Environmental and historical controls of floristic composition across the South American Dry Diagonal

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ORIGINAL
ARTICLE
Environmental and historical controls of
floristic composition across the South
American Dry Diagonal
1
Danilo M. Neves
1,2
*, Kyle G. Dexter
1,3
,R. Toby Pennington
1
,
Marcelo L. Bueno
2
and Ary T. Oliveira Filho
2
2
1
Royal Botanic Garden Edinburgh, Edinburgh,
Midlothian EH3 5LR, UK,
2
Programa de
P
os-Graduac
ß
~
ao em Biologia Vegetal,
Universidade Federal de Minas Gerais –
UFMG, Campus Pampulha, Belo Horizonte,
MG 31270–090, Brazil,
3
School of
GeoSciences, University of Edinburgh, King’s
Buildings, Edinburgh, Midlothian EH9 3JN ,
UK
*Correspondence: Danilo M. Neves, Royal
Botanic Garden Edinburgh, 20a Inverleith
Row, Edinburgh, Midlothian EH3 5LR, UK.
E-mail: danilormn@gmail.com
ABSTRACT
Aim The aim of this study was to test the role of environmental factors and
spatially autocorrelated processes, such as historical fragmentation and dispersal
limitation, in driving floristic variation across seasonally dry tropical forests
(SDTFs) in eastern South America.
Location SDTFs extending from the Caatinga phytogeographical domain of
north-eastern Brazil to the Chaco phytogeographical domain of northern
Argentina, an area referred to as the Dry Diagonal.
Methods We compiled a database of 282 inventories of woody vegetation in
SDTFs from across the Dry Diagonal and combined this with data for 14 envi-
ronmental variables. We assessed the relative contribution of spatially autocor-
related processes and environmental factors to the floristic turnover in SDTFs
across the Dry Diagonal using variation partitioning methods. In addition, we
used multivariate analyses to determine which environmental factors were most
important in explaining the turnover.
Results We found that the environmental factors measured (temperature, pre-
cipitation and edaphic conditions) explained 21.3% of the variation in species
composition, with 14.1% of this occurring independently of spatial autocorre-
lation. A spatially structured fraction of 4.2% could not be accounted for by
the environmental factors measured. The main axis of compositional variation
was significantly correlated with a north–south gradient in temperature regime.
At the extreme south of the Dry Diagonal, a cold temperature regime, in which
frost occurred, appeared to underlie floristic similarities between chaco wood-
lands and southern SDTFs.
Main conclusions Environmental variables, particularly those related to tem-
perature regime, seem to be the most significant factors affecting variation in
species composition of SDTFs. Thus historical fragmentation and isolation
alone cannot explain the turnover in species composition within SDTFs, as is
often assumed. Compositional and environmental heterogeneity needs to be
taken into account both to understand the past distribution of SDTFs and to
manage and conserve this key tropical biome.
Keywords
Caatinga woodlands, chaco woodlands, environmental niche, Pleistocene
arc hypothesis, seasonally dry tropical forests, species turnover, variation
partitioning.
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ª2015 John Wiley & Sons Ltd http://wileyonlinelibrary.com/journal/jbi 1
doi:10.1111/jbi.12529
Journal of Biogeography (J. Biogeogr.) (2015)
J B I 12529
Dispatch: 10.4.15 CE: Malarvizhi
Journal Code Manuscript No.
No. of pages: 11 PE: Pravin Kumar

INTRODUCTION
Seasonally dry tropical forests (SDTFs) occur as fragments of
varying size throughout Latin America, from northern
Argentina and north-east Brazil to north-west Mexico (Pen-
nington et al., 2006). These SDTFs comprise a recognized
biome (Pennington et al., 2000, 2009) that is characterized
by <1600 mm precipitation year
1
, a marked dry season of
5–6 months and high rates of deciduousness during the dry
season (Bullock et al., 1995; Gentry, 1995; Oliveira-Filho
et al., 2006). SDTFs have received increased attention in
recent years because of both their highly threatened status
(e.g. Mooney et al., 1995; Pennington et al., 2006, 2009; Dir-
zo et al., 2011) and the influential Pleistocene Arc Hypothe-
sis (PAH; Prado & Gibbs, 1993; Pennington et al., 2000).
