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Received: 21 August 2020
Revised: 30 December 2020
Accepted: 30 December 2020
On the floristic identity of Amazonian vegetation types
Ary T. Oliveira- Filho1 | Kyle G. Dexter2,3 | R. Toby Pennington3,4 |
Marcelo F. Simon5 | Marcelo L. Bueno6 | Danilo M. Neves1
© 2021 The Association for Tropical Biology and Conservation
1Institute of Biological Sciences, Federal
University of Minas Gerais, Belo
2School of GeoSciences, University of
Edinburgh, Edinburgh, UK
3Department of Tropical Diversity, Royal
Botanic Garden Edinburgh, Edinburgh, UK
4Department of Geography, College
of Life and Environmental Sciences,
University of Exeter, Exeter, UK
5EMBRAPA Recursos Genéticos e
Biotecnologia, Brasília, Brazil
6Unidade Universitária de Mundo Novo,
Universidade E stad ual de Mato Grosso d o
Sul, Mundo Novo, Brazil
Danilo M. Neves, Institute of Biological
Sciences, Federal University of Minas
Gerais, Belo Horizonte 31270– 090, Brazil.
Conselho Nacional de Desenvolvimento
Científico e Tecnológico— CNPq/Brazil
to A.T.O.- F. (301644/88- 8); Instituto
Serrapilheira/Brazil to D.M.N. (Serra-
1912- 32082); US National Science
Foundation to D.M.N. (DEB- 1556651);
Coordenação de Aperfeiçoamento de
Pessoal de Nível Superior— CAPES/PrInt/
Brazil to D.M.N. (88887.474387/2020-
00); UK National Environmental Research
Council to R.T.P., K.G.D., D.M.N. (NE/
I028122/1); UK Leverhulme Trust
International Academic Fellowship to
Associate Editor: Ferry Slik
Handling Editor: Rakan Zawahi
The Amazon forest is far from uniform, containing different forest types and even
savannas, but quantitative analyses of this variation are lacking. Here, we applied
ordination analyses to test the floristic differentiation among Amazonian vegetation
types using data for virtually all known tree species occurring in the Amazon (8224),
distributed across 1584 sites. We also performed multiple regressions to assess the
role of climate and substrate in shaping continental- scale patterns of community com-
position across Amazonia. We find that the traditional classification of Amazonian
vegetation types is consistent with quantitative patterns of tree species composition.
High elevation and the extremes of substrate- related factors underpin the floristic
segregation of environmentally “marginal” vegetation types and terra firme forests
with climatic factors being relatively unimportant. These patterns hold at continental
scales, with sites of similar vegetation types showing higher similarity between them
regardless of geographic distance, which contrasts with the idea of large- scale vari-
ation among geographic regions (e.g., between the Guiana Shield and southwestern
Amazon) representing the dominant floristic pattern in the Amazon. In contrast to
other tropical biomes in South America, including the Mata Atlântica (second largest
rain fore st biome in the neotropics), the main floristic unit s in the Amazon are not ge o-
graphically separated, but are edaphically driven and spatially interdigitated across
Amazonia. Two thirds of terra firme tree species are restricted to this vegetation type,
while among marginal vegetation types, only white- sand forests (campinaranas) have
a substantial proportion of restricted species, with other vegetation types sharing
large numbers of species.
community composition, edaphic conditions, environmental gradients, environmentally
marginal habitats, ordination analysis, terra firme forests, tree species, white- sand forest
1 | INTRODUCTIO N
The Amazon forest, which spreads across the lowlands of the
Amazon, Orinoco and other northern drainages of South America, is
the world's largest continuous expanse of tropical rain forest, with an
ever- inc reasing numb er of desc ribe d pla nt sp ecie s (Ca rdos o et al., 2017;
ter Steege et al., 2016). Since the first scientific exploration of the 18th
and 19th centuries, it has been clear that the region is far from a con-
tinuous and undifferentiated rain forest, as there are striking contrasts
among forest physiognomies and even patches of savanna vegetation.
OLIVEIR A- FILHO Et AL.
Two main dichotomies in vegetation types have long been est ab-
lished, both using divisions based upon which environments are in-
terpreted to be more marginal (Salovaara et al., 2005). One contrasts
upland, terra firme forests growing on flood- free interfluves (literally
solid or firm ground; tierra firme in Spanish) with those growing on
the seasonally inundated floodplains along wide and slow flowing,
larger rivers (Luize et al., 2018). The other dichotomy contrasts both
terra firme and flooded forests with forest occurring on pockets of
highly leached deposits of podzolized hypo- dystrophic white- sand
(Adeney et al., 2016). But while the environmental differences be-
tween terra firme, flooded, and white- sand forests are somewhat
striking, the lines between these forests and the other vegetation
types in the Amazon are not always sharp, contributing to some no-
menclatural confusion (Phillips et al., 2003).
