Divergent
drivers of tree community composition in lowland and highland forests of the
northern tropical Andes, Colombia
Divergencia en los determinantes de la composición de
comunidades arbóreas entre bosques de tierras bajas y tierras altas del noroeste
de los Andes tropicales, Colombia
Álvaro Idárraga1,
4, Álvaro J. Duque-Montoya2,
5, Kenneth Feeley3,
6
Abstract
Identifying the
determinants of tree species composition among contrasting altitudinal tropical
forest types will improve our understanding of the main factors and processes
controlling tree species’ distributions and patterns of diversity. The study
area is located in the northwest region of Colombia. We used Redundancy
Analysis (RDA) and a semi-log
distance-decay model to analyze the influence of climate, soil fertility, and
spatial processes, such as dispersal limitation, on community composition.
There were 3 distinct forest types: one in the highlands and two in the
lowlands. In the lowlands, both the RDA and the semi-log linear models
identified calcium concentrations as the most important explanatory variable
for species composition (R2adj = 0.24; p = 0.001 and RMantel
= 0.68; p = 0.006, respectively). In the highlands, the RDA only identified
longitude as being a significant explanatory variable (R2adj
= 0.24; p = 0.001), primarily determined by the biogeographical location of
forests on either the West or the Central Cordillera of the Andes. In these
neotropical forests, the factors determining tree species composition between lowlands
and highlands varied in both extent and nature. Overall, our findings do not
support the idea of a higher habitat-plant specialization in highlands than in
lowlands due to greater geomorphologic and edaphic variation. Since tropical
Andean ecosystems, and in particular highland forests, have received less
attention than their lowland counterparts, our findings help to expand the
current knowledge of factors and processes determining community composition of
tropical montane forests.
Key
words: Colombia, elevational gradient, environmental
filtering, montane forests, spatial analysis
Resumen
Identificar los determinantes de la composición de
especies arbóreas entre tipos de bosques tropicales altitudinalmente
contrastantes incrementarán nuestro conocimiento de los principales factores y
procesos que controlan los patrones de diversidad y distribución de las
especies. El área de estudio se localiza en la región noroeste de Colombia,
principalmente en el departamento de Antioquia. Se empleó el análisis de
redundancia (RDA) y un modelo
semi-logarítmico linealizado para analizar la influencia del clima, fertilidad
del suelo, y procesos espaciales, tales como la limitación en dispersión, sobre
la composición de la comunidad arbórea. Se encontraron tres tipos de bosques:
uno en tierras altas y dos en tierras bajas. En las tierras bajas, ambos
modelos, el RDA y el modelo semi-logarítmico linealizado, identificaron las
concentraciones de calcio como la variable que mejor explica la composición de
especies (R2adj = 0,24; p = 0,001 y RMantel =
0,68; p = 0,006, respectivamente). En las tierras altas, el RDA solo identificó
la longitud como una variable explicativa significativa (R2adj
= 0,24; p = 0,001), determinada principalmente por la ubicación biogeográfica
de los bosques en la cordillera Occidental o Central de los Andes. En estos
bosques neotropicales, los factores que determinan la composición de especies
de árboles entre tierras bajas y altas varió en magnitud y naturaleza. En
general, nuestros resultados no apoyan la idea que existe una mayor
especialización de hábitat en tierras altas que en tierras bajas debido a mayor
variación geomorfológica y edáfica. Los ecosistemas tropicales andinos y en
particular los bosques de tierras altas, han recibido menos atención que sus
contrapartes de tierras bajas; nuestros hallazgos ayudan a ampliar el
conocimiento actual de los factores y procesos que determinan la composición de
las comunidades de los bosques montanos tropicales.
Palabras claves: análisis ambientales, bosques de montaña, Colombia,
filtros ambientales, gradiente de elevación
INTRODUCTION
Changes in tree
species composition along spatial or environmental gradients can be driven by
either environmental filtering, which is associated with abiotic factors such
as climate, topography and soil characteristics (Aiba and Kitayama 1999, Gentry
1988, Hemp 2005, Vásquez and Givnish 1998), or by spatially-driven stochastic
processes, such as dispersal limitation (Condit et al. 2002, Hubbell 2001, Vormisto et al. 2004). Climate is expected to be the most important factor
controlling species distributions at the regional scale (Clinebell et al. 1995, Engelbrecht et al. 2007), while topography and soils
are expected to play more important roles at the meso and local scales (Clark et al. 1999, Condit et al. 2013, Duque et al.
