Acta Botanica Brasilica 28(4): 569-576. 2014.
doi: 10.1590/0102-33062014abb3432
Structure and floristic diversity of remnant semideciduous
forest under varying levels of disturbance
Darlene Gris1,4, Lívia Godinho Temponi2 and Geraldo Alves Damasceno Junior3
Received: 21 November, 2013. Accepted: 2 June, 2014.
ABSTRACT
The perturbation of Neotropical forests generates large disturbances in biological communities. The species that
suffer least from the resulting habitat fragmentation are the pioneers, because they possess greater ability to inhabit
disturbed environments. Therefore, it is expected that species diversity will be greater in areas subjected to intermediate
disturbance, such as the opening of gaps, because a large number of pioneer species will develop and coexist with
species of more advanced successional stages. This study aimed to compare two forest remnants that differed in size
and disturbance intensity, in order to determine the effects of disturbances on species diversity and the size ratios of
individual trees. This was accomplished with comparative analyses of diversity, richness and diameter ratios obtained
for 10 plots at two semideciduous forest sites. We recorded a total of 85 species, of which 70 were in the private nature
reserve Fazenda Santa Maria, 58 were in Iguaçu National Park, and 43 were at both sites. Diversity was greater in the
more disturbed remaining forest, because this area showed higher species richness, which is in accordance with some
premises of the intermediate disturbance theory. There was also an increase in the number of pioneer individuals, and
the less disturbed area showed individuals with larger diameters, which is likely attributable to the removal of large
individuals from the more disturbed area during the anthropogenic process of forest modification.
Key words: Intermediate disturbance, species richness, Neotropical forest, tree communities
Introduction
The constant disturbance of tropical forests, whether
by natural events or human activities (destruction of vegetation and conversion or loss of habitat), has led to the
fragmentation of these forests into small isolated patches.
Disturbances occur more frequently in the fragments,
drastically altering species richness, diversity and forest
structure (Tanizaki-Fonseca & Moulton 2000; Campos
2006). Tropical forests in general have high spatial and
temporal heterogeneity, which strongly influence species
distribution patterns. Plant species in tropical forests grow
and establish in a mosaic of different successional stages,
whereby the distribution and density of plant populations
are influenced by disturbance dynamics (Brokaw 1985;
Young & Hubbell 1991).
Upon the occurrence of a natural disturbance in a forest,
such as canopy openings or border effects, pioneer species
increase in density in response to increased light availability.
The same phenomenon occurs in response to anthropogenic disturbances such as selective logging or changes in
land use, and varying intensities and frequencies of these
disturbances have different effects on a plant community
(Hill & Curran 2003; Laurance et al. 2006; Bongers et al.
2009). One observed effect is the decrease in diameter of
trees and the occurrence of many small individuals (Gomes
et al. 2004; Villela et al. 2006), due to the increased number
of young individuals and pioneer species, and reduction
of the number of large individuals by selective logging, for
example. Such alterations in vegetation structure as a result
of disturbance have been observed in several studies on
effects of fragment size, edge dynamics, and canopy gaps
on woody plant composition in the Atlantic Forest (Alves
& Santos 2002; Bertoncini & Rodrigues 2008; Lopes et al.
2009; Oliveira et al. 2004; Oliveira et al. 2008; Ribeiro et al.
2009; Santos et al. 2008).
Considering those disturbances to the vegetation, it is
expected that, as proposed in the intermediate disturbance
theory (Connell 1978), higher species diversity may be
maintained at moderate levels of disturbance frequency and
intensity because superior competitors, which dominate
communities at more advanced successional stages, are
more susceptible to disturbance. Therefore, gaps are open
for the development of pioneer species, which tolerate
Universidade Estadual do Oeste do Paraná, Programa de Pós-Graduação em Conservação e Manejo de Recursos Naturais, Cascavel, PR.
Universidade Estadual do Oeste do Paraná, Herbário UNOP, Cascavel, PR.
3
Universidade Federal de Mato Grosso do Sul, Departamento de Botânica, Campo Grande, MS.