There are several additional prominent vegetation types in the
Amazon, growing on and around rock outcrops and coastal sands. In
both edaphic situations, the vegetation shows a wide array of phys-
iognomic expressions, including forests, dwarf- forests, scrublands,
and bushlands, often mixed in mosaics. Rock outcrops are particu-
larly evident across the chain of sandstone highlands of the Guiana
Shield (often referred to as tepuis; Berry & Riina, 2005; Huber, 1997),
and on the top of the numerous inselbergs of both the Brazilian and
Guiana Shields (Gröger, 2000; Raghoenandan, 2000). Coastal veg-
etation mosaics include extensive tracts of mangrove forests that
run almost uninterrupted from the Brazilian island of São Luís to
the Orinoco Delta in Venezuela and may penetrate inland as far as
40 km where they gradually blend with flooded forests (González,
2011; Nascimento et al., 2013). Away from the mangroves, pockets
of stabilized coastal sands bear a mosaic of vegetation types usually
referred to as restingas and matas de maré in Brazil (Silva et al., 2010).
Although virtually all the environmentally marginal vegetation
types can include open physiognomies that may resemble savan-
nas, the Amazon is also home to savannas sensu stricto, that is, those
associated with the existence of a dry season lasting for at least
3 months, and a flammable grass ground layer that may trigger fire
outbreaks (Huber, 1997). Most of these savannas experience some
form of waterlogging during the rainy season (Pennington et al.,
2006; Sarmiento, 1984).
From previous studies, we know that tree species distribution
patterns do match some of these pre- defined vegetation types at
local and regional scales (10– 100,000 km2; e.g., Draper et al., 2018;
Draper et al., 2019; Duivenvoorden, 1995; Guitet et al., 2015;
Higgins et al., 2011; Pitman et al., 2008; Scudeller, 2018; Stropp
et al. , 2011; ter St eege et al., 2000) but, so far, this has not bee n scru-
tinized for the Amazon region as a whole and all its main vegetation
types. A common conclusion stemming from the few Amazon- wide
floristic studies is that distinct vegetation types in one region tend
to resemble one another more closely than they do the same vege-
tation types in other regions (Silva- Souza & Souza, 2020; ter Steege
et al., 2006; Terborgh & Andresen, 1998). Such conclusions have led
to a view of floristic regionalization that has neglected the differ-
ent vegetation types of Amazonia. For example, there is a consistent
west to east gradient in tree community composition, congruent
with an Amazon- wide variation in soil fertility and drought (soils in
the eastern Amazon are poorer and climate is drier; ter Steege et al.,
2006). These continental- scale analyses have either been conducted
at coarser taxonomic scales— at the family (Terborgh & Andresen,
1998) and genus- level (ter Steege et al., 2006)— or have lumped taxa
from distinct vegetation types into large geographic “grid cells” (e.g.,
4° × 6° in ter Steege et al., 2006; up to 20 km distance in Silva- Souza
& Souza, 2020). Here, we bring together the most comprehensive,
species- level dataset to date on the composition of tree communi-
ties across the entire Amazon basin, where individual communities
have been assigned a priori to one of the predominant vegetation
types in the Amazon.
Our objectives are threefold. Firstly, we test the floristic dif-
ferentiation of nine vegetation types, following the classification
system proposed by Oliveira- Filho (2015). We predict that by using
comprehensive, species- level tree community surveys, most (if
not all) vegetation types will show an Amazon- wide compositional
Secondly, we test whether variation in edaphic and climatic con-
ditions controls the floristic differentiation between terra firme for-
est and other vegetation types, with marginal vegetation types being
placed in environments sometimes interpreted to be more stressful
(Salovaara et al., 2005). We predict that the floristic segregation of
lowland vegetation t ypes is primarily associated with edaphic fac-
tors (e.g., rockiness, sandiness, salinity, soil waterlogging), with cli-
mate being only important in segregating highland vegetation types
(e.g., montane forest, tepuis) from all others.
Finally, to give context to our results and to explore the floris-
tic distinctiveness of vegetation types, we also examine patterns of
species shared among these vegetation types and the propor tion of
species restricted to individual vegetation types.
2 | MATERIALS AND METHODS
2.1 | Study area
The Amazon forest, as circumscribed here (see outline in Figure 1),
includes most of the Amazon and Orinoco river basins (excluding
the Andean headwaters of some rivers and the mid- Orinoco Llanos),
and the North Atlantic coastal river basins between the states of
Delta Amacuro, in Venezuela, and Maranhão, in Brazil. With regards
to elevation, a maximum altitude of 1100 m was established on the
Andean flanks to exclude the complex and extensive vegetation and
environment gradients associated with the massive mountain chain.
No altitudinal limit was established, however, for the highlands of the
Guiana Shield, which are entirely embedded in the Amazon Province.
