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- Materials and Methods
Throughout the lifespan of the plants, cambial cells maintain their ability to divide and, even in 4700-yr-old Pinus longaeva, no evidence has been found of an age-related change in the cambial meristems (Lanner & Connor, 2001; Lanner, 2002). However, older trees, or older parts of the stem, exhibit thinner tree rings than younger trees or younger parts of the stem, resulting in a declining trend of ring-width series across the diameter from pith to bark (Cook et al., 1990; Panyushkina et al., 2003). This long-term growth pattern, typical in all trees, is related to advancing age and, as a result, increasing size (Fritts, 1976). Trees with larger stem diameters show higher numbers of cambial cells around the circumference, and, as a consequence, need fewer cells on the radial files to maintain the required water supply for the crown. Is there a specific age-related timing associated with this changing tree ring width? Compared with younger trees, the thin tree rings of old trees could result from either slower growth rates or shorter growing periods. The question whether the dynamics of intra-annual wood growth, such as timing, duration and rate, changes over a tree's lifespan remains unanswered.
The period when xylem is developing corresponds to the time window during which trees and their wood cells are open to directly receive environmental signals (Frankenstein et al., 2005), resulting in tree rings being an archive of long-term meteorological proxy data (Alley, 2001; Bräker, 2002). Dendrochronology uses these proxies, which originate from the bridging technique of shorter time-series of tree-ring widths. The technique requires rings produced by young plants to be connected and alternate in the chronology with rings produced by old trees (Kaennel & Schweingruber, 1995). These procedures are based on the adoption of James Hutton's uniformitarian principle, which states that the mechanisms linking biological activities in tree rings to environmental conditions remain unaltered over time (Hutton, 1788 in Bräker, 2002; Hughes, 2002). One assumption behind the adoption of Hutton's principle in biology is that no difference in timing and duration of tree-ring formation should occur during the lifespan of a tree, but this has never been proved.
In climate–growth relationships based on tree-ring chronology, tree age is never considered except to remove low-frequency variations from the time series (Cook et al., 1990; Kaennel & Schweingruber, 1995). Growth responses are supposed to be age-independent on standardized series even if Bräker (2002) asserts that the elimination of ageing could result in considerable differences in the remaining residual signal. In Pinus cembra and Larix decidua, young trees (< 100 yr) were weakly influenced by climate variability, whereas growth responses to maximum temperatures were higher in older trees (Carrer & Urbinati, 2004). The responses of radial growth to temperatures in Picea glauca showed different values between trees under and over 200 yr old, although there were unclear site-specific components in the results (Szeicz & MacDonald, 1994). Shifts in temperature responses were also observed: the period with significant positive responses to growing season temperatures became shorter with tree age (Szeicz & MacDonald, 1995). At an anatomical level, Deslauriers et al. (2003) described xylem cell formation in Abies balsamea, observing early onsets of radial enlargement in stems of younger trees. It is reasonable to suppose from these results that there are age-related changes in patterns or timings of cambial activity and/or xylem cell formation.
This paper tests the hypothesis that timing and duration of xylogenesis, one of the most important features of stem radial growth, changes with tree age. Xylem cell production and differentiation were analysed at weekly scale for 2 yr on 15 adult (50–80 yr) and 15 old (200–350 yr) trees of the three main conifers in the Alps in order to compare age-related intra-annual dynamics of tree-ring formation.
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- Materials and Methods
With their long lifespan and their ‘eternally youthful’ meristem cells, trees present an extraordinary challenge to the general theories of biological ageing, given that the concept of senescence appears not to apply to woody plants (Briand et al., 1993; Lanner & Connor, 2001; Larson, 2001; Thomas, 2002). According to Connor & Lanner (1990), neither anatomical change nor cambial abnormality caused by deleterious mutational phenomena and leading to malfunctions in metabolic processes appear in 4700-yr-old trees of Pinus longaeva. However, because of intrinsic or extrinsic factors related to age or size, timing and duration of tree-ring formation change during the tree lifespan. This work has clearly demonstrated that in older trees (> 250 yr) of timberline L. decidua, P. cembra and P. abies, xylogenesis occurs in a shorter period and at lower rates of tracheid production along a radial file than in adult trees (< 80 yr). Cambium division and postcambial growth are strictly connected: delays in cell production obviously lead to delays in all differentiation processes (Rossi et al., 2003, 2006b). So, the 2–3 wk earlier reactivation of cambial activity observed in adult trees corresponded to the 7–17 d earlier start of all other phases of cell differentiation. The higher the number of cells produced along a radial row, the longer the overall period of tree ring formation becomes (Gričar et al., 2005; Rossi et al., 2006b). For this reason, adult trees concluded lignification of latewood tracheids later than older trees despite similar endings of cell division in the cambium.
