Ecological Research

, Volume 29, Issue 4, pp 593–606 | Cite as

Winter climate change in plant–soil systems: summary of recent findings and future perspectives

  • Kobayashi Makoto
  • Takuya Kajimoto
  • Lina Koyama
  • Gaku Kudo
  • Hideaki Shibata
  • Yosuke Yanai
  • J. H. C. Cornelissen
Special Feature Winter Climate Change

Abstract

The winter climate is changing in many parts of the world, and it is predicted that winter climate change will modify the structure and function of plant–soil systems. An understanding of these changes and their consequences in terrestrial ecosystems requires knowledge of the linkage between above- and below-ground components as well as the species interactions found in plant–soil systems, which have important implications for biogeochemical cycles. However, winter climate-change studies have focused on only a part of the ecosystem or ecological process. We summarize here recent findings related to the effects of winter climate and its changes on soil nitrogen (N) dynamics, greenhouse gas (N2O) emissions from the soil, N use by individual plants, vegetation development, and interactions between vegetation and pollinators to generate an integrative understanding of the response of the plant–soil system to winter climate change. This review indicates that the net effects on plants, soil microbes, pollinators, and the associated biogeochemical cycles are balanced among several processes and are highly variable depending on the context, such as the target species/functional group, original winter condition of the habitat, and type of climate change. The consequences of winter climate change for species interactions among plants, associated animals, and biogeochemical cycles are largely unknown. For further research, a large-scale comparative study to measure ecosystem-level functions is important, especially in less-cold ecosystems.

Keywords

Nitrogen Species interaction Context dependence Comparative study design Winter–summer relationship Ecosystem service 

References

  1. Aldridge G, Inouye DW, Forrest JRK, Barr WA, Miller-Rushing AJ (2011) Emergence of a mid-season period of low floral resources in a montane meadow ecosystem associated with climate change. J Ecol 99:905–913Google Scholar
  2. Alford DV (1969) A study of the hibernation of bumblebees (Hymenoptera: Bombidae) in southern England. J Anim Ecol 38:149–170Google Scholar
  3. Amin MR, Suh SJ, Kwon YJ (2007) Impact of artificial photoperiodism on the colony development of the bumblebee Bombus terrestris. Ecol Sci 10:315–321Google Scholar
  4. Augspurger CK (2009) Spring 2007 warmth and frost: phenology, damage and refoliation in a temperate deciduous forest. Funct Ecol 23:10031–11039Google Scholar
  5. Bale JS, Hayward SAL (2010) Insect overwintering in a changing climate. J Exp Biol 213:980–994PubMedGoogle Scholar
  6. Bardgett RD, Manning P, Morriën E, De Vries FT (2013) Hierarchical responses of plant–soil interactions to climate change: consequences for the global carbon cycle. J Ecol 101:334–343Google Scholar
  7. Bascuñán-Godoy L, Sanhueza C, Cuba M, Zuñiga GE, Corcuera LJ, Bravo LA (2012) Cold-acclimation limits low temperature induced photoinhibition by promoting a higher photochemical quantum yield and a more effective PSII restoration in darkness in the Antarctic rather than the Andean ecotype of Colobanthus quitensis Kunt Bartl (Cariophyllaceae). BMC Plant Biol 12:114PubMedCentralPubMedGoogle Scholar
  8. Baskin CC, Milberg P, Andersson L, Baskin JM (2000) Germination studies of three dwarf shrubs (Vaccinium, Ericaceae) of northern hemisphere coniferous forests. Can J Bot 78:1552–1560Google Scholar
  9. Baskin CC, Zackrisson O, Baskin JM (2002) Role of warm stratification in promoting germination of seeds of Empetrum hermaphroditum (Empetraceae), a circumboreal species with a stony endocarp. Am J Bot 89:486–493PubMedGoogle Scholar
  10. Beekman M, van Stratum P, Lingeman R (1998) Diapause survival and post-diapause performance in bumblebee queens (Bombus terrestris). Entomol Exp Appl 89:207–214Google Scholar
  11. Bell KL, Bliss LC (1979) Autecology of Kobresia bellardii—why winter snow accumulation limits local distribution. Ecol Monogr 49:377–402Google Scholar
  12. Blankinship JC, Hart SC (2012) Consequences of manipulated snow cover on soil gaseous emission and N retention in the growing season: a meta-analysis. Ecosphere 3:1–20Google Scholar
  13. Boggs CL, Inouye DW (2012) A single climate driver has direct and indirect effects on insect population dynamics. Ecol Lett 15:502–508PubMedGoogle Scholar
  14. Bokhorst S, Bjerke JW, Bowles FW, Melillo J, Callaghan TV, Phoenix GK (2008) Impacts of extreme winter warming in the sub-Arctic: growing season responses of dwarf shrub heathland. Global Change Biol 14:2603–2612Google Scholar
  15. 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. Global Change Biol 18:1152–1162Google Scholar