2002, John et al. 2007). Regarding
stochastic factors, in forested areas it is expected that dispersal limitation
will not play a significant role in determining community composition at
geographic distances larger than approximately 50-100 km (Chain-Guadarrama et al. 2012, Condit et al. 2002). Dispersal limitation has been proposed as the main
mechanism determining species neutrality due to its capability to overcome
differential competitive advantages associated with species life history
(Hubbell 2001). However, the presence of major physical barriers (e.g., the
Andean mountain ridges) may cause habitat isolation and promotes dispersal
limitation, thereby determining species distributions at large spatial scales
as well (Nekola and White 1999).
In the northern
part of the Andes, lowland valleys are isolated by of the presence of mountain
ranges that reach up to 4000 m.a.s.l. (meters above sea level). Therefore,
under the assumption of dispersal limitation as key determinant of community
composition, forests located on similar ranks of elevation (e.g., lowlands or
highlands) within the same valley or catchment may demonstrate higher floristic
similarity when compared to those located on the opposite sides of ridges
(Chain-Guadarrama et al. 2012, Condit
et al. 2002, Nekola and White 1999).
Otherwise, environmental filters imposed by either climatic variability or soil
fertility (Condit et al. 2013,
Engelbrecht et al. 2007, Garibaldi et al. 2014, Jones et al. 2011), are expected to be the primary determinants of
species distributions.
Some authors
(e.g., Gentry 1982, Hemp 2005, Jones et
al. 2011) have proposed that the turnover in plant species composition
between highland ecosystems of the same elevation is greater than turnover
between lowland ecosystems because of lack of habitat connectivity as well as
higher habitat specialization associated with a greater climatic, edaphic, and
topographic variation. Overall, habitat similarity in the high mountain forests
is expected to decrease rapidly with geographic distance and similar habitats
can be highly fragmented. This isolation poses limits
to dispersal (Garibaldi et al.
2014) and could also enhance differences in habitat
response or habitat-specialization among taxa (Nekola and White 1999). However, extreme environmental conditions and
highly variable climates could promote decreased habitat specialization and
broader species ranges due to greater tolerance to thermal variation in the
highlands. If this is the case, in the northern Andes we would expect community
composition to be relatively homogeneous between highland forests located on
the same mountain range, and species composition to be mainly differentiated by
dispersal constrains caused by geographical barriers, such as the interandean
valleys. The hypothesis about floristic homogenization in highlands of tropical
mountains due to species tolerance to high climate variability is analogous to
the expected increase of the species’ geographic ranges with latitude caused by
higher tolerances to environmental variation (Stevens 1992).
The primary goal
of the current study was to identify the main factors and processes that
determine patterns of community composition for woody plant species inhabiting
tropical forests at contrasting elevations. In tropical forests, comparisons of
changes in species turnover among forest types with different edaphic and
climatic characteristics will improve our understanding of the main processes
and factors that control species distributions in environmentally complex ecosystems
(Davidar et al. 2007). In particular,
we aim to test the hypothesis about the congruence among environmental factors
that determine tree species composition at large scales in the lowlands and
highlands of tropical forests in this region of Colombia. Thus, based on a
survey of 16 1-ha plots conducted along a complex environmental gradient that
was largely defined by the Andean mountains, we aimed to answer the following
research question: To what extent do environmental factors associated with environmental
and/or spatial processes coincide and determine the tree community composition
at large scale in lowlands and highlands of montane ecosystems in the northern
Andes? We did not find support for a higher habitat-plant specialization in
highlands than in lowlands. Improving our understanding of the main factors
determining plant community composition in this region will assist in defining
conservation strategies for protecting these highly threatened tropical forests
(Duque et al. 2014, Myers et al. 2000).
