Tree Physiology 33, 887–890
doi:10.1093/treephys/tpt087
Commentary
Take a tree to the limit: the stress line
Roberto Tognetti1,2,3 and Caterina Palombo1
1Dipartimento
di Bioscienze e Territorio, Università degli Studi del Molise, 86090 Pesche, Italy; 2The EFI Project Centre on Mountain Forests (MOUNTFOR), Edmund Mach
Foundation, 38010 San Michele all’Adige, Trento, Italy; 3Corresponding author ([email protected])
Received August 11, 2013; accepted September 4, 2013; handling Editor Danielle Way
A change in climate would be expected to shift plant distribution as species expand in newly favourable areas and decline
in increasingly hostile locations (Kelly and Goulden 2008).
Even under conservative scenarios, future climate changes are
likely to include further increases in mean temperature with
significant drying in some regions, as well as increases in the
frequency and severity of extreme droughts, and heat waves
(Allen et al. 2010). As climate changes rapidly with height over
relatively short horizontal distances, so does vegetation and
ecohydrology (Beniston 2003), and alpine regions have been
suggested to be particularly vulnerable to climate change
(Elkin et al. 2013). If the treeline moves up in elevation, the
increased carbon storage and evapotranspiration from this
effect may provide a partial negative feedback to climate
change. Nevertheless, vegetation influences the absorption of
energy by the surface via modification of the surface albedo. A
shift to evergreen forest at the mountain treeline would amplify
the alteration of the physical characteristics of the land surface
induced by forest expansion, decreasing surface albedo, while
increasing net evaporation and surface roughness.
In the present issue of Tree Physiology, Charrier et al. (2013)
provide a valuable study on the physiology of frost resistance
at the altitudinal limit of 11 common European tree species
(Betula pendula, Fagus sylvatica, Pinus sylvestris, Quercus robur,
Corylus avellana, Juglans regia × nigra, Acer pseudoplatanus,
Alnus cordata, Carpinus betulus, Prunus cerasifera and Robinia
pseudoacacia). The central question of this study was to model
potential altitudinal limits of these trees by monitoring ecophysiological and physiological parameters during the cold
season. These authors applied an original multi-parametric
analysis focused on frost resistance of living xylem cells (rays
and the paratracheal parenchyma), embolism vulnerability of
non-living water conduits (tracheids and vessel elements) and
avoidance of spring frosts depending on timing of budburst.
While wood anatomy appeared to be the main driver of altitudinal limit (narrow vessels being an important adaptive trait in
frost exposed environments), osmotic-related parameters were
also highly significant. Another important outcome of this study
was that the maximal percentage of loss of conductivity was
directly related to vessel and living-cell resistance and indirectly related to physiological or anatomical parameters,
explaining these resistances. Once established, a tree growing
at high elevation must reinforce mechanically (against wind
and snow accumulation), and this process involves the capability of the species to accumulate carbon, providing the structural strength of cells, which will be diverted towards
reinforcement and away from building an efficient hydraulic
system. Nevertheless, the evidence for a trade-off between
mechanical strength and hydraulic efficiency along climatic
gradients is still ambiguous, and a trade-off between efficiency
and strength may not occur.
Frost resistance to winter embolism was addressed by
Charrier et al. (2013) by examining the physical resistance to
xylem cavitation (percentage of loss of conductivity after one
freeze/thaw event) and the active refilling of embolized elements (maximal frost hardiness). They confirmed that hydraulic
architecture integrity, considered the key physiological process
in plant survival, is not only critical for trees under drought conditions (Choat et al. 2012) but also during winter freezing conditions. Survival under extreme climatic conditions and the
potential altitudinal limit of trees would depend on the resilience
of both living cells and non-living water transport systems to
freezing events. In particular, the interaction between embolism
and refilling might rely on the contribution of living cells undamaged by frost for the development of pressurization mechanisms for refilling. The frequency of freeze/thaw events (and
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888 Tognetti and Palombo
total time the xylem is above and below freezing), representing
a measure of interaction between climate and geomorphology,
might indicate the relative potential for site-specific treeline
advance. McDowell et al. (2008, 2011) highlighted with a logical chain of causal links that hydraulic failure and carbon starvation are integrated as an interdependent set of processes at
local scales (disturbance and species interactions), driving tree
mortality. At regional (biogeographical) scales, however, there
is little evidence of directional change in the distribution of forests attributable to on-going climate change (Beck et al. 2011).
In this sense, treeline ecosystems would represent promising
sensors to discern when prolonged negative carbon balance
meets recurrent water conduit damage in trees.
Charrier et al. (2013) emphasize the interplay between
steep environmental gradients over short distances and the
adaptive morphological and physiological balance between
xylem structure and water conduction in trees. In addition to
hydraulic limitation, low temperatures play a major role on tree
growth impairments at the treeline, limiting carbon supply
(restricted source of carbohydrates; photosynthesis) or more
probably sink activity (direct inhibition of growth; meristems)
(Shi et al. 2008). Rossi et al. (2008) and Moser et al. (2010)
observed a reduction in the period and amount of xylem production along elevation gradients. Yet, despite the research
progress and growing interest, we still know very little about
the ecophysiological and anatomical adaptations of trees to
changing environment, which could allow understanding the
plasticity of xylem in response to climate, thus disentangling
the effects of global climate and regional land-use on future
tree survival/mortality. Moreover, predicting the future climate
of mountainous regions is not yet settled. However, trees are
affected by low temperature in such a way that their elevational
limit follows a common isotherm across mountain terrain, with
functional and structural traits varying most at the same scale
as the process that most affects them. To demonstrate this
tight association between treeline and temperature, the linkage
between tree canopy temperature and the altitudinal gradient
of temperature of the free atmosphere should be further investigated with other potential limiting factors for tree growth.
