Global Change Biology

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11/28/2007
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Contents
1 Prediction of the distribution of Arctic-nesting pink-footed geese under a warmer climate scenario
Rikke A. Jensen, Jesper Madsen, Mark O’Connell, Mary S. Wisz, Hans Tømmervik and Fridtjof Mehlum
11 Climate control on the long-term anomalous changes of zooplankton communities in the Northwestern Mediterranean
Juan Carlos Molinero, Frédéric Ibanez, Sami Souissi, Emmanuelle Buecher, Serge Dallot and Paul Nival
39 Estimation of the carbon dioxide (CO2) fertilization effect using growth rate anomalies of CO2 and crop yields since 1961
David B. Lobell and Christopher B. Field
46 Genotypic differences in leaf biochemical, physiological and growth responses to ozone in 20 winter wheat cultivars
released over the past 60 years
D. K. Biswas, H. Xu, Y. G. Li, J. Z. Sun, X. Z. Wang, X. G. Han and G. M. Jiang
60 Ozone and density affect the response of biomass and seed yield to elevated CO2 in rice
Chantal D. Reid and Edwin L. Fiscus
77 Water, temperature, and vegetation regulation of methyl chloride and methyl bromide fluxes from a shortgrass
steppe ecosystem
Yit Arn Teh, Robert C. Rhew, Alyssa Atwood and Triffid Abel
92 Developing an empirical model of stand GPP with the LUE approach: analysis of eddy covariance data at five
contrasting conifer sites in Europe
Annikki Mäkelä, Minna Pulkkinen, Pasi Kolari, Fredrik Lagergren, Paul Berbigier, Anders Lindroth,
Denis Loustau, Eero Nikinmaa, Timo Vesala and Pertti Hari
109 Biomass and carbon accumulation in a fire chronosequence of a seasonally dry tropical forest
Rodrigo Vargas, Michael F. Allen and Edith B. Allen
125 Ecological and site historical aspects of N dynamics and current N status in temperate forests
Rainer Brumme and Partap K. Khanna
142 Simulated chronic nitrogen deposition increases carbon storage in Northern Temperate forests
Kurt S. Pregitzer, Andrew J. Burton, Donald R. Zak and Alan F. Talhelm
VOLUME 14, NUMBER 1, JANUARY 2008, pp. 1–205
27 Detecting the impact of oceano-climatic changes on marine ecosystems using a multivariate index:
The case of the Bay of Biscay (North Atlantic-European Ocean)
Georges Hemery, Frank D’Amico, Iker Castege, Bernard Dupont, Jean D’Elbee, Yann Lalanne and Claude Mouches
GLOB AL CHANGE BIOLOGY
Global
Change
Biology
VOLUME 14
NUMBER 1
JANUARY 2008
ISSN 1354–1013
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Global
Change
Biology
VOLUME 14
NUMBER 1
JANUARY 2008
154 Feedbacks between phosphorus deposition and canopy cover: The emergence of multiple stable states
in tropical dry forests
Marcia Delonge, Paolo D’Odorico and Deborah Lawrence
161 Regeneration patterns and persistence of the fog-dependent Fray Jorge forest in semiarid Chile during the
past two centuries
Alvaro G. Gutiérrez, Olga Barbosa, Duncan A. Christie, Ek Del-Val, Holly A. Ewing, Clive G. Jones,
Pablo A. Marquet, Kathleen C. Weathers and Juan J. Armesto
177 Nitrous oxide emissions from a cropped soil in a semi-arid climate
Louise Barton, Ralf Kiese, David Gatter, Klaus Butterbach-Bahl, Renee Buck, Christoph Hinz and Daniel V. Murphy
193 Temperature and vegetation effects on soil organic carbon quality along a forested mean annual temperature gradient
in North America
Cinzia Fissore, Christian P. Giardina, Randall K. Kolka, Carl C. Trettin, Gary M. King, Martin F. Jurgensen,
Christopher D. Barton and S. Douglas Mcdowell
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• Regeneration dynamics of fog-dependent forest
• Wheat cultivar biochemical, physiological and growth
responses to ozone
• Detecting the impact of oceano-climatic changes on marine
ecosystems
• Nitrous oxide emissions from a cropped soil in a semi-arid climate
Global Change Biology (2008) 14, 161–176, doi: 10.1111/j.1365-2486.2007.01482.x
Regeneration patterns and persistence of the fogdependent Fray Jorge forest in semiarid Chile during
the past two centuries
A L VA R O G . G U T I É R R E Z *w , O L G A B A R B O S A z§ , D U N C A N A . C H R I S T I E } ,
E K D E L - VA L k, H O L L Y A . E W I N G **, C L I V E G . J O N E S w w , P A B L O A . M A R Q U E T w § ,
K A T H L E E N C . W E A T H E R S w w and J U A N J . A R M E S T O w § w w
*Department of Ecological Modelling, Helmholtz Centre for Environmental Research (UFZ), Permoser Strae 15, 04318 Leipzig,
Germany, wDepartamento de Ciencias Ecológicas, Instituto de Ecologı́a y Biodiversidad (IEB). Facultad de Ciencias. Universidad de
Chile. Casilla 653, Santiago, Chile, zDepartment of Animal & Plant Sciences, Biodiversity & Macroecology Group, The University of
Sheffield, S10 2TN, UK, §Departamento de Ecologı́a, Center for Advanced Studies in Ecology & Biodiversity (CASEB), Facultad de
Ciencias Biológicas, Pontificia Universidad Católica de Chile, Alameda 340, Santiago, Chile, }Laboratorio de Dendrocronologı́a,
Facultad de Ciencias Forestales, Universidad Austral de Chile, Casilla 567, Valdivia, Chile, kCentro de Estudios Ecosistemas,
Universidad Nacional Autónoma de México, Ap. 27–3, Santa Maria de Guido Morelia, Michoacán 58089, México, **Program
in Environmental Studies, Bates College, 111 Bardwell St., Lewiston, ME 04240, USA, wwInstitute of Ecosystem Studies, Box AB,
Millbrook, NY 12545, USA
Abstract
The persistence of rainforest patches at Fray Jorge National Park (FJNP) in semiarid Chile
(30140 0 S), a region receiving approximately 147 mm of annual rainfall, has been a source
of concern among forest managers. These forests are likely dependent on water inputs
from oceanic fog and their persistence seems uncertain in the face of climate change.
