Article

Structure, Diversity, and Environmental Determinants of

High-Latitude Threatened Conifer Forests
Carlos Esse 1, *, Francisco Correa-Araneda 1 , Cristian Acuña 1 , Rodrigo Santander-Massa 1 ,
Patricio De Los Ríos-Escalante 2,3 , Pablo Saavedra 4 , Ximena Jaque-Jaramillo 1 , Roberto Moreno 1 ,
Paola Massyel García-Meneses 5 and Daniel P. Soto 6

1 Instituto Iberoamericano de Desarrollo Sostenible (IIDS), Unidad de Cambio Climático y Medio

Ambiente (UCCMA), Universidad Autónoma de Chile, Avenida Alemania 01090, Temuco 4780000, Chile;
[email protected] (F.C.-A.); [email protected] (C.A.);
[email protected] (R.S.-M.); [email protected] (X.J.-J.);
[email protected] (R.M.)
2 Departamento de Ciencias Biológicas y Químicas, Facultad de Recursos Naturales,
Universidad Católica de Temuco, Avenida Rudecindo Ortega N◦ 02950 Campus San Juan Pablo II,
Temuco 4780000, Chile; [email protected]
3 Núcleo de Estudios Ambientales, Universidad Católica de Temuco, Temuco 4780000, Chile
4 Facultad de Ciencias Forestales y Recursos Naturales, Escuela de Graduados, Universidad Austral de Chile,
Valdivia 5090000, Chile; [email protected]
5 Laboratorio Nacional de Ciencias de la Sostenibilidad (LANCIS), Instituto de Ecología,
Universidad Nacional Autónoma de México, Ciudad de México 04510, Mexico;



[email protected]

 6 Departamento de Ciencias Naturales y Tecnología, Universidad de Aysén, Coyhaique 5950000, Chile;
[email protected]
Citation: Esse, C.; Correa-Araneda,
* Correspondence: [email protected]
F.; Acuña, C.; Santander-Massa, R.;
De Los Ríos-Escalante, P.; Saavedra,
Abstract: Pilgerodendron uviferum (D. Don) Florin is an endemic, threatened conifer that grows in
P.; Jaque-Jaramillo, X.; Moreno, R.;
South America. In the sub-Antarctic territory, one of the most isolated places in the world, some
García-Meneses, P.M.; Soto, D.P.
Structure, Diversity, and
forest patches remain untouched since the last glaciation. In this study, we analyze the tree structure
Environmental Determinants of and tree diversity and characterize the environmental conditions where P. uviferum-dominated stands
High-Latitude Threatened Conifer develop within the Magellanic islands in Kawésqar National Park, Chile. An environmental matrix
Forests. Forests 2021, 12, 775. using the databases WorldClim and SoilGrids and local topography variables was used to identify
https://doi.org/10.3390/f12060775 the main environmental variables that explain the P. uviferum-dominated stands. PCA was used to
reduce the environmental variables, and PERMANOVA and nMDS were used to evaluate differences
Academic Editor: Christel Kern among forest communities. The results show that two forest communities are present within the
Magellanic islands. Both forest communities share the fact that they can persist over time due to the
Received: 23 April 2021
high water table that limits the competitive effect from other tree species less tolerant to high soil
Accepted: 7 June 2021
water table and organic matter. Our results contribute to knowledge of the species’ environmental
Published: 12 June 2021
preference and design conservation programs.

Publisher’s Note: MDPI stays neutral

Keywords: sub-Antarctic; Patagonia; Pilgerodendron uviferum; biodiversity indexes; Kawésqar Na-
with regard to jurisdictional claims in
tional Park; WorldClim; SoilGrids
published maps and institutional affil-
iations.

1. Introduction

Copyright: © 2021 by the authors.

The coastal temperate forests of southwestern South America are considered one
Licensee MDPI, Basel, Switzerland.
of the 25 hotspots for biodiversity conservation [1]. This is due to their high level of
This article is an open access article
endemism (ca. 50%) and the dramatic reduction of their original forest area (ca. 70%) due
distributed under the terms and to human impacts [2,3]. This region is home to three endemic and monotypic Cupressaceae
conditions of the Creative Commons family members, and all have conservation issues [4,5]. One of them, the ciprés de las
Attribution (CC BY) license (https:// Guaitecas (Pilgerodendron uviferum (D. Don.) Florin), is the world’s southernmost conifer
creativecommons.org/licenses/by/ and covers the greatest latitudinal distribution range (39◦ 350 –54◦ 200 S; ca. 1600 km) [6]
4.0/). in the temperate region of South America. Specifically, this dioecious conifer dominates

