Advertisement

Polar Biology

, Volume 41, Issue 5, pp 1013–1018 | Cite as

Stable C and N isotope ratios reveal soil food web structure and identify the nematode Eudorylaimus antarcticus as an omnivore–predator in Taylor Valley, Antarctica

  • E. Ashley Shaw
  • Byron J. Adams
  • John E. Barrett
  • W. Berry Lyons
  • Ross A. Virginia
  • Diana H. Wall
Short Note

Abstract

Soil food webs of the McMurdo Dry Valleys, Antarctica are simple. These include primary trophic levels of mosses, algae, cyanobacteria, bacteria, archaea, and fungi, and their protozoan and metazoan consumers (including relatively few species of nematodes, tardigrades, rotifers, and microarthropods). These biota are patchily distributed across the landscape, with greatest faunal biodiversity associated with wet soil. Understanding trophic structure is critical to studies of biotic interactions and distribution; yet, McMurdo Dry Valley soil food web structure has been inferred from limited laboratory culturing and microscopic observations. To address this, we measured stable isotope natural abundance ratios of C (13C/12C) and N (15N/14N) for different metazoan taxa (using whole body biomass) to determine soil food web structure in Taylor Valley, Antarctica. Nitrogen isotopes were most useful in differentiating trophic levels because they fractionated predictably at higher trophic levels. Using 15N/14N, we found that three trophic levels were present in wet soil habitats. While cyanobacterial mats were the primary trophic level, the nematode Plectus murrayi, tardigrade Acutuncus antarcticus, and rotifers composed a secondary trophic level of grazers. Eudorylaimus antarcticus had a 15N/14N ratio that was 2–4‰ higher than that of grazers, indicating that this species is the sole member of a tertiary trophic level. Understanding the trophic positions of soil fauna is critical to predictions of current and future species interactions and their distributions for the McMurdo Dry Valleys, Antarctica.

Keywords

Dry Valleys Predator Trophic levels Isotopic fractionation Feeding ecology Connectivity 