Here, we assessed tree radial growth and establishment during the last two centuries and
their relation to trends in climate and canopy disturbance. Such evaluation is critical to
understanding the dynamics of these semiarid ecosystems in response to climate change.
We analyzed forest structure of six forest patches (0.2–22 ha) in FJNP based on sampling
within 0.1 ha permanent plots. For the main canopy species, the endemic Aextoxicon
punctatum (Aextoxicaceae), we used tree-ring analysis to assess establishment periods,
tree ages, growing trends and their relation to El Niño Southern Oscillation (ENSO),
rainfall, and disturbance. The population dynamics of A. punctatum can be described by
a continuous regeneration mode. Regeneration of A. punctatum was sensitive to different
canopy structures. Growth release patterns suggest the absence of large scale human
impact. Radial growth and establishment of A. punctatum were weakly correlated with
rainfall and ENSO. If water limits forests patch persistence, patches are likely dependent
on the combination of fog and rain water inputs. Forest patches have regenerated
continuously for at least 250 years, despite large fluctuations in rainfall driven by ENSO
and a regional decline in rainfall during the last century. Because of the positive
influence on fog interception, forest structure should be preserved under any future
climate scenario. Future research in FJNP should prioritize quantifying the long-term
trends of fog water deposition on forests patches. Fog modeling is crucial for understanding the interplay among physical drivers of water inputs under climate change.
Keywords: Chile, climate change, dendroecology, disturbance regimes, fog-dependent rainforest, fog,
fragmented forest, Fray Jorge, relict forest, tree regeneration dynamics
Received 18 April 2007; revised version received 19 August 2007 and accepted 5 October 2007
Correspondence: Alvaro G. Gutiérrez, Department of Ecological
Modelling, Helmholtz Centre for Environmental Research – UFZ,
Permoser Strae 15, 04318 Leipzig, Germany, fax 1 49 0 341 235
3500, e-mail: [email protected]
r 2007 The Authors
Journal compilation r 2007 Blackwell Publishing Ltd
161
162 A . G . G U T I É R R E Z et al.
Introduction
Isolated patches of temperate rainforest are found on
the summits of coastal mountains in semiarid Chile
(30140 0 S), about 1000 km north of their continuous geographic range along the western margin of southern
South America (371–431S). These forest patches are
likely dependent on fog water inputs (Kummerow,
1966; del-Val et al., 2006) in a region receiving only
147 mm of annual rainfall and subjected to strong
interannual rainfall variability driven by El Niño Southern Oscillation (ENSO) (Aceituno, 1992; Trenberth,
1997). The conservation status of these temperate rainforest patches, presently protected within Fray Jorge
National Park (FJNP), has raised concern among forest
managers in the face of future climate change and
human impact (Squeo et al., 2004). Such concerns reflect
general scientific uncertainty about the effects of longterm climatic trends on terrestrial ecosystems (Shugart,
1998). Fog or cloud-dependent forests have been described in tropical, subtropical and semiarid regions of
the world (Hursh & Pereira, 1953; Juvik & Nullet, 1995;
Hutley et al., 1997; Liu et al., 2004; Hildebrandt, 2005;
Hildebrandt & Eltahir, 2006), and these may be especially sensitive to the effects of changes in hydrological
variables that regulate tree regeneration and long-term
survival. Possible consequences of climatic disruption
of these semi-arid forests include biodiversity loss
(Pounds et al., 1999), altitudinal shifts in species ranges
(Sperling et al., 2004) and possibly forest loss due to
increasing fragmentation and edge effects (Foster, 2001).
The forests of FJNP became separated and fragmented from the main range of coastal rainforests by
climatic drying during the Quaternary (Villagrán et al.,
2004). This process of aridization segmented the distributional range of rainforests, leaving scattered and
isolated remnants in the northernmost limit of their
main range, in the semiarid region (Villagrán et al.,
2004). Forest patches in FJNP likely have a strong
dependence on coastal fogs, which may double the
effective precipitation and affect forest patch structure
and the spatial pattern of tree regeneration and mortality (del-Val et al., 2006). Changes in fog frequency due to
changes in sea-surface temperature or the height of the
inversion (Cereceda et al., 2002), land-use practices
(Nair et al., 2003) or changes in forest structure that
may affect fog capture (e.g. Hildebrandt & Eltahir, 2006)
could also have consequences for tree growth and
recruitment patterns.
Remnant forest patches in FJNP have been subjected
to strong, inter-annual fluctuations in rainfall associated
with ENSO during the past millennia (Maldonado &
Villagrán, 2002). In addition, a drying trend has occurred in the last century in central Chile (Quinn &
Neal, 1983; Le Quesne et al., 2006). Both climatic fluctuations due to ENSO or current rainfall patterns could
also affect tree growth, recruitment and patch persistence. Alternatively, if the amount of fog water intercepted by trees is sufficient (i.e. it equals or exceeds
their hydrological requirements), then rainfall variations would be expected to have more limited influence
on tree growth and regeneration.
Here, we assessed patterns of tree establishment
relative to recent changes in rainfall and the response
of tree regeneration to anthropogenic (i.e. cutting or
burning) or natural disturbance. We used tree-ring
analysis to examine the regeneration dynamics and
radial growth patterns of the dominant tree species A.
punctatum (only member of the endemic family Aextoxicaeae) for the past 200 years, with the following specific
goals: (1) to describe the current and past trends in the
regeneration of the dominant canopy tree as an indication of forest patch persistence, (2) to develop a tree-ring
chronology for A. punctatum, (3) to assess the main
components of the canopy disturbance regime, and (4)
to assess whether canopy disturbance and regeneration
patterns of A. punctatum have been affected by recent
climate trends. Finally, we discuss the importance of fog
in delivering water to these forests in the context of
climate change.
Materials and methods
Study area
The study was conducted in forest patches located
between 400 and 600 m elevation on the coastal mountains of the semiarid region of Chile, within FJNP (FJNP,
30140 0 S, 71130 0 W, Fig. 1). The park was created in 1941
to protect fragments of evergreen temperate rainforest,
dominated by A. punctatum. These forest patches represent the northernmost extension of southern temperate
rainforests, which have a continuous distribution about
1000 km to the south (371–431S), with a rainfall regime
exceeding 2000 mm yr1 (Smith-Ramirez et al., 2005). In
FJNP, A. punctatum-dominated forests are found on
coastal summits influenced by oceanic fog (Fig. 1) and
are surrounded by a matrix of xerophytic vegetation.
