Oecologia

, Volume 163, Issue 1, pp 267–276 | Cite as

Summer freezing resistance decreased in high-elevation plants exposed to experimental warming in the central Chilean Andes

Global change ecology - Original Paper

Abstract

Alpine habitats have been proposed as particularly sensitive to climate change. Shorter snow cover could expose high-elevation plants to very low temperatures, increasing their risk of suffering damage by freezing, hence decreasing their population viability. In addition, a longer and warmer growing season could affect the hardening process on these species. Thus, understanding the ability of these species to withstand freezing events under warmer conditions is essential for predicting how alpine species may respond to future climate changes. Here we assessed the freezing resistance of 11 species from the central Chilean Andes by determining their low temperature damage (LT50) and freezing point (FP) after experimental warming in the field. Plants were exposed during two growing seasons to a passive increase in the air temperature using open top chambers (OTCs). OTCs increased by ca. 3 K the mean air and soil daytime temperatures, but had smaller effects on freezing temperatures. Leaf temperature of the different species was on average 5.5 K warmer inside OTCs at midday. While LT50 of control plants ranged from −9.9 to −22.4, that of warmed plants ranged from −7.4 to −17.3°C. Overall, high-Andean species growing inside OTCs increased their LT50 ca. 4 K, indicating that warming decreased their ability to survive severe freezing events. Moreover, plants inside OTCs increased the FP ca. 2 K in some studied species, indicating that warming altered processes of ice crystal formation. Resistance of very low temperatures is a key feature of high-elevation species; our results suggest that current climate warming trends will seriously threaten the survival of high-elevation plants by decreasing their ability to withstand severe freezing events.