  16. Brooks PD, Grogan P, Templer PH, Groffman P, Oquist MG, Schimel J (2011) Carbon and nitrogen cycling in snow-covered environments. Geogr Compass 5:682–699Google Scholar
  17. Burkle L, Irwin R (2009) The importance of interannual variation and bottom-up nitrogen enrichment for plant–pollinator networks. Oikos 118:1816–1829Google Scholar
  18. Campbell JL, Mitchell MJ, Groffman PM, Christensen LM, Hardy JP (2005) Winter in northeastern North America: a critical period for ecological processes. Front Ecol Environ 3:314–322Google Scholar
  19. Chapin FS (1983) Direct and indirect effects of temperature on arctic plants. Polar Biol 2:47–52Google Scholar
  20. Chen WN, Wu Y, Wu N, Wang Q (2011) Effect of snowmelt time on growth and reproduction of Pedicularis davidii var. pentodon in the eastern Tibetan Plateau. Plant Biosyst 145:802–808Google Scholar
  21. Choi G, Robinson DA, Kang S (2010) Changing northern hemisphere snow seasons. J Clim 23:5305–5310Google Scholar
  22. Christopher SF, Shibata H, Ozawa M, Nakagawa Y, Mitchell MJ (2008) The effect of soil freezing on N cycling: comparison of two headwater subcatchments with different vegetation and snowpack conditions in the northern Hokkaido Island of Japan. Biogeochemistry 88:15–30Google Scholar
  23. Cleavitt NL, Fahey TJ, Groffman PM, Hardy JP, Henry KS, Driscoll CT (2008) Effects of soil freezing on fine roots in a northern hardwood forest. Can J Forest Res 38:82–91Google Scholar
  24. Coop JD, Givnish TJ (2008) Constraints on tree seedling establishment in montane grasslands of the Valles Caldera, New Mexico. Ecology 89:1101–1111PubMedGoogle Scholar
  25. Davidson EA (2009) The contribution of manure and fertilizer nitrogen to atmospheric nitrous oxide since 1860. Nat Geosci 2:659–662Google Scholar
  26. de Bruijn AMG, Butterbach-Bahl K, Blagodatsky S, Grote R (2009) Model evaluation of different mechanisms driving freeze–thaw N2O emissions. Agric Ecosyst Environ 133:196–207Google Scholar
  27. DeLuca TH, Keeney DR, McCarty GW (1992) Effect of freeze–thaw events on mineralization of soil nitrogen. Biol Fert Soils 14:116–120Google Scholar
  28. Densmore RV (1997) Effect of day length on germination of seeds collected in Alaska. Am J Bot 84:274–278PubMedGoogle Scholar
  29. Dias T, Neto D, Martins-Loução MA, Sheppard L, Cruz C (2011) Patterns of nitrate reductase activity vary according to the plant functional group in a Mediterranean maquis. Plant Soil 347:363–376Google Scholar
  30. Diekmann M (1996) Relationship between flowering phenology of perennial herbs and meteorological data in deciduous forests of Sweden. Can J Bot 74:528–537Google Scholar
  31. Drescher M, Thomas SC (2013) Snow cover manipulations alter survival of early life stages of cold-temperate tree species. Oikos 122:541–554Google Scholar
  32. Drotz SH, Sparrman T, Nilsson MB, Schleucher J, Oquist MG (2010) Both catabolic and anabolic heterotrophic microbial activity proceed in frozen soils. Proc Natl Acad Sci USA 107:21046–21051PubMedCentralPubMedGoogle Scholar
  33. Dunne JA, Harte J, Taylor KJ (2003) Subalpine meadow flowering phenology responses to climate change: integrating experimental and gradient methods. Ecol Monogr 73:69–86Google Scholar
  34. Duxbury JM, Bouldin DR, Terry RE, Tate RL III (1982) Emissions of nitrous oxide from soils. Nature 298:462–464Google Scholar
  35. Ellwood ER, Diez JM, Ibáñez I, Primack RB, Kobori H, Higuchi H, Silander JA (2012) Disentangling the paradoz of insect phenology: are temporal trends reflecting the response to warming? Oecologia 168:1161–1171PubMedGoogle Scholar
  36. Elmendorf SC, Henry GH, Hollister RD, Björk RG, Bjorkman AD, Callaghan TV, Collier LS, Cooper EJ, Cornelissen JH, Day TA, Fosaa AM, Gould WA, Grétarsdóttir J, Harte J, Hermanutz L, Hik DS, Hofgaard A, Jarrad F, Jónsdóttir IS, Keuper F, Klanderud K, Klein JA, Koh S, Kudo G, Lang SI, Loewen V, May JL, Mercado J, Michelsen A, Molau U, Myers-Smith IH, Oberbauer SF, Pieper S, Post E, Rixen C, Robinson CH, Schmidt NM, Shaver GR, Stenström A, Tolvanen A, Totland O, Troxler T, Wahren CH, Webber PJ, Welker JM, Wookey PA (2012) Global assessment of experimental climate warming on tundra vegetation: heterogeneity over space and time. Ecol Lett 15:164–175PubMedGoogle Scholar
  37. Feng S, Hu Q (2007) Changes in winter snowfall/precipitation ratio in the contiguous United States. J Geophys Res Atmos 112(D15109)Google Scholar
  38. Field C, Mooney HA (1986) The photosynthesis–nitrogen relationship in wild plants. In: Givnish TJ (ed) On the economy of form and function. Cambridge University Press, Cambridge, pp 25–55Google Scholar
  39. Fitter ML, Fitter RSR (2002) Rapid changes in flowering time in British plants. Science 296:1689–1691PubMedGoogle Scholar
  40. Flessa H, Dörsch P, Beese F (1995) Seasonal variation of nitrous oxide and methane fluxes in differently managed arable soils in southern Germany. J Geophys Res Atmos 100:23115–23124Google Scholar