MATERIALS
AND METHODS
The study area is
located in the northwest region of Colombia between 5º 50’ and 8º 61’ N; and
74º 61’ and 77º 33’ W. This region encompasses an altitudinal gradient from sea
level to 4000 m.a.s.l. and is highly variable in terms of its topography,
climate and soils. The annual precipitation in this region ranges from 1000 to
almost 7000 mm. Likewise, the topography and geology are highly variable
because of the presence of two mountain ranges influencing patterns of drainage,
rainfall and soil fertility at local scales (IGAC 2007).
The study was
conducted using data collected from 16 permanent 1-ha forest inventory plots.
The permanent plots were distributed across a large geographic area that covers
approximately 64 000 km2, mostly in the province of Antioquia. Plot
locations span an altitudinal gradient from 50 to 2950 m.a.s.l. (table 1). The
average distance between plots was 172.6 km (ranging from 24.5 to 423.1 km).
Plots were established in randomly selected areas meeting the following
criteria: 1) no signs of recent
disturbance; 2) located in either a
public or private protected area; 3)
located in an accessible area in which work could be performed for long
periods; and 4) located in a
relatively-secure area without the current presence of guerrillas or any other
illegal group. The historical settlement in the region since the 18th century
lead to a massive occupation in the central cordillera, which has promoted an
intensive deforestation and forest degradation (Cabrera et al. 2011). Overall, the current forest cover only accounts for
roughly 30% of the original vegetation (Duque et al. 2014). Four plots (Carepa, El Bagre, Necoclí, and Támesis)
are located in small forest fragments (~ 50 ha), and may have faced prior
degradation and edge effects such as elevated tree mortality.
Table
1.
The site description of the 16 permanent plots established in this study (the
number of individuals and species include all individuals with 1 cm ≤ diameter
at breast height (DBH) < 10 cm
found within the 40 × 40 m subplot)
All plots were 100
x 100 m with the exception of one plot of 40 x 250 m which was shaped to fit
within the only remaining forest fragment in the Támesis geographic area. In
each plot, all woody plant individuals (shrubs, trees, palms, and tree ferns)
with a diameter at breast height (DBH)
≥ 10 cm were mapped, tagged, and measured. All individuals with a DBH between 1
and 10 cm were counted in a 40 x 40 m subplot located near the center of each
plot. Voucher collections were made for each potentially-unique species in each
plot. All of the vouchers are kept at the University of Antioquia’s Herbarium (HUA). Individuals that could not be
identified to the species level were classified as morphospecies based on
differences in the morphology of vegetative characters. Approximately 1.2%
(333) of individuals were excluded from the analysis due to low-quality
vouchers resulting from a lack of clear botanical characters, earlier stages of
development, or incorrect enumeration.
For soil sampling,
plots were divided into 20 x 20 m quadrats, except for the Támesis plot, which
was divided in 10 x 10 m quadrats. We collected samples of the soil A horizon
(mineral soil after removing organic layer) from five points in each quadrat.
Composite samples (500 g) per quadrat were obtained and air-dried after
macroscopic organic matter removal. The chemical properties and texture of the
soil samples were analyzed at the Biogeochemical Analysis Laboratory at the
Universidad Nacional de Colombia in Medellín. The exchangeable Ca, K, and Mg
were extracted with 1 M ammonium acetate and analyzed using atomic-absorption.
The available P was extracted with L-ascorbic acid and analyzed using a
spectrophotometer UV-VIS. The soil pH was measured in water solution as one
part soil to two parts water. The organic matter (O.M.) was determined according to the Walkley and Black volumetric
method. Mean values (from quadrats samples) of soil properties per plot, were
used for subsequent analyses.
Data
analysis.
Community composition. Because many species can be
artificially classified as unique or rare due to the relatively low density of
plots dispersed over our large study area, we included only those species recorded
in two or more plots in our analyses. We a
priori designated the six plots occurring above 1700 m asl as “highland”
forests since these plots are located within the cloud-immersion zone and are
sometimes exposed to sub-zero temperatures (°C; A. Duque, personal
observations). The remaining ten plots (all below 1100 m.a.s.l.) were
classified as lowland forests (table 1).
