Journal of

Plant Ecology
Research Article
Differences between species in seed bank and vegetation
helps to hold functional diversity in a floodable

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Neotropical savanna
Evaldo B. de Souza1,*, , Francielli Bao2, , Geraldo A. Damasceno Junior1,3, and
Arnildo Pott3,
Programa de Pós-graduação em Ecologia e Conservação, Instituto de Biociências, Universidade Federal de Mato Grosso do Sul, Campo
1

Grande, Brazil, 2Programa de Pós-graduação em Biologia Vegetal, Instituto de Biociências, Universidade Estadual Paulista, Rio Claro, SP,
Brazil, 3Programa de Pós-graduação em Biologia Vegetal, Instituto de Biociências, Universidade Federal de Mato Grosso do Sul, Campo
Grande, Brazil

*Corresponding author. E-mail: bs.evaldo@gmail.com

Handling Editor: Frank Gilliam

Received: 21 May 2020, First Decision: 27 September 2020, Accepted: 25 January 2021, Online Publication: 16 February 2021

Abstract
Aims  Our objective was to quantify the contributions of the seed bank and the established vegetation to the
species composition, functional composition and diversity, and discuss the implications of these differences in
regeneration and persistence of floodplain plant communities.
Methods  We sampled all ground cover vegetation up to 1.5 m height and seed bank in 25 plots (10 m × 1 m)
distributed across five sites in dry and rainy seasons in a periodically flooded savanna in the Pantanal wetland,
Brazil. We evaluated the soil seed bank by seedling emergence method.
Important Findings The seed bank species had traits that conferred regeneration to the communities, while
persistence traits characterized the vegetation. The seed bank had higher functional richness and lower functional
evenness than the vegetation. The existence of different plant traits between seed bank and vegetation allowed
the coexistence of species with functionally contrasting persistence and regeneration traits, which may help
maintain functional diversity. It may allow the community to be more resilient when dealing with different
environmental filters such as drought, fire and flood.
Keywords  environmental filters, functional diversity, hydrochoric dispersal, Pantanal wetland, persistence,
regeneration

种子库和植被物种之间的差异有助于保持新热带稀树草原的功能多样性
摘要：本研究的目的是量化种子库和建立的植被对物种组成、功能组成和多样性的贡献，并讨论这些
差异对冲积平原植物群落更新和稳定性的影响。我们在巴西潘塔纳尔湿地的一个周期性洪水泛滥的稀
树大草原上，在旱季和雨季对分布在5个地点的25个地块(10 m × 1 m)的1.5 m高度的地面覆盖植被和
种子库进行了采样。采用出苗法对土壤种子库进行了评价。研究结果表明，种子库物种具有赋予群落
更新的特征，而植被则具有稳定性特征。种子库的功能丰富度高于植被，而功能均匀度则低于植被。
由于种子库和植被的植物特征不同，使得具有不同功能稳定性和更新特性的物种得以共存，这将有助

© The Author(s) 2021. Published by Oxford University Press on behalf of the Institute of Botany, Chinese Academy of Sciences and the Botanical Society of China.
All rights reserved. For permissions, please email: journals.permissions@oup.com