4
Author for correspondence: darlenegris@hotmail.com
1
2
Darlene Gris, Lívia Godinho Temponi and Geraldo Alves Damasceno Junior
unfavorable conditions. Conversely, when disturbance
levels are very high, after intense human intervention, for
example, all species are at risk of being eliminated. This
study therefore aimed to evaluate the effects of disturbance
on tree species richness and diversity, as well as on the
proportional distribution by diameter, in forest fragments,
comparing two sites: a large area of continuous forest that is
less disturbed; and a nearby forest fragment that is smaller
and more heavily disturbed by human activities.
Material and Methods
Study area
To compare effects of increased disturbance on plant
community in forest remnants, we selected two areas. One
was a small private nature reserve, the Fazenda Santa Maria,
hereafter referred to as the FSM, which was heavily disturbed, whereas the other was less disturbed, representing
a large tract of more advanced stage forest, Iguaçu National
Park (INP).
The FSM is located in the municipality of Santa Terezinha do Itaipu, in the state of Paraná, and covers 242 ha.
This area has been protected since 1955 and was designated a private nature reserve in 1997. The fragment had
suffered a moderate degree of human intervention prior
to the year 1955, when several species of economic interest were extracted and forest loss in the surrounding land
was pronounced. Therefore, edge effects are evident in the
remnant, as are gaps caused by logging.
The INP is an ecological reserve in the southwestern
region of the state of Paraná, created in 1939 and currently
encompassing 185,262 ha (Salamuni et al. 2002). It contains
patches of Araucaria forest (rain forest) and semideciduous
forest (Veloso 1991; IBGE 2012).
Both sampled sites are fragments of semideciduous forest and are on the Third Paraná Plateau, near Foz do Iguaçu,
with elevations ranging from 120 m to 540 m (Santos et al.
2006; Maack 2012). At both sites, the soils are red Oxisols
and the climate is humid subtropical (Köppen type Cfa),
with an annual mean temperature of 21.5°C and annual
rainfall of approximately 1800 mm, of which two thirds are
distributed from October to March, mainly in December
and January (Bhering & Santos 2008; SIMEPAR 2011).
Sampling and Analysis
We installed 10 permanent plots using a 20 × 20
m spacing regime, for a total of 0.4 ha in each forest
remnant. Plots were demarcated at a distance of approximately 400 m from the forest edge, preventing any
clearing or trail opening. Plots in the INP were located
between the coordinates 25°31’56.79”S;54°17’32.14”W and
25°31’55.56”S;54°17’22.61”W, and plots in the FSM were located between the coordinates 25°29’30.70”S;54°21’30.61”W
570
and 25°29’32.94”S;54°21’41.36”W, and the distance between
the two areas is approximately 8 km. Trees whose circumference at breast height (CBH) was ≥ 15 cm were included in
the sampling, as per Rodrigues & Gandolfi (2004), as were
bifurcated stems, if at least one had a diameter ≥ 15 cm. The
selected individuals were numbered and observed monthly
from September 2010 to November 2011, in order to sample
the maximum number of species in flower.
When found, fertile specimens were collected, identified
and processed using usual herbarium techniques (Mori et
al. 1989; Bridson & Forman 2004). Voucher specimens were
registered at Western Paraná State University Herbarium
(code, UNOP). Sterile individuals were also collected,
identified and added to a sterile collection in the UNOP
Herbarium. For identification of the plant material, we
used regional checklists, as well as identification keys,
specific bibliography (Lorenzi 2002a, 2002b, 2010; Ramos
et al. 2008) and comparison with specimens in the UNOP
Herbarium and the Herbarium of the Curitiba Municipal
Botanical Museum (code, MBM). The lists were produced
with the botanical families organized according to the Angiosperm Phylogeny Group III guidelines (APG III 2009)
and the species names and the authors organized according
to the List of Species in the Flora of Brazil (Lista de Espécies
da Flora do Brasil 2013).
