Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e51290, enero-diciembre 2023 (Publicado Ago. 28, 2023)

Spatio-temporal variation of seed rain between urban

and rural fragments of humid tropical forests

Priscila Silva dos Santos1; https://orcid.org/0000-0001-8902-9691

Kleber Andrade da Silva2*; http://orcid.org/0000-0002-7011-8800

Elcida de Lima Araújo1; https://orcid.org/0000-0002-3379-3540

Danielle Melo dos Santos1; https://orcid.org/0000-0003-0839-967X

Josiene Maria Falcão Fraga dos Santos3; https://orcid.org/0000-0002-9780-2784

Gicélia Lira dos Prazeres4; https://orcid.org/0000-0003-1192-6530

Elba Maria Nogueira Ferraz4; https://orcid.org/0000-0003-4998-9772

1. Universidade Federal Rural de Pernambuco, Departamento de Biologia, Programa de Pós-Graduação em Botânica,

Brasil; biopri13@hotmail.com, elcida.araujo@ufpe.br, danmelo_bio@hotmail.com

2. Universidade Federal de Pernambuco, Centro Acadêmico de Vitória, Brasil; kleber.andrade@ufpe.br (*Correspondence)

3. Universidade Estadual de Alagoas, Departamento de Biologia, Brasil; josiene.falcao@uneal.edu.br

4. Instituto Federal de Pernambuco, Departamento de Meio Ambiente, Saúde e Segurança, Brasil; gicelialp13@hotmail.

com, elbanogueira08@gmail.com

Received 15-VI-2022. Corrected 28-VI-2023. Accepted 18-VIII-2023.

ABSTRACT

Introduction: The type of land use surrounding the remnants of tropical forest may generate changes in the

characteristics of plant populations and communities. Consequently, there may be a significant reduction in

processes of pollination and diasporas dispersion. Therefore, causing changes in some parameters of seed rain.

Objective: To characterize and compare seed density, species richness, floristic composition, habit, dispersal

syndrome, and successional category of seed rain between urban and rural fragments of Atlantic Forest, in the

2015 and 2016 weather seasons.

Methods: The study areas were defined after mapping and quantification of urban and rural occupations around

the remnants, based on satellite images. In each fragment, were installed 36 collectors of 0.25 m2. The material

was collected monthly during two consecutive years.

Results: Seed rain richness was higher in the urban fragment during the rainy season in the two years, whereas it

was similar between the fragments in the dry season. The seed density in the rural fragment was higher than in

the urban during the rainy season; did not vary in urban between years or between seasons; and it was higher in

the rural fragment in the rainy season of one year. There was a difference in the floristic composition of the seed

rain between the fragments along time. The variations in the functional attributes of habit, dispersal syndrome,

and successional category, were explained by the variables fragment, season, and year.

Conclusions: Differences in the characteristics of the seed rain between the fragments might reflect the spatial

and temporal heterogeneity, due to the diverse uses of the soil and external pressures (anthropogenic actions)

present in the surroundings of the forest fragments and temporal variation in precipitation.

Key words: Atlantic Forest; seed dispersal: surrounding landscape; seasonal and annual variation.

https://doi.org/10.15517/rev.biol.trop..v71i1.51290

TERRESTRIAL ECOLOGY

2Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e51290, enero-diciembre 2023 (Publicado Ago. 28, 2023)

INTRODUCTION

Different uses of the land have caused

changes in the landscapes, promoting strong

environmental impacts on the biota (Benítez-

Malvido et al., 2022). In this context, the process

of urbanization and rise of agricultural fron-

tiers are responsible for the fragmentation of

habitats and promote changes in the dynamics

and structure of forests along the urban-rural

gradient (Overdyck & Clarkson, 2012; Pivello

et al., 2006; Santos et al., 2020). For example,

the fragmentation will lead to reduced species

richness and changes in floristic composition

of aboveground vegetation. These changes pro-

mote a significant reduction in the ecosystem

services of habitat and resource to wildlife, and

microclimate for the establishment and growth

of plants. Consequently, there may be a signifi-

cant reduction in the pollination and disper-

sion of diasporas processes (Benítez-Malvido

et al., 2022; Overdyck & Clarkson, 2012) and,

therefore, causing changes in some parameters

of seed rain, such as density, richness, species

composition, habit, and successional category

of plants (Overdyck & Clarkson, 2012; Piv-

ello et al., 2006). Thus, the disturbance degree

reaching an environment may influence seed

rain, and hence the process of natural regenera-

tion (Benítez-Malvido et al., 2022; César et al.,

2017; Pivello et al., 2006).

Seed rain represents one of the most

important mechanisms in the forest’s regen-

eration process, enabling the entry of seeds and

consequently establishment and recruitment of

new individuals and species in the forest frag-

ments (Jara-Guerrero et al., 2020; Werden et

al., 2021; Yang et al., 2020). The compilation of

works carried out in tropical rain forests shows

that the urban fragments are surrounded by

residences, industries, roads, and highways,

while rural fragments are surrounded by sug-

arcane and Eucalyptus spp. monocultures, pas-

tures, and greenery; these differences in the

surrounding matrix of fragments cause changes

in the attributes of seed rain (Freitas et al., 2013;

RESUMEN

Variación espacio-temporal de la lluvia de semillas entre fragmentos urbanos

y rurales de bosques tropicales húmedos

Introducción: El tipo de uso del suelo que rodea los remanentes de bosque tropical puede generar cambios en las

características de las poblaciones y comunidades vegetales. En consecuencia, puede haber una reducción signifi-

cativa en los procesos de polinización y dispersión de las diásporas. Por lo tanto, provocando cambios en algunos

parámetros de la lluvia de semillas.

Objetivo: Caracterizar y comparar la densidad de semillas, la riqueza de especies, la composición florística, el

hábito, el síndrome de dispersión y la categoría sucesional de la lluvia de semillas entre fragmentos urbanos y

rurales de Mata Atlántica, en las estaciones climáticas del 2015 y 2016.

Métodos: Las áreas de estudio se definieron luego del mapeo y cuantificación de las ocupaciones urbanas y rurales

alrededor de los remanentes, con base en imágenes satelitales. En cada fragmento se instalaron 36 colectores de

0.25 m2. El material fue recolectado mensualmente durante dos años consecutivos.

