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Tree Physiology 31, 258–261
doi:10.1093/treephys/tpr010
Editorial: part of a special section on adaptations of forest ecosystems to
air pollution and climate change
Adaptations of forest ecosystems to air pollution and
climate change
Marc D. Abrams
307 Forest Resources Building, School of Forest Resources, Penn State University, University Park, PA 16802, USA; Corresponding author ([email protected])
Received November 19, 2010; accepted February 1, 2011; handling Editor Ram Oren
The IUFRO Research Group 7.01 focuses on the ­monitoring,
modeling and assessment of climate change and air pollution
impacts on tree physiology and ecosystem water and nutrient
cycles. In March 2010, this group held a conference entitled
‘Adaptation of Forest Ecosystems to Air Pollution and Climate
Change’ in Antalya, Turkey. The main sessions of the conference were: response indicators and mechanisms of action;
water cycles; atmospheric deposition; soils and nutrient cycles;
reproduction; succession and molecular approaches; monitoring; modeling and risk assessment; ecological impacts and
genetic aspects; social and political aspects including ecosystem services; and integrated assessment of anthropogenic
stressors and adaptations of forest ecosystems under temperate and xeric conditions. From these sessions, five authors
contributed research papers based on their talks for this special section of Tree Physiology (Arend et al. 2011, Centritto
et al. 2011, Eastaugh 2011, Levanič et al. 2011, Tene et al.
2011). Two other papers from this IUFRO meeting were published in previous issues of Tree Physiology (Johnson and
Abrams 2009, Bohler et al. 2010). This Editorial will review the
major findings of these seven papers and other related papers
in relation to global climate change and pollution impacts, as
well as their implications for future research directions.
Carbon dioxide is considered the most important greenhouse
gas and has increased from 280 ppm prior to the Industrial
Revolution (since 1750) to 390 ppm present day, primarily as a
result of the burning of fossil fuels. These are the highest CO2
levels during the last 650,000 years and have produced the
highest CO2 radiative forcing in the last 20,000 years (IPCC
2007). The impacts of elevated CO2 on tree physiology and
growth have been the subject of an enormous amount of
­scientific investigation over the last 50 years (Bazzaz 1990).
Because CO2 uptake and fixation is the primary ­function of
plant photosynthesis, increasing amounts of this gas have fertilizing, stimulatory effects, within limits, on tree physiology
and growth (Karnosky 2003, Norby et al. 2010). However, forest trees may now be CO2 saturated and further increases
in atmospheric CO2 will not lead to further enhancements in
photosynthesis and growth (Korner 2003).
In contrast to the enhancement effect of elevated CO2, the
increase in tropospheric ozone in many parts of the world typically has detrimental impacts on trees (Karnosky et al. 2007).
These negative impacts on tree physiology and growth typically counteract the positive impacts of elevated CO2 (Isebrands
et al. 2001). However, the impacts of ozone are much more
localized than those of elevated CO2. Globally, the highest
ozone levels, those most capable of seriously impacting tree
physiology and growth, exist primarily in the northeast USA,
California and China. In the IUFRO paper by Bohler et al.
(2010), sapling clones of Populus ­tremula × P. alba were grown
in charcoal-filtered air versus those exposed to 120 ppb ozone.
Leaves were harvested weekly for biochemical and proteome
analyses, allowing for a comparison between expanding and
adult leaves. During the leaf expansion phase (Days 0–7), the
enzymatic machinery of the leaves is set up and remains
dynamically stable in the adult leaves (Days 14–28). The
authors report that ozone had no apparent effect on expanding
leaves, while the metabolism in fully expanded leaves was disturbed after 2 weeks of exposure. Thus, the inhibitory impact
of ozone on tree physiology varies with leaf ontogeny.
Over the last century, the forest macro- and micro-environment has changed dramatically in most parts of the world.
