An Acad Bras Cienc (2022) 94(1): e20201079 DOI 10.

1590/0001-3765202220201079
Anais da Academia Brasileira de Ciências | Annals of the Brazilian Academy of Sciences
Printed ISSN 0001-3765 I Online ISSN 1678-2690
www.scielo.br/aabc | www.fb.com/aabcjournal

ECOSYSTEMS

Reference values and drivers of diversity for

South Brazilian grassland plant communities

LUCIANA S. MENEZES, CLEUSA V. ELY, DIÓBER B. LUCAS, GRAZIELA H. MINERVINI-

SILVA, EDUARDO VÉLEZ-MARTIN, HEINRICH HASENACK, RAFAEL TREVISAN, ILSI
IOB BOLDRINI, VALÉRIO D. PILLAR & GERHARD E. OVERBECK

Abstract: The South Brazilian grasslands (Campos Sulinos) form the dominant
vegetation in southern Brazil. They are species-rich ecosystems that occur under distinct
geomorphological and climatic conditions but spatial variation of plant species diversity
remains understudied. Here, we present a detailed description of plant communities
across the region. Our data were obtained in 1080 plots, representing well-preserved
grasslands in different ecological systems. Apart from describing alpha and beta diversity,
we investigated the relations of plant communities with environmental features. We
identified 759 plant species and found clear differences in community composition
across the region. Northern and Southern highland grasslands, humid and dry coastal
grasslands and the mesic Pampa grassland were clearly distinct, related to climatic and
edaphic features. While species abundance distribution was markedly uneven, local
species richness was high, above 20 species/m2, especially in the highlands and in mesic
Pampa sites, on shallow soils. The predominant component of beta diversity was species
turnover, which suggests that a network of well-conserved grasslands distributed across
the region would be the best strategy to protect plant diversity. Our results establish
regionalized reference values for richness and diversity that can be useful for initiatives
of restoration and conservation of these grasslands.
Key words: Beta diversity, conservation, environmental gradient, species richness,
turnover.

INTRODUCTION uses between 1985 and 2018 (Souza et al. 2020)

and in some regions less than 20% of the
Open ecosystems such as grasslands often still
original grassland cover remain. Even more
are mistakenly considered as deforested areas
alarming, 40% of the original vegetation cover of
(Silveira et al. 2020) or as potential sites for
the Cerrado was lost by 2002 (Sano et al. 2010).
restoration through tree plantations (Veldman et
At the basis of this conservation problem, along
al 2015a). In contrast, recent research has clearly
with the communication gap between science
established that many tropical and subtropical
and stakeholders (Azevedo-Santos et al. 2017),
grasslands are, in fact, old-growth ecosystems
is our limited knowledge about the biodiversity
that harbor high biodiversity, economic and
of these ecosystems (Oliveira et al. 2017),
cultural values (Parr et al. 2014, Veldman et
jeopardizing conservation of natural resources
al. 2015b). Natural grasslands in Brazil are
(Bini et al. 2006).
threatened by rapid land use conversion. For
Particularly relevant for improving
example, 24% of original grassland area in
biodiversity knowledge is quantitative
Brazil’s Pampa biome was converted to other

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LUCIANA S. MENEZES et al. REFERENCE VALUES AND DRIVERS OF DIVERSITY

vegetation sampling, which is complementary to southernmost part of Brazil, include the Pampa
the recording of floristic lists. Only quantitative grasslands, in the southern half of Rio Grande
data allows to understand the processes behind do Sul state, and the highland grasslands in the
community assembly, for instance by considering southernmost part of the Atlantic Forest (IBGE
patterns of species co-occurrence, relationships 2019, Overbeck et al. 2007). The number of plant
between vegetation and environmental factors, community studies in the region has increased
and how plant species themselves influence the over the last 25 years, but with a clear bias to
local environment (HilleRisLambers et al. 2012, few areas, primarily those situated closer to
Weiher & Keddy 2004). Understanding diversity research institutions (see Boldrini & Overbeck
changes across space (i.e., beta diversity) is 2015). Only recently the first comprehensive
essential to unveil the factors driving community study on grasslands for the entire region was
structure, including deterministic processes published (Andrade et al. 2019). This study used
(such as environmental filtering, species plant community data obtained in standardized
interactions) and neutral processes (such as sampling at 156 sites to investigate patterns
random extinctions and ecological drift) (Chase of species spatial distribution associated
& Myers 2011). Environmental filters are often with climatic and edaphic factors. It provided
considered as drivers of plant community an important first step towards knowledge of
assembly (Laliberté et al. 2014). Disentangling grassland plant communities in the region as
relations between different drivers not only a whole. It also established, for the first time,
allows us to interpret current vegetation a classification of South Brazilian grasslands
dynamics, but also to develop scenarios for the based on quantitative data, confirmed floristic
future, for example, in the face of climate change, differences between highland grassland, mesic
and to reveal specific habitat characteristics and humid Pampa grasslands, and listed
that need to be protected or restored. indicator species for each grassland type.
Data from quantitative sampling may However, Andrade et al. (2019) did not focus on
be also relevant for environmental planning a more detailed analysis of the influence of soil
(Magnusson et al. 2005). It allows to decompose features on species distribution, the sampling
beta diversity patterns into their turnover and sites were placed on coarse spatial resolution
nestedness components, a crucial step to guide soil maps (scale of 1:5,000,000) and no data on
conservation (Socolar et al. 2016). When beta local edaphic characteristics was used in their
diversity is mainly due to species substitution study.
from one site to the next (turnover), the best Given that most parts of the globe are
conservation option is to target multiple sites. influenced by human activities, it is important
However, when it is due to species loss from – apart from the obvious and urgent need to
a richer set to a poorer one (nestedness), it reduce pressure on the environment and on
may be more efficient to target the richest site. biodiversity in general – to study biological
Importantly, both relations of environmental communities and their ecological determinants
factors with biodiversity patterns and effective in well-conserved regions in order to obtain
conservation strategies vary with spatial scale reference data for conservation and restoration
(Bini et al. 2006). purposes. A study conducted in the region has
The Campos Sulinos region (hereafter shown that even grassland areas in regions with
South Brazilian grasslands), located in the an intermediate degree of habitat loss (areas