The patterns of
community composition in the entire region were defined by means of a Principal
Component Analysis (PCA) performed
on the Hellinger-transformed species abundances (Legendre and Gallagher 2001,
Legendre and Legendre 2012). We then performed an Analysis of Similarities (ANOSIM) with 999 permutations prior to
the calculation of the Euclidean distances between the Hellinger-transformed
species abundances per plot to identify the different forest types as depicted
by the PCA (Borcard et al. 2011,
Legendre and Legendre 2012). The ANOSIM test confirms if predefined sampling units are
statistically distinct in their species composition under the assumption that
compositional intergroup dissimilarities should be greater than intragroup
dissimilarities (Oksanen et al.
2016). The species contribution to beta diversity (SCBD), which was derived from the total community composition
variance following the methodology proposed by Legendre and De
Cáceres (2013), was quantified for each species.
Community
composition and environment. Based on the forest types
defined by the PCA on the floristic data, we performed a one-way analysis of
variance (ANOVA) to evaluate the
differences in pH, and the log transformed contents of O.M., Ca, K, Mg, and P.
Tukey's tests were performed to compare means. Independent Redundancy Analyses (RDA) based on the Hellinger
transformed species abundances was performed to analyze the influence of
climate, soil fertility, and spatial processes on compositional patterns
(Legendre and Legendre 2012) for both lowland and highland plots. Climatic
variables were mean annual rainfall (mm), the number of dry months per year,
and the elevation of each plot (m.a.s.l.). Elevation was taken from the NASA
shuttle radar topography mission digital elevation model (DEM) at a resolution of 30 arc seconds and was used as a proxy for
temperature variation since the Pearson correlation of elevation with both
annual mean temperature and minimum temperature was extremely high (r = -0.99).
Soil fertility was evaluated by means of the soil pH and the log-transformed
content of O.M., Ca, K, Mg, and P. The geographical space was then employed to
evaluate the biological spatially driven processes, such as either dispersal
limitation (see Jones et al. 2008) or
biogeographical similarity. The spatial variables were described by a third-order
polynomial of the geographical coordinates, which were centered on their
respective means prior to analysis. This method is recommended for modeling
spatial structures that operates at large spatial scales (Legendre and Legendre
2012).
In both the lowlands
and highlands, the forward selection option was applied to each independent set
of explanatory variables (climatic, edaphic, or spatial) to select all
significant factors (P < 0.05 after 999 random permutations) explaining the
variation of the plant community composition (Borcard et al. 2011). In order to have the most parsimonious RDA model,
forward selection was run again on the complete set of selected climatic,
edaphic and spatial variables. The distance-decay approach (Nekola and White
1999, Tuomisto et al. 2003) was then
applied to analyze the relationship between the floristic similarities and
either the log-transformed spatial distances or the environmental distance of
the log-transformed variables left in the RDA independent models. The correlation
between the floristic distances and spatial or environmental distances was
evaluated by a Mantel test (Legendre and Legendre 2012). We transformed the
floristic dissimilarities (D) to
similarities (S) through a
subtraction S = 2-D. A semi-log
linear model was then fitted to plot the distance decay of floristic
similarity. The approximately linear distance-decay along the logarithm of
geographical distance can be used as an explicit prediction (and test) of
Hubbell’s neutral theory (Hubbell 2001, Tuomisto and Ruokolainen 2006). The RDA
and the distance decay methods are complementary methods that aim to explain
changes in plant community composition (Tuomisto and Ruokolainen 2006).
RESULTS
In the entire
survey, we tallied a total of 26,512 individuals woody plants (DBH ≥ 1 cm)
belonging to 1622 species or morphospecies. Of the total species, 959 (59%)
could be identified as named species, 577 (36%) were identified only to the
genus level, 79 (4.9%) were identified only to the family level, and 7 (0.1%)
remained unidentified. In total, 541 species were present in two or more plots
and therefore could be included in our analyses.