Greenhouse gas levels have increased and the atmosphere
has warmed, on average, by ~1°C (IPCC 2007). The growing
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Adaptations of forest ecosystems 259
s­ eason has been extended by ~10–20 days in temperate
regions (Menzel and Fabian 1999, IPCC 2007). Some regions
are now receiving more precipitation while other areas are
receiving less. Widespread forest cutting and subsequent wildfires have replaced old-growth forests with younger, fastergrowing forests (Abrams 2003). The overall stimulatory effect
of these factors is present in many tree physiology and forest
growth studies. Way and Oren (2010) reviewed the positive
temperature effects on tree physiology and growth, which vary
by species (conifer versus hardwood) and between boreal,
­temperate and tropical regions. Precipitation chemistry has
become more acidic but richer in nitrogen from the burning of
fossil fuels (Aber et al. 1989). These seemingly positive
impacts on trees and forest ecosystems from environmental
pollution (the burning of fossil fuels) are what I call ‘convoluted
benefits’. The IUFRO paper by Eastaugh (2011) used data from
several hundred climate recording stations of the Austrian
National Forest Inventory. Austria has experienced a warming
trend over the past 50 years, but little overall change in precipitation amounts. A major finding of Eastaugh’s study is that
most of the increase in tree growth since 1960 can be primarily ­attributed to increased nitrogen deposition rather than climate change. Forest stemwood increased by 20–40 kg per
additional kilogram of nitrogen deposition.
The IUFRO paper by Centritto et al. (2011) reported on the
interaction between high growth temperature (+10°C) and
water stress on the gas-exchange properties of Populus nigra.
They found that isoprene emission and photosynthesis did not
acclimate in response to elevated temperature, whereas dark
and light respiration acclimated to higher temperature. Water
stress and high growth temperature caused a significant
decline in photosynthesis and respiration. Photosynthesis was
restored in about a week following re-watering, indicating the
transient nature of biochemical limitations. Water stress uncoupled the emission of isoprene from photosynthesis and stomatal conductance, suggesting that temperature interactions
with water stress may dominate poplar’s acclimatory capability
with future climate change. The authors concluded that predicted temperature increases in arid environments may exacerbate the effects of water stress even if soil water availability is
not directly affected. While small increases in temperature
often result in increased photosynthesis and tree growth (Way
and Oren 2010), large increases in temperature are inhibitory.
Dendrochronology (the study of tree rings) provides important information for reconstructing past climate and assessing
the impacts of climate change and disturbance events on tree
growth (Abrams and Orwig 1995, Mann et al. 1999, Abrams
2003). Four of the IUFRO papers published in Tree Physiology
used tree rings in their climate change research. Provenancespecific growth responses to experimentally applied drought
and air warming were studied in saplings of three European
oak species by Arend et al. (2011). For each species, four
provenances were subjected to four climates: control, periodic
drought, air warming or their combination over a 3-year period.
They reported that drought reduced shoot height growth and
stem diameter growth, while air warming stimulated shoot
height growth but reduced stem diameter growth and root
length growth. The growth responses in shoots and stems
were highly variable among provenances, but not always consistent with the climate conditions of provenance origin. Shoot
height growth was found to be more sensitive to drought in
provenances from northern latitudes than in provenances from
southern latitudes. The authors concluded that differential
treatment responses altered allometric growth relations and
that genetic factors related to the postglacial immigration history of European oaks may have caused selective pressure at
provenance origins.
The IUFRO paper by Levanič et al. (2011) investigated the
associations between tree growth, wood anatomy (hydraulic
architecture), carbon isotope discrimination and tree mortality
following drought induced by site drainage. The authors were
motivated by a lack of specific research dealing with the
increasing forest mortality in relation to climate change that
has been observed globally. The authors utilized a local soil
water drainage event in 1982 that resulted in increased mortal­
ity within a stand of oak trees (Quercus robur). They found that
pre-dawn water potentials were more negative for trees in the
process of dying compared with those that survived. Tree rings
formed over the 123 years prior to the onset of mortality were
used to estimate tree productivity from basal area increment
(BAI), xylem hydraulic parameters via anatomical measurements and crown-level gas exchange via carbon isotope discrimination. Significantly higher mortality occurred in oak trees
with high BAI prior to the drainage event. In trees that died,
hydraulic diameter and conductivity of vessels were higher
than in surviving trees. Trees that died had consistently lower
isotope discrimination than trees that survived. The authors
concluded that tree mortality was associated with anatomical
and physiological differences prior to the onset of soil drainage
and that dying trees may have had hydraulic limitations under
drought.