The PAH postulates that SDTFs had a more widespread and
contiguous distribution in South America during Pleistocene
glaciation phases, including areas that are currently covered
by rain forest or savanna. The PAH is based upon the wide-
spread distributions of multiple, unrelated tree species found
in disjunct SDTF areas from north-east Brazil through cen-
tral and southern Brazil to Paraguay and Argentina and, in
some cases, as far as the dry inter-Andean valleys of western
South America. It is suggested that the putative Pleistocene
Arc, a more continuous area of SDTF, connected these areas
during the cooler and drier climates of Pleistocene glacia-
tions (Prado & Gibbs, 1993; Pennington et al., 2000).
Subsequent research, however, has shown that these wide-
spread species represent a small minority of SDTF tree spe-
cies and that floristic variation between SDTF sites across the
Neotropics is high (e.g. Gillespie et al., 2000; Trejo & Dirzo,
2002; Linares-Palomino, 2006; Lott & Atkinson, 2006; Pen-
nington et al., 2006; Queiroz, 2006; Castillo-Campos et al.,
2008; Linares-Palomino et al., 2011). For instance, Linares-
Palomino et al. (2011) found that less than 2% of 3839
SDTF tree species are found in 10 or more of 21 disjunct
SDTF nuclei across the Neotropics. On the other hand, the
same authors (Linares-Palomino et al., 2011) found higher
floristic similarity (Sørensen similarity index values >0.25)
among SDTF nuclei in Brazil and southern South America
and suggested that this offers some support for the idea that
SDTF was more widespread and continuous within this
region during Pleistocene glacial phases.
When explaining the disjunct distributions of SDTF spe-
cies and floristic variation of SDTFs in general, recent studies
have focused primarily on the role of historical biogeograph-
ical processes, namely habitat fragmentation and dispersal
limitation (e.g. Pennington et al., 2006, 2009). However,
environmental conditions are also expected to affect species
distribution. This study is the first to examine the role of
environmental, primarily climatic, determinants in shaping
the distribution of tree species across a large expanse of
Neotropical SDTF sites.
We aimed to test the role of historical fragmentation and
dispersal limitation versus environmental factors in driving
floristic differentiation among SDTFs across eastern South
America. Understanding the roles of these two processes is
an important and unsolved issue in many systems (e.g. in
the Amazon: Haffer, 1969; ter Steege et al., 2006; 3in the Cer-
rado: Werneck et al., 2012a; in South American subtropical
forests: Oliveira-Filho et al., 2013). Variation partitioning
methods provide a means of assessing the relative contribu-
tion of measured environmental factors and spatially auto-
correlated processes (potentially including unmeasured
environmental factors) in driving species turnover (Legendre
et al., 2012). This approach has been used mostly at small
spatial scales (e.g. within plots; Legendre et al., 2009) to
address the influence of steady-state, small-scale dispersal
limitation. However, it can also be used at much broader
spatial scales (Vetaas & Ferrer-Cast
an, 2008) to address habi-
tat fragmentation and isolation at historical time-scales, and
may be particularly useful in ecosystems with limited palaeo-
ecological data, such as SDTFs.
We compiled a database of SDTF floristic inventories from
sites extending from the caatinga woodlands of north-eastern
Brazil to the chaco woodlands of northern Argentina, an area
referred to as the Dry Diagonal (following Prado & Gibbs,
1993; also see Vanzolini, 1963; Werneck et al., 2012b). This
region was particularly appropriate because it was the main
area studied by Prado & Gibbs (1993) in the development of
the PAH and because it has been the target of previous stud-
ies on SDTF biogeography (de Andrade-Lima, 1954, 1982;
Ratter et al., 1988; Caetano & Naciri, 2011; Werneck et al.,
2011; Collevatti et al., 2012, 2013a,b). If the floristic varia-
tion of SDTFs is solely the result of fragmentation and subse-
quent dispersal limitation between SDTF patches, climatic
and edaphic variables should not be important factors in
explaining the variation in community composition. Alterna-
tively, if previously unrecognized environmental conditions
within SDTFs are the principal factors driving floristic turn-
over, then climatic and edaphic factors should explain a large
proportion of the variation in community composition.