Forests 2021, 12, 775. https://doi.org/10.3390/f12060775 https://www.mdpi.com/journal/forests

Forests 2021, 12, 775 2 of 13

Chile’s sub-Antarctic forests and Magellanic moorlands and occupies poorly drained soils
with high water tables [7–12]. Pilgerodendron uviferum has been intensely exploited since
the beginning of the 17th century [13] due to the excellent quality of its wood [14]. Forest
fires have significantly reduced the area where these forest communities develop [8,15]. To
date, there is no accurate estimate of the surface burned, but some experts estimate that
up to 90% of the area where this species is present has been impacted by fire, including
remote areas in the southern Chilean archipelago. Due to these threats, P. uviferum has
been classified as vulnerable by the IUCN (World Conservation Union) [5,16,17] and has
been included in CITES Convention Appendix 1, which regulates international trade of
threatened species.
Based on research conducted in southwestern Chile, specifically in the Magellanic
islands of Puerto Eden (49◦ 080 S), [18] described P. uviferum stands as turbulent forests
typical of the rainy temperate coastal zone and as one of the least studied forests in
South America [19]. According to the literature [8], primary succession in the southern
Magellanic region usually begins in flat sectors without drainage, where the initial species
are Sphagnum spp. and grasses. These species generate peatlands, and better soil drainage
allows P. uviferum seedlings to establish. These areas are called “bog forests” [12]. This
species can develop in wet and poorly drained soils, which means that it presents oxide
reduction processes on the mineral horizon, generating gleysols with a large amount of
organic matter, mostly due to the presence of peat moss (Sphagnum spp.) [6,8,11,12,20].
These communities then transition from bog forests to open cypress forests with
uneven-aged structure and abundant regeneration in the absence of major disturbances [21].
Late successional forests are dominated by P. uviferum and characterized by having open
to very open canopy conditions, which often present around 10% cover [8,22,23]. In flat
areas with poor soil drainage, forests dominated by P. uviferum form a hydrosere [23] due
to the accumulation of organic matter, mainly from Sphagnum spp., which is accompanied
by abundant regeneration with high overstory mortality [6,23]. The species has faced
various threats due to human disturbances over a large part of its territory [23], including
pre-Hispanic burns that reduced and degraded the species’ habitats [24]. As a result,
P. uviferum regenerates poorly and may be replaced by other species, such as Drimys winteri
(J.R. and G. Forst.), Tepualia stipularis (Hook. and Arn.) Griseb., and Saxegothaea conspicua
(Lindl). In the case of low-intensity fires, P. uviferum regeneration is abundant and can be
characterized as an open peat forest dominated by P. uviferum and in the lower canopies
dominated by T. stipularis and Nothofagus betuloides (Mirb.) Oerst., covering less than 30%
of the surface area [8,11,12].
Research conducted in remote Magellanic islands, especially in the northern part of
Kawésqar National Park (KNP), [21] has proposed a classification of vegetation using the
so-called “vegetation floors”. This corresponds to a standardized cartographic classification
of Chilean vegetation based on a 1 km2 grid. Forests in which P. uviferum is the main tree
component are classified as coastal antiboreal peatlands [21]. P. uviferum has become a
dominant tree in the forests, and they share the overstory with T. stipularis and N. betuloides
in locations covered by peat and bog that are less waterlogged. However, very little is
known about these forests due to intense human disturbances along their distribution
range [11,12,21]. Some studies on this species have revealed important changes and
impacts due to stressors, such as wind, fire, climate change, and glaciation [19,25,26]. Our
hypothesis is that forests on Magellanic islands present different structures, community
composition, and diversity that are influenced by climate (temperature and precipitation)
and edaphic variables (water and carbon), where the main driver among the stands is
the high soil water table. This study thus contributes to an ecological understanding that
can inform the design of conservation programs in the southern cone of the American
continent.
 Forests 2021, 12, 775 3 of 13
s 2021, 12, x FOR PEER REVIEW 3 of 14

2. Materials and Methods

2.1. Study Area
2.1. Study Area
The study area is located
The within
study area is Kawésqar National
located within Park, the
Kawésqar insular Park,
National part ofthe
theinsular
prov- part of the
inces of Última Esperanza
provinces and Magallanes
of Última Esperanza in and
southwestern
Magallanes Chile (Figure 1). TheChile
in southwestern climate
(Figure 1). The
is consideredclimate
a hyperoceanic antiboreal
is considered bioclimate with
a hyperoceanic humidbioclimate
antiboreal to hyperhumid soils [21].
with humid to hyperhumid
The local climate is isothermal tundra and presents a mean annual temperature
soils [21]. The local climate is isothermal tundra and presents a mean annual of 6.5 °C temperature
[20]. Annual of ◦
rainfall
6.5 Ccan reach
[20]. up to
Annual 6000 mm,
rainfall making
can reach it one
up to 6000of themaking
mm, rainiestitareas
one ofinthe
therainiest areas
world [27,28].inThe
thepresence
world [27,28].
of Pilgerodendron of Pilgerodendron
The presenceuviferum occurs fromuviferum occurs
Valdivia from Valdivia
Province (39° Province
(39◦ Province
S) to Magallanes S) to Magallanes Province (54◦ S) [29,30].
(54° S) [29,30].