Floristically, forest patches are characterized by the
dominance of A. punctatum in the canopy, and the
presence of the trees Myrceugenia correaefolia (Myrtaceae), Drimys winteri (Winteraceae), and Rhaphithamnus
spinosus (Verbenaceae), without the presence of the
sclerophyllous vegetation typical of central Chile (Villagrán et al., 2004). The patches include a species-rich
assemblage of epiphytic ferns (i.e. Polypodium feillei,
several Hymeophyllaceae) and woody vines (i.e.
Sarmienta repens, Mitaria coccinea, Griselinia racemosa)
r 2007 The Authors
Journal compilation r 2007 Blackwell Publishing Ltd, Global Change Biology, 14, 161–176
R E G E N E R AT I O N D Y N A M I C S O F F O G - D E P E N D E N T F O R E S T
163
Fig. 1 Study site and overview of the Fray Jorge landscape showing the mosaic of forest patches (dark spots) on a coastal mountaintop
of semiarid Chile (right side). Topographic lines of equal elevation (every 50 m) are shown. Forest patches are found above 500 m. The
main distribution of southern temperate rain forests (dark shading) and semiarid ecosystems (stippled) in southern South America are
shown on the left side.
which are shared with southern temperate rain forests
(Villagrán et al., 2004).
The predominant climate is mediterranean-arid, with
hot and dry summers and cool winters (Di Castri &
Hajek, 1976). Mean annual precipitation is 147 mm,
most of which occurs (490% of total) between June
and August (austral winter), with large interannual
variation in rainfall (CV 5 81%, N 5 21 years) which
has been associated with ENSO events (López-Cortés
& López, 2004). Fog drip is spatially and temporally
variable within patches (del-Val et al., 2006). Fog supplements water inputs to forest patches by an estimated
500–850 mm (Kummerow, 1966) or up to 200 mm yr1
(del-Val et al., 2006). Fog deposition is a result of
r 2007 The Authors
0.8
0.8
1.4
2.1
3.1
3.9
6.9
7.8
9.2
0.4
5.6
2.9
16.7
1.0
14.1
9.3
The Berger–Parker Index indicates vertical stratification.
SE, standard error of the mean; FJNP, Fray Jorge National Park.
3.75
3.95
3.61
3.75
SE
SW
SW
SW
35
10
42
38
2.0
3.9
14.2
22.0
F3
F4
F5
F6
495
566
635
639
7.7 1.5
0.3
F2
529
1
W
3.28
2.0 0.8
Cutting of the woody vine Griselinia,
fire in surrounding matrix
Cutting of the woody vine Griselinia,
fire in surrounding matrix
None
Tourist trail, fire in surrounding matrix
None
None
3.4 1.0
W
11
566
0.2
F1
Aspect
Altitude
Patch name
3.33
3.5 1.9
Evidence of recent
human impact
Juveniles trees
(N m2 SE)
Total number of
seedlings and saplings
(N m2 SE)
Berger–Parker
index
We used one permanently marked plot (50 m 20 m
each) in the interior of each selected forest patch to
characterize forest structure. Evidence of human impact
(stumps or fire scars) was recorded if present (Table 1).
We marked, identified to species and recorded the
diameters at 1.3 m above the base (dbh) of all trees
(stems 41.3 m height and dbh45 cm) inside each permanent plot. Trees were classified as alive (healthy),
some branches dead, or standing dead (snags). The
presence of vegetative stems (i.e. derived from sprouting) was also recorded. Because vertical stratification is
relevant to fog interception by the forest patches
(Weathers, 1999), we assessed the heterogeneity of
vertical canopy structure using the Berger–Parker diversity index (d) (Magurran, 2004). This index is based
on tree-crown positions and provides a measure of
stratification and canopy heterogeneity though the proportional importance of the most abundant canopy
class: 1/d 5 1/(Nmax/N) where Nmax is the number of
individuals in the most abundant canopy class and N is
the total number of individuals. A high value of the
index reflects greater vertical heterogeneity. Canopy
classes of each tree inside the plots were recorded as:
emergent, above canopy height; dominant, in the canopy tier; intermediate, directly under the canopy with
Slope
(%)
Patch structure
Forest patch
area (ha)
stratocumulus cloud formation over huge areas in the
South Pacific, that advance toward the west coast of
South America (Cereceda et al., 2002) and are intercepted by the vegetation on coastal mountains. The
presence of fog is probably associated with the offshore
cold water generated by the Humboldt current and
changes in the thermal inversion layer along the coast
produced by strong subsidence of the South Pacific
Anticyclone (Cereceda & Schemenauer, 1991; Cereceda
et al., 2002).
Forest patches (Fig. 1) on coastal mountain summits
of FJNP cover an area of 86.7 ha (Squeo et al., 2005),
ranging in size from 0.1 to 25 ha. Six forest patches were
selected for this study encompassing the entire range of
patch sizes in the landscape (Table 1). These are the
same patches sampled by del-Val et al. (2006). According to locals, some forest patches were disturbed by
selective logging of D. winteri and occasional grazing by
cattle, brought in from lower grazing lands, until 1943
(Muñoz & Pisano, 1947). Fires may have affected some
forest patches in the 17th and 19th centuries; limited
agriculture was concentrated in the southern part of the
park and at lower elevations, and it may have led to
clearing of some patches (Fuentes & Torres, 1991). The
intensity and spatial and temporal extent of these disturbances, however, is unknown.
Table 1 Characterization and summary of structural parameters for all tree species found in six forest patches sampled in FJNP, Chile
r 2007 The Authors
light only from above; and subcanopy, permanently
shaded.
Along three linear transects inside each selected
patch, separated from one another by 10–25 m depending on patch size, we distributed seven sampling points
20 m apart. At each sampling point, tree seedlings and
saplings (stems o1.3 m height) were counted and identified to species within a 1 m2 quadrat, while juveniles
(stems 41.3 m in height but dbho5 cm) were counted
and identified within a circular plot of 2 m radii (del-Val
et al., 2006).