  41. Forbis TA, Diggle PK (2001) Subnivean embryo development in the alpine herb Caltha leptosepala (Ranunculaceae). Can J Bot 79:635–642Google Scholar
  42. Fornara DA, Tilman D (2008) Plant functional composition influences rates of soil carbon and nitrogen accumulation. J Ecol 96:314–322Google Scholar
  43. Forrest JRK, Thomson JD (2011) An examination of synchrony between insect emergence and flowering in Rocky Mountain meadows. Ecol Monogr 81:469–491Google Scholar
  44. Fujiyama S (1996) Annual thermoperiod regulating an eight year life-cycle of a periodical diplopod, Parafontaria laminata armigera VerhoeV (Diplopoda). Pedobiologia 40:541–547Google Scholar
  45. Galen C, Stanton ML (1993) Short-term responses of alpine buttercups to experimental manipulations of growing-season length. Ecology 74:1052–1058Google Scholar
  46. Gilliam FS, Cook A, Lyter S (2010) Effects of experimental freezing on soil nitrogen dynamics in soils from a net nitrification gradient in a nitrogen-saturated hardwood forest ecosystem. Can J Forest Res 40:436–444Google Scholar
  47. Goldberg SD, Borken W, Gebauer G (2010) N2O emission in a Norway spruce forest due to soil frost: concentration and isotope profiles shed a new light on an old story. Biogeochemistry 97:21–30Google Scholar
  48. Gordo O, Sanz JJ (2005) Phenology and climate change: a long-term study in a Mediterranean locality. Oecologia 146:484–495PubMedGoogle Scholar
  49. Gordo O, Sanz JJ (2006) Temporal trends in phenology of the honey bee Apis mellifera (L.) and the small white Pieris rapae (L.) in the Iberian Peninsula (1952–2004). Ecol Entomol 31:261–268Google Scholar
  50. Grant RF, Pattey E (1999) Mathematical modeling of nitrous oxide emissions from an agricultural field during spring thaw. Global Biogeochem Cycles 13:679–694Google Scholar
  51. Griffith AB, Loik ME (2010) Effects of climate and snow depth on Bromus tectorum population dynamics at high elevation. Oecologia 164:821–832PubMedCentralPubMedGoogle Scholar
  52. Groffman PM, Driscoll CT, Fahey TJ, Hardy JP, Fitzhugh RD, Tierney GL (2001) Colder soils in a warmer world: a snow manipulation study in a northern hardwood forest ecosystem. Biogeochemistry 56:135–150Google Scholar
  53. Groffman PM, Hardy JP, Fashu-Kanu S, Driscoll CT, Cleavitt NL, Fahey TJ, Fisk MC (2011) Snow depth, soil freezing and nitrogen cycling in a northern hardwood forest landscape. Biogeochemistry 102:223–238Google Scholar
  54. Grogan P, Jonasson S (2003) Controls on annual nitrogen cycling in the understory of a subarctic birch forest. Ecology 84:202–218Google Scholar
  55. Haei M, Rousk J, Ilstedt U, Öquist MG, Bååth E, Laudon H (2011) Effects of soil frost on growth, composition and respiration of the soil microbial decomposer community. Soil Biol Biochem 43:2069–2077Google Scholar
  56. Haei M, Öquist MG, Kreyling J, Ilstedt U, Laudon H (2013) Winter climate controls soil carbon dynamics during summer in boreal forests. Environ Res Lett 8:024017Google Scholar
  57. Harada Y, Tsuchiya F, Takeda K, Muneoka T (2009) Characteristics of ground freezing and thawing under snow cover based on long-term observation. Seppyo 71:241–251 (in Japanese with English summary)Google Scholar
  58. Hättenschwiler S, Smith WK (1999) Seedling occurrence in alpine treeline conifers: a case study from the central Rocky Mountains, USA. Acta Oecol 20:219–224Google Scholar
  59. Hegland SJ, Nielsen A, Lázaro A, Bjerknes A-L, Totland Ø (2009) How does climate warming affect plant–pollinator interactions? Ecol Lett 12:184–195PubMedGoogle Scholar
  60. Hirota T, Iwata Y, Hayashi M, Suzuki S, Hamasaki T, Sameshima R, Takayabu I (2006) Decreasing soil-frost depth and its relation to climate change in Tokachi, Hokkaido, Japan. J Meteorol Soc Japan 84:821–833Google Scholar
  61. Högberg P, Granström A, Johansson T, Lundmark-Thelin A, Näsholm T (1986) Plant nitrate reductase activity as an indicator of availability of nitrate in forest soils. Can J Forest Res 16:1165–1169Google Scholar
  62. Högberg P, Högbom L, Näsholm T (1992) Shoot nitrate reductase activities of field-layer species in different forest types. II. Seasonal variation and effects of temperature. Scand J Forest Res 7:1–14Google Scholar
  63. Holdo RM (2007) Elephants, fire and frost can determine community structure and composition in Kalahari woodlands. Ecol Appl 17:558–568PubMedGoogle Scholar
  64. Hoover SER, Ladley JJ, Shchepetkina AA, Tisch M, Gieseg SP, Tylianakis JM (2012) Warming, CO2, and nitrogen deposition interactively affect a plant–pollinator mutualism. Ecol Lett 15:227–234PubMedGoogle Scholar
  65. Hosaka M, Nohara D, Kitoh A (2005) Changes in snow cover and snow water equivalent due to global warming simulated by a 20 km-mesh global atmospheric model. SOLA 1:93–96Google Scholar
  66. Høye TT, Forchhammer MC (2008) Phenology of high-arctic arthropods: effects of climate on spatial, seasonal, and inter-annual variation. Adv Ecol Res 40:299–324Google Scholar
