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Ecosystems
ISSN 1432-9840
Ecosystems
DOI 10.1007/s10021-012-9574-7
Persistence of the Slow Growing Conifer
Pilgerodendron uviferum in Old-Growth
and Fire-Disturbed Southern Bog Forests
Jan R.Bannister, Pablo J.Donoso &
Jürgen Bauhus
1 23
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Persistence of the Slow Growing
Conifer Pilgerodendron uviferum
in Old-Growth and Fire-Disturbed
Southern Bog Forests
Jan R. Bannister,
1
* Pablo J. Donoso,
2
and Ju
¨rgen Bauhus
1
1
Institute of Silviculture, Faculty of Forest and Environmental Sciences, Albert-Ludwigs University Freiburg, Tennenbacherstrasse 4,
79106 Freiburg, Germany;
2
Institute of Silviculture, Faculty of Forest Sciences and Natural Resources, Universidad Austral de Chile,
Casilla 567, Valdivia, Chile
ABSTRACT
In spite of the extensive area of bogs in the
southern cone of South America, there have been
very few studies on structure and dynamics of
conifer bog forests in this region. Previously, it has
been assumed that in the absence of intensive
disturbance, the dominant conifer Pilgerodendron
uviferum (D. Don) Florin would be replaced
through other angiosperm species. Here we
hypothesized (a) that this conifer can persist
without intensive disturbances and develop into
old-growth forests with continuing regeneration
and (b) that high-severity disturbances through fire
threaten its local persistence. To test this hypothe-
ses, we analyzed diameter and age structure, foliar
and soil nutrient levels and the light environment
of old-growth and fire-disturbed P. uviferum stands
on Chiloe
´Island (43ºS) in North Patagonia. Lon-
gevity (>880 years), extremely slow growth
(<1 mm diameter per year) and tolerance to shade
and stress are the main mechanisms of P. uviferum
persistence in nutrient-poor and waterlogged con-
ditions. Hence, old-growth P. uviferum forests are
not a transitional phase in forest succession and
may be maintained in the landscape for many
centuries or millennia. However, in fire-disturbed
stands, live trees of the species were rare and
regeneration negligible, showing that high-severity
fires can eliminate the species from parts of the
landscape, where neither propagules nor seed trees
survive. This underpins the importance of biologi-
cal legacies such as seed trees for the recovery of
disturbed sites, and points to the need for active
restoration approaches to restore fire-degraded
P. uviferum forests.
Key words: Chiloe
´Island; Forest dynamics; Light
availability; N/P ratio; Persistence mechanisms;
Sphagnum.
INTRODUCTION
Boreal and artic wetlands cover almost 3.5 mil-
lion km
2
of terrestrial land surface (Shaw and
others 2003). Owing to the disequilibrium between
carbon fixation and decay processes in these eco-
systems, they accumulate vast quantities of peat. It
is estimated that one-third of the global carbon pool
is stored in northern peatlands, which currently
Received 28 February 2012; accepted 3 June 2012
Author Contributions: Jan R. Bannister conceived, designed and per-
formed the research, analyzed the data and wrote the paper. Pablo J.
Donoso helped with the design of the research and writing. Ju
¨rgen
Bauhus conceived and designed the research and helped with data
analysis and writing.
*Corresponding author; e-mail: jan.bannister@waldbau.uni-freiburg.de
Ecosystems
DOI: 10.1007/s10021-012-9574-7
2012 Springer Science+Business Media, LLC
Author's personal copy
function as a net sink for atmospheric carbon
(Gorham 1991). Although the majority of peat-
lands and wetlands are concentrated in the boreal
zone (3.5 million km
2
), millions of ha of these
ecosystems are also found in subantarctic areas in
parts of Australia, New Zealand, and southern Chile
and Argentina (Shaw and others 2003).
Paludification, the accumulation of peat moss
over formerly terrestrial soils (Lavoie and others
2005), increases soil moisture, reduces soil tem-
perature and nutrient availability, and alters the
vertical distribution of roots to an extent that the
productivity of bog forests may decline by 50–80%
after 100 years of succession (Simard and others
2007). However, some tree species, in particular
some conifers can grow, albeit very slowly, and
persist on these unfavorable sites (Bond 1989;
Coomes and others 2005). Most information for
these types of ecosystems relates to bog forests
dominated by conifers such as Picea mariana in the
boreal zones of Canada (in example, Fenton and
others 2005; Simard and others 2007; Moroni and
others 2010)orPicea abies in Scandinavia (in
example, Ho
¨rnberg and others 1995; Kuuluvainen
and others 2002). In spite of the extensive area of
bogs in the southern cone of South America, there
have been very few studies that have investigated
structure and dynamics of the bog forests occurring
there (in example, Szeicz and others 2003).
In contrast to other conifers of the southern cone
of South America that grow on terrestrial sites
(Araucaria araucana, Austrocedrus chilensis, Fitzroya
cupressoides), Pilgerodendron uviferum forests are
found in landscapes and on substrates shaped by
glaciation, on acidic and poorly drained soils and
wet sites with high annual rainfall (2,500–
8,000 mm), often associated with Sphagnum bogs
(Lara and others 2006). Pilgerodendron uviferum
(D. Don) Florin (Cipre
´s de las Guaitecas) is an en-
demic cupressaceae of Patagonia that covers an
area of more than 1 million ha from 40Sto55S,
making it the southernmost conifer in the world
(Martı´nez 1981). It is considered a long-lived spe-
cies of slow growth that may live for more than
850 years (Aravena 2007) and has remarkably
decay-resistant wood (Solı´s and others 2004).
These P. uviferum bog forests are some of the least-
studied coastal temperate rainforests in southern
South America (Holz and Veblen 2009) and there is
practically no information about their dynamics, in
particular not in the old-growth stage (Bannister
and others 2008).
Succession in P. uviferum bog forests has been
related to an improvement in soil drainage condi-
tions. It has been hypothesized that establishment
pulses of the species occur in open sites with
waterlogged soils and when seed is available (Cruz
and Lara 1981). Further it has been proposed that
in the absence of disturbances, as the soil drainage
improves, establishment of P. uviferum will gradu-
ally decline and it may be replaced by more shade-
tolerant angiosperm species (Cruz and Lara 1981;
Bannister and others 2008). In accordance with
this commonly held view, old-growth stands of this
species would represent only a transitional phase in
forest succession. According to the ‘‘slow seedling
hypothesis’’ (Bond 1989), slow-growing gymno-
sperms, which are poor competitors in relation to
angiosperms in productive habitats, are restricted
to those areas, where growth of angiosperms is
reduced, for example, on poorly drained and
nutrient-poor soils. Some mechanisms of conifers
that have been postulated to explain conifer per-
sistence on unproductive sites are slow growth,
longevity, reduced stature, long-leaf life spans and
some morphological and biochemical adaptations
(Crawford and others 2003; Coomes and others
2005; Gaxiola and others 2010). Against this
background, our first hypothesis is that the conifer
P. uviferum can persist in bog forests in the absence
of intensive large-scale disturbances. This is the
pre-condition for the development of old-growth
forests in which this species maintains its domi-
nance through continuing regeneration. To address
this hypothesis, we examined how regeneration of
P. uviferum can persist under conditions of low light
and nutrient availability, typical for undisturbed
conditions.
