Polar Biology

, Volume 39, Issue 4, pp 583–592 | Cite as

Impact of diurnal freeze–thaw cycles on the soil nematode Scottnema lindsayae in Taylor Valley, Antarctica

  • Matthew A. Knox
  • Diana H. Wall
  • Ross A. Virginia
  • Martijn L. Vandegehuchte
  • Inigo San Gil
  • Byron J. Adams
Original Paper


Global climate change scenarios predict not only higher temperatures, but also increased climatic variability. In cold regions, these changes may bring about a shift in the frequency of soil freeze–thaw cycles (FTCs), which represent a significant physiological challenge, especially for small, poikilothermic animals with limited mobility. To assess the impact of FTCs on cold-adapted soil biota, we evaluated freeze–thaw dynamics (i.e., 0 °C crossings) and demographics of the dominant nematode Scottnema lindsayae (proportion of adults, population size) over 20 years in soils at two locations in Taylor Valley, Antarctica. Based on hourly soil temperature data, we demonstrate that FTCs are a frequent feature in Taylor Valley, but with high inter-annual and spatial variability. Valley topography and soil moisture were found to impact FTC frequency, suggesting that basins within Taylor Valley have different susceptibilities to environmental variability. Increased FTC frequency in 1999–2001 coincided with a shift in S. lindsayae populations, with fewer juveniles reaching maturity. In the years following decreased adult proportions, overall S. lindsayae numbers were reduced, implying a strong negative effect of FTCs on in situ recruitment. Our results suggest that increased FTC frequency in the Dry Valleys slows S. lindsayae development, reducing reproductive success, and may take years to impact population size, which demonstrates the importance of long-term research to accurately predict the consequences of climate change on soil biota and biogeochemical cycling in the cold regions.


Dry Valleys Nematodes Anhydrobiosis Climate change Extreme environment Demographics Soil fauna Long-term research 



This research was funded by McMurdo LTER NSF OPP Grant 1115245 to DHW, RAV, and BJA. The lab and fieldwork for this project was carried out with the indispensible help of numerous postdocs and students associated with the MCM LTER. We gratefully acknowledge the assistance of the Crary Laboratory staff, Raytheon Polar Services, and PHI Helicopters Inc. for supporting the logistical aspects of this project.

Supplementary material

300_2015_1809_MOESM1_ESM.docx (104 kb)
Supplementary material 1 (DOCX 103 kb)
300_2015_1809_MOESM2_ESM.docx (104 kb)
Supplementary material 2 (DOCX 104 kb)
300_2015_1809_MOESM3_ESM.docx (89 kb)
Supplementary material 3 (DOCX 89 kb)