Resultados: La riqueza de lluvia de semillas fue mayor en el fragmento urbano durante la estación lluviosa en

los dos años, mientras que fue similar entre los fragmentos en la estación seca. La densidad de semillas en el

fragmento rural fue mayor que en el urbano durante la estación lluviosa; no varió en urbano entre años o entre

estaciones; y fue mayor en el fragmento rural en la estación lluviosa del primer año. Hubo una diferencia en la

composición florística de la lluvia de semillas entre los fragmentos a lo largo del tiempo. Las variaciones en los

atributos funcionales de hábito, síndrome de dispersión y categoría sucesional, fueron explicadas por las variables

fragmento, estación y año.

Conclusiones: Las diferencias en las características de la lluvia de semillas entre los fragmentos podrían reflejar la

heterogeneidad espacial y temporal, debido a los diversos usos del suelo y presiones externas (acciones antropogé-

nicas) presentes en el entorno de los fragmentos de bosque y variación temporal de la precipitación.

Palabras clave: Bosque Atlántico; dispersión de semillas; paisaje circundante; variación estacional y anual.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e51290, enero-diciembre 2023 (Publicado Ago. 28, 2023)

Overdyck & Clarkson, 2012). For example, spe-

cies richness and seed density from the seed

rain are higher in rural fragments than in urban

fragments (Campos et al., 2009; Cole et al.,

2010; Cutway & Ehrenfeld, 2010; Freitas et al.,

2013; Knorr & Gottsberg, 2012); species rich-

ness and seed density of the seed rain may be

higher during the dry season or dry-rainy tran-

sition in urban and rural fragments (Gratzer et

al., 2022; Jara-Guerrero et al., 2020); seed rain

composition differs between urban and rural

fragments (Overdyck & Clarkson, 2012).

The predominant factors and practices in

each type of surrounding matrix (i.e., sugarcane

monoculture and urban centers) may affect

the dynamics of the forests and interfere in the

seed characteristics of each fragment. Then, it

is expected that surrounding type of the rural

fragment plays an important role in the species

richness of the seed rain and affecting the flo-

ristic composition. The surrounding matrix of

rural fragment is more uniform. Consequently,

there is a greater flow of species in fragments

with an agricultural surrounding when com-

pared to the fragments with urban surrounding

(Knapp et al., 2008; Lososová et al., 2006). We

also need to consider the existence of other

adjacent fragments to the rural studied, as

they may influence the seed entry in the area,

depending on species dispersal syndrome. In

this way, we could not discard the possibility

of seed arrival from other fragments near the

rural, mainly because the composition of the

seed rain from a certain area is closely related

to its surroundings, i.e., with the immediate

neighborhood and with the landscape in which

it is inserted (Gratzer et al., 2022; Werden et al.,

2021). Therefore, it is expected that the type of

surroundings leads to changes in species rich-

ness, seed density, floristic composition, and

functional attributes of seed rain.

It was also observed that in the rural or

urban fragments there is a predominance of

trees species, zoocoric dispersal syndrome, and

pioneer species (Cole et al., 2010; Freitas et

al., 2013; Marangon et al., 2010; Oliveira et al.,

2011). However, the proportion of the habit,

dispersal syndrome, and successional category

of seed rain varies according to the fragments

type (rural or urban) and seasons.

Few studies have incorporated both the

spatial context and temporal variability in the

analysis of seed rain abundance, composition,

and taxonomic and functional diversity. There-

fore, our study aims to characterize and com-

pare species richness, seed density, floristic

composition, habit, dispersal syndrome, and

successional category of seed rain in urban and

rural fragments of Atlantic Forest, between cli-

matic seasons and years. Considering that char-

acteristics of seed rain in fragments of tropical

rain forests may vary depending on the type of

environment, climatic seasons, and years, we

assume the hypotheses: 1) The species richness

and seed density will be highest in the rural

fragment during the rainy and dry seasons and

during the years; 2) the floristic composition of

seed rain differs between fragments, and this

difference continue along years and seasons;

3) the variations in the functional attributes of

dispersal syndrome (Van Der Pijl, 1982), habit,

and successional category (Gandolfi et al.,

1995) are explained by the surrounding matrix

of rural and urban fragments, and seasonal and

annual variation in precipitation.

MATERIALS AND METHODS

Study area: The study was carried out in

two remnants of Atlantic rainforest in North-

eastern Brazil, which have been protected as

integral protection Conservation Units (C.U.)

since 1987. They are part of a complex of

protected areas, inserted in the Metropolitan

Recife Region (CPRH, 2003) (Fig. 1). The C.U.s

boundaries were mapped on a mosaic of ortho-

photo maps at a scale of 1: 20 000, dated from

the 1980s.

The urbanization degree on the surround-

ings of forest remnants was defined by mapping

and quantification of urban and rural occupa-

tions in the area that extends from the forest

boundary up to 3 km (buffer), according to the

methodology presented by Guerra (2016). The

mapping was based on the Atlas of the Atlan-

tic Forest Remnants, in partnership with the

4Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e51290, enero-diciembre 2023 (Publicado Ago. 28, 2023)

National Institute of Space Research (INPE).

For the Atlas work, were used OLI images of

the Landsat 8 satellite and the Google Earth

program, from the period of 2009 to 2015 and

updated mainly in the second half of 2016.

These images are of high spatial resolution and

scale approximately of 1:50 000. In the rural

and urban fragments, field conferences were

also held to verify the presence of consistent

changes in the use of the surrounding soil

within the mapped area.

Urban fragment was considered that with

residential, commercial, or industrial agglom-

erates, roads, highways, and areas without veg-

etation, with exposed soils in the vicinity of

these agglomerates; the rural fragment is that

predominates agro-pastoral activities, small vil-

lages and roads, highways, and areas without

vegetation distant from urban centers (Guerra,

2016). The urban fragment (08°01’15.1” S &

34°56’3.2” W) is characterized by a single veg-

etation stretch in different stages of secondary

succession; and has land use in its surroundings

sites, farms, villages, roads, and highways. (San-

tos et al., 2020). The rural fragment (08º10’00”

& 08º15’00” S, 35º02’30” & 35º05’00” W) in its

surroundings have predominantly sugarcane

production, and some areas of subsistence agri-

culture, fruit growing, livestock, and timber

extraction (Lyra-Neves et al., 2004; Santos et al.,

2020). Mapping of the buffer area of urban frag-

ment recorded a total area of 5 540 ha, whose

30 % corresponds to the native forest area, 33

% the urban area, and 37 % were not defined

by the mapping/sensor. Mapping of the buffer

area of rural fragment recorded a total area of

10 349 ha, whose 41 % corresponds to native

forest area, and 59 % to areas of agricultural

use (Fig. 1).