However, little is known about the disturbance
forces that shape P. uviferum forests. Locally,
changes in water table due to tectonic movements
can be important (Szeicz and others 2003). In the
high-rainfall environment of coastal Patagonia,
fires are most likely restricted to human activity,
even though individual trees may be struck
by lightning (Holz and Veblen 2009). Because
P. uviferum trees are commonly of low stature and
deep rooted, they are not easily uprooted by wind
storms. In this situation, there may be long periods
of time without significant disturbances. For
example, a pollen sequence on the Taitao peninsula
(46ºS) showed a period of approximately
10,000 years after the last glaciation with a relative
continuous presence of P. uviferum (Lumley and
Switsur 1993). However, following the arrival of
Euro-Chilean settlers in the eighteenth and nine-
teenth centuries, there has been a considerable
increase in fire frequency in North Patagonia (Holz
2010). The historical utilization of these forests for
fence posts, railroad sleepers, and boat and building
J. R. Bannister and others
Author's personal copy
construction has caused the destruction of exten-
sive areas of Pilgerodendron forest (‘‘cipresales’’)
through broad-scale burning to facilitate access to
the trees (Lara and others 2006; Bannister and
others 2008). Because there has been no co-evo-
lution of the species with fire disturbances, it lacks
obvious traits to withstand fires (in example, thick
bark) like other conifers of Chile (in example,
Araucaria araucana, Burns 1993). The historic fires
have degraded P. uviferum forests to such an extent
(Cruz and Lara 1981; Bannister and others 2008)
that the species has been classified by the IUCN as
vulnerable (Walter and Gillet 1998) and has been
included in Appendix I of CITES (Hechenleitner
and others 2005). Therefore it is not surprising that
most studies about this species have focused on
disturbed forests and only very few have investi-
gated old-growth stands (Cruz and Lara 1981;
Bannister and others 2008).
In this context, our second hypothesis is that
large-scale fire disturbances threaten the local
persistence of the species. To answer our two
hypotheses, we analyzed forest structure, the light
environment and foliar nutrients of P. uviferum and
its companion angiosperm species in old-growth
and fire-disturbed P. uviferum stands. We expected
that this information will provide an ecological
basis for future conservation and restoration strat-
egies for P. uviferum forests.
METHODS
Study Area and Forest Types
‘‘Tantauco Park’’ (43º10¢S and 74º05¢W) on
Chiloe
´Island, North Patagonia, was selected as a
study site because it contains the majority of eco-
logical site types in which Pilgerodendron uviferum
grows and has both old-growth and fire-disturbed
forests on comparable sites. In the remote area,
disturbed sites that have not been salvage-logged
can be found. This allowed us to investigate the
influence of fire-disturbance separately from addi-
tional effects that subsequent logging might have
had. Field sites were located in old-growth and
disturbed forests of the ‘‘Rı´o Zorra’’ valley and in
disturbed areas around Lake Chaiguata and Cha-
iguaco. Southern Chiloe
´, including the area of
Chaiguata lake, was burned in an extensive fire
between 1942 and 1944 (Bannister and others
2008; Holz 2010).
Southern Chiloe
´has a cool-temperate climate
with strong oceanic influence with a mean annual
temperature of 10ºC, and high annual precipitation
that can reach up to 6,000 mm in some places (di
Castri and Hajek 1976;Pe
´rez and others 2008). The
landscape in the study area has been shaped by the
last glaciation (glacial-postglacial transition ca.
13,000 year. BP), which created a mix of hills from
glacial till and shallow valleys, over Pre-Cambrian
and Tertiary Metamorphic rocks with extremely
acidic, poorly drained soils with Gley horizons
(Villagra
´n1988). Altitudes range between 50 and
280 m above see level. In depressions, sites are
mostly covered by Sphagnum bogs and cushion
plants, and where drainage is better, coniferous
species like P. uviferum and Podocarpus nubigena or
hardwood species like Tepualia stipularis, Nothofagus
nitida, Nothofagus betuloides, Drimys winteri, and
Weinmannia trichosperma dominate the vegetation.
For the purpose of this study, P. uviferum forests
in the study area were classified into undisturbed
and disturbed bog and upland forests (Figure 1).
Undisturbed bog forests corresponded to old-
growth stands located in flat areas on raised peat
bogs (Sphagnum and cushion plants), where
P. uviferum was accompanied by other tree species.
The disturbed bog forests selected for this study had
been burned but subsequently not salvage-logged.
These stands occurred also on peat bogs and were
characterized by large quantities of standing dead
trees of P. uviferum with some regrowth (post-dis-
turbance cohorts) of mostly other tree species.
Undisturbed upland forests corresponded to old-
growth stands on moraine deposits with till sub-
strate and hence better drainage when compared
to bog forests. These stands were dominated by
P. uviferum and T. stipularis, where the latter species
creates very complex structures owing to its hori-
zontal growth habit. Finally, selected disturbed
upland forests had also been burned but not sal-
vage-logged and were characterized by dead trees
of P. uviferum and T. stipularis with some regrowth
of other tree species.
Field Methods
In 2009, for each of the four forest categories, four
replicate stands were selected to capture the vari-
ation in conditions, and one circular plot of 500 m
2
was established within each replicate. All trees
(‡5 cm diameter at 1.3 m height, dbh) within these
plots were identified at the species level and mea-
sured for dbh, diameter at 0.3 m height (d0.3), and
total height. Because of the lack of an effective
method to inventory the stems of T. stipularis
(horizontal growth), they were excluded from the
inventory. This makes the inventory incomplete,
Persistence of Pilgerodendron uviferum
Author's personal copy
but it does not influence the analyses and inter-
pretation of ecological processes in this study. To
determine tree age, one or two increment cores
were obtained at the lowest possible stem height
(ca. 30 cm) from a sample of up to three living and
dead trees for each tree species and 6 dbh classes if
possible (dbh classes: 5–10, 10–20, 20–30, 30–40,
40–50, >50 cm), corresponding to 392 cores in
total (268 trees). Although we collected increment
cores of other species in addition to P. uviferum,
these cores were of low quality or contained rotten
wood and therefore could not be used in a consis-
tent enough way for determining tree ages.
To assess regeneration, four transects of 25 m
length and 2 m width (total area = 200 m
2
) were
located in radial direction from the center of
each circular plot towards each hemispherical
direction (N, S, W, E). For each transect, all seed-
lings (<1.3 m height) and saplings (<5 cm dbh
and >1.3 m height) were identified by species and
their height was recorded. In addition, 115
P. uviferum seedlings were collected for age deter-
mination from stands located in the forests types.
