Forest Ecology and Management 460 (2020) 117906

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Forest Ecology and Management

journal homepage: www.elsevier.com/locate/foreco

Fine-scale effects of bamboo dominance on seed rain in a rainforest T

a,⁎ b c a,d
Ketlen Bona , Keila N. Purificação , Thiago B. Vieira , Henrique A. Mews
a
Universidade Federal do Acre, Programa de Pós-Graduação em Ecologia e Manejo de Recursos Naturais, Caixa Postal 500, 69920-900, Rio Branco, AC, Brazil
b
Universidade do Estado de Mato Grosso, Programa de Pós-Graduação em Ecologia e Conservação, Caixa Postal 08, 78690-000, Nova Xavantina, MT, Brazil
c
Universidade Federal do Pará, Programa de Pós-Graduação em Biodiversidade e Conservação, Rua Coronel José Porfírio, 2515, São Sebastião, 68372-040, Altamira,
Pará, Brazil
d
Universidade Federal do Acre, Centro de Ciências Biológicas e da Natureza, Caixa Postal 500, 69920-900, Rio Branco, AC, Brazil

A R T I C LE I N FO A B S T R A C T

Keywords: Bamboo dominance in tropical forests drives changes in floristic composition and vegetation structure. However,
Seed dispersal the role of bamboo dominance over ecosystem functions - including those related to forest regeneration - has
Ecological filters received less attention. This study evaluated the fine-scale effects of the dominance of native bamboo Guadua
Ecosystem functions weberbaueri Pilg. (Poaceae) on seed rain in a terra-firme forest in the southwest of the Brazilian Amazon to
Guadua
understand how bamboos remain a dominant element where they occur. We tested the hypothesis that bamboo
Natural regeneration
dominance (i) reduces seed diversity and biomass and (ii) changes floristic composition and frequencies of seed
dispersal mechanisms. For one year, we sampled seeds from seed rain in adjacent bamboo-dominated (BD) and
bamboo-free (BF) environments in a forest without major anthropogenic disturbances. We found lower seed
species richness in the BD environment and similar seed biomass between BD and BF. In addition, the seed
species composition differed between BD and BF, with higher frequency of abiotic mechanisms to seeds dispersal
in BD. We conclude that the dominance of bamboos acts as a filter for species that arrive via seed rain, modifying
the floristic composition and dispersal mechanisms and, consequently, the dynamics of natural regeneration
processes of terra-firme forests in the Amazon. This process can promote the permanence and expansion of the
distribution area of bamboos in tropical forests.

1. Introduction
The dominance of biotic elements within communities can interfere
with ecological processes essential for maintaining biodiversity
(Hooper et al., 2005; Marimon et al., 2012; Steege et al., 2013). Bam-
boos, for example, are an important structural component of the ve-
getation and flora of many tropical terrestrial ecosystems, mainly be-
cause they respond positively to local environmental changes and
become dominant in many places (Bystriakova et al., 2004; Lima et al.,
2012; Santana and Anjos, 2010; Zhang and Xue, 2018). Aggressive
growth strategies and competitive superiority allow bamboos to easily
spread opportunistically in forests (Montti et al., 2014; Yang et al.,
2015). As consequence, higher bamboo densities decrease the richness
of woody species (Silvério et al., 2010; Suzaki and Nakatsubo, 2001),
open the canopy (Carvalho et al., 2013; Lima and Gandolfi, 2009;
Silveira, 2005), alter the structure (e.g., forest physiognomy and density
of woody individuals) and the dynamics of vegetation and carbon
(Taylor and Zisheng, 1988; Zaninovich et al., 2017; Zhang and Xue,
2018) and make the effects of fire on plants more severe (Mews et al.,
2013; Smith and Nelson, 2011) in natural environments. These effects
can change luminosity and the temperature and humidity of air and
soil, altering the ecosystem functions in forest, by the homogenization
of the local microclima (Chen et al., 1999).
Recent evidence has shown that bamboo dominance also interferes
with nutrient cycling, like carbon fixation, decreasing the soil quality
and aggravating the forest degradation by decrease primary production
(e.g., Xu et al., 2019; Zaninovich et al., 2017). Similarly, other eco-
system functions may be affected by the dominance of biotic elements
on species composition and vegetation structure, such as those linked to
forest regeneration and resilience. Seed dispersion patterns can be
modified in anothers monodominances vegetation, such as mono-
dominant forest of Brosimum rubescens Taub. (Moraceae) present in the
southern edge of the Brazilian Amazon (Marimon and Felfili, 2007).
Another study conducted on an urban forest fragment in the Atlantic
Forest of southeastern Brazil revealed that areas dominated by the
bamboo Aulonemia aristulata (Döll) McClure (Poaceae) have lower seed
richness and differ in dispersed seed composition (Guaratini et al.,
2014) when compared to free-bamboo areas. These results highlight the

⁎
Corresponding author.
E-mail address: bonaketlen@gmail.com (K. Bona).

https://doi.org/10.1016/j.foreco.2020.117906
Received 18 November 2019; Received in revised form 10 January 2020; Accepted 12 January 2020
0378-1127/ © 2020 Elsevier B.V. All rights reserved.
K. Bona, et al.
role of dominant species on the structure of vegetation communities
and provide insights into the mechanisms by which a species can re-
main dominant in the ecosystem.
In the southwest of the Brazilian Amazon, bamboos are widely
distributed and are present in five of the 11 existing forest typologies
(Silveira, 2005). Patches dominated by bamboos are so common in this
region that it has been cited as the largest area of bamboo-dominated
forest in the entire Neotropical region (Carvalho et al., 2013; Griscom
et al., 2007). These patches are so large that they can be observed even
from satellite images (Nelson, 1994), which shows the effect of bamboo
dominance on the structure and physiognomy of the vegetation in this
region. Moreover, in this portion of the Amazon, bamboo patches are
favored by frequent human disturbances, such as logging and the use of
fire in deforestation for pastures (Medeiros et al., 2013). This can in-
duce maintaining the current dominance of bamboo in the region and
promote their demographic expansion, which tends to affect biodi-
versity conservation and resilience of ecosystem functions and decrease
the productivity of these forests (Oliver et al., 2015a; Guilherme et al.,
2004; Silveira, 2005).