MATERIALS AND METHODS
Study area
The Dry Diagonal stretches from north-eastern Brazil to
Argentina, Paraguay and Bolivia, and occurs primarily in
three phytogeographical domains (IBGE, 1993) that are
named after the main vegetation types that occur within them:
Caatinga (tropical semi-arid thorn woodlands, called caatinga
woodlands in Brazil), Cerrado (seasonal woody savannas,
called cerrado woodlands in Brazil) and Chaco (subtropical/
tropical semi-arid thorn woodlands, called chaco woodlands
in Brazil and elsewhere) (Fig. 1). Prado & Gibbs (1993)
defined three major nuclei of SDTFs in the Dry Diagonal: (1)
the Caatinga nucleus, which occurs in north-eastern Brazil
and is the largest nucleus (essentially the same area as the Ca-
atinga phytogeographical domain); (2) the Misiones nucleus,
which extends from the lower course of the Paraguay and
Paran
a rivers to the upper Uruguay River in Misiones,
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Argentina; and (3) the Piedmont nucleus, which occurs along
the eastern base of the Andes in north-eastern Argentina.
SDTFs also occur in the Chiquitania region of Bolivia (Lin-
ares-Palomino et al., 2011) and in patches scattered through-
out the Cerrado phytogeographical domain (Ratter et al.,
1988; Pennington et al., 2000) in areas of fertile soil.
One environmental element in the definition of SDTFs is
that they are a frost-free vegetation (Prado, 1993a,b; Pen-
nington et al., 2000), which would suggest that the chaco
woodlands, found in northern Argentina, western Paraguay,
south-eastern Bolivia and the extreme western edge of Mato
Grosso do Sul state in Brazil, are not SDTFs because they
suffer regular winter frost. However, large areas delimited as
SDTF in the schematic maps of previous studies (e.g. Pied-
mont and Misiones; Prado & Gibbs, 1993; Oliveira-Filho
et al., 2006; Pennington et al., 2009) also receive significant
frost (see Results). Thus we chose to include the chaco
woodlands in our analyses because they meet other criteria
of SDTF vegetation as defined by the same authors (Prado,
1993a,b; Pennington et al., 2000), such as seasonality of rain-
fall and deciduousness.
The SDTF database
We extracted floristic inventory data from the NeoTropTree
database (available at http://prof.icb.ufmg.br/treeatlan). This
database consists of >2000 georeferenced localities for which
lists of tree species (trees defined here as woody plants
>3 m in height) were compiled from an extensive survey of
published and unpublished literature. A NeoTropTree site is
defined by a single vegetation type contained within a circu-
lar area with a 5-km radius. Therefore, where two or more
vegetation types co-occur in one 10-km area, there may be
two geographically overlapping sites in the NeoTropTree
database, each for a distinct vegetation type. The NeoTrop-
Tree data were derived primarily from inventories of woody
vegetation (i.e. plots, transects and vegetation surveys). Sur-
veys of specimens at major herbaria were then used to aug-
ment the lists for each NeoTropTree site with any tree
species that were collected within the 5-km radius of the ori-
ginal NeoTropTree site and within the same vegetation type.
Moreover, all NeoTropTree species were checked regarding
their taxonomy and synonymies by using the Flora do Brasil
Figure 1 5
Map showing the location of tree species surveys and major vegetation types used for the study of environmental and
historical controls of floristic composition across the South American Dry Diagonal. Circles denote the location of tree species surveys
used in this study (n=282). The phytogeographical domains that form the South American Dry Diagonal are shaded (Ca, Caatinga;
Ce, Cerrado; Ch, Chaco; Cq, Chiquitania) while moist forest phytogeographical domains are white (Am, Amazon rain forest; At,
Atlantic rain forest). The Misiones and Piedmont seasonally dry tropical forest (SDTF) nuclei (Prado & Gibbs, 1993) are delimited by
dashed lines (1, Misiones; 2, Piedmont); the Caatinga nucleus covers the same area as the Caatinga phytogeographical domain. The
phytogeographical domains are named after the major vegetation type that occurs within them (e.g. chaco woodlands, caatinga
woodlands and savanna vegetation; the latter is called Cerrado in Brazil). Note that each phytogeographical domain may contain several
additional vegetation types (e.g. the Cerrado phytogeographical domain contains SDTF and gallery forest in addition to the main
vegetation type of savanna).