JOURNAL OF PLANT ECOLOGY | doi:10.1093/jpe/rtab014 605

 于维持植物的功能多样性。这可能会让植物种群在应对干旱、火灾和洪水等不同的环境选择时更具有
弹性。
关键词：环境选择，功能多样性，水溶扩散，潘塔纳尔湿地，稳定性，更新
INTRODUCTION
Plants that grow in environments subjected to
seasonal events such as flood and fire develop various
strategies to overcome the limitations posed by
environmental filters. Such strategies can be divided
into two main classes, one representing persistence
[persistent niche (Bond and Midgley 2001)] and
another representing regeneration [regeneration
niche (Grubb 1977)] strategies. The persistence
strategies can be defined by longevity, drought
tolerance and capacity of established individuals to
respond to environmental changes through sprouting
(Bond and Midgley 2001). In turn, the regeneration
strategies express the requirements for a high chance
of success of a mature individual to be replaced by a
new one (Grubb 1977).
Many species in periodically flooded savannas
and grasslands are annual forbs, graminoids or
subshrubby growth habit, exclusive propagation
via seeds (Elsey-Quirk and Leck 2015; van der Valk
1981), hydrochoric dispersal of their long-lived
seeds, and having an amphibious life form (Oliveira
et al. 2015). Mainly because of the briefer life cycle
and long-lived seeds, these characteristics are most
often expected in the seed bank than vegetation
(Capon and Brock 2006; Lu et al. 2010). These traits
indicate that these species can replace individuals
within their populations through the seed bank.
Consequently, seed banks have an essential role in
maintaining diversity under environmental filters.
However, species that invest more in survival traits,
essentially basal sprouting (vegetative propagation)
and storage structures, such as rhizome or tuber are
expected to be more frequent in the vegetation than
seed bank (Lu et al. 2010; Yang and Li 2013). These
differences between the strategies may depend on
how much seed bank and vegetation are influenced
by interactions, as competition (e.g. biomass,
reproductive effort), and by environmental filters,
like fire and flood (Catian et  al. 2018; Gremer and
Venable 2014; Klimkowska et  al. 2009; Pausas and
Keeley 2014), which are periodic in the Brazilian
Pantanal.
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Tropical floodplain environments such as the
Pantanal are the largest contributors to global
diversity (Myers et  al. 2000), since the species
abundance and their distribution usually increase
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and or reduce the diversity of each place (Scheiner
and Rey-Benayas 1994). That also depends on the
environmental filters (e.g. extreme flood, droughts
and fire), as they can influence diversity differently
between seed bank and vegetation.
In the Pantanal floodplain, seasonal floods can
homogenize the seed bank between neighbouring
fields due to hydrochoric dispersion. Seed bank
homogenization leads to reduced species turnover
compared with vegetation (Hopfensperger et  al.
2009; Leyer 2006; Pagotto et al. 2011). However, in
the vegetation, differences in flood levels change
the species composition at short spatial scales
(Nunes da Cunha and Junk 2001; Pott and da Silva
2015), making differences in composition between
communities greater than in the seed bank.
Since regeneration strategies are frequent in the
seed bank and strategies of persistence are more
frequent in the vegetation (Gremer and Venable
2014; Grubb 1977; Pakeman and Eastwood 2013;
Pausas and Keeley 2014), differences in composition
and functional diversity between seed banks and
aboveground vegetation are expected. Functional
diversity is the morphological, anatomical,
physiological and phenological variety of organisms
and how they affect the ecosystem (Petchey and
Gaston 2006; Tilman 2001). Functional diversity can
be evaluated by using well-established metrics, such
as functional richness (FRic), functional evenness
(FEve) (Villéger et al. 2008) and functional dispersion
(FDis) (Laliberté and Legendre 2010).
According to Pakeman and Eastwood (2013), the
FRic of the seed bank is affected in two ways: (i) it can
have lower FRic owing to restriction of many species
in maintaining a persistent seed bank, or (ii) the
highest number of species in the seed bank can cause
higher FRic because it frequently contains species
absent in the vegetation (Biswas and Mallik 2011).
Seasonal events can keep vegetation in an initial
successional stage and make the environmental filter
JOURNAL OF PLANT ECOLOGY | 2021, 14:605–615
effect override competition (Lohbeck et  al. 2014).
Considering that competition can generate lower
FEve (Laliberté et  al. 2013) and that species in the
seed bank are less susceptible to competition, FEve
is expected to be higher in the vegetation. However,
higher competition effects on vegetation species may
generate higher FDis than in the seed bank (Laliberté
and Legendre 2010).
Some recent studies have approached the seed
bank functional diversity in front of ecological
filters (Helsen et  al. 2015; Lipoma et  al. 2018).
However, only one discussed the differences between
functional diversity in the seed bank and vegetation
(Pakeman and Eastwood 2013). To better understand
the maintenance and replacement of species, aiming
to conserve native species in wetlands, we evaluated
a floodable savanna contrasting functional and
species composition and functional and species
diversity between seed bank and vegetation. Thus,
the following specific hypotheses were tested: (H1)
The species diversity will be higher in the vegetation;
(H2) functional diversity (FRic, FEve and FDis) will
be different between seed bank and vegetation, with
higher FRic in the seed bank, and higher FDis and
FEve in the vegetation and (H3) functional and
species composition of the seed bank will be different
from the vegetation and can be a diversity reserve
during periods of drought and flood.
Figure 1: Location of study area and the five floodable vegetation types in the Pantanal wetland. Abbreviations:
GL  =  grassland, PD  =  paleodike, SS  =  spiny scrub, TB  =  T.  aurea savanna, TBS  =  Tabebuia aurea/Byrsonima cydoniifolia
savanna.
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MATERIALS AND METHODS
Study area
The Pantanal is a vast floodplain in the centre of South
America, influenced by coalescence of the Paraguay
River and its affluents, and periodically flooded by
local rain and river overflow (Hamilton et al. 1996).
According to the classification of Köppen–Geiger, the
climate is of the Tropical type Aw, with dry winter
(Kottek et al. 2006). Annual mean temperatures vary
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between 22 and 26 °C. Average annual precipitation is
1396 mm, ranging from 800 to 1600 mm (Gonçalves
et al. 2011).
Our study was carried out in the Nabileque
subregion, located near the Miranda river and
the Park Road, in the municipality of Corumbá
(Fig. 1). The area belongs to the Miranda River
sub-basin. The main vegetation types in this
subregion are periodically flooded Park Savanna
with monodominant stands of Tabebuia aurea and
Byrsonima cydoniifolia, grassy and shrubby ground
cover interspersed with treeless open grasslands
with a few shrubs (Pott et al. 2011). The vegetation
is generally used as natural pasture for cattle,
except at flooding. The soils are mainly vertisols
and planosols (Soares et  al. 2006). Sampling was
performed in permanent plots established according
to the Program for Biodiversity Research (PPBio),
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following RAPELD [RAP  =  Rapid Assessment, +
PELD  =  LTER  =  Long Term Ecological Research].
For details, see Costa and Magnusson (2010). Five
250-m-long transect lines, 1000 m apart, were
installed in a 5 km grid. Each site presents a different
vegetation type: (i) savanna with scattered T. aurea
and B. cydoniifolia trees; (ii) grassland; (iii) savanna
park with monodominance of T. aurea; (iv) paleodike
with seasonal semideciduous forest and (v) spiny
scrub (dense spiny shrubby vegetation).
unidentified transplanted for later identification.
The number of emerged seedlings was converted to
density (seed/m2).
Since germinative and dormancy characteristics
vary between species and under different
conditions, two samples of each plot were placed
in trays and submerged to 25  cm deep water for
30  days in fibreglass tanks to detect aquatic and
amphibious species present in the seed bank
and then taken back to the greenhouse to assess