Light conditions within stands (% photosyn-
thetic photon flux density, %PPFD) were measured
based on the one-point overcast sky condition
method (sensu Parent and Messier 1996). To
describe light conditions at the plot level, two 24 m
long transects were located from the plot center
toward the north and south and every 2 m a light
measurement at 0.3 and 1.3 m height was taken
along these transects. Relative %PPFD change with
height was calculated according to the formula:
L1 L2ðÞ=L1½100;
where L1 is the %PPFD at 0.3 m height and L2 is
%PPFD at 1.3 m height. To assess the relationship
between light and growth of regeneration, we
measured %PPFD immediately above the termi-
nal shoot of seven seedlings per tree species of
P. uviferum, T. stipularis, N. nitida, N. betuloides,
P. nubigena, and D. winteri per plot. In addition,
length of the last annual shoot, total height, and
root collar diameter (rcd) were determined for
these seedlings. Leaves or needles from the top of
these seedlings were collected for nutrient analysis.
Figure 1. Forest types of P. uviferum forests defined for the study area. Aold-growth, undisturbed bog forests. Bold-
growth, undisturbed upland forests. Cdisturbed bog forests, and Ddisturbed upland forests.
J. R. Bannister and others
Author's personal copy
Finally, five soil samples were collected in each
plot following a systematic design. At each sample
point, the thickness and pH of the organic and
mineral layers were measured. The five samples
were bulked to form one composite sample per plot
for the organic and mineral layer, respectively, for
nutrient analysis.
Age Estimation of Trees and Seedlings
Tree cores were mounted and sanded following
standard procedures (Stokes and Smiley 1968). In
cases where tree cores did not reach the pith, the
number of rings to the tree center was estimated.
If cores passed close to the pith, so that the arcs of
the inner rings were visible, the number of rings
to the center was estimated using the correction
method of Duncan (1989). To estimate the
number of missing rings on cores that did not
show the arc of inner rings, we extrapolated
the mean radial growth of the 50 innermost rings
(or all rings for cores with <50 rings) to the
remaining radius to the center or pith (Rozas
2003). We selected three types of cores from liv-
ing trees (total 149 cores): (1) those that reached
the pith (n= 63), (2) those where the measured
age was more than 75% of the estimated age by
the Duncan method (n= 69), and (3) partial
cores, where the length of the core was greater
than 50% of total radius of the tree (n= 17). To
estimate the radius of the tree at coring height, a
linear regression between dbh and diameter at
0.3 m was used (r
2
= 0.866; P<0.001). To pre-
dict age from tree size, a single linear regression
model with dbh, forest type and their interaction
(dbh*forest_type) as explanatory variables was
developed for the 149 cores (Figure 2). Because
the interaction component of the model was sig-
nificant (P£0.05) different slopes and intercepts
for each forest type were used. The model pro-
vided a high fit (r
2
= 0.854; P<0.001) and was
used to estimate the age structure of each forest
type (see functions in Figure 2).
Age estimation of seedlings was difficult because
the root collar, which represents the true age, was
not always easily identifiable. Because the ground
surface on bogs moves upwards with the growth of
moss and seedlings develop new adventitious roots
below this surface, the section of seedling stems
above the surface may not be the original root
collar. To determine the age of P. uviferum seed-
lings, we marked the estimated location of the root
collar on stems of all collected P. uviferum seedlings.
Stems were cut with a scalpel at the estimated
location of the root collar and also at 1 and 2 cm
distance in either direction of the stem, analogous
to the method used by Niklasson (2002). Depend-
ing on the length of the stem section, which might
have contained the true root collar, additional cuts
were made at the upper and the lower end of
this section. All stem sections were sanded and to
improve the visibility by the counting of rings, a
phloroglucin-dilution was applied to the wood
surface. The oldest section of the stem was recorded
as seedling age.
Figure 2. Relationship between size and age of P. uviferum trees. Linear regression model of the form: age dbh +
forest_type + dbh:forest_type (r
2
= 0.854; P<0.001). Abog P. uviferum forests (BF-D: age = 18.614 + 3.551*dbh; BF-
UD: age = 137.081 + 6.553*dbh) and Bupland P. uviferum forests (UF-D: age = 34.998 + 1.392*dbh; UF-UD:
age = 88.091 + 5.873*dbh). BF-D, BF-UD disturbed and undisturbed bog forests. UF-D, UF-UD disturbed and undisturbed
upland forests.
Persistence of Pilgerodendron uviferum
Author's personal copy
Nutrient Analyses
Soil samples were dried before removing roots and
coarse woody fragments, and then passed through
a 2-mm mesh sieve. The fraction smaller than
2 mm was used for analyses. Cation exchange
capacity (CEC) and base saturation (%) of mineral
samples were determined after extraction with 1 M
NH
4
Cl (Weinzierl and Dietze 2000) using Induc-
tively Coupled Plasma-Optical Emission Spectros-
copy (ICP-OES), (Spectro, Kleve, Germany).
Organic samples, forest floor material as well as leaf
and needle samples, were finely ground in a swing
ball mill (MM301, Retsch, Germany) and digested
with concentrated nitric acid (Ko
¨nig 2005). Ele-
ment concentrations in the digests were also
quantified with ICP-OES. Total organic C and
total N in mineral soil and organic material were
determined using a Leco TruspecCN analyser
(St. Joseph, MI, USA).
Data Analyses
Analyses of normality and homogeneity of variance
for all variables (concerning stand structure, age,
growth, irradiance, and nutrient elements) were
done with Shapiro–Wilk W, Kolmogorov–Smirnov,
and Levene tests. Data for stand structure, irradi-
ance within plots and nutrient elements exhibited
heteroscedascity or non-normal distributions even
after various transformations. Thus we used for
comparisons of pairs of groups the non-parametric
Mann–Withney U-test and for significant differ-
ences among forest types, species and/or soil types,
Kruskal–Wallis tests were performed. Where sig-
nificant differences were found, further analyses
for differences were done with post hoc compari-
sons based on Mann–Whitney U-tests and the
Bonferroni method. To identify effects of forest
types and tree species on the element concentra-
tions of needles and leaves, instead of a two-way
ANOVA, the Scheirer-Ray-Hare extension of the
Kruskal–Wallis test (Sokal and Rohlf 1995) was
used followed by the same post hoc comparisons as
above. Analysis of leaves of those individuals of the
two Nothofagus species, which could be clearly
identified, showed that there were no significant
differences in their nutrient concentrations.
Therefore, leaves of N. nitida and N. betuloides were
grouped in one ‘‘Nothofagus’’ group for statistical
analysis.
Pearson’s correlation and linear regressions were
used to test for relationships between shoot growth
and %PPFD and between age and root collar
diameter of P. uviferum seedlings. In the latter case,
the regression model was done with rcd, forest type
and their interaction (rcd*forest_type) as explana-
tory variables, and age as response variable. All
statistical analyses were performed using the SPSS
v.17.0 package (SPSS, Chicago, Illiniois, USA) and
the R package (R Development Core Team 2010).