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LUCIANA S. MENEZES et al. REFERENCE VALUES AND DRIVERS OF DIVERSITY

with more than 50% of natural grasslands) As a third goal, we present values of
are affected by land-use change: suppression grassland plant community descriptors, such as
of grasslands leads to species losses and species richness and diversity, at different spatial
homogenization of remnant plant communities scales. Our aim is that these values may be used
(Staude et al. 2018). Furthermore, conservation as reference, or practical targets, to achieve
through sustainable use (Boavista et al. 2019) in grassland conservation and restoration
and active restoration (Thomas et al. 2019) are initiatives. They include soft (easy to access) and
increasingly relevant topics in the region but are popular indexes, such as species richness and
still in need of conceptual underpinning and Shannon diversity, but also more ecologically
field evidence, also to support restoration or meaningful indexes, such as beta diversity and
conservation goals (e.g., Prach et al. 2019). its components (turnover and nestedness). So
Here, we use field data collected in the far, this kind of information has rarely been
PPBio Campos Sulinos project to investigate available at a scale beyond the local plot (i.e.,
and discuss diversity patterns of the South sampling unit). Since studies often vary in terms
Brazilian grasslands plant communities. The of sampling scale, and statistical methods that
Brazilian Research Program on Biodiversity allow to compare species richness at different
(acronym PPBio, from Programa de Pesquisa spatial scales are seldom applied outside the
em Biodiversidade), established in the context scientific community, we expect that presenting
of the Convention on Biological Diversity, these descriptive metrics at different spatial
includes a total of fifteen sites in the South scales will help stakeholders to better evaluate
Brazilian grassland region in which grassland South Brazilian grasslands conservation status
plant communities, forest tree communities, and restoration success.
amphibians, birds and fishes were sampled
(e.g. Dala-Corte et al. 2016, Fontana et al. 2018,
Madalozzo et al. 2017). Our first objective was MATERIALS AND METHODS
to explore patterns of spatial distribution of Study region
plant species. We expected to confirm the The South Brazilian grasslands span over the
patterns observed by Andrade et al. (2019), three southernmost states of Brazil, under
with three major grassland groups (highland, subtropical climate, with the proportion of
mesic Pampa and humid Pampa grasslands). grasslands in the landscape increasing towards
Secondly, we searched for relations between the south. The climate in the region ranges from
observed patterns of species distribution and Cfa, at lower altitudes, to Cfb at altitudes above
environmental and spatial filters, using locally 600 m (Alvares et al. 2013). Precipitation is well
obtained soil data and climatic variables. Due to distributed along the year, without a dry season,
the large extent of the entire gradient (660 km) ranging from 1,000 mm to 2,200 mm, with
and differences in altitude (from the sea level decreasing values towards the southern part of
to more than 900 m.a.s.l.), we expected to find the region (Alvares et al. 2013). However, recent
strong effects of spatially structured climatic climate series (years 2006 to 2016) indicate high
filters shaping species distribution patterns precipitation variability: the average monthly
in the South Brazilian grasslands, especially precipitation in the driest year was 86 mm in
related to temperature and precipitation. Jaguarão municipality (coordinates 32°14’ S,
53°46’ W), and 341 mm in the wettest year in

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Alegrete municipality (coordinates 29°46’ S, map presents ten ecological systems where
55°23’ W). grasslands are the dominant vegetation type.
Different types of geological substrate occur Grassland vegetation sampling was
in the study region: igneous volcanic rocks conducted at eight sites in the Pampa grasslands
(basalt) in the northern part, igneous plutonic and four sites in the highland grasslands (Figure
and metamorphic rocks (granite) in the south, 1), with one site in each ecological system. For site
and sedimentary material mainly in the coastal selection, areas with low degree of conversion
region (for details on geology and soils see to other land uses were chosen. In the Aristida
Andrade et al. 2019). Most grasslands in the grassland ecological system, where land-use
region are under grazing by domestic livestock, change is especially strong (Andrade et al. 2015),
and fire is commonly used as a management it was not possible to find areas matching this
tool mainly in the highland grasslands (Andrade requirement, therefore it was not included in
et al. 2015, Overbeck et al. 2007). Fire and grazing our study. At each site, a 5 x 5 km grid of five
are known to influence vegetation structure vertical lines and five horizontal lines was drawn
and composition in the region (e.g., Boavista et on the map with the orientation angle set to
al. 2019, Koch et al. 2016, Overbeck et al. 2018). better encompass grasslands remnants. Among
Under moderate intensity or frequency, they the 25 intersection points of the grid lines, nine
are considered key processes for maintenance were randomly chosen to place a 250 m long
of the characteristics of natural systems, as in transect (totalling 108 transects across the 12
other productive grassland systems around the grids). At each transect we placed 10 plots (1 m
world (Lezama et al. 2014). x 1 m), equally distanced following the isocline
to reduce local heterogeneity. In each plot,
Sampling design and procedures the cover of each vascular plant species was
PPBio sites were established in the different estimated.
ecological systems defined for Rio Grande do Sul Field sampling was conducted during spring
state by H. Hasenack et al. (unpublished data) and summer in 2014, 2015, and 2016, and plant
and, additionally, in Santa Catarina and Paraná communities at each site were sampled only
states. The classification of ecological systems once. All vascular plants had their taxonomic
aims at presenting a mesoscale biophysical identity verified with specific literature.
characterization of the landscape. Ecological Nomenclature follows the Brazilian Floristic List
systems were defined based on a combination (Flora do Brasil 2020). Plants that could not be
of topographic variables (altitude and slope; identified to the species level corresponded to
EMBRAPA 2013, IBGE 2019) and soil functional 4% of total vegetation cover and were excluded
classes (soil map from SAA/RS-IBGE/SC (2013) from statistical analysis.
reclassified according to soil hydromorphism,
fertility and depth). While the variables used Predictive variables
to differentiate the ecological systems do not We obtained edaphic and climatic data for all
include explicit quantitative vegetation data, 108 transects. Soil samples were collected at
a description of typical plant species in the three points per transect, to a depth of 30 cm
different systems was made based on expert whenever possible (but never less than 15 cm)
knowledge (Boldrini et al. 2009). The resultant and were mixed into one composite soil sample
per transect. The collected soil was analysed