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Collection of data
In each site, we randomly set five plots of 10 m ×
1 m (10 m2). To best characterize composition and
diversity, we sampled in both dry (June 2012)  and
rainy (March 2013)  seasons. We estimated the
cover and species composition of the ground cover
(including herbs, shrubs and young trees up to 1.50
m tall), with values from 1 to 5, where 1 = 1%–5%,
2  =  6%–25%, 3  =  26%–50%, 4  =  51%–75% and
5  =  76%–100% cover (Braun-Blanquet 1979).
Each plot (10 m × 1 m) was considered a replicate
of vegetation. We sampled the seed bank in each
random vegetation plot, by collecting five soil blocks
of 20 cm × 20 cm (0.04 m2), 3 cm deep, equidistant in
1.80 m. The five soil blocks in each 10 m2 vegetation
plot were combined to constitute 0.2 m2 of seed bank
replicates; thus, in total, 25 vegetation replicates (10
m2) and 25 soil seed bank replicates (0.2 m2).
To evaluate the soil seed bank, we applied the
seedling emergence method (Thompson et al. 1997).
We spread the soil forming a layer c.  2  cm thick,
over a 3 cm layer of sterilized sand for drainage, into
perforated plastic trays of 30  cm × 20  cm × 6  cm.
The trays were placed in a greenhouse covered with
transparent plastic and 20% shade screen, watered
twice a day. In each season, seedling emergence was
recorded at 15-day intervals for 120 days. Seedlings
were identified, removed and counted, and the
seedling emergence of terrestrial species (Bao et al.
2020a).
Functional traits
We established five categorical functional traits
representing the ability of establishment and
persistence (Table 1). We determined functional
traits through observation and information from
the literature (Kissmann 1997; Kissmann and Groth
1999, 2000; Lorenzi 2008; Pott and Pott 1994).
When a species presented more than one category
within the same trait, the most cited trait prevailed
(Table 1). In a few species, it was impossible to select
just a single category, and then we adopted two
(Supplementary Table S1).
Analyses of data
Species diversity
The diversity indices of species richness (S), Shannon
(H) and Simpson (D) were converted into true
diversity (Hill numbers) to describe how species
diversity differs between seed bank and vegetation.
Hill numbers integrate species richness and one
conversion of the indices H and D represented by
different orders of q. Where q  =  0 represents the
species richness (S) and ignores the abundance, q = 1
represents the exponential of Shannon’s entropy
index [exp(H)], which gives more weight to the
rare species, and q  =  2 the inverse of Simpson’s