  67. Hülber K, Winkler M, Grabherr G (2010) Intraseasonal climate and habitat-specific variability controls the flowering phenology of high alpine plant species. Funct Ecol 24:245–252Google Scholar
  68. Igarashi T, Cheng D (1988) Fungal damage caused by Racodium therryanum to regeneration of Japanese larch by natural seeding. Res Bull Coll Exp Forests Hokkaido Univ 45:213–219Google Scholar
  69. Iler AM, Inouye DW, Høye TT, Miller-Rushing AJ, Burkle LA, Johnston EB (2013) Maintenance of temporal synchrony between syrphid flies and their floral resources despite differential phenological responses to climate change. Global Change Biol 19:2348–2359Google Scholar
  70. Inari N, Hiura T, Toda MJ, Kudo G (2012) Pollination linkage between canopy flowering, bumble bee abundance, and seed production of understory plants in a cool-temperate forest. J Ecol 100:1534–1543Google Scholar
  71. Inouye DW (2008) Effects of climate change on phenology, frost damage, and floral abundance of montane wildflowers. Ecology 89:353–362PubMedGoogle Scholar
  72. IPCC (2007) IPCC fourth assessment report: climate change 2007Google Scholar
  73. Ishijima K, Nakazawa T, Aoki S (2009) Variations of atmospheric nitrous oxide concentration in the northern and western Pacific. Tellus B 61:408–415Google Scholar
  74. Jefferies RL, Walker NA, Edwards KA, Dainty J (2010) Is the decline of soil microbial biomass in late winter coupled to changes in the physical state of cold soils? Soil Biol Biochem 42:129–135Google Scholar
  75. Johnson DM, Germino MJ, Smith WK (2004) Abiotic factors limiting photosynthesis in Abies lasiocarpa and Picea engelmannii seedlings below and above the alpine timberline. Tree Physiol 24:377–386PubMedGoogle Scholar
  76. Kaiser WM, Huber SC (2001) Post-translational regulation of nitrate reductase: mechanism, physiological relevance and environmental triggers. J Exp Bot 52:1981–1989PubMedGoogle Scholar
  77. Kaneko N, Salamanca EF (1999) Mixed leaf litter effects on decomposition rates and soil microarthropod communities in an oak-pine stand in Japan. Ecol Res 14:131–138Google Scholar
  78. Kariyapperuma KA, Wagner-Riddle C, Furon AC, Li C (2011) Assessing spring thaw nitrous oxide fluxes simulated by the DNDC model for agricultural soils. Soil Sci Soc Am J 75:678–690Google Scholar
  79. Karl TR, Melillo JM, Peterson TC (2009) Global climate change impacts in the United States. Cambridge University Press, New YorkGoogle Scholar
  80. Katayanagi N, Hatano R (2012) N2O emissions during the freezing and thawing periods from six fields in a livestock farm, southern Hokkaido, Japan. Soil Sci Plant Nutr 58:261–271Google Scholar
  81. Kato T, Kubota S (1982) Reduction and assimilation of 15N-nitrate by citrus trees in cold season in comparison with summer. J Jpn Soc Hortic Sci 50:413–420Google Scholar
  82. Kato T, Kubota S, Bambang S (1982) Uptake of 15 N-nitrate by Citrus trees in winter and repartitioning in spring. J Japan Soc Hortic Sci 50:421–426Google Scholar
  83. Kielland K, Olson K, Ruess RW, Boone RD (2006) Contribution of winter processes to soil nitrogen flux in taiga forest ecosystems. Biogeochemistry 81:349–360Google Scholar
  84. Kim Y, Kimball JS, Zhang K, McDonald KC (2012) Satellite detection of increasing northern hemisphere non-frozen seasons from 1979 to 2008: implications for regional vegetation growth. Remote Sens Environ 121:472–487Google Scholar
  85. Kimball SL, Bennet SD, Salisbury FB (1973) The growth and development of montane species at near freezing temperatures. Ecology 54:168–173Google Scholar
  86. Koga N (2013) Nitrous oxide emissions under a four-year crop rotation system in northern Japan: impacts of reduced tillage, composted cattle manure application and increased plant residue input. Soil Sci Plant Nutr 59:1–13Google Scholar
  87. Koponen HT, Jaakkola T, Keinänen-Toivola MM, Kaipainen S, Tuomainen J, Servomaa K, Martikainen PJ (2006) Microbial communities, biomass, and activities in soils as affected by freeze thaw cycles. Soil Biol Biochem 38:1861–1871Google Scholar
  88. Körner C (2003) Alpine plant life: functional plant ecology of high mountain ecosystems, 2nd edn. Springer, Berlin Heidelberg New YorkGoogle Scholar
  89. Koyama L, Tokuchi N, Fukushima K, Terai M, Yamamoto Y (2008) Seasonal changes in nitrate use by three woody species: the importance of the leaf-expansion period. Trees 22:851–859Google Scholar
  90. Kreyling J (2010) Winter climate change: a critical factor for temperate vegetation performance. Ecology 91:1939–1948PubMedGoogle Scholar
  91. Kreyling J, Henry HAL (2011) Vanishing winters in Germany: soil frost dynamics and snow cover trends, and ecological implications. Clim Res 46:269–276Google Scholar
  92. Kreyling J, Jurasinski G, Grant G, Retzer V, Jentsch A, Beierkuhnlein C (2011) Winter warming pulses affect the development of planted temperate grassland and dwarf-shrub heath communities. Plant Ecol Divers 4:13–21Google Scholar