RESULTS
Soils
Across all forest types, the soil profile was charac-
terized by a thick organic layer of up to 44 cm
(Table 1). There were no significant differences in
organic layer thickness between bog and upland
forest types (P= 0.073). However, undisturbed
sites had significantly thicker organic layers than
disturbed sites (P= 0.021). There were no differ-
ences in chemical soil properties between the forest
types (Table 1). The C/N values were similar in
organic layers and mineral soil and ranged between
19.7 and 26.7. The phosphorus content in the
organic layer was very low as reflected in very high
C/P and N/P values (807–1,353 and 33.9–53.3,
respectively).
Forest Structure
Because stand structure variables presented high
range values within forest types, there were almost
no significant differences between types (Table 2).
However, bog and upland forests were character-
ized by trees of low stature and small diameters and
height and diameter of trees were higher in the
undisturbed sites, especially in upland stands
(Table 2). All undisturbed stands were dominated
by P. uviferum as indicated by its contribution to
stand density and basal area. The basal area in
disturbed stands was dominated by dead P. uviferum
trees (snags) and a secondary forest stratum dom-
inated by D. winteri, N. nitida,N. betuloides, and W.
trichosperma. P. uviferum was infrequent in disturbed
stands and completely absent in some. Neverthe-
less, in plots of disturbed bog forests with presence
of live P. uviferum, the species occurred at higher
density and basal area (Table 2).
In undisturbed forests dominated by P. uvife-
rum, the species occurred in all diameter classes
(Figure 3c, d). In undisturbed bog forests, the
diameter distribution of P. uviferum followed a
negative exponential curve (J-shaped). Other spe-
cies like N. betuloides,N. nitida and P. nubigena oc-
curred only in smaller diameter classes and with
low densities. In undisturbed upland forests, the
diameter distribution of P. uviferum was flat and
extended to very large diameters of up to 95 cm
J. R. Bannister and others
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(Figure 3). N. nitida was the second species in
importance, with slightly more individuals than
P. uviferum in small and medium size classes. Other
species like D. winteri,N. betuloides and P. nubigena
were also present but with lower density and in
smaller diameter classes. Weinmannia trichosperma
was absent in both undisturbed types. The diam-
eter structure of dead individuals of P. uviferum
in the disturbed forests was similar to that of live
trees in undisturbed forests (Figure 3). However,
the regrowth component in disturbed bog and
upland forests was dominated by D. winteri and W.
Table 1. Soil Properties of the Organic and Mineral Layer in Each Forest Type
Forest type
BF-D BF-UD UF-D UF-UD
Organic layer (n=4) (n=4) (n=4) (n=4)
Depth (cm) 19.0 (±2.85)
a
30.9 (±8.95)
a
25.3 (±7.55)
a
31.3 (±9.46)
a
pH 4.42 (±0.16)
a
4.22 (±0.22)
a
4.57 (±0.17)
a
4.50 (±0.29)
a
C/N 22.49 (±1.74)
a
25.48 (±5.00)
a
23.74 (±1.96)
a
25.16 (±2.27)
a
C/P 872.7 (±121.4)
a
1,351.9 (±367.2)
a
806.7 (±202.3)
a
930.3 (±246.4)
a
N/P 38.97 (±6.57)
a
53.27 (±12.7)
a
33.91 (±7.76)
a
36.71 (±8.63)
a
Mineral layer (n=3) (n=4) (n=3) (n=4)
pH 5.06 (±0.19)
a
4.69 (±0.20)
a
4.96 (±0.26)
a
5.07 (±0.39)
a
C/N 26.65 (±1.38)
a
25.43 (±6.87)
a
19.71 (±4.24)
a
24.19 (±3.35)
a
CEC (lmol c g
-1
) 52.73 (±12.28)
a
84.96 (±31.60)
a
73.79 (±8.96)
a
37.91 (±10.63)
a
Base saturation (%) 13.26 (±2.06)
a
11.94 (±5.24)
a
11.95 (±5.22)
a
16.31 (±2.89)
a
BF-D, BF-UD disturbed and undisturbed bog forests, UF-D, UF-UD disturbed and undisturbed upland forests. Values in brackets represent standard deviations. For each
layer, values sharing the same letters in superscript were not significantly different at P £0.05.
Table 2. Stand Variables for the Four Different Forest Types
Forest type
BF-D BF-UD UF-D UF-UD
Living trees (P. uviferum)
Mean Dbh
1
(cm) 7.1–16.8
a
10.1–24.9
a
12.0
a
21.5–34.2
a
Mean H
1
(m) 4.9–7.1
a
3.5–9.3
a
5.9
a
7.7–16.6
a
Density (N ha
-1
) 0–680
a
0–75.6
a
420–1,060
a
63.4–85.5
a
0–220
a
0–16.9
a
160–820
a
21.6–70.7
a
(%)
Basal area (m
2
ha
-1
) 0–2.9
a
0–60.5
a
9.9–24.3
a
66.8–96.6
a
0–2.8
a
0–23.3
a
13.0–38.2
a
54.3–81.5
a
(%)
Living trees (other tree species)
Mean Dbh
1
(cm) 7.8–10.0
a
7.9–12.5
a
7.7–9.7
a
13.5–21.7
a
Mean H
1
(m) 3.6–4.1
a
3.4–6.2
a
3.1–4.9
a
6.7–11.0
a
Density (N ha
-1
) 0–220
a
160–420
a
160–1,080
a
320–580
a
Basal area (m
2
ha
-1
) 0–1.9
a
0.9–6.6
a
0.8–9.3
a
8.3–14.2
a
Observed Ages (P. uviferum)
2
Dead trees (years) 75–610
a
– 86–576
a
–
Living trees (years) 23–282
B
109–566
A
35–77
B
67–886
A
MDGR (mm year
-1
) 0.80–6.25
A
0.30–1.64
C
1.03–4.59
A
0.44–2.13
B
Regeneration (P. uviferum)
Density (seedl ha
-1
) 0–2,100
a
0–21.9
a
500–9,000
a
1.9–48.4
a
0–1,750
a
0–3.5
a
100–1,900
a
0.4–6.9
a
(%)
Age (years) 13–46
BC
14–117
AB
12–34
C
13–99
A
MDGR (mm year
-1
) 0.114–0.857
A
0.086–0.441
B
0.114–1.000
A
0.134–0.278
B
1
Calculated only from plots with living trees.
2
Observed ages were corrected with methods of Duncan (1989) and Rozas (2003).
Ranges of mean diameter (dbh, cm), mean height (H, m), density (N ha
-1
), basal area (m
2
ha
-1
), age (years), regeneration density (seedl ha
-1
) and mean diameter growth
rate (MDGR, mm year
-1
). BF-D, BF-UD disturbed and undisturbed bog forests, UF-D, UF-UD disturbed and undisturbed upland forests. For each variable, values with
different letters in superscript were significantly different (capital letters: P £0.001; lower case letters: P £0.05).
Persistence of Pilgerodendron uviferum
Author's personal copy
trichosperma (Figure 3a, b). The Nothofagus species
were also present but in low frequency. In dis-
turbed bog forests, P. uviferum presented high
densities in small diameter classes. However, this
was attributable to only two stands with seed trees
and a high number of seedlings. In disturbed up-
land forests, P. uviferum occurred with few indi-
viduals in small diameter classes.