Table 1: Functional traits of species recorded in the seed bank and vegetation of periodically flooded savanna in the
Pantanal wetland

Functional traits Categories

Growth form Graminoida; forb; liana; shrub; subshrub; tree; vine

Life history Annual; perennial

Dispersal syndrome Anemochory; autochory; hydrochory; zoochory

Propagation Basal resprouting; rooting nodes; stolon; rhizome; seeds (exclusively)

Life form Terrestrial; amphibious; emergent; rooted-floating; rooted-submerged

Species of Poaceae, Cyperaceae and Typhaceae were included in Graminoids.

a

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concentration index [1/(1  − D)] which gives less
weight to the rare species (Jost 2006). To show
the sampling representativeness, we utilized the
Hill numbers of seed bank and vegetation to build
rarefaction curves, which combine interpolation
(rarefaction) and extrapolation (prediction) (Chao
et al. 2014).
Functional diversity
To verify differences in functional diversity between
seed bank and vegetation, we utilized the metrics
of FRic, FEve and FDis utilizing the ‘R’ package FD
and the function dbFD. FDis represents the mean
distance in the multidimensional space of the trait of
individual species to the centroid of all species. When
abundance is considered, it can change the position
of the centroid toward the most abundant species.
Thereby, it is a convenient index for not being
affected by species richness (Laliberté and Legendre
2010). Since the variables are categorical, the FRic
was measured as the number of single combinations
of traits, not as the volume of the minimum convex
hull (Laliberté and Legendre 2010). As for the
functional traits, the differences in the functional
diversity metrics (FRic, FEve and FDis) between seed
bank and vegetation were tested with the Mann–
Whitney test.
Species and functional composition
To visualize a pattern in differences of species and
functional composition between the seed bank
and vegetation (H1), we performed a non-metric
multidimensional scaling (NMDS). For the NMDS
of the species composition, we utilized matrices
of Bray–Curtis distances generated from the
matrix of abundance (SB) and cover (Veg) of the
standardized species in relative values per sample
(Pakeman and Eastwood 2013). To construct the
NMDS of functional composition between seed
bank and vegetation, we utilized the matrix with
the community-weighted mean (CWM) values of
each functional trait. CWM is the mean value of
the trait of all species weighted by their relative
abundances (Ricotta et al. 2014). To calculate CWM
values, we utilized the ‘R’ package FD and the
function functcomp (Laliberté and Legendre 2010).
We calculated CWM for each seed bank sample
(n  =  25) and the vegetation (n  =  25). Differences
in species composition and functional composition
between seed bank and vegetation were assessed
by analysis of similarity (ANOSIM) with 999
permutations. For NMDS and ANOSIM, we applied
JOURNAL OF PLANT ECOLOGY | 2021, 14:605–615
the functions metaMDS and anosim of the vegan
‘R’ package (Oksanen et  al. 2019). To test CWM
differences of each category between seed bank
and vegetation, we utilized the Wilcoxon–Mann–
Whitney test, with the function wilcox.test. We
excluded from this analysis the categories rooted-
floating, rooted-submerged and hydro-zoochoric
dispersal, represented only by five, three and five
species, respectively, with very low abundance in
both seasons in both seed bank and vegetation
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(Supplementary Table S1).
RESULTS
Species diversity
In the rainy season, the diversity in three orders of
Hill numbers was higher in the vegetation than in the
seed bank. However, in the dry season, the diversity
between the seed bank and the vegetation was
similar (Fig. 2). As indicated by the rarefaction and
extrapolation curves, our sampling effort captured
the species diversity in these periodically flooded
savannas, mainly for the seed bank (Fig.  2). We
recorded a total of 201 species, 161 in the vegetation
and 121 in the seed bank, with 80 shared species
(Supplementary Table S1).
Functional diversity
FRic was higher in the seed bank only in the dry
season (P < 0.01), which means that the seed bank
has a broader niche amplitude than the vegetation
(Fig. 3a and b). FEve was significantly higher in the
vegetation in both seasons (Fig. 3c and d). However,
FDis did not vary between seed bank and vegetation
in both seasons (Fig. 3e and f).
Species and functional composition
Species composition was clearly different
between the seed bank and vegetation in the dry
(ANOSIM: R  =  0.48, P  =  0.001) and in the rainy
seasons (ANOSIM: R  =  0.43, P  =  0.001, Fig. 4a).
The functional traits composition was different
between the seed bank and vegetation in the dry
(ANOSIM: R = 0.2968, P = 0.001) and in the rainy
seasons (ANOSIM: R = 0.2075, P = 0.001, Fig. 4b).
The dissimilarity of functional traits composition
between the seed bank and vegetation was lower
than the species composition. Some functional
traits were different between the seed bank and
the vegetation (Table 2). The CWM values of forbs,
annual cycle, zoochoric and autochoric dispersal
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Figure 2: Sample-based rarefaction for species diversity (Hill numbers) of seed bank (black lines) and established
vegetation (grey lines) in dry (a, b, c) and rainy season (d, e, f) in periodically flooded savanna in the Pantanal floodplain.
Full line = interpolation, dashed line = extrapolation up to double number of individuals. Shaded area = 95% confidence
interval.

