- Top of page
- Materials and methods
The physiological mechanisms of alpine tree line formation have been discussed for over a century (Tranquillini 1979; Körner 2003a). However, many explanations were deduced from regional studies, often leading to an overemphasis of very local, site-specific drivers, rather than overarching mechanisms for this global phenomenon (Körner 1998a), with the inclusion of disturbances (including anthropogenic) further complicating the issue (Holtmeier & Broll 2007). In search of a functional explanation for climatic tree line positions globally, a recent model suggests a 6·7 ± 0·8 °C mean growing season temperature threshold (Körner & Paulsen 2004). The consistency of this tree line isotherm, irrespective of latitude, season length, geology, moisture regime and tree taxa suggests a common low temperature impact on plant metabolism (Hoch & Körner 2003), either related to carbon gain (source activity, photosynthesis) or sink activity (tissue formation).
A photosynthesis-related low temperature limitation of growth would translate into a depletion in tissue concentrations of mobile photo-assimilates (source-limitation hypothesis, Stevens & Fox 1991); a direct inhibition of meristematic activity at otherwise sufficient C-supply (sink- or growth-limitation hypothesis, Körner 1998a) should cause the mobile carbon pools to become larger as it gets colder. In both cases an imbalance between C-acquisition and C-processing should be mirrored by the size of the trees’ non-structural carbon pools (i.e. concentrations of sugars, starch, neutral lipids, etc.; Chapin, Schulze & Mooney 1990; Dickson 1991). Numerous growth chamber and field studies have demonstrated soluble (low molecular weight sugars) and insoluble (starch) non-structural carbohydrates (NSC) in leaves and stems to rise when carbon supply exceeds, and to decline as carbon compounds get short relative to carbon demand (e.g. Abod & Webster 1991; Jordan & Habib 1996; Iglesias et al. 2002). Commonly, environmental constraints affect carbon investments (growth) long before they affect the carbon assimilation (Körner 2003b; Smith & Stitt 2007).
Mobile carbon pools in tree tissues should decline with altitude as one approaches the tree line, should carbon supply play a critical role (Hoch, Popp & Körner 2002). In contrast, a direct low temperature impact on growth should cause mobile carbon pools to increase with altitude (reduced carbon demand) at otherwise sufficient photosynthetic activity. To date, analyses of non-structural carbon reserves at tree line were restricted to a few sites and taxa (Hoch et al. 2002; Hoch & Körner 2003; Shi, Körner & Hoch 2006), with one location at the world's highest tree line position in the Bolivian Andes (Polylepis, Hoch & Körner 2005). In no case were carbons reserves depleted at tree line, but rather increased as one approaches the tree limit in support of the sink-limitation hypothesis.
In line with these observations, Pinus uncinata showed no stimulation of growth when exposed to elevated CO2 concentrations over 4 years at tree line (Handa, Körner & Hättenschwiler 2005, 2006). In contrast, the summer-green Larix decidua exhibited a significant stimulation of growth by elevated CO2 within the same experiment, although this effect seemed to decline after 5 years (T. Handa, pers. commun.). It thus remains unresolved whether the deciduous Larix is carbon limited at tree line. These experimental trees were relatively young and isolated, so they could expand their growth in any direction. This, however, is a common situation at tree line, which might facilitate CO2-sensitivity of growth (Körner 2006a). The limited number of experiments, as well as the bias of existing NSC data towards a few evergreen taxa, does not allow for a conclusive judgment about the general carbon supply status of trees at alpine tree lines.
Here, we present data for two deciduous and two evergreen tree genera at different tree line sites in the highest landmass on earth. The lift of the Himalayan chains resulted in some of the world's highest tree lines (Körner 1998a,b; Shi & Li 2000) enhanced by the ‘Massenerhebungseffect’ in interior ranges (i.e. higher temperatures for a given altitude in the centre of a large mountain system compared to its front ranges (Körner 2003a). The tree line altitude climbs from 3600 m at the eastern border to 4700 m in the interior of the Tibetan Plateau. Moreover, tree lines are formed by a suite of different taxa in this region (Shi & Li 2000). Species of Abies, Picea, Betula, Larix and Juniperus (in the later text all addressed by genus) form increasingly higher tree lines as one moves from east to west. Here, we present data for the carbon charging of tree line trees between 4300 and 4700 m in the eastern part of the Himalayas.