A total of 66 species are presents in the

urban fragment and 52 in the rural. The family

with the greatest species richness in the urban

and rural fragments is Euphorbiaceae. Twen-

ty-six species are present only in the urban

Fig. 1. Location of the urban and rural fragments of Atlantic rainforest evaluated in the metropolitan region of Recife.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e51290, enero-diciembre 2023 (Publicado Ago. 28, 2023)

fragment; and 12 in the rural fragment; and 40

are commons in both fragments. The floristic

similarity by Sorensen index is 68 % (Santos et

al., 2020).

The fragments were chosen because they

have common characteristics: the same As’ cli-

mate type (hot and humid) (Kottek et al., 2006),

the same soil type (latosols) (Embrapa, 1998;

Jacomine et al., 1972), the same vegetal forma-

tion (Lowland Ombrophylous Forest) (IBGE,

2012), and average annual rainfall with little

variation (2 450 - 2 460 mm). Rainfall totals in

rural and urban fragments were, respectively, 1

666.11 and 1 973.8 mm in 2015, and 1 445.50

and 1 602.00 mm in 2016.

Seed rain sampling: For the sampling of

seed rain in each fragment (urban and rural),

36 collectors were installed from 5 m of the

border, totaling 72. The collectors were distrib-

uted in three transects of 300 m, approximately

interspaced 100 m away. In each transect, 12

equidistant collectors were installed at 25 m.

Our collectors covered a total area of 6 ha

(border-center direction). The collectors are

0.25 m2 area (0.5 m × 0.5 m), and they were

installed 30 cm above the ground. This method

is appropriate to include herbaceous plants

(Benítez-Malvido et al., 2022; Knorr & Gotts-

berger, 2012). These were made in a square

shape, with 1 mm nylon mesh, and a depth of ≈

20 cm, whose function is to retain all the depos-

ited material (César et al., 2017), and they were

fixed in tree trunks with nylon threads and

identified with a numbered plaque. The mate-

rial was collected monthly (Freitas et al., 2013)

during two consecutive years (February 2015

to January 2017). Each collected sample was

packed in polyethylene bags, labeled according

to the collector numbering, and placed to dry

in stove with a controlled temperature of 65 °C.

At the laboratory, the seeds were manu-

ally separated from other materials eventually

found, quantified, and classified with the aid

of a stereomicroscope. The fruits present in the

samples were opened for the seed’s removal.

Seeds were separated, classified by morpho-

type, and numbered, until their taxonomic

identification according to Angiosperm Phy-

logeny Group System (The Angiosperm Phy-

logeny Group et al., 2016). The spelling of

species names was verified at the Index Kew-

ensis (www. ipni.org/ipni/plantnamesearch-

page.do) and the Missouri Botanical Garden’s

(MOBOT) database (www.mobot.mobot.org/

W3T /Search/vast.html). Abbreviation of the

author names of the species was made by con-

sultation with Brummit and Powell (1992) and

MOBOT. The number of seeds was expressed

as seed/0.25 m2. For seed identification, we

used the specific bibliography (Barroso et al.,

1999; Lorenzi, 1992; Lorenzi, 1998a; Lorenzi,

1998b; Lorenzi, 2009), besides taxonomy spe-

cialist help. In addition, a survey of the indi-

viduals close to the collectors was carried out,

mainly of the individuals with the reproductive

material in the collection period.

Collected seeds were classified according

to the Van Der Pijl (1982) proposal in anemo-

choric, zoochoric, and autochoric. The species

were classified as tree, shrub, woody climbing

plant (lianas), and herbaceous and in relation

to the successional category in pioneers, early

secondary, and late secondary (Gandolfi et

al., 1995). The syndrome and the successional

category corresponding to each species was

evaluated by consultations in the local literature

(Marangon et al., 2010; Oliveira et al., 2011;

Silva & Rodal, 2009).

Data analysis: Differences in the species

richness of seed rain between the rural and

urban fragments over time were verified by

the rarefaction analysis using Estimate S 9.1.0

(Colwell, 2013). The sample-based rarefaction

curve shows the mean species number (± stan-

dard deviation). Plotted values are means of 100

randomizations. There is significant difference

when deviations do not touch (Colwell, 2013;

Gotelli & Colwell, 2001).

The Generalized Linear Model (GLM) was

used to verify the effect of predictor variables

(urban and rural fragment, seasonal and annual

variation) on seed density. The differences in

mean seed density between urban and rural

fragments, during dry and rainy seasons, and

6Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e51290, enero-diciembre 2023 (Publicado Ago. 28, 2023)

during 2015 and 2016 years were verified by

the Tukey a posteriori test. These analyzes

were carried out by the Statistic software 7.0

(StatSoft Inc., 2003).

The floristic composition of the seed rain

between the rural and urban fragments, and in

each fragment between seasons and between

years was compared through the Non-Metric

Multidimensional Scaling (NMDS) Analysis,

using the Bray-Curtis dissimilarity matrix,

based on the species density present in the 72

collectors from the study areas. ANOSIM was

used to verify the significance of the formed

cluster in the NMDS. To verify the contribution

of the density of each species between rural and

urban fragments and in each fragment between

years we performed the SIMPER analysis

(Similarity percentage). NMDS, ANOSIM, and

SIMPER analyzes were performed at the Primer

version 7 software (Clarke & Gorley, 2015).

Differences in species abundance among

the fragments, years, and seasons within the

functional attributes habit, dispersal syndrome,

and successional category were verified by

Log-Linear model (Sokal & Rohlf, 1995). Only

models with significant interactions were con-

sidered. The model significance was verified

by the Chi-Square test. Analyzes were per-

formed in the Systat Software 10.0 (Systat

Software Inc, 2006).

RESULTS

Species richness: During the two years of

study, a total of 99 species were found in the

seed rain, being 80 species in the urban frag-

ment and 61 in the rural (SMT1). From the

total number of species, eight were identified at

the family level, four at genus, 69 at the specific

level, and 17 morphospecies. Additionally, 39

species occurred exclusively in the urban frag-

ment and 19 in the rural fragment (SMT1).