Figure 1. General location of the study area and sample units established in Kawésqar National Park (KNP), Chile.
Figure 1. General location of the study area and sample units established in Kawésqar National
Park (KNP), Chile.
These soils present great fragility and susceptibility to degradation [31]. They also
have a low concentration of O and high Al and Fe. Their pH ranges from 3.5 to 5, they
These soils present great fragility and 2susceptibility to degradation [31]. They also
have a high water table, and they are generally classified as gleysols and histosols [8,28].
have a low concentration of O2 and high Al and Fe. Their pH ranges from 3.5 to 5, they
have a high water table, and
2.2. Sampling andthey
Dataare generally classified as gleysols and histosols [8,28].
Collection
Four stands without apparent human disturbances were selected in the insular area of
2.2. Sampling and Data Collection
KNP (e.g., without the presence of domestic animals (dung), tree logging (stumps), and
Four stands without
hiking trails).apparent human sampling
Simple random disturbances
waswere selected
performed in in thestand.
each insular
Wearea
sampled a total
of KNP (e.g., of
without the presence of domestic animals (dung), tree logging (stumps), and
18 sample units (plots) within the stands. These sampling units were circular plots of
hiking trails).500
Simple random
m2 , where thesampling
diameterwas performed
at breast height in each stand.
(DBH), We sampled
total height (m), andaassociated
total vertical
of 18 sample position
units (plots) within the stands. These sampling units were circular
for dominant, codominant, intermediate, submerged, and suppressed plots of trees were
500 m2, where the diameter at breast height (DBH), total height (m), and associated vertical
position for dominant, codominant, intermediate, submerged, and suppressed trees were
Forests 2021, 12, 775 4 of 13

recorded [6]. In each plot, we considered as trees those individuals with a DBH equal to or
greater than 5 cm.
The quantitative overstory structure of the stands was described in terms of density
(D), mean square diameter (MSD), average height (Havg ), and total basal area (BA). In
addition, a circular and concentric subsampling unit of 2 m radius was established in each
sample unit (n = 18) to quantify tree regeneration. The nomenclature of the tree species was
based mainly on literature descriptions [32], and its phytogeographic origin followed [33].
To determine the age of the stands, the annual growths of three dominant individuals in
terms of tree height were sampled per plot. Two increment cores were obtained at 0.3 m
above ground using Pressler’s borer. The relationship between age and DBH was assessed
through simple linear regression [34]. Coefficient of determination (r2 ), standard deviation,
and structure of residuals were visually evaluated. The cores were processed following
standard tree ring procedures [35] and measured using WinDendroTM software (Regents
Instruments Inc., Québec, QC, Canada).

2.3. Diversity
A diversity analysis was conducted in each plot based on the richness index (S), the
number of tree species in each stand [36]; total abundance (N), density of trees per plot; and
Shannon–Wiener diversity index (H0 ), which indicates the uniformity of the values across
all stand species [37]. The indices were obtained using PAST 3 [38] and the Biodiversity
package in R software [39].

2.4. Environmental Matrix Based on Biophysical Variables

To identify the environmental variables that explain the presence of P. uviferum in the
stands, an environmental matrix was built using climate, soil, and topography variables.
The variables selected are listed in Table 1. Climate information was obtained from the
WorldClim database [40]. The WorldClim data consist of raster layers generated using the
interpolation of average monthly climate based on data from weather stations. A 30-arc-
second resolution grid is provided, which includes precipitation and temperature data
for the entire world. On the other hand, soil variables were obtained from the SoilGrids
database [41], which display basic soil properties based on the FAO world reference, and
the USDA soil taxonomy suborders in raster format for the whole world. The geographic
coordinates at the center of each sampling point were recorded using a GPS instrument
(Garmin map 64sx). Information from WorldClim and SoilGrids was extracted using the
vector coverage of sampling points in a spatial analysis using the GIS ArcMap v10.8.1
software. Finally, the topographic variables were obtained from the “catastro de los recursos
vegetacionales nativos de Chile” database [42].