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Figure 1. Spatial distribution of the 12 sampled sites in the South Brazilian grasslands in the different ecological
systems (based on H. Hasenack et al., unpublished data). Numbers correspond to the location of sites in the
following states and municipalities: Rio Grande do Sul (RS) state: 1 São Gabriel (sgb), 2 Quaraí (qua), 3 Soledade
(sol), 4 Lavras do Sul (lav), 5 Tavares (tav), 6 Santo Antônio das Missões (sam), 7 Santana da Boa Vista (sbv), 8
Jaguarão (jag), 9 Vacaria (vac), 10 Alegrete (ale); Santa Catarina (SC) state: 11 Painel (pai); and Paraná (PR) state: 12
Palmas (pal). At right, example of a site with nine randomly selected points to place the transects and a detail of a
transect with the ten plots (1 m x 1 m) represented by the red dots.

following protocols presented by Tedesco et ten-year time series (2006 to 2016). Data were
al. (1995). We considered the following edaphic interpolated through inverse distance weighting
variables (see Table I for measurement units and extracted to the transects coordinates
and analytical method of soil variables): with Qgis software (version 3.4.10). We used the
percentage of clay, coarse sand, fine sand and following variables: maximum daily temperature,
silt, organic matter content, pH, phosphorus, minimum daily temperature, minimum daily air
potassium, nitrogen, aluminium, calcium and humidity, maximum monthly precipitation, and
magnesium contents, cation exchange capacity, minimum monthly precipitation.
base saturation and aluminium saturation. The To account for the influence of the nested
complete data can be found in Supplementary sampling design (i.e., transects within sites),
Material (Tables SII and SIII). as well as to evaluate which environmental
Climatic data were compiled from 33 variables were spatially structured, we added
meteorological stations of the Instituto Nacional spatial variables to our analysis. We extracted
de Meteorologia (INMET) within the region, for a ordination axes of a principal coordinate

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Table I. Environmental, spatial variables (and analytical method) and their correlation with grassland plant
communities from South Brazilian grasslands. Only variables selected as significantly correlated (p<0.05) with the
species composition variance are shown. For complete set of explanatory variables see supplementary material.

Code Variable Unit Method of analysis R² AIC p

Environmental:

Al Exchangeable aluminium cmolc/dm³ Extracted with KCl 1mol L¹ 0.12 208.38 0.002

minT Minimum temperature °C Extracted from INMET database 0.05 203.00 0.002

Clay Clay % Densimeter method 0.03 199.36 0.002

minAH Minimum air humidity % Extracted from INMET database 0.03 196.22 0.002

minP Minimum precipitation mm Extracted from INMET database 0.02 193.54 0.002
Bases extracted with ammonium
BSat Base saturation % 0.02 187.99 0.002
acetate
Ca Exchangeable calcium cmolc/dm³ Same as Al 0.02 190.87 0.002

pH pH - In water 0.02 189.37 0.002

maxT Maximum temperature °C Extracted from INMET database 0.02 185.08 0.002

OM Organic matter % Humid digestion 0.02 186.59 0.002

Csand Coarse sand % Granulometry from 0.2 to 2 mm 0.01 184.30 0.004

Spatial:

MEM1 1st ordination axis - PCoA based on spatial coordinates 0.14 205.43 0.002
nd
MEM2 2 ordination axis - PCoA based on spatial coordinates 0.03 186.78 0.002

MEM3 3rd ordination axis - PCoA based on spatial coordinates 0.03 183.10 0.002

MEM4 4th ordination axis - PCoA based on spatial coordinates 0.07 196.70 0.002

MEM5 5th ordination axis - PCoA based on spatial coordinates 0.03 193.46 0.002

MEM6 6th ordination axis - PCoA based on spatial coordinates 0.02 181.27 0.002

MEM12 12th ordination axis - PCoA based on spatial coordinates 0.02 179.58 0.002
th
MEM13 13 ordination axis - PCoA based on spatial coordinates 0.03 190.23 0.002

analysis based on central spatial coordinates of were under traditional grazing management,
the transects (Moran’s Eigenvector Maps - MEM, which for South Brazilian grasslands means
Borcard et al. 2011). To produce the MEMs, the high grazing intensity (Carvalho & Batello 2009),
matrix of distance among pairs of coordinates indicated by the overall low vegetation height
was truncated at the smallest distance that kept (average 15.8 cm, standard deviation ± 13.2 cm).
all points connected, i.e. 221.2 km.
We did not include grazing intensity proxies Data analysis
in our analysis since we considered grazing levels Using transects described by plant species
to be similar across the region. All study sites composition, we performed hierarchical

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LUCIANA S. MENEZES et al. REFERENCE VALUES AND DRIVERS OF DIVERSITY

clustering, based on UPGMA after Jaccard- diversity (H’) and its expression by the effective
based pairwise species turnover comparing all number of species (Jost 2006) were calculated
pairs of transects (Baselga 2012). Consistency for each plot; we present average levels per site.
of groups was tested with approximately The effective number of species, was calculated
unbiased p-values obtained via 999 multiscale through the exponential of H’, this estimates
bootstrap resampling (Shimodaira 2004). how many species with equitable abundances
Groups with p<0.05 were considered consistent. would be required to obtain the same value of
The dendrogram was cut at the height of 0.75 H’ (Jost 2006, Magurran 1988). To further describe
resulting in five consistent and ecological plant species abundance relationships in the
meaningful groups. Approximately unbiased communities, we also calculated the evenness
p-values for all dendrogram nodes are shown in index (E) at the plot level, which expresses the
the Figure S2. ratio between observed diversity and maximum
To elucidate the relations of plant community diversity (i.e., if all species were equally abundant
patterns and soil and climate characteristics, in communities) (Magurran 1988).
we performed redundancy analysis (RDA) based W e e x p l o re d p a t t e r n s o f s p a t i a l
on the Hellinger-transformed matrix of relative heterogeneity in species composition by
species cover per transect (Legendre & Gallagher calculating beta diversity and its components,
2001). We also performed variance partitioning turnover and nestedness. We used the Jaccard-
(Borcard et al. 2011) to verify how much of based multiple-site dissimilarity index (β-jac)
compositional variance was related only to the to calculate beta diversity, turnover and
environment (climate and soil), only to space nestedness (Baselga 2012), comparing species
(MEM) and to the shared effect of environment composition among the nine transects at each
and space. To avoid inflation in both procedures, site and thus obtaining one value representative
we first removed all environmental variables of the heterogeneity per site.
that had a collinearity factor greater than 10 All analyses were performed in the R
(Oksanen et al. 2017). Collinearity was detected environment. Package ‘iNEXT’ and function
using a variance inflation factor calculated for ‘ChaoShannon’ were applied to calculate metrics
each environmental explanatory variable using of Shannon diversity and effective number of
the r² value of the regression of that variable species (Chao et al. 2014). Package ‘betapart’
against all other explanatory variables. The was used to calculate beta diversity, turnover
remaining variables were submitted to forward and nestedness (Baselga & Orme 2012). From
selection of predictive variables. This procedure the package ‘vegan’ (Oksanen et al. 2017), we
adds and drops variables in a model, aiming to used functions ‘vif.cca’ to verify for collinearity
maximize R² at every step, the procedure stops in explanatory variables, ‘ordistep’ to perform
when the R² starts to decrease, or when the R² forward selection of explanatory variables, ‘rda’
of the scope is exceeded (R² with all explanatory to run redundancy analysis and ‘varpart’ to
variables = 0.34), or when the p-value threshold run variance partitioning analysis. Hierarchical
(p>0.05) is exceeded (Blanchet et al. 2008). For a Clustering analysis was performed with the
graphical representation of the selected spatial ‘pvclust’ package, function ‘pvclust’ (Suzuki &
variables see Figure S1. Shimodaira 2015).
We calculated indexes of species richness
(S) at the site, transect and plot levels. Shannon