  1. Adams BJ et al (2006) Diversity and distribution of Victoria Land biota. Soil Biol Biochem 38:3003–3018. doi: 10.1016/j.soilbio.2006.04.030 CrossRefGoogle Scholar
  2. Adams BJ, Wall DH, Virginia RA, Broos E, Knox MA (2014) Ecological biogeography of the terrestrial nematodes of Victoria Land. ZooKeys, Antarctica. doi: 10.3897/zookeys.419.7180 Google Scholar
  3. Adhikari BN, Adams BJ (2011) Molecular analysis of desiccation survival in Antarctic nematodes. In: Perry RN, Wharton DA (eds) Molecular and physiological basis of nematode survival. CABI International, WallingfordGoogle Scholar
  4. Adhikari BN, Wall DH, Adams BJ (2010) Effect of slow desiccation and freezing on gene transcription and stress survival of an Antarctic nematode. J Exp Biol 213:1803–1812. doi: 10.1242/jeb.032268 CrossRefPubMedGoogle Scholar
  5. Ashcroft MB, Gollan JR (2013) Moisture, thermal inertia, and the spatial distributions of near-surface soil and air temperatures: understanding factors that promote microrefugia. Agr For Meteorol 176:77–89. doi: 10.1016/j.agrformet.2013.03.008 CrossRefGoogle Scholar
  6. Barrett JE, Virginia RA, Wall DH, Parsons AN, Powers LE, Burkins MB (2004) Variation in biogeochemistry and soil biodiversity across spatial scales in a polar desert ecosystem. Ecology 85:3105–3118. doi: 10.1890/03-0213 CrossRefGoogle Scholar
  7. Barrett JE, Virginia RA, Parsons AN, Wall DH (2006a) Soil carbon turnover in the McMurdo Dry Valleys, Antarctica. Soil Biol Biochem 38:3065–3082. doi: 10.1016/j.soilbio.2006.03.025 CrossRefGoogle Scholar
  8. Barrett JE, Virginia RA, Wall DH, Cary SC, Adams BJ, Hacker AL, Aislabie JM (2006b) Co-variation in soil biodiversity and biogeochemistry in northern and southern Victoria Land, Antarctica. Antarct Sci 18:535. doi: 10.1017/s0954102006000587 CrossRefGoogle Scholar
  9. Barrett JE, Virginia RA, Wall DH, Adams BJ (2008a) Decline in a dominant invertebrate species contributes to altered carbon cycling in a low-diversity soil ecosystem. Glob Change Biol 14:1734–1744. doi: 10.1111/j.1365-2486.2008.01611.x CrossRefGoogle Scholar
  10. Barrett JE, Virginia RA, Wall DH, Doran PT, Fountain AG, Welch KA, Lyons WB (2008b) Persistent effects of a discrete warming event on a polar desert ecosystem. Glob Change Biol 14:2249–2261. doi: 10.1111/j.1365-2486.2008.01641.x CrossRefGoogle Scholar
  11. Bing H, Ma W (2011) Laboratory investigation of the freezing point of saline soil. Cold Reg Sci Technol 67:79–88. doi: 10.1016/j.coldregions.2011.02.008 CrossRefGoogle Scholar
  12. Block W, Lewis Smith RI, Kennedy AD (2009) Strategies of survival and resource exploitation in the Antarctic fellfield ecosystem. Biol Rev 84:449–484. doi: 10.1111/j.1469-185X.2009.00084.x CrossRefPubMedGoogle Scholar
  13. Bokhorst S, Phoenix GK, Bjerke JW, Callaghan TV, Huyer-Brugman F, Berg MP (2012) Extreme winter warming events more negatively impact small rather than large soil fauna: shift in community composition explained by traits not taxa. Glob Change Biol 18:1152–1162. doi: 10.1111/j.1365-2486.2011.02565.x CrossRefGoogle Scholar
  14. Boström S, Holovachov O, Nadler SA (2011) Description of Scottnema lindsayae Timm, 1971 (Rhabditida: Cephalobidae) from Taylor Valley, Antarctica and its phylogenetic relationship. Polar Biol 34:1–12. doi: 10.1007/s00300-010-0850-8 CrossRefGoogle Scholar
  15. Campbell IB, Claridge GGC, Balks MR, Campbell DI (1997) Moisture content in soils of the McMurdo sound and Dry Valley region of Antarctica. In: Lyons B, Howard-Williams C, Hawes I (eds) Ecosystem processes in Antarctic ice-free landscapes. Balkerna, RotterdamGoogle Scholar