Notes

Acknowledgements

This work was funded by the United States National Science Foundation (NSF), McMurdo Dry Valleys Long Term Ecological Research (MCM LTER) site, PLR 1115245. Geospatial support for this work was provided by the Polar Geospatial Center under NSF OPP awards 1043681 & 1559691. We are grateful to many people who helped with this work, especially the McMurdo Dry Valleys LTER group. Matthew Knox helped collect samples in the field. Members of the Wall Lab at Colorado State University, in particular Amber Cavin, Cecilia Milano de Tomasel, and Emily Bernier, helped with lab work. Thanks also to the Crary Laboratory staff, Stable Isotope Mass Spectrometry Laboratory at Kansas State University, and PHI helicopters whose assistance with lab and fieldwork helped make this work possible.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Adams BJ et al (2006) Diversity and distribution of Victoria Land biota. Soil Biol Biochem 38:3003–3018.  https://doi.org/10.1016/j.soilbio.2006.04.030 CrossRefGoogle Scholar
  2. Adams B, Wall D, Virginia R, Broos E, Knox M (2014) Ecological biogeography of the terrestrial nematodes of Victoria Land, Antarctica. ZooKeys 419:29–71.  https://doi.org/10.3897/zookeys.419.7180 CrossRefGoogle Scholar
  3. Adhikari BN, Tomasel CM, Li G, Wall DH, Adams BJ (2010) Culturing the Antarctic nematode Plectus murrayi. Cold Spring Harb Protoc.  https://doi.org/10.1101/pdb.prot5522 Google Scholar
  4. Ayres E, Wall DH, Adams BJ, Barrett JE, Virginia RA (2007) Unique similarity of faunal communities across aquatic–terrestrial interfaces in a polar desert ecosystem: soil–sediment boundaries and faunal community. Ecosystems 10:523–535.  https://doi.org/10.1007/sl0021-007-9035-x CrossRefGoogle Scholar
  5. Bamforth SS, Wall DH, Virginia R (2005) Distribution and diversity of soil protozoa in the McMurdo Dry Valleys of Antarctica. Polar Biol 28:756–762.  https://doi.org/10.1007/s00300-005-0006-4 CrossRefGoogle Scholar
  6. Barrett JE, 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.  https://doi.org/10.1111/j.1365-2486.2008.01611.x CrossRefGoogle Scholar
  7. Burkins MB, Virginia RA, Chamberlain CP, Wall DH (2000) Origin and distribution of soil organic matter in Taylor Valley, Antarctica. Ecology 81:2377–2391.  https://doi.org/10.1890/0012-9658(2000)081 CrossRefGoogle Scholar
  8. Burkins MB, Virginia RA, Wall DH (2001) Organic carbon cycling in Taylor Valley, Antarctica: quantifying soil reservoirs and soil respiration. Glob Change Biol 7:113–125.  https://doi.org/10.1046/j.1365-2486.2001.00393.x CrossRefGoogle Scholar
  9. Campbell IB, Claridge GC, Campbell DI, Balks MR (1998) The soil environment of the McMurdo Dry Valleys, Antarctica. In: Priscu JC (ed) Ecosystem dynamics in a polar desert: the McMurdo Dry Valleys, Antarctica. American Geophysical Union, Washington DC, pp 297–322Google Scholar
  10. Darby B, Neher D (2012) Stable isotope composition of microfauna supports the occurrence of biologically fixed nitrogen from cyanobacteria in desert soil food webs. J Arid Environ 85:76–78.  https://doi.org/10.1016/j.jaridenv.2012.06.006 CrossRefGoogle Scholar
  11. de Tomasel CM, Adams BJ, Tomasel FG, Wall DH (2013) The life cycle of the Antarctic nematode Plectus murrayi under laboratory conditions. J Nematol 45:39–42PubMedPubMedCentralGoogle Scholar
  12. Ferris V, Ferris J (1989) Why ecologists need systematists: importance of systematics to ecological research. J Nematol 21:308–314PubMedPubMedCentralGoogle Scholar
  13. Fountain AG, Lyons WB, Burkins MB, Dana GL, Doran PT, Lewis KJ, McKnight DM, Moorhead DL, Parsons AN, Priscu JC, Wall DH, Wharton RA, Virginia RA (1999) Physical controls on the Taylor Valley ecosystem, Antarctica. Bioscience 49:961–971.  https://doi.org/10.2307/1313730 CrossRefGoogle Scholar
  14. Fountain A, Levy J, Gooseff MN, Van Horn D (2014) The McMurdo Dry Valleys: a landscape on the threshold of change. Geomorphology 225:25–35.  https://doi.org/10.1016/j.geomorph.2014.03.044 CrossRefGoogle Scholar
  15. Freckman D (1988) Bacterivorous nematodes and organic matter decomposition. Agric Ecosyst Environ 24:195–217.  https://doi.org/10.1016/0167-8809(88)90066-7 CrossRefGoogle Scholar
  16. Freckman D, Virginia R (1993) Extraction of nematodes from Dry Valley Antarctic soils. Polar Biol 13:483–487.  https://doi.org/10.1007/BF00233139 CrossRefGoogle Scholar
  17. Freckman DW, Virginia RA (1997) Low-diversity Antarctic soil nematode communities: distribution and response to disturbance. Ecology 78:363–369.  https://doi.org/10.2307/2266013 CrossRefGoogle Scholar
  18. Gooseff MN, Wlostowski A, McKnight DM, Jaros C (2017a) Hydrologic connectivity and implications for ecosystem processes—lessons from naked watersheds. Geomorphology 277:63–71.  https://doi.org/10.1016/j.geomorph.2016.04.024 CrossRefGoogle Scholar
  19. Gooseff MN, Barrett JE, Adams BJ, Doran PT, Fountain AG, Lyons WB, McKnight DM, Priscu JC, Sokol SR, Takacs-Vesbach C, Vandegehuchte ML, Virginia RA, Wall DH (2017b) Decadal ecosystem response to an anomalous melt season in a polar desert in Antarctica. Nat Ecol Evol 1:1334–1338.  https://doi.org/10.1038/s41559-017-0253-0 CrossRefPubMedGoogle Scholar
  20. Hollis JP (1957) Cultural studies with Dorylaimus ettersbergensis. Phytopathology 47:468–473Google Scholar
  21. Hooper DJ (1970) Extraction of free-living stages from soil. In: Southey JF (ed) Laboratory methods for work with plant and soil nematodes, 6th edn. Ministery of Agriculture, Fisheries and Food, London, pp 5–30Google Scholar