This is a controversial issue in the sense that some authors consider
the Guiana Highlands as a separate biogeographic province (e.g.,
Cabrera & Willink, 1980; Cardoso et al., 2017), supported by the high
number of endemic species, many of which are restricted to particu-
lar tepuis or highlands (Berry & Riina, 2005). We based our decision
on the following facts: (a) unlike the Andes, which make up a natural
OLIVEIR A- FILHO Et AL.
limit, the Guiana Highlands are encircled and pervaded by Amazonian
lowlands; (b) the highest altitudes reached by the Guiana Highlands
(2500– 3000 m) are modest compared to those of the Andes; and (c)
tepuis and highlands also share a considerable number of species with
lowland Amazonian vegetation types (Steyermark et al., 1995– 2005).
2.2 | Nomenclature
The white- sand vegetation complex is particularly thorny when it
comes to nomenclature. The main reason for this is the remarkable
variation in physiognomy, which ranges from grass/shrublands to for-
ests with slender- trunked trees and more open canopies compared
to those of adjacent terra firme forests growing on more clayey soils
(Adeney et al., 2016). Throughout the Amazon, various local terms
are also used to designate both the whole white- sand complex and
its physiognomic expressions, for example, bana, caatinga amazônica,
campina, campinarana, varillal, and chamizal (Demarchi et al., 2018;
Fine et al., 2010; García- Villacorta et al., 2016; Stropp et al., 2011).
Following Daly et al. (2016), we here adopt campinarana, because
of its official use in Brazil (IBGE, 2012) and because it embraces the
whole array of physiognomies growing on podzolized sands liable
to ground water saturation, but conveniently excludes white- sand
floodplain forests, which we distinguish in this paper.
Nomenclature for vegetation occurring on seasonal floodplains is
less complex. We use the prevailing nomenclature for two main sea-
sonally flooded vegetation types in the Amazon, distinguishing igapó
and várzea fo rests, de pen ding on th e ty pes of ri vers al o ng whi c h they
occur (see Junk et al., 2011; Kubitzki, 1987; Prance, 1979). Vár zea
forests are found along rivers carrying copious quantities of sedi-
ments (and nutrients), mostly brought from the Andes, with variation
in the amount of clay resulting in waters that are many shades of
brown. Confusingly, these rivers are often called white- water rivers
(ríos de agua blanca, rios de água branca). In contrast, igapó forests
are found along rivers with small amounts of suspended mineral
particles, which are called black or clear- water rivers (ríos de agua
negra o clara, rios de água negra ou clara). These rivers drain basins
where white sands or other highly leached soils prevail (e.g., flowing
from the Brazilian and Guiana Shields) and can carry vast loads of
humic acid colloids resulting from the arrested litter decay in these
hypo- dystrophic soils. A similar process takes place in black- water
oxbow lakes severed from white- water rivers as well as in narrower
upstream floodplains throughout the basin. The dichotomy of várzea
and igapó falls short when it comes to rivers with “mixed” waters,
and rivers with temporal and spatial variations in suspended par ti-
cles, of which the Casiquiare Channel in Venezuela is an example. In
both igapós and várzeas, vegetation structure varies from tall forests
to floodplains with more open formations, depending on local flood-
ing dynamics and related processes of either erosion or sedimenta-
tion (Kalliola et al., 1992; Luize et al., 2018; Salo et al., 1986; Worbes
et al., 1992). The timing and duration of flooding in these forests
can be variable, from once every few decades in rivers close to the
Andes (e.g., on the Manu River in Peru, pers. comm. John Terborgh)
to multiple months annually for the iconic várzeas and igapós along
major rivers such as the Amazon and the Rio Negro.
2.3 | Dataset
We extracted the dataset from the NeoTropTree (NTT) database
(http://www.neotr optree.info/), which consists of tree species
checklists compiled for geo- referenced sites, from southern Florida
FIGURE 1 Distribution of the 1584
Amazonian sites used in the analyses
with their a priori classification into nine
vegetation types. Blue and white contours
illustrate major rivers and national
borders, respectively. Our delimitation of
the Amazon is outlined in a darker, gray-
OLIVEIR A- FILHO Et AL.
(U.S.A.) and Mexico to Patagonia in Argentina and Chile. Trees here
are defined as freely standing woody plants >3 m in height, including
tree ferns. NTT currently holds 7485 sites/checklists, 20,562 tree
species, and 1,206,314 occurrence records. A site/checklist in NTT
is defined by a single vegetation type, following the classification
system proposed by Oliveira- Filho (2015), contained in a circular
area with a 10 km diameter. Where two or more vegetation types
co- occur in the area, there can be multiple geographically overlap-
ping sites in the NTT database.
The data were originally compiled from an extensive survey
of published and unpublished (e.g., PhD theses) literature, partic-
ularly those on tree community sur veys and floristic inventories.
Additional occurrence records obtained from both major herbaria
and taxonomic monographs have been added to the checklists when
they were collected within the 10- km diameter of the original NTT
site, and within the same vegetation type. NTT does not include
sites with an indication of high anthropogenic disturbance nor those
with low species richness, because this is of te n du e to low sampling/
collecting efforts, which results in poor descriptive power. Thus,
secondary forests, which might be considered a distinct vegetation
type, are not included in our study. Lowest species richness in the
Amazon dataset ranged from 20 species in savanna s.s. and campina-
rana to 100 in terra firme forest, while plot size (in tree community
surveys derived from plot data) ranged from 1 to 5 ha.