Seed dispersal is a key ecosystem function for maintaining plant
diversity in forests, which in turn provides resources for the seed dis-
perser faunal. Thus, the absence or limitation of seed dispersal can
compromise the natural regeneration of forests (Holl, 1999). Seed rain,
for example, is one of the main sources of recruitment and replacement
of new individuals and species, as well as the availability of propagules
and dispersal agents (Grombone-Guaratini and Ribeiro, 2002). How-
ever, to date there is no information in the literature about the influence
of the dominance of native bamboo species on seed rain of forest species
on small spatial scales. Furthermore, understanding the effects of
bamboo dominance is essential to unravel the mechanisms that favor
the population expansion of bamboo patches mediated by the increase
in the occupied area. If dense bamboo patches tend to increase in size
by temporal expansion of their spatial boundaries, it is reasonable to
conjecture that changes in ecosystem functions (e.g., seed dispersal) can
be detected even on small spatial scales (Powell and Aráoz, 2018;
Viswanathan et al., 2014). In this way, this study aimed to reveal one of
the mechanisms that promote the maintenance of bamboo populations
as dominant elements through a feedback loop amidst the natural re-
generation of forests in fine spatial scale.
Our objective was to evaluate the fine-scale effects of the dominance
of the native bamboo Guadua weberbaueri Pilg. on seed rain in the
southwest of the Brazilian Amazon to understand how bamboos remain
dominant. Specifically, we tested the hypothesis that bamboo dom-
inance (i) reduces seed diversity and biomass and (ii) changes floristic
composition and frequencies of seed dispersal mechanisms.
2. Material and methods
2.1. Study area
This study was conducted at the Catuaba Experimental Farm (CEF;
10°04′S and 67°37′W), Senador Guiomard, state of Acre, southwestern
of the Brazilian Amazon (Fig. 1). This site is located in the largest area
of bamboo-dominated forest of the entire Neotropical region (Griscom
et al., 2007). The CEF has an area of 1,200 ha (Medeiros et al., 2013)
and includes tropical terra-firme rainforest vegetation, secondary forests
in different successional stages and dense forest (Medeiros et al., 2013;
Silveira, 2005). More specifically, CEF is part of an Open Ombrophilous
Forest fragment whose natural vegetation has not been subjected to
major environmental disturbances (e.g., deforestation and fire). In this
forest there are dense patches of bamboo of the species Guadua we-
berbaueri and palm trees. In CEF, as well as with much of the region’s
vegetation, bamboo patches often get sharp limits with areas not oc-
cupied by bamboos within the same landscape.
In the CEF region, predominant soils are classified as Oxisols, oc-
curring in areas of undulating relief, and Ultisols, found in areas where
2
Forest Ecology and Management 460 (2020) 117906
relief is smooth to undulating (Bardales et al., 2010). The average of
temperature is 21.9°C to 25.9°C and annual rainfall is 2,200–2,500 mm
and is mainly concentrated from December to March, with the highest
monthly rainfall in January (297 mm), while the driest period corre-
sponds to the months from May to August, with the lowest rainfall in
August (43 mm) (Alvares et al., 2013). Over the study period (Jan/
2018–Dec/2018), monthly rainfall and temperature averages had no
significant variations from historical data in the region (see
Supplemental Material, Figure S1).
G. weberbaueri bamboo has a life cycle of 28–32 years and is a se-
melparous species (i.e., dies after flowering and fruiting), making it an
important part of the forest dynamics in the region (Carvalho et al.,
2013; Castro et al., 2013). Guadua bamboos are C3 woody plants
(Taylor et al., 2010) whose the long-necked pachymorph rhizomes
(Judziewicz et al., 1999) spread horizontally over tens of meters and
sprout according to the availability of resources essential for their co-
lonization (i.e., space and light) (Silveira, 2005; Torezan and Silveira,
2000). Besides that, G. weberbaueri has thorny branches that intensify
their aggressiveness during development, as they facilitate support of
the stem on trees and enable continuous stem growth, which promotes
rapid dominance in the understory and allows bamboo reaches the
canopy at 35 m (Griscom and Ashton, 2006; Silveira, 1999).
2.2. Sampling design and data collection
We delimited and georeferenced the boundaries between a bamboo
patch of approximately 13 ha (bamboo-dominated forest - BD) and an
adjacent forest area without bamboo (bamboo-free forest - BF). We then
defined and marked the BD-BF contact area, which was approximately
1.1 km long. Mapping the BD-BF boundaries followed the sinuosities of
the bamboo patch boundaries, so that the experiment could be installed
exactly at the boundaries between adjacent BD and BF environments
(Fig. 1). Adjacent BD and BF environments have a clear difference in
vegetation structure, as BD environments have smaller trees and lower
density than BF environments (Supplemental Material, Figure S2).
Along the BD-BF boundary, we installed 30 pairs of 10 × 10 m plots
(100 m2 each), totaling 60 plots (Fig. 1) and 6,000 m2 sampling area.
These plots were established in order to characterize the environments
(i.e., counting and measuring trees and counting bamboo culms) around
of the seed traps (see Supplemental Material, Figure S2). We defined
approximately 30 m between the plots of the same treatment and ap-
proximately 50 m between different treatments. The BD environment
plots were located in sites where the culm density was ≥ 10/100 m2
(10 bamboo culms on a 10 × 10 m plot), as this criterion is an indicator
of bamboo-dominated forests (Griscom and Ashton, 2003). On the other
hand, all plots of the BF environment were set in areas without bamboo
culms or where the density of culms was less than 2/100 m2 (this oc-
curred only on two plots).