The ages of P. uviferum reached maxima of
566 and 886 years in undisturbed bog and upland
forests with extremely slow growth rates
(<1 mm year
-1
), respectively (Table 2). Living
P. uviferum trees, even the remnants from the pre-
disturbance forest, were considerably younger in
disturbed forests. Dead P. uviferum trees in dis-
turbed stands were of similar ages as those living
trees in the undisturbed stands, reaching maxima
of 610 and 576 years in disturbed bog and upland
forests, respectively (Table 2). Stands in both types
of undisturbed forests were clearly uneven-
aged and indicative of continuous recruitment
(Figure 4). The apparent lack of individuals
(>5 cm dbh) younger than 150 years in undis-
turbed bog forests and younger than 100 years in
undisturbed upland stands (Figure 4) was attrib-
utable to the minimum dbh used in the tree
inventory (5 cm) and the slow growth rate of the
species. The disturbed forests presented typical
post-disturbance age structures with individuals of
P. uviferum concentrated in younger age classes.
Light Environment
In all forest types, there was more light (%PPFD) at
1.3 m than at 0.3 m height above the ground
(P£0.001). However, this reduction in %PPFD
Figure 3. Diameter structures by tree species in Adisturbed bog forests, Bdisturbed upland forests, Cundisturbed bog
forests and Dundisturbed upland forest. Inset in Aand Bshow the diameter structure of dead P. uviferum trees (prior to fire
situation). Note the different scale of ‘‘x’’ axis in D).
J. R. Bannister and others
Author's personal copy
was significantly higher in upland forests than in
bog forests (P£0.001). The light environment
was highly variable, but significantly different be-
tween the four forest types (P£0.001) (Figure 5).
Light levels were highest in the disturbed bog for-
ests, and lowest in undisturbed upland forests. The
undisturbed bog forests and disturbed upland for-
ests ranked intermediate and had similar light
conditions at 0.3 m above the ground (Figure 5).
However, at 1.3 m height, they were significantly
higher in the disturbed (46.9%) than the undis-
turbed (39.4%) sites.
Regeneration Dynamics
Occurrence of P. uviferum regeneration was highly
variable between the four forest types but not sig-
nificantly different (Table 2). Regeneration was
abundant in undisturbed bog forests, in contrast to
all other forest types. Despite the relatively low
proportion of P. uviferum (0.4–6.9% of all species),
there was abundant regeneration in the undisturbed
upland forests. In both types of disturbed forests,
regeneration of P. uviferum was only found in stands,
where seed trees had either survived the fire or must
have developed shortly afterwards from protected
seeds. In these situations, P. uviferum seedlings were
abundant (700–2,100 seedlings ha
-1
). However,
their relative density was considerably lower in
disturbed upland stands (3.2–3.5%) than in dis-
turbed bog forests (11.2–21.9). This was attributable
to the relatively high abundance of other species
such as W. trichosperma (3–45%), L. ferruginea (0.3–
63%), D. winteri (8–35%), E. coccineum (4–39%), and
N. nitida (0–14%) in the regeneration layer of the
disturbed upland stands (Table 2).
Root collar diameters (rcd) of P. uviferum seedlings
were significantly correlated with age (P£0.01).
The annual diameter increment at the root collar
of P. uviferum seedlings was extremely slow
(<1 mm year
-1
) and significantly higher (P£
0.001) in disturbed than in undisturbed forests
(Table 2). Hence the slope of the regression was also
Figure 4. Age structure of P. uviferum trees (trees >5 cm dbh) in the four forest types. Adisturbed bog forests. B
disturbed upland forests. Cundisturbed bog forests. Dundisturbed upland forests. Brackets in Cand Dcorrespond to
information about seedling and sapling regeneration, which needs several decades to reach the minimum dbh considered
in the stand inventory.
Persistence of Pilgerodendron uviferum
Author's personal copy
higher in undisturbed than in disturbed forest types
(Figure 6). There was a significant positive correla-
tion between root collar diameter and seedling
height in disturbed forests (bog forests: r
2
= 0.652;
upland forests: r
2
= 0.703, P£0.001) and in
undisturbed upland forests (r
2
= 0.270, P£0.05),
but in undisturbed bog forests this relationship was
not significant (r
2
= 0.029, P= 0.385). There was no
significant relationship between annual shoot
growth of P. uviferum seedlings and %PPFD in any of
the four forest types (Figure 7). However, the same
applies to seedlings of all other species, except for
T. stipularis in disturbed bog forest (r
2
= 0.322,
P£0.01). Yet, annual shoot growth of P. uviferum
seedlings was significantly higher in disturbed forest
types (bog forests: 9.6 ±3.2 cm; upland forests:
11.6 ±3.5 cm) than in undisturbed forests (bog
forests: 3.8 ±1.1 cm; upland forests: 4.6 ±1.7 cm)
(Figure 7).
Foliar N and P concentrations in seedlings were
higher on disturbed sites, but were not influenced
by landscape position (upland or bog) (P>0.05).
In addition, species identity influenced N and P
concentrations of seedlings (P£0.01). P. uviferum
seedlings had significantly higher P and N con-
centrations (P£0.05) than most other tree spe-
cies (Figure 8), except for N concentrations in
D. winteri and Nothofagus sp. seedlings, which were
similar on disturbed sites. Foliar N:P ratios were
high in all species and exceeded in most cases the
value of 16, which typically indicates P limitation
(Koerselman and Meuleman 1996).
DISCUSSION
Persistence of P. uviferum in the Absence
of Large-Scale Disturbances
In agreement with our first hypothesis, the stand
structure and regeneration dynamics of the ana-
lyzed P. uviferum forests indicated that P. uviferum
can persist in the absence of large-scale distur-
bances and that old-growth forests dominated by
the species are not a transitional phase in succes-
sion. According to Oliver and Larson (1996), the
term ‘‘old-growth’’ describes stands composed
entirely of trees that have developed in the absence
of allogenic processes. Although some studies have
suggested that partial disturbances such as changes
in the water table or trees struck by lightning occur
in P. uviferum forests (Szeicz and others 2003; Holz
and Veblen 2009), there is no evidence that these
partial disturbances prevent the development of
old-growth stands and the persistence of P. uvife-
rum.
Despite the low mean height of trees, light levels
near the ground in old-growth P. uviferum forests
were relatively low (Figure 5), but still higher than
in many other closed forests like in the Valdivian
Andes (Saldana and Lusk 2003) or New Zealand
(Coomes and others 2005). Light near the ground
was particularly influenced by the lower vegetation
stratum formed principally by T. stipularis, which
was sometimes up to 2 m high and covered in
moss. The high within-stand variability of light
near the ground showed that this vegetation layer
is not constant in space and that seedlings can
receive more light within short vertical distances,
in particular in the undisturbed upland forests.