All species and their occurrence records were checked for taxo-
nomic circumscriptions and geographical distributions as accepted
by the teams of specialists responsible for the online projects Flora
do Brasil, Catalogue of the Vascular Plants of Ecuador, Peru Checklist,
Bolivia Catalogue (available at http://flora dobra sil.jbrj.gov.br/, http://
www.tropi cos.org/Proje ct/CE/, http://www.tropi cos.org/Proje ct/
PEC, and http://www.tropi cos.org/Proje ct/BC/, respectively) and
published floras (Bernal et al., 2016; Boggan et al., 1997; Cardoso
et al., 2017; Steyermark et al., 1995– 2005). We eventually eliminated
records for 111 species due to synonymy (59), invalid or dubious
name s (7), in correc t growth hab it (15), and incorr ect dist ribution (30).
The final dataset contained presence/absence data for 8224 tree
species across 1584 sites, with a total of 364,965 presences. Sites
derived exclusively from herbarium data represented 41% of the full
matrix (654 sites). The dataset also included 24 environmental vari-
ables (30 arc- sec resolution) for all its sites, derived from multiple
sources. Procedures and protocols concerning variables’ sources and
extraction are thoroughly detailed at http://www.neotr optree.info/.
We adopted the vegetation descriptors provided by NTT and
based on Oliveira- Filho (2015) to classify the sites into nine vege-
tation types: 776 terra firme forests, 171 campinaranas, 291 várzeas,
176 igapós, 55 rock outcrops, 36 tepuis, 29 coastal mosaics, 28 sa-
vannas sensu stricto (hereafter savanna s.s.), and 22 montane forests
(Figure 1; Table S1). All sites classified as tepuis and montane for-
ests occur above 1100 m of altitude (see Study Area), with tepuis
differing from montane forests in their rocky soils and dwarfish
physiognomy. The map in Figure 1 was designed using the packages
maptools (Bivand & Lewin- Koh, 2017) and raster (Hijmans, 2016) in
R Statistical Environment (R Core Team, 2018).
The NTT database also includes environmental variables for all
its sites, derived from multiple sources (at a 30 arc- second resolu-
tion). Altitude at the NTT site center was used as an integrative en-
vironmental variable. Variables representing average climate (mean
annual precipitation and temperature) as well as climate extremes
(e.g., precipitation in driest month) and seasonality (e.g., precipi-
tation seasonality) were obtained from WorldClim 1.4 data layers
(Hijmans et al., 2005). Frost frequency (days) and cloud interception
(mm) were obtained from interpolating known values as response
variables (data obtained from 135 and 57 Brazilian Meteorological
Stations measuring frost frequency and cloud interception, respec-
tively) with elevation, latitude, and the WorldClim layers as pre-
dicting variables. Soil coarseness (% sand) and soil fertility (% base
saturation) and surface rockiness (% exposed rock) were obtained
from the Harmonized World Soil Database v1.2 (available at http://
www.fao.org/soils - porta l/soil- surve y/soil- maps- and- datab ases/
harmo nized - world - soil- datab ase- v12/en/) and ranked afterward by
mid- class percentage. The use of classes was adopted because high
local soil heterogeneity can make raw figures unrepresentative. Soil
Water Storage capacity (%) was obtained from the International Soil
Moisture Network (available at www.ipf.tuwien.ac.at/insit u/).
2.4 | Analyses of community composition
We fir st explored the patterns of floristic differentiation among pre-
viously defined vegetation types by performing non- metric multidi-
mensional scaling (NMDS; McCune & Grace, 2002), and tested its
overall significance by applying an analysis of similarities (ANOSIM;
Clarke, 1993). Beforehand, we excluded 832 singletons (species
found at a single site), as they commonly increase the noise in ordi-
nation analyses without contributing information (Lepš & Šmilauer,
2003), and then computed pairwise compositional distances be-
tween all sites using Simpson distance as the dissimilarity metric
(Simpson, 1960), which describes community turnover without the
influence of richness gradients (Baselga, 2010).
We used the vegetation types confirmed in the ordination anal-
ysis to produce sets of diagnostic species based on their coef ficient
of fidelity (phi; Tichý & Chytr ý, 2006). An advantage of this coeffi-
cient is that they can take negative values, which expresses the fact
that a species tends to “avoid” a particular habitat and its environ-
mental conditions (De Cáceres & Legendre, 2009; De Cáceres et al.,
2008). In this study, diagnostic species represent those statistically
associated with one or more vegetation types so that their presence
in species lists may be a strong indicator of the veget ation types
themselves. Significance of phi was obtained via Monte Carlo per-
mutations (999). Species’ phi for each vegetation type are provided
as Supplementary Information (see Table S2).
