- Top of page
- Materials and Methods
- Supporting Information
Among the abiotic factors that control the global distribution of taxa, freezing temperatures are possibly the most decisive. For plants, this selective filter varies with life stage, tissue type and, most importantly, seasonal development (Sakai & Larcher, 1987). In temperate climates, deciduous trees have adopted a strategy to escape winter freezing damage to foliage by shedding their leaves in autumn. However, deciduous trees must exhibit freezing tolerance in all other overwintering organs, particularly in buds, because they contain pre-formed leaves and flowers for the following growing season. Freezing damage is ultimately linked to the rupture of biomembranes (Ziegler & Kandler, 1980; Sung et al., 2003; see review by Larcher, 2005). Therefore, a major part of freezing resistance is to maintain membrane fluidity during the freezing process and to tolerate freezing-induced dehydration in the cell plasma. To do so, plants synthesize dehydrins and antifreeze proteins and reduce the amount of membrane-located carriers and receptors during the pre-hardening stage in late autumn. Next, plants change the ultrastructure of the cytoplasm and increase the proline and polyol concentration during the early stage of hardening. The final stage of hardening is reached by a repeated exposure to freezing temperatures during dormancy in winter, leading to the species-specific maximum freezing resistance. In early spring, before bud burst, freezing resistance decreases progressively as temperature rises (dehardening period), reaching a minimum when the new leaves emerge (Till, 1956; Weiser, 1970). Once development starts in spring, freezing resistance is irreversibly lost and plants cannot re-acclimate to low temperatures (Sakai & Larcher, 1987; Repo, 1991; Rapacz, 2002). During the maturation of the new leaves, the freezing resistance of foliage increases slightly by 2–3 K; the maximum freezing resistance of active leaves is reached by mid-summer (Till, 1956). By the end of summer, after budset, freezing resistance begins to increase again (hardening period) in response to the shortening photoperiod and decreasing temperature (Weiser, 1970; Christersson, 1978; Larcher, 2005). The freezing resistance of deciduous trees is therefore tightly linked to their phenology, especially the state of bud dormancy (Larcher & Mair, 1968; Weiser, 1970; Campbell & Sorensen, 1973; Ibanez et al., 2010).
Past attempts to explain species range limits have largely adopted a correlative approach, looking for correlations between species boundaries and some presumably important isotherms (e.g. Iversen, 1944; Woodward, 1987). Until now, it has remained unclear which facet of the temperature regime is critical and at which time of the year or developmental stage this critical temperature acts in a decisive way. In long-lived organisms, such as trees, freezing resistance controls species persistence over long time scales, with a single extreme event potentially eliminating a species beyond a certain isotherm. The good relationship between the winter freezing resistance of tree species and the minimum annual temperatures at the distribution limits of tree species suggests that winter temperatures control cold distribution limits (e.g. Sakai & Weiser, 1973; Sakai, 1978). However, several studies have suggested that spring freezing events are most important for the distribution limit of deciduous temperate tree species (e.g. Rubner, 1921; see review by Parker, 1963). Trees are particularly vulnerable in spring, when they start to grow and lose their freezing resistance during a period in which freezing events are still likely. Spring freezing events can seriously affect the growth and reproduction of trees at the cold edge of their range through either the loss of new leaves or damage to flowers, subsequently affecting the tree's reproductive success (Inouye, 2000; Augspurger, 2009; Hufkens et al., 2012). The loss of a first cohort of leaves and the need for a new cohort may delay seasonal xylogenesis and can lead to a significant reduction in annual ring width (Dittmar et al., 2006).
Earlier spring phenology as a result of climate warming has been observed for > 400 plant species in Europe (Menzel et al., 2006), as well as for many tree species in Europe and America (reviewed in Bertin, 2008). Earlier spring phenology and subsequently earlier dehardening of tree tissues can possibly lead to a higher risk of freezing damage (Cannell & Smith, 1986; Gu et al., 2008), particularly for early flushing species. However, warming affects phenology only after trees have received sufficient periods of chilling winter temperatures, and some tree species employ photoperiodic controls of phenology as a safeguard against warm spells at the ‘wrong time’ (Cannell, 1997; Körner & Basler, 2010; Basler & Körner, 2012). Thus, dormancy release is co-controlled by several factors, with temperature controlling the last step. In spite of this co-control of dormancy release, a freezing event in spring damaged both crops and tree species in the eastern part of the USA in 2007 as a result of an exceptionally warm early spring that caused a very early bud burst (Gu et al., 2008; Augspurger, 2009). In most regions, freezing events in spring are generally more severe at higher elevations because of the decline in temperature as elevation increases. However, because the beginning of the growing season is also delayed at higher elevations, it remains unclear whether tree populations growing close to their upper elevational limits are at greater risk of freezing damage than those inhabiting lower elevations.
