The interaction between freezing tolerance and phenology in temperate deciduous trees

Abstract

Temperate climates are defined by distinct temperature seasonality with large and often unpredictable weather during any of the four seasons. To thrive in such climates, trees have to withstand a cold winter and the stochastic occurrence of freeze events during any time of the year. The physiological mechanisms trees adopt to escape, avoid, and tolerate freezing temperatures include a cold acclimation in autumn, a dormancy period during winter (leafless in deciduous trees), and the maintenance of a certain freezing tolerance during dehardening in early spring. The change from one phase to the next is mediated by complex interactions between temperature and photoperiod. This review aims at providing an overview of the interplay between phenology of leaves and species-specific freezing resistance. First, we address the long-term evolutionary responses that enabled temperate trees to tolerate certain low temperature extremes. We provide evidence that short term acclimation of freezing resistance plays a crucial role both in dormant and active buds, including re-acclimation to cold conditions following warm spells. This ability declines to almost zero during leaf emergence. Second, we show that the risk that native temperate trees encounter freeze injuries is low and is confined to spring and underline that this risk might be altered by climate warming depending on species-specific phenological responses to environmental cues.

Keywords: biogeographical limits; cold acclimation; freezing resistance; fundamental niche; leaf-out; phenology; plant–climate interactions; temperate trees.

FIGURE 1

Distribution range of Fagus sylvatica along with climatic characteristics at the northern and southern edge of the distribution and at low versus high elevation in central Europe. Absolute maximum, mean maximum, mean minimum, and absolute minimum temperature for a given day of the year in the period 1901–2000 are shown. The selected stations were Toulouse (France, 43.6°N 1.4°E, 151 m a.s.l) in the West, Nordby (Denmark, 55.5°N 8.4°E, 4 m a.s.l) in the North, Baia Mare (Romania, 47.7°N, 23.5°E, 216 m a.s.l) in the East, Binningen (Switzerland, 47.5°N 7.6°E, 316 m a.s.l) at low elevation, and Davos (Switzerland, 46.8°N 9.8°E, 1594 m a.s.l) at high elevation.

FIGURE 2

Daily variation of minimum air temperature at five extreme locations within the distribution of Fagus sylvatica (see Figure 1 for the location of the sites) for a same date among the five locations (A, spatial scale), and within a site for the same day of the year across years from 1900 to 2010 (B, temporal scale). Note that the extent of temperature variation within a site for a given day exceed the maximum variation of temperature that occurs at a given date between the two extreme locations of the distribution area of the species.

FIGURE 3

Marsham phenological records (Sparks and Carey, 1995). The upper panel shows the frequency of distribution of the leaf-out dates in Norfolk (UK) for eight temperate tree species over the period 1736–1958 (between 158 and 178 years available, depending on species). The distribution was fitted by a Gaussian–Kernel density distribution with a bandwidth of 7 days for each species. The box-plots show median, quartiles, and extremes of the phenological data, with the mean given as filled circle. Species names followed by an asterisk indicate that this is the probable species but we are uncertain.