  16. Chapman WL, Walsh JE (2007) A synthesis of Antarctic temperatures. J Clim 20:4096–4117. doi: 10.1175/jcli4236.1 CrossRefGoogle Scholar
  17. Courtright EM, Wall DH, Virginia RA (2001) Determining habitat suitability for soil invertebrates in an extreme environment: the McMurdo Dry Valleys, Antarctica. Antarct Sci 13:9–17. doi: 10.1017/S0954102001000037 CrossRefGoogle Scholar
  18. Cozzetto K, McKnight D, Nylen T, Fountain A (2006) Experimental investigations into processes controlling stream and hyporheic temperatures, Fryxell Basin, Antarctica. Adv Water Resour 29:130–153. doi: 10.1016/j.advwatres.2005.04.012 CrossRefGoogle Scholar
  19. Crowe JH, Madin KAC (1975) Anhydrobiosis in nematodes: evaporative water loss and survival. J Exp Zool 193:323–334. doi: 10.1002/jez.1401930308 CrossRefGoogle Scholar
  20. Dam M, Vestergård M, Christensen S (2012) Freezing eliminates efficient colonizers from nematode communities in frost-free temperate soils. Soil Biol Biochem 48:167–174. doi: 10.1016/j.soilbio.2012.01.017 CrossRefGoogle Scholar
  21. Doran PT et al (2002) Antarctic climate cooling and terrestrial ecosystem response. Nature 415:517–520. doi: 10.1038/nature710 CrossRefPubMedGoogle Scholar
  22. Doran PT, McKay CP, Fountain AG, Nylen T, McKnight DM, Jaros C, Barrett JE (2008) Hydrologic response to extreme warm and cold summers in the McMurdo Dry Valleys, East Antarctica. Antarct Sci 20:499–509. doi: 10.1017/s0954102008001272 CrossRefGoogle Scholar
  23. Fogt RL, Scambos TA (2012) Antarctica: in “state of the climate in 2011”. B Am Meteorol Soc 93:S149–S162Google Scholar
  24. Forcada J, Trathan PN (2009) Penguin responses to climate change in the Southern Ocean. Glob Change Biol 15:1618–1630. doi: 10.1111/j.1365-2486.2009.01909.x CrossRefGoogle Scholar
  25. Fountain AG, Levy JS, Gooseff MN, Van Horn D (2014) The McMurdo Dry Valleys: a landscape on the threshold of change. Geomorphology 225:25–35. doi: 10.1016/j.geomorph.2014.03.044 CrossRefGoogle Scholar
  26. Freckman D, Virginia RA (1997) Low-diversity Antarctic soil nematode communities: Distribution and response to disturbance. Ecology 78:363–369. doi: 10.2307/2266013 CrossRefGoogle Scholar
  27. Frenot Y, Chown SL, Whinam J, Selkirk PM, Convey P, Skotnicki M, Bergstrom DM (2005) Biological invasions in the Antarctic: extent, impacts and implications. Biol Rev 80:45–72. doi: 10.1017/s1464793104006542 CrossRefPubMedGoogle Scholar
  28. IPCC (2013) Climate change 2013: the physical science basis. In: Contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change. Cambridge University Press, CambridgeGoogle Scholar
  29. Kozlowski T (2009) Some factors affecting supercooling and the equilibrium freezing point in soil–water systems. Cold Reg Sci Technol 59:25–33. doi: 10.1016/j.coldregions.2009.05.009 CrossRefGoogle Scholar
  30. Larsen KS, Jonasson S, Michelsen A (2002) Repeated freeze–thaw cycles and their effects on biological processes in two arctic ecosystem types. Appl Soil Ecol 21:187–195. doi: 10.1016/S0929-1393(02)00093-8 CrossRefGoogle Scholar
  31. Levy J (2012) How big are the McMurdo Dry Valleys? Estimating ice-free area using Landsat image data. Antarct Sci 25:119–120. doi: 10.1017/S0954102012000727 CrossRefGoogle Scholar
  32. Marshall KE, Sinclair BJ (2015) The relative importance of number, duration and intensity of cold stress events in determining survival and energetics of an overwintering insect. Funct Ecol 29:357–366. doi: 10.1111/1365-2435.12328 CrossRefGoogle Scholar