2.5. Statistical Analyses

The nonparametric Kruskal–Wallis (H-test) test was used to identify significant dif-
ferences between the stand parameters and the diversity indices at a level of 95%. We
previously checked the parametric assumptions (i.e., normality and variance homoscedas-
ticity), which were not met for all variables used. A Wilcox post hoc test was run when
significant differences were obtained from the H-test (p < 0.05) with the Holm method to
correct the level of significance [43,44]. This analysis was carried out with Kruskal function
in the R package agricolae [45].
Principal components analysis (PCA) with a correlation matrix was performed to
identify the environmental variables that best explain the variability of the data set along
the multivariate space (i.e., axes) [34]. The R packages factoextra [46] and FactoMineR [47]
were used for this purpose. Finally, Pearson correlation analysis was run between the main
PCA axes with the reduced environmental variables to interpret the main environmental
gradients driving the P. uviferum-dominated forest communities.
Forests 2021, 12, 775 5 of 13

Table 1. Factors and environmental variables analyzed (soil variables estimated at a depth of 0.3 m).

Factor Variable Unit Description Reference

AMT ◦C Annual mean temperature
MDR ◦C Mean diurnal range (mean of monthly (max temp−min temp))
ISO Index Isothermality (BIO2/BIO7) (×100)
TSS Index Temperature seasonality (standard deviation × 100)
MTW ◦C Max temperature of warmest month
MTC ◦C Min temperature of coldest month
TAR ◦C Temperature annual range (BIO5–BIO6)
MTQ ◦C Mean temperature of wettest quarter
MTD ◦C Mean temperature of driest quarter
MWQ ◦C Mean temperature of warmest quarter Hijmans et al. [40]
1. Climate
MCQ ◦C Mean temperature of coldest quarter
APP mm Annual precipitation
PWM mm Precipitation of wettest month
PDM mm Precipitation of driest month
PPS % Precipitation seasonality (coefficient of variation)
PWQ mm Precipitation of wettest quarter
PDQ mm Precipitation of driest quarter
PPW mm Precipitation of warmest quarter
PCQ mm Precipitation of coldest quarter
PWP % Available soil water capacity (volumetric fraction) until wilting point
Silt % Silt content (2–50 micrometer) mass fraction
Sand % Sand content (50–2000 micrometer) mass fraction
OC kg m−3 Soil organic carbon density
C permille Soil organic carbon content SoilGrids
2. Edaphic
pH scale Soil pH × 10 in H2 O Hengl et al. [41]
CEC Cmol kg−1 Cation exchange capacity of soil
Clay % Clay content
BD kg m−3 Bulk density
SD cm Absolute depth to bedrock
Aspect range Aspect (rank)
3. Topographic Slope % Slope (degree in %) CONAF et al. [42]
Elevation m asl m asl (meter above sea level)

To evaluate potential differences among communities (stands), we conducted the

permutational multivariate analysis of variance (PERMANOVA) with a post hoc test using
the Bray–Curtis distance [48,49]. This analysis was performed with 1000 permutations
with significant p-values > 95%. To visualize stands in the multivariate space, nonmetric
multidimensional scaling (nMDS) analysis was performed using the original abundance
matrix. Analysis was carried out using the adonis function in the R package vegan [50].