and propagation via stolon were higher in the seed
bank. In contrast, shrubs, trees and vines, perennial
cycle, zoochoric dispersal and basal regrowth were
higher in the vegetation.
DISCUSSION
We demonstrate that in this periodically flooded
savanna, the seed bank has strategies that can ensure
flexibility, allowing the germination of species in dry
and flooded phases (Bao et al. 2018). Also, differences
between the seed bank and the vegetation indicate
complementation of diversity, ensuring higher
functional diversity and, therefore, greater resilience
under seasonal variations and stochastic events.
Species diversity
The three orders of diversity were higher in the
vegetation. Furthermore, the rarefaction curves
were more bent in the seed bank than in the
vegetation. These results demonstrate higher species
turnover in the vegetation, i.e. higher variation in
species composition in the vegetation in relation
to the seed bank. The seed bank has lower species
turnover than the vegetation due to homogenization
caused by hydrochory (Hopfensperger et  al. 2009;
Lee et  al. 2014; Leyer 2006; Nilsson et  al. 2010),
which may have reduced the number of exclusive
species in each seed bank sample compared with the
vegetation.
In turn, higher diversity and species turnover in the
vegetation can be explained by one of the main features
of the Pantanal; the multifaceted composition of
different vegetation physiognomies within short spatial
scales caused by variations in flood levels on account of
small topographic variations (Girard et al. 2010; Pott and
da Silva 2015). Thereby, seasonal floods represent the
primary environmental filter in this region, selecting
species in each topographic level according to their
degree of tolerance (Bao et al. 2014, 2015, 2018; Pott and
da Silva 2015). The higher diversity in the vegetation
than seed bank only in the rainy season probably