We then used the major axes of compositional variation sum-
marized by the ordination analysis to test whether the obser ved
patterns of floristic differentiation in the Amazon are underpinned
by extreme environmental conditions segregating terra firme forests
from environmentally marginal vegetation types. First, we selected
OLIVEIR A- FILHO Et AL.
a subset of significant environmental variables for each of the major
NMDS axes through an AIC- based forward selection method for
generalized linear models and then performed an additional and
progressive elimination of collinear variables based on their vari-
ance inflation factor (VIF), informed by their ecological relevance,
until maintaining only those with VIF < 4 (Quinn & Keough, 2002).
We tested the significance of the selected environmental variables
by applying ANOVA permutation tests (999 permutations). We ex-
plored the result s visually by fitting the values of the most important
environmental variables in ordination space (NMDS). The variable
selection, VIF, NMDS and phi analyses were conducted using the
vegan (Oksanen et al., 2016), recluster (Dapporto et al., 2015), usdm
(Naimi et al., 2014) and indicspecies (De Cáceres & Legendre, 2009)
packages in R Statistical Environment (2018).
Finally, we used a chord diagram to assess the patterns of com-
positional overlap among Amazonian vegetation types. The chord
diagr am was designed using the D3 Java Environment (Bostock et al.,
2011; custom codes available at https://bl.ocks.org/nbremer).
3 | RESULTS
The distribution of the sites in ordination space yielded by NMDS
(K = 2; stress = 0.17; Figure 2) largely segregated the previously de-
fined Amazonian vegetation types (ANOSIM R = 0.85; p = 0.001). We
found a negligible decrease in stress values by adding a third NMDS
axis, and a high correlation between the distances summarized by
the first two axes and the full distance matrix (Pearson's r = 0.83).
Thus, we focused subsequent analyses on the two- dimensional ordi-
nation space, and the results are detailed below.
Axis 1 places both terra firme forests and campinaranas at inter-
mediate scores and is congruent with two gradient s: the first toward
seasonally flooded forests (várzeas and igapós), placed at one ex-
treme, and the second toward montane forests and open formations
(coastal mosaic, rock outcrops, savanna s.s., and tepuis), at the other
extreme. Axis 2 segregated várzeas, tepuis, terra firme, and montane
forests at one extreme, and igapós, campinaranas, and the remaining
open formations at the other. It is worth noting that campinaranas
seem to be closer to savannas s.s. than to terra firme forests along
this axis. In addition, the differentiation between terra firme forest,
savanna s.s., and the coastal mosaic is more nuanced and suggests
a forest- to- savanna gradient. These patterns are robust to exclud-
ing sites (checklists) compiled exclusively from herbarium data (654
sites; Figure S1).
The furthest extremes of substrate- related variables lead to
distinct, environmentally marginal vegetation types (Figure 2). The
selected environmental predictors account for 72% and 62% of the
variation in community composition summarized by the first two
NMDS axes, respectively (Table 1). An increase in sandiness was
congruent with the floristic differentiation of campinaranas from all
other vegetation types, while an increase in soil water storage ca-
pacity (a proxy of seasonal soil waterlogging) was associated with
the floristic dif ferentiation between seasonally flooded forests
(várzeas and igapós) and all other vegetation types. The somewhat
nuanced differentiation between the two seasonally flooded vege-
tation t ypes is congruent with decreasing soil fertility from várzeas
to igapós. Precipitation seasonality was associated with the floris-
tic differentiation of coast al mosaics and savanna s.s. from all other
vegetation types, with the segregation between these two being as-
sociated with higher soil sandiness in coastal mosaics. High sur face
rockiness (a proxy of soil water deficit) was congruent with the flo-
ristic segregation of forests associated with tepuis and rock outcrops
from all other vegetation types. Altitudinal gradients in cloud inter-
ception and mean annual temperature drive the floristic differenti-
ation between highland vegetation types, namely montane forests
and tepuis, and all other vegetation types. Te pui s are associated with
higher cloud interception, thus reflecting lower water deficit when
compared to rock outcrops. Finally, both tepuis and montane forests
are found under lower mean annual temperature, with intermediate
conditions of cloud interception segregating mont ane forests from
tepuis (high cloud interception) and lowland terra firme forests (low
There are a considerable number of species restricted to terra
firme forests in our dataset (4424 species), which far surpasses the
number of species terra firme shares with other vegetation types
(2032 species; Figure 3). There is also a high proportion of species
in campinaranas that are res tricted to that vegetation type (42%). In
contrast, the other seven vegetation types have a low proportion
of species restricted to them, ranging from 6% in coastal mosa-
ics and savanna s.s. to 25% in tepuis. Species shared between terra
FIGURE 2 Ordination of 1584 tree communities in the Amazon
inferred from non- metric multidimensional scaling of their species
composition. Colors indicate the a priori classification into nine
main vegetation types, and darker shades in each color indicate
overlapping circles (i.e., two or more sites show high similarity
in species composition). PrecSeas = precipitation seasonality;
CloudItcp = cloud interception; SoilFert = soil fertility; SWS = soil
water storage capacity; TempAnn = mean annual temperature
OLIVEIR A- FILHO Et AL.