Our results demonstrate that, in some environments, age is important in tree-ring formation and should be considered when performing growth–climate relationships. Although the same climate variables control tree growth throughout its lifespan, these variables become more limiting with age (Carrer & Urbinati, 2004) because the time window of tree-ring production shortens. As different timings of xylem formation were observed in adult and old timberline conifers, environmental conditions might be experienced in different time-windows during the lifespan, thus explaining the age-related periods and intensities of the observed responses to climate. The declining period, from several months to one, of significant response to growing season temperatures in Picea glauca over 100 yr old (Szeicz & MacDonald, 1994, 1995) was the result of the shortening of the time-window available for tree-ring formation in older plants. The longer xylogenetic activity in the younger trees produces a dilution, and then an attenuation, of the climatic signal over a longer period (up to 15–25% longer for cambial activity and cell differentiation in our data) and reduces the response level to climate, as observed by Carrer and Urbinati (2004).
Is the delay in cambial reactivation age or size related? Is the change directly connected to intrinsic physiological features in old trees or induced by the environment? Reactivation of the vascular cambium is promoted by indol-3-acetic acid (IAA). This hormone is produced in the younger shoots of plants and exported basipetally into the subjacent stem to induce the production of xylem and phloem (Larson, 1969; Aloni, 2001) and regulate rate and duration of developmental processes during xylogenesis (Tuominen et al., 1997; Uggla et al., 1998). Larson's hypothesis affirms that, with the IAA basipetal movement, periclinal divisions in the cambium should also begin at the base of the buds and spread downwards toward branches and stem (Larson, 1969; Denne, 1979; Lachaud et al., 1999). As a consequence, cambial activity at the stem base should begin later in taller trees because of the basipetal migration of the cambial growth wave. The 2–3 wk delay in the onset of cell production between adult and old trees compared with the height difference of the two age classes (Table 1) should lead to estimating a cambial growth wave moving at 50–80 cm d−1 along the stem of 20 m tall trees – a very high value compared with the 6 cm d−1 observed in young Fagus sylvatica (Lachaud, 1989). However, there is evidence that the IAA required for cambial resumption is available in dormant conifer tissues in autumn and winter (Little & Wareing, 1981; Sundberg et al., 1991) and Larson's hypothesis still remains to be clearly demonstrated or refuted (Riding & Little, 1986; Sundberg et al., 1991; Uggla et al., 1998; Sundberg et al., 2000; Funada et al., 2002).
In cold climates, cambial activity and tissue production are driven by temperature (Schmitt et al., 2004; Deslauriers & Morin, 2005; Rossi et al., 2007). In spring, the increases in tissue temperature among different stem diameters are partly uncoupled because of the longer-lasting frozen inner parts of the stems and the insulating effect of the thicker bark, thus shifting the reaching of warmer temperature in large old trees (Mayr et al., 2006). Since below a given temperature threshold, assessed as 7–9°C for the stem, cell formation (i.e. cell division and differentiation) could not occur or, if there is any, it will be slowed down (James et al., 1994; Körner, 2003; Rossi et al., 2007), xylogenesis in an old tree could be delayed because of the colder environment induced by the plant size itself. The observed shorter xylogenesis in older plants at the Alpine timberline could then be related to the size effect and not to age per se.
In conclusion, this study has demonstrated that, in conifers at the Alpine timberline, timing and duration of xylogenesis are not constant during a tree's lifespan, with older plants showing shorter and delayed periods of cambial activity and xylem cell differentiation. The shorter time-window during which tracheids are open to directly receive environmental signals could explain the age-dependent climate growth responses found previously. These results suggest that the supposed principle linking age-independent processes between environment and tree-ring growth might not be fully applicable in some environments (i.e. in cold climates such as the timberline). As a consequence, the time-independent growth–climate computed models could be partly incorrect. As tree rings are the most diffuse and replicated proxy for reconstructing the past climate, there is now a need to take age-dependent responses into account. The assumption that environment affects tree-ring formation in the same way independently of tree age should be reformulated.