Seed rain was sampled with seed traps of 50 cm in diameter (cir-
cular collectors measuring 1,963.5 cm2), at one meter from the ground
in the center of each plot in both environments, totaling 60 seed traps
and total sampling area of 117.810 cm2. The seed traps were con-
structed with 6 mm thick steel rebar and 50 cm deep bags made from
2 mm nylon mesh, which were fixed to the circular steel structures. We
collect all the fruits and seeds deposited in the seed traps every 15 days
for a year, between December 2017 and December 2018. Since most of
the dispersed seeds are still inside a fruit when they are dispersed by the
mother plant (Cousens et al., 2010; Dardick and Callahan, 2014), we
consider all diaspores (i.e., dispersion units) as seed rain. Thus, in ad-
dition to the dispersed seeds we collect the dehiscent and indehiscent
fruits that have fallen into the seed traps.
After the biweekly screening of material accumulated in the traps,
all diaspores (hereafter ‘seeds’) were packed in paper bags, separated
into morphotypes, counted and photographed on graph paper to com-
plement identification. We then identified seeds to the lowest possible
taxonomic category by comparison with identification guides (e.g.,
K. Bona, et al.
Fig. 1. Geographic position of the field experiment and arrangement of the adjacent sampling sites of bamboo-dominated (●) and bamboo-free (▲) in the Catuaba
Experimental Farm (CEF; 10°04′S and 67°37′W), Senador Guiomard, Acre State.
Camargo et al., 2008; Cornejo and Janovec, 2010), with material de-
posited in virtual herbaria and at the Herbarium of the Universidade
Federal do Acre (UFAC, Federal University of Acre) and consultation
with local parabotanists. We checked the spellings of names, the clas-
sification of botanical families and whether the morphospecies were
native or non-native to Brazil in the List of Species of the Brazilian Flora
(Flora do Brasil 2020 under construction, 2019). Then, seeds were dried
in a forced-air oven at 65°C for 72 h or until constant weight. After
drying, we weighed all seeds on an analytical balance accurate to
0.001 g. We determined the total seed biomass of seed rain from each
environment using the equation proposed by Honorio-Coronado and
Baker (2010), after adjusting the collector area, which was:
Average weight (g ) 108 cm2 1 Mg
Seed biomass = * * = XX Mg ha−1
Traps area (cm2) 1 ha 106 g
This protocol provides calculations that make it possible to obtain
the biomass (Mg ha−1) of seeds and fruits from the dry weight of the
samples.
To evaluate dispersal mechanisms, seeds were classified into two
categories: dispersed by abiotic mechanisms (AM) (i.e., anemochory,
barochory and autochory) and by biotic mechanisms (BM) (i.e.,
zoochory) (Van der Pijl, 1982). Here, we consider only primary dis-
persal, since seeds were intercepted before reaching the ground, which
excludes the participation of invertebrates (e.g., ants) that potentially
promote secondary seed dispersal in forests (Christianini and Oliveira,
2010; Magalhães et al., 2018). We defined the mechanisms of dispersal
by consulting the specialized literature (e.g., Clobert et al., 2012; Howe
and Smallwood, 1982; Van der Pijl, 1982) and by observing the mor-
phological characteristics of seeds (e.g., fleshy fruits and seeds, with
regurgitation and defecation of animals and the presence or absence of
winged structures).
3
Forest Ecology and Management 460 (2020) 117906
2.3. Data analysis
The seed species richness was compared between BD and BF en-
vironments by individual-based rarefaction analysis (Gotelli and
Colwell, 2001) with interpolations and extrapolation derived from Hill
series, with no weight for abundance (order q = 0). In this analysis, we
used the iNEXT function of the iNEXT package (Hsieh et al., 2016).
To compare the seed rain biomass between BD and BF environ-
ments, we performed a paired t-test using the average dry weight of
seeds from both environments. The t.test function was performed in the
statistics package (R Core Team, 2019).
To identify idiosyncrasy in species composition we perform two
Permutational Multivariate Analysis of Variance (PerMANOVA;
Anderson, 2001) to comparing the abundance and presence/absence of
seed species between BD and BF environments. The heterogeneity be-
tween groups with respect to species composition was tested with a
Permutational Multivariate Analysis of Dispersion (PERMDISP;
Anderson et al., 2006). These analyses were performed with Bray-Curtis
for abundance and Jaccard presence/absence as distance index, with
the adonis and betadisper functions, respectively, in the vegan package
(Oksanen et al., 2019). Subsequently, the Similarity Percentage analysis
(SIMPER; Clarke, 1993) was applied to verify which species have the
greatest contribution to dissimilarity between groups. To do so, we used
the simper function in the vegan package (Oksanen et al., 2019). Finally,
the frequency of biotic and abiotic seed dispersal mechanisms was
compared between BD and BF environments using a chi-square test
using the chisq.test function on the stats package (R Core Team, 2019).
All analyses were performed on R 3.6.1 environment (R Core Team,
2019) from the specific functions and packages mentioned above and
using a significance level of 5%. We employed 999 unrestricted Monte
Carlo permutations in all randomization-based analyses.
K. Bona, et al.
3. Results
3.1. General characterization of seed assemblages
A total of 4,635 seeds were recorded in both environments, of which
2,161 (46.6% total) occurred in the environment with bamboo (BD)
and 2,474 (53.4%) in the environment without bamboo (BF). The mean
density was 3.7 ± 2.9 seeds/m2 in the BD environment and 4.2 ± 4.1
seeds/m2 in the BF environment. The total biomass of seeds was
1.38 Mg ha−1, of which 0.54 Mg ha−1 was recorded in the BD en-
vironment and 0.83 Mg ha−1 in the BF environment.
The 4,613 seeds were distributed in 264 species, 146 genera and 55
botanical families. Thirty-nine morphospecies (14.8% total) were
identified at the species level, 184 (69.7%) at the genus level, 42
(15.9%) at the family level and 13 morphotypes remained un-
determined. Seven morphospecies (2.7%) belonged to species not na-
tive to the Amazon and Brazil (see Supplementary Material, Table S1).