Dendrochronology
We used the empirical dbh distribution of A. punctatum
trees (stems 45 cm dbh) in the permanent plots to
randomly and uniformly select a sample of 30 A.
punctatum trees for coring, across the dbh size classes
(of 10 cm each) represented within each patch. Additional cores were taken from the largest trees in each
patch (nine per patch). Cores were taken at about 1.3 m
from the base of the stem and processed following
standard dendrochronological techniques (Stokes &
Smiley, 1968). Samples with o25% of the stem radii
intact or without distinguishable tree-rings were discarded (n 5 38); a total of 196 cores (from 180 trees) were
suitable for tree-ring analysis.
Minimum tree ages were estimated by counting treerings of each core. Tree rings were visually cross-dated
assigning a calendar year to each tree ring, based on the
date of the latest ring (Stokes & Smiley, 1968). We
assigned to each tree-ring the date in which radial
growth started (Schulman, 1956). When the pith was
missing (23% of all cores), the number of rings to the
pith was estimated using a geometrical method (Duncan, 1989). After visual cross-dating, radial growth
increments were measured to the nearest 0.01 mm with
an increment-measuring device and recorded in a computer. The computer program COFECHA (Holmes, 1983)
was used to detect errors in measurements and cross
dating. We used the best crossdated trees (N 5 28 trees)
from different patches to produce the tree-ring chronology. Ring-width records for each tree were standardized and then averaged with the other trees to produce
a mean chronology (Fritts, 1976). Standardization involves fitting the observed ring width series to a curve
or a straight line and computing an index of the
observed ring widths divided by the expected value.
This reduces variances among cores and transforms
ring widths into dimensionless index values. Thus,
standardization permits computation of average treering chronology without the average being dominated
solely by the faster growing trees with large ring widths
(Fritts, 1976; Villalba & Veblen, 1997). The standard
165
chronology was done with the ARSTAN program (Cook,
1985).
For all complete cores of A. punctatum, we defined the
year when the tree became established in the forest,
corrected by age to coring height (1.3 m), which was
estimated as 10 years from dbh–age linear regression.
All trees 4100 years old (n 5 45 overall) were examined
for releases of radial growth. Releases were taken as
evidence of canopy opening (presumably due to disturbance) and used to infer patch dynamics (Lorimer &
Frelich, 1989). We defined a major growth release as an
increase 4100% in the average radial growth of the
current year relative to the previous year, which lasted
for at least 15 years afterwards. A moderate release was
defined as an increase of 450% in average radial
growth between subsequent years, lasting for at least
15 years afterwards (Lorimer & Frelich, 1989). The
sustained release criterion of 15 subsequent years was
used to eliminate short-term climatic pulses and gradual ring-width changes due to tree aging, bole geometry, and long-term climate shifts (Lorimer & Frelich,
1989).
Statistical analyses
Tree regeneration (seedling and sapling mean densities)
was compared among forest patches using analysis of
variance. Age–dbh regression analysis for A. punctatum
was performed to evaluate if dbh distributions were
indicative of age structures. Dbh distributions for all
species pooled and for A. punctatum populations were
tested with models often assumed to represent a continuously regenerating population (Veblen, 1992). Dbh
distributions in each patch were described using a
nonlinear least-squares fit of a power function: y 5 axb,
where y is stem density, x represents dbh class, a and b
are parameters. Spearman’s rank correlations were used
to assess the relationship between patch size, Berger–
Parker index and forest patch structure variables. Structural variables considered were vegetative reproduction
(percent sprouting stems), snag (percent standing dead
trees) and potential tree regeneration (density of seedlings and saplings, plus juveniles).
We evaluated the effect of climate variables on the
ring-width index (RWI) of A. punctatum (standard
chronology) using a correlation function analysis (Fritts,
1976). RWI was correlated against monthly rainfall data
over the period 1900–2002 using rainfall data from
La Serena (29154 0 S, 71112 0 W), the nearest meteorological
station to FJNP and the longest climate record in
the area (1870–2000). We also analyzed the relationship
between RWI and the Southern Oscillation index
(SOI; Aceituno, 1992; Trenberth, 1997; data from the
Bureau of Meteorology, Australian Government).
r 2007 The Authors
We examined a sequence of months starting with the
previous growing season (September–May previous
year of growth) and ending in May of the year in which
the ring was formed (i.e. at the end of the current
growing season). Limited, discontinuous historical fog
data based on field observations of daily frequency of
stratus clouds (fog) since 1970 were available for FJNP
from CONAF and Dirección Metereológica (Chile).
Cross-correlations were used to check for dependencies between climate (annual values of fog, precipitation, SOI), RWI, releases and the recruitment time
series. Data analysis involved the use of a ‘prewhitening’ procedure to remove autocorrelation before crosscorrelation analysis (Box & Jenkins, 1976). First, the time
series were analyzed for the presence of autoregressive
structure and, if present, its order was determined by
examining the partial autocorrelation functions (Box &
Jenkins, 1976). We used a maximum likelihood fitting of
autoregressive-moving average models to estimate an
appropriate model for each time series. Residual series
were computed by subtracting the observed values
from those predicted by the autoregressive model. After
removal of autocorrelations, cross-correlations using
different time lags were computed between the residual
time series to see how they related in time. All statistical
analyses were conducted in R STATISTICAL software (RDevelopment-Core-Team, 2005).
Results
Patch structure and current regeneration
Mean seedling and sapling density (stems o1.3 m
height) ranged from 1 to 16.7 ind. m2 and mean juve-
niles densities (stems 41.3 m height but o5 cm dbh)
ranged from 3.1 to 7.8 ind. m2 (Table 1). No differences
were detected in mean seedling density (F(5, 12) 5 2.48,
P 5 0.09) and mean juvenile density (F(5, 12) 5 2.13,
P 5 0.13) among patches. Forest patches varied in terms
of their vertical canopy structure. Lower values of the
Berger–Parker index were found in smaller patches Fl
and F2, and larger values in both intermediate and large
patches, indicating higher vertical heterogeneity in the
latter (Table 1). However, no significant correlation was
found between patch size and the Berger–Parker index
(P 5 0.32).