  33. McGill LM et al (2015) Anhydrobiosis and freezing-tolerance: adaptations that facilitate the establishment of Panagrolaimus nematodes in polar habitats. PLoS ONE 10:e0116084. doi: 10.1371/journal.pone.0116084 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Moorhead DL, Wall DH, Virginia RA, Parsons AN (2002) Distribution and life-cycle of Scottnema lindsayae (Nematoda) in Antarctic soils: a modeling analysis of temperature responses. Polar Biol 25:118–125. doi: 10.1007/s003000100319 CrossRefGoogle Scholar
  35. Nielsen UN, Wall DH, Adams BJ, Virginia RA, Ball BA, Gooseff MN, McKnight DM (2012) The ecology of pulse events: insights from an extreme climatic event in a polar desert ecosystem. Ecosphere 3:art17. doi: 10.1890/es11-00325.1 CrossRefGoogle Scholar
  36. Nkem JN, Virginia RA, Barrett JE, Wall DH, Li G (2006) Salt tolerance and survival thresholds for two species of Antarctic soil nematodes. Polar Biol 29:643–651. doi: 10.1007/s00300-005-0101-6 CrossRefGoogle Scholar
  37. Overhoff A, Freckman DW, Virginia RA (1993) Life cycle of the microbivorous Antarctic Dry Valley nematode Scottnema lindsayae (Timm 1971). Polar Biol 13:151–156. doi: 10.1007/BF00238924 CrossRefGoogle Scholar
  38. Pickup J (1990) Strategies of cold-hardiness in three species of Antarctic dorylaimid nematodes. J Comp Physiol B 160:167–173. doi: 10.1007/BF00300949 CrossRefGoogle Scholar
  39. 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. doi: 10.1657/1523-0430%2806-051%29%5BPOAGE%5D2.0.CO%3B2 CrossRefGoogle Scholar
  40. Porazinska DL, Wall DH, Virginia RA (2002) Population age structure of nematodes in the Antarctic Dry Valleys: perspectives on time, space, and habitat. Arct Antarct Alp Res 34:159–168. doi: 10.2307/1552467 CrossRefGoogle Scholar
  41. Powers LE, Freckman DW, Virginia RA (1995) Spatial distribution of nematodes in polar desert soils of Antarctica. Polar Biol 15:325–333. doi: 10.1007/BF00238482 CrossRefGoogle Scholar
  42. R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  43. Robinson S, Wasley J, Tobin AK (2003) Living on the edge—plants and global change in continental and maritime Antarctica. Glob Change Biol 9:1681–1717. doi: 10.1046/j.1529-8817.2003.00693.x CrossRefGoogle Scholar
  44. Sharma S, Szele Z, Schilling R, Munch JC, Schloter M (2006) Influence of freeze-thaw stress on the structure and function of microbial communities and denitrifying populations in soil. Appl Environ Microb 72:2148–2154. doi: 10.1128/AEM.72.3.2148-2154.2006 CrossRefGoogle Scholar
  45. Simmons BL, Wall DH, Adams BJ, Ayres E, Barrett JE, Virginia RA (2009) Long-term experimental warming reduces soil nematode populations in the McMurdo Dry Valleys, Antarctica. Soil Biol Biochem 41:2052–2060. doi: 10.1016/j.soilbio.2009.07.009 CrossRefGoogle Scholar
  46. Smith TE, Wall DH, Hogg ID, Adams BJ, Nielsen UN, Virginia RA (2012) Thawing permafrost alters nematode populations and soil habitat characteristics in an Antarctic polar desert ecosystem. Pedobiologia 55:75–81. doi: 10.1016/j.pedobi.2011.11.001 CrossRefGoogle Scholar
  47. Sutinen M-L, Mäkitalo K, Sutinen R (1996) Freezing dehydration damages roots of containerized Scots pine (Pinussylvestris) seedlings overwintering under subarctic conditions. Can J For Res 26:1602–1609. doi: 10.1139/x26-180 CrossRefGoogle Scholar
  48. Timm RW (1971) Antarctic soil and freshwater nematodes from the McMurdo Sound region. Proc Helminthol Soc Wash 38:42–52Google Scholar
  49. Treonis AM, Wall DH (2005) Soil nematodes and desiccation survival in the extreme arid environment of the Antarctic Dry Valleys. Integr Comp Biol 45:741–750. doi: 10.1093/icb/45.5.741 CrossRefPubMedGoogle Scholar