LOW RESOLUTION FIG
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Environmental controls of floristic variation in dry forests
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database for plants that occur in Brazil, and the Tropicos
database for plants that do not occur in Brazil (available at
http://floradobrasil.jbrj.gov.br/ and http://tropicos.org/,
respectively). NeoTropTree does not include occurrence
records without an indication or evidence of vegetation type,
nor sites with very incomplete species lists. The latter is an
important filter because different sampling efforts across sites
may bias their descriptive power.
The 282 NeoTropTree inventories used in this study com-
prised 134 SDTF sites from the Caatinga phytogeographical
domain, 14 from the Misiones nucleus, five from the Pied-
mont nucleus, 91 from SDTF enclaves scattered throughout
the Cerrado phytogeographical domain, six from the Bolivian
Chiquitania and 32 chaco woodland sites from the Chaco
phytogeographical domain. This does not represent an even
geographical coverage of inventories, but we believe our
results are not excessively biased because nuclei covered by
just a few sites often had many species, whereas nuclei with
many sites could only have a few species. For example, the
Misiones nucleus was represented by 398 species from just
14 lists, whereas 891 species were recorded from 134 lists
from the Caatinga phytogeographical domain. The final spe-
cies matrix contained presence–absence data for 1765 tree
species across the 282 SDTF sites, with a total of 25,650 pres-
ences (Fig. 1).
The NeoTropTree database also included environmental
data for all its sites, derived from multiple sources. Eight
variables were related to edaphic substrate: mean, mini-
mum and maximum monthly soil moisture (%), obtained
from the International Soil Moisture Network (http://
www.ipf.tuwien.ac.at/insitu/); prevailing slope and aspect,
obtained from CGIAR-CSI (2006); and soil fertility (%
base saturation), soil coarseness (% sand) and substrate
rockiness (% surface of rock outcrops), extracted from a
detailed map of soil types produced by EMBRAPA &
IBGE (2003) using the RadamBrasil Soil Survey of the
1970s and 1980s. Climatic variables included the mean
duration (days) and severity (mm) of water-deficit periods,
both extracted from Walter diagrams (Walter, 1985); the
19 bioclimatic variables produced by WorldClim 1.4, a
high-resolution (1-km) database of global climate layers cre-
ated by Hijmans et al. (2005); mean frequency of frosts (days),
cloud cover (%) and cloud interception (mm), obtained from
gridded datasets produced by Jones & Harris (2008); and three
additional variables, potential and actual evapotranspiration
(mm) and an aridity index, derived from WorldClim by Zo-
mer et al. (2007, 2008). A full description with details of the
protocols for NeoTropTree can be found at http://prof.ic-
b.ufmg.br/treeatlan.
Analyses of species composition
We first explored the patterns of similarity in community
composition by conducting a hierarchical clustering analysis
of all 282 sites. We used Jaccard distance as the dissimilarity
metric and unweighted paired groups as the linkage method
(McCune & Grace, 2002). We assessed the confidence for
each node of the hierarchical cluster using multi-scale boot-
strapping (Shimodaira, 2004) in the pvclust package (Su-
zuki & Shimodaira, 2011) in the R statistical environment (R
Core Team, 2012) 4. Because singletons (species found at a
single site) commonly increase the intrinsic noise in most
analyses without contributing information (Lep
s&

Smilauer,
2003), we excluded the 318 singleton species from this and
all subsequent analyses.
We obtained the relative contribution of measured envi-
ronmental factors and unmeasured spatially autocorrelated
factors in explaining variation in community composition
by following methods similar to those proposed by Dray
et al. (2012) and Legendre et al. (2012). This routine com-
prises (1) the compilation of significant spatial and environ-
mental variables through a forward selection method for
canonical correspondence analysis (CCA), with a permuta-
tion-based test for each variable added (Borcard et al.,
2011); (2) an additional and progressive elimination of col-
linear variables based on their variance inflation factor
(VIF) until maintaining only those with VIF <10 (Quinn
& Keough, 2002); and (3) variation partitioning of the
community composition matrix with respect to the signifi-
cant spatial and environmental variables. As spatial vari-
ables, we used Moran’s eigenvector maps (MEMs), which
represent the diagonalization of a centred spatial weighting
matrix (Dray et al., 2012). We tested the overall significance
of the spatial fraction (controlled for measured environmen-
tal variation) and the environmental fraction (controlled for
spatial autocorrelation) by applying a permutation test (999
permutations) for CCA. All variation partitioning analyses
were conducted using the spacemakeR (Dray, 2010), spdep
(Bivand, 2012), tripack (Gebhardt, 2009) and vegan (Oksa-
nen et al., 2012) packages in the R statistical environment
(R Core Team, 2015).