Keywords

Alpine Climate change Freezing temperatures Frost damage Open top chambers 

References

  1. Anisko T, Lindstrom OM (1996) Cold hardiness and water relations parameters in Rhododendron cv Catawbiense Boursault subjected to drought episodes. Physiol Plant 98:147–155CrossRefGoogle Scholar
  2. Arft AM, Walker MD, Gurevitch J, Alatalo JM, Bret-Harte MS, Dale M, Diemer M, Gugerli F, Henry GHR, Jones MH, Hollister RD, Jonsdottir IS, Laine K, Levesque E, Marion GM, Molau U, Molgaard P, Nordenhall U, Raszhivin V, Robinson CH, Starr G, Stenstrom A, Stenstrom M, Totland O, Turner PL, Walker LJ, Webber PJ, Welker JM, Wookey PA (1999) Responses of tundra plants to experimental warming: meta-analysis of the international tundra experiment. Ecol Monogr 69:491–511Google Scholar
  3. Bannister P, Colhoun CM, Jameson PE (1995) The winter hardening and foliar frost resistance of some New Zealand species of Pittosporum. NZ J Bot 33:409–414Google Scholar
  4. Bannister P, Maegli T, Dickinson K, Halloy S, Knight A, Lord J, Mark A, Spencer K (2005) Will loss of snow cover during climatic warming expose New Zealand alpine plants to increased frost damage? Oecologia 144:245–256CrossRefPubMedGoogle Scholar
  5. Barker DH, Loveys BR, Egerton JJG, Gorton H, Williams WE, Ball MC (2005) CO2 enrichment predisposes foliage of eucalypt to freezing injury and reduces spring growth. Plant Cell Environ 28:1506–1515CrossRefGoogle Scholar
  6. Beck EH, Heim R, Hansen J (2004) Plant resistance to cold stress: mechanisms and environmental signals triggering frost hardening and dehardening. J Biosci 29:449–459CrossRefPubMedGoogle Scholar
  7. Beeling DJ, Terry AC, Mitchell PL, Callaghan TV, Gwynn-Jones D, Lee JA (2001) Time to chill: effects of simulated global change on leaf ice nucleation temperatures of subarctic vegetation. Am J Bot 88:628–633CrossRefGoogle Scholar
  8. Bertrand A, Castonguay Y (2001) Plant adaptations to overwintering stresses and implications of climate change. Can J Bot 81:1145–1152CrossRefGoogle Scholar
  9. Björk RG, Molau U (2007) Ecology of alpine snowbeds and the impact of global change. Arct Antarct Alp Res 39:34–43CrossRefGoogle Scholar
  10. Cannone N, Sgorbati S, Guglielmin M (2007) Unexpected impacts of climate change on alpine vegetation. Front Ecol Environ 5:360–364CrossRefGoogle Scholar
  11. Cavieres LA, Peñaloza A, Arroyo MTK (2000) Altitudinal vegetation belts in the high-Andes of central Chile (33°S). Rev Chil Hist Nat 73:331–344CrossRefGoogle Scholar
  12. Cavieres LA, Badano EI, Sierra-Almeida A, Gómez-González S, Molina-Montenegro MA (2006) Positive interactions between alpine plants species and the nurse cushion plant Laretia acaulis do not increase with elevation in the Andes of central Chile. New Phytol 169:59–69CrossRefPubMedGoogle Scholar
  13. Cavieres LA, Badano EI, Sierra-Almeida A, Molina-Montenegro MA (2007) Microclimatic modifications of cushion plants and their consequences for seedling survival of native and non-native herbaceous species in the high Andes of central Chile. Arct Antarct Alp Res 39:229–236CrossRefGoogle Scholar
  14. Chen PM, Li PH, Burke MJ (1977) Induction of frost hardiness in stem cortical tissues of Cornus stolonifera Michx. by water stress. Plant Physiol 59:236–239CrossRefPubMedGoogle Scholar
  15. CONAMA (2006) Estudio de la variabilidad climática en Chile para el siglo XXI. Informe final. Departamento de Geofísica, Facultad de Ciencias Físicas y Matemáticas, Universidad de Chile, SantiagoGoogle Scholar
  16. Danby RK, Hik DS (2007) Responses of white spruce (Picea glauca) to experimental warming at a subarctic alpine treeline. Glob Chang Biol 13:437–451CrossRefGoogle Scholar
  17. Dirnböck T, Dullinger S, Grabherr G (2003) A regional impact assessment of climate and land-use change on alpine vegetation. J Biogeogr 30:401–417Google Scholar
  18. Dytham C (2003) Choosing and using statistics: a biologist’s guide, 2nd edn. Blackwell, OxfordGoogle Scholar
  19. Easterling DR, Meehl GA, Parmesan C, Changnon SA, Karl TR (2000) Climate extremes: observations, modeling, and impacts. Science 289:2068CrossRefPubMedGoogle Scholar
  20. Goldstein G, Rada F, Azócar A (1985) Cold hardiness and supercooling along an altitudinal gradient in Andean giant rosette species. Oecologia 68:147–152CrossRefGoogle Scholar
  21. Gottfried M, Pauli H, Reiter K, Grabherr G (2002) Potential effects of climate change on alpine and nival plants in the Alps. In: Körner C, Spehn E (eds) Mountain biodiversity, a global assessment. Parthenon, Boca Raton, pp 213–223Google Scholar
  22. Guisan A, Theurillat JP (2000) Assessing alpine plant vulnerability to climate change: a modeling perspective. Integr Assess 1:307–320CrossRefGoogle Scholar
  23. Henry GHR, Molau U (1997) Tundra plants and climate change: the International Tundra Experiment (ITEX). Glob Chang Biol 3:1–3CrossRefGoogle Scholar
  24. Hollister RD, Webber PJ, Tweedie CE (2005) The response of Alaskan arctic tundra to experimental warming: differences between short- and long-term responses. Glob Chang Biol 11:525–536CrossRefGoogle Scholar
  25. Inouye DW (2000) The ecological and evolutionary significance of frost in the context of climate change. Ecol Lett 3:457–463CrossRefGoogle Scholar
  26. Inouye DW (2008) Effects of climate change on phenology, frost damage, and floral abundance of montane wildflowers. Ecology 89:353–362CrossRefPubMedGoogle Scholar