The number of
individuals per plot (including all individuals with DBH ≥ 1 cm found within
the 40 x 40 m subplot) ranged between 862 and 2855. The number of species per
plot ranged between 55 and 303 (table 1). In the lowlands, there were 358
species (13,303 individuals) that were present in two or more plots, while in
highlands there were 169 species (6898 individuals) that occurred in two or
more plots.
Definition
of forest types. In the entire study area, we identified 3
distinct forest types: one in the highlands and two in the lowlands (figure 1).
Along the first PCA axis, which explained 12.7% of the total variation, the
highlands were separated from lowlands. The first PCA axis was highly
correlated with elevation (r = -0.75), which confirmed the expected strong
effect of temperature in determining tree community composition at large scale
along the whole elevation gradient from lowlands to highlands. Along the second
PCA axis, which explained 11.4% of the total variation, the lowland forests
were also divided into two major forest types - henceforth referred to as
lowlands 1 and lowlands 2 (figure 1). The ANOSIM confirmed the existence of
significant differences in the community composition among the three forest
types identified by means of the PCA (R = 0.89, p = 0.001).
Figure
1.
The forest types according to the Principal Coordinates Analysis of tree
species in the northwest region of Colombia [the
size of the symbols is proportional to the total contribution to total
diversity made by each plot (Legendre and De Cáceres 2013)].
The lowlands 1
group was composed of five plots, including Sapzurro and Puerto Triunfo, which
were located at the farthest distance apart of any pair of plots (table 1). The
three species with the highest contribution to the total beta diversity
belonging to this forest type were Acalypha
diversifolia, Clarisia biflora,
and Clavija mezii (table 2). The
lowlands 2 group was composed of the remaining 5 lowland plots established
which were all located within the Cauca basin in the northeast part of the
Antioquia province (table 1). The three species with the highest contribution
to the total beta diversity belonging to the lowlands 2 forest type were Oenocarpus minor, Pourouma bicolor, and Virola
sebifera (table 2). The highlands forest type was dominated by Quercus humboldtii, which was the most
abundant species in the entire study area (table 2). The three highland species
that contributed most to beta diversity were Billia rosea, Q. humboldtii,
and Wettinia kalbreyeri. Understory
species, such as Miconia resima and Palicourea demissa had also an important
contribution to total beta diversity. For both the entire dataset and for only
the 30 species with the highest contribution to beta diversity, total abundance
was highly correlated with SCBD (r = 0.9 and r = 0.83, respectively).
Table
2. Species
contribution to beta diversity (SCBD %).
All 541 species included in the analysis add up to 1. The species presented
here are the 30 species with the highest values of SCBD organized in decreasing
order of importance by forest type
Determinants
of community composition and species turnover.
Soil fertility in the lowlands 1 forest, as represented by Ca, Mg, and pH, was
significantly higher than the soil fertility in the lowlands 2 and the highland
forests, which did not differ between each other. However, P concentrations
were higher in the highlands than in the lowlands (table 3). In the lowlands,
the correlations between Ca, K, and Mg with P were high, but none of them were
significant (table 4).
Table
3.
The mean and standard deviations of soil variables by forest type according to
the PCA on floristic composition. Except for pH, significance was evaluated on
the log-transformed values of all variables [NS = non significant; * = p ≤ 0.05; ** = p ≤
0.01; *** = p ≤ 0.001. Different
letters indicate significant differences (Tukey´s HSD test)]
Table
4.