We also performed a detrended correspondence analysis
(DCA) to derive orthogonal eigenvectors representing gradi-
ents in floristic variation and used post hoc correlations to
assess their relationship with environmental factors. We
tested the significance of the post hoc correlation coefficients
by applying a permutation test (999 permutations). There
was a negligible increase in explained variation with the
addition of >2 DCA axes, and we therefore focused on the
first two axes for comparisons with environmental variables.
We also explored the results visually by plotting the site
scores of the DCA axes and the values of the environmental
variables in geographical space. These analyses were per-
formed in the statistical package vegan (Oksanen et al.,
2012) and the maps were designed using the package map-
tools (Lewin-Koh & Bivand, 2012), both in the R statistical
environment.
RESULTS
The hierarchical clustering results were largely congruent
with the previously defined SDTF nuclei. The classification
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segregated the 282 sites into two principal groups, hereafter
termed the northern and southern groups. The northern
group consisted of 232 sites from the Caatinga nucleus,
Cerrado phytogeographical domain SDTFs and Bolivian
Chiquitania, whereas the southern group consisted of 50
sites from the Misiones and Piedmont nuclei and the chaco
woodlands from the Chaco phytogeographical domain
(Fig. 2).
The forward selection procedure retained 14 out of 36
environmental variables for modelling variation in species
composition (Table 1). After partitioning the variation
explained by the selected spatial and environmental predic-
tors, we found that the measured environmental factors
explained 21.3% of the variation in species composition,
with 14.1% of this occurring independently of spatial auto-
correlation. A spatially structured fraction of 4.2% could not
be accounted for by the measured environmental factors;
74.5% of the variation remained unexplained (Fig. 3).
When investigating which environmental variables
explained species turnover across the Dry Diagonal, we
found that the variation in species composition summarized
by the first DCA axis revealed a large-scale gradient (Fig. 4a)
that was correlated with a north–south gradient in the mean
minimum temperature of the coldest month (Fig. 4c,
Table 1). The first DCA axis was also congruent with a
north–south segregation in days of frost (dashed black line
in Fig. 4a). The mean minimum of the coldest month in
southern SDTFs ranged from 0.1 °C to 15.4 °C, while some
southern SDTFs, such as those from the Piedmont nucleus,
could experience up to 18 days of frost. In the northern
group, four sites experienced up to 3 days of frost, while the
other 228 sites experienced none. The first DCA axis was also
correlated with a north–south gradient in isothermality
(Fig. 4e, Table 1), suggesting that the high seasonality,
including both hot summers and winter frosts in the south-
ern group, was a relevant factor driving variation in commu-
nity composition.
The community composition variation summarized by the
second DCA axis revealed a rainfall gradient that was most
strongly correlated with the precipitation of the wettest
month (Fig. 4d, Table 1). In fact, the species composition
variation summarized by the second DCA axis was congruent
Figure 2 Hierarchical clustering of seasonally dry tropical forests (SDTFs) and chaco woodlands across the South American Dry
Diagonal based on their tree species composition. The dissimilarity measure and linkage methods used were Jaccard and unweighted
group average, respectively. Black bullets at the base of clusters indicate approximately unbiased bootstrap values ≥0.90 (Suzuki &
Shimodaira, 2011). The size of the triangles is proportional to the number of sites, and the floristic nuclei are discriminated by different
colours: red, 134 caatinga woodlands; orange, 91 Cerrado SDTFs; yellow, six SDTFs from Chiquitania; green, 14 SDTFs from Misiones;
light blue, five SDTFs from Piedmont; dark blue, 32 chaco woodlands.
Table 1 Environmental variables selected for the study of
environmental controls of floristic composition across the South
American Dry Diagonal. The variables shown are ordered by the
post hoc correlation coefficient with the first detrended
correspondence analysis (DCA) axis. The post hoc correlation
coefficient of each environmental variable with the second DCA
axis is also shown. VIF, variance inflation factor, obtained using
the r-squared value of the regression of one variable against all
other explanatory variables; n.s., not significant; P<0.05, except
for n.s. correlation coefficients.