firme forest (the largest species pool) and other marginal vegeta-
tion types are high. Among marginal vegetation types, the number
of species shared ranges from 18, between igapó and tepui, to 655
shared between igapó and várzeas (Figure 3). These results indi-
cate that, apart from terra firme forests, most of the tree flora of
Amazonian vegetation types are shared among t wo or more vege-
tation types, with their community compositions, which are distinct
(Figure 2), representing unique combinations of the Amazonian
4 | DISCUSSION
4.1 | Continental- scale patterns
The composition of the tree flora across the Amazon region shows
variation congruent with traditional vegetation classifications. The
most species rich and geographically widespread vegetation type
is terra firme forest, while marginal vegetation types, such as campi-
narana, savanna s.s., igapó or várzea, diverge in species composition
along distinct environmental gradients. These marginal vegetation
types house many t ree species not found in terra firme fores t, yet large
numbers of them are shared among the dif ferent marginal vegetation
types themselves, for example between savanna s.s. and campinarana.
The marginal vegetation types are placed at extreme values of
the significant environmental gradients, potentially indicating eco-
physiological stress, and our results highlighted that substrate, not
climate, is the most important environmental driver controlling the
major axes of composition in Amazonian tree communities. Different
from other forest biomes in South America, where variation in
temperature and water availability are clearly the most important
factors controlling continental- scale patterns of tree community
composition (e.g., in seasonally dry tropical forests (Neves et al.,
2015), or in the Mata Atlântica (Neves et al., 2017)), climatic condi-
tions are relatively unimportant in Amazonia (but see discussion for
montane forests and tepuis).
Moreover, because these edaphic gradients are consistently
important in segregating Amazonian vegetation types from local to
continental scales, our results run counter to previous findings which
have suggested that tree community composition in the Amazon is
primarily driven by Amazon- wide gradients in environmental con-
ditions (e.g., precipitation seasonality, soil fertility; Silva- Souza &
Souza, 2020; ter Steege et al., 2006). Previous Amazon- wide studies
analyzed tree species composition data without separating or con-
sidering the different Amazonian vegetation types. If composition is
summarized within geographic grid cells (e.g., Silva- Souza & Souza,
2020; ter Steege et al., 2006), then a given grid cell may take on
NMDS1 pNMDS2 pVIF
Cloud interception 0.2 24 <0.0001 0.059 <0.0001 2.398
Mean annual temperature 0.228 <0.0001 0.225 <0.0001 2.812
Precipitation seasonality 0.041 <0.0001 – – 1.046
Sandiness 0.051 <0.0001 0.294 <0.0001 1.990
Soil fertility – – 0.207 <0.0001 2.087
Soil water storage capacity 0.656 <0.0001 0.013 <0.0001 3.095
Surface rockiness 0.327 <0.0001 0.019 <0.0001 2.534
All variables 0.723 <0.0001 0.623 <0.0001 –
Note: Values under NMDS1 and NMDS2 represent the coefficients of determination (adjusted R2,
and their respective p- values) of generalized linear models (GLMs) between the first two axes of a
non- metric multidimensional scaling and environmental variables. Values in the last row represent
coefficients of determination of GLM- based multiple regressions between each NMDS axis and
all significant variables. VIF = variation inflation factor, as a measure of collinearity between all
variables in the analyses (variables were progressively eliminated until VIF < 4).
TAB LE 1 Significant climatic and
edaphic predictors of large- scale gradients
of tree community composition in the
FIGURE 3 Overlap in tree species composition among
Amazonian vegetation types. Values in white express the number
of species that are shared among vegetation types or restricted
to a given vegetation type, respectively (the sum of these values
represent the total species richness in that vegetation type). Chord
width is proportional to the number of shared species
OLIVEIR A- FILHO Et AL.
the compositional identit y of the dominant vegetation type in the
grid cell, and if there are geographic gradients in the prevalence
of vegetation types, the geographic grid cell approach may lead to
geographically driven results, which mask vegetation heterogeneity
within grid cells. Our approach ensured that every sample unit (i.e.,
site or community) represents only a single vegetation type, which
is likely why we find a clearer signal for vegetation type than for
geography in our results. That these vegetation types are floristi-
cally coherent across the Amazon basin also suggests that dispersal
among areas of the same vegetation type is not particularly limited
by geographic distance, in agreement with a recent study of several
Amazonian tree genera (Dexter et al., 2017).
Below we delve into the main floristic patterns observed in our
results to discuss the compositional identity and environmental dis-
tinctiveness of Amazonian vegetation types. Because the dataset
used in this study does not include sites with a high indication of
anthropogenic disturbance, we stress that analyses including com-
munity inventories (e.g., floristic checklists, plot data) from recently
degraded areas, such as early- stage secondary forests, may reveal
additional vegetation types.