3. Results
3.1. Quantitative Structure of the Stands
The dasometric parameters showed differences between stands. Stand 1 had the
lowest average dominant height, followed by Stands 3 and 4. Stand 2 had the bigger trees
in terms of quadratic mean diameter (p < 0.05, Table 2). The oldest stands were Stands 3
(245 years) and 2 (242 years), and the youngest were Stands 4 (201 years) and 1 (214 years)
(p < 0.05, Table 2).
The diameter distribution showed that Stand 2 had the most developed forest structure,
unlike the stands that had greatest density in the first diameter classes. This suggests that
there is a trend towards reverse-J diameter distribution based on evidence that a larger
number of individuals are in the smaller size classes (Figure 2).
 Table 2. General background of the stands measured. Havg = average height; MSD = mean square
diameter; D = density; BA = basal area.
Forests 2021, 12, 775 6 of 13
Stands
Parameters p-Value
S1 S2 S3 S4
Aspect SW FLAT SW FLAT -
Descrip-of the stands measured. Havg = average height; MSD = mean square diameter; D = density;
Table 2. General background Area (ha) 41.83 175.71 22.31 112.23 -
BA = basal area. tive
Age (years) 214 (1.0) c 242 (0.5) b 245 (1.0) a 201 (1.0) d 0.001
Havg (m) 5.80 (0.2) d 11.00 (1.1) a 6.30 (0.2) c 7.20 (0.2) b
Stands 0.001
Parameters Dasomet- MSD (cm) 18.57 (4.3) ab 25.13 (5.0) a 17.40 (4.0) b 18.20 (2.4) b p-Value
0.044
S1 S2 S3 S4
ric D (trees ha−1) 806 (208.2) 856 (290.0) 1087 (477.0) 1187 (290.0) 0.237
Aspect SW FLAT SW FLAT -
Descriptive Area (ha) BA (m 2 ha ) 21.27 (6.8)
41.83
−1
175.7140.43 (14.7) 22.31
23.57 (7.1) 30.10 (5.3)
112.23 0.081 -
AgeNote: Significant214
(years) differences
(1.0) c (Kruskal–Wallis
242 (0.5) b test, p < 0.05) are indicated
245 (1.0) a by
201different
(1.0) d letters. The
0.001
values are means and standard deviations (ina brackets). c
Havg (m) 5.80 (0.2) d 11.00 (1.1) 6.30 (0.2) 7.20 (0.2) b 0.001
MSD (cm) 18.57 (4.3) ab 25.13 (5.0) a 17.40 (4.0) b 18.20 (2.4) b 0.044
Dasometric The diameter distribution showed that Stand 2 had the most developed forest struc-
D (trees ha−1 ) 806 (208.2) 856 (290.0) 1087 (477.0) 1187 (290.0) 0.237
ture, unlike the21.27
BA (m2 ha−1 )
stands that had 40.43
(6.8)
greatest density in23.57
(14.7)
the (7.1)
first diameter classes. This suggests
30.10 (5.3) 0.081
that there is a trend towards reverse-J diameter distribution based on evidence that a
Note: Significant differences (Kruskal–Wallis test, p < 0.05) are indicated by different letters. The values are means and standard deviations
(in brackets). larger number of individuals are in the smaller size classes (Figure 2).

Figure Figure 2. Diameter

2. Diameter distribution
distribution and age and age diameter
diameter relationship
relationship per standper stand
(inside (insideInpanels).
panels). In 1,
(A) Stand (A)(B)
Stand
Stand1,2,(B)
(C)Stand 2,
(C) Stand 3, and
Stand 3, and (D) Stand 4.(D) Stand 4.

3.2. Analysis
3.2. Analysis of the Environmental
of the Environmental Matrix Matrix
Based onBased on Biophysical
Biophysical Variables
Variables
The PCA suggests that the first three axes accounted for 78.44%for
The PCA suggests that the first three axes accounted of 78.44% of the var-
the explained explained
variance, the
iance, reducing reducing the 33 variables
33 variables to the threeto the
mainthree main dimensions
dimensions with 16with 16 variables.
variables. Specifi-Specifi-
cally,
cally, the theaxis
first firstaccounted
axis accounted for 40.34%
for 40.34% of theofexplained
the explained variance
variance and and
waswas represented by
represented
by the the climate
climate factor
factor (APP,
(APP, PWP,PWP,PDM PDM,
, PWQ,PWQ,
PDQ,PDQ,
PPW,PPW,
and PCQand), PCQ),
in thisin thisrelated
case case related
to to
precipitation variables. The second axis accounted for 22.33%
precipitation variables. The second axis accounted for 22.33% of the explained varianceof the explained variance
and was and was represented
represented by the by the climate
climate (MTC, (MTC,
MTD, and MTD, and MCQ),
MCQ), topographic
topographic (elevation),
(elevation), and and
soil factors (C and OC), and in this case the greatest contribution
soil factors (C and OC), and in this case the greatest contribution was made by elevation was made by elevation
(r = 0.348). The third axis accounted for 15.77% of the explained variance represented by the
climate factor (MTW, MWQ, and MTQ), in this case related to the mean annual temperature
of the warmest quarter (r = 0.354) (Table 3). Figure 3 depicts the biplot obtained by PCA,
and Table 3 shows the correlation (r) between selected environmental variables with the
first three dimensions.
Forests 2021, 12, 775 7 of 13

Table 3. Pearson correlation analysis (r) of environmental variables with the first three principal
components (selected variables appear in italics and bold).