The canopy of all six forest patches was dominated by
A. punctatum, except for patches F1 and F5, which were
co-dominated by M. correifolia and A. punctatum or by
D. winteri and A. punctatum, respectively (Table 2).
R. spinosus and Azara microphylla, were occasionally
(o7%) represented in the canopy of the forest
patches. M. correifolia and D. winteri had their greatest
representation in patches F1 and patch F5, respectively
(Table 2).
Pooling all tree species, seedling densities were uncorrelated with patch size or with the Berger–Parker
index (Table 3). Seedlings of M. correifolia declined with
increases in patch size (Table 3). The relative density of
A. punctatum seedlings and juveniles also varied significantly among patches (F(5, 12) 5 15.71, Po0.01) increasing with patch area (Tables 3 and 4). Myrceugenia
had the highest relative density of juveniles in smaller
patches, accounting for 450% of juveniles, and decreasing with patch size (Table 3). In contrast, relative
density of A. punctatum juveniles and of A. punctatum
trees was positively correlated with the Berger–Parker
index (Table 3). Total densities of juveniles and trees,
Table 2 Relative density (N%) and relative basal area (BA%) for all live stems (45 cm dbh), snags (standing dead trees) and
vegetative stems (% of all stems in the plot, horizontal and/or vertical, originating from other stems) in six forest patches (F1–F6) in
FJNP, Chile
Patches
F1
Tree species
Aextoxicon punctatum
Drimys winteri
Myrceugenia correifolia
Other species*
Proportion of vegetative stems
Snags
Totals
Live stems
F2
F3
F4
F5
F6
N%
BA%
N%
BA%
N%
BA%
N%
BA%
N%
BA%
N%
BA%
10.6
0.0
89.0
0.4
65.9
16.6
2270
49.0
0.0
50.8
0.2
65.8
23.0
49.4
33.6
0.0
51.3
15.1
68.0
11.1
1520
75.7
0.0
21.6
2.7
86.0
19.4
61.6
45.6
0.0
38.9
15.4
61.7
6.0
1490
71.3
0.0
24.6
4.2
80.5
9.0
46.7
86.9
2.8
5.6
4.7
44.6
5.6
3590
93.9
0.8
4.0
1.3
59.8
1.3
90.4
15.2
77.3
0.8
6.6
21.1
9.1
3610
46.4
52.0
0.3
1.3
36.9
1.2
125.1
77.4
19.4
0.4
2.8
41.9
13.4
2520
88.8
10.8
0.2
0.3
57.1
9.0
102.6
*Azara michropylla, Raphithamnus spinosum, Griselinia racemosa (vine), and Adenopeltis serrata (understory shrub).
Totals represent accumulated stem density (N ha1) and basal area (m2 ha1) per patch.
SE, standard error; FJNP, Fray Jorge National Park.
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167
Table 3 Spearman rank correlations (rs) for the relationship of patch area and Berger–Parker index (n 5 6) with other demographic
and structural variables analysed
Patch area
Total seedlings density
Total juveniles density
Total snag density
Total vegetative stems density
Relative seedling density
Drimys winteri
Relative juvenile density
Drimys winteri
Relative snag density
Relative vegetative stems density
Berger–Parker index
rs
t(N2)
P-level
rs
t(N2)
P-level
0.03
0.77
0.14
0.14
0.06
2.42
0.29
0.29
ns
ns
ns
ns
0.03
0.03
0.03
0.37
0.06
0.06
0.06
0.80
ns
ns
ns
ns
0.94
0.88
0.83
5.66
3.71
2.96
***
**
**
0.66
0.46
0.71
1.74
1.02
2.04
ns
ns
ns
0.77
0.94
0.94
2.42
5.57
5.66
ns
***
***
0.89
0.58
0.66
3.82
1.41
1.74
ns
ns
0.54
1.29
ns
0.54
1.29
ns
0.26
0.53
ns
0.94
5.66
***
**
***Po0.01.
**Po0.05.
ns, not significant.
Table 4 Regeneration of Aextoxicon punctatum (N m2 standard error) observed in six forest patches (F1–F6) in FJNP, Chile, and
regression parameters (a and b, see ‘Materials and methods’) estimated for the power function fitted to stem density by dbh class in
each patch (all trees and A. punctatum trees, dbh45 cm)
Aextoxicon punctatum regeneration
Regression parameters for dbh distributions
Aextoxicon punctatum trees
All trees
Patch
Seedlings/saplings
F1
F2
F3
F4
F5
F6
0.05
0.05
1.0
0.14
3.0
2.62
0.05
0.05
0.54
0.08
0.86
0.87
Juveniles
a
P-level
b
P-level
a
P-level
b
P-level
0.05 0.24 0.52 1.71 1.57 2.38 199 5000.0
35 400.0
35 7300.0
24 0800.0
85 7949.6
22 576.7
***
***
***
**
**
***
3.4
2.2
3.0
2.5
3.0
1.9
***
***
***
***
***
***
272.6
300.6
16 098.3
14 7800.0
71 321.3
7140.0
ns
ns
1.28
1.10
2.21
2.42
2.81
1.61
***
***
***
***
***
***
0.05
0.20
0.21
0.74
0.65
1.88
***
**
**
**
***Po0.01.
**Po0.05.
ns, not significant; FJNP, Fray Jorge National Park.
analyzed separately, were uncorrelated with patch vertical structure (Table 3).
Dbh-distributions in all six patches fitted the power
function model (Table 4). Accordingly, there were trees
in most size classes describing a continuously regenerating forest community. Dbh distributions of A. punctatum followed this general tendency except in patches F1
and F2, which had nonsignificant fit for power function
parameter a (Table 4). In all the patches, larger dbh
classes (460 cm dbh, maximum dbh 5 155 cm) were
dominated by A. punctatum. In contrast, M. correifolia
was characterized by numerous small stems in smaller
patches Fl, F2 and F3 (dbho45 cm). D. winteri dominated the canopy of patch F5 (Table 2), with a population of small and medium size trees (dbho45 cm,
Fig. 2).