In the BD environment, there were 141 species (53.4% total) dis-
tributed in 89 genera and 44 families, while in the BF environment
there were 198 species (75%), 121 genera and 52 families. Seventy-two
species (27.3%) were common to both environments, while 62 (23.5%)
and 124 (46.9%) occurred exclusively in BD and BF environments, re-
spectively.
3.2. Comparison of the seed assemblage structure
The rarefaction analysis revealed a smaller richness in the BD en-
vironment in relation to the BF after making the sample effort equal,
both for observed richness and for the estimated richness (Fig. 2).
The average dry weight of the seeds that arrived by seed rain did not
differ between the BD and BF environments (t = -1.416; df = 58;
p = 0.162). The seed species composition differed between BD and BF
environments considering both abundance (PerMANOVA, Pseudo-F (1,
58) = 1.873; p = 0.002) and species presence and absence
(PerMANOVA, Pseudo-F (1, 58) = 1.704; p = 0.001), which demon-
strates the consistency of the groups. However, these groups did not
differ with respect to how species composition varies among samples,
suggesting homogeneity with both abundance (PERMDISP, Pseudo-F (1,
58) = 2.770; p = 0.101) and species presence and absence data (PER-
MDISP, Pseudo-F (1, 58) = 1.069; p = 0.305). The similarity percentage
analysis (SIMPER) pointed to six species that contributed to the dif-
ference in composition between groups (Table 1).
The frequencies of abiotic mechanisms (AM) for seed dispersal did
not differ between the two environments. On the other hand, the BD
environment presented smaller frequency of seed dispersal by biotic
mechanisms (BM) (35.1%) than the BF environment (64.9%) (Table 2),
Fig. 2. Individual-based rarefaction curve showing seed species richness in
adjacent bamboo-dominated (●) and bamboo-free (▲) forest environments in
the southwestern Brazilian Amazon. The continuous and dotted lines represent
the observed (interpolation) and estimated (extrapolation) species richness,
respectively. Lines represent mean values and ranges represent 95% confidence
intervals.
4
Forest Ecology and Management 460 (2020) 117906
Table 1
Seed species identified by the Similarity Percentage
analysis (SIMPER) as those that contributed most to
species composition dissimilarity in adjacent bamboo-
dominated and bamboo-free forest environments in
the southwestern Brazilian Amazon.
Species p-value
Ochroma pyramidale 0.013
Bellucia sp. 0.008
Chorisia sp. 2 0.019
Casearia sp. 1 0.004
Carica sp. 4 0.002
Solanum sp. 5 0.028
Table 2
Number (and proportion - %) of the frequency of occurrence of seed dispersal
mechanisms sampled in adjacent bamboo-dominated and bamboo-free forest
environments in the southwestern Brazilian Amazon.
Environment Abiotic mechanism Biotic mechanism
Bamboo-dominated 334 (49.5%) 222 (35.1%)
Bamboo-free 341 (50.5%) 412 (64.9%)
which changed the frequencies of seed dispersal mechanisms between
BD and BF environments (χ2 = 27.41; df = 1; p less than 0.001).
4. Discussion
Our study provides unprecedented information on the interference
of native bamboo population densities with the colonization and nat-
ural regeneration mediated by the arrival of plant species propagules in
forests. This confirms our initial expectations that the dominance of
bamboo in forests reduces diversity, modifies the composition of species
that arrived via seed rain and, consequently, alters animal seed dis-
persal strategies even on small spatial scales. However, the results did
not support our hypothesis that the seed biomass is lower in bamboo-
dominated forest patches. Our results revealed for the first time one of
the mechanisms by which bamboos maintain their dominance and still
expand demographically in forests of the southwest Amazon. In the
following, we present explanations for these results and point out the
possible implications of these findings for the conservation of functions
related to the colonization and natural regeneration of tropical forests.
Differences in seed species richness between adjacent environments
with and without bamboos indicate that bamboo dominance limits
species arrived via seed dispersal. Usually, the dominance of bamboo in
forests reduces tree species richness (Silvério et al., 2010) and the
competitive aggressiveness of bamboos promotes mortality of woody
species (Medeiros et al., 2013), which may interfere with production
and dispersal of propagules. Nevertheless, contrary to our initial ex-
pectations, the lower seed richness in environments with bamboo did
not reflect lower seed biomass in these sites. This can be explained by
the fact that areas dominated by bamboo usually have sharp canopy
(Carvalho et al., 2013; Lima and Gandolfi, 2009), which should in-
crease the arrival of wind-transported seeds, for example. Moreover, the
proximity of the two environments puts them in the same regional
species pool. If local species richness is low despite the regional species
pool, we can assume that local processes limit species diversity (Cornell
and Harrison, 2014; Srivastava, 1999). Thus, our results suggest that
bamboos do not limit the seeds arrival but filter the species that get can
arrive via dispersal. This can interfere with the stability of the local
community, given the ecosystem functions performed by species. In
addition, the impacts of bamboo dominance on ecological processes
through loss of biodiversity may compromise the resistance of these
forests to disturbances (Oliver et al., 2015a, 2015b) and keep them in a
stable condition for maintenance of bamboos populations.
K. Bona, et al.
Changes in the composition of seed species between environments
with and without bamboos are in according the pattern found in other
tropical forests and reveal that such changes can also be seen on a small
spatial scale. Alterations in floristic composition related to areas with
dense populations of bamboos are frequently reported, both for woody
species that can provide propagules (Griscom et al., 2007; Silveira,
2005; Silvério et al., 2010) as well as for the arrival of propagules in
tropical forests (Guaratini et al., 2014; Rother et al., 2009). Our findings
show the effect of bamboos in the structure of the dispersed seed as-
semblage, since bamboos reduces the number, composition and abun-
dance of seed species at these sites. The seeds of the species that most
contributed to the differences in composition (Ochroma pyramidale,
Bellucia sp., Chorisia sp. 2 and Casearia sp.) reached at a smaller pro-
portion in environments with bamboos, while seeds of Solanum sp. 5,
for example, did not reach these environments. Most of these species
have zoochoric dispersal, suggesting that there is a decline in seed
dispersal agents in bamboo-dominated forest environments.