  27. IPCC (2007) Climate Change 2007. In: Pachauri RK, Resinger A (eds) The AR4 synthesis report of the Working Group I of the International Panel on Climate Change. IPCC, GenevaGoogle Scholar
  28. Klein JA, Harte J, Zhao XQ (2004) Experimental warming causes large and rapid species loss, dampened by simulated grazing, on the Tibetan Plateau. Ecol Lett 7:1170–1179CrossRefGoogle Scholar
  29. Körner C (2000) The alpine zone under global change. Gayana Bot 57:1–17CrossRefGoogle Scholar
  30. Körner C (2003) Alpine plant life, 2nd edn. Springer, BerlinGoogle Scholar
  31. Kudernatsch T, Fischer A, Bernhardt-Römermann M, Abs C (2008) Short-term effects of temperature enhancement on growth and reproduction of alpine grassland species. Basic Appl Ecol 9:263–274CrossRefGoogle Scholar
  32. Kudo G, Suzuki S (2003) Warming effects on growth, production, and vegetation structure of alpine shrubs: a five-year experiment in northern Japan. Oecologia 135:280–287PubMedGoogle Scholar
  33. Larcher W (2000) Temperature stress and survival ability of Mediterranean sclerophyllous plants. Plant Biosys 134:279–295CrossRefGoogle Scholar
  34. Larcher W (2003) Physiological plant ecology: ecophysiology and stress physiology of functional group, 4th edn. Springer, BerlinGoogle Scholar
  35. Loik ME, Still J, Huxman TE, Harte J (2004) In situ photosynthetic freezing tolerance for plants exposed to a global warming manipulation in the Rocky Mountains, Colorado, USA. New Phytol 162:331–341CrossRefGoogle Scholar
  36. Loveys BR, Egerton JJG, Ball MC (2006) Higher daytime leaf temperatures contribute to lower freeze tolerance under elevated CO2. Plant Cell Environ 29:1077–1086CrossRefPubMedGoogle Scholar
  37. Lutze JL, Roden JS, Holly CJ, Wolfe J, Egerton JJG, Ball MC (1998) Elevated atmospheric [CO2] promotes frost damage in evergreen tree seedlings. Plant Cell Environ 21:631–635CrossRefGoogle Scholar
  38. Marchand FL, Kockelbergh F, van de Vijver B, Beyens L, Nijs I (2006) Are heat and cold resistance of arctic species affected by successive extreme temperature events? New Phytol 170:291–300CrossRefPubMedGoogle Scholar
  39. Marion GM, Henry GHR, Freckman DW, Johnstone J, Jones G, Jones MH, Le′vesque E, Molau U, Molgaard P, Parsons AN, Svoboda J, Virginia RA (1997) Open-top designs for manipulating field temperature in high-latitude ecosystems. Glob Chang Biol 3:20–32CrossRefGoogle Scholar
  40. Matthei O (1995) Manual de las malezas que crecen en Chile. Alfabeta Impresores, SantiagoGoogle Scholar
  41. Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668CrossRefPubMedGoogle Scholar
  42. Menzel A, Fabian P (1999) Growing season extended in Europe. Nature 397:659CrossRefGoogle Scholar
  43. Molina-Montenegro MA, Briones R, Cavieres LA (2009) Does global warming induce segregation among alien and native beetle species in a mountain-top? Ecol Res 24:31–36CrossRefGoogle Scholar
  44. Neuner G, Buchner O (1999) Assessment of foliar frost damage: a comparison of in vivo chlorophyll fluorescence with other viability tests. J Appl Bot 73:50–54Google Scholar
  45. Neuner G, Ambach D, Aichner K (1999) Impact of snow cover on photoinhibition and winter desiccation in evergreen Rhodondendron ferrugineun leaves during subalpine winter. Tree Physiol 19:725–732PubMedGoogle Scholar
  46. Repo T, Hänninen H, Kellomäki S (1996) The effects of long-term elevation of air temperature and CO2 on the frost hardiness of Scots pine. Plant Cell Environ 19:209–216CrossRefGoogle Scholar
  47. Sakai A, Larcher W (1987) Frost survival of plants: responses and adaptation to freezing stress. Springer, BerlinGoogle Scholar
  48. Sakai A, Ötsuka K (1970) Freezing resistance of alpine plants. Ecology 54:665–671CrossRefGoogle Scholar
  49. Sierra-Almeida A, Cavieres LA, Bravo LA (2009) Freezing resistance varies within the growing season and with the elevation in high-Andean species of central Chile. New Phytol 182:461–469CrossRefPubMedGoogle Scholar
  50. Squeo FA, Rada F, García C, Ponce M, Rojas A, Azócar A (1996) Cold resistance mechanisms in high desert Andean plants. Oecologia 105:552–555CrossRefGoogle Scholar
  51. Takahashi K (2005) Effects of artificial warming on shoot elongation of alpine dwarf pine (Pinus pumila) on Mount Shogigashira, Central Japan. Arct Antarct Alp Res 37:620–625CrossRefGoogle Scholar
  52. Taschler D, Neuner G (2004) Summer frost resistance and freezing patterns measured in situ in leaves of major alpine growth forms in relation to their upper distribution boundary. Plant Cell Environ 27:737–746CrossRefGoogle Scholar
  53. Wilson S, Nilsson C (2009) Arctic alpine vegetation change over 20 years. Glob Chang Biol 15:1676–1684CrossRefGoogle Scholar
  54. Woldendorp G, Hill MJ, Doran R, Ball MC (2008) Frost in a future climate: modelling interactive effects of warmer temperatures and rising atmospheric [CO2] on the incidence and severity of frost damage in a temperate evergreen (Eucalyptus pauciflora). Glob Chang Biol 14:294–308CrossRefGoogle Scholar
  55. Woodward FI (1987) Climate and plant distribution. Cambridge University Press, CambridgeGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Angela Sierra-Almeida
    • 1
    • 2
  • Lohengrin A. Cavieres
    • 1
    • 2
  1. 1.ECOBIOSIS, Departamento de Botánica, Facultad de Ciencias Naturales y OceanográficasUniversidad de ConcepciónConcepciónChile
  2. 2.Instituto de Ecología y Biodiversidad (IEB)SantiagoChile

Personalised recommendations