4.2 | Forest types
Flooded forests share a similar environmental condition driving
their compositional distinction from terra firme forests: seasonal
flooding, potentially combined with soil waterlogging during the
low water season. This, however, does not lead to homogeneous
stands of flooded forests throughout the Amazon, and one of their
main variations was captured here as follows: the floristic, edaphic
and distributional differentiation of igapós and várzeas. Vá rzea
forests are more evenly distributed across major river basins in
Amazonia, while most igapó forests are concentrated in the Rio
Negro and upper Orinoco River Basins where the substrate is of
highly leached and impoverished white sands. Nonetheless, igapó
forests are also found in other Amazonian regions under similar
edaphic conditions (Montero et al., 2014; Wittman et al., 2010). In
addition, both types of flooded forests have species restricted to
them in our dataset (160 species restricted to várzeas and 168 to
igapós), though the largest proportion of their species composition
is either shared bet ween them or with terra firme forests (Figure 3;
The tree flora of montane forests in Amazonia is compositionally
coherent with the main floristic patterns described for Neotropical
montane flora in general, such as the presence of some genera that
are rare to absent in the lowland flora, including Bonnetia, Brunellia,
Drimys, Hedyosmum, Ilex, Laplacea, Meriania, Podocarpus, Symplocos
and Weinmannia (Webster, 1995). The overall lack of these taxa in
lowland Amazonia is likely driven by temperature, an important
environmental factor driving floristic differentiation between mon-
tane and terra firme forests in our dataset. Nonetheless, variation
in temperature across the range and location of elevations sampled
in our study is not large, thus explaining the high proportion of tree
species shared between montane forests and other Amazonian hab-
itats (88%), and supporting the claim that these forests should be
treated as Amazonian (contrasting with views in Cabrera & Willink,
1980; Cardoso et al., 2017). Igapó forests, for instance, share a lower
proportion of tree species with other Amazonian habitats (82%),
yet igapós are consistently treated as Amazonian (Wittmann et al.,
2010). The fact is that many lowland terra firme species do extend
their distribution toward high altitudes (1100– 3000 m), such as
Annona symphyocarpa, Coussapoa crassivenosa, Cyathea bipinnati-
fida, Cyathea macrosora, Elaeoluma nuda, Hieronyma oblonga, Miconia
dodecandra, Miconia pseudocapsularis, Miconia punctata, Mollinedia
ovata, Nectandra reticulata and Quiina cruegeriana; to cite a few di-
agnostic species of both mont ane and terra firme forests (Table S2).
The scarcity of mineral nutrients in white- sand environments is
probably the leading environmental distinction of campinaranas, and
plant species there are known to have acquired morphological, phys-
iological and mutualistic traits to maximize both nutrient capture
and retention (Adeney et al., 2016). This specialized flora explains
much of the differentiation of campinaranas from other vegetation
types, which is evident in the high proportion of restricted species
(42%; Figure 3). This is almost twice the proportion of endemics in
western Amazonian campinaranas found by Garcia- Villacorta et al.
(2016; 23%), but this is probably explained by the fact that those
authors worked with the whole spectrum of growth habits, and not
only trees, considered all available herbarium voucher data (not just
those collected near NTT sites as done here) and concentrated their
efforts only in western Amazonia.
4.3 | Open formations
Th e coa stal sand dep osi ts along th e Atl ant ic sho res, co vered by a mo -
saic of mangroves and sandy beaches, represent another Amazonian
vegetation type associated with white- sand substrates. However,
soils in these coast al mosaics are more fertile than in campinaranas,
and they are mostly found in the eastern Amazon, where precipita-
tion seasonality is relatively more pronounced. Nonetheless, these
white- sand, seasonally dry coastal environments are not too exten-
sive (Cremers & Hoff, 2003; González, 2011; Silva et al., 2010), nor do
they seem to be restrictive floristically, as 94% of species in coastal
mosaics are also found in other vegetation types. Accordingly, they
have one of the lowest proportions of restricted tree species in
Amazonian habitats— only 15 tree species are restricted to coastal
sand de pos its in this anal ysis, nine of which are typic al of mangroves .
Water deficit intervals, mediated by climate, substrate or both,
drive tree community differentiation in two other environments:
savannas s.s. and rock outcrops. Most savannas s.s. are found where
the dr y season is longest in the Amazon, and where fire outbreaks
may occur in the dry season. Interestingly, many of these savannas
are hyper- seasonal (sensu Sarmiento, 1983), in that they also face
some form of water excess in the rainy season, mostly due to soil
waterlogging either caused by poor drainage or floods, as in the
Bolivian Llanos de Moxos and in the Brazilian estuarine island of
OLIVEIR A- FILHO Et AL.
Marajó. Nevertheless, there are also non- hyper- seasonal savannas,
particularly on hills with shallow soils in the Brazilian state of Pará,
where the flora shares a great number of species with that of the
Cerrado savannas in Central Brazil (Devecchi et al., 2020). In fact,
the tree flora of most Amazonian savannas does show some floristic
affinity with the savannas of either the Brazilian Cerrados or the
Venezuelan Llanos (Buzatti et al., 2018; Ratter et al., 2006; see also
Devecchi et al. 2020 for comparisons between all plant life- forms).
