Molecular methods reveal controls on nematode community structure and unexpectedly high nematode diversity, in Svalbard high Arctic tundra

Abstract

Nematodes are among the most abundant metazoans in soils, but their true diversity and distribution patterns remain poorly investigated, especially in polar environments. Here, we studied three high Arctic tundra sites at Kongsford, NW Svalbard (78°55′N) to understand: (1) Whether there is detectable small-scale habitat variation, (2) What the predictors of diversity and community variation are, and (3) Whether molecular methodology reveals greater diversity than morphological studies. DNA was extracted using the Baermann funnel method, and PCR amplified for the 18S rRNA gene, followed by 454-pyrosequencing. Our samples revealed no difference in nematode OTU α-diversity between different tundra habitats. Similarly, we found no correlation between nematode α-diversity in individual samples and soil properties or vegetation coverage. However, β-diversity was lower in the highly vegetated tundra than in the other tundra. There was no evidence of distinct nematode communities between individual 1 m2 quadrats of different vegetation cover and soil parameters. Overall, the community composition of highly vegetated tundra clustered separately from less vegetated tundra. The phylogenetic community assembly analysis indicated that the variation of nematode community was deterministic. This suggests that—despite the ‘extreme’ environment—nematodes in the high Arctic tundra are still to some extent habitat specialized. This study also revealed a much greater overall nematode diversity than has been previously detected in Svalbard. The nematode OTU diversity in our samples was considerably higher than the total species previously reported. This suggests the potential of DNA-based methods to rapidly reveal the true diversity of metazoans.

This is a preview of subscription content, access via your institution.

Fig. 1

(Modified after http://toposvalbard.npolar.no/)

Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. Aguiar MR, Sala OE (1999) Patch structure, dynamics and implications for the functioning of arid ecosystems. Trends Ecol Evol 14:273–277

    CAS  Article  PubMed  Google Scholar 

  2. Alsos IG, Ehrich D, Thuiller W, Eidesen PB, Tribsch A, Schönswetter P, Brochmann C (2012) Genetic consequences of climate change for Northern plants. Proc R Soc Lond B Biol Sci 279(1735):2042–2051. doi:10.1098/rspb.2011.2363

  3. Anderson MJ et al (2011) Navigating the multiple meanings of β-diversity: a roadmap for the practicing ecologist. Ecol Lett 14:19–28

    Article  PubMed  Google Scholar 

  4. Andrassy I (1998) The genus Boreolaimus gen. n. and its six species (Dorylaimida: Qudsianematidae), nematodes from the European Arctic. Fundam Appl Nematol 21:553–568

    Google Scholar 

  5. Andrássy I (1986) The genus Eudorylaimus Andrássy, 1959 and the present status of its species (Nematoda: Qudsianematidae). Opusc Zool Bp 22:1–42

    Google Scholar 

  6. Barrett J, Virginia RA, Wall DH, Adams BJ (2008) Decline in a dominant invertebrate species contributes to altered carbon cycling in a low-diversity soil ecosystem. Glob Change Biol 14:1734–1744

    Article  Google Scholar 

  7. Boag B, Yeates GW (1998) Soil nematode biodiversity in terrestrial ecosystems. Biodivers Conserv 7:617–630

    Article  Google Scholar 

  8. Bölter M, Blume H-P, Schneider D, Beyer L (1997) Soil properties and distributions of invertebrates and bacteria from King George Island (Arctowski Station), maritime Antarctic. Polar Biol 18:295–304

    Article  Google Scholar 

  9. Bongers T, Ferris H (1999) Nematode community structure as a bioindicator in environmental monitoring. Trends Ecol Evol 14:224–228

    CAS  Article  PubMed  Google Scholar 

  10. Burke IC, Lauenroth WK, Riggle R, Brannen P, Madigan B, Beard S (1999) Spatial variability of soil properties in the shortgrass steppe: the relative importance of topography, grazing, microsite, and plant species in controlling spatial patterns. Ecosystems 2:422–438

    CAS  Article  Google Scholar 

  11. Clark K, Gorley R (2006) PRIMER v6: user manual. Plymouth Marine Laboratory, Plymouth

    Google Scholar 

  12. Cockell CS, Lee P, Schuerger AC, Hidalgo L, Jones JA, Stokes MD (2001) Microbiology and vegetation of micro-oases and polar desert, Haughton impact crater, Devon Island, Nunavut, Canada. Arct Antarct Alp Res 33:306–318

    Article  Google Scholar 

  13. Coulson S (2012) Checklist of the terrestrial and freshwater invertebrate fauna of Svalbard Accessed on the internet at http://www.unis.no/35_STAFF/staff_webpages/biology/steve_coulson/default.htm on various dates in June