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RESULTS and coastal Pampa grassland group 2 (CG2) four

transects from Tavares site.
At the twelve sites (total of 108 transects and
Among the 759 plant species found, almost
1080 plots), 759 plant species from 72 families
half (308) were shared by Pampa and highland
were found (see Table SI for complete species
grasslands. The Pampa grasslands (comprising
list). The most species-rich families were
MPG, CG1 and CG2) presented the higher number
Poaceae (154 species, Figure 2b), Asteraceae (136),
of exclusive species (258) compared to the
Cyperaceae (65), and Fabaceae (58). Considering
highland grasslands (SHG and NHG, 193 species).
species cover, Poaceae stood out as the most
Species richness varied from 119 species at the
important family (64.6%, Figure 2a).
site in Tavares to 262 species at the Soledade
Cluster analysis showed five consistent
site (Table II). At all but two sites, equivalent
groups with distinct species composition
number of species had a value of less than half
(Figure 3). Two distinct groups were at the
of the mean species richness per plot, which
highland grassland region: southern highland
indicates high dominance by few species at this
grassland (SHG), comprising sites from Painel,
scale in the South Brazilian grasslands (Table II).
Soledade and Vacaria, and northern highland
At all sites, the sum of the cover of the
grassland (NHG), represented by the Palmas
five most abundant species added up to more
site, the northernmost site of our sampled
than 40% of total vegetation cover (Table III).
gradient. The Pampa region was subdivided in
A large fraction of these abundant species
three different groups: mesic Pampa grassland
occurred throughout most parts of the South
(MPG), the largest group, represented by seven
Brazilian grasslands. A notable exception were
sites (Alegrete, Jaguarão, Lavras do Sul, Quaraí,
the two grassland groups in the coastal region,
Santana da Boa Vista, Santo Antônio das Missões
characterized by the dominance of species that
and São Gabriel) and two groups in the coastal
are absent in the other sites, such as Axonopus
region coastal Pampa grassland group 1 (CG1)
sp. and Paspalum vaginatum (dominant species
five out of the nine transects from Tavares site;

Figure 2. Plant families contributing the most to (a) the total relative cover and (b) number of species found in the
South Brazilian grasslands.

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Figure 3. Hierarchical clustering analysis, based on

UPGMA method and using Jaccard-based pairwise
species turnover as dissimilarity metric, showing
the separation of South Brazilian grasslands in five
groups, top to bottom: Southern highland grassland
(in Portuguese campos de altitude do sul), Northern
highland grassland (campos de altitude do norte),
Mesic Pampa grassland (campos mésicos do Pampa),
Coastal Pampa grassland group 1 (campos costeiros
do Pampa grupo 1) and Coastal Pampa grassland
group 2 (campos costeiros do Pampa grupo 2). Group
consistency was tested with approximately unbiased
p-values obtained via 999 multiscale bootstrap
resampling, groups with p<0.05 were considered
consistent (see for dendrogram with all p-values).

at CG1 and CG2, respectively). Considering this

list of 27 plant species with highest cover values
per site, 19 were grasses, five belonging to the
genus Paspalum Schizachyrium tenerum was
very important at the NHG and SHG groups,
representing the dominant species in three out
of the four highland grassland sites (Vacaria,
Painel and Palmas). Paspalum notatum and
Andropogon lateralis were the most important
plant species in terms of cover in the MPG sites.
Accordingly, the RDA analysis showed
the separation of NHG and SHG dominated
by S. tenerum (the positive portion of RDA1
axis in Figure 4) from MPG sites dominated
by A. lateralis (the negative portion of RDA1
axis). P. notatum was also characteristic of the
MPG sites, but positively correlated with the
second RDA axis (RDA2, Figure 4). The RDA also
showed a strong relation between vegetation
and soil pH, with the highest concentration
of aluminum, i.e., acid soils, in SHG sites (see
Table I, aluminum has the highest R² and AIC
values). Climatic variables were also important
to explain species composition patterns.
Increased maximum monthly precipitation was
particularly related with highland sites (NHG
and SHG), whereas higher values of minimum
temperature were associated to the coastal
area, CG1 and CG2 (Figure 4). Indeed, the model

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with environmental variables explained 34% diversity was due to species substitution across
of species composition variance (Table IV). transects (the turnover component in Figure 5).
However, the spatial variables had almost the
same importance (R2 = 0.35). By controlling for
the spatial influence in environmental variables, DISCUSSION
the model explanation decreased (R 2 = 0.12), Around the world, grassland vegetation has been
indicating that environmental variables along neglected in terms of science and conservation
the South Brazilian grassland region are highly (Overbeck et al. 2015, Veldman et al. 2015a,b). The
spatially structured (Table IV). results we present here contribute to a detailed
Although most abundant species were well characterization of still rather intact grassland
distributed along the entire gradient, spatial landscapes in terms of species richness and
heterogeneity per site was generally high, dominance patterns in the plant community;
especially at the coastal grassland site (‘tav’ in our results thus can serve to establish regional
Figure 5). At all sites, the greater part of beta reference values for grassland conservation or

Table II. Richness and diversity metrics of vegetation in South Brazilian grasslands. Richness (S) given for the three
sampling scales: site 25 km², transect 250 m² and plot 1 m². Shannon diversity (H’), effective number of species
and equability (E) were calculated for each plot, values presented are average and standard deviation for the 90
plots at each site, except for Tavares site where two groups of grasslands could be differentiated: Coastal Pampa
grassland group 1 with 50 plots and Coastal Pampa grassland group 2 with 40 plots. *All plots from Tavares were
grouped to calculate the metrics at the site level in order to preserve the 25 km² scale.

