ARTICLE IN PRESS Flora 205 (2010) 3–18 Contents lists available at ScienceDirect Flora journal homepage: www.elsevier.de/flora Survival types of high mountain plants under extreme temperatures Walter Larcher Ã, Christine Kainmuller,¨ Johanna Wagner Institut fur¨ Botanik, Universitat¨ Innsbruck, Sternwartestrasse 15, A-6020 Innsbruck, Austria article info abstract Article history: Extreme temperatures are a main factor limiting plant growth in high mountain habitats. During winter, Received 20 September 2008 the risk of frost damage is highest at windblown and often snow-free sites. During summer, actively Accepted 2 December 2008 growing plants are particularly endangered by episodic cold spells, but also by short-term overheating. The current review gives an overview of extreme temperatures in the European Alps and observations of Keywords: temperature damage on plants in their natural habitats. Furthermore, seasonal time courses of frost and Bioclimate temperatures heat resistance derived from laboratory tests on different plant growth forms are presented. Study Frost resistance species were the cushion plants Silene acaulis, Minuartia sedoides, Saxifraga oppositifolia and Carex firma Heat resistance collected on wind-exposed ridges; the rosette plant Soldanella alpina collected on snow-protected sites, Cross-tolerance and three Sempervivum species collected in xerothermic habitats. Adaptation The temperature resistance of leaves, stems, rhizomes and roots were tested in two annual time Winter drought courses. Frost treatments were conducted in controlled freezers by rapid cooling (10 K hÀ1, for current resistance) as well as by stepwise cooling (1–3 K hÀ1, for hardening capacity). Heat treatments followed a standardised procedure by exposing samples to heat for 30 min in hot water baths. The damage was visually estimated using the topographic tetrazolium test. During winter, cushion plants from exposed sites were fully hardened (LT50 below À70 1C). Rosette plants, which are protected by a constant snow cover, survived temperatures of down to À25 1C. During the growing period, foliage and shoot tips of the investigated species were damaged at À5toÀ8 1C (LT50). Stems and rhizomes were only partially damaged by temperatures of À10 to À15 1C. Heat resistance in cushion plants generally reached 56–58 1C(LT50), shoots and rhizomes of C. firma could reach 60 1C. Succulent plants like Sempervivum arachnoideum and S. tectorum from hot and dry microsites were the most heat resistant among the tested species (62–64 1C). The investigated mountain plant species showed highly varying resistance patterns, with variation in maximum hardening capability and seasonal time courses of resistance. Plants were capable of rapid adjustments to extreme temperatures, which is crucial for survival in a high mountain climate. & 2009 Elsevier GmbH. All rights reserved. Introduction snow-free sites, however, plants must be fully frost resistant to survive temperatures of down to À30 1C and lower (e.g. Franz, Among the various environmental factors in the mountains, 1979). In summer in the alpine zone, rosette and cushion plants in the climate operates as an altitudinal selection filter and adapta- wind-protected niches bear the greatest risk of overheating, tion force (Larcher, 1980). Above the timberline, air temperatures particularly if solar radiation is high and precipitation low and microclimate temperatures become more extreme and thus (Buchner and Neuner, 2003; Korner,¨ 2003; Larcher and Wagner, limiting. Therefore, only specialised mountain plants can survive 1976). in these high altitudes. During the main growing period, high Frost and heat resistance of herbaceous mountain plants at mountain plants are particularly threatened by temperature mid and higher latitudes have been the subject of a number of constraints such as frosts caused by cold spells but also short- studies. Most data stem from the European Alps (e.g. Buchner and term overheating. During winter, the risk of frost damage is Neuner, 2003; Kainmuller,¨ 1975; Larcher and Wagner, 1976, 1983; relatively low for prostrate plants that are permanently covered Neuner et al., 1999, 2000; Pisek et al., 1967, 1968; Taschler and with snow at constant temperatures of between 0 and À5 1C Neuner, 2004; Ulmer, 1937), with some additional data from (e.g. Aulitzky, 1961; Aulitzky et al., 1982). On windblown and often mountains of Scandinavia (Gauslaa, 1984; Junttila and Robberecht, 1993; Robberecht and Junttila, 1992), and the temperate moun- tains on other continents (Bannister et al., 2005; Marchand et al. Ã Corresponding author. 