We analyzed the data using the programs R, version
3.0.1 (R Development Core Team 2013), PAST (Hammer
et al. 2001) and FITOPAC, version 2.1.2 (Shepherd 2010).
Shannon diversity and evenness indices were obtained for
the remnants, as were importance values (IVs) for each
species. The IV is an outcome of phytosociological analysis,
obtained by summing the percentages of relative density,
relative frequency and relative dominance (Shepherd 2010).
To compare diversity indices, we used Hutcheson’s t-test
(Hutcheson 1970; Zar 1999).
Rarefaction curves, with their respective 95% confidence
intervals, were built according to the number of individuals,
in order to compare the species richness estimated for both
areas. Results of rarefaction curves constitute an unbiased
comparison with other studies, because they are not influenced by variations in the density of individuals and can
simulate small sample sizes (Colwell & Coddington 1994;
Gotelli & Colwell 2001). Therefore, the curves were constructed to compare the estimated richness between sites,
in case the sampling number were equal between them.
On the basis of data in the literature, were classified the
species, by successional stage, as pioneer or non-pioneer
species. As is well known, sites that are more disturbed, have
canopy gaps or are under greater edge effects are colonized
by greater numbers of species and individuals. Therefore,
we made two calculations to determine the differences in
patterns between the two sites: the chi-square test for total
non-pioneer and pioneer species per site; and the chi-square
test for proportions of individuals belonging to the pioneer
and non-pioneer groups per site.
Acta bot. bras. 28(4): 569-576. 2014.
Structure and floristic diversity of remnant semideciduous forest under varying levels of disturbance
To examine the difference between the mean diameters
in the studied fragments, we used the nonparametric Wilcoxon test at a 5% significance level to identify differences
in distributions of tree diameters in the FSM and INP (Zar
1999). In addition, to determine the differences between
the two sites, in terms of the diameter ratios, the number
of individuals per class at intervals of 5 cm was calculated,
as proposed by Soares et al. (2006), starting from a minimum inclusion diameter of 4.77 cm, corresponding to the
minimum CBH of 15 cm.
Results
In the study area as a whole, we found a total of 1032
individuals belonging to 85 species (Tab. 1): 70 species were
present in the FSM, 58 were present in the INP, and 43 were
present at both sites. We sampled only one exotic species,
Citrus X aurantium, which occurred in the INP.
The first 10 species, in order of IV, accounted for 50%
of the total, reflecting a few species with high IVs. The
species that were the most well represented, in terms of
the number of individuals, were Euterpe edulis, Sorocea
bonplandii and Guarea kunthiana (in both areas); Chrysophyllum gonocarpum and Balfourodendron riedelianum
(in the FSM only); and Citrus X aurantium and Trichilia
catigua (in the INP only).
The Shannon-Wiener diversity values were 2.71 for
the IPN and 3.37 for the FSM (Tab. 2), and the difference
between the two was statistically significant (t=−6.48,
p=1.33−11). The evenness values were 0.67 for the INP and
0.79 for the FSM. The higher richness in the FSM was observed in the rarefaction curves (Fig. 1).
As can be seen in Tab. 3, there was no significant difference between the two sites with respect to the number of
species belonging to the analyzed successional groups, pioneer (χ2=1.50, p=0.22) and non-pioneer (χ2=0.35, p=0.56).
Furthermore, the number of individuals belonging to the
non-pioneer group did not differ between the two areas
(χ2=0.34, p=0.56). However, the FSM had a significantly
higher number of individuals of pioneer species than did
the INP (χ2=19.63, p=0.93−5) (Tab. 3).
The diameter class distribution was significantly different between the two sites (W=110215.5, p=4.26−6). Despite
the fact that individuals with a diameter < 15 cm accounted
for 80% of the individuals in the FSM (n = 412) and 86%
of the individuals in the INP (n = 447), the INP presented
some specimens with a diameter > 70 cm, whereas the FSM
did not (Fig. 2).