  14. Coulson S, Leinaas H, Ims R, Søvik G (2000) Experimental manipulation of the winter surface ice layer: the effects on a high Arctic soil microarthropod community. Ecography 23:299–306

    Article  Google Scholar 

  15. Coulson SJ, Convey P, Aakra K, Aarvik L, Ávila-Jiménez ML, Babenko A, Biersma EM, Boström S, Brittain JE, Carlsson AM, Christoffersen K (2014) The terrestrial and freshwater invertebrate biodiversity of the archipelagoes of the Barents Sea; Svalbard, Franz Josef Land and Novaya Zemlya. Soil Biol Biochem 68:440–470

    CAS  Article  Google Scholar 

  16. De Deyn GB et al (2003) Soil invertebrate fauna enhances grassland succession and diversity. Nature 422:711–713

    Article  PubMed  Google Scholar 

  17. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200. doi:10.1093/bioinformatics/btr381

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  18. Fonseca VG et al (2010) Second-generation environmental sequencing unmasks marine metazoan biodiversity. Nat Commun 1:98

    Article  PubMed  PubMed Central  Google Scholar 

  19. Haldorsen S, Heim M (1999) An Arctic groundwater system and its dependence upon climatic change: an example from Svalbard. Permafr Periglac Process 10:137–149

    Article  Google Scholar 

  20. Holovachov O (2014) Nematodes from terrestrial and freshwater habitats in the Arctic. Biodivers Data J 2:e1165

    Article  Google Scholar 

  21. Hooper DU, Bignell DE, Brown VK, Brussard L, Dangerfield JM, Wall DH, Wardle DA, Coleman DC, Giller KE, Lavelle P, Van Der Putten WH (2000) Interactions between aboveground and belowground biodiversity in terrestrial ecosystems: patterns, mechanisms, and feedbacks: we assess the evidence for correlation between aboveground and belowground diversity and conclude that a variety of mechanisms could lead to positive, negative, or no relationship-depending on the strength and type of interactions among species. Bioscience 50:1049–1061

    Article  Google Scholar 

  22. Hoschitz M, Kaufmann R (2004) Soil nematode communities of Alpine summits–site differentiation and microclimatic influences. Pedobiologia 48:313–320

    Article  Google Scholar 

  23. Huse SM, Welch DM, Morrison HG, Sogin ML (2010) Ironing out the wrinkles in the rare biosphere through improved OTU clustering. Environ Microbiol 12:1889–1898

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  24. Jónsdóttir IS (2005) Terrestrial ecosystems on Svalbard: heterogeneity, complexity and fragility from an Arctic island perspective. In: Biology and Environment Proceedings of the Royal Irish Academy, JSTOR, pp 155–165

  25. Kito K, Shishida Y, Ohyama Y (1996) A new species of the genus Eudorylaimus Andrássy, 1959 (Nematoda: Qudsianematidae) from East Antarctica. Polar Biol 16:163–169

    Article  Google Scholar 

  26. Klekowski RZ, Opalinski KW (1986) Matter and energy flow in Spitsbergen ornithogenic tundra. Polar Res 4:187–197

    Article  Google Scholar 

  27. Knops JM, Wedin D, Tilman D (2001) Biodiversity and decomposition in experimental grassland ecosystems. Oecologia 126:429–433

    Article  Google Scholar 

  28. Koleff P, Gaston KJ, Lennon JJ (2003) Measuring beta diversity for presence-absence data. J Anim Ecol 72:367–382. doi:10.1046/j.1365-2656.2003.00710.x

    Article  Google Scholar 

  29. Lavelle P et al (2006) Soil invertebrates and ecosystem services. Eur J Soil Biol 42:S3–S15

    Article  Google Scholar 

  30. Lawton J, Bignell D, Bloemers G, Eggleton P, Hodda M (1996) Carbon flux and diversity of nematodes and termites in Cameroon forest soils. Biodivers Conserv 5:261–273

    Article  Google Scholar 

  31. Poage MA, Barrett JE, Virginia RA, Wall DH (2008) The influence of soil geochemistry on nematode distribution, McMurdo Dry Valleys, Antarctica. Arct Antarct Alp Res 40:119–128

    Article  Google Scholar 

  32. Porazinska DL, Bardgett RD, Blaauw MB, Hunt HW, Parsons AN, Seastedt TR, Wall DH (2003) Relationships at the aboveground-belowground interface: plants, soil biota, and soil processes. Ecol Monographs 73:377–395