The higher frequency of dispersion by abiotic mechanisms in
bamboo-dominated environments may be related to the fact that these
sites usually have lower density of tree species (Supplementary
Material, Figure S2; Silvério et al., 2010), which makes them even less
attractive to seed-dispersing fauna (Anjos, 2006; Lima et al., 2012).
Although bamboos markedly open the forest canopy (Lima and
Gandolfi, 2009; Silveira, 2005) and possibly facilitate the arrival of
wind-dispersed seeds, they quickly dominate the sub-canopy (Silveira,
1999). This may limit the presence and affect the movement of po-
tentially seed-dispersing fauna within forests and thus to facilitate the
bamboos cycle. Although birds are one of the most important groups for
tropical forest seed dispersal services (Fleming and Kress, 2011; Kissling
et al., 2009), most bird species associated with environments with
bamboo are insectivorous (Areta et al., 2009; Rother et al., 2013;
Socolar et al., 2013). Moreover, increased density of the understory
vegetation acts as a filter for bats, another important group of seed
dispersers (Bello et al., 2017), which forage on the forest understory
(Marciente et al., 2015; da Silva and Silveira, 2016). Consequently, the
lower movement of frugivorous animals in environments dominated by
bamboo hinders the regeneration process of these sites due to the
smaller number of seed species being transported. Fauna-mediated seed
dispersal in forests is the initial step in restoring impacted areas and,
even in stable forests or at an advanced succession process, is essential
in conserving natural forests (Catterall, 2018; Wunderle, 1997). Thus,
the role of bamboo as a filter for species that attract seed-dispersing
fauna contributes to the reduction of biodiversity in these locations,
which may lead to the loss of essential ecosystem functions linked to
colonization and forest regeneration. Taken together, these finds sug-
gest that bamboos act as a filter for seed species where they occur,
implying one of the mechanisms that support the feedback loop of
bamboos amidst the natural regeneration of forests, even on a fine
spatial scale.
5. Conclusions
In conclusion, bamboo dominance reduces diversity and alters the
composition of seed species that arrive into forests via seed rain, which
directly affects the dynamics of Amazonian terrestrial ecosystems,
particularly the functions related to colonization and regeneration. Our
study deepens the understanding of the mechanisms by which bamboos
remain the dominant element by revealing that bamboos filter seed
species that arrive in forests. Further, bamboos interfere with the way
these seeds are dispersed and increase the circulation of dispersed
propagules via abiotic dispersal mechanisms. With climate change and
intense transitions in land use in the Amazon, it is possible that bam-
boos will find increasingly favorable conditions for proliferation. As
consequence of the positive response to environmental changes, bam-
boos can stabilize in forests subject to frequent impacts and thus pro-
mote the replacement of woody plants with permanent and dense
5
Forest Ecology and Management 460 (2020) 117906
populations of bamboo.
CRediT authorship contribution statement
Ketlen Bona: Writing - original draft, Methodology, Data curation,
Formal analysis. Keila N. Purificação: Writing - review & editing,
Conceptualization. Thiago B. Vieira: Writing - review & editing,
Formal analysis. Henrique A. Mews: Conceptualization, Methodology,
Supervision, Resources, Writing - review & editing.
Declaration of Competing Interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influ-
ence the work reported in this paper.
Acknowledgements
To the Coordination for the Improvement of Higher Education
Personnel (CAPES) for scholarships to K. B. and K. N. P. (Financing
Code 001). To Universidade Federal do Acre (UFAC) for logistical
support and financial support. To Gehaka for donating a precision
balance. To the team of the Laboratório de Ecologia Florestal (LabeFlor)
for their help in field collection and material screening.
Author statement
All persons who meet the criteria for authorship are listed as au-
thors, and all authors certify that they have participated sufficiently in
the work to assume public responsibility for the content. In addition,
each author certifies that this material or similar material was not
published in any other publication prior to its submission to Forest
Ecology and Management.
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://
doi.org/10.1016/j.foreco.2020.117906.
References
Alvares, C.A., Stape, J.L., Sentelhas, P.C., De Moraes Gonçalves, J.L., Sparovek, G., 2013.
Köppen’s climate classification map for Brazil. Meteorol. Zeitschrift 22, 711–728.
https://doi.org/10.1127/0941-2948/2013/0507.
Anderson, J.M., Kari, E.E., Brian, H.M., 2006. Multivariate dispersion as a measure of beta
diversity. Ecol. Lett. 9, 683–693. https://doi.org/10.1111/j.1461-0248.2006.
00926.x.
Anderson, M.J., 2001. A new method for non parametric multivariate analysis of var-
iance. Austral Ecol. 26, 32–46. https://doi.org/10.1111/j.1442-9993.2001.01070.
pp.x.
Anjos, L., 2006. Bird species sensitivity in a fagmented landscape of the Atlantic Forest in
southern Brazil. Biotropica 38, 229–234. https://doi.org/10.1111/j.1744-7429.2006.
00122.x.
Areta, J.I., Bodrati, A., Cockle, K., 2009. Specialization on Guadua bamboo seeds by three
bird species in the Atlantic forest of Argentina. Biotropica 41, 66–73. https://doi.org/
10.1111/j.1744-7429.2008.00458.x.
Zhang, H., Xue, J., 2018. Spatial pattern and competitive relationships of moso bamboo in
a native subtropical rainforest community. Forests 9. https://doi.org/10.3390/
f9120774.