The families with the greatest species rich-

ness in the urban fragment during the two years

study were Euphorbiaceae (with four species),

Annonaceae, Chrysobalanaceae, Erythroxyla-

ceae, Lauraceae, Malpighiaceae, Melastomata-

ceae, Moraceae, Rubiaceae, and Sapindaceae

(with three species each); and in the rural frag-

ment were Fabaceae (with eight species), Ana-

cardiaceae, Annonaceae, Erythroxylaceae,

Euphorbiaceae, Melastomataceae, Moraceae,

and Sapindaceae (with three species each).

The total species richness of seed rain from

the urban fragment was significantly higher

than the rural (Fig. 2A). The richness was

significantly higher in the urban fragment in

2015 (Fig. 2B) and 2016 (Fig. 2C). Considering

each season separately, during the rainy season

the species richness was significantly higher

in the urban fragment (Fig. 2D), while in the

dry season it was similar among the fragments

(Fig. 2E).

Seeds density: The GLM analysis showed

that there was a significant effect of fragment,

climatic season, and their interaction on seed

density of seed rain (Table 1). The Tukey test

showed that the mean seed density (± 95 % CI)

of rural fragment was higher than the mean

seed density (± 95 % CI) of urban fragment in

2016 (F(1, 1720) = 0.59602; P = 0.046437; Fig. 3A)

and during the rainy season (F(1, 1720) = 11.144;

P = 0.000067; Fig. 3B). There was no significant

difference in mean seed density (± 95 % CI)

between the rural and urban fragments in 2015

(F(1, 1720) = 0.59602; P = 0.434458; Fig. 3A) and

during the dry season (F(1, 1720) = 11.144; P =

0.989715; Fig. 3B).

Species composition: The ANOSIM ana-

lyze showed that the seed rain composition

of the rural fragment was different from the

urban fragment (Rglobal = 0.317; P = 0.001).

The formed cluster in the NMDS can be seen

in Fig. 4A. The floristic composition among

the fragments was different in 2015 (Rglobal =

0.226; P = 0.001; Fig. 4B) and 2016 (Rglobal =

0.254; P = 0.001; Fig. 4C). The floristic compo-

sition between the fragments was different in

the rainy season (Rglobal = 0.225; P = 0.001; Fig.

4D) and in the dry season (Rglobal = 0.295; P =

0.001; Fig. 4E).

SIMPER analysis showed high dissimilar-

ity in the seed rain between the rural and urban

fragments (80.11 %), and this behavior remained

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e51290, enero-diciembre 2023 (Publicado Ago. 28, 2023)

Fig. 2. A. Sample-based rarefaction curve with the mean species number (± standard deviation) from the seed rain in rural

and urban fragments; B. in 2015; C. in 2016; D. in rainy and E. dry season; of Atlantic Forest in Northeast Brazil. There is

significant difference when deviations do not touch (Colwell, 2013; Gotelli & Colwell, 2001).

Table 1

General Linear Model (GLM) analysis showing the influence of the rural and urban fragments, climatic season, years, and

their interactions on the seed density of seed rain in an Atlantic Forest in Northeast Brazil

DF SS MS F P

Intercept 12 723.697 2 723.697 1 246.575 0.000000

Year 1 3.044 3.044 1.393 0.238052

Fragment 1 18.380 18.380 8.412 0.003775

Season 1 8.859 8.859 4.055 0.044202

Year*Fragment 1 1.302 1.302 0.596 0.440208

Year*Season 1 3.179 3.179 1.455 0.227893

Fragment*Season 1 24.349 24.349 11.144 0.000861

Year*Fragment*Season 1 0.321 0.321 0.147 0.701640

Error 1720 3 758.105 2.185

Total 1727 3 817.539

P value < 0.05 denote significant difference (DF = degrees of freedom, SS = sun of square, MS = mean square, F = Fisher

test, P = significance).

8Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e51290, enero-diciembre 2023 (Publicado Ago. 28, 2023)

over the years in each fragment (Table 2). The

five species that most contributed to the dif-

ferences between the fragments were Miconia

amacurensis Wurdack, Miconia prasina (Sw.)

DC., Maprounea guianensis Aubl., Schefflera

morototoni (Aubl.) Manguire, Steyerm. &

Frodi, and Cecropia pachystachya Trécul., with

a cumulative percentage of 31.4 %. In rural

areas, the species that contributed most to

the differences were Miconia prasina, Maprou-

nea guianensis, Schefflera morototoni, Cecropia

pachystachya, Helicostilis tomentosa (Poepp. &

Endl.) Rusby, and Miconia minutiflora (Blonpl.)

DC., with an accumulated percentage of 38.83

%. In the urban area, the species that contrib-

uted most to the dissimilarities were Miconia

amacurensis, Schefflera morototoni, Asteraceae

sp1, Cecropia pachystachya, and Parkia pendula

(Willd.) Benth. ex. Walper., with an accumu-

lated value of 31.81 %.

Functional attributes: The log-lin-

ear analysis for the abundance of seed rain

of the studied species showed a significant

Fig. 3. A. Mean seed density variation in urban and rural fragments of Atlantic Forest in Pernambuco, during 2015 and 2016

years and B. during dry and rainy seasons. Different lowercase letters denote significant difference between the urban and

rural fragments by the Tukey HSD test at 5 %. Vertical bars denote 95 % of the confidence interval.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e51290, enero-diciembre 2023 (Publicado Ago. 28, 2023)

second-order interaction among the variables

fragment, season, and habit (c2 = 9.20; df = 3;

P = 0.0268). This means that seed abundance is

not explained in isolation by any of these vari-

ables. Then, they should be evaluated together.

Although in the general set, the total density of

tree seeds was higher than the seed density of

the other habits, it was observed that the pro-

portion of seeds of trees, shrubs, herbaceous,

and woody climbing plant (lianas) changes

according to the seasons and the fragments.

For example, the seed number of woody climb-

ing plant species was higher in the dry season

than in the rainy season. However, in the urban

fragment, the variation between dry and rainy

season was higher (4.53 times more seeds in the

dry season) than the rural fragment (1.73 times

more seeds in the dry season) (Fig. 5).

There were two first-order interactions,

between the fragments and dispersal syndromes

(c2 = 26.11, df = 2; P < 0.0001) and between sea-

sons and dispersal syndromes (c2 = 28.02, df =

Fig. 4. A. Non-Metric Multidimensional Scaling (NMDS) analysis of seed rain species between rural and urban fragments of

the Atlantic Forest in Pernambuco, Brazil; and B. in the 2015 and C. 2016 years; and D. in the rainy and E. dry season, based

on species richness. Graph symbols represent the species present in seed rain of each fragment.