Variable PC1 PC2 PC3

Aspect −0.034 0.180 0.006
Slope −0.028 0.135 0.208
Elevation −0.002 0.348 −0.117
AMT −0.023 −0.257 0.296
MDR 0.205 0.169 0.199
ISO 0.160 0.120 0.013
TSS 0.201 0.132 0.234
MTW 0.141 −0.053 0.354
MTC −0.152 −0.288 0.103
TAR 0.208 0.157 0.193
MTQ −0.160 −0.005 0.317
MTD −0.193 −0.256 0.010
MWQ 0.062 −0.181 0.356
MCQ −0.118 −0.297 0.160
APP −0.273 0.008 −0.008
PWM −0.272 −0.001 −0.038
PDM −0.272 −0.017 −0.029
PPS −0.229 0.130 0.120
PWQ −0.273 0.003 −0.014
PDQ −0.273 0.008 −0.003
PPW −0.272 0.010 0.000
PCQ −0.273 0.004 −0.010
Tex −0.100 0.216 0.114
PWP 0.150 −0.229 −0.207
Silt 0.185 −0.141 −0.130
Sand −0.116 0.204 0.168
OC 0.094 −0.259 −0.124
C 0.116 −0.278 −0.058
pH −0.199 0.141 −0.043
CEC 0.057 0.033 −0.296
Clay −0.013 −0.196 −0.125
BD −0.063 0.068 −0.244
Forests 2021, 12, x FOR PEER REVIEW 8 of 14
SD −0.036 −0.138 0.182

Figure 3. PCA biplot based on the main environmental variables extracted from the WorldClim and SoilGrids databases
Figure 3. PCA biplot based on the main environmental variables extracted from the
and topographic variables per stand.
WorldClim and
SoilGrids databases and topographic variables per stand.
3.3. Composition, Diversity, and Community Structure
Pilgerodendron uviferum, Tepualia Stipularis (Hook et Arn.) Griseb, Drimys Winteri J.R.
et G. Forster., Maytenus Magellanica (Lam.) Hook. F., Nothofagus Betuloides (Mirb) Oerst.,
Pseudopanax laetevirens K. Koch., Nothofagus antarctica (G. Forst.) Oerst., and Podocarpus
nubigenus Lindl. were found in this study. Regarding tree species that represent the major
overstory composition (n) for each stand, nine were identified in Stand 4, six in Stand 2,
Forests 2021, 12, 775 8 of 13

3.3. Composition, Diversity, and Community Structure

Pilgerodendron uviferum, Tepualia Stipularis (Hook et Arn.) Griseb, Drimys Winteri J.R.
et G. Forster., Maytenus Magellanica (Lam.) Hook. F., Nothofagus Betuloides (Mirb) Oerst.,
Pseudopanax laetevirens K. Koch., Nothofagus antarctica (G. Forst.) Oerst., and Podocarpus
nubigenus Lindl. were found in this study. Regarding tree species that represent the major
overstory composition (n) for each stand, nine were identified in Stand 4, six in Stand 2, six
in Stand 1, and five in Stand 3. P. uviferum was the most abundant tree species in all stands,
followed by N. betuloides and T. stipularis (Table 4).

Table 4. Abundance of species in each stand in Kawésqar National Park. The values are the means
and standard error (in brackets) per stand.

Abundance by Stand
Species Stand 1 Stand 2 Stand 3 Stand 4
P. uviferum 16.33 (6.89) 26.68 (10.74) 35.70 (16.37) 32.19 (7.33)
T. stipularis 39.53 (22.54) 1.17 (0.98) 2.67 (2.19) 17.41 (11.74)
D. winteri 2.33 (1.45) 4.17 (2.43) 10.00 (4.93) 9.83 (2.30)
L. ferruginea - - - 2.50 (1.23)
M. magellanica 0.33 (0.33) 1.33 (1.33) - 0.67 (0.33)
N. betuloides 13.00 (3.51) 25.38 (3.74) 13.35 (1.86) 17.02 (1.06)
P. laetevirens 2.35 (1.46) 4.70 (3.73) 6.38 (5.88) 3.18 (1.46)
N. antarctica - - - 2.00 (0.86)
P. nubigena - - - 2.33 (1.12)

Significant differences among the stands were observed in terms of species richness
(S0 ) and Shannon index (p < 0.05, Table 5). For example, the Shannon index values showed
low diversity. Stand 4 was the most diverse, with a value of 1.45, and Stand 2 was the
least diverse, with a value of 0.89. There were significant differences between the stands
in terms of species richness. Stand 4 was the most diverse, followed by Stands 1, 2, and 3,
which were similar. No significant differences were found among the stands in terms of
abundance.

Table 5. Diversity indices for species in different stands in Kawésqar National Park.

Diversity Index by Stand

p-Values
Index Stand 1 Stand 2 Stand 3 Stand 4
Richness (S0 ) 4.67 (0.33) b 3.83 (0.40) b 4.33 (0.33) b 6.33 (0.21) a 0.005
Abundance (N) 74.00 (32.13) 63.33 (10.81) 68.00 (19.00) 87.17 (17.47) 0.870
Shannon index (H0
1.21 (0.09) ab 0.89 (0.14) b 1.08 (0.22) ab 1.45 (0.04) a 0.028
loge)
Significant differences (Kruskal–Wallis test, p < 0.05) are indicated by different letters. The values are means and standard deviations (in
brackets).