Pearson correlation matrix for the log-transformed soil variables assessed in
this study (Upper right half panels: Highlands; lower left half panels: Lowlands; values in bold were significant; NS = non significant; * = P ≤ 0.05; ** = P ≤
0.01; *** = P ≤ 0.001)
In the lowlands,
Ca, longitude, and elevation were retained as significant explanatory variables
by the forward selection performed on the separated sets of edaphic, spatial,
and climatic explanatory variables, respectively. However, when we ran the
forward selection on just Ca, longitude, and elevation only Ca (R2 =
0.24; p = 0.001) remained in the model (figure 2A). Ca was the only variable
that remained in the model primarily due to the negative and significant
correlation with longitude (r = -0.72) and elevation (r = -0.61). The semi-log
linear models confirmed the importance of the increase in Ca contents in soils
(RMantel = 0.68; p = 0.006) as well as the increase in the
log-transformed geographical distances (RMantel = 0.49; p = 0.004)
as significantly associated with compositional turnover in the lowlands (figure
3), but not for elevation (RMantel = 0.25; p = 0.065). In the
highlands, the independent forward selection of the RDA on each of the edaphic,
spatial, or climatic explanatory set of factors only identified longitude as a
significant explanatory variable (R2 = 0.24). The spatial trend in
the plant community composition detected by the constrained RDA ordination was
determined primarily by the biogeographical location of the plots, which showed
a higher floristic similarity between plots located on either the West or the
Central Cordillera (figure 2B). However, the semi-log linear model did not
support a significant decrease in floristic similarity with the increase in
(log-transformed) geographic distances (RMantel = 0.23; p = 0.18;
figure 3).
Figure
2.
Redundancy Analysis after applying forward selection on both lowlands (A) and highlands (B)
Figure
3.
Distance-decay on species similarity for all significant variables submitted to
forward selection in the RDA both in lowlands and highlands. Similarity was
derived from a Hellinger distance and ranges between 0 and 2. The dashed line
represents the semi-log linear model that was significant and the continuous
line the semi-log linear models that were not significant according to the
Mantel test (see text)
DISCUSSION
We documented the
occurrence of three major forest types in the Northern Andean study region that
were dominated by different woody plant species. Highland plots (e.g., those
located above the cloud-base at 1700 m.a.s.l.) had higher dominance and
abundance of species when compared to lowland plots. For example, in the
highlands, Q. humboldtii was twice as
abundant as any species in the lowlands. Interestingly, the plot located at the
lowest elevation within the highland forest type (Anorí) had a mixture of
species typical of highlands, such as Billia
rosea and Q. humboldtii , and
species typical of the lowlands, such as Pouteria
torta and Virola sebifera,
emphasizing its location within an ecotonal climatic-zone. Gentry (1988)
proposed that some plant families, such as Arecaceae and Moraceae, are more
abundant and diverse in fertile soils, while others like Burseraceae,
Lauraceae, and Sapotaceae, are better-adapted to poorer soils. Although the
species that had the highest contribution to the total beta diversity in the
richer soils of lowlands belonged to the Moraceae family (Clarisia biflora), our results do not support this generalization.
Since some species belonging to the Arecaceae and Moraceae families, such as Pseudolmedia laevis and Oenocarpus minor, respectively, were
within the most important species for the total beta diversity in the poorer
soils of lowlands, we found it difficult to generalize any likely effect of
soils fertility on species distribution in the lowlands at taxonomic levels
higher than species.
We assessed the
degree to which various climatic, topographic and edaphic variables explain
floristic variation in contrasting forest types within this diverse and
understudied region of the Neotropics. Our findings did not shed support for
the generalized idea about a greater habitat-plant specialization in highlands
than in lowlands. Therefore, we reject the main hypothesis about the expected
congruence between either environmental or spatial structured factors that
determine species composition of tree communities in this region of the
northern Andes. Overall, in lowlands, deterministic processes associated with
internal ecotones defined by soil properties showed to be the main determinants
of tree species composition. In highlands, the biogeographical position along
the longitudinal axis created differences in tree community composition between
mountain ranges, which were likely driven by isolation due to the barrier
imposed by interandean valleys.
In lowland
forests, we found that changes in the floristic composition were primarily
explained by variation in soil fertility. This suggests that environmental
filtering may be the main mechanism determining the structure of the plant
community (Gentry 1988, Tuomisto et al.
2003). The fact that the Puerto Triunfo plot appeared as part of the lowlands 1 forest type, even though this plot is
located 400 km away from some of the other lowland 1 plots, and is separated
from the other lowland 1 plots by the mountain ranges of the Central and West
Cordilleras of Colombia and the coastal plains in the north, supports the idea
that sites with more similar soil characteristics tend to have greater
similarity in species composition regardless of distance or geographic
separation. Therefore, plant communities in the lowlands were clearly
non-randomly distributed and the associated tree communities could, to a
significant degree, be predicted based on environmental factors (Clark et al. 1999, Gentry 1988). Our findings
support the importance of niche differences in structuring tree communities
across large spatial scales in the lowlands of the Neotropics (Condit et al. 2013, Gentry 1988).