610 JOURNAL OF PLANT ECOLOGY | 2021, 14:605–615


Figure 3: Functional diversity between seed bank (S)
and vegetation (V) in dry and rainy season in periodically
flooded savanna in the Pantanal floodplain. Significant
differences according to Wilcoxon–Mann–Whitney test
(*P < 0.05, **P < 0.01, ***P < 0.001, ns = non-significant).
Abbreviations: FRic = functional richness (a, b), FEve =
functional evenness (c, d) (Villéger et al. 2008), FDis =
functional dispersal (e, f) (Laliberté and Legendre 2010).
happened due to detectability, e.g. higher showiness of
the aerial parts of the plants, and because more species
emerge from the seed bank in the rainy season.
Functional diversity
Our hypothesis for differences in functional diversity
between seed bank and vegetation was partially
supported. The FRic was higher in the seed bank only
in the dry season. Even though species richness was
similar to the vegetation (Fig. 2), a higher FRic in the
dry season indicates that seed bank species occupy a
wider niche amplitude, and fills functional space more
than vegetation in these periodically flooded savannas.
Such a result points out the importance of seed banks
during unfavourable periods for germination and
establishment. Differently, in the rainy season, there
was no difference in FRic between seed bank and
vegetation. Considering that species richness increases
FRic (Petchey and Gaston 2006), it may have occurred
due to higher species richness in the vegetation.
JOURNAL OF PLANT ECOLOGY | 2021, 14:605–615
The abundance of functional traits was more
uniform (higher FEve) in the vegetation than seed
bank in both seasons. It indicates that the abundance of
functional traits of the vegetation is better distributed
in the niche space (Villéger et al. 2008), and, despite
lower FRic, the vegetation exerts functions more
homogeneously in the whole amplitude of niches.
The more homogeneous utilization of the niche space
tends to hinder the income of invasive species (Bao
et al. 2014, 2015; Mason et al. 2005). The invasion of
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exotic species in this region is hindered by the flood-
and-dry cycle (Bao et al. 2014) and by the presence
of native aquatic and amphibious plants (Bao et  al.
2020b), with high productivity at flood and receding
phases (Penha et al. 1999).
We detected no FDis difference between seed bank
and vegetation. The similar values of FDis indicate
that species of the seed bank and vegetation are
similarly dispersed in the multivariate space of the
functional traits. That indicates that the vegetation
is conditioned to a weaker effect of competition and
a stronger environmental filtering effect. That will
equate it to the seed bank because it is under less
competition (Klimkowska et al. 2009). Such a result
may have been caused by the intrinsic recurrence of
seasonal floods and fire events (Arruda et al. 2016),
that maintain the vegetation at an early stage of
succession, which reduces the effect of competition
on structuring the community. Minor competition
can lead to the presence of functionally distinct
species. Accordingly, it is possible that either seed
bank or vegetation, species are conditioned by
similar stronger effects of environmental filters than
by competition.
Species and functional composition
Differences in species and functional traits
composition between seed bank and vegetation
may be caused by dispersal capacity by wind, water
or animals (Goodson et  al. 2001), germination and
dormancy characteristics, seed longevity, growth and
development under the variability of environmental
conditions (Carta et  al. 2013; Gurnell et  al. 2006;
Yang and Li 2013). For lack of proper conditions,
sometimes due to seasonal variation, several species
found in the seed bank do not succeed to germinate
in specific patches; others germinate but are not
able to establish, for lack of resource or for being
outcompeted (McGraw and Shaver 1982; Poschlod
and Rosbakh 2018).
The results showed that the most abundant seed
bank traits (forbs habit, annual cycle, autochoric
611

Figure 4:  NMDS for species (a) and functional composition
(b) of soil seed bank and established vegetation in dry
and rainy season of a periodically flooded savanna in the
Pantanal floodplain.
dispersal and propagation via stolon) were
regeneration strategies associated with early stages of
succession. Thereby, they seem to be more selected
by environmental factors such as inundation than
by competition (Lohbeck et  al. 2014). Depending
on the frequency and intensity of inundations,
fast growth and persistent seed bank, which are
characteristics frequently present in annual plants
(Philippi 1993), can be the main strategies to ensure
higher resilience in the community (van Andel
and Grootjans 2005). Some studies indicate that
the higher the unpredictability and intensity of
the environmental filters such as flood, the higher
the proportion of regeneration strategies than
competitive and persistence strategies (Angert et  al.
612
2009; Klimkowska et  al. 2009; Philippi 1993). In
the Pantanal, seasonal floods are predictable, with
fluctuations in level (Hamilton et  al. 1996; Nunes
da Cunha and Junk 2004) less intense than Brazilin
Amazonian floodplains (Parolin et al. 2010).
As expected, the vegetation showed more
abundant traits associated with persistence strategies
and with more advanced stages of succession (e.g.
arboreal, shrubby and liana habit, perennial cycle,
zoochoric dispersal and basal resprouting). These
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traits, in general, belong to species with well-
developed storage organs and sprouting systems.
Their vegetative regrowth expresses competitive
abilities, such as underground reserves to provide
post-flood resprouting, allowing their persistence
in the community (Bellingham et  al. 2000; Bond
and Midgley 2001; Pott and Pott 1994). On the
other hand, we found that approximately one-
third of the woody species (trees and shrubs) in the
vegetation are reproduced mainly by seeds. Some
woody species (e.g. Cecropia pachystachya) may show
abundant seedlings emerged from the seed bank (see
Supplementary Table S1 and de Souza et  al. 2019).
This trade-off between seed production and regrowth
in woody plants depends on the type and intensity
and frequency of environmental filters (Bellingham
et al. 2000; Slik et al. 2015).
Whereas many flood-tolerant species have
strategies to withstand flood (such as aerenchyma,
adventitious roots, germination delay, hypertrophied
lenticels), other species are somehow flood
dependent. Several annual herbs of the study area
need saturated or wet soils to germinate and grow;
others depend on inundation to enhance recruitment,
such as Richardia grandiflora, Euploca procumbens
and Cyperus surinamensis (de Souza et  al. 2016).
Besides determining establishment, acting as an
environmental filter, inundation is also determinant
in dispersal; consequently, in the spatial distribution
of species regenerating from the seed bank (Oliveira
et al. 2015).
In conclusion, the environmental filters in
these periodically flooded savannas select for both
regeneration and persistence strategies, which
can be seen separately between the seed bank and
vegetation. These strategies allow the coexistence
of species functionally contrasting, which allows
the community to be more resilient when subjected
to the different environmental filters that occur in
this periodically flooded savanna. On account of
JOURNAL OF PLANT ECOLOGY | 2021, 14:605–615
Table 2:  Wilcoxon–Mann–Whitney test for CWM of functional traits between seed bank (S) and vegetation (V) in dry and
rainy seasons in a periodically flooded savanna in the Pantanal wetland