  93. Kreyling J, Wiesenberg GLB, Huber G, Jentsch A, Konnert M, Thiel D, Walter J, Wohlfahrt C, Beierkuhnlein C (2012) Cold hardiness of Pinus nigra Arnold as influenced by geographic origin, warming, and extreme summer drought. Environ Exp Bot 78:99–108Google Scholar
  94. Kudo G (2006) Flowering phenologies of animal-pollinated plants: reproductive strategies and agents of selection. In: Harder LD, Barrett SCH (eds) Ecology and evolution of flowers. Oxford University Press, New York, pp 139–158Google Scholar
  95. Kudo G (2013) Vulnerability of phenological synchrony between plants and pollinators in an alpine ecosystem. Ecol Res. doi:10.1007/s11284-013-1108-z
  96. Kudo G, Hirao AS (2006) Habitat-specific responses in the flowering phenology and seed set of alpine plants to climate variation: implications for global-change impacts. Popul Ecol 48:49–58Google Scholar
  97. Kudo G, Ida T (2013) Early onset of spring increases the phenological mismatch between plants and pollinators. Ecology 94:2311–2320PubMedGoogle Scholar
  98. Lambrecht SC, Shattuck AK, Loik ME (2007) Combined drought and episodic freezing effects on seedlings of low- and high-elevation subspecies of sagebrush (Artemisia tridentata). Physiol Plant 130:207–217Google Scholar
  99. Larsen KS, Michelsen A, Jonasson S, Beier C, Grogan P (2012) Nitrogen uptake during fall, winter and spring differs among plant functional groups in a subarctic heath ecosystem. Ecosystems 15:927–939Google Scholar
  100. Lillo C (1994) Light regulation of nitrate reductase in green leaves of higher plants. Physiol Plant 90:616–620Google Scholar
  101. Lipson DA, Schadt CW, Schmidt SK (2002) Changes in soil microbial community structure and function in an alpine dry meadow following spring snow melt. Microb Ecol 43:307–314PubMedGoogle Scholar
  102. Ludwig B, Wolf I, Teepe R (2004) Contribution of nitrification and denitrification to the emission of nitrous oxide in a freeze–thaw event in an agricultural soil. J Plant Nutr Soil Sci 167:678–684Google Scholar
  103. Ludwig B, Teepe R, de Gerenyu VL, Flessa H (2006) CO2 and N2O emissions from gleyic soils in the Russian tundra and a German forest during freeze–thaw periods—a microcosm study. Soil Biol Biochem 38:3516–3519Google Scholar
  104. Lundell R, Saarinen T, Åström H, Hänninen H (2008) The boreal dwarf shrub Vaccinium vitis-idea retains its capacity for photosynthesis through the winter. Botany 86:491–500Google Scholar
  105. Makoto K, Klaminder J (2012) The influence of non-sorted circles on species diversity of vascular plants, bryophytes and lichens in sub-arctic tundra. Polar Biol 35:1659–1667Google Scholar
  106. Maljanen M, Kohonen AR, Virkajärvi P, Martikainen PJ (2007) Fluxes and production of N2O, CO2 and CH4 in boreal agricultural soil during winter as affected by snow cover. Tellus B 59:853–859Google Scholar
  107. Matzner E, Borken W (2008) Do freeze–thaw events enhance C and N losses from soils of different ecosystems? A review. Eur J Soil Sci 59:274–284Google Scholar
  108. McKinney AM, CaraDonna PJ, Inouye DW, Barr B, Bertelsen CD, Waser NM (2012) Asynchronous changes in phenology of migrating Broad-tailed Hummingbirds and their early-season nectar resources. Ecology 93:1987–1993PubMedGoogle Scholar
  109. Memmott J, Craze PG, Waser NM, Price MV (2007) Global warming and the disruption of plant–pollinator interactions. Ecol Lett 10:710–717PubMedGoogle Scholar
  110. Milbau A, Graae BJ, Shevtsova A, Nijs I (2009) Effects of a warmer climate on seed germination in the subarctic. Ann Bot 104:287–296PubMedCentralPubMedGoogle Scholar
  111. Miller-Rushing AJ, Høye TT, Inouye DW, Post E (2010) The effects of phenological mismatches on demography. Philos Trans R Soc B 365:3177–3186Google Scholar
  112. Mitchell MJ, Driscoll CT, Kahl JS, Likens GE, Murdoch PS, Pardo LH (1996) Climatic control of nitrate loss from forested watersheds in the northeast United States. Environ Sci Technol 30:2609–2612Google Scholar
  113. Miyazawa Y, Kikuzawa K (2005) Winter photosynthesis by saplings of evergreen broad-leaved trees in a deciduous temperate forest. New Phytol 165:857–866PubMedGoogle Scholar
  114. Mørkved PT, Dörsch P, Henriksen TM, Bakken LR (2006) N2O emissions and product ratios of nitrification and denitrification as affected by freezing and thawing. Soil Biol Biochem 38:3411–3420Google Scholar
  115. Mote PW, Hamlet AF, Clark MP, Lettenmaier DP (2005) Declining mountain snowpack in western North America. Bull Am Meteorol Soc 86:39–49Google Scholar
  116. Muller O, Hikosaka K, Hirose T (2005) Seasonal changes in light and temperature affect the balance between light utilisation and light harvesting components of photosynthesis in an evergreen understorey. Oecologia 143:501–508PubMedGoogle Scholar
  117. Muller O, Oguchi R, Hirose T, Werger MJA, Hikosaka K (2009) The leaf anatomy of a broad-leaved evergreen allows an increase in nitrogen content in winter. Physiol Plant 136:299–309PubMedGoogle Scholar