Although our model
identified Ca concentrations as the most-important explanatory variable for
species composition in the lowlands, the significant correlation of Ca with
both Mg concentration and soil pH, suggests a general soil fertility gradient
across the sites that distinguishes forest types within the lowlands.
Specifically, the lowlands 1 forests have relatively more fertile soils
compared to the lowlands 2 plots. These results are similar to those found in
other neotropical rainforests, where concentrations of Ca, K, Mg, and pH
controlled patterns of tree species composition in both canopy and understory species
(Duque et al. 2002, Phillips et al. 2003). As described by Condit et al. (2013), tree species may depend
on several nutrients in concert but with Ca and P generally being the two key
elements. In our case, there was little variation and low concentrations of P
in the lowland plots, which may explain why it was not identified as an
explanatory variable of tree community composition. Perhaps, a very high demand
of P in forests with high productivity has depleted the soil stock of this
important element.
Geographical
distances also played important roles in explaining the assemblages of species
in the lowlands, as suggested by the negative and significant relationship
between compositional similarity and the log-distances between plots. The fact
that longitude was not retained as an explanatory variable in the final RDA
model was primarily due to the co-linearity with Ca concentrations, which
correlation increases with distance. An additional partial Mantel test showed
that geographic distances remained significant on controlling the floristic
composition after accounting for the effects of Ca (RPartial.Mantel
= 0.38; p = 0.019). Disentangling how much of the influence of
spatially-structured soil components in structuring tree communities is due to
either the soils effect per se or to
spatially-structured biological processes such as dispersal limitation, has
previously been debated in plant communities (Duivenvoorden et al. 2002, Duque et al. 2009); in this particular case, it appears that plant
community composition within the lowlands is largely determined by soil
fertility (Garibaldi et al. 2014).
This contention is supported by the fact that plots located on similar soils
but with different geologies in different catchments showed high similarity in
their species composition. In contrast, in mountainous ecosystems of Costa
Rica, plots of canopy tree species located below 1500 m.a.s.l. showed
significant spatial autocorrelation at distances of up to 40 to 50 km and
biologically-structured factors such as dispersal limitation were proposed as
one of the major determinants of tree species distributions (Chain-Guadarrama et al. 2012).
Similar to
longitude, in the lowlands, elevation was not retained in the final RDA model
due to it being significantly correlated with Ca contents (RMantel =
0.33; p = 0.042). In studies of elevational gradients, local thermal conditions
have been found to play an important role in shaping species distributions and
compositional patterns (Feeley et al. 2013,
Hemp 2005). However, in the lowlands of our study area, the results of both
analyses were not conclusive due to the RDA and the semi-log linear models
producing different outputs at pinpointing elevation as a significant factor.
On the one side, according to the RDA model, we found a small but still
significant effect of temperature on the plant communities that was masked by
the correlation with Ca. Contrasting this, the log-linear model that tests the
neutral hypothesis of a constant decrease in species similarity with increasing
difference in elevation, did not support a significant effect of elevation on
structuring tree communities below 1000 m.a.s.l. (see also Chain-Guadarrama et al. 2012, Gentry 1995). A partial
Mantel test showed that elevation did not remain as a significant explanatory
variable of floristic changes after removing the effect of Ca (RPartial.Mantel
= 0.19; p = 0.11). More detailed analysis about thermal ranges of tree species
distributions at large geographical scales (e.g., Feeley et al. 2013) are still needed to improve the effectiveness of
conservation strategies aimed at ameliorating global warming effects in lowland
tropical forests.