In this study, we investigated the freezing resistance of buds and leaves before, during and after the period of leaf emergence in eight major European deciduous broadleaved tree species at their upper elevational limits in the Swiss Alps. The high sampling resolution allowed us to assess freezing resistance according to the development of buds in spring. Because freezing resistance in spring is physiologically linked to phenology (e.g. Larcher & Mair, 1968; Campbell & Sorensen, 1973; Ibanez et al., 2010), we reconstructed the spring phenology of these species over the last eight decades via a thermal sum model. This allowed us to link freezing resistance with long-term minimum temperature data along elevational gradients. We addressed the following questions. What is the seasonal variation in the freezing resistance of deciduous broadleaved trees at their elevational limit? Does the difference between the minimum temperature experienced and the freezing resistance of a certain species, that is the temperature safety margin against freezing damage, approach a critical level at the tree species limit? The results of this study permit a better understanding of the decisive controls of low temperature on species range limits.
- Top of page
- Materials and Methods
- Supporting Information
Our study demonstrated that deciduous broadleaved trees of temperate regions are prone to freezing damage during winter and spring, but are mostly safe during summer. However, late spring freezing events have a higher probability of damaging tree species than freezing events during winter. As a result of the high sampling resolution, we could measure directly the freezing resistance of the investigated tree species at defined phenological stages, which allowed us to compare freezing resistance with long-term temperature records during the flushing period in spring. Interestingly, as a result of the phenological shift in response to a decrease in temperature, we did not find an increase in potentially damaging freezing events with increasing elevation during the flushing period. By contrast, our results show, for the first time, that temperate deciduous tree species experience similar risks of freezing damage along an elevational gradient from 600 m up to the species-specific maximum elevational limits, and exhibit a mean safety margin against freezing damage of 5–8.5 K (Fig. 4). This similar mean safety margin against freezing damage across elevations suggests a probabilistic linkage between leaf-out phenology, the course of spring freezing resistance and the regional likelihood of occurrence of a critical freezing temperature (Leinonen, 1996; Cannell, 1997). The results underline that tree phenology has evolved in such a way that trees face similar risks of freezing damage in spring under various climatic conditions. The analysis also reveals that damaging events mostly occur with a recurrence rate of 8–16 yr depending on species. However, this frequency of potentially damaging freezing events does not reveal the severity of damage per se. Freezing events only slightly below the LT50 of leaf primodia or leaves are certainly less severe than strong frosts well below the LT50. Strong freeze events might also damage meristematic tissue, wood parenchyma and phloem, which generally have LT50 values several K below that of leaves, and consequently lead to severe damage of the entire tree (Sakai & Larcher, 1987; Augspurger, 2011).
Freezing resistance from full dormancy to full activity
Overall, observed maximum freezing resistance values during winter are in line with those of previous studies on other temperate deciduous tree species (Till, 1956; Sakai & Weiser, 1973; Sakai, 1978). For the dehardening period, only few freezing resistance data are available, and data of high temporal resolution are particularly scarce (Till, 1956; Tranquillini & Plank, 1989). Our assessment of freezing resistance on a weekly basis permitted the assessment of freezing resistance during defined developmental stages in spring. To our knowledge, this assessment has only been performed once previously, by Taschler et al. (2004). Those authors studied three conifer species, one dwarf shrub and Sorbus aucuparia at the treeline, but, unfortunately, the freezing resistances during distinct phenological stages were not compared with long-term temperature records to assess the long-term risk of freezing damage in spring in these species. Thus, the present study is the first to provide a long-term risk assessment along a large elevational gradient.
Once metabolic activity is resumed in spring and the development of buds begins, freezing resistance is irreversibly lost (Sakai & Larcher, 1987). Therefore, it is crucial that early flushing species are more freezing resistant than late flushing species in early phenological stages, as was found here. Hence, freezing resistance during the flushing period is not closely related to the elevational limit of tree species, but depends more strongly on the phenological stage of development and the phenological strategy (i.e. early or late flushing species). However, within an individual tree, the timing of flushing, which is known to be highly responsive to temperature, is adjusted to actual environmental conditions rather than the actual freezing resistance during flushing. This adjustment may explain why no difference was reported in freezing resistance in spring among different provenances of various tree species from contrasting latitudes, whereas, in autumn and winter, large differences were found (Flint, 1972; Alexander et al., 1984; Li et al., 2003). Our study therefore adds to the old knowledge that the timing of flushing secures an appropriate ‘escape’ from risk periods, and thus the long-term persistence of deciduous temperate trees at a given location.
Risk of freezing damage during the flushing period
In temperate climates, the beginning of the growing season differs between understorey and canopy trees, with the phenology of the understorey generally earlier by several days or weeks (Vitasse, 2013). Our uncertainty analysis revealed, first, that all investigated uncertainties lie within the error of the model used to calculate the mean safety margin against freezing damage, and, second, that, overall, the pattern of a constant safety margin against freezing damage along elevation does not change substantially if the model is run with slightly earlier or later flushing dates. Obviously, the mean safety margin must increase when a later flushing date is assumed (Fig. S2). Any projection of future risks of freezing damage and species range limits will thus depend on accurate predictions of phenology.