- Top of page
- Materials and methods
This broad survey of tree line ecotones in the eastern Himalayas revealed no indication of a systematic decline of carbohydrate charging of trees as they reach their upper limits. Rather, we detected a trend of increasing NSC concentrations with altitude, which was statistically significant in about half of all investigated tissues, although the investigated elevational gradients measured only a few hundred meters. Thus, based on the existing evidence that NSC mirrors a trees’ carbon balance (see Introduction), carbon does not appear to be a limiting resource at tree line in these Himalayan test sites, matching observations from other tree lines (Hoch et al. 2002; Hoch & Körner 2003; Shi et al. 2006; Piper et al. 2006), including the highest elevation Polylepis-trees in the Andes (Hoch & Körner 2005).
mean growing season soil temperature and tree line distribution patterns
Although amongst the highest tree lines in the world (Shi & Li 2000), the seasonal mean soil temperature measured at the Mt Sygera tree limit matches the global mean temperature at tree lines of 6·7 ± 0·8 °C, as well as the average of 6·5 ± 0·7 °C at other warm temperate tree lines in Asia (Körner & Paulsen 2004). The narrow range of growing season temperatures at tree lines of widely differing altitudes around the globe suggests a common low temperature limit of tree growth. High carbon charging of trees even at the highest tree lines (with c. 45% lower air pressure than at sea-level, Hoch & Körner 2005) suggests that the pronounced reduction in partial pressure of CO2 does not reduce carbon assimilation to an extent that would affect tissue NSC concentrations.
Remarkably, the Juniperus tree line on Mt Sygera (as well as in other places) exceeds the limit of Abies by c. 200 m of elevation on south to east exposed slopes. This staggered altitudinal distribution of Abies and Juniperus awaits a physiological explanation. The temperature regime from the inverted tree line site (river plain) at Mt Sygera may hold the answer. Although the floodplain (with Juniperus only) was slightly warmer than the flanks (the lower Abies limit), the thermal extremes and short-term changes in temperature were more pronounced at the bottom of the valley. We therefore suggest that Abies is excluded from a site when severe nighttime radiative cooling is combined with pronounced daytime warming. It is well known that rapidly oscillating temperatures from very cold to warm exert more severe constraints on plants than steady deep-freezing temperatures (Strimbeck, Johnson & Vann 1993). There is evidence that B. pubescence in North Sweden experiences massive damage at variable, but not at stable, low temperatures (Björn Holmgren, Abisko, Sweden, pers. commun.). Mayr, Rothart & Damon (2003) demonstrated that repeated freeze-thaw cycles induce massive xylem embolism in conifers, especially under drought-stressed conditions. Abies is much more sensitive to cavitation than Juniperus, since it experiences a complete loss of hydraulic conductivity at a much higher (less negative) needle water potential than does Juniperus (Larcher 2003). Hence, freezing-warming cycles of the magnitude found in this study may select for Juniperus and deter Abies from the river plain. A frost-induced inverse tree line has also been described for different Eucalyptus species associated with temperature inversion in a depression (Paton 1988). The higher elevation tree line of Juniperus at Mt Sygera and other sites in Tibet may thus also relate to late winter conditions in this monsoonal climate, with clear sky and little snow throughout most of the winter. Juniperus turkestanica can even survive the harsh and dry climate of the mountains of the Pamir and Karakorum, although with a short, stunted stature (Miehe 1996; Miehe & Miehe 2000).