Variables
DCA
1
DCA
2 VIF
Isothermality 0.62 0.06 7.64
Minimum temperature of the coldest
month
0.52 n.s. 8.43
Severity of water deficit 0.48 0.02 8.87
Precipitation of the driest month 0.34 0.03 7.57
Cloud cover 0.32 0.12 4.08
Sediment coarseness 0.31 n.s. 4.85
Days of frost 0.21 n.s. 3.08
Soil fertility 0.13 0.02 5.43
Soil water storage capacity 0.09 0.44 9.29
Precipitation of the coldest quarter 0.03 0.04 3.74
Precipitation of the wettest month 0.02 0.43 7.47
Elevation 0.01 0.04 3.69
Surface rockiness 0.01 n.s. 2.02
Cloud interception 0.01 0.02 1.45
COLOR
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with most of the precipitation-related variables (Table 1),
segregating a dry group (Caatinga nucleus, chaco woodlands,
Piedmont nucleus and Bolivian chiquitania) from a wet
group (Cerrado phytogeographical domain SDTFs and Misi-
ones nucleus). Furthermore, the second DCA axis correlated
with maximum soil water storage capacity (Fig. 4f), suggest-
ing an interaction between rainfall and soil characteristics in
driving the turnover in species composition summarized by
this axis.
DISCUSSION
Previous large-scale floristic analyses of South American
SDTFs have focused on historical fragmentation and dis-
persal limitation when explaining patterns of species turn-
over within communities (e.g. Pennington et al., 2006,
2009; Linares-Palomino et al., 2011). Our analyses indicate
that climatic and edaphic conditions also merit attention.
Because of the strong environmental correlations we found
(Table 1), it is inappropriate to designate historical frag-
mentation and dispersal limitation as the sole factors shap-
ing species composition in SDTFs. Most of the variation in
species composition that we were able to explain was
assigned to environmental factors that were independent of
spatial autocorrelation (14.1%). On the other hand, another
7.2% of the variation was accounted for by spatially struc-
tured environmental variation, signifying that the predic-
tions made by spatial and niche-based models converged.
However, considering that correlations between community
composition and environmental variables are known to be
important to plants (discussed below), we believe that it is
more parsimonious to attribute most of the spatially struc-
tured environmental variation to niche-based controls (cf.
Legendre et al., 2009).
At a broad scale within the South American tropics, pre-
cipitation regime is likely to be a primary determinant of the
presence versus absence of an SDTF; at a much smaller spa-
tial scale (within north-eastern and central-western Brazil),
Santos et al. (2012) found that precipitation regime was the
chief factor determining the species composition of SDTF
communities. Nevertheless, in analysing SDTF communities
at a larger spatial scale across the entire Dry Diagonal, we
found temperature-related variables to be the most signifi-
cant factors affecting variation in species composition within
SDTFs and chaco woodlands. In agreement with this result,
the fundamental division in our clustering analysis was
between two geographically segregated groups, with the
northern group experiencing mild temperatures in the cold-
est month, no frost (except for three sites with ≤3 days frost
year
1
) and a low annual temperature range compared with
the southern group.
This fundamental latitudinal division reflects marked dif-
ferences in the frequencies of species from different families.
Species in the Leguminosae, Bignoniaceae, Moraceae and An-
nonaceae are more frequent in the northern group, which
indicates that the northern flora primarily comprise species
incapable of coping with freezing temperatures. Punyasena
et al. (2008) classified these families as temperature-sensitive
because their abundance and richness decrease in low tem-
peratures. Meanwhile, Lauraceae, Asteraceae and Melastom-
ataceae have higher frequencies in the cooler southern group.
Rainfall regime correlated strongly with the second gradi-
ent of species composition, as summarized by the second
DCA axis. The precipitation division reflects the fact that the
relative frequencies of Leguminosae, Capparaceae and Polyg-
onaceae are higher in drier areas, whereas the relative fre-
quencies of Rubiaceae, Moraceae, Arecaceae and Annonaceae
are higher in wetter areas. The lower frequencies of the latter
families in the drier areas match the results of Punyasena
et al. (2008), who showed that their abundance and richness
decrease in areas with marked drought.