Physiological and mechanical damage due to environmental
disturbances do alter the plant carbon and water balance priorities of processes, limiting growth at the treeline. If predictions of global warming hold true, the upward shift of mountain
treelines will likely depend on the ratio of temperature and precipitation increases more than on their absolute values.
However, while treelines are global in nature and can be compared with climate (Körner et al. 2011), the mechanisms behind
their existence act at smaller scales (Holtmeier and Broll 2005,
Palombo et al. 2013). Individuals respond to their local environment and form populations that are used to define the
treeline boundary (Malanson et al. 2007). Although physical
disturbances (e.g., storms, avalanches, fire) can prevent trees
Tree Physiology Volume 33, 2013
from growing anywhere, biological disturbances related to tree
development (e.g., insects, pathogens), metabolic constraints
or the action of environmental extremes prevent tree growth
above the high elevation treeline (Körner 2012). By synchronizing the biological mechanisms limiting tree growth with their
interacting environmental drivers (cf., Cocozza et al. 2009,
2012), it will be possible to better model how and where the
progressive coexistence of more numerous stresses with
increasing altitude sets the potential threshold of tree mortality
(Figure 1). In this conceptual framework, tree growth may
increase as air temperature rises at high elevation, while it
decreases at low elevation, with growth at mid-elevations
depending more on precipitation. Warming conditions and
land-use changes have already caused elevational shifts in the
distribution of mountain forests (e.g., Peñuelas and Boada
2003), but climate change may shift temperatures beyond the
physiological optimum for tree growth at elevational treeline
(D’Arrigo et al. 2004). As long as increases in temperature
persist, low-altitude forests will experience intensified stress,
mortality and composition changes (Adams et al. 2010), while
the transitional ecotones of the treeline will become climatically
more suitable for enhanced tree growth (Körner 2012). In this
sense, understanding the role that carbon demand and hydraulic constraints play in structuring treelines, as outlined by
Figure 1. Conceptual framework illustrating the progressive influence
of global change factors on the relative importance of hydraulic failure
and carbon starvation (including anatomical features, stomatal strategies, turgor properties and growth traits) with increasing altitude.
While these factors may directly alter the importance of water transport and carbohydrate accumulation relative to one another and in the
short term, other factors like tree height and low temperature can
modulate treeline fluctuation indirectly and in the long term (e.g.,
­species evolution, global circulation). The arrow on the left mountainside indicates increasing stress in trees (loss of hydraulic efficiency,
loss of photosynthetic carbon), while that on the right shows decreasing way to cope (shorter growing season to gain carbon, less xylem
produced to withstand drought). The fluctuation of the ‘stress line’
(treeline) determined by non-linear dynamic uncertainties is indicated
by dashed lines. The main global change factors are specified in the
heart of the mountain.
Take a tree to the limit: the stress line 889
Charrier et al. (2013), is critical because different components
of environmental change work synergistically to alter the ecological importance of tree structure and atmospheric circulation, namely air moisture.
Synergies and differences in water and energy balance
across regional gradients and site conditions need to be
implemented in models of the response of trees at the treeline
to varying climatic conditions. Philipona (2013) has recently
found that temperature rose at a lower rate at high elevation
in the Alps than at low elevation in Central Europe in the last
30 years, due to increased atmospheric moisture associated
with a consistent increase of forest cover and changes in
atmospheric circulation. In mountain environments, the close
relationship between climatic conditions and stand canopies
may influence the direct physiological and mechanical effects
of wind on trees, overriding low temperature. Once a climatic
limitation is lifted, other factors (biotic and abiotic) might
become limiting to tree growth, which warrants integrative
studies of non-uniform tree function and structure and investigating vulnerability to drought and freezing stress together.
We also advocate for extending analyses from tissues to
whole plants, to groups of trees sampled along nutrient and
climatic gradients, and from short durations to seasons and
years since the response of plants to disturbances associated
with elevation is not driven by altitude per se, but by complex
biological and physical interactions. Charrier et al. (2013)
established the mean vessel diameter as a major driver of
altitudinal limit, defining a threshold in sensitivity to embolism
~30 µm (cf., Davis et al. 1999), which needs to be reconciled
with the tapered structure of xylem conduits (Anfodillo et al.
2012).
The relative importance of temperature stress in treeline
dynamics is influenced by changes in other factors that are
undergoing global changes. For example, an increase in
water vapour at high elevation may decrease the importance
of solar brightening and increase the importance of low temperature, as water availability to plants increases. Quantifying
the tolerance of different tree species to frost will advance an
ecological classification scheme that is critical to explaining
the distribution of plant species and forms along elevational
gradients, as well as the fluctuation of future treeline ecosystems where the availability of heat, moisture and light are
likely to be altered. Nevertheless, alternative trait combinations for treeline environments are probable, limiting the
application of organ-level indicators to predict species performance in gradient analysis. Focusing on whole trees and
quantifying frost tolerance, and interactions with evaporative
demand and drought events or nitrogen deposition, would
generate a synergistic understanding of the ecophysiology of
trees and their patterns over altitudinal gradients.
Standardized protocols for measuring functional and structural strategies of trees are required for scaling to a broader
context. Overall, the change in tree physiology of mountain
forests in response to climate erraticism will not be a simple
oscillating movement of a stress line, and the data of Charrier
et al. (2013) point to substantial between-species variation
around this treeline.
Acknowledgments
We are grateful to Danielle Way for her helpful suggestions.
Conflict of interest
None declared.
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