Morphological plasticity may contribute to the relative success of Juniperus at such winter-dry, high elevation sites. Larix and Abies rarely form stunted, polycorm (i.e. multi-stemmed) individuals at tree line, Juniperus, however, does and forms shrub, krummholz, and stunted polycorm bush above the tree line. Dense thickets may have a warmer canopy climate due to decoupling from free atmospheric convection during the growing season (Goldstein, Meinzer & Rada 1994; Körner 2003a). Seedlings and saplings of Larix and Abies may also profit from higher temperatures as long as they are nested within shrubs, especially Rhododendron species. But this ‘nursering’ effect by shrubs (Hättenschwiler & Smith 1999; Smith et al. 2003) disappears as soon as these monocormic tree species emerge from the shelter, and become exposed to low atmospheric temperatures, which restrict growth.
Enhanced solar radiation in the drier, continental part of mountain ranges (‘Massenerhebungseffect’) is well known to facilitate tree growth at higher elevations as is the case at the Nagarze J. tibetica tree line (at 4680 m a.s.l.), in the driest region examined here. Higher rainfall and thus cloudiness explains the nearly 200 m lower tree line of J. saltuaria near Nyingchi, closer to the eastern front ranges of the Tibetan Plateau. Polylepis species in the Andes also reach highest elevations in very dry regions (Kessler 1995; Hoch & Körner 2005).
altitudinal trends of growth and seedling establishment
The current study documented stronger reductions in tree height than in width (tree-ring) growth towards tree line for all species, similar to previous reports on sub-alpine conifers in the European Alps (Bernoulli & Körner 1999; Li, Yang & Kräuchi 2003), who also documented a more pronounced reduction in tree height compared to stem diameter as one approaches the altitudinal tree limit.
While seedling establishment is an unquestioned prerequisite for any plant recruitment, it does not seem to be critical for the formation of the tree lines studied here. There were crippled, multi-stemmed tree-like individuals of presumably substantial age above the tree line, but they appear to be unable to grow into upright trees. Tree seedlings above tree line in fact profit from facilitation by grasses and shrubs (Smith et al. 2003). But as they grow in height and gradually face increasing aerodynamic coupling, they eventually become the coldest structures and frequently face the fate of dieback in the landscape (Körner 2006b). Thus, it seems that the crucial phase is the sapling to tree transition, where trees enter a thermal regime different from that in low-stature plants.
altitudinal trends of nsc and carbon supply at tree line
The altitudinal patterns of NSC do not indicate any difference between evergreen and deciduous taxa. Both Larix and Betula had higher tissue NSC concentrations at tree lines, hence do not appear to be C-limited. This contrasts responses of (c. 35-years-old) L. decidua in the European Alps which showed enhanced radial stem growth and annual shoot increment in response to 4 years of free air CO2 enrichment at tree line (Handa et al. 2005, 2006). From our findings, we would expect that the initial effect of CO2 fertilization observed at the Swiss Larix tree line site is of transitory nature as has been found in many other experiments with young trees (Körner 2006a).
The exceptional pattern in branchwood NSC concentration in J. tibetica at 4680 m most likely resulted from the significantly older age, much narrower growth rings and thus greater wood volume density in comparison to the lower sites. NSC concentration is well known to decline from the cambium towards the pith (Fischer & Höll 1992; Magel, Einig & Hampp 2000; Hoch, Richter & Körner 2003), and smaller ring width (Yao 1970) and older cambial age (Oliva et al. 2006) lead to higher wood densities.
In conclusion, the observed decline in tree vigour with elevation is not associated with a depletion of tissue carbohydrate reserves in this highest tree lines of Eurasia. In most cases, NSC concentration rather increases as one approach the tree limit. This holds true for both deciduous and evergreen taxa and for the eastern (lower altitude) as well as the western (very high altitude) tree lines of the eastern Himalayan. Tree line temperatures measured at our sites match the global mean and underpin the c. 6 °C threshold for any significant meristematic activity, including that in roots (Alvarez-Uria & Körner 2007). While small trees and krummholz co-occur with alpine dwarf-shrubs and herbaceous vegetation at much higher altitude, upright tree crowns are at an aerodynamic disadvantage and thus are confined to lower altitudes. Our data support the sink-limitation hypothesis for tree line formation in the worldwide largest and highest mountain system.