The distinctiveness of the chaco woodlands
Previous authors have excluded the chaco woodlands from
the SDTF biome, citing floristic differences, with the expla-
0 102030405060708090100
% variation
Environmental
variation
Spatial
structure
(a)
14.1
(b)
7.2
(c)
4.2
Unexplained
74.5
Figure 3 Variation partitioning by canonical correspondence analysis to determine how much of the spatial variation in floristic
composition across the South American Dry Diagonal was accounted for by the environmental variables measured. Fraction (a)
represents non-spatial environmental variation, fraction (b) spatially structured environmental variation, i.e. the overlap between
environmental and spatial components, and fraction (c) the spatial structure not explained by the measured environmental variables. All
values are expressed as percentages.
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nation that SDTF occurs only in frost-free areas (Prado,
1993a,b; Pennington et al., 2000; Werneck et al., 2011).
However, we found that the sites we analysed in the Chaco
domain were compositionally similar to southern SDTFs
(Fig. 4a; additionally some Chaco domain sites clustered
with SDTFs from the Cerrado domain and vice versa in
Fig. 2). In fact, the chaco woodlands from our dataset shared
82% of their species with at least one of the SDTF nuclei of
the Dry Diagonal. These results, combined with the finding
that many sites considered as SDTF experience significant
frost (e.g. in the Piedmont and Misiones nuclei), suggest that
the chaco woodlands may not be abruptly distinct from
SDTFs and they may represent one extreme of a floristic gra-
dient driven primarily by temperature. In support of the idea
of chaco woodlands being at one end of an SDTF tempera-
ture gradient, a previous study (Sarkinen et al., 2011) found
that 8.4% of SDTF specialist species occurred in the Chaco
phytogeographical domain. However, further analyses of sites
across the Chaco domain and surrounding areas are needed
to address its distinctness versus similarity compared with
(a) (b)
(c) (d)
(e) (f)
Figure 4
6Geographical variation in
seasonally dry tropical forest (SDTF) and
chaco woodlands characteristics across the
South American Dry Diagonal. The
northern group from the hierarchical
clustering analysis is discriminated by
triangles and the southern group by bullets
(see Figs 1 and 2 and Results). Values are
illustrated by the colour of the symbols:
warmer colours indicate higher values.
Numbers in the header for each panel
indicate minimum and maximum values.
(a) Scores from the first axis of the
detrended correspondence analysis (DCA)
analysis of species community composition.
The black dashed line delimits frost-free
(northern SDTFs) and frost-affected
(southern SDTFs and chaco woodlands)
areas; (b) scores from the second DCA axis;
(c) mean minimum temperature of the
coldest month; (d) precipitation of the
wettest month; (e) isothermality; and (f)
maximum soil water storage capacity.
LOW RESOLUTION COLOR FIG
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Neotropical SDTFs, in particular analyses that focus on the
potentially distinct edaphic conditions often present in the
Chaco phytogeographical domain (i.e. hypersaline soils)
(Prado, 1993a).
Affinities of the arboreal caatinga
Within northern SDTFs, Santos et al. (2012) classified the
arboreal caatinga (sites that occur along the border with
the Cerrado phytogeographical domain) as part of the Ca-
atinga nucleus. However, performing the hierarchical clus-
tering with a larger database we found that the arboreal
caatinga (shown as red within the orange Cerrado phyto-
geographical domain cluster in Fig. 2) is more similar to
SDTFs found in the Cerrado phytogeographical domain
(support value ≥0.9 in Fig. 2), which could be related to
edaphic similarities between arboreal caatinga and the the
Cerrado phytogeographical domain SDTFs (calcareous, rich
soils). The soil fertility (measured as a percentage of base
saturation), for instance, of the arboreal caatinga and Cer-
rado phytogeographical domain SDTFs from our database
were 57 2 (mean SD) and 46 13, respectively,
whereas other caatinga woodlands had poorer soils
(35 14).
Unexplained variation
While the environmental correlates of species composition
in SDTF were fairly clear and straightforward to interpret,
we still failed to explain a large fraction (74.5%) of the
variation in species composition. There are many poten-
tially important factors in determining the species composi-
tion of assemblages that we have not accounted for
adequately, such as: (1) ecological drift (cf. Hubbell, 2001)
driving stochastic rearrangements of species distribution
ranges through time; (2) biotic processes that were not
measured (e.g. competition and natural enemies); (3) false
absences in the surveys (e.g. researcher error and misiden-
tification of species); (4) unmeasured descriptors of habitat
quality (e.g. succession stage and degree of land degrada-
tion); (5) unsaturation, i.e. when species do not occupy all
patches of suitable habitat (Titeux et al., 2004); and (6)
other spatially and non-spatially structured environmental
factors that were not measured. Moreover, a high propor-
tion of unexplained variation, ranging from about 33% to
75% (e.g. Legendre et al., 2009; Oliveira-Filho et al., 2013;
reviewed in Soininen, 2014), is a common outcome in
studies of floristic composition over similar spatial scales,
as statistical noise is very high in analyses with species
presence–absence data (ter Braak, 1986; Guisan et al.,
1999).