Finally, PERMANOVA shows a solution where the four stands under study form
two main forest communities (R = 0.53, p < 0.05). Post hoc test showed significant differ-
ences (p < 0.05) between Stand 2 and Stands 1, 3, and 4, which were similar in terms of
composition. The difference between two communities was confirmed by an nMDS biplot
(Figure 4).
 Finally, PERMANOVA shows a solution where the four stands under study form
two main forest communities (R = 0.53, p < 0.05,). Post hoc test showed significant differ-
ences (p < 0.05) between Stand 2 and Stands 1, 3, and 4, which were similar in terms of
Forests 2021, 12, 775 composition. The difference between two communities was confirmed by an nMDS biplot 9 of 13
(Figure 4).

Nonmetric
Figure4.4.Nonmetric
Figure multidimensional
multidimensional scaling
scaling (nMDS)
(nMDS) showing
showing Pilgerodendron
Pilgerodendron uviferum
uviferum stands
stands
sampledininthe
sampled theMagellanic
Magellanicislands
islandsofofKawésqar
KawésqarNational
NationalPark.
Park.

4. Discussion
This study contributes to our understanding of the structure, diversity, and dynamics
of pristine forests dominated by P. uviferum and the environmental variables that influence
its presence in the southwestern Patagonia archipelago. The results may help to expand
and refine current knowledge about the ecology and dynamics of forest communities
dominated by P. uviferum, since most studies have been conducted in the northern limit
of its distribution range [11,30,31] and in some locations of southern Chiloé [8,12,15,51],
where the soils and climate characteristics and even anthropogenic threats may cloud the
interpretation of the ecology of these threatened conifer forests.
The forests dominated by P. uviferum have a wide latitudinal distribution, which could
indicate that the species is capable of adapting to different environmental conditions if
the water table remains high [11,12]. These forests are most abundant in the southernmost
parts of Chile, especially in southern Chiloé and the Magellanic islands, where the mean
annual precipitation is above 2000 mm [7,11,52]. In that way, climate seems to be the
major factor driving the occurrence and abundance of these forests, where high rainfall
and low temperature regimes are preferred by a P. uviferum-dominated forest community.
In our study, we highlight that precipitation is the main variable driving the presence of
P. uviferum-dominated communities, followed by soil variables, such as carbon and organic
matter, but more importantly, the elevation above sea level. Finally, variables from the
third group that explain the presence of P. uviferum are those related to temperature during
the warmest months. These interpretations are supported by earlier studies [7,29].
Specifically, the climate factors influence the presence and abundance of P. uviferum
communities on Magellanic islands. The high mean annual precipitation (up to 6000 mm)
and low mean annual temperature are the main variables that explain the communities’
distribution. We also found that high levels of soil carbon and/or organic material explain
the presence of these communities on smaller scales. This is consistent with the studies
conducted by [12,53] on Chiloé and the research performed at the northern edge of the
coastal range of the Valdivian ecoregion [12]. However, the common variable among
Forests 2021, 12, 775 10 of 13