Surprisingly, growth of P. uviferum seedlings was
not related to light availability (Figure 7), which
suggest that the species may not be as shade-
intolerant as previously proposed (in example,
Veblen and others 1995; Rovere and others 2004;
Soto and Figueroa 2008), or that growth may be
limited by other factors like nutrient availability.
Age and diameter distributions of P. uviferum in
old-growth forests (Figures 3,4) were indicative of
continuous recruitment of regeneration (sensu
Oliver and Larson 1996). Age structures were based
on individuals greater than 5 cm dbh and a pre-
liminary view of the age structures of P. uviferum
individuals in undisturbed forests might suggest an
apparent discontinuity in regeneration younger
Figure 5. Percent of photosynthetic photon flux density
(%PPFD) in the different forest types at 0.3 m (grey) and
1.3 m height (white) above the ground. For a given
height, different letters indicate significant differences
(P£0.001) between forest types. Rel. Drelative change
in %PPFD with height, BF-D, BF-UD disturbed and
undisturbed bog forests, UF-D, UF-UD disturbed and
undisturbed upland forests.
J. R. Bannister and others
Author's personal copy
than 100–150 years, as has been reported previ-
ously (Bannister and others 2008; Lara and others
1999; Mansilla 2008). However, when considering
the regeneration assessments in addition to the tree
inventory, it is evident that there is abundant and
continuous recruitment of individuals, which,
owing to their slow growth, simply take a very long
time to reach the 5 cm threshold. This continuous
pattern is similar to that shown for Picea abies bog
forests in Scandinavia (Ho
¨rnberg and others 1995).
Inclusion of seedlings and saplings into analyses of
tree population dynamics appears to be particularly
important in these forests, because seedlings need
many decades to reach the minimum dbh consid-
ered in stand inventories. The extremely slow
diameter and shoot growth of seedlings in undis-
turbed forests (Figures 6,7) is indicative of a spe-
cies with a stress-tolerant strategy (sensu Grime
1977). If the regression between root collar diam-
eter and age is extrapolated, seedlings of P. uviferum
in undisturbed forests would need between
172 years in bogs and 188 years in upland sites to
reach a root collar diameter of 5 cm. These values
represent conservative estimates because it can be
Figure 6. Relationship between root collar diameter (rcd) and age in P. uviferum seedlings in disturbed and undisturbed
bog and upland forests. The linear model used was of the form: age rcd + forest_type + rcd:forest_type (r
2
= 0.817;
P<0.001). Abog P. uviferum forests (BF-D: age = 17.442 + 10.505*rcd; BF-UD: age = 5.616 + 33.214*rcd). Bupland P.
uviferum forests (UF-D: age = 16.611 + 4.574*rcd; UF-UD: age = 14.121 + 34.837*rcd). BF-D, BF-UD disturbed and
undisturbed bog forests, UF-D, UF-UD disturbed and undisturbed upland forests.
Figure 7. ARelationship between % of photosynthetic photon flux density (%PPFD) and shoot growth of P. uviferum
seedlings in disturbed and undisturbed bog and upland forests. All regressions were not significant (P>0.05): BF-D:
r
2
= 0.134; BF-UD: r
2
= 0.014; UF-D: r
2
= 0.004; UF-UD: r
2
= 0.066. BShoot growth of P. uviferum seedlings in the
different forest types. Forest types sharing the same letter were not significantly different at P£0.001. BF-D, BF-UD
disturbed and undisturbed bog forests, UF-D, UF-UD disturbed and undisturbed upland forests.
Persistence of Pilgerodendron uviferum
Author's personal copy
assumed that diameter growth accelerates with tree
size (diameter growth is higher in P. uviferum trees
than seedlings, Table 2). In this context, our esti-
mates indicate that there is no lack of recruitment
of individuals.
In the absence of major catastrophic disturbances
in boreal bog forests, ongoing paludification will
lead to decreasing forest productivity with time
(Fenton and others 2005; Lavoie and others 2005).
Under these conditions, peat accumulation is pri-
marily under strong autogenic control (succession),
whereas peat reduction is mostly under allogenic
control such as through fires (Simard and others
2007). In the old-growth P. uviferum forests of this
study, there was a positive but not significant cor-
relation between depth of the organic layer and the
age of the oldest tree (as a proxy for time without
disturbances). On these sites, dead lying P. uviferum
stems are covered by more than 50 cm of peat
(Bannister, pers. observation). This obvious palu-
dification contradicts the common concept of
succession in these forests, which postulates an
improvement of drainage conditions under P. uvife-
rum and subsequent colonization of these sites by
other species (Cruz and Lara 1981). As indicated by
foliar nutrient levels, P. uviferum was apparently
best adapted among all tree species analyzed to
cope with the low nutrient content of mineral soils
and organic layers (especially P). Hence, it appears
unlikely that ongoing paludification disadvantages
nutrition of P. uviferum when compared to com-
panion angiosperm species. This is consistent with
results about conifer persistence in nutrient-poor or
waterlogged conditions for Picea mariana in Canada
(Taylor and Chen 2011), for Picea abies in Scandi-
navia (Ho
¨rnberg and others 1995) or for some
Podocarpaceae dominated forests in New Zealand
(Coomes and others 2005).
In this context, longevity (>880 years),
extremely slow growth capacity (<1 mm diameter
per year), tolerance to shade and stress and also
decay-resistance may be the primary mechanisms
that lead to the persistence of P. uviferum in these
unproductive sites. In addition, the capacity to
develop adventitious roots facilitates the supply of
oxygen in waterlogged soils (Crawford and others
2003). Finally, the advantage of conifers on P-de-
pleted soils has been attributed to long life spans of
needles and other morphological and biochemical
adaptations like shallow-rooting systems or venti-
lating tissues in roots (Lusk 2001; Richardson and
others 2004; Coomes and others. 2005). There is
no published information on leaf life spans for
P. uviferum, but analyses of shoots indicate that it is
more than 5 years (Bannister, pers. observation).
Picea abies and Picea marina growing in bog forests in
the Northern Hemisphere have reported leaf life
spans of 8.5 and 2.5–19 years, respectively (Wright
and others 2004).
Figure 8. Foliar N and P concentrations and N/P ratios
in seedlings of the main tree species in disturbed and
undisturbed forests. N. nitida and N. betuloides were
combined to one Nothofagus group. Dashed lines and ar-
rows indicate P and N limitation. Tree species sharing the
same letter were not significantly different at P£0.05.
J. R. Bannister and others
Author's personal copy
The Effect of Intensive Disturbances
on P. uviferum Population Structure
The widespread fire of the early 1940s caused
dramatic changes in structure and composition of
bog and upland forests in the study area (Figure 2).