A high proportion of all sampled stems (46%,
n 5 1504) in all patches were derived from vegetative
r 2007 The Authors
Fig. 2 Diameter (dbh) class distribution of main canopy trees (dbh 45 cm) in six forest patches in Fray Jorge National Park. Data for
Aextoxicon punctatum only (dark bars) and for all other tree species pooled (white bars) are shown.
sprouting. Furthermore, 52% of all A. punctatum stems
sampled (n 5 705) were of vegetative origin. Vegetative
sprouting represented 460% of total stem density and
468% of total basal area in the smaller patches (F1–F3;
Table 2). The relative density of vegetative stems of A.
punctatum in each patch was negatively correlated with
the Berger–Parker index (Table 3). Snags comprised
415% of stems and 19% of the total basal area in the
smaller patches F1 and F2 while large patches generally
had o10% of stems and basal area as snags. Large
patches had greater numbers of smaller size, dead trees
under the canopy than smaller patches, where all dead
trees were found along edges (Table 2).
Age structure and growth patterns of A. punctatum
Across all patches, minimum ages estimated for A.
punctatum trees ranged from 25 to 213 years (n 5 196).
With the exception of F4, A. punctatum had similar age
structures in the patches, (Kruskal–Wallis H 5 9.39,
P 5 0.06, F4 excluded from analysis; Fig. 3). For A.
punctatum, we found a significant linear regression
between age and dbh [ln(age) 5 0.6435 ln(dbh)
1 2.2478, r2 5 0.77, F(1, 130) 5 434.4, Po0.01]. Thus, for
A. punctatum in FJNP dbh distributions were roughly
indicative of age structures.
Regeneration history of adult A. punctatum stems
(45 cm dbh) across all patches showed tree recruitment
in all 5-year intervals between 1860 and 1965 (Fig. 4a).
Recruitment peaks were recorded during 1925–1930
and 1950–1960 especially in F4 (Figs 3 and 4a). The
youngest tree dated was recruited in 1977, thus trees
o5 cm represent relatively frequent recruitment during
the last two decades. Based on age–dbh regressions,
most large individuals of A. punctatum (dbh41 m) in
the forest patches were probably recruited before 1810.
r 2007 The Authors
169
Fig. 3 Age distribution (stems 45 cm dbh) of Aextoxicon punctatum in six forest patches in Fray Jorge National Park. Sample sizes
(complete plus incomplete cores) are given in parentheses. Patches are named as in Table 1.
The recruitment date expected for the largest tree in the
sample was approximately 1760 (dbh 5 155 cm), about
240 years ago.
Radial growth patterns of A. punctatum showed several releases from suppression that suggest local disturbance at small scale (i.e. tree falls), which opened the
forest canopy, increasing the radial growth of previously suppressed trees. Trees tended to grow faster
in larger patches (1.4 mm yr1, patches F3–F6) than in
smaller patches (0.9 mm yr1, patches F1–F2) (Kruskal–
Wallis H 5 17.3, Po0.001). Although some trees
sampled produced sustained releases of 43 times than
the magnitude of previous growth, moderate releases
were more common than major releases (Table 5) and
were present in all 5-year intervals since 1870 to the
present (Fig. 4b). Releases comprising a large number of
trees in the patches studied occurred during the periods
1925–1930 and 1875–1880. From 1955 to the present, the
frequency of moderate releases declined relative to the
previous century (Fig. 4b). Growth releases were entirely
absent between 1850 and 1870, even though 410 trees
covered this time period. No differences were detected in
the number of releases recorded between patches (major
releases Kruskal–Wallis H 5 2.6, P 5 0.27; moderate releases, Kruskal–Wallis H 5 4.1, P 5 0.13).
The tree ring chronology for A. punctatum covered the
period from 1795 to 2002 (Fig. 4c). The chronology does
not show any obvious tendencies in radial growth,
except for large fluctuations around the mean in the
period 1830–1915. Fluctuations decreased towards the
present as sample size increased. Tree radial growth
declined slightly after 1900 (linear regression, r2 5 0.20,
F(1, 102) 5 12.73, Po0.01), a trend that became more
pronounced from 1950 to the present. During this latter
r 2007 The Authors
(a)
(b)
(c)
(d)
Fig. 4 (a) Recruitment frequency of Aextoxicon punctatum (stems 45 cm dbh) in each 5-year interval over the past 150 years in six forest
patches of Fray Jorge National Park (FJNP) (pooled sample from all patches). (b) Major and moderate radial growth releases recorded per
5-year interval in 100-year-old A. punctatum trees in six forest patches in FJNP (samples pooled); (c) tree-ring width chronology of A.
punctatum in FJNP (from all six patches). Continuous line represents radial growth departures from the expected mean value (horizontal
line). Dashed lines in (b) and (c) represent the sample size for each 5-year period; (d) rainfall departures (mm yr1) from the mean annual
rainfall calculated for instrumental records from 1876 to the present (horizontal line) in La Serena meteorological station (301S) about
50 km north of FJNP. Points and dotted lines indicate percentage of fog days during each year, estimated by the presence/absence of low
clouds in the forest area from daily records by Fray Jorge park guards.
period, tree growth was predominantly below the mean
(Fig. 4c). Some depressions of growth rates (0.5 unit
below the mean, i.e. 1959, and 1997–1998) were recorded. The greatest peak in radial growth since the
1920s occurred in 1952 despite the general trend toward
slower growth.
Correlations with climate
We found a weak correlation between ring width of A.
punctatum, rainfall and SOI (Fig. 5a). A significant,
positive correlation between RWI and the spring rainfall of the previous growing season (November) was
detected while a negative correlation was seen with late
winter rainfall (August) of the current year of growth
(Fig. 5a). We found a negative correlation between RWI
and SOI of winter of the current year (July). Quantitative analysis of fog influences (Fig. 5b) was not conducted due to the lack of consistent long-term fog
records but these data were plotted, as a reference,
relative to RWI and rainfall (Fig. 4d). The recruitment
pattern of A. punctatum during the past 175 years was
significantly correlated with the mean accumulation of
rainfall over the previous 5 years (Fig. 5c). Finally, SOI
was uncorrelated with observed periods of tree recruitment and growth releases.
