TN (1993) A comparative biogeographical study of myxomycetes in the mid-Appalachians of eastern North America and two regions of India. J Biogeogr 20:645–657

    Article  Google Scholar 

  • Stephenson SL, Fiore-Donno AM, Schnittler M (2011) Myxomycetes in soil. Soil Biol Biochem 43:2237–2242

    Article  CAS  Google Scholar 

  • Tamayama M (2000) Nivicolous taxa of the myxomycetes in Japan. Stapfia 73:121–129

    Google Scholar 

  • Unterseher M, Schnittler M, Dormann C, Sickert A (2008) Application of species richness estimators for the assessment of fungal diversity. FEMS Microbiol Lett 282:205–213

    Article  PubMed  CAS  Google Scholar 

  • Wuyts J, Van de Peer Y, Winkelmans T, De Wachter R (2002) The European database on small subunit ribosomal RNA. Nucleic Acids Res 30:183–185

    Article  PubMed  CAS  Google Scholar 

  • Yajima Y, Nishikawa T, Yamamoto A (2006) Studies on the myxomycetes of Hokkaido, Japan (II). Nivicolous species of Mt. Asahidake in Mts. Taisetsu. Rep Taisetsuzan Inst Sci 40:53–57

    Google Scholar 

Download references

Acknowledgments

We gratefully acknowledge logistical help provided by A.N. Bok (Teberda State Biosphere Reserve) and V.N. Khramtzov (Komarov Botanical Institute RAS) as well as technical support of SEM by L.A. Kartzeva (Komarov Botanical Institute). For help with sequencing we are indebted to A. Klahr, for help with alignments to A.M. Fiore-Donno (both Greifswald). Travel and laboratory work were supported by the grant RFBR 10–04–00536a to the first author as well as a scientific program “Bioraznoobrazie” from the Russian Academy of Sciences. Travel for the second author was supported by grants from Greifswald University, sequencing in part by a grant from the Deutsche Forschungsgemeinschaft (SCHN1080/2-1). We are grateful to David Mitchell for comments and linguistic correction and Marianne Meyer for help with identification of specimens.

Author information

Authors and Affiliations

  1. Komarov Botanical Institute of the Russian Academy of Sciences, Prof. Popov St. 2, 197376 St., Petersburg, Russia

    Y. K. Novozhilov, D. A. Erastova, M. V. Okun & O. N. Schepin

  2. Institute of Botany and Landscape Ecology, Ernst Moritz Arndt University Greifswald, Grimmer Str. 88, 17487, Greifswald, Germany

    M. Schnittler & E. Heinrich

  3. CIBIV – Center for Integrative Bioinformatics in Vienna, Max F. Perutz Laboratories (MFPL), University of Vienna, Medical University of Vienna, Campus Vienna Biocenter 5 (VBC5), 1030, Vienna, Austria

    M. V. Okun

Authors
  1. Y. K. Novozhilov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. Schnittler
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. D. A. Erastova
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. V. Okun
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. O. N. Schepin
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. E. Heinrich
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Y. K. Novozhilov.

Electronic supplementary materials

Below is the link to the electronic supplementary material.

Supplement S1

List of specimens found in this survey, presented as a data base in Microsoft Excel. 2003. (XLS 214 kb)

Supplement S2

Alignment of the partial SSU sequences for Stemonitales (including the genus Diachea which can be seen as a member of the Physarales as well) in fasta format; including matching sequences drawn from GenBank as well as unpublished comparison material. To avoid long-branch attraction in the resulting trees, Stemonitopsis spp. and Lamproderma arcyrionema, showing extremely divergent partial SSU sequences, have been omitted. (FAS 217 kb)

Supplement S3

Maximum likelihood phylogenetic tree of the partial SSU sequences for Stemonitales, reconstructed with IQTree software (http://www.cibiv.at/software/iqpnni/) under the GTR + I + G model, in Newick format, readable with free software like FigTree v.1.3.1. (http://tree.bio.ed.ac.uk/software/figtree/). Although the topology of the tree basically corresponds to a tree constructed using complete SSU sequences published by Fiore-Donno et al. (2012), it should be noted that the short partial SSU sequences are not suitable to derive correct phylogenetic relationships between species. (PDF 9 kb)

Supplement S4

Alignment of the partial SSU sequences for Physarales (including the genus Diachea) in fasta format; including matching sequences drawn from GenBank as well as unpublished comparison material. (FAS 114 kb)

Supplement S5

Maximum likelihood phylogenetic tree of the partial SSU sequences for Physarales, reconstructed with IQTree software under the GTR + I + G model, in Newick format. (PDF 8360 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Novozhilov, Y.K., Schnittler, M., Erastova, D.A. et al. Diversity of nivicolous myxomycetes of the Teberda State Biosphere Reserve (Northwestern Caucasus, Russia). Fungal Diversity 59, 109–130 (2013). https://doi.org/10.1007/s13225-012-0199-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13225-012-0199-0

Keywords

Search

Navigation