GC31A-1013
Predisposing trees to die during drought:
How physiology and climate history influence mortality of piñon pine in the Southwest, U.S.A.
*A. K. Macalady1,2, N.B. English3, N.G. McDowell4 and T.W. Swetnam1
1 Laboratory of Tree-Ring Research, 2 School of Geography and Development, University of Arizona, Tucson, AZ, USA.
3School of Earth and Environmental Sciences, James Cook University, Townsville, QLD, Australia
4Los Alamos National Laboratory, Los Alamos, NM, USA. *Corresponding Author: amacalad@email.arizona.edu
Climate-induced tree mortality is an emerging global
phenomenon that will have wide-ranging consequences
for forest composition, structure and function1. However,
predisposing factors and tree physiological mechanisms
that underlie episodes of mortality remain uncertain1,2.
Warm drought and associated eruptions of engraver
beetles recently resulted in extensive tree mortality in
piñon-juniper woodlands of the Southwestern U.S.A.
(Fig. 1). We are developing annually-resolved, tree-ring
based records of growth and carbon isotope ratios from
pinon pines (Pinus edulis) that died and survived during
drought to test leading hypotheses of tree mortality
during drought (Fig. 2).
2
Short
H1. Dying trees close stomata to avoid hydraulic failure,
limiting photosynthesis and resulting in lower Δ and
lower growth than in trees that survive.
H2. Dying trees maintain more open stomata, resulting
in greater Δ and higher growth than in surviving trees,
but leading to death via hydraulic failure.
H3. If chronic water stress is the driver of low growth
and greater Δ in trees that die, growth and Δ in dead
trees should be more sensitive to drought than surviving trees.
Research Questions
Carbon
Hydraulic and
symplastic
failure
From McDowell et al. 2008
8
Figure 5. We sampled 118 pairs of dead and surviving
trees (example below). Six pairs per site/drought were selected for isotope analyses, with preliminary isotope data
from one site presented below. Pairs were selected based
on similarity in size, age and proximity.
Greater Discrimination
More open stomata (less water stress)
Lower photosynthetic rates
13Catm 13Cplant
1 + 13Cplant
/1000
BNM
c
a + (b - a) * c ca
Less Discrimination
More closed stomata (more water stress)
Higher photosynthetic rates
Figure 4. Discrimination (Δ) is calculated from measured δ
13Cplant and δ13C values of CO in the atmosphere. Plants dis2
criminate against 13CO2 as as CO2 diffuses into open stomata (a,
4.4‰) and through biological fractionation during photosynthesis
5
(b, 27‰) . Carbon isotope discrimination in plant tissue, including
wood, are a function of this fractionation and the ratio of CO2 concentration inside plant chloroplast (cc) and CO2 concentration of
the atmosphere (ca). Δ in plants is thus a function of stomatal conductance (related to drought stress), and photosynthetic rate,
which influences cc by regulating the consumption of CO2 in chlo-
Figure 6. All sites include samples representing recent
(2000’s) mortality. SEV and BNM also include archived
and remnant wood samples with outer rings dating to
the 1950’s drought. This allows for an unprecedented
window into mortality processes across space and time.
TRP
2000s
1950s
n
RW
mm/yr
BAI
cm2/yr
BAI/BA
cm2/yr/yr
29 30
NA NA
0.115
NA
0.669
NA
0.003
NA
BNM
2000s
1950s
10 10
22 23
0.107
0.180
0.399
0.154
0.004
0.020
SEV
2000s
1950s
30 30
27 27
0.252
0.236
0.644
0.245
0.012
0.022
69 70
49 50
118 120
0.172
0.210
0.188
0.612
0.202
0.443
0.007
0.021
0.013
L
D
Ring Width Index
Mortality
Episode
1830
1850
1870
1930
1950
1970
1990
2010
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ponderosa elevational transect. GCB, 16, 399-415 5 Farquhaur et al. 1982, On the relationshipbetween carbon isotope discrimination and the intercellularcarbon dioxide concentration in
leaves. Australian Journal of Plant Physiology, 9:121–137. 6 Biondi & Quedan 2008, A Theory-Driven Approach to Tree-Ring Standardization: Defining the Biological Trend from Expected
Basal Area Increment, Tree-Ring Research, 64(2):81. 7 Daly. et al. 2008. Physiographically-sensitive mappingg of temperature and precipitation across the coterminous United States.
IJCLIM 28:2031-2064 8 Hamon, 1961. Estimating potential evapotranspiration. Proc Am Soc of Civil Engineering 871: 107–120. 9 Whitehead & Jarvis1981. Coniferous forest and planta-
1970
1990
2010
Figure 9. Preliminary
values of Δ calculated
from δ13C of whole
wood in trees that died
and survived the 2000’s
mortality episode at SEV.
Mean values are plotted
for each year. Dead and
live tree values are significantly different (repeatmeasures AOV (p=0.036).
14.0
13.0
12.0
1990
1993
Divergence of dead and live tree growth decades before mortality at some sites points to mortality processes that operate on long timescales, with previous droughts likely
weakening trees and increasing the chances of future mortality.
1 Allen et al. 2010, Global Overview of Drought-Induced Forest Mortality Reveals Emerging Climate Change Risks. FEM, 259, 660-6840; 2 McDowell et al. 2011, The interdependence of
1950
15.0
Conclusions
survive while others succumb to drought? NewPhyto, 178, 719-739 4 McDowell et al. 2010, Growth, carbon-isotope discrimination, and drought-associated mortality across a Pinus
1930
Live, n=4 trees
16.0
Our results suggest that tree hydraulic characterics and gas exchange parameters are important for predicting piñon mortality during drought. However, our data do not conform simply to our original hypotheses regarding the role of carbon starvation, hydraulic failure and chronic water stress in determining the fate of trees. Two scenarios are
consistent with combined growth and isotope data from SEV 2000’s:
1) Dead trees may have had lower crown area/root area ratios, leading to less water stress and greater stomatal conductance. Small crowns, however, lead to low growth
and eventual death via constraints on whole tree photosynthesis and carbon storage capacity.