  118. Müller C, Martin M, Stevens RJ, Laughlin RJ, Kammann C, Ottow JCG, Jäger H-J (2002) Processes leading to N2O emissions in grassland soil during freezing and thawing. Soil Biol Biochem 34:1325–1331Google Scholar
  119. Norman J, Jansson P-E, Farahbakhshazad N, Butterbach-Bahl K, Li C, Klemedtsson L (2008) Simulation of NO and N2O emissions from a spruce forest during a freeze/thaw event using an N-flux submodel from the PnET-N-DNDC model integrated to CoupModel. Ecol Model 216:18–30Google Scholar
  120. Ohlson M, Högbom L (1993) Species-specific dynamics in nitrate reductase activity in coexisting swamp forest plants. J Ecol 81:739–744Google Scholar
  121. Olofsson J, Ericson L, Torp M, Stark S, Baxter R (2011) Carbon balance of Arctic tundra under increased snow cover mediated by a plant pathogen. Nat Clim Change 1:220–223Google Scholar
  122. Onipchenko VG, Makarov MI, van Logtestijn RS, Ivanov VB, Akhmetzhanova AA, Tekeev DK, Ermak AA, Salpagarova FS, Kozhevnikova AD, Cornelissen JHC (2009) New nitrogen uptake strategy: specialized snow roots. Ecol Lett 12:758–764PubMedGoogle Scholar
  123. Öquist MG, Nilsson M, Sörensson F, Kaisimir-Klemedtsson Å, Persson T, Weslien P, Klemedtsson L (2004) Nitrous oxide production in a forest soil at low temperatures—processes and environmental controls. FEMS Microbiol Ecol 49:371–378PubMedGoogle Scholar
  124. Osawa A, Matsuura Y, Kajimoto T (2010) Characteristics of permafrost forests in Siberia and potential responses to warming climate. In: Osawa A, Zyryanova OA, Matsuura Y, Kajimoto T, Wein RW (eds) Permafrost ecosystems: Siberian larch forests. Ecological studies, vol 209. Springer, Berlin Heidelberg New York, pp 459–482Google Scholar
  125. Park JH, Duan L, Kim B, Mitchell MJ, Shibata H (2010) Potential effects of climate change and variability on watershed biogeochemical processes and water quality in northeast Asia. Environ Int 36:212–225PubMedGoogle Scholar
  126. Parmesan C (2007) Influences of species, latitudes and methodologies on estimates of phenological response to global warming. Global Change Biol 13:1860–1872Google Scholar
  127. Pearson J, Ji YM (1994) Seasonal variation of leaf glutamine synthetase isoforms in temperate deciduous trees strongly suggests different functions for the enzymes. Plant Cell Environ 17:1331–1337Google Scholar
  128. Pelster DE, Chantigny MH, Rochette P, Angers DA, Laganière J, Zebarth B, Goyer C (2013) Crop residue incorporation alters soil nitrous oxide emissions during freeze–thaw cycles. Can J Soil Sci 93:1–11Google Scholar
  129. Phillips RL (2008) Denitrification in cropping systems at sub-zero soil temperatures—a review. Agron Sustain Dev 28:87–93Google Scholar
  130. Phoenix GK, Lee JA (2004) Predicting impacts of arctic climate change: past lessons and future challenges. Ecol Res 19:65–74Google Scholar
  131. Rafferty NE, Ives AR (2011) Effects of experimental shifts in flowering phenology on plant–pollinator interactions. Ecol Lett 14:69–74PubMedGoogle Scholar
  132. Ramirez N (2010) Vegetation structure and pollination in the Venezuelan Central Plain. Flora 205:229–241Google Scholar
  133. Ravishankara AR, Daniel JS, Portmann RW (2009) Nitrous oxide (N2O): the dominant ozone-depleting substance emitted in the 21st century. Science 326:123–125PubMedGoogle Scholar
  134. Reich PB, Naeem S, Tilman D, Ellsworth D, Knops J, Craine J, Trost J, Wedin D (2004) Species and functional group diversity independently influence biomass accumulation and its response to elevated CO2 and N. Proc Natl Acad Sci USA 101:10101–10106PubMedCentralPubMedGoogle Scholar
  135. Reynolds DN (1984) Alpine annual plants: phenology, germination, photosynthesis, and growth of three Rocky Mountain species. Ecology 65:759–766Google Scholar
  136. Root TL, Price JF, Hall KR, Schneider SH, Rosenzweig C, Pounds JA (2003) Fingerprints of global warming in wild animals and plants. Nature 421:57–60PubMedGoogle Scholar
  137. Röver M, Heinemeyer O, Kaiser E-A (1998) Microbial induced nitrous oxide emissions from an arable soil during winter. Soil Biol Biochem 30:1859–1865Google Scholar
  138. Rustad LE, Campbell J, Marion GM, Norby RJ, Mitchell MJ, Hartley AE, Cornelissen JHC, Gurevitch J, GCTE Network of Ecosystem Warming Studies (2001) A meta-analysis of the response of soil respiration, net N mineralization, and aboveground plant growth to experimental ecosystem warming. Oecologia 126:543–562Google Scholar
  139. Sakai A, Larcher W (1987) Frost survival of plants: responses and adaptation to freezing stress. Springer, Berlin Heidelberg New YorkGoogle Scholar
  140. Sala OE (1988) The effect of herbivory on vegetation structure. In: Werger MJA, van der Aart PJM, During HJ, Verboeven JTA (eds) Plant form and vegetation structure. SPB Academic Publishing, The Hague, pp 317–330Google Scholar
  141. Schaberg PG, Hennon PE, D’Amore DV, Hawley GJ (2008) Influence of simulated snow cover on the cold tolerance and freezing injury of yellow-cedar seedlings. Global Change Biol 14:1282–1293Google Scholar