10 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e51290, enero-diciembre 2023 (Publicado Ago. 28, 2023)

2; P < 0.0001). It was also observed a second-

order interaction between fragments, years, and

seasons (c2 = 4.14, df = 1; P = 0.0418). These

results also can be evaluated together. Although

the total density of zoochoric seeds was higher

than the seed density of the other syndromes, it

was observed that the proportion of zoochoric,

anemochoric, and autochoric seeds changes

according to the fragment, season, and year.

For example, the seed number of anemochoric

species was higher in the dry season in the rural

fragment in 2016; and in the dry season of the

urban fragment in 2015 and 2016 (Fig. 6).

Finally, there was a first-order interaction

between the year and successional category

variables (c2 = 14.89, df = 2, P = 0.0006) and

Table 2

SIMPER analysis between rural (R) and urban (U) fragments between years (2015 and 2016) and in each fragment, including

the species contribution in the dissimilarity between the sampled fragments

R and U R between years U between years

D.L. = 80.11 D.L.= 77.55 D.L. = 79.43

Species D.L. Species D.L. Species D.L.

Miconia amacurensis 7.68 M. prasina 9.38 M. amacurensis 9.89

Miconia prasina 6.89 M. guianensis 8.92 S. morototoni 5.87

Maprounea guianensis 5.71 S. morototoni 8.38 Asteraceae sp1 5.85

Schefflera morototoni 5.57 C. pachystachya 7.69 C. pachystachya 5.13

Cecropia pachystachya 5.55 H. tomentosa 4.46 P. p e ndu l a 5.07

Asteraceae sp1 4.22 M. minutiflora 3.92 G. blanchetiana 4.37

Parkia pendula 4.11 P. p e ndu l a 3.81 S. salzmanniana 4.13

Gouania blanchetiana 3.57 G. blanchetiana 3.60 T. guianensis 3.72

Helicostilis tomentosa 3.24 Asteraceae sp1 3.54 M. prasina 3.63

Miconia minutiflora 2.84 A. dolichocarpa 2.66 H. tomentosa 3.07

Serjania salzmanniana 2.83 M. amacurensis 2.48 A. dolichocarpa 3.07

Anaxagorea dolichocarpa 2.83 B. adenopoda 1.91 L. kunthiana 2.41

Tapirira guianensis 2.60 O. glomerata 1.54 O. glomerata 1.95

Ocotea glomerata 1.61 P. heptaphyllum 1.53 P. schomburgkiana 1.76

Licania kunthiana 1.36 T. guianensis 1.03 P. heptaphyllum 1.34

Protium heptaphyllum 1.23 T. spruceanum 0.85 Morfo 29 1.21

Banisteriopsis adenopoda 1.21 Passiflora sp1 0.85 Passiflora sp1 0.98

Pogonophoschomburgkiana 1.21 D. guianensis 0.74 T. brevistaminea 0.95

Passiflora sp1 1.06 X. frutescens 0.67 E. citrifolium 0.86

Tovomita brevistaminea 0.80 M. aegyptia 0.66 B. adenopoda 0.81

Morfo 29 0.76 P. schomburgkiana 0.66 C. mollis 0.76

Erythroxylum citrifolium 0.67 S. salzmanniana 0.64 S. rugosum 0.64

Thyrsodium spruceanum 0.52 E. ovata 0.49 S. densiflorum 0.57

Xylopia frutescens 0.50 S. hilarii 0.57

Serjania hebecarpa 0.49 S. hebicarpa 0.75

Merremia aegytia 0.49 B. lucida 0.55

Coccoloba mollis 0.45 P. violaceus 0.48

Eschweilera ovata 0.41 G. americana 0.43

Simarouba amara 0.39 B. virgiloides 0.41

Sloanea guianensis 0.34 M. salzmannii 0.41

Pterocarpus violaceus 0.32 E. ovata 0.39

Soroceae hilarii 0.31

(D.L = Dissimilarity Level).

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e51290, enero-diciembre 2023 (Publicado Ago. 28, 2023)

a second-order interaction between fragment,

season, and successional category (c2 =11.45,

df = 2, P = 0.0033). Additionally, evaluating all

the variables together, it was observed that the

proportion of early, secondary, and late sec-

ondary species changes according to the year,

fragment, and season. For example, the seed

number of secondary species was higher in

2015 than in 2016, however, the variation was

higher in the rural fragment in 2016 (1.52 times

more seeds in 2016) than in the urban one (1.06

times more seeds in 2016) (Fig. 7).

Fig. 6. Differences in seed abundance within the category of dispersal syndrome (zoochoric, anemochoric, and autochoric)

between Atlantic Forest fragments (rural and urban), years (2015 and 2016), and seasons (rain and dry).

Fig. 5. Differences in seed abundance within the habit category (tree, shrub, herbaceous, and woody climbers) between

Atlantic Forest fragments (rural and urban), and seasons (rain and dry).

12 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e51290, enero-diciembre 2023 (Publicado Ago. 28, 2023)

DISCUSSION

Species richness, seed density and species

composition: Our findings show that the urban

fragment species richness was higher during

the two years and this superiority is maintained

due to the high number of species present dur-

ing the rainy season. During the dry season,

the urban fragment species richness reduces

and equals the rural fragment species richness.

Thus, the hypothesis of greater species richness

in the rural fragment was not accepted. This

behavior is opposite to that registered in the

literature, where is a trend of greater species

richness in rural fragments over time (Campos

et al., 2009; Cutway & Ehrenfeld, 2010; Freitas

et al., 2013; Knorr & Gottsberg, 2012; Overdyck

& Clarkson, 2012).

The greater species richness in urban frag-

ment can be explained by the peaks in the

phenological patterns of flowering occur con-

centrated both in the rainy season (Morellato

et al., 2013; Talora & Morellato, 2000), as in

the dry-rainy transient period (Medeiros et al.,

2007; Morellato et al., 2013); and fructification

peaks, although not seasonally patterned, tend

to occur more commonly in the rainy season

(Medeiros et al., 2007; Morellato et al., 2013;

Talora & Morellato, 2000). New studies are

needed to test this hypothesis.