Bardales, N.G., Rodrigues, T.E., Oliveira, H., Amaral, E.F., Araújo, E.A., Lani, J.L., Melo,
A.W.F., Amaral, E.F., 2010. Formação, classificação e distribuição geográfica dos
solos no Estado do Acre, in: Recursos Naturais: Geologia, Geomorfologia e Solos Do
Acre. SEMA, Rio Branco, pp. 64–91.
Bello, C., Galetti, M., Montan, D., Pizo, M.A., Mariguela, T.C., Culot, L., Bufalo, F.,
Labecca, F., Pedrosa, F., Constantini, R., Emer, C., Silva, W.R., Silva, F.R.,
Ovaskainen, O., Jordano, P., 2017. Atlantic-frugivory: a plant-frugivore interaction
dataset for the Atlantic forest. Ecology 98. https://doi.org/10.1111/ijlh.12426.
Bystriakova, N., Kapos, V., Lysenko, I., 2004. Bamboo biodiversity, UNEP-WCMC/INBAR.
UNEP-WCMC/INBAR, Cambridge.
Camargo, J.L.C., Ferraz, I.D.K., Mesquita, M.R., Santos, B.A., Brum, H.D., 2008. Guia de
Propágulos e Plântulas da Amazônia. INPA, Manaus.
Carvalho, A.L., Nelson, B.W., Bianchini, M.C., Plagnol, D., Kuplich, T.M., Daly, D.C.,
2013. Bamboo-dominated forests of the southwest Amazon: detection, spatial extent,
K. Bona, et al.
life cycle length and flowering waves. PLoS One 8, e54852. https://doi.org/10.1371/
journal.pone.0054852.
Castro, W., Salimon, C.I., Medeiros, H., 2013. Bamboo abundance, edge effects, and tree
mortality in a forest fragment in Southwestern Amazonia. Sci. For. 41, 159–164.
https://doi.org/10.1590/S1676-06032013000200002.
Catterall, C.P., 2018. Fauna as passengers and drivers in vegetation restoration: a
synthesis of processes and evidence. Ecol. Manag. Restor. 19, 54–62. https://doi.org/
10.1111/emr.12306.
Chen, J., Saunders, S.C., Crow, T.R., Naiman, R.J., Brosofske, K.D., Mroz, G.D.,
Brookshire, B.L., Franklin, J.F., 1999. Microclimate in forest ecosystem and landscape
ecology. Bioscience 49, 288–297. https://doi.org/10.2307/1313612.
Christianini, A.V., Oliveira, P.S., 2010. Birds and ants provide complementary seed dis-
persal in a neotropical savanna. J. Ecol. 573–582. https://doi.org/10.1111/j.1365-
2745.2010.01653.x.
Clarke, K.R., 1993. Non-parametric multivariate analyses of changes in community
structure. Austral Ecol. 18 (1), 117–143. https://doi.org/10.1111/j.1442-9993.1993.
tb00438.x.
Clobert, J., Baguette, M., Benton, T.G., 2012. Dispersal Ecology and Evolution 2012.
Oxford University Press. https://doi.org/10.1093/acprof:oso/9780199608898.001.
0001.
Cornejo, F., Janovec, J., 2010. Seeds of Amazonian Plants. Princeton Field Guides, New
Jersey.
Cornell, H.V., Harrison, S.P., 2014. What are species pools and when are they important?
Annu. Rev. Ecol. Evol. Syst. 45, 45–67. https://doi.org/10.1146/annurev-ecolsys-
120213-091759.
Cousens, R.D., Young, K.R., Tadayyon, A., 2010. The role of the persistent fruit wall in
seed water regulation in Raphanus raphanistrum (Brassicaceae). Ann. Bot. 105,
101–108. https://doi.org/10.1093/aob/mcp268.
Dardick, C., Callahan, A.M., 2014. Evolution of the fruit endocarp: molecular mechanisms
underlying adaptations in seed protection and dispersal strategies. Front. Plant Sci. 5.
https://doi.org/10.3389/fpls.2014.00284.
Fleming, T.H., Kress, W.J., 2011. A brief history of fruits and frugivores. Acta Oecologica
37, 521–530. https://doi.org/10.1016/j.actao.2011.01.016.
Gotelli, N.J., Colwell, R.K., 2001. Quantifying biodiversity: procedures and pitfalls in the
measurement and comparison of species richness. Ecol. Lett. 4, 379–391. https://doi.
org/10.1046/j.1461-0248.2001.00230.x.
Griscom, B.W., Ashton, P.M.S., 2006. A self-perpetuating bamboo disturbance cycle in a
neotropical forest. J. Trop. Ecol. 22, 587–597. https://doi.org/10.1017/
S0266467406003361.
Griscom, B.W., Ashton, P.M.S., 2003. Bamboo control of forest succession: Guadua sar-
cocarpa in Southeastern Peru. For. Ecol. Manage. 175, 445–454. https://doi.org/10.
1016/S0378-1127(02)00214-1.
Griscom, B.W., Daly, D.C., Ashton, P.M.S., 2007. Floristics of bamboo-dominated stands
in lowland terra-firma forests of southwestern Amazonia. J. Torrey Bot. Soc. 134,
108–125. https://doi.org/10.3159/1095-5674(2007)134[108:FOBSIL]2.0.CO;2.
Grombone-Guaratini, M.T., Ribeiro, R.R., 2002. Seed bank and seed rain in a seasonal
semi-deciduous forest in south-eastern Brazil. J. Trop. Ecol. 18, 759–774. https://doi.
org/10.1017/S0266467402002493.
Guaratini, M., Alves, L., Vinha, D., Franco, G.A.D., 2014. Seed rain in areas with and
without bamboo dominance within an urban fragment of the Atlantic Forest. Acta
Bot. Brasilica 28, 76–85. https://doi.org/10.1590/S0102-33062014000100008.
Guilherme, F.A.G., Oliveira-Filho, A.T., Appolinário, V., Bearzoti, E., 2004. Effects of
flooding regime and woody bamboos on tree community dynamics in a section of
tropical semideciduous forest in South-Eastern Brazil. Plant Ecol. 174, 19–36.
https://doi.org/10.1023/B:VEGE.0000046051.97752.cd.