all of the sites is the high soil water table, which is considered key for the recovery of
P. uviferum-dominated communities after disturbance [8,12,24,53]. Therefore, soil water
and organic matter amounts in conjunction with high amount of precipitation and low
temperatures during the warmest months have an important influence on the structure
and composition of these forest communities.
Stand 4 had a low water table that may have been improved through natural succes-
sion. One factor of this argument is the regeneration of conspecific tree species that are less
tolerant of high water tables, such as Nothofagus betuloides and Tepualia stipularis, which was
higher in that stand than in the rest [6]. The forest structure and composition of Stand 4 are
comparable to the forest described in southern Chiloé Island by [8,54], who named it the
“upland forest” due to the more favorable drainage conditions, which allow for irregular
structures and mixed overstory composition. In waterlogged soils, P. uviferum-dominated
communities tend to generate sparse and open forests, which coincide with the “open
cypress forests” proposed by [8]. This forest type coincides with Stand 2 of our study,
which presents greater tree species diversity, larger basal area, and the tallest and oldest
trees included in our study (Table 2). This argument is consistent with the positive relation-
ship between biodiversity and productivity on a global scale [55]. Moreover, its diameter
distribution shows advanced stand development compared with the others, consistent
with the maximum age registered for this stand (i.e., 374-year-old trees). Age–diameter
relationship was positive and significant, consistent with previous studies conducted for
P. uviferum in northern stands [12,54]. Stand 1 showed a similar trend to Stand 3 regarding
age (263 and 288 years), but with shorter P. uviferum and a smaller basal area. The structure
and composition of this stand were different from those of the rest, and they were similar
to those described by [12,54]. This is reflected in the clear separation between Stands 1, 3,
and 4 and Stand 2 (i.e., PERMANOVA and nMDS analysis).
Ecologically, stands without disturbances and in flat areas have extremely high soil
water table and present lower soil temperature and low nutrient availability [12]. In these
site conditions, P. uviferum may undergo root modification [12,56]. This may be attributed
to species adaptation and avoidance of death by maintaining low growth rates [53]. This
morphological modification can be seen as the species’ approach for adapting to extreme
soil conditions in order to live for extended periods of time (e.g., 566 to 886 years in age) [12].
Under these swampy conditions, P. uviferum presents lower heights and diameters com-
pared with forests with lower soil water tables or those growing in upland conditions [12].
The upland conditions described by [12] are similar to those reported for Stands 2 and 4 in
our study.
In a broader perspective, according to the classification proposed by [22], Stands 1,
2, and 3 are located on the P91 floor, which is characterized by lowest species diversity.
This is consistent with our results. Stand 4 is located on vegetation floor P94, where
P. uviferum is the main canopy species along with the shrub species S. magellanicum. In
this sense, Stand 1 presented low density of P. uviferum, which may be associated with
harsh macroclimate conditions. If these are characterized by low temperatures and high
precipitation in conjunction with a high water table, conditions may produce mortality and
open forests with high abundance of Sphagnum spp. This is consistent with the conditions
reported by [8] and [12] in southern Chiloé.

Implication for the Conservation of High-Latitude Conifer Forests

Monitoring remote forests poses economic, technical, and scientific challenges [57],
but these efforts reveal how ecological factors and pressures could impact the structure
and diversity of P. uviferum stands on Magellanic islands. Many conservation programs
are incorporating remote sensing and other GIS tools to monitor hard-to-reach ecosystems,
and these tools can be useful for conducting research in remote areas. These tools have
been used for UAV biodiversity monitoring of Mount Venere, Italy [58]. The methodology
utilized by [59] was used in a temporal study of forest degradation and deforestation in
Brazil [60]. In addition, and considering pressures from other global phenomena, such
Forests 2021, 12, 775 11 of 13

as changes in precipitation and precipitation regimes and the intensification of extreme

climatic events (e.g., droughts and heatwaves during summer and cold events and in-
tense rainfall in winter), forests such as the ones studied here could serve as a proxy for
environmental changes and as a reference to compare with other forests that have been
degraded.

5. Conclusions
This study documented the structure, composition, and diversity of Pilgerodendron
uviferum-dominated stands on Magellanic islands in Kawésqar National Park, located in
in the southwestern part of South America. We identified two major community groups
that differ in tree structure, composition, and diversity. They are influenced by contrasting
precipitation, temperature, soil carbon, and elevation and share their dependence on high
water tables in order to persist in these forest communities. The information gathered
in this study may help to improve conservation and restoration programs and to refine
ecological knowledge of this understudied forest type.

Author Contributions: C.E.: conceptualization, formal analysis, funding acquisition, methodology,

visualization, and writing—review and editing. R.S.-M., P.M.G.-M., and D.P.S.: formal analysis,
software, validation, and writing—original draft. R.M. and P.D.L.R.-E.: data curation and validation.
P.S. and X.J.-J.: formal analysis and visualization. C.A.: data curation, funding acquisition, and
investigation. F.C.-A.: funding acquisition, formal analysis, and visualization. All authors have read
and agreed to the published version of the manuscript.
Funding: This research was funded by the National Forestry Corporation (CONAF) of Chile and
FONDECYT Projects, grant numbers 11160650 and 11170390 of ANID Chile, and Project MECESUP
UCT 0804.
Data Availability Statement: The data presented in this study are available on request from the
corresponding author. The data are not publicly available due to privacy.
Acknowledgments: The authors would like to thank the CONAF (Chilean Forest Service) of Chile,
especially the Última Esperanza Province office. They are grateful for the assistance of Cristian
Ruiz Huichapani, Patricio Salinas Dillems, Giovanny Serey Caba, Jovito González Chambla, Captain
German Coronado Vázquez, and the crew of the Yepayek. C.E. acknowledges the support received
through FONDECYT No. 11160650. F.C.-A. acknowledges the support received through FONDECYT
No. 11170390. R.S.-M. acknowledges the funding received for the fourth author’s graduate studies
from Human Capital Training Fund Project No. 21150903. The authors express their gratitude to M.I.
and S.M.A. for their valuable suggestions to improve the manuscript.
Conflicts of Interest: The authors declare no conflict of interest.

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