Samp.
Site Plot H’ Hill
site Equivalent
Municipality Ecological system (spp/25 (spp/1 (nats/ E numbers
(spp/250 S
km²) m²) ind) (q=1)
m²)
70.33 21.8 (± 2.06 (± 0.67 (± 87.17 (±
Alegrete (ale) Sandy grassland 175 8.27 (± 2.76)
(±4.72) 4.61) 0.31) 0.07) 2.49)
Atlantic submontane 83.33 22.94 (± 2.53 (± 13.17 (± 0.77 (± 111.56 (±
Jaguarão (jag) 196
grassland (±18.28) 5.15) 0.3) 4.18) 0.05) 2.21)
87.77 (± 24.45 (± 2.36 (± 0.72 (± 97.45 (±
Lavras do Sul (lav) Shortgrass grassland 197 11.62 (± 4.9)
14.24) 8.19) 0.44) 0.07) 2.11)
Shallow soil 111.55 (± 30.5 (± 2.51 (± 13.32 (± 0.74 (± 140.304 (±
Quaraí (qua) 252
grassland 18) 9.84) 0.41) 5.24) 0.06) 2.7)
Santo Antônio das 84.22 (± 25.48 (± 2.23 (± 10.24 (± 0.7 (± 105.83 (±
Park grassland 196
Missões (sam) 13.8) 8.7) 0.44) 4.42) 0.08) 2.19)
Santana da Boa 96.88 (± 26.85 (± 2.38 (± 11.50 (± 0.73 (± 121.61 (±
Bush grassland 247
Vista (sbv) 14.53) 6.33) 0.32) 3.97) 0.08) 2.77)
Inland submontane 85.55 (± 25.41 (± 2.34 (± 10.95 (± 0.72 (± 110.17 (±
São Gabriel (sgb) 225
grassland 11.41) 6.15) 0.32) 3.62) 0.06) 2.99)
30.77 (± 10.41 (± 1.56 (± 5.40 (± 0.69 (± 63.14 (±
Tavares (tav) Coastal grassland 119
14.26) 4.65) 0.55) 2.39) 0.09) 2.42)
97.44 (± 26.44 (± 2.44 (± 12.08 (± 0.75 (± 121.72 (±
Painel (pai) Highland grassland 256
10.52) 6.15) 0.33) 3.61) 0.07) 2.71)
22.91 (± 2.32 (± 0.74 (± 126.64 (±
Palmas (pal) Highland grassland 244 87 (± 8.8) 10.89 (± 4)
5.85) 0.35) 0.06) 3.36)
105.55 (± 31.4 (± 2.52 (± 13.42 (± 0.73 (± 120.397 (±
Soledade (sol) Highland grassland 262
20.01) 6.9) 0.38) 5.37) 0.07) 3.04)
98.77 (± 30.85 (± 2.52 (± 13.28 (± 0.74 (± 103.526 (±
Vacaria (vac) Highland grassland 218
9.01) 8.29) 0.36) 4.44) 0.05) 2.21)

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LUCIANA S. MENEZES et al. REFERENCE VALUES AND DRIVERS OF DIVERSITY

restoration. The total number of 759 species all physiognomies existent in the region, 2.150
in our data set represents roughly one fourth plant species have been confirmed (Andrade et
of the 3.000 plant species estimated for the al. 2018), and our sampling with 566 species at
South Brazilian grasslands (Overbeck et al. Pampa sites thus also presents one fourth of the
2007). For the Pampa as a whole, considering species from this region. However, it is important

Table III. Relative cover of the five most abundant species occurring at each site. When one species is top five
abundant for a given site its relative cover value is given for all sites where it was present. Acronyms for sites and
grassland groups are given in Table II. Cover values in bold indicate the species with highest abundance per site.

Sites
Species ale jag lav qua sam sbv sgb tav sol vac pai pal
Agenium villosum (Nees) Pilg. - <0.1 - - - - - - 1.1 1.2 4.3 -

Andropogon lateralis Nees 33.7 6.3 4.7 10.9 22.6 6.6 12.4 3.7 <0.1 - 0.5 4.3

Andropogon macrothrix Trin. - - - 0.1 - <0.1 - - 0.1 <0.1 1.3 6.7

Axonopus affinis Chase 1.8 9 11.1 2.5 2.1 7.8 6.8 2.2 1.6 2.6 3.4 4.8

Axonopus sp. - - - - - - - 12 - - - -

Baccharis crispa Spreng. 0.3 1.8 1.6 0.4 - 2.1 1.6 - 4.3 3.1 3.1 1

Centella asiatica (L.) Urb. 0.1 3.5 - - <0.1 0.1 5.4 1.4 - - - 0.4

Dichondra sericea Sw. 2.8 1.2 2 1 1.4 2.2 1.1 0.3 1.7 1.2 0.5 0.2

Eleocharis viridans Kük. ex Osten - 1.3 3.5 2.5 2.7 0.9 3 6.4 - - - 0.8

Elionurus muticus (Spreng.) Kuntze - - - - - - - - 0.1 - - 4.9

Eryngium horridum Malme - 0.3 1 0.4 0.1 4.2 0.5 - 6.7 - - 0.1

Ischaemum minus J. Presl - 0.2 - - - - <0.1 5.6 - - - -

Panicum aquaticum Poir. - - <0.1 <0.1 - - <0.1 5.5 - - - <0.1

Paspalum indecorum Mez - - - 5.2 4.9 - - - - - - -

Paspalum notatum Flüggé 20.5 15.2 17.2 11.5 18.8 18.9 14.1 0.4 22.8 16.6 3.2 0.7

Paspalum plicatulum Michx. 0.5 2.9 0.3 1.1 0.7 0.5 <0.1 - 2.1 3.5 7.8 1.7

Paspalum pumilum Nees 0.3 6.6 0.9 - - 0.1 1.2 4.4 0.3 - 4.8 2.1

Paspalum vaginatum Sw. - - - - - - - 17.2 - - - -

Piptochaetium montevidense
2.7 3.2 1.9 1.7 0.7 5.5 1.7 - 7.6 7.8 5.7 7.1
(Spreng.) Parodi
Saccharum angustifolium (Nees)
- 0.1 6.2 - 0.1 - - - 1.7 - 2.3 2.3
Trin.