Dry season Rainy season

Traits V (md) S (md) P value V (md) S (md) P value

Habit

 Graminoid 0.218 0.226 0.491 0.200 0.194 0.922

 Herbaceous 0.238 0.502 <0.001 0.296 0.552 <0.001

 Liana 0.012 0.000 0.083 0.015 0.000 0.045

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 Shrub 0.147 0.012 0.003 0.134 0.007 <0.001

 Subshrub 0.087 0.066 0.542 0.092 0.101 0.229

 Tree 0.053 0.000 <0.001 0.025 0.000 <0.001

 Vine 0.086 0.005 0.002 0.088 0.011 0.009

Life cycle

 Annual 0.169 0.378 <0.001 0.192 0.370 <0.001

 Perennial 0.831 0.622 <0.001 0.808 0.630 <0.001

Dispersal

 Anemochoric 0.161 0.081 0.096 0.102 0.064 0.136

 Autochoric 0.267 0.423 <0.001 0.273 0.391 0.007

 Autochoric–hydrochoric 0.117 0.081 0.634 0.081 0.114 0.345

 Hydrochoric 0.209 0.305 0.325 0.255 0.282 0.107

 Zoochoric 0.136 0.000 <0.001 0.137 0.039 <0.001

Propagation

  Node rooting 0.002 0.004 0.853 0.005 0.004 0.989

 Stolon 0.017 0.068 0.003 0.040 0.126 0.003

  Seeds (exclusively) 0.334 0.440 0.114 0.380 0.402 0.290

  Basal resprouting 0.316 0.171 0.005 0.317 0.184 0.009

 Rhizome 0.216 0.248 0.491 0.195 0.186 0.944

Life form

 Amphibious 0.299 0.251 0.312 0.267 0.242 0.790

 Emergent 0.136 0.141 0.474 0.126 0.123 0.375

 Emergent-amphibious 0.078 0.097 0.149 0.046 0.099 0.060

 Terrestrial 0.433 0.354 0.458 0.450 0.424 0.046

Significant differences in bold (P < 0.05). Abbreviation: md = median.

the distinct characteristics found between seed bank Supplementary Material

and vegetation, the seed bank can be able to replace
species and functional traits in the vegetation, and
therefore it is a fundamental strategy for diversity
maintenance after flood events, or in a scenario of
prolonged drought.
Supplementary material is available at Journal of
Plant Ecology online.
Table S1: List of species with respective functional traits
and values of seed bank density (seeds/m2) and vegetation
cover (%) in floodable grasslands in the Pantanal wetland.

JOURNAL OF PLANT ECOLOGY | 2021, 14:605–615 613

Funding
This work was supported by the Coordenação de
Aperfeiçoamento de Pessoal de Nível Superior
(CAPES) under grant PNADB-17/2009.
Acknowledgements
To Instituto Nacional de Áreas Úmidas (INAU)/CNPq
and Programa de Pós-Graduação em Biologia Vegetal
of UFMS (Universidade Federal de Mato Grosso do
Sul) for facilities. To Rosa Helena da Silva, Fernando
A. Ferreira and Vali J. Pott for the help in field work
and seedling identification.
Conflict of interest statement. The authors declare that
they have no conflict of interest.
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