2) Low photosynthetic capacity, driven by low leaf nitrogen may be driving greater Δ in dead trees. Chronic constraints on photosynthetic rate would also lead to low
growth and mortality during drought via limited carbon uptake and/or reserves.
References
1910
Year
Dead, n=6 trees
Figure 8. Response of live and
dead trees to climate assesed by
testing for differences in slopes of
regressions between BAI/BA and climate (see ref. 4) for the 30 years previous to each mortality episode.
Live tree slopes were significantly
greater than dead slopes (p<0.05,
ANCOVA) at (a) BNM 1950’s, (c) SEV
1950’s and (d) SEV 2000’s, but not at
(b) BNM 2000’s. Differences at TRP
are also not significant (not shown).
P-PE June-July (mm)
mechanisms underlying climatedriven vegetation mortality. TREE 26 : 523–532. 3 McDowell et al. 2008, Mechanisms of plant survival and mortality during drought: Why do some plants
1890
Figure 7. Growth of trees that died and survived at SEV. Ring width index chronologies of trees from
1950’s (top) and 2000’s (middle) mortality episodes in black (live) and dark gray (dead). Individual trees
are plotted in light gray, and a smoothing spline (live = blue, red=dead) is plotted over each chronology.
June-July P-PE (bottom) is plotted with a 7-year running mean. Sub-decadal wet and dry periods shaded
in blue and red, respectively. Light blue vertical bars show how growth of survivors diverges during wet
periods decades before mortality events.
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40
30
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50
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50
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L
P-PE (mm)
Table 1. Mean growth in live trees minus mean growth in dead trees (10
years prior to death). Ring width, BAI and BAI/BA are shown, with significant differences shaded (ANOVA, p<0.05). BAI/BA is a relative metric of
growth that facilitates comparison of between trees of different sizes.
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tions. WaterDeficits and Growth, Vol 6 , Kozlawski TT (ed). Academic Press: NewYork
1910
0
20
4
1890
3
Discrimination (
Preliminary isotope data from trees that died and survived during the 2000’s mortality episode at SEV indicate
that dead trees had greater Δ based on whole wood δ
13C than live trees, consistent with dead trees maintaining greater stomatal conductance in the years before
death (H2) (Fig. 9).
Site
All 2000s
All 1950s
All trees
BAI / BA cm2 / yr / yr *1000
Piñon growth is most sensitive to PRISM derived precipitation - potential evapotraspiration (P-PE)8 over the
twelve month period ending in July of the growing
season (correlations between a standard RWI chronologies and climate for each site: r = .82 (TRP), r = .70 (BNM),
r = .78 (SEV), p<.001). Live tree BAI/BA at BNM and SEV
appear more responsive to P-PE than dead trees, although the effect is not significant in all cases (Fig. 8).
This result is inconsistent with H3.
TRP
SEV
Ring Width Index
7
What is the role of chronic
water stress in driving piñon
death?
Figure 2. Trees may die during drought via hydraulic failure,
carbon starvation, or some combination, with biotic agents reducing mortality thresholds. Piñon may conserve water and
minimize hydraulic failure through stomatal closure, resulting
in carbon starvation as photosynthesis is curtailed2,3.
Photo by C. Allen
Growth, Δ and climate
response of live and dead trees
Dead trees generally had lower growth in the years
before death than surviving trees (Table 1), consistent
with H1. Ring width index (RWI) chronologies6 from SEV
reveal that growth of live and dead trees began to diverge decades before mortality episodes, after prior
droughts (Fig. 7). A similar pattern was found at BNM,
though it was not as pronounced (not shown).
Do dead piñon trees have hydraulic characteristics that
predisposed them to mortality via hydraulic failure or
carbon starvation during
drought and associated
beetle attack?
Amplifying starvation
1810
3
Long
Biotic agents
High
Growth and Δ from tree rings
Basal area increments (BAI and BAI/BA) and discrimination (Δ) based on δ13C in tree-rings are integrated parameters of whole tree physiological function, and established proxies for tree carbon balance3,4 and gas exchange (Fig. 4)4. Using records from trees that died and
survived current and historic droughts (2000’s and
1950’s, repectively) (Fig. 5, Fig 6.), we aim to test three
related hypotheses:
Duration of water stress
Low
Figure 1. Needleless carcasses of piñon pine in a woodland near Los Alamos, NM.
Intesnity of water stress
Climate-induced tree mortality
1
1996
1999
Year
5
2002
2005
Next steps
Extend isotope data back in time to uncover
processess underlying observed growth divergences.
Generate isotope data for all study
sites/drought episodes.
Employ a simple hydraulic model9,4 to test
whether changes in crown area could produce observed differences in Δ.
Acknowledgements
This work is funded by LANL IGPP, contract number 131481 .
A. Macalady supported by an DOE Global Change Graduate
Research Education Fellowhip . We aknowledge Harald Bugmann, Craig Allen and Julio Betancourt for help with his work ,
Julia Guiterman and Ken LeRoy for laboratory assistance and
Colin Haffey and many others for help with field work. Special
thanks to D. Griffin for help with site map and poster layout