Discussion
The two analyzed areas shared important species for the
Atlantic Forest Biome, such as Aspidosperma polyneuron, Cedrela fissilis and Balfourodendron riedelianum. These species
Acta bot. bras. 28(4): 569-576. 2014.
are rare and endangered because they are attractive targets
for illegal logging, which underscores the importance of
preserving the remaining fragments of semideciduous forest
(Hatschbach & Ziller 1995; Ribas et al. 2003; IUCN 2009).
Ten species collectively accounted for 50% of the total
IV, and seven of those species occurred at both study sites.
These high IVs may be related to large diameters, combined
with a reasonable number of individuals, reflecting a higher
basal area, as noted for Aspidosperma polyneuron, Alchornea
triplinervia, Cabralea canjerana and Chrysophyllum gonocarpum, or to small diameters, combined with high numbers
of individuals, as noted for Euterpe edulis; Guarea kunthiana
and Sorocea bonplandii. In addition, excepting G. kunthiana
and S. bonplandii, the five species with the highest IVs were
also the most representative for basal area at both sites.
The Shannon-Wiener diversity indices differed between
the INP and the FSM. Although other studies of semideciduous forest (Tab. 2) have yielded results consistent with
those we obtained for the FSM, the index we obtained for the
INP was lower than those reported in all of the studies we
reviewed. The same pattern was observed for the evenness
index for the INP, which was lower in the present study than
in other studies, whereas the evenness index for the FSM was
consistent with those of the same studies (Ivanauskas et al.
1999; Bianchini et al. 2003; Jurinitz & Jarenkov 2003; Silva
et al. 2004; Costa-Filho et al. 2006; Prado-Júnior et al. 2011).
Connell (1978) proposed that higher species diversity
is maintained under intermediate levels of disturbance.
Such disturbances occurring at moderate frequency and
intensity should promote increased environmental heterogeneity, because pioneer species coexist with species of
more advanced successional stages (shade-tolerant species),
thus increasing diversity. Therefore, it was not surprising
that the more heavily disturbed FSM site, with a history
of more intense human activity, had higher diversity and
more individuals of pioneer species, which also directly
affect diversity, than did the INP site, given that degradation and loss of natural habitat at intermediate levels enable
a wider range of species to become established (Hunter
1996; Wilson 1997; Hernandez-Stefanoni 2005). Nunes et
al. (2003) found similar results in a study conducted in a
semideciduous forest, where the borders of fragments were
more diverse than were the interiors, due to the emergence
of light-demanding pioneer species. In dry areas of a tropical forest, similar to our study area, Bongers et al. (2009)
showed that increases in pioneer species and diversity were
interconnected with increased disturbance, supporting the
theory of intermediate disturbance. However, the authors
found that the occurrence of disorders did not significantly
alter the diversity in wetlands.
We can conclude that the alterations caused by disturbances in the FSM did not lead to a significant increase
in the richness of pioneer species, as would have been
expected, but rather in the number of pioneer individuals
compared to the pattern observed in the INP. Disturbed
571
Darlene Gris, Lívia Godinho Temponi and Geraldo Alves Damasceno Junior
Table 1. Families, species, number of individuals, successional groups and importance values of the analyzed fragments. Successional group (SG) of the species
observed: pioneer (P) and non-pioneer (NP). Number of individuals for the species present in the Iguaçu National Park (INP) and Fazenda Santa Maria RPPN
(FSM), basal areas for species in INP ((AB(INP)) and FSM (AB(FSM)) and importance values for species in INP (V(INP)) and FSM (V(FSM)).
Family
Scientific names
SG
INP
FSM
AB(INP)
AB(FSM)
V(INP)
V(FSM)
Anarcadiaceae
Astronium graveolens Jacq.
NP
0
3
0.00
0.14
0.00
0.77
Annonaceae
Annona neosalicifolia H.Rainer
NP
0
1
0.00
0.01
0.00
0.21
P
1
4
0.03
0.39
0.30
0.95
Aspidosperma polyneuron Müll.Arg.