Schizachyrium tenerum Nees 0.1 1.2 0.2 0.3 - 0.8 - - 4.2 17.1 13.8 10.2

Steinchisma hians (Elliott) Nash 1.5 2.7 0.9 4.8 3.4 0.1 2.1 0.2 0.9 0.9 0.2 0.2

Trifolium polymorphum Poir. - 0.2 5.9 0.6 1.1 0.6 0.5 - - - - -

Vernonanthura nudiflora (Less.) H.

0.4 - - 0.3 - 0.2 3.5 0.2 - 0.1 1.2 <0.1
Rob.

Total: 64.7 55.7 57.4 43.3 58.6 50.6 53.9 59.5 55.2 54.1 52.1 47.5

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LUCIANA S. MENEZES et al. REFERENCE VALUES AND DRIVERS OF DIVERSITY

to recognize that our study was conducted These environments often present a specific
mostly in rather homogenous grazed areas of flora (Porembski & Barthlott 2000, Trindade et al.
mesic grasslands that dominate the landscapes 2008) and are characterized by the presence of
(with the exception for the coastal region, where species-rich genera, such as Parodia (Cactaceae:
humid grasslands cover considerable areas). 26 species in the region, Larocca & Zappi 2015)
Thus, we did not include azonal environments and Dyckia (Bromeliacaceae: 29 species in the
that are found inserted in the grassland matrix, region, Forzza et al. 2015) on rock outcrops.
such as rock outcrops or sand depositions.

Figure 4. Redundancy analysis (RDA) based on the relative frequency of plant species in 108 transects across the
South Brazilian grasslands and predictive (edaphic and climatic) variables. Environmental variables explained
34% of species variance. Cluster analysis supported five groups of distinct plant species composition represented
by the polygons (see also Figure 3). Acronyms for the environmental variables are given in Table I. For better
visualization only species highly correlated (r²>0.25) with RDA axis were plotted. Species acronyms are: andlat
Andropogon lateralis, axopel Axonopus pellitus, baccri Baccharis crispa, cenasi Centella asiatica, cheacu Chevreulia
acuminata, chesar Chevreulia sarmentosa, chrasc Chrysolaena ascendens, desinc Desmodium incanum, dicsab
Dichanthelium sabulorum, dicser Dichondra sericea, carpha Carex phalaroides, chagra Chaetogastra gracilis,
cyclep Cyclospermum leptophyllum, elevir Eleocharis viridans, ichpro Ichnanthus procurrens, macpro Macroptilium
prostratum, oxabra Oxalis brasiliensis, pasnot Paspalum notatum, paspum Paspalum pumilum, paspli Paspalum
plicatulum, pipmon Piptochaetium montevidense, setpar Setaria parvifolia, schten Schizachyrium tenerum, solses
Soliva sessilis, tepadu Tephrosia adunca, tripol Trifolium polymorphum.

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LUCIANA S. MENEZES et al. REFERENCE VALUES AND DRIVERS OF DIVERSITY

The high importance of Poaceae and Environment-vegetation relations reflecting

Asteraceae in the South Brazilian grasslands grasslands groups
in terms of species richness has been shown As to the climatic variables, maximum monthly
previously. Interestingly, however, Fabaceae, precipitation and minimum daily temperature
shown in many studies to be the third family in were related to community composition patterns
terms of species number (Andrade et al. 2016, indicated by plant species composition in the
Ferreira et al. 2010), was replaced by Cyperaceae South Brazilian grasslands (see Figure 4). The
in our study, a family previously shown to have highland region had higher values of maximum
high importance in grasslands in the coastal monthly precipitation, the higher precipitation
region (Bonilha et al. 2017, Ferreira & Setubal in this region is one of the factors causing
2009, Menezes et al. 2015). Until now, the high forest expansion over grasslands (Müller et al.
richness of Cyperaceae in the South Brazilian 2012). In contrast, some regions in the southern
grasslands might have been underestimated half of Rio Grande do Sul State (in the Pampa,
due to the lack of taxonomic treatment for comprising MPG sites), present historical
species-rich genera. Improved knowledge of records of hydric deficits, especially in years of
Cyperaceae species, including the description La Niña-Southern Oscillation events (Cordeiro et
of new species, may now reveal more accurately al. 2018). Higher values of minimum temperature
the real importance of this plant group to the were associated to the coastal grasslands,
South Brazilian grasslands flora (e.g. Hefler & indicating high climatic stability, expected in the
Longhi-Wagner 2012, Silva-Filho et al. 2017, coastal region.
Trevisan & Boldrini 2008). Soil features also separated Pampa
grasslands from highland grasslands. The
concentrations of exchangeable aluminum (Al+3)

Table IV. Summary of the variation partitioning of species composition in the South Brazilian grasslands.
Environmental and spatial features used as predictive variables are given in Table I. Explanation factors are
accepted as significant with p<0.05, ‘n.t’ accounts for non-testable fractions.

Effect of the main variable Explained variation (R²) Df p

Total effect

Environment + space 0.47 19 0.001

Partial effects

Environment 0.33 11 0.001

Environment [space] 0.13 11 0.001

Space 0.34 8 0.001

Space [environment] 0.14 8 0.001

Shared effect

Environment + space 0.20 - n.t.

Residuals 0.53 - n.t.