  142. Schadt CW, Martin AP, Lipson DA, Schmidt SK (2003) Seasonal dynamics of previously unknown fungal lineages in tundra soils. Science 301:1359–1361PubMedGoogle Scholar
  143. Scherff EJ, Galen C, Stanton ML (1994) Seed dispersal, seedling survival and habitat affinity in a snowbed plant: limits to the distribution of the snow buttercup, Ranunculus adoneus. Oikos 69:405–413Google Scholar
  144. Schimel JP, Mikan C (2005) Changing microbial substrate use in Arctic tundra soils through a freeze–thaw cycle. Soil Biol Biochem 37:1411–1418Google Scholar
  145. Scott PA, Rouse WR (1995) Impacts of increased winter snow cover on upland tundra vegetation—a case example. Clim Res 5:25–30Google Scholar
  146. Serreze MC, Walsh JE, Chapin FS, Osterkamp T, Dyurgerov M, Romanovsky V, Oechel WC, Morison J, Zhang T, Barry RG (2000) Observational evidence of recent change in the northern high-latitude environment. Clim Change 46:159–207Google Scholar
  147. Sgolastra F, Kemp WP, Buckner JS, Pitts-Singer T, Maini S, Bosch J (2011) The long summer: pre-wintering temperatures affect metabolic expenditure and winter survival in a solitary bee. J Insect Physiol 57:1651–1659PubMedGoogle Scholar
  148. Shibata H, Hasegawa Y, Watanabe T, Fukuzawa K (2013) Impact of snowpack decrease on net nitrogen mineralization and nitrification in forest soil of northern Japan. Biogeochemistry. doi:10.1007/s10533-013-9882-9
  149. Shimono Y, Kudo G (2005) Comparisons of germination traits of alpine plants between fellfield and snowbed habitats. Ecol Res 20:189–197Google Scholar
  150. Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (2007) Climate change 2007: the physical science basis, contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, New YorkGoogle Scholar
  151. Stadler J, Gebauer G (1992) Nitrate reduction and nitrate content in ash trees (Fraxinus excelsior L.): distribution between compartments, site comparison and seasonal variation. Trees 6:236–240Google Scholar
  152. Sturm M, Schimel J, Michelson G, Welker J, Oberbauer SF, Liston G, Fahnestock J, Romanovsky VE (2005) The role of winter biological processes in converting arctic tundra to shrubland. Bioscience 55:17–26Google Scholar
  153. Sulkava P, Huhta V (2003) Effects of hard frost and freeze–thaw cycles on decomposer communities and N mineralisation in boreal forest soil. App Soil Ecol 22:225–239Google Scholar
  154. Tauber MJ, Tauber CA (1976) Insect seasonality: diapause maintenance, termination, and postdiapause development. Ann Rev Entomol 21:81–107Google Scholar
  155. Teepe R, Vor A, Beese F, Ludwig B (2004) Emissions of N2O from soils during cycles of freezing and thawing and the effects of soil water, texture and duration of freezing. Euro J Soil Sci 55:357–365Google Scholar
  156. Templer PH (2012) Changes in winter climate: soil frost, root injury, and fungal communities. Plant Soil 353:15–17Google Scholar
  157. Thomson JD (2010) Flowering phenology, fruiting success and progressive deterioration of pollination in an early-flowering geophyte. Philos Trans R Soc B 365:3187–3199Google Scholar
  158. Tierney GL, Fahey TJ, GroVman PM, Hardy JP, Fitzhugh RD, Driscoll CT (2001) Soil freezing alters fine root dynamics in a northern hardwood forest. Biogeochemistry 56:175–190Google Scholar
  159. Tilman D, Downing JA (1994) Biodiversity and stability in grasslands. Nature 367:363–365Google Scholar
  160. Troelstra SR, Wagenaar R, Smant W, De-Boer W (1995) Soil nitrogen transformations and nitrate utilization by Deschampsia flexuosa (L.) Trin. at two contrasting heathland sites. Plant Soil 176:81–93Google Scholar
  161. Ueda MU, Mizumachi E, Tokuchi N (2010) Winter nitrate uptake by the temperate deciduous tree Quercus serrata. J Forest Res 15:411–414Google Scholar
  162. Ueda MU, Muller O, Nakamura M, Nakaji T, Hiura T (2013) Soil warming decreases inorganic and dissolved organic nitrogen pools by preventing the soil from freezing in a cool temperate forest. Soil Biol Biochem 61:105–108Google Scholar
  163. Ushio M, Makoto K, Klaminder J, Nakano S-I (2013) CARD-FISH analysis of prokaryotic community composition and abundance along small-scale vegetation gradients in a dry arctic tundra ecosystem. Soil Biol Biochem 64:147–154Google Scholar
  164. van der Putten WH, Bardgett RD, Bever JD, Bezemer TM, Casper BB, Fukami T, Kardol P, Klironomos JN, Kulmatiski A, Schweitzer JA, Suding KN, Van de Voorde TFJ, Wardle DA (2013) Plant–soil feedbacks: the past, the present and future challenges. J Ecol 101:265–276Google Scholar
  165. Virkajärvi P, Maljanen M, Saarijärvi K, Haapala J, Martikainen PJ (2010) N2O emissions from boreal grass and grass-clover pasture soils. Agric Ecosyst Environ 137:59–67Google Scholar
  166. Vitousek PM, Howarth RW (1991) Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13:87–115Google Scholar