2006; Mooney and Billings,1961; Sakai and Otsuka, 1970). Most E-mail address: [email protected] (W. Larcher). investigations concerned frost or heat resistance of leaves and 0367-2530/$ - see front matter & 2009 Elsevier GmbH. All rights reserved. doi:10.1016/j.flora.2008.12.005 ARTICLE IN PRESS 4 W. Larcher et al. / Flora 205 (2010) 3–18 shoots during the growing season. Less information is available À4 1C in July and August whereas at the height of summer (July, about temperature resistance during winter (Junttila and August) frosts of about À7 1C occur in the subnival zone and À8to Robberecht, 1993; Sakai and Otsuka, 1970), and hardly anything À10 1C in glacial regions. is known about resistance changes in the course of a year In high mountain regions, considerable temperature differ- (Bannister et al., 2005; Kainmuller,¨ 1975). Similarly rare are ences can be measured between the free atmosphere and the reports about the temperature resistance of belowground organs boundary layer climate. This is exemplified by two annual (Kainmuller,¨ 1975; Sakai and Otsuka, 1970). boundary layer temperature curves from microsites in an upper We investigated species of different growth forms from various alpine zone (Mt Hafelekar; Fig. 1) and a subnival region (Stubai habitats including cushion plants growing on rocky locations, Glacier; Fig. 2). Plant temperatures were recorded at hourly rosette plants needing constant snow cover as well as species intervals using small data loggers of 3 cm diameter and 1.2 cm growing in xerothermic mountain habitats. The current resis- height with a NTC-pearl sensor (‘‘StowAway Tidbit’’, Onset tance, the maximum resistance (by hardening) and the minimum Computer Corp. Pocasset, MA, USA). On the sites with open resistance (by dehardening) of vegetative aboveground and vegetation, loggers were placed in plant cushions so that the belowground organs were determined in the course of a year. In sensors were shaded by leaves. Temperature databases also some cases some insight could be gained from the synergism indicated the duration of snow cover at the different sites. between frost resistance and heat tolerance through winter In winter, prostrate plants are mostly covered with snow. drought. The data mostly stem from investigations carried out Beneath a layer of snow thicker than 50 cm the temperature in between 1970 and 1980, which have not yet been published or at winter seldom sinks below À5 1C in intermediate latitudes least not in full. (Aulitzky et al., 1982; Sakai and Larcher, 1987). At sheltered This publication should bridge the information gap on whole microsites in the alpine zone, plants can survive temperatures plant resistance of herbaceous high mountain plants and their between 0 and À3 1C until the end of May. Under a thin snow seasonal resistance dynamics. This capability of adjusting to cover and on windy ridges plants, particularly pioneer plants, have seasonally changing temperatures determines a species’ persever- to endure air temperatures; this means that on the western slope ance in stressful habitats and shows species-specific limits, of Mt Hafelekar, where Silene acaulis and Saxifraga oppositifolia which can arise as a result of changes in climate. Current pro- grow, the temperatures range from À8toÀ14 1C due to strong jects dealing with susceptibility to extreme temperatures of snow-drift in winter. Also the study site on the Stubai Glacier is flower buds, open flowers, developing and germinating seeds, very much exposed to wind, which is why cushion plants and survival of seedlings in open habitats – will give further (e.g. Saxifraga bryoides) frequently grow there. Microclimate information about reproductive fitness under extreme tempera- temperatures as low as À20 to À22 1C have been measured there. tures and thus a species’ capability of maintaining population After the thawing period and during the growing season there turnover and colonising new habitats. are repeated frosts in the sparse vegetation and on the soil surface. In midsummer (July and August) about 20 frost days (between À2 and À3 1C) were recorded in the subnival ecotone Extreme temperatures in high mountain regions and about 50 frost days (down to À5 1C) on a nival summit. Clear nights can induce particularly low temperatures in the morning In the Alps the absolute lowest air temperatures ever due to thermal re-radiation. measured in standard weather stations were À36 to À37 1C High microclimate temperatures in mountain regions are (Cappel, 1977; Steinhauser, 1954; Swiss Institute for Meteorology, brought about by intensive incoming radiation, shelter from the 1930). These temperatures are of course exceptional. Most of the wind and dry superficial soil on southern and south-western absolute minimum air temperatures of the free atmosphere in inclinations. During summer, prostrate plants of the alpine zone winter range from À17 to À24 1C in the alpine