Holl, K.D., 1999. Factors limiting tropical rain forest regeneration in abandoned pasture:
seed rain, seed germination, microclimate, and soil. Biotropica 31, 229–242. https://
doi.org/10.1111/j.1744-7429.1999.tb00135.x.
Honorio-Coronado, E.N.M., Baker, T.R., 2010. Manual para el monitoreo del ciclo del
carbon en bosques amazónicos. Instituto de Investigaciones de la Amazonia Peruana,
Universidad de Leeds, Lima.
Hooper, D.U., Chapin, F., Stuart, I., Hector, A., Inchausti, P., Lavorel, S., Lawton, J.H.,
Lodge, D.M., Loreau, M., Naeem, S., Schmid, B., Setala, H., Symstad, A.J.,
Vandermeer, J., Wardle, D.A., 2005. Effects of biodiversity on ecosystem functioning:
a consensus of current knowledge. Ecol. Monogr. 75, 3–35. https://doi.org/10.1890/
04-0922.
Howe, H.F., Smallwood, J., 1982. Ecology of seed dispersal. Annu. Rev. Ecol. Syst. 13,
201–228. https://doi.org/10.1146/annurev.es.13.110182.001221.
Hsieh, T.C., Ma, K.H., Chao, A., 2016. iNEXT: an R package for rarefaction and extra-
polation of species diversity (Hill numbers). Methods Ecol. Evol. 7, 1451–1456.
https://doi.org/10.1111/2041-210X.12613.
Judziewicz, E.J., Clark, L.G., Londoño, X., Stern, M.J., 1999. American bamboos, Travel &
Tourism Analyst. Smithsonian Institution Press, Washington DC.
Kissling, W.D., Böhning-Gaese, K., Jetz, W., 2009. The global distribution of frugivory in
birds. Glob. Ecol. Biogeogr. 18, 150–162. https://doi.org/10.1111/j.1466-8238.
2008.00431.x.
Lima, R.A.F., Gandolfi, S., 2009. Structure of the herb stratum under different light re-
gimes in the Submontane Atlantic Rain Forest. Brazilian J. Biol. 69, 289–296. https://
doi.org/10.1590/s1519-69842009000200008.
Lima, R.A.F., Rother, C.D., Muler, E.A., Lepsch, F.I., Rodrigues, R.R., 2012. Bamboo
overabundance alters forest structure and dynamics in the Atlantic Forest hotspot.
Biol. Conserv. 147, 32–39. https://doi.org/10.1016/j.biocon.2012.01.015.
Magalhães, V.B., Espírito Santo, N.B., Salles, L.F.P., Soares Jr, H., Oliveira, P.S., 2018.
Secondary seed dispersal by ants in Neotropical cerrado savanna: species-specific
effects on seeds and seedlings of Siparuna guianensis (Siparunaceae). Ecol. Entomol.
665–674. https://doi.org/10.1111/een.12640.
6
Forest Ecology and Management 460 (2020) 117906
Marciente, R., Bobrowiec, P.E.D., Magnusson, W.E., 2015. Ground-vegetation clutter af-
fects Phyllostomid bat assemblage structure in lowland Amazonian forest. PLoS One
1–16. https://doi.org/10.1371/journal.pone.0129560.
Marimon, B.S., Fel, J.M., William, C., Marimon-junior, B.H., Umetsu, R.K., Oliveira-
santos, C., Morandi, P.S., Lima, H.S., Terra, A.R., 2012. Monodominance in a forest of
Brosimum rubescens Taub. (Moraceae): structure and dynamics of natural regenera-
tion. Acta Oecol. 43, 134–139. https://doi.org/10.1016/j.actao.2012.07.001.
Marimon, B.S., Felfili, J.M., 2007. Brosimum rubescens Taub. e em uma floresta mista
adjacente no Vale do Araguaia, MT, Brasil. Acta Botanica Brasilica 20 (2), 423–432.
https://doi.org/10.1590/s0102-33062006000200017.
Medeiros, H., Castro, W., Salimon, C.I., da Silva, I.B., Silveira, M., 2013. Tree mortality,
recruitment and growth in a bamboo dominated forest fragment in southwestern
Amazonia, Brazil. Biota Neotrop. 13, 29–34. https://doi.org/10.1590/S1676-
06032013000200002.
Mews, H.A., Silvério, D.V., Lenza, E., Marimon, B.S., 2013. Influência de agrupamentos de
bambu na dinâmica pós-fogo da vegetação lenhosa de um cerrado típico, Mato
Grosso, Brasil. Rodriguésia 64, 211–221. https://doi.org/10.1590/S2175-
78602013000200002.
Montti, L., Villagra, M., Campanello, P.I., Gatti, M.G., Goldstein, G., 2014. Functional
traits enhance invasiveness of bamboos over co-occurring tree saplings in the semi-
deciduous Atlantic Forest. Acta Oecologica 54, 36–44. https://doi.org/10.1016/j.
actao.2013.03.004.
Nelson, B.W., 1994. Natural forest disturbance and change in the Brazilian Amazon.
Remote Sens. Rev. 10, 105–125. https://doi.org/10.1080/02757259409532239.
Oksanen, J., Blanchet, F.G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., Minchin, P.
R., O’Hara, R.B., Simpson, G.L., Solymos, P., Stevens, M.H.H., Szoecs, E., Wagner, H.,
2019. Vegan: Community Ecology Package. R package version 2.5-5 https://CRAN.R-
project.org/package=vegan.
Oliver, T.H., Heard, M.S., Isaac, N.J.B., et al., 2015a. Biodiversity and resilience of eco-
system functions. Trends Ecol. Evol. 30, 673–684. https://doi.org/10.1016/j.tree.
2015.08.009.