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LUCIANA S. MENEZES et al. REFERENCE VALUES AND DRIVERS OF DIVERSITY

on distinct species composition, edaphic and

climatic characteristics. Our two groups of
highland sites, NHG and SHG, had the same
dominant plant species (S. tenerum and
P. notatum), and the distinction in species
composition seems to be related with a slightly
higher content of aluminium and organic
matter in NHG group (NHG: Al = 3.8, OM = 7.2;
and SHG: Al = 3.1, OM = 5.2, average values, see
Figure 5. Beta diversity (numbers above bars), based table SII). In coastal Pampa grasslands the
on Jaccard-Index, decomposed into turnover and
nestedness contribution at the twelve grassland sites
dominant species in CG2 (P. vaginatum and S.
in the South Brazilian grasslands. secundatum) had low coverage, or were absent,
in CG1. Considering edaphic differences, in CG2
and differences in soil granulometry were the we found higher base saturation (over 50% in
principal variables associated to this distinction all transects, characterizing eutrophic soils)
(Table I). The soils in the highland region are than in CG1, also acid elements were absent
formed by volcanic rocks (basalt, rhyolite, or indetectable (aluminium mostly) in CG2. In
rhyodacite), leading to high aluminum content. fact, transects belonging to the CG2 group were
As aluminum has low mobility and is easily located closer to the Lagoa do Peixe lagoon,
bounded by organic matter (Li & Johnson 2016), where the proximity to the water body may
we could observe both components in high influence soil chemical composition due to
proportion in the highland region. more frequent flooding events, shallower water
It is important to consider the shared effect table (Kozlowski 1984) and possible influence
of space and environment when we discuss the of seasonally higher salinity. More scale-refined
role of environmental drivers shaping grassland analysis would help to better disentangle the
community patterns. Both environmental factors that drive changes in plant community
features and space (i.e., dispersal limitation) are composition within this region.
potentially filters of community assembly acting Classification of the South Brazilian
at different spatial scales (Menezes et al. 2016). grasslands historically had been based on
Climatic variables are intrinsically spatially coarse physiognomic descriptors, such as
structured at broader scales (Bell et al. 1993), ‘shrubby or dirty grassland’ (campos arbustivos
which makes it difficult to discern between the ou sujos, sensu Lindman 1974) or considering
effects of climate and other spatially structured very broadly defined environmental features,
environmental or biotic factors, such as dispersal such as by using terms like ‘dry grasslands’
limitation, on community composition. Soil (campos secos, sensu Rambo 1942). Andrade
properties, in contrast, are usually more influent et al. (2019) provided the first attempt to
at local spatial scales (Menezes et al. 2016). classify grasslands based on plant community
Overall, the results presented here composition, and our results agree with their
corroborate Andrade et al. (2019), separating the classification. Nontheless, we must recognize
South Brazilian grasslands in three groups of that data availability is still too limited for a
grasslands (highland grassland, mesic Pampa comprehensive fine-scale classification based
grassland and coastal Pampa grassland) based on species composition that would be needed

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LUCIANA S. MENEZES et al. REFERENCE VALUES AND DRIVERS OF DIVERSITY

to define grassland habitats of specifically high become dominant. On the long term, it may
conservation value or threat status. lead to the substitution of natural grasslands
A classification of landscapes based by shrub- or tree-dominated ecosystems (Koch
primarily on geomorphological variables, on et al. 2016). Here, working on areas with cattle
the other hand, such as the classification grazing throughout, we do not expect strong
by Hasenack H et al. (unpublished data) that interference in the overall structure of grassland
was used for definition of our study sites communities due to management as found in
(see Figure 1) is useful for the description of Andrade et al. (2019), where one ungrazed site
different environments and regions. However, clearly differed from the other sites. However,
geomorphological features may not be directly it would be interesting to further investigate
related to species composition patterns. In fact, this in future studies to better define optimum
the classification of floristic regions, based on grazing levels (or fire frequencies, for that
plant species composition, has not matched matter, see e.g., Overbeck et al. 2018) from both
previous classifications in other regions of Brazil conservation and production perspectives.
as well (Cantidio & Souza 2019, Silva & Souza While dominant species are widespread
2018, Silva-Souza & Souza 2020). It is important among regions (Table III), rarer species differ
to underline that conservation and restoration more, even within sites. This was highlighted
planning at local or regional scales require by the high beta diversity observed, with a
larger data sets about plant community and greater contribution of species substitution
that quantitative field sampling is essential. (turnover) among transects (Figure 5). In fact, a
recent meta-analysis has shown that turnover
Evenness, richness, and diversity patterns seems to be the dominant pattern over a broad
Species abundance distribution at our sites was range of ecosystems and organisms (Soininen
remarkably uneven. The cover sums of the five et al. 2018), while nestedness patterns are
most abundant species per site represented restricted to extreme climates in high latitudes
over 40% of vegetation cover in all sites, (Dobrovolski et al. 2012). Concerning plant
despite the high species richness (average S in species conservation, high beta diversity due to
sites was 215) (Table III). All studied sites were turnover means that the best way to protect the
under traditional grazing management that also most of biodiversity is defining a network of well-
shapes grassland community composition and conserved grasslands distributed over regions
structure. Farmers usually maintain rather high along the entire environmental gradient. The
stocking rates, which can even lead to overgrazing Brazilian Native Vegetation Protection Law (Law
(Carvalho & Batello 2009). This process possibly 12.651/2012) obliges rural properties to maintain
enhances dominance of few species that are or restore native vegetation up to 20% of their
adapted to high grazing pressure (Sosinski total area as Legal Reserve for the conservation
& Pillar 2004) and may also lead to a certain of biodiversity and ecosystem services (see
homogenization of plant communities, as found Metzger et al. 2019). While our data indicate
in general for biotic communities under land that the distribution of protected grassland
use intensification (Gossner et al. 2016). Lack remnants in space – as favored by the Legal
of disturbance, i.e., exclusion from grazing or Reserve – will be beneficial for conservation
fire, on the other hand, has been shown to of plant diversity, other studies point negative
lead to biodiversity loss once few taller species effects of fragmentation (Staude et al. 2018)