It seems that the spring phenology of deciduous trees has evolved to optimize the timing of bud burst in relation to the probability of spring freezing events (Cannell, 1997). However, trees do not ‘measure’ directly the occurrence of extreme temperatures, but have developed complex mechanisms to adjust the onset of their bud development in spring to the complex interaction of photoperiod and temperature (Körner & Basler, 2010; Polgar & Primack, 2011; Basler & Körner, 2012). The probability of certain means or sums coinciding with certain extremes is a central issue in plant–climate interactions and in the global warming debate. Both an increase and/or decrease in freezing damage in a future climate have been suggested (e.g. Cannell & Smith, 1986; Inouye, 2000).
Trade-off between freezing damage and growing season length
Species range limits are assumed to be driven by a trade-off between growing season length and escape from damaging freezing events (Loehle, 1998; Koehler et al., 2012). The constant temperature safety margin against freezing damage across elevations found here indicates that freezing events are such a strong selective pressure that tree species delay flushing until they are safe from damage caused by freezing temperatures. Vitasse et al. (2013) reported delays in the date of leaf unfolding for the studied tree species of between 2.6 d K−1 (c. 200 m increase in elevation) in Fagus sylvatica and 5.4 d K−1 in Fraxinus excelsior at the seedling life stage. Similar values were found for adults of the same species in the Pyrenees Mountains (Vitasse et al., 2009b). This delay is such that the period available to recover from occasional spring freezing damage before the end of the growing season becomes dramatically shorter at high elevations. This shortened period may explain why common garden experiments generally showed that, in deciduous tree species, populations from high elevation are genetically differentiated from low elevation populations by exhibiting later spring phenology irrespective of actual weather (Vitasse et al., 2009a; a review of the older literature in Körner, 2012; Vitasse et al., 2013). A short growing season restricts fruit ripening and seed maturation in deciduous trees (particularly large-seeded species), potentially shaping northern distribution limits (Chuine & Beaubien, 2001; Morin et al., 2008). This may explain why seed size often decreases with decreasing temperatures (Murray et al., 2004; Moles et al., 2007; Kollas et al., 2012), with fewer seeds sometimes produced at higher latitudes (Moles et al., 2009). In addition to seed maturation, latitudinal tree species distribution has been suggested to be limited by minimum metabolic requirements to fulfil life history traits for different tree species (Morin & Chuine, 2006). Within a recent growth chamber study, we found that deciduous trees developed no late wood and immature leaf buds when treated with short and cold growing seasons typically found at temperate alpine treelines (A. Lenz & G. Hoch, unpublished data). We suggest that tree species differ in their minimum requirement of growing season length that enables them to complete their annual life cycle successfully with respect to species-specific life history traits, for instance, seed-related traits, wood anatomy, bud formation or leaf traits. Thus, species-specific minimum growing season length requirements may be the ultimate range-limiting factor, with thermal conditions during the growing season modulating that requirement in a non-linear fashion (the cooler the conditions, the longer the required minimum growing season).
Risk of freezing damage in winter and summer
The actual freezing resistance in winter depends on the depth of dormancy and shows a high plasticity to actual in situ temperatures (Pisek & Schiessl, 1947; Sakai & Larcher, 1987). We found an increase in maximum freezing resistance during full dormancy with an increase in the elevational limits of species (i.e. species having a higher elevational limit have a higher freezing resistance). Because genetic differentiation in freezing resistance among populations growing at contrasting elevations has been reported, especially in winter (Eiga & Sakai, 1984; see review by Körner, 2012), it is important that we sampled populations growing near their upper elevational limits. The increase in freezing resistance with elevational limit found here was much stronger than the minimum temperature lapse rate along the same elevational gradient. As a result, tree species having the highest elevational limits exhibit freezing resistances that largely exceed actual minimum temperatures in winter. As a result of the high plasticity of freezing resistance to temperature in winter, the freezing resistance values obtained here are most probably too low for species with a low elevational limit and damage is probably overestimated. Thus, winter freezing resistance most probably does not explain the upper elevational limits of temperate deciduous trees. By contrast, freezing resistance in summer shows no correlation with the elevational limits of species. Indeed, the leaves of the examined tree species showed similar freezing resistance between −7 and −4°C during summer, similar to the observations by Taschler & Neuner (2004). Our study demonstrated that, over the past 81 yr, deciduous trees have generally been safe from damaging freezing events during summer at their upper elevational limits.
In conclusion, the risk of freezing damage to the buds or leaves of deciduous tree species is close to zero in summer and rare or zero in winter. By contrast, freezing damage during spring occurs every 7–60 yr (mostly 8–16 yr) depending on species, with a similar mean safety margin against freezing damage in all species at all elevations controlled by species-specific and elevation-specific phenology. Freezing events during flushing appear to be the main selective pressure controlling the timing of flushing in the studied temperate deciduous tree species. However, this tracking of climate by phenology inevitably leads to shorter growing seasons at higher elevations. We therefore suggest that trees have a species-specific minimum requirement for growing season length that is tied to their life history and freezing resistance during flushing, which, in turn, defines the required timing of spring phenology.