Rock outcrops are another common feature in the Amazon
that may experience local water shortage, even in ever- wet areas,
because rainwater is promptly drained from the substrate. Rock
outcrops are particularly common across inselbergs on both
the Guiana and Brazilian Crystalline Shields, where they host
tree species not found elsewhere in the Amazon (Gröger, 2000;
Raghoenandan, 2000). The xeric nature of rock outcrops is con-
firmed by the disjunct occurrences of a considerable number of
species that are also typic al of seasonally dr y deciduous forests
outside of the Amazon, such as Aspidosperma cuspa, Brasiliopuntia
brasiliensis, Bursera simaruba, Cereus hexagonus, Guapira cuspidata,
Senegalia riparia and Vachellia farnesiana. Apart from rock out-
crops, another substrate related to periods of water deficit in the
Amazon is the hardened surface of some mudflats, such as those
found on the Guyanese coastal plains and on the meanders of the
Lower Amazon and mid- Marañon rivers. This condition probably
explains the occurrence of a typical savanna vegetation and flora
in these regions, even under year- round wet climates.
The tepuis are formed of the steep slopes and plateaus of the
massive Paleozoic sandstones atop the Guiana Shield. Environmental
factors along altitudinal gradients are hardly ever easily summarized
by one varia ble and include fa ctors such as incre asing cloud intercep -
tion (an important factor in our models) and declining temperatures
toward higher altitudes. Additional sources of environmental het-
erogeneity include slope, aspect, and surface rockiness, and there
is usually a local combination of stressful factors at play. In general,
scrubs and savannas prevail on the shallow soils and bare rocks at
the summits of tepuis (Huber, 2005), where cloud interception is the
major source of water, and are replaced by montane forests in colder
environments with deeper soils.
It is important to bear in mind that, different from forest
types, the open formations in our analyses do not represent a
tree- dominated habitat. Therefore, our comparisons are based on
the few tree species that occur in these plant communities, while
he rbs , forbs an d shrub s are not in clu ded . If data for the who le pla nt
community were available, we would expect even higher dissim-
ilarities between these open habitats and other tree- dominated
habitats, with increased number of endemic species in the former.
5 | CONCLUSIONS
Our findings show that the traditional classification of Amazonian
vegetation formations is consistent with quantitative patterns of
tree species distribution. We also demonstrate how the terra firme
forest is the core vegetation type from which the eight marginal
habitat s differentiate floristically in a manner consistent with more
extreme environmental conditions. These patterns, which have been
previously described at a regional scale, are documented here for
the first time across the entire Amazon Basin.
In addition, we show that a large proportion of tree species found
in the eight marginal vegetation types are shared among each other
and with terra firme fores ts. In fact, apar t from terra firme forests and
campinaranas, there is a small percentage of tree species restricted
to a single vegetation type in the Amazon. Nonetheless, if future
conservation strategies aim to protect the full set of tree species in
the Amazon, they must consider the identity and distribution of the
multiple vegetation types there, as well as their current status of
conservation. Many of the localities in our analyses may have been
impacted by the recent increase in deforestation and forest fires in
the Amazon, especially those found across the south and eastern
borders of the Brazilian Amazon— a region known as the “arc of de-
forestation” (Soares- Filho et al., 2006).
We are grateful to Hans ter Steege and an anonymous reviewer for
their constructive comments on the manuscript.
CONFLICT OF INTEREST
The authors declare no conflict of interest.
A.O.F compiled the database, conceived the idea, and designed the
manuscript. D.M.N. analyzed the data. A.O.F. and D.M.N. led the
writing with substantial input from R.T.P., K.G.D., and M.F.S. All au-
thors commented on the manuscript and approved the final version.
DATA AVAIL AB I LI T Y STATE MEN T
Presence/absence data for the 8224 tree species found across the
1584 Amazonian communities were extracted from the NeoTropTree
database (available at http://www.neotr optree.info/data).
Bioclimatic variables and altitude were obtained from WorldClim 1.4
data layers (available at: http://www.world clim.org/download). Soil
variables were obtained from the Harmonized World Soil Database
v 1.2 (available at: http://www.fao.org/soils - porta l/soil- surve y/soil-
maps- and- datab ases/harmo nized - world - soil- datab ase- v12/en/).
Soil Water Storage capacity was obtained from the International Soil
Moisture Network (available at https://ismn.geo.tuwien.ac.at/en/).
Ary T. Oliveira- Filho https://orcid.org/0000-0002-6766-1407
Kyle G. Dexter https://orcid.org/0000-0001-9232-5221
R. Toby Pennington https://orcid.org/0000-0002-8196-288X
Marcelo F. Simon https://orcid.org/0000-0002-5732-1716
Marcelo L. Bueno https://orcid.org/0000-0001-6146-1618
Danilo M. Neves https://orcid.org/0000-0002-0855-4169
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Supporting Information section.
How to cite this article: Oliveira- Filho AT, Dexter KG,
Pennington RT, Simon MF, Bueno ML, Neves DM. On the
floristic identity of Amazonian veget ation types. Biotropica.