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LUCIANA S. MENEZES et al. REFERENCE VALUES AND DRIVERS OF DIVERSITY

which would occur if grasslands were restricted that needs to be considered. In fact, during the
to Legal Reserves. More studies on the relevance field sampling of our study, the ‘record’ value of
of scale and grain for conservation purposes are 56 species in one grassland plot was registered
needed. Moreover, conservation requirements at the Quaraí site, on shallow soil (Menezes et
may differ among groups of organisms, since al. 2018). Thus, for conservation and restoration
beta diversity, turnover and nestedness show purposes, overall compositional patterns,
specific patterns for organisms at different dominant species, and species richness should
trophic levels and dispersal capabilities (e.g., be simultaneously used as references.
Soininen et al. 2018). Future scenarios point out to continued
pressure from agricultural expansion on natural
Establishing reference values for conservation ecosystems in southern Brazil (Dobrovolski et al.
and restoration 2011), resulting in additional biodiversity losses
The species richness values we found at (e.g., Staude et al. 2018). Only the implementation
three spatial scales (sites, transects, plots) of effective conservation measures can
are informative for a pragmatic definition avoid more severe transformation of natural
of reference values for conservation and habitats, preserving important ecosystem
restoration of the major ecological systems services (Metzger et al. 2019). We suggest that
in the South Brazilian grasslands. Although environmental agencies should establish
ecological restoration of converted or degraded clear criteria for environmental licensing and
areas may not achieve the levels of richness and restoration/conservation monitoring based on
diversity of natural areas, it is important to set field information as presented here, and that
clear goals for restoration projects. Grasslands these criteria should be periodically updated
still represent a small portion of areas under to include more recent data. We further urge to
restoration in Brazil (Guerra et al. 2020) and continue with standardized vegetation sampling
determining when a grassland is successfully in the region, in order to improve the information
restored is yet to be discussed (but see Wortley basis both for science and conservation.
et al. 2013). Species richness, for instance, can
be obtained relatively easily and already is a Acknowledgments
piece of valuable information for conservation We thank all landowners for allowing the research
on their properties and anonymous reviewers and
(Menezes et al. 2018, Wilson et al. 2012) that
the editor for helpful comments that improved the
should also be useful for restoration purposes. manuscript. This research received financing from PPBio
As shown by equivalent richness and Rede Campos Sulinos - Vegetação Campestre MCTI/CNPq
evenness values, South Brazilian grasslands (457447/2012-5 to GEO and 457531/2012-6 to VDP) and was
further supported by Coordenação de Aperfeiçoamento
can present highly uneven species abundance
de Pessoal de Nível Superior (CAPES - Finance Code 001),
distribution, with high dominance of Poaceae National Institutes for Science and Technology (INCT) in
species, especially Andropogon lateralis, Ecology, Evolution and Biodiversity Conservation, MCTIC/
Paspalum notatum and Schizachyrium tenerum. CNPq (465610/2014-5) and FAPEG (201810267000023).
EVM, CVE, DBL, GHMS and LSM were supported by
However, to evaluate grassland conservation
MCTI/CNPq. RT (313306/2018-4), VDP (307689/2014-0)
status or define restoration targets, it does and GEO (310345/2018-9) received Conselho Nacional
not appear to be sufficient to consider only de Desenvolvimento Científico e Tecnológico - CNPq
composition of dominant species, since South productivity grants.

Brazilian grassland have high species richness

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LUCIANA S. MENEZES et al. REFERENCE VALUES AND DRIVERS OF DIVERSITY

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WILSON JB, PEET RK, DENGLER J & PÄRTEL M. 2012. Plant

1
Universidade Federal do Rio Grande do Sul, Programa
species richness: the world records. J Veg Sci 23: 796-802. de Pós-Graduação em Botânica, Laboratório
de Estudos em Vegetação Campestre, Av. Bento
WORTLEY L, HERO JM & HOWES M. 2013. Evaluating ecological
Gonçalves, 9500, 91501-970 Porto Alegre, RS, Brazil
restoration success: A review of the literature. Restor
2
Ecol 21: 537-543. Universidade Federal do Rio Grande do Sul, Programa de Pós-
Graduação em Ecologia, Laboratório de Ecologia Quantitativa,
Av. Bento Gonçalves, 9500, 91501-970 Porto Alegre, RS, Brazil
3
Universidade Federal do Rio Grande do Sul, Programa de Pós-
SUPPLEMENTARY MATERIAL Graduação em Ecologia, Laboratório de Geoprocessamento,
Tables SI-SIII Av. Bento Gonçalves, 9500, 91501-970 Porto Alegre, RS, Brazil
4
Figures S1-S2 Universidade Federal do Rio Grande do Sul,
Departamento de Ecologia, Av. Bento Gonçalves,
9500, 91501-970 Porto Alegre, RS, Brazil
How to cite
5
MENEZES LS, ELY CV, LUCAS DB, MINERVINI-SILVA GH, VÉLEZ-MARTIN Universidade Federal de Santa Catarina, Departamento
E, HASENACK H, TREVISAN R, BOLDRINI II, PILLAR VD & OVERBECK GE. de Botânica, Rua Eng. Agronômico Andrei Cristian
2022. Reference values and drivers of diversity for the South Brazilian Ferreira, Trindade, 88040-900 Florianópolis, SC, Brazil
grassland plant communities. An Acad Bras Cienc 94: e20201079. DOI 6
Universidade Federal do Rio Grande do Sul,
10.1590/0001-3765202220201079.
Departamento de Botânica, Av. Bento Gonçalves,
9500, 91501-970 Porto Alegre, RS, Brazil
Manuscript received on July 14, 2020;
accepted for publication on November 11, 2020
Correspondence to: Luciana da Silva Menezes
LUCIANA S. MENEZES 1 E-mail: [email protected]
https://orcid.org/0000-0002-2961-0190
Author contributions
CLEUSA V. ELY1
https://orcid.org/0000-0001-9094-9524
LSM performed field work, plant species identification, leading
data analysis and manuscript writing. CVE, DBL, GHMS, RT and IIB
DIÓBER B. LUCAS1 contributed with field work and plant species identification. EVM
https://orcid.org/0000-0002-3293-492X contributed with sampling design conception, environmental
data acquisition and contacted land-owners. HH contributed
GRAZIELA H. MINERVINI-SILVA1 with sampling design conception and environmental data
https://orcid.org/0000-0003-3835-7753
acquisition. VDP contributed with the conception of the study.
GEO contributed with the conception of the study, field work
EDUARDO VÉLEZ-MARTIN2
https://orcid.org/0000-0001-8028-8953
and manuscript writing. All authors reviewed the manuscript.

HEINRICH HASENACK3,4
https://orcid.org/0000-0002-8521-1266

RAFAEL TREVISAN5
https://orcid.org/0000-0002-4817-3141

ILSI IOB BOLDRINI1,6

https://orcid.org/0000-0003-1028-8864

VALÉRIO D. PILLAR2,4
https://orcid.org/0000-0001-6408-2891

GERHARD E. OVERBECK1,6
https://orcid.org/0000-0002-8716-5136

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