NP
5
13
1.58
1.52
3.04
3.68
Aspidosperma tomentosum Mart.
NP
0
1
0.00
0.01
0.00
0.22
Rauvolfia sellowii Müll.Arg.
NP
3
0
0.56
0.00
1.46
0.00
P
0
1
0.00
0.03
0.00
0.23
Annona sylvatica A.St.-Hil.
Apocynaceae
Tabernaemontana fuchsiaefolia A. DC
Araliaceae
P
0
9
0.00
0.84
0.00
2.30
Schefflera calva (Cham.) Frodin & Fiaschi
NP
0
3
0.00
0.11
0.00
0.73
Arecaceae
Euterpe edulis Mart
NP
159
125
2.33
2.58
15.04
12.18
Syagrus romanzoffiana (Cham.) Glassman
NP
5
17
0.51
1.55
1.72
3.69
Bignoniaceae
Jacaranda micrantha Cham.
P
1
3
0.17
0.10
0.47
0.72
Boraginaceae
Cordia americana (L.) Gottschling & J.S.Mill.
NP
0
1
0.00
0.01
0.00
0.22
Cordia ecalyculata Vell.
NP
2
13
0.04
0.41
0.56
2.26
P
1
1
0.01
0.06
0.26
0.27
Cardiopteridaceae Citronella paniculata (Mart.) R.A.Howard
NP
2
5
0.01
0.24
0.53
1.28
Caricaceae
NP
0
9
0.00
0.63
0.00
1.95
Cannabaceae
Dendropanax cuneatus (DC.) Decne. & Planch.
Trema micrantha (L.) Blume
Jacaratia spinosa (Aubl.) A.DC.
Celastraceae
Peritassa campestris (Cambess.) A.C.Sm.
NP
0
1
0.00
0.03
0.00
0.23
Euphorbiaceae
Actinostemon concolor (Spreng.) Müll.Arg.
NP
4
2
0.03
0.00
0.49
0.44
Alchornea triplinervia (Spreng.) Müll.Arg.
NP
12
11
1.48
2.43
3.95
3.93
Apuleia leiocarpa (Vogel) J.F.Macbr.
NP
1
0
0.43
0.00
0.79
0.00
Calliandra foliolosa Benth.
NP
1
1
0.02
0.02
0.29
0.23
Enterolobium contortisiliquum (Vell.) Morong
NP
1
2
0.41
0.11
0.77
0.38
Holocalyx balansae Micheli
NP
2
7
0.24
1.03
0.62
2.22
Inga marginata Willd.
NP
7
3
0.19
0.03
1.85
0.65
Inga striata Benth.
NP
1
1
0.01
0.02
0.27
0.23
Lonchocarpus cultratus (Vell.) A.M.G.Azevedo
& H.C.Lima
NP
1
11
0.13
0.79
0.42
2.24
Lonchocarpus muehlbergianus Hassl.
NP
0
8
0.00
0.07
0.00
1.16
Fabaceae
Machaerium paraguariense Hassl.
NP
0
2
0.00
0.01
0.00
0.43
Machaerium stipitatum Vogel
NP
2
4
0.02
0.17
0.54
1.00
P
0
2
0.00
0.21
0.00
0.63
NP
6
2
0.58
0.27
1.87
0.69
Mimosa bimucronata (DC.) Kuntze
Parapiptadenia rigida (Benth.) Brenan
Peltophorum dubium (Spreng.) Taub.
NP
1
2
0.01
0.06
0.28
0.48
Senegalia polyphylla (DC.) Britton & Rose
NP
0
3
0.00
0.47
0.00
1.11
Lamiaceae
Aegiphila integrifolia (Jacq.) Moldenke
P
2
4
0.40
0.16
0.81
0.70
Lauraceae
Endlicheria paniculata (Spreng.) J.F.Macbr.
NP
2
9
1.89
0.43
2.84
1.73
Nectandra megapotamica (Spreng.) Mez.