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171
Fig. 5 (a) Correlation functions (Pearson’s r) between current year monthly rainfall, monthly Southern Oscillation index and tree ring
width of Aextoxicon punctatum for the past 100 years. (b) Monthly variation in rainfall (mm, open bars) and proportion number of fog
days (line) as in Fig. 4d. (c) Cross-correlation function between the tree recruitment time series (total number of live trees recruited per
year between 1875 and 1980) and total rainfall accumulated during the previous 5 years. Simple prewhitening of all time series was done
before computation (see ‘Materials & methods’). Dotted lines in (a) and (c) represent the 95% confidence intervals for the correlations.
r 2007 The Authors
Discussion
Regeneration and patch structure
A clear pattern emerges from the analysis of tree
regeneration. Seedling densities of A. punctatum were
higher in the larger and vertically more structured
patches (meaning higher heterogeneity in canopy
classes). The same pattern held for other tree species,
with the exception of M. correifolia, which had a greater
density in smaller patches. Smaller patches in FJNP
have greater susceptibility to soil and litter desiccation
due to increased edge effects (Barbosa, 2005) and more
herbivore abundance (del-Val et al., 2007), which may be
responsible for the lower seedling and juvenile densities. The importance of vegetative reproduction as a
form of persistence under stress conditions has been
reported in a diversity of ecosystems (Bond & Midgley,
2001), including semiarid, fog-dependent forests
(Hildebrandt, 2005). In the case of A. punctatum,
natural regeneration coupled with high vegetative
reproduction is likely to ensure its persistence in
medium and large forest patches (42 ha). Persistence
of A. punctatum is less certain in small patches
(o2 ha) because of limited seedlings densities
(Table 3, Fig. 2).
The relative success of seedlings in reaching juvenile
size appears to be dependent on forest patch
structure. Juvenile densities of A. punctatum showed
no relationship to patch size, but heterogeneity of
vertical structure was significantly correlated with
juvenile densities as well as with vegetative reproduction of A. punctatum (Table 3). Because vertical structures such as trunks, limbs, branches and leaves are
responsible for fog interception and water drip within
the forest (Kerfoot, 1968; Dawson, 1998; Weathers et al.,
2001), patch structure may play an important role
in increasing the potential for fog capture. A. punctatum
is the dominant canopy species, and thus is likely
responsible for much of the current fog interception.
To the extent that this system depends on water
inputs from fog, regeneration and persistence of other
tree species in forest patches may be dependent on
A. punctatum’s continued successful regeneration and
growth. These results point to the importance of forest
structure in recruitment and suggest an important
role of fog and water drip, whose delivery amounts
are dependent on vertical structure (Weathers, 1999;
Weathers et al., 2001).
Disturbance and regeneration of A. punctatum
A continuous regeneration mode best represents the
pattern of recruitment of A. punctatum in forest patches
of FJNP over the past 250 years. Despite some exceptions, such as less establishment in small patches during
the past 50 years, most forest patches showed fairly
continuous tree regeneration, with some moderately
marked recruitment pulses (especially in F4). This regeneration pattern has resulted in an uneven-aged
canopy of A. punctatum. Such pattern of recruitment
has not been previously reported in A. punctatumdominated coastal forests. A single-cohort population
was reported in another fog forest on Santa Ines hill
(311S), about 200 km south of Fray Jorge, suggesting that
A. punctatum became established there following standdisrupting disturbance (Le Quesne et al., 1999). Whether
such disturbance was climatic or human related is
unknown. Such large disturbances, affecting entire
patches, were not apparent in the FJNP forest. Fire scars
were absent from trees in all patches. Small canopy
disturbances are shown by frequent moderate growth
releases in 1875–1880 and 1920–1930, as suggested by
coincident release chronologies of various trees (Fig.
4b). Although Lorimer & Frelich (1989) caution against
interpretation of releases in environments with prolonged dry seasons, the lack of strong correlation of
RWI with rainfall (discussed below) supports the idea
that these are disturbance-related releases. Moderate
releases imply the occurrence of circumscribed, lowintensity disturbances, such as small canopy openings
arising from individual tree falls (Lorimer & Frelich,
1989). Such disturbances were present in all 5-year
intervals from 1870 to present suggesting a relatively
unstable canopy, which may be related to shallow soils
and root systems. The predominance of low-intensity
disturbance suggests that individual tree-falls could
happen at any time as a consequence of windstorms,
especially on steep slopes. There was no evidence of
significant canopy disturbance in the last 50 years,
suggesting either a less windy climate or a reduction
of spatially discrete human impact after the creation of
FJNP in 1941.
Climate influences on tree regeneration and radial growth
The tree ring chronology for A. punctatum (Table 5)
showed strong interannual fluctuations of tree growth,
which may reflect variable local environmental conditions and past disturbance (Fritts, 1976). Only a small
proportion of the variation in tree ring widths was
explained by differences in annual rainfall (r 5 0.2,
Fig. 5a). Similar results have been reported for another
tree species (Prosopis chilensis) characteristic of semiarid
vegetation near our study area (Holmgren et al., 2006).
In the case of Prosopis, lack of correlation with rainfall is
related to its deep tap root dependence on deep soil
water sources. These results, however, are in contrast
r 2007 The Authors
Table 5 Radial growth patterns of Aextoxicon punctatum trees
in six forest patches in FJNP
Chronology statistics
Sample size (number of trees)
Period
Mean radial growth (mm/year) SE
Average mean sensitivity
Standard deviation
First order autocorrelation
Mean correlation between trees
Dendroecological statistics
Sample size (number of trees)
Maximum radial growth (mm/year)
[95% percentile]
Maximum sustained release*
Moderate release frequency
(releases/100 years)w
Major release frequency
(releases/100 years)w
28
1795–2002
0.94 0.24
0.31
0.35
0.29
0.33
45
15.3 [3.15]
9.4
2.2
0.7
Releases defined after Lorimer & Frelich (1989).
*Average growth rate for the 15 years period following the
release event, divided by the growth rate for the 15 years prior
to release.
wRelease frequencies for the past 100 years were calculated
averaging the number of growth releases recorded for each
tree and dividing by tree age.
SE, standard error of the mean; FJNP, Fray Jorge National
Park.
with the high correlations between radial growth and
rainfall (Pearson 40.4) observed in Austrocedrus chilensis, further south in the central Chilean Andes (Le
Quesne et al., 2006), where annual rainfall (ca.
400 mm yr1) is greater than in our study area and
oceanic fog is absent. At FJNP, foggy days are more
numerous when rainfall is minimal (Fig. 5b), and fog
inputs as well as water drip in 2003–2004 was greatest
in the austral spring and summer (Barbosa, 2005; delVal et al., 2006).