Our hypothesis of greater seed density in

rural fragment was accepted. However, we veri-

fied that this superiority in not maintained over

time. The high seed density in the rural frag-

ment was a consequence of the high number

of dispersed diaspores during the rainy season

(Fig. 3). Therefore, the dry season contributed

little to the differences in seed density between

the fragments studied. The high seed density

in the rural fragment can be a reflect of the

increase in the number of vertebrates acting as

dispersing agents due to the greater food avail-

ability, and the species phenology that makes

up this area (Medeiros et al., 2007; Morellato

et al., 2013; Oliveira et al., 2011). According

to DeWalt et al. (2003), the abundance of

plants with fleshy fruits acts as a quality indi-

cator of habitat.

The compilation of the studies carried out

in tropical rainforests, that were developed

only in rural fragments or only in urban ones,

showed a great variation in the seed density, so

Fig. 7. Differences in seed abundance within the successional category (pioneer, early secondary, and late secondary -

Gandolfi et al., 1995) between Atlantic Forest fragments (rural and urban), years (2015 and 2016), and seasons (rain and

drought).

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e51290, enero-diciembre 2023 (Publicado Ago. 28, 2023)

that in rural fragment (Cole et al., 2010; Freitas

et al., 2013; Knorr & Gottsberg, 2012; Overdyck

& Clarkson, 2012) the seed density was higher

than recorded for urban forests (Campos et

al., 2009; Cutway & Ehrenfeld, 2010; Overdyck

& Clarkson, 2012; Pivello et al., 2006). When

the seed density of rural and urban fragments

inserted in the same landscape is compared, as

in the case of this study, it is verified that the

seed number remains superior in the rural frag-

ment. Thus, we infer that the dynamics of soil

use in the rural fragment studied, such as the

use of fire, fertilizers, and pesticides, that occur

in some months of the dry season, probably did

not interfere in the action of pollinators and

dispersants in the rainy season, which may have

contributed to an increase in seed density of

this fragment during the rainy season.

The floristic composition of the seed rain

differed between the rural and urban fragments

for two years, confirming the hypothesis of this

study. In fact, the literature shows that sur-

rounding matrix of rural and urban fragments

may limit the dispersion of seeds and con-

sequently, reduce the entry of allochthonous

seeds. Over time, there is a growing trend in

the number of unique species in each fragment,

significantly increasing the dissimilarity (Cut-

way & Ehrenfeld, 2010; Overdyck & Clarkson,

2012; Pivello et al., 2006). In this sense, our

results indicate that the differences in floristic

composition between the fragments may have

been in response to the process of urbaniza-

tion and rise of agricultural frontiers. These

processes promote a significant reduction in

the ecosystem services of habitat and resource

to wildlife, and microclimate for the establish-

ment and growth of plants. Consequently, there

may be a significant reduction in the pollina-

tion and dispersion of diasporas processes and,

therefore, causing changes in floristic composi-

tion (Benítez-Malvido et al., 2022; Overdyck &

Clarkson, 2012).

Functional Attributes: The variation in

the functional attributes of habit, dispersal

syndrome, and successional category were

explained by the variable surrounding matrix

of rural and urban fragments, confirming our

hypothesis. In general, the rural and urban frag-

ments presented a high density of tree seeds,

zoochoric, and pioneer species when compared

to the other habits, dispersal syndrome, and

successional category. However, the proportion

of these attributes of seed rain changed accord-

ing to the studied fragment, with the rural

one presenting a greater number of tree seeds,

zoochoric, and pioneers than the urban.

It is probable that greatest quantity of seeds

with these functional attributes in the rural

fragment results from the phenology of the

species that make up this area, and the great

availability of fleshy fruits that are attractive

to the dispersing animals. For the pioneer spe-

cies, the high quantity of seeds may indicate

that the forest has not reached maturity, or that

maturity has been reached, but the presence of

some natural or anthropic disturbance, such as

the opening of clearings, has led to the appear-

ance of a greater number of these species. The

high representativeness of trees, zoochoric, and

pioneer species corroborates the assumptions

reported by several authors that in tropical

rainforests (rural or urban) and specifically in

the Atlantic Forest, there is a domain of tree

habit, zoochoric dispersion, and early succes-

sion species (Cole et al., 2010; Marangon et al.,

2010; Oliveira et al., 2011).

In addition, the opening of clearing can

be contributed to an increase in the wind inci-

dence and greater light input, easing the disper-

sion of anemochoric seeds and the emergence

of pioneer species that produce small and light

seeds (César et al., 2017; Plohák et al., 2021).

Therefore, we infer that the canopy disconti-

nuity due to the presence of clearings, as well

as the increase in the velocity of the winds in

the dry season of the studied urban fragment,

may have favored the displacement of woody

climbing plant seeds because they are small and

because they are light.

Finally, our findings show that the spe-

cies richness, seed density, and floristic com-

position were influenced by the surrounding

matrix of rural and urban fragments over time.

There was greater species richness in the urban

14 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e51290, enero-diciembre 2023 (Publicado Ago. 28, 2023)

fragment and higher seed density in the rural

fragment. Seed input is more intense during the

rainy season in the rural fragment and similar

between seasons in the urban fragment. The

species recorded in the seed rain of the rural

fragment are not the same as those recorded

in the urban fragment. During the two years of

study, the rural and urban fragments presented

a high seeds density of tree, zoochoric dispersal

syndrome, and pioneer species.

Our results suggest that landscape distur-

bance measures can be effectively used to assess

the impact of land use in seed rain studies,

especially in urban and rural fragments. How-

ever, it is necessary to identify the cause-effect

relationship of the impact from different uses

of the surrounding soil, and the characteristics

of the plants in larger time series. This investi-

gation will be useful in the current and future

management of remnants of rural and urban

fragments. Future studies could sample more

forest fragment in rural and urban conditions

to identify process governing the seed rain.

Ethical statement: the authors declare that

they all agree with this publication and made

significant contributions; that there is no con-

flict of interest of any kind; and that we fol-

lowed all pertinent ethical and legal procedures

and requirements. All financial sources are fully

and clearly stated in the acknowledgments sec-

tion. A signed document has been filed in the

journal archives.

See supplementary material: a47v71n1-ms1

ACKNOWLEDGMENTS

The authors thank the State Environmen-

tal Agency (CPRH) and the administrators of

the study remnants for the authorization to

carry out this research (Forest Wildlife Refuge

of the Gurjaú System and the State Park Dois

Irmãos), and for all the logistical support; to the

researchers of the laboratory of Plant Ecology

Laboratory of Natural Ecosystems (LEVEN)

for the support; to Dárdano de Andrade-Lima

Herbarium.

