Cold-induced photoinhibition limits regeneration of snow gum at tree-line

Cold-induced photoinhibition was studied in relation to the distribution of juvenile Eucalyptus pauciflora Sieb. ex. Spreng near the low temperature limits of its distribution in southeastern Australia. In early autumn, there were no differences in the photosynthetic properties of leaves from juvenile plants naturally growing in canopy-shaded or fully exposed sites, with all leaves having photosynthetic characteristics typical of leaves from high light environments. In mid-winter, cold-induced photoinhibition, as indicated by loss of quantum yield, increased with increase in exposure to high irradiances, with quantum yield in the most exposed leaves averaging 51% less than that expected in fully functional leaves of C3 species. However, decrease in photosynthetic efficiency at limiting photon flux densities was not accompanied by a parallel decrease in photosynthetic capacity at higher light intensities. This implies that cold-induced photoinhibition in E. pauciflora was due to protective dissipation of absorbed light energy rather than damage to photosystem II. The density of juveniles was highest in canopy-shaded sites on the eastern to south-western sides of trees where juveniles received intermittent high intensity irradiance from sunflecks but were protected from prolonged exposure to bright sunlight, particularly in winter when solar angle is low and the sun follows a more northerly path. Thus, the distribution of juvenile plants was correlated with the occurrence and severity of cold-induced photoinhibition. Key-words: Cold-induced photoinhibition, Eucalyptus pauciflora, quantum yield, regeneration niche, stress tolerance Introduction In ecological studies, light is regarded as a resource, but it can also be a major source of stress. Environmental stresses, such as low temperatures (Greer, Berry & Bjbrkman, 1986), are well known to induce light-dependent loss in photosystem II activity, which is manifest in intact leaves as a loss in photosynthetic capacity under limiting photon flux densities (Osmond, 1981). Such photoinhibition results from direct damage to photosystem II reaction centres (Kyle, 1987) and/or increased dissipation of absorbed light by protective quenching mechanisms (Krause & Behrend, 1986; Demmig & Bjdrkman, 1987; Weis & Berry, 1987). In either case, some of the absorbed quanta become ineffective in driving electron transfer from photosystem II to the plastoquinone pool, thereby decreasing quantum yield (i.e. mol oxygen evolved per mol quanta absorbed). Cold-induced photoinhibition naturally occurs in northern coniferous forests (Oquist, 1983; Leverenz & Oquist, 1987), but the ecological significance of such photoinhibition is unknown (Oquist, Greer & Ogren, 1987). Loss of quantum yield should affect the carbon balance of a leaf because leaves generally experience photon flux densities which are limiting to photosynthesis. Indeed cold-induced photoinhibition has been associated with reduced productivity of tea (Aoki, 1986) and rape (Baker et al., 1989) during winter. It follows from physiological studies that species should be most vulnerable to photoinhibition near their limits of tolerance to environmental variables such as low temperatures, and that seedlings should be more vulnerable than established plants to reductions in carbon gain associated with chronic photoinhibition. Thus, cold-induced photoinhibition may play a role in limiting regeneration, and hence also distribution, of species along climatic gradients and at timberlines. This study considers cold-induced photoinhibition as a factor limiting regeneration of the snow gum, Eucalyptus pauciflora Sieb. ex. Spreng, near the low temperature limits of its distribution. This evergreen, broad-leaved species is found over a This content downloaded from 157.55.39.203 on Sat, 27 Aug 2016 04:26:10 UTC All use subject to http://about.jstor.org/terms 664 wide elevational range from sea level up to 1900 m M. C. Ball et in south-eastern Australia, with the highest probal. ability of occurrence being in areas of high rainfall .(>1400mm) where the mean annual temperature ranges from 5 to 80C (Austin, Nicholls & Margules, 1990). These conditions, in which E. pauciflora is typically the dominant canopy species, occur up to the alpine tree-line as well as at lower elevations around valley floors receiving cold air drainage. Above the snow-line, seedlings are buffered from extremes of temperature by an insulating layer of snow. Below the snow-line, seedlings exposed to radiative frost on clear winter nights experience extremely low night temperatures which could cause cellular damage, predisposing leaves to photoinhibition in the succeeding photoperiod (Oquist, 1987). However, such damage is not a prerequisite for photoinhibition which can occur even at relatively low photon flux densities if the orderly dissipation of absorbed light energy is disrupted by low leaf temperatures (Oquist, 1987). In either case, leaves would be most susceptible to photoinhibition shortly after dawn, when exposure to the combination of low leaf temperatures and high photon flux densities could occur. The duration of such conditions would be brief as alpine leaf temperatures rise rapidly with exposure to solar radiation (K6rner & Larcher, 1988). However, once leaves become photoinhibited, prolonged exposure to high photon flux densities could have devastating consequences for chloroplast metabolism, resulting in irreversible damage and cell death. If cold-induced photoinhibition does influence regeneration by the snow gum, then responses should be evident in at least two levels of functioning. Firstly, quantum yield of individual leaves should decline in winter with the severity of decrease dependent on exposure to irradiance. Secondly, the distribution of juveniles should be consistent with minimizing exposure during winter to both extreme low temperatures and prolonged high irradiance. Materials and methods Seasonal variation in photosynthetic responses to light was studied in relation to microclimate and distribution of juvenile E. pauciflora in the Orroral Valley (elevation 950m ASL), Australian Capital Territory, Australia (latitude 350 37'S, longitude 1480 57 'E). Juvenile E. pauciflora of similar height were selected for study from the naturally occurring pool of individuals which were either fully exposed or shaded by tree canopies. Two additional treatments were imposed on the exposed juveniles. One set was protected from direct, early morning sunlight by vertical screens of shade cloth transmitting 30% incident sunlight. Another set was fully covered with shade cloth such that the maximum light intensity received by the foliage would not exceed 30% incident sunlight throughout the day. Thus, there were four treatments hereafter referred to as exposed, canopy shaded, vertical screen and covered. There were three replicates per treatment, with a replicate plant for each treatment associated with each of three large trees. Monitoring of leaf temperatures during winter with 0 2 mm diameter precision bead thermisters referenced against a platinum resistance thermometer showed that minimum leaf temperatures varied less than 2 C between all treatments. Leaves under natural canopy shade were warmest, with leaf temperatures progressively decreasing in covered, vertical screen and exposed treatments. On one clear night of measurement, pre-dawn leaf temperature (5 min moving average of three leaves) under natural canopy shade was -8 2 C when air temperature was -8 3 C, whereas the temperature of exposed leaves was -10 C when air temperature was