In contrast to
expectations, in the highland forest plots, longitude was the only explanatory
variable significantly associated with tree community composition in the RDA
analysis (figure 3). Similar to elevation in lowlands, in the highlands, the
expected decrease in species similarity with the increase in the geographic
distance proposed by the neutral theory (Hubbell 2001) was rejected. Thus, the
significance of longitude in the RDA model as an explanatory variable of
floristic composition is in accord with the observations that tree species
composition was more similar between plots established on the same Cordillera
(either Central or Western; figure 2B). This may be due to the Cauca river
valley constraining the movement of propagules between mountain chains
producing an anisotropic effect (sensu
Tuomisto and Ruokolainen 2006) from east to west (and vice versa) in the tree
community composition. However, we acknowledge that additional studies with
increased sample sizes are needed to clarify this floristic-geographic
differentiation.
Another
explanation for the lack of environmental effects on floristic composition in
the highlands is the fact that soil fertility was fairly homogeneous between
sites. The highland plots were located on metamorphic and volcanic intrusive
rocks that originate in the West and Central Cordilleras, respectively. It is
expected that the volcanic intrusive rocks should have high soil fertility
because of its geological origin and high concentrations of volcanic ashes.
Therefore, some unknown processes may have driven soils fertility or nutrient
release to similar levels independent of their geological origin promoting the
relative floristic homogeneity found in this study, and thus, the lack of
significance of soils in determining tree communities in highlands. In the
highlands, for example, neither Ca nor P had any significant influence on structuring
highland tree communities. The lack of importance of P in the models could
indicate that P is not a limiting resource in these forests. Alternatively, the
relatively high P concentrations found in highland soils (in relation to
lowlands) may not be available for the plant uptake due to the low pH of the
soils that could promote P precipitation. However, a complementary explanation
to the lack of importance of environmental factors in structuring the highland
tree communities may be the existence of broad distributional ranges for many
species. Broad distributional ranges of species that occur within the
cloud-immersion zone may be the consequence of the regionally homogeneous soils
fertility as well as physiological adaptations to extreme climatic conditions
and variation (Stevens 1992).
The results of
this study proposes that different factor may play important roles on
determining the tree communities inhabiting the quite diverse forests of the
northern Andes in Colombia. Although in the whole study area either elevation
or temperature was the most important factor determining tree communities
(Duque et al. 2015), our findings
proposed that the extent and nature of the main factors determining species
composition varied according to the altitudinal position. Although additional
assessments of this question are needed, they emphasize on the need to develop
different strategies to protect the already quite endangered forests of this
region. In cases such as those found in lowlands, including within reserves as
much as possible of the environmental variation will be a key issue for
conservation. In highlands, on contrary, the larger the reserve the more
effective the conservation strategy will be.
It is important to
note that many Andean forests have been highly degraded and fragmented (Myers et al. 2000), which may limit seed
dispersal because of the lack of connectivity and forest continuity in the
region. In fact, in the northwest Andean lowlands of Colombia and their
surroundings, where forest occupancy by human beings spans several centuries,
the local populations of plant species may be a product of physical and genetic
isolation. Species isolation by habitat loss and forest fragmentation
represents a major threat to this extremely diverse area of the Neotropics and
will likely drive local and global extinctions if we do not stop the current
deforestation trends (Duque et al.
2014). Since tropical Andean ecosystems, and in particular highland forests,
have received less attention than their lowland counterparts, our findings help
to expand the current knowledge on these important habitats.
ACKNOWLEDGEMENTS
We thank Fundación
Berta Arias, CORANTIOQUIA, Fundación Colibrí, Empresas Pecuarias del Bajo
Cauca, Mineros S. A., Rodrigo Celis, and Andrés Upegui for allowing us to
install and maintain the plots on their properties. The authors are grateful to
James Dalling for his comments and suggestions to a prior version of this
manuscript. We also thank Herbarium Universidad de Antioquia for allowing the
identification and storage of collections. A. Duque was funded by a Visitant
Researcher Fulbright Colombia grant (2014-2015) that was hosted in Miami (FL,
U.S.A.) by the International Center for Tropical Botany at Florida
International University and the Fairchild Tropical Botanic Garden. K. J.
Feeley is supported by the U.S. National Science Foundation (DEB-1350125).
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