Almost 70 years after the fire, forest regrowth has
been extremely slow and was dominated by species
like D. winteri,W. trichosperma,N. betuloides,N. nit-
ida, and T. stipularis. In general, P. uviferum was
absent after the fire and occurred only where seed
trees had survived (Table 2). Holz and Veblen
(2009) documented two patterns of fire occurrence
in P. uviferum disturbed forests: (a) infrequent high-
severity crown fires in association with severe,
extensive drought in upland forests and (b) more
frequent low-severity surface fires in association
with less severe droughts in bog forests. Appar-
ently, the intensive crown and surface fires in the
study area 70 years ago exceeded the resistance of
P. uviferum to fire, especially in upland forests,
which accumulate higher basal areas with a com-
plex and dense T. stipularis understorey. This
underpins the importance of residual, surviving
structures (biological legacies) such as seed trees for
the recovery of disturbed sites (Cruz and Lara 1981;
Bannister and others 2008; Franklin 1990; Franklin
and others 2002). These findings are consistent
with our second hypothesis that large-scale fires
not only kill existing P. uviferum trees but also
destroy propagules and thus threaten the local
persistence of the species.
Radial growth and shoot elongation of P. uvife-
rum seedlings were higher in disturbed than in
undisturbed forests, although these growth vari-
ables were not related to light availability. Thus,
light is obviously not the most limiting factor for
the development of P. uviferum seedlings. Better
height growth in disturbed sites may be related to
thinner organic layers and improved nutrition of
seedlings (Simard and others 2007), as indicated
here by higher N and P concentrations. In com-
parison to undisturbed forests, the species needs an
average of 70 years in bogs and 40 years in upland
disturbed sites to reach a root collar diameter of
5 cm. However, our estimates contrast with other
considerably higher estimates for P. uviferum seed-
ling growth in disturbed stands (Mansilla 2008;
Holz 2010). The differences could be explained by
possible problems in the method used by these
authors to estimate the true location of the root
collar, resulting in underestimates of seedling age.
However, data on the occurrence and growth of
seedlings in our study show that P. uviferum does
not need severe disturbances to establish.
Pilgerodendron uviferum is obviously a highly
stress-tolerant conifer that can grow under adverse
conditions of low light, low nutrient availability
and water logging. Owing to the associated growth
strategy, it can persist without severe disturbances
in Patagonian bog forests. Once fire disturbances
have occurred, the recovery of P. uviferum domi-
nated forests is highly dependent on the survival of
trees or seeds and apparently takes a long time.
ACKNOWLEDGMENTS
We are especially grateful to the administration and
staff of the Tantauco Park for constant help
and support in the field. N. Carrasco, R. Ramirez,
G. Lo
¨ffler, J. Flade and D. Rieck assisted under dif-
ficult conditions in the field. Without their help this
study could not have been done. For assistance in the
laboratory we thank R. Nitschke, N. Briggs, G. Lo
¨ffler
and M. Schmidt. D. Forrester, T. Kahl and H. Stark
helped with statistical analyses. Jan Bannister
received a DAAD-CONICYT scholarship to support
his PhD studies at the University of Freiburg, where
he participated in the graduate school ‘‘Environ-
ment, Society and Global Change’’. This research
was also financially supported through grants by the
Georg-Ludwig-Hartig and Futuro foundations.
REFERENCES
Aravena JC. 2007. Reconstructing climate variability using tree
rings and glacier fluctuations in the Southern Chilean Andes.
PhD thesis. Ontario: University of Western Ontario.
Bannister JR, Lara A, Le Quesne C. 2008. Estructura y dina
´mica
de bosques de Pilgerodendron uviferum afectados por incendios
en la Cordillera de la Costa de la Isla Grande de Chiloe
´. Bosque
29:33–43.
Bond WJ. 1989. The tortoise and the hare: ecology of angio-
sperm dominance and gymnosperm persistence. Biol J Linn
Soc 36:227–49.
Burns BR. 1993. Fire-induced dynamics of Araucaria araucana-
Nothofagus antarctica forest in the Southern Andes. J Biogeogr
20:669–85.
Coomes DA, Allen RB, Bentley WA, Burrows LE, Canham CD,
Fagan L, Forsyth DM, Gaxiola-Alcantar A, Parfitt RL, Ruscoe
WA, Wardle DA, Wilson DJ, Wright EF. 2005. The hare, the
tortoise and the crocodile: the ecology of angiosperm domi-
nance, conifer persistence and fern filtering. J Ecol 93:918–35.
Crawford RMM, Jeffree CE, Rees WG. 2003. Paludification and
forest retreat in northern oceanic environments. Ann Bot
91:213–26.
Cruz G, Lara A. 1981. Tipificacio
´n, cambio de estructura y nor-
mas de manejo para Cipre
´s de las Guaitecas (Pilgerodendron
uviferum D. Don Florin) en la isla Grande de Chiloe
´. For. Eng.
thesis. Santiago: Universidad de Chile.
di Castri F, Hajek E. 1976. Bioclimatologı´a de Chile. Santiago:
Vicerrectorı´a Acade
´mica de la Universidad Cato
´lica de Chile.
Persistence of Pilgerodendron uviferum
Author's personal copy
Duncan RP. 1989. An evaluation of errors in tree age estimates
based on increment cores in Kahikatea (Dacrycarpus dacrydio-
ides). N Z Nat Sci 16:31–7.
Fenton N, Lecomte N, Legare S, Bergeron Y. 2005. Paludification
in black spruce (Picea mariana) forests of eastern Canada: po-
tential factors and management implications. Forest Ecol
Manage 213:151–9.
Franklin JF. 1990. Biological legacies: a critical management
concept from Mt. St. Helens. Trans N Am Wildlife Nat Resour
Conf 55:215–19.
Franklin JF, Spies TA, Pelt RV, Carey AB, Thornburgh DA, Berg
DR, Lindenmayer DB, Harmon ME, Keeton WS, Shaw DC,
Bible K, Chen J. 2002. Disturbances and structural develop-
ment of natural forest ecosystems with silvicultural implica-
tions, using Douglas-fir forests as an example. Forest Ecol
Manage 155:399–423.
Gaxiola A, McNeill SM, Coomes DA. 2010. What drives retro-
gressive succession? Plant strategies to tolerate infertile and
poorly drained soils. Funct Ecol 24:714–22.
Gorham E. 1991. Northern Peatlands: role in the carbon cycle
and probable responses to climatic warming. Ecol Appl 1:182–
95.
Grime JP. 1977. Evidence for the existence of three primary
strategies in plants and its relevance to ecological and evolu-
tionary theory. Am Nat 111:1169–94.
Hechenleitner P, Gardner M, Thomas P, Echeverria C, Escobar B,
Brownless P, Martı´nez C. 2005. Plantas amenazadas del cen-
tro-Sur de Chile. Distribucio
´n, conservacio
´n y propagacio
´n.
Chile: Universidad Austral de Chile and Real Jardı´n Bota
´nico
de Edimburgo.
Holz A. 2010. Climatic and human influences on fire regimes
and forest dynamics in temperate rainforests in southern
Chile. PhD. thesis. Boulder: University of Colorado.
Holz A, Veblen TT. 2009. Pilgerodendron uviferum: the southern-
most tree-ring fire recorder species. Ecoscience 16:322–9.