    Article  Google Scholar 

  33. Porazinska DL et al (2009) Evaluating high-throughput sequencing as a method for metagenomic analysis of nematode diversity. Mol Ecol Resour 9:1439–1450. doi:10.1111/j.1755-0998.2009.02611.x

    CAS  Article  PubMed  Google Scholar 

  34. Porazinska DL, Sung W, Giblin-Davis RM, Thomas WK (2010) Reproducibility of read numbers in high-throughput sequencing analysis of nematode community composition and structure. Mol Ecol Resour 10:666–676

    CAS  Article  PubMed  Google Scholar 

  35. Porazinska DL, Giblin-Davis RM, Powers TO, Thomas WK (2012) Nematode spatial and ecological patterns from tropical and temperate rainforests. Plos One 7:e44641

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  36. Schloss PD et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541. doi:10.1128/AEM.01541-09

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  37. Sørensen LI, Holmstrup M, Maraldo K, Christensen S, Christensen B (2006) Soil fauna communities and microbial respiration in high Arctic tundra soils at Zackenberg, Northeast Greenland. Polar Biol 29:189–195

    Article  Google Scholar 

  38. Stafford Smith D, Pickup G (1990) Pattern and production in arid lands. In: Proceedings of the Ecological Sociey of Australia, pp 195–200

  39. Thorne G (1961) Principles of nematology. McGraw-Hill publications in the agricultural sciences. McGraw-Hill, New York

    Google Scholar 

  40. Vinciguerra M, Orselli L (1998) Nematodes from Italian sand dunes. 3. Four new species of Qudsianematidae (Dorylaimida, Nematoda). Nematol Mediterr 26:255–266

    Google Scholar 

  41. Wall DH, Virginia RA (1999) Controls on soil biodiversity: insights from extreme environments. Appl Soil Ecol 13:137–150

    Article  Google Scholar 

  42. Wardle D, Nicholson K (1996) Synergistic effects of grassland plant spcies on soil microbial biomass and activity: implications for ecosystem-level effects of enriched plant diversity. Funct Ecol 10:410–416

    Article  Google Scholar 

  43. Wardle D, Bonner K, Nicholson K (1997) Biodiversity and plant litter: experimental evidence which does not support the view that enhanced species richness improves ecosystem function. Oikos 79:247–258

    Article  Google Scholar 

  44. Webb CO, Ackerly DD, Kembel SW (2008) Phylocom: software for the analysis of phylogenetic community structure and trait evolution. Bioinformatics 18:2098–2100

    Article  Google Scholar 

  45. Welker J, Wookey P, Parsons A, Press M, Callaghan T, Lee J (1993) Leaf carbon isotope discrimination and vegetative responses of Dryas octopetala to temperature and water manipulations in a high Arctic polar semi-desert, Svalbard. Oecologia 95:463–469

    Article  Google Scholar 

  46. Wookey P, Parsons A, Welker J, Potter J, Callaghan T, Lee J, Press M (1993) Comparative responses of phenology and reproductive development to simulated environmental change in sub-arctic and high Arctic plants. Oikos 67:490–502

    Article  Google Scholar 

  47. Wu T, Ayres E, Bardgett RD, Wall DH, Garey JR (2011) Molecular study of worldwide distribution and diversity of soil animals. Proc Natl Acad Sci 108:17720–17725

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  48. Yeates G (1977) Soil nematodes in New Zealand pastures. Soil Sci 123:415–422

    Article  Google Scholar 

  49. Yeates G (1999) Effects of plants on nematode community structure. Annu Rev Phytopathol 37:127–149

    CAS  Article  PubMed  Google Scholar 

  50. Yeates GW, Bongers T, De Goede RG, Freckman DW, Georgieva SS (1993) Feeding habits in soil nematode families and genera-an outline for soil ecologists. J Nematol 25:315–331

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Yergeau E, Bokhorst S, Huiskes AH, Boschker HT, Aerts R, Kowalchuk GA (2007) Size and structure of bacterial, fungal and nematode communities along an Antarctic environmental gradient. FEMS Microbiol Ecol 59:436–451

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by a Grant of the Polar Academic Program (PAP) funded by Korea Polar Research Institute (KOPRI) under the number 0409-20140091.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Jonathan M. Adams.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 449 kb)

Supplementary material 2 (XLSX 56 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Kerfahi, D., Park, J., Tripathi, B.M. et al. Molecular methods reveal controls on nematode community structure and unexpectedly high nematode diversity, in Svalbard high Arctic tundra. Polar Biol 40, 765–776 (2017). https://doi.org/10.1007/s00300-016-1999-6

Download citation

Keywords

  • High Arctic
  • Metagenetics
  • Nematode
  • Svalbard
  • Tundra
  • 18S rRNA gene