The paper by Tene et al. (2011) reports a methodology to
better identify and understand how commonly measured tree
proxies, such as dendrochronology, stable isotopes, ring density, blue reflectance and forest biometrics, relate to environmental parameters and climatic events. The authors utilized a
thinning experiment in Ireland to test a methodology for monitoring drought stress based on the analysis of growth rings.
The study incorporated three thinning regimes (light, moderate
and heavy) and a multidisciplinary approach to assess tree
response to the interaction of thinning and climate. Their results
showed that radial growth was a good proxy for monitoring
changes to moisture deficit, while maximum wood density and
blue reflectance were appropriate to assess changes in ­growing
Tree Physiology Online at http://www.treephys.oxfordjournals.org
260 Abrams
season temperature. Rainfall amount was a major factor in stable
carbon and oxygen discrimination, but mostly in the latewood,
rather than earlywood, formation phase. Stable oxygen isotope
analysis was more accurate than radial growth analysis in
drought detection. This research provides recommendations to
better understand how commonly used tree-ring proxies relate
to environmental parameters.
A range-wide dendrochronology study of eight tree species
in the eastern USA was reported by IUFRO presenters Johnson
and Abrams (2009). This study explored growth rate (BAI)
relationships across age classes (from young to old) for one
or more species within the genera Populus, Quercus, Pinus,
Tsuga and Nyssa. We found that most trees in all age classes
exhibited an increasing BAI throughout their lives. This is particularly unusual for trees in the older age classes, which were
expected to have declining growth in the later years, based on
­physiological growth models. There existed an inverse relationship between growth rate and increasing age class. The
oldest trees within each species have consistently slow growth
throughout their lives, implying an inverse relationship between
growth rate and longevity. Younger trees (<60 years of age)
within each species were consistently growing more quickly
than the older trees when they were of the same age due to a
higher proportion of fast-growing trees in the young age
classes. Slow, but increasing, BAI in the oldest trees in recent
decades is a continuation of their growth pattern established
in previous centuries. High growth in trees may be related to
the stimulatory effects of global change phenomena (climate
and land-use history) over the last 50–100 years. A recent
increase in tree-ring growth was also reported for 4000-yearold bristlecone pine in the western USA (Salzer et al. 2009).
There is normally an inverse relationship between tree age
and tree growth and between tree growth and longevity
(Johnson and Abrams 2009). Therefore, the continuation of
global change factors that have a stimulatory effect on tree
growth may act to reduce tree longevity in the future, as fastgrowing trees are less likely to obtain the maximum longevity
for the species.
We live in a unique time when the impacts of elevated greenhouse gases have moved from the field of meteorology to the
ecological and environmental arenas. This natural experiment
provides almost limitless opportunities for tree physiologists
and other environmental scientists. The IUFRO papers reviewed
here point to some important directions of future environmental pollution and global climate change research. These include
the importance of studying plant genotype and environmental
interactions, such as the impacts of temperature coupled with
water stress, pollution impacts in relation to plant and tissue
ontogeny, the importance of tree anatomy (e.g., hydraulic architecture) to assess environmental change responses, and using
dendrochronology (tree-ring analysis) to monitor the inter­
action of climate change, pollution, nitrogen deposition and
Tree Physiology Volume 31, 2011
f­orest disturbance. Tree rings are unique in their ability to
reveal ­long-term tree growth (ring width) patterns in relation to
­environmental change and the uptake and sequestration of
­pollutants (via tree-ring chemistry). The IUFRO papers also
demonstrate the importance of physiological thresholds in tree
responses to climate change that low to moderate increases in
greenhouse gases, nitrogen deposition and temperature oftentimes have a stimulatory impact on tree physiology and growth
(convoluted benefits), while large increases are often detrimental or provide no further benefit to the tree. Future research
that utilizes the approaches outlined in these papers should
greatly increase our understanding of global climate change as
we move further into the twenty-first century.
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