Ho
¨rnberg G, Ohlson M, Zackrisson O. 1995. Stand dynamics,
regeneration patterns and long-term continuity in boreal old-
growth Picea abies swamp-forests. J Veg Sci 6:291–8.
Koerselman W, Meuleman AFM. 1996. The vegetation N:P ratio:
a new tool to detect the nature of nutrient limitation. J Appl
Ecol 33:1441–50.
Ko
¨nig N. 2005. Handbuch forstliche Analytik. Gessellschaft fu
¨r
Analytik. Bonn: Bundesministerium fu
¨r Verbraucherschutz,
Erna
¨hrung und Landwirtschaft.
Kuuluvainen T, Aapala K, Ahlroth P, Kuusinen M, Lindholm T,
Sallantaus T, Siitonen J, Tukia H. 2002. Principles of ecological
restoration of boreal forested ecosystems: Finland as an
example. Silva Fennica 36:409–22.
Lara A, Fraver S, Aravena JC, Wolodarsky-Franke A. 1999. Fire
and the dynamics of Fitzroya cupressoides (alerce) forests of
Chile¢s Cordillera Pelada. Ecoscience 6:100–9.
Lara A, Donoso C, Escobar B, Rovere A, Premoli A, Soto DP,
Bannister JR. 2006. Pilgerodendron uviferum (D. Don) Florin.
In: Donoso C, Ed. Las especies arbo
´reas de los bosques
templados de Chile y Argentina, autoecologı´a. Valdivia:
Marisa Cuneo. p 82–91.
Lavoie M, Pare
´D, Fenton N, Groot A, Taylor K. 2005. Paludifi-
cation and management of forested peatlands in Canada: a
literature review. Environ Rev 13:21–50.
Lumley S, Switsur R. 1993. Late Queaternary chronology of the
Taitao Peninsula, southern Chile. J Q Sci 8:161–5.
Lusk CH. 2001. Leaf life spans of some conifers of the temperate
forests of South America. Rev Chil Hist Nat 74:711–18.
Mansilla C. 2008. Reclutamiento post—disturbios de Cipre
´sde
las Guaitecas (Pilgerodendron uviferum (D. Don) Florin) en
comunidades de turbera, Penı´nsula de Brunswick, Regio
´nde
Magallanes, Chile. Ms. Sc. thesis. Punta Arenas: Universidad
de Magallanes.
Martı´nez O. 1981. Flora y fitosociologı´a de un relicto de Pilg-
erodendron uvifera (D. Don) Florin en el fundo San Pablo de
Tregua (Valdivia-Chile). Bosque 4:3–11.
Moroni MT, Hagemann U, Beilman DW. 2010. Dead wood is
buried and preserved in a Labrador boreal forest. Ecosystems
13:452–8.
Niklasson M. 2002. A comparison of three age determination
methods for suppressed Norway spruce: implications for age
structure analysis. For Ecol Manage 161:279–88.
Oliver C, Larson B. 1996. Forest stand dynamics. New York:
Wiley.
Parent S, Messier C. 1996. A simple and efficient method to
estimate microsite light availability under a forest canopy. Can
J For Res 26:151–4.
Pe
´rez CA, Armesto JJ, Torrealba C, Carmona MR. 2008. Litterfall
dynamics and nitrogen use efficiency in two evergreen tem-
perate rainforests of southern Chile. Austral Ecol 28:591–600.
Richardson SJ, Peltzer DA, Allen RB, McGlone MS, Parfitt RL.
2004. Rapid development of phosphorus limitation in tem-
perate rainforest along the Franz Josef soil chronosequence.
Oecologia 139:267–76.
Rovere A, Premoli A, Aravena JC, Lara A. 2004. Variacio
´nen
Pilgerodendron uviferum (D.Don) Florı´n (Cipre
´s de las Guaite-
cas). In: Donoso C, Premoli A, Gallo L, Ipinza R, Eds. Variacio
´n
intraespecı´fica en las especies arbo
´reas de los bosques temp-
lados. Santiago: Editorial Universitaria. p. 253–75.
Rozas V. 2003. Tree age estimates in Fagus sylvatica and Quercus
robur: testing previous and improved methods. Plant Ecol
167:193–212.
Saldana A, Lusk C. 2003. Influence of overstorey species identity
on resource availability and variation in composition of ad-
vanced regeneration in a temperate rainforest in southern
Chile. Rev Chil Hist Nat 76:639–50.
Shaw AJ, Cox CJ, Boles SB. 2003. Global patterns in peatmoss
biodiversity. Mol Ecol 12:2553–70.
Simard M, Lecomte N, Bergeron Y, Bernier PY, Pare
´D. 2007.
Forest productivity decline caused by successional paludifi-
cation of boreal soils. Ecol Appl 17:1619–37.
Sokal R, Rohlf FJ. 1995. Biometry. The principles and practice of
statistics in biological research. New York: W.H. Freeman and
Company.
Solı´s C, Becerra J, Flores C, Robledo J, Silva M. 2004. Antibac-
terial and antifungal terpenes from Pilgerodendron uviferum (D.
Don) Florin. J Chil Chem Soc 49:157–61.
Soto DP, Figueroa H. 2008. Efectos de las alteraciones antro
´picas
sobre la estructura y composicio
´n de rodales de Pilgerodendron
uviferum en la Cordillera de la Costa de Chile. Ecol Austral
18:13–25.
Stokes MA, Smiley TL. 1968. An introduction to tree-ring dating.
Chicago: University of Chicago Press.
Szeicz JM, Haberle SG, Bennett KD. 2003. Dynamics of North
Patagonian rainforests from fine-resolution pollen, charcoal
and tree-ring analysis, Chonos Archipelago, Southern Chile.
Austral Ecol 28:413–22.
J. R. Bannister and others
Author's personal copy
Taylor AR, Chen HYH. 2011. Multiple successional pathways of
boreal forest stands in central Canada. Ecography 34:208–19.
Veblen TT, Burns BR, Kitzberger T, Lara A, Villalba R. 1995. The
ecology of the conifers of southern South America. In: Enright
NJ, Hill RS, Eds. Ecology of the Southern Conifers. Mel-
bourne: Melbourne University Press. p 120–55.
Villagra
´n C. 1988. Late quaternary vegetation of southern Isla
Grande de Chiloe
´, Chile. Quat Res 29:294–306.
Walter KS, Gillet HJ. 1998. 1997 IUCN Red list of threatened
plants. Gland: IUCN.
Weinzierl W, Dietze G. 2000. Bestimmung der austauschbaren
Kationen ohne Vera
¨nderung des natu
¨rlichen Boden-pH, auch
effektive Kationenaustauschkapazita
¨t genannt. Freiburg:
Landesamt fu
¨r Geologie, Rohstoffe und Bergbau: Methode-
nanleitung.
Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers
F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M,
Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont
BB, Lee T, Lee W, Lusk C, Midgley JJ, Navas M-L, Niinemets
U, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI,
Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R.
2004. The worldwide leaf economics spectrum. Nature
428:821–7.
Persistence of Pilgerodendron uviferum
Author's personal copy