  167. Wagner-Riddle C, Furon A, McLaughlin NL, Lee I, Marbeau J, Jayasundara S, Parkin G, von Bertoldi P, Warland J (2007) Intensive measurement of nitrous oxide emissions from a corn-soybean-wheat rotation under two contrasting management systems over 5 years. Global Change Biol 13:1722–1736Google Scholar
  168. Wagner-Riddle C, Hu QC, van Bochove E, Jayasundara S (2008) Linking nitrous oxide flux during spring thaw to nitrate denitrification in soil profile. Soil Sci Soc Am J 72:908–916Google Scholar
  169. Wahren CHA, Walker MD, Bret-Harte MS (2005) Vegetation responses in Alaskan arctic tundra after 8 years of a summer warming and winter snow manipulation experiment. Global Change Biol 11:537–552Google Scholar
  170. Walker DA, Halfpenny JC, Walker MD, Wessman CA (1993) Long-term studies of snow-vegetation interactions. Bioscience 43:287–301Google Scholar
  171. Walker MD, Walker DA, Welker JM, Arft AM, Bardsley T, Brooks PD, Fahnestock JD, Jones MH, Losleben S, Parsons AN, Seastedt TR, Turner PL (1999) Long-term experimental manipulation of winter snow regime and summer temperature in arctic and alpine tundra. Hydrol Process 13:2315–2330Google Scholar
  172. Walker MD, Wahren CH, Hollister RD, Henry GH, Ahlquist LE, Alatalo JM, Bret-Harte MS, Calef MP, Callaghan TV, Carroll AB, Epstein HE, Jónsdóttir IS, Klein JA, Magnússon B, Molau U, Oberbauer SF, Rewa SP, Robinson CH, Shaver GR, Suding KN, Thompson CC, Tolvanen A, Totland Ø, Turner PL, Tweedie CE, Webber PJ, Wookey PA (2006) Plant community responses to experimental warming across the tundra biome. Proc Natl Acad Sci USA 103:1342–1346PubMedCentralPubMedGoogle Scholar
  173. Wesche K, Pietsch M, Ronnenberg K, Undrakh R, Hensen I (2006) Germination of fresh and frost-treated seeds from dry Central Asian steppes. Seed Sci Res 16:123–136Google Scholar
  174. White J, Son Y, Park Y-L (2009) Temperature-dependent emergence of Osmia cornifrons (Hymenoptera: Megachilidae) adults. J Econ Entomol 102:2026–2032PubMedGoogle Scholar
  175. Wielgolaski F, Inouye DW (2013) Phenology at High Latitude. In: Schwartz MD (ed) Phenology: An Integrative Environmental Science. Springer, Berlin Heidelberg New York, pp. 225-247Google Scholar
  176. Wipf S (2010) Phenology, growth, and fecundity of eight subarctic tundra species in response to snowmelt manipulations. Plant Ecol 207:53–66Google Scholar
  177. Wipf S, Rixen C (2010) A review of snow manipulation experiments in Arctic and alpine tundra ecosystems. Polar Res 29:95–109Google Scholar
  178. Wipf S, Rixen C, Mulder CPH (2006) Advanced snowmelt causes shift towards positive neighbour interactions in a subarctic tundra community. Global Change Biol 12:1496–1506Google Scholar
  179. Wipf S, Stoeckli V, Bebi P (2009) Winter climate change in alpine tundra: plant responses to changes in snow depth and snowmelt timing. Clim Change 94:105–121Google Scholar
  180. Wu Z, Dijkstra P, Koch GW, Hungate BA (2012) Biogeochemical and ecological feedbacks in grassland responses to warming. Nature Clim Change 2:458–461Google Scholar
  181. 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 50:821–829Google Scholar
  182. Yanai Y, Toyota K, Okazaki M (2007) Response of denitrifying communities to successive soil freeze–thaw cycles. Biol Fert Soils 44:113–119Google Scholar
  183. Yanai Y, Hirota T, Iwata Y, Nemoto M, Nagata O, Koga N (2011) Accumulation of nitrous oxide and depletion of oxygen in seasonally frozen soils in northern Japan—snow cover manipulation experiments. Soil Biol Biochem 43:1779–1786Google Scholar
  184. Yang LH, Rudolf VHW (2010) Phenology, ontogeny and the effects of climate change on the timing of species interactions. Ecol Lett 13:1–10PubMedGoogle Scholar
  185. Ye HC (2008) Changes in frequency of precipitation types associated with surface air temperature over northern Eurasia during 1936–90. J Clim 21:5807–5819Google Scholar
  186. Zhang T, Barry RG, Knowles K, Heginbottom JA, Brown J (1999) Statistics and characteristics of permafrost and ground ice distribution in the northern hemisphere. Polar Geogr 23:147–169Google Scholar

Copyright information

© The Ecological Society of Japan 2013

Authors and Affiliations

  • Kobayashi Makoto
    • 1
    • 8
  • Takuya Kajimoto
    • 2
  • Lina Koyama
    • 3
  • Gaku Kudo
    • 4
  • Hideaki Shibata
    • 5
  • Yosuke Yanai
    • 6
  • J. H. C. Cornelissen
    • 7
  1. 1.Graduate School of Environment and Information SciencesYokohama National UniversityYokohamaJapan
  2. 2.Forestry and Forest Products Research InstituteTsukubaJapan
  3. 3.Graduate School of InformaticsKyoto UniversityKyotoJapan
  4. 4.Faculty of Environmental Earth ScienceHokkaido UniversitySapporoJapan
  5. 5.Field Science Center for Northern BiosphereHokkaido UniversitySapporoJapan
  6. 6.NARO Institute of Vegetable and Tea ScienceTsukubaJapan
  7. 7.System Ecology, Department of Ecological Science, Faculty of Earth and Life SciencesVU University AmsterdamAmsterdamThe Netherlands
  8. 8.Nakagawa Experimental Forest, Field Science Center for Northern BiosphereHokkaido UniversityOtoineppuJapan

Personalised recommendations