REFERENCES

The Angiosperm Phylogeny Group, Chase, M. W., Christ-

enhusz, M. J. M., Fay, M. F., Byng, J. W., Judd, W. S.,

Soltis, D. E., Maabberley, D. J., Sennikov, A. N., Slotis,

P. S., & Stevens, P. F. (2016). An update of the Angios-

perm Phylogeny Group classification for the order

and families of flowering plants: APG IV. Botanical

Journal of the Linnean Society, 181(1), 1–20. https://

dx.doi.org/10.1111/boj.12385

Barroso, G. M., Amorim, M. P., Peixoto, A. L. E., & Ichaso,

C. L. F. (1999). Frutos e sementes: Morfologia aplica-

da à sistemática de dicotiledôneas. UFV Publishing

Company.

Benítez-Malvido, J., Álvarez-Añorve, M. Y., Ávila-Cabadilla,

L. D., González-Di Pierro, A. M., Zermeño-Hernán-

dez, I., Méndez-Toribio, M., González-Rodríguez, A.,

& Lombera, R. (2022). Phylogenetic and functional

structure of tree communities at different life stages

in tropical rain forest fragments. Global Ecology and

Conservation, 36, e02113. https://doi.org/10.1016/j.

gecco.2022.e02113

Brummit, R. K., & Powell, C. E. (1992). Authors of plant

names. Royal Botanic Gardens.

Campos, E. P., Vieira, M. F., Silva, A. F., Martins, S. V.,

Carmo, F. M. S., Moura, V. M., & Ribeiro, A. S. S.

(2009). Chuva de sementes em Floresta Estacional

Semidecidual em Viçosa, MG, Brasil. Acta Botani-

ca Brasilica, 23, 451–458. https://doi.org/10.1590/

S0102-33062009000200017

César, R. G., Rother, D. C., & Brancalion, P. H. S.

(2017). Early esponse of tree seed arrival after

liana cutting in a disturbed tropical forest. Tro-

pical Conservation Science, 10(1), 1–7. https://doi.

org/10.1177/19400829177235860

Clarke, K. R., & Gorley, R. N. (2015). Primer v7: user

manual/tutorial (1st ed.). Primer-E Ltd.

Cole, R. J., Holl, K. D., & Zahawi, R. A. (2010). Seed

rain under tree islands planted to restore degra-

ded lands in a tropical agricultural landscape. Eco-

logical Applications, 20, 1255–1269. https://doi.

org/10.1890/09-0714.1

Colwell, R. K. (2013). EstimateS, Version 9.1.0: Statistical

estimation of species richness and shared species from

samples (Software and User’s Guide). Freeware for

Windows and Mac OS.

CPRH - Agência Estadual de Meio Ambiente. (2003). Diag-

nóstico socioambiental do litoral norte de Pernambuco.

CPRH Publishing Company.

Cutway, H. B., & Ehrenfeld, J. G. (2010). The influence

of urban land use on seed dispersal and wetland

invasibility. Plant Ecology, 210, 153–167. https://doi.

org/10.1007/s11258-010-9746-5

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e51290, enero-diciembre 2023 (Publicado Ago. 28, 2023)

DeWalt, S. J., Maliakal, S. K., & Denslow, J. S. (2003). Chan-

ges in vegetation structure and composition along a

tropical forest chronosequence: implications for wild-

life. Forest Ecology and Managenment, 182, 139–151.

https://doi.org/10.1016/S0378-1127(03)00029-X

EMBRAPA - Empresa Brasileira de Pesquisa Agronômica.

(1998). Centro Nacional de Pesquisa de Solos. Levanta-

mento do reconhecimento de baixa e média intensidade

de solos do Estado de Pernambuco. Mimeografica

Publishing Company.

Freitas, C. G., Dambros, C., & Camargo, J. L. C. (2013).

Changes in seed rain across Atlantic Forest frag-

ments in Northeast Brazil. Acta Oecologica, 53, 49–55.

https://doi.org/10.1016/j.actao.2013.08.005

Gandolfi, S., Leitão-Filho, H. F., & Bezerra, C. L. F. (1995).

Levantamento florístico e caráter sucessional das

espécies arbustivo-arbóreas de uma Floresta Mesófila

Semidecídua no Município de Guarulhos, SP. Revista

Brasileira de Biologia, 55, 753–767.

Gotelli, N. J., & Colwell, R. K. (2001). Quantifying

biodiversity: procedures and pitfalls in the mea-

surement and comparasion in species rich-

ness. Ecology Letters, 4, 379–391. https://doi.

org/10.1046/j.1461-0248.2001.00230.x

Gratzer, G., Pesendorfer, M. B., Sachser, F., Wachtveitl,

L., Nopp-Mayr, U., Szwagrzyk, J., & Canham, C. D.

(2022). Does fine scale spatiotemporal variation in

seed rain translate into plant population structure?

Oikos, 2022, e08826. doi: 10.1111/oik.08826

Guerra, T. N. F. (2016). Influência do tipo de entorno na

intensidade do efeito de borda: diversidade, respostas

funcionais e regeneração da vegetação lenhosa de frag-

mentos protegidos de floresta Atlântica (PhD thesis).

Rural Federal University of Pernambuco, Brasil.

IBGE - Instituto Brasileiro de Geografia e Estatística.

(2012). Manual técnico da vegetação brasileira, Série

manuais Técnicos em Geociências (2th ed.). IBGE

Publishing Company.

Jacomine, P. K. T., Cavalcanti, A. C., Burgos, N., Pessoa, S.

C. P., & Silveira, C. O. (1972). Levantamento explora-

tório – Reconhecimento de solos do estado de Pernam-

buco. DPP/SUDENE.

Jara-Guerrero, A., Espinosa, C. I., Méndez, M., De la

Cruz, M., & Escudero, A. (2020). Dispersal syndrome

influences the match between seed rain and soil seed

bank of woody species in a Neotropical dry forest.

Journal of Vegetation Science, 31, 995–1005. https://

doi.org/10.1111/jvs.12894

Knapp, S., Kühn, I., Mosbrugger, V., & Klotz, S. (2008).