Concluding remarks
Our demonstration that the floristic composition of SDTFs
is highly correlated with temperature regime (variation in
species composition summarized by the first DCA axis in
Table 1) suggests that SDTF formations would have been
affected by Pleistocene climatic changes (cf. Prado & Gibbs,
1993; Pennington et al., 2000), assuming that species occu-
pied similar climatic niches in the Pleistocene as they do at
present. However, these climatic relationships may have had
more complex effects than producing a simple Pleistocene
arc of SDTF. Palaeoecological studies are beginning to reveal
this complexity (Behling & Lichte, 1997; Burbridge et al.,
2004; Whitney et al., 2011, 2013) and more such studies are
needed. Palaeodistribution modelling also holds promise for
understanding the past distribution of SDTFs (cf. Werneck
et al., 2011) but, given the high floristic variation of SDTFs
documented here, SDTFs clearly cannot be treated as a single
unit (as in Werneck et al., 2011). Rather, the distributions of
floristically homogeneous subunits of SDTFs and/or individ-
ual species should be modelled, both to understand the past
distribution of SDTF and its future under global climate
change.
Regarding the identity of SDTFs of the Dry Diagonal,
our results showed that the chaco woodlands are not as
floristically distinct from the other SDTFs of the Dry
Diagonal as has been assumed previously. Also, the second
DCA axis supports the view that these southern sites have
floristic similarities with various sites of the northern
group (i.e. the Misiones nucleus grouping with the Cerra-
do phytogeographical domain SDTFs and chaco woodlands
grouping with the Caatinga nucleus; Fig. 4b). Therefore,
we suggest that the identity of the chaco woodlands and
how they relate to surrounding SDTFs merits further
attention.
Finally, we highlight the necessity of revisiting conserva-
tion priorities for dry forests in Brazil. Our results demon-
strate the floristic similarity between the arboreal caatinga
and SDTFs from the Cerrado phytogeographical domain,
suggesting they have equal conservation merit in terms of
their flora. However, under the current Brazilian environ-
mental law the arboreal caatinga receives full protection,
whereas other SDTFs that are equally important, such as
the Cerrado domain SDTFs, are unprotected and highly
threatened.
ACKNOWLEDGEMENTS
D.M.N. thanks the Brazilian government funding agency
CAPES for supporting a 12-month study period at the Royal
Botanic Garden Edinburgh (grant BEX 2415/11-9), where
most of the ideas for this study were developed. D.M.N. and
A.O.F. received additional funding from Conselho Nacional
de Pesquisa Cient
ıfica–Brazil (CNPq). D.M.N. and R.T.P.
were supported by the National Environmental Research
Council (grant NE/I028122/1). K.G.D. was funded by an
NSF International Research Fellowship (OISE-1103573) dur-
ing the time this research was completed. We are indebted
to Ole Vetaas and the anonymous referees for their valuable
contributions to the manuscript.
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DATA ACCESSIBILITY
A full description with details of data accessibility for Neo-
TropTree can be found at http://prof.icb.ufmg.br/treeatlan
BIOSKETCH
Danilo M. Neves is a Brazilian Research Fellow at the
Royal Botanic Garden Edinburgh, UK. He is interested in
tropical ecology and evolutionary biology of plants, with an
emphasis on niche evolution of Neotropical trees.
Author contributions: D.M.N., K.G.D. and A.O.F. designed
the paper; D.M.N., A.O.F. and M.L.B. assembled the data-
base; D.M.N. and K.G.D. analysed the data; A.O.F. and
M.L.B. commented on earlier versions of the manuscript;
D.M.N., K.G.D. and R.T.P. led the writing. All authors read
and approved the final manuscript.
Editor: Ole Vetaas
Journal of Biogeography
ª2015 John Wiley & Sons Ltd
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