Because rain contributes only a portion of the tree
water budget in Fray Jorge forest, then fluctuations in
rainfall are unlikely to be the major determinants of tree
growth, although the seasonality of water inputs is
likely to be important as well (Weathers, 1999). While
reduced radial growth of A. punctatum in the last
century might result from the gradual decrease in
average annual rainfall reported for semiarid Chile
(Quinn & Neal, 1983; Le Quesne et al., 2006), only late
winter rainfall in the previous year was positively
correlated with RWI over the last 100 years (Fig. 5a).
Because of the high likelihood that A. punctatum growth
is water limited in this region (del-Val et al., 2006), and
not light-limited as it is farther south (Donoso et al.,
1999), slower tree growth in the past 50 years may be
173
the result of a decrease in late winter rain or total water
input (i.e. rainfall plus fog). The lack of long-term fog
data does not allow us to assess fog influences on longterm patterns of tree growth relative to other phenomena such as lagged responses to habitat fragmentation
(Vellend et al., 2006). However, the forest structure
and recruitment data presented here and earlier work
in these forests (Barbosa, 2005; del-Val et al., 2006)
suggests that a relationship with fog variability could
be present.
Climate in semiarid Chile is connected to SOI patterns. Rainy years are generally associated with the
positive phase of ENSO cycles (Montecinos & Aceituno,
2003) and changes in cloud cover and height are also
possible due to a higher subsidence inversion during
strong ENSO events (Rutllant et al., 2003). Some decreases in radial-growth (i.e. 1997 and 1845) could be
partially explained by the influence of strong ENSO
events (Ortlieb, 1994; Montecinos & Aceituno, 2003).
However, we currently do not know how this variability in SOI may affect coastal fog input to coastal
mountain forests. The recruitment pattern of A. punctatum was positively correlated with the accumulation of
rainfall during the previous 5 years (Fig. 5c), and RWI
was positively related to the previous year’s late winter
rainfall (Fig. 5a). However, neither of these patterns are
sufficient for us to be able to detect the effects of
reductions in rainfall on tree recruitment, such as
characteristic drought conditions of La Niña episodes
during the negative phase of ENSO (Montecinos
& Aceituno, 2003; Fig. 4a). Clearly there is a need
o understand the role of ENSO cycles in fluctuations
of fog and rain because it might influence the recruitment patterns of A. punctatum on subdecadal time
scales (e.g. observed gaps in the recruitment patterns
of A. punctatum over the last century, Fig. 4a). A combined index of fog plus rain could be useful in understanding growth patterns of A. punctatum in this
semiarid region.
Decrease in winter rainfall (60–80% of current
amount) has been predicted in the study area for year
2100 (DGF & CONAMA, 2006), but changes in fog
frequency and fog base over time are uncertain (e.g.
Pounds et al., 1999; Nair et al., 2003; Sperling et al., 2004).
Fog frequency may vary in response to changes in sea
temperature, the height of the inversion layer (Cereceda
& Schemenauer, 1991; Cereceda et al., 2002) or wind
direction. These changes in precipitation, fog frequency
and water content may affect the position, size and
shapes of forest patches via influences on tree growth
and recruitment (del-Val et al., 2006). Because these
water sources may respond to different climatic drivers,
it is especially important that multiple dimensions of
climate change be considered.
r 2007 The Authors
Forest persistence assessment
Overall, our findings indicate that A. punctatum has
recruited consistently in these forest patches for at least
250 years, despite large fluctuations in rainfall driven by
ENSO cycles, which have characterized this region for
the past millennia (Maldonado & Villagrán, 2002). No
evidence for decreased recruitment following declining
rainfall (Quinn & Neal, 1983; Le Quesne et al., 2006) in
the last century was found in large patches, but recruitment in small patches may be more susceptible because
of their propensity for drying. Although regeneration
patterns of A. punctatum are sensitive to patch size and
canopy structure, a continuous regeneration mode has
prevailed over the past 150 years. Tree radial growth
and establishment success of A. punctatum were weakly
related to rainfall, but may be responsive to variability
in fog input or to total fog and rain input among years.
Nevertheless, the complex interplay between rain and
fog water inputs and their direct bearing on tree growth
patterns over long time periods still needs to be elucidated. A better understanding of how changes in climate may affect the timing and distribution of water
sources and the development of models predicting fog
trends will be important in assessing the ability of these
forests to persist in the face of climate change. Vertical
heterogeneity of patches has favorable effects on the
recruitment success of A. punctatum, likely because of
the positive influence on fog interception. Thus, preservation of forest structure may be critical to patch
hydrology under any future climate scenario. In fact,
complex patch structure may compensate at the landscape scale for declining long-term trends in rainfall, as
long as fog capture remains high. Further research of
FJNP should prioritize the maintenance of long-term
records of fog and rainfall in order to make reasonable
predictions about the future of the forest and tree
growth patterns. Fog modeling; in particular, needs to
be better incorporated in current global or regional
climate models.
Acknowledgements
CONAF kindly gave permission to work in FJNP. We thank Todd
Dawson for his intellectual contribution in the beginning of this
project; the people involved in fieldwork; N. Carrasco, M. P. Peña
and A. Rivera for laboratory assistance; P. Aceituno for SOI data;
M. Masiokas for the tree-ring analysis routine and J. Barichivich
for crossdating assistance. A. Hildebrandt, S. Luna, and two
anonymous reviewers provided useful comments. Financial
support was provided by grants from DAAD (to A. G. G.),
Andrew Mellon Foundation (to O. B.), BIOCORES (Contract
ICA 4-CT-2001-10095, funded by EC, INCO IV program), Millennium Scientific Initiative (CMEB, IEB P02-051-F ICM, ICM
P05-002), FONDAP-FONDECYT 1501-0001 to CASEB; NSF (International Americas Program, INT–0313927). P. A. M. was a
Sabbatical Fellow at the National Center for Ecological Analysis
and Synthesis (NSF center, Grant #DEB-072909, University of
California, Santa Barbara). This work is a contribution to the
research programs of the Institute of Ecosystem Studies and
Senda Darwin Foundation. Other than the first and last author,
order of authorship is alphabetical.
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Page 1
Global
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Biology
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Cover: Fog covers an isolated patch of temperate rainforest at
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Global Change Biology

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