Do protected areas in urban and rural landscapes

differ in species diversity? Biodiversity and Con-

servation, 17, 1595–1612. https://doi.org/10.1007/

s10531-008-9369-5

Knorr, U. C., & Gottsberger, G. (2012). Differences in seed

rain composition in small and large in the northeast

Brazilian Atlantic Forest. Plant Biology, 14, 811–819.

https://doi.org/10.1111/j.1438-8677.2011.00558.x

Kottek, M., Grieser, J., Beck, C., Rudolf, B., & Rubel, F. (2006).

World Map of the Köppen-Geiger climate classifica-

tion updated. Meteorologische Zeitschrift, 15, 259–263.

https://doi.org/10.1127/0941-2948/2006/0130

Lorenzi, H. (1992). Árvores Brasileiras. Instituto Plantarum,

Brasil.

Lorenzi, H. (1998a). Árvores brasileiras: manual de identi-

ficação e cultivo de plantas arbóreas nativas do Brasil

(vol. 1). Instituto Plantarum, Brasil.

Lorenzi, H. (1998b). Árvores brasileiras: manual de identi-

ficação e cultivo de plantas arbóreas nativas do Brasil

(vol. 2). Instituto Plantarum, Brasil.

Lorenzi, H. (2009). Árvores brasileiras: manual de identifi-

cação e cultivo de plantas arbóreas nativas do Brasil

(2th ed.). Instituto Plantarum, Brasil.

Lososová, Z., Chytrý, M., Kühn, I., Hájek, O., Horáková, V.,

Pysek, P., & Tichý, L. (2006). Patterns of plant traits

in annual vegetation of man-made habitats in cen-

tral Europe. Perspectives in Plant Ecology, Evolution

and Systematics, 8, 69–81. https://doi.org/10.1016/j.

ppees.2006.07.001

Lyra-Neves, R. M., Dias, M. M., Azevedo-Júnior, S.

M., Telino-Júnior, W. R., & Larrazábal, M. E. L.

(2004). Comunidade de aves da Reserva Estadual

de Gurjaú, Pernambuco, Brasil. Revista Brasileira

de Zoologia, 21, 581–592. https://doi.org/10.1590/

S0101-81752004000300021

Marangon, G. P., Cruz, A. F., Barbosa, W. B., Loureiro, G.

H., & Holanda, A. C. (2010). Dispersão de sementes

de uma comunidade arbórea em um remanescente

de mata atlântica, município de Bonito, PE. Revista

Verde, 5, 80–87.

Medeiros, D. P. W., Lopes, A. V., & Zickel, C. S. (2007). Phe-

nology of woody species in tropical coastal vegeta-

tion, northeastern Brazil. Flora, 202, 513–520. https://

doi.org/10.1016/j.flora.2006.11.002

Morellato, L. P. C., Camargo, M. G. G., & Gressler, E.

(2013). A review of plant phenology in South and

Central America. In M. D. Schwartz (Ed.), Phenology:

an integrative environmental science (pp. 91–113).

Springer.

Oliveira, L. S. B., Maragon, L. C., Feliciano, A. L. P., Lima,

A. S., Cardoso, M. O., & Silva, V. F. (2011). Florística,

classificação sucessional e síndromes de dispersão em

um remanescente de Floresta Atlântica, Moreno-PE.

Revista Brasileira de Ciências Agrárias, 6, 502–507.

https://doi.org/10.5039/agraria.v6i3a1384

16 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e51290, enero-diciembre 2023 (Publicado Ago. 28, 2023)

Overdyck, E., & Clarkson, B. D. (2012). Seed rain and

soil seed banks limit native regeneration within

urban forest restoration plantings in Hamilton City,

New Zealand. New Zealand Journal Ecology, 36(2),

177–190.

Pivello, V. R., Petenon, D., Jesus, F. M., Meirelles, S. T.,

Vidal, M. M., Alonso, R. A. S., Franco, G. A. D.

C., & Metzger, J. P. (2006). Chuva de sementes

em fragmentos de floresta atlântica (São Paulo, SP,

Brasil), sob diferentes situações de conectividade,

estrutura florestal e proximidade da borda. Acta Bota-

nica Brasilica, 20, 845–859. https://doi.org/10.1590/

S0102-33062006000400010

Plohák, P., Švehláková, H., Rajdus, T., & Turčová, B. (2021).

Seed rain of selected subsidence basins in Karviná

region – preliminary results. GeoScience Engineering,

67(3), 85–94. https://doi.org/10.35180/gse-2021-0055

Santos, P. S., Araújo, E. L., Andrade, J. R., Silva, K. A., San-

tos, D. M., Santos, J. M. F. F., Prazeres, G. L., & Ferraz,

E. M. N. (2020). Urban or rural fragments: which

soil use in forest surroundings induces greater litter

deposition? Urban Ecosystems, 23, 865–874. https://

doi.org/10.1007/s11252-020-00931-5

Silva, M. C. N. A., & Rodal, M. J. N. (2009). Padrões das

síndromes de dispersão de plantas em áreas com dife-

rentes graus de pluviosidade, PE, Brasil. Acta Botanica

Brasilica, 23(4), 1040–1047. https://doi.org/10.1590/

S0102-33062009000400014

Sokal, R. R., & Rohlf, F. J. (1995). Biometry. Freeman and

Company.

StatSoft Inc. (2003). Statistica for Windows (Data Analysis

Software System - Version 7.0). StatSoft, Inc.

Systat Software Inc. (2006). SigmaPlot for windows (Version

10.0). Systat Software.

Talora, D. C., & Morellato, P. C. (2000). Phenology of coas-

tal-plain forest tree species from Southeastern Brazil.

Brazilian Journal of Botany, 23, 13–26. http://dx.doi.

org/10.1590/S0100-84042000000100002

Van der Pijl, L. (1982). Principles of dispersal in higher

plants. Springer.

Werden, L. K., Holl, K. D., Chaves-Fallas, J. M., Oviedo-Bre-

nes, F., Rosales, J. A., & Zahawi, R. A. (2021). Degree

of intervention affects interannual and within-plot

heterogeneity of seed arrival in tropical forest res-

toration. Journal of Applied Ecology, 58, 1693–1704.

https://doi.org/10.1111/1365-2664.13907

Yang, X., Yan, C., Gu, H., & Zhang, Z. (2020). Interspecific

synchrony of seed rain shapes rodent-mediated indi-

rect seed–seed interactions of sympatric tree species

in a subtropical forest. Ecology Letters, 23, 45–54.

https://doi.org/10.1111/ele.13405