  50. Treonis AM, Wall DH, Virginia RA (1999) Invertebrate biodiversity in Antarctic Dry Valley soils and sediments. Ecosystems 2:482–492. doi: 10.1007/s100219900096 CrossRefGoogle Scholar
  51. Treonis AM, Wall DH, Virginia RA (2000) The use of anhydrobiosis by soil nematodes in the Antarctic Dry Valleys. Funct Ecol 14:460–467. doi: 10.1046/j.1365-2435.2000.00442.x CrossRefGoogle Scholar
  52. Wall DH, Virginia RA (1999) Controls on soil biodiversity: insights from extreme environments. Appl Soil Ecol 13:137–150. doi: 10.1016/s0929-1393(99)00029-3 CrossRefGoogle Scholar
  53. Weicht T, Moorhead D (2004) The impact of anhydrobiosis on the persistence of Scottnema lindsayae (Nematoda): a modeling analysis of population stability thresholds. Polar Biol 27:507–512. doi: 10.1007/s00300-004-0621-5 CrossRefGoogle Scholar
  54. Wharton DA (2003) The environmental physiology of Antarctic terrestrial nematodes: a review. J Comp Physiol B 173:621–628. doi: 10.1007/s00360-003-0378-0 CrossRefPubMedGoogle Scholar
  55. Wharton DA, Barclay S (1993) Anhydrobiosis in the free-living antarctic nematode Panagrolaimus davidi (Nematoda: Rhabditida). Fund Appl Nematol 16:17–22Google Scholar
  56. Wharton DA, Block W (1993) Freezing tolerance in some Antarctic nematodes. Funct Ecol 7:578–584. doi: 10.2307/2390134 CrossRefGoogle Scholar
  57. Wharton DA, Ferns DJ (1995) Survival of intracellular freezing by the Antarctic nematode Panagrolaimus davidi. J Exp Biol 198:1381–1387PubMedGoogle Scholar
  58. Wharton DA, Goodall G, Marshall CJ (2003) Freezing survival and cryoprotective dehydration as cold tolerance mechanisms in the Antarctic nematode Panagrolaimus davidi. J Exp Biol 206:215–221. doi: 10.1242/jeb.00083 CrossRefPubMedGoogle Scholar
  59. Yanai Y, Toyota K, Okazaki M (2004) Effects of successive soil freeze-thaw cycles on soil microbial biomass and organic matter decomposition potential of soils. Soil Sci Plant Nutr 50:821–829. doi: 10.1080/00380768.2004.10408542 CrossRefGoogle Scholar
  60. Yeates GW, Scott MB, Chown SL, Sinclair BJ (2009) Changes in soil nematode populations indicate an annual life cycle at Cape Hallett, Antarctica. Pedobiologia 52:375–386. doi: 10.1016/j.pedobi.2009.01.001 CrossRefGoogle Scholar
  61. Yergeau E, Kowalchuk GA (2008) Responses of Antarctic soil microbial communities and associated functions to temperature and freeze-thaw cycle frequency. Environ Microbiol 10:2223–2235. doi: 10.1111/j.1462-2920.2008.01644.x CrossRefPubMedGoogle Scholar
  62. 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. doi: 10.1111/j.1574-6941.2006.00200.x CrossRefPubMedGoogle Scholar
  63. Zhu R, Liu Y, Ma E, Sun J, Xu H, Sun L (2009) Greenhouse gas emissions from penguin guanos and ornithogenic soils in coastal Antarctica: effects of freezing–thawing cycles. Atmos Environ 43:2336–2347. doi: 10.1016/j.atmosenv.2009.01.027 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.Department of BiologyColorado State UniversityFort CollinsUSA
  2. 2.School of Global Environmental SustainabilityColorado State UniversityFort CollinsUSA
  3. 3.Environmental Studies ProgramDartmouth CollegeHanoverUSA
  4. 4.Research Unit Community EcologySwiss Federal Institute for Forest, Snow and Landscape ResearchBirmensdorfSwitzerland
  5. 5.LTER Network Office, Department of BiologyUniversity of New MexicoAlbuquerqueUSA
  6. 6.Department of Biology, and Evolutionary Ecology LaboratoriesBrigham Young UniversityProvoUSA

Personalised recommendations