  22. Kudrin AA, Tsurikov SM, Tiunov AV (2015) Trophic position of microbivorous and predatory soil nematodes in a boreal forest as indicated by stable isotope analysis. Soil Biol Biochem 86:193–200.  https://doi.org/10.1016/j.soilbio.2015.03.017 CrossRefGoogle Scholar
  23. Lawson J, Doran PT, Kenig F, Des Marais DJ, Priscu JC (2004) Stable carbon and nitrogen isotopic composition of benthic and pelagic organic matter in lakes of the McMurdo Dry Valleys, Antarctica. Aquat Geochem 10:269–301.  https://doi.org/10.1007/s10498-004-2262-2 CrossRefGoogle Scholar
  24. McCutchan JH, Lewis WM, Kendall C, McGrath CC (2003) Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102:378–390.  https://doi.org/10.1034/j.1600-0706.2003.12098.x CrossRefGoogle Scholar
  25. McSorley R (2012) Ecology of the dorylaimid omnivore genera Aporcelaimellus, Eudorylaimus and Mesodorylaimus. Nematology 14:645–663.  https://doi.org/10.1163/156854112x651168 CrossRefGoogle Scholar
  26. Newsham KK, Rolf J, Pearce DA, Strachan RJ (2004) Differing preferences of Antarctic soil nematodes for microbial prey. Eur J Soil Biol 40:1–8.  https://doi.org/10.1016/j.ejsobi.2004.01.004 CrossRefGoogle Scholar
  27. Nielsen UN, Wall DH, Adams BJ, Virginia RA (2011) Antarctic nematode communities: observed and predicted responses to climate change. Polar Biol 34:1701–1711.  https://doi.org/10.1007/s00300-011-1021-2 CrossRefGoogle Scholar
  28. Overhoff A, Freckman D, Virginia R (1993) Life cycle of the microbivorous Antarctic Dry Valley nematode Scottnema lindsayae (Timm 1971). Polar Biol 13:151–156.  https://doi.org/10.1007/BF00238924 CrossRefGoogle Scholar
  29. Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718.  https://doi.org/10.2307/3071875 CrossRefGoogle Scholar
  30. Powers LE, Ho MC, Freckman DW, Virginia RA (1998) Distribution, community structure, and microhabitats of soil invertebrates along an elevational gradient in Taylor Valley, Antarctica. Arc Alp Res 30:133–141.  https://doi.org/10.1007/BF00238482 CrossRefGoogle Scholar
  31. Shaw EA, Denef K, Milano de Tomasel C, Cotrufo MF, Wall DH (2016) Fire affects root decomposition, soil food web structure, and carbon flow in tallgrass prairie. Soil 2:199–210.  https://doi.org/10.5194/soil-2-199-2016 CrossRefGoogle Scholar
  32. Sohlenius B, Boström S (2005) The geographic distribution of metazoan microfauna on East Antarctic nunataks. Polar Biol 28:439–448.  https://doi.org/10.1007/s00300-004-0708-z CrossRefGoogle Scholar
  33. Spaulding SA, McKnight DM (1998) Diatoms as indicators of environmental change in antarctic freshwaters. In: Smol J, Stoermer EF (eds) The diatoms: applications for the environmental and earth sciences. Cambridge University Press, Cambridge, pp 249–263Google Scholar
  34. Stirling G (2014) Biological control of plant-parasitic nematodes: soil ecosystem management in sustainable agriculture, 2nd edn. CABI, BostonCrossRefGoogle Scholar
  35. Tjepkema J, Ferris V, Ferris J (1971) Review of the Genus Aporcelaimellus Heyns, 1965 and Six Species Groups of the Genus Eudorylaimus Andrassy, 1959 (Nematoda: Dorylaimida). Purdue University Agricultural Research Bulletin, 882, West LafayetteGoogle Scholar
  36. Treonis AM, Wall DH, Virginia RA (1999) Invertebrate biodiversity in Antarctic Dry Valley soils and sediments. Ecosystems 2:482–492.  https://doi.org/10.1007/s100219900096 CrossRefGoogle Scholar
  37. Van Horn DJ, Wolf CR, Colman DR, Jiang X, Kohler TJ, McKnight DM, Stanish LF, Yazzie T, Takacs-Vesbach CD (2016) Patterns of bacterial biodiversity in the glacial meltwater streams of the McMurdo Dry Valleys, Antarctica. FEMS Microbiol Ecol 92:1–16.  https://doi.org/10.1093/femsec/fiw148 Google Scholar
  38. Velásquez D, Jungblut AD, Rochera C, Rico E, Camacho A, Quesada A (2017) Trophic interactions in microbial mats on Byers Peninsula, maritime Antarctica. Polar Biol 40:1115–1126.  https://doi.org/10.1007/s00300-016-2039-2 CrossRefGoogle Scholar
  39. Virginia RA, Wall DH (1999) How soils structure communities in the Antarctic Dry Valleys. Bioscience 49:973–983.  https://doi.org/10.1525/bisi.1999.49.12.973 CrossRefGoogle Scholar
  40. Wall DH (2007) Global change tipping points: above- and below-ground biotic interactions in a low diversity ecosystem. Philos Trans R Soc Lond B Biol Sci 362:2291–2306.  https://doi.org/10.1098/rstb.2006.1950 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Wall DH, Virginia RA (1999) Controls on soil biodiversity: insights from extreme environments. Appl Soil Ecol 13:137–150.  https://doi.org/10.1016/S0929-1393(99)00029-3 CrossRefGoogle Scholar
  42. Wood FH (1973) Nematodes feeding relationships: feeding relationships of soil-dwelling nematodes. Soil Biol Biochem 5:593–601.  https://doi.org/10.1016/0038-0717(73)90049-7 CrossRefGoogle Scholar
  43. Yeates G, Bongers T, de Goede R, Freckman D, Georgieva S (1993) Feeding habits in soil nematode families and genera: an outline for soil ecologists. J Nematol 25:315–331PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Biology and Natural Resource Ecology LaboratoryColorado State UniversityFort CollinsUSA
  2. 2.Department of Biology, Evolutionary Ecology Laboratories, and Monte L. Bean MuseumBrigham Young UniversityProvoUSA
  3. 3.Biological SciencesVirginia Polytechnic Institute and State UniversityBlacksburgUSA
  4. 4.School of Earth Science, Byrd Polar Research CenterThe Ohio State UniversityColumbusUSA
  5. 5.Environmental Studies ProgramDartmouth CollegeHanoverUSA

Personalised recommendations