Oliver, T.H., Isaac, N.J.B., August, T.A., et al., 2015b. Declining resilience of ecosystem
functions under biodiversity loss. Nat. Commun. 6, 10122. https://doi.org/10.1038/
ncomms10122.
Powell, P.A., Aráoz, E., 2018. Biological and environmental effects on fine-scale seed
dispersal of an invasive tree in a secondary subtropical forest. Biol. Invasions 20,
461–473. https://doi.org/10.1007/s10530-017-1548-4.
R Core Team (2019). R: A Language and Environment for Statistical Computing. R
Foundation for Statistical Computing, Vienna, Austria. URL: https://www.R-project.
org/.
Rother, D.C., Alves, K.J.F., Pizo, M.A., 2013. Avian assemblages in bamboo and non-
bamboo habitats in a tropical rainforest. Emu - Austral Ornithol. 113, 52–61. https://
doi.org/10.1071/MU12017.
Rother, D.C., Rodrigues, R.R., Pizo, M.A., 2009. Effects of bamboo stands on seed rain and
seed limitation in a rainforest. For. Ecol. Manage. 257, 885–892. https://doi.org/10.
1016/j.foreco.2008.10.022.
Santana, C.R., Dos Anjos, L., 2010. Associação de aves a agrupamentos de bambu na
porção Sul da Mata Atlântica, Londrina, Estado do Paraná. Brasil. Biota Neotrop. 10,
39–44. https://doi.org/10.1590/S1676-06032010000200003.
Silva, R. da C., Silveira, M., 2016. Efeitos da estratificação vertical e obstrução vegeta-
cional sobre a assembleia de morcegos de dois fragmentos florestais do leste do
Estado do Acre, Brasil. Universidade Federal do Acre.
Silveira, M., 2005. A floresta aberta com bambu no sudoeste da Amazônia: padrões e
processos em múltiplas escalas. EDUFAC, Rio Branco.
Silveira, M., 1999. Ecological aspects of bamboo-dominated forest in southwestern
Amazonia: an ethnoscience perspective. Ecotropica 5, 213–216.
Silvério, D.V., Mews, H.A., Lenza, E., Marimon, B.S., 2010. Impactos do agrupamento do
bambu Actinocladum verticillatum (Nees) McClure ex Soderstr. (POACEAE) sobre a
vegetação lenhosa de duas fitofisionomias de Cerrado na transição Cerrado-Floresta
Amazônica. Acta Amaz. 40, 347–356. https://doi.org/10.1590/S0044-
59672010000200013.
Smith, M., Nelson, B.W., 2011. Fire favours expansion of bamboo-dominated forests in
the south-west Amazon. J. Trop. Ecol. 27, 59–64. https://doi.org/10.1017/
S026646741000057X.
Socolar, S.J., Robinson, S.K., Terborgh, J., 2013. Bird diversity and occurrence of bamboo
specialists in two bamboo die-offs in southeastern Peru. Condor 115, 253–262.
https://doi.org/10.1525/cond.2013.120061.
Srivastava, D.S., 1999. Using local-regional richness plots to test for species saturation:
pitfalls and potentials. J. Anim. Ecol. 68, 1–16. https://doi.org/10.1046/j.1365-
2656.1999.00266.x.
Steege, H., et al., 2013. Hyperdominance in the Amazonian Tree Flora. Science (80-.) 342,
1243092. https://doi.org/10.1126/science.1243092.
Suzaki, T., Nakatsubo, T., 2001. Impact of the bamboo Phyllostachys bambusoides on the
light environment and plant communities on riverbanks. J. For. Res. 6, 81–86.
https://doi.org/10.1007/bf02762492.
Taylor, A.H., Zisheng, O., 1988. Tree replacement patterns in subalpine Abies-Betula
forests, Wolong Natural Reserve, China. Vegetatio 78, 141–149. https://doi.org/10.
1007/BF00033423.
Taylor, S.H., Hulme, S.P., Rees, M., Ripley, B.S., Ian Woodward, F., Osborne, C.P., 2010.
Ecophysiological traits in C3 and C4 grasses: a phylogenetically controlled screening
experiment. New Phytol. 185, 780–791. https://doi.org/10.1111/j.1469-8137.2009.
03102.x.
Torezan, J.M.D., Silveira, M., 2000. The biomass of bamboo (Guadua weberbaueri Pilger)
in open forest of the southwestern Amazon. Ecotropica.
Van der Pijl, L., 1982. Principles of Dispersal in Higher Plants. Springer, Heidelberg.
Viswanathan, A., Naniwadekar, R., Datta, A., 2014. Seed dispersal by avian frugivores:
K. Bona, et al.
non-random heterogeneity at fine scales. Biotropica 1–8. https://doi.org/10.1111/
btp.12179.
Wunderle, J.M., 1997. The role of animal seed dispersal in accelerating native forest
regeneration on degraded tropical lands. For. Ecol. Manage. 99, 223–235. https://
doi.org/10.1016/S0378-1127(97)00208-9.
Xu, Q.-F., Liang, C.-F., Chen, J.-H., Li, Y.-C., Qin, H., Fuhrmann, J.J., 2019. Rapid bamboo
invasion (expansion) and its effects on biodiversity and soil processes +. Glob. Ecol.
Forest Ecology and Management 460 (2020) 117906
Conserv. 21, e00787. https://doi.org/10.1016/j.gecco.2019.e00787.
Yang, Q.-P., Yang, G.-Y., Song, Q.-N., Shi, J.-M., Ouyang, M., Qi, H.-Y., Fang, X.-M., 2015.
Ecological studies on bamboo expansion: process, consequence and mechanism
Chinese. J Plant Ecol. 39, 110–124. https://doi.org/10.17521/cjpe.2015.0012.
Zaninovich, S.C., Montti, L.F., Alvarez, M.F., Gatti, M.G., 2017. Replacing trees by
bamboos: changes from canopy to soil organic carbon storage. For. Ecol. Manage.
400, 208–217. https://doi.org/10.1016/j.foreco.2017.05.047.