NP
8
9
0.89
0.45
2.38
1.75
P
3
6
0.12
0.52
0.73
1.63
Ocotea silvestris Vattimo-Gil
NP
7
1
0.40
0.15
2.10
0.36
Ocotea diospyrifolia (Meisn.) Mez
Ocotea puberula (Rich.) Nees
NP
0
1
0.00
0.31
0.00
0.52
Loganiaceae
Strychnos trinervis (Vell.) Mart
NP
1
2
0.01
0.00
0.27
0.44
Malvaceae
Ceiba speciosa (A. St.-Hil.) Ravena
NP
4
5
0.25
0.46
0.95
1.36
P
2
0
0.11
0.00
0.46
0.00
Heliocarpus americanus L.
Continues.
572
Acta bot. bras. 28(4): 569-576. 2014.
Structure and floristic diversity of remnant semideciduous forest under varying levels of disturbance
Table 1. Continuation.
Family
Scientific names
SG
INP
FSM
AB(INP)
AB(FSM)
V(INP)
V(FSM)
Melastomataceae
Miconia pusilliflora (DC.) Naudin
NP
0
1
0.00
0.01
0.00
0.21
Meliaceae
Cabralea canjerana (Vell.) Mart.
NP
7
12
1.68
3.12
3.68
5.13
Cedrela fissilis Vell.
NP
2
12
0.54
2.60
1.18
4.46
Guarea guidonia (L.) Sleumer
NP
1
0
0.01
0.00
0.27
0.00
Guarea kunthiana A.Juss.
NP
57
27
2.06
0.44
8.14
3.19
Guarea macrophylla Vahl
NP
0
1
0.00
0.02
0.00
0.23
Trichilia casaretti C.DC.
NP
0
1
0.00
0.02
0.00
0.23
Trichilia catigua A.Juss.
NP
13
4
0.20
0.02
2.43
0.71
Moraceae
Trichilia elegans A.Juss.
NP
2
0
0.01
0.00
0.53
0.00
Trichilia pallida Sw.
NP
1
0
0.05
0.00
0.31
0.00
Ficus insipida Willd.
NP
3
0
0.69
0.00
1.62
0.00
Maclura tinctoria (L.) D.Don ex Steud.
NP
9
3
1.19
0.42
3.01
1.05
Sorocea bonplandii (Baill.) W.C.Burger et al.
NP
99
30
0.76
0.28
9.24
3.51
Myrsinaceae
Myrsine umbellata Mart.
NP
0
3
0.00
0.12
0.00
0.74
Myrtaceae
Campomanesia guazumifolia (Cambess.) O.Berg
NP
1
0
0.02
0.00
0.28
0.00
Campomanesia xanthocarpa (Mart.) O.Berg
NP
1
8
0.01
0.70
0.27
1.94
Eugenia burkartiana (D.Legrand) D.Legrand
NP
2
2
0.05
0.02
0.57
0.43
Eugenia florida DC.
NP
0
1
0.00
0.00
0.00
0.21
Eugenia ramboi D. Legrand.
NP
3
4
0.10
0.17
0.71
0.86
Plinia rivularis (Cambess.) Rotman
NP
9
2
0.82
0.03
2.75
0.45
Peraceae
Pera glabrata (Schott) Poepp. ex Baill.
P
0
1
0.00
0.01
0.00
0.21
Phytolaccaceae
Seguieria guaranitica Speg.
P
1
1
0.01
0.02
0.26
0.23
Piperaceae
Piper amalago L.
NP
2
0
0.02
0.00
0.54
0.00
Rosaceae
Prunus myrtifolia (L.) Urb.
NP
0
4
0.00
0.51
0.00
1.21
Rutaceae
Balfourodendron riedelianum (Engl.) Engl.
NP
5
21
0.97
1.71
2.30
4.26
Citrus X aurantium L.*
NP
22
0
0.75
0.00
3.89
0.00
Pilocarpus pauciflorus A.St.-Hil.
NP
1
0
0.01
0.00
0.28
0.00
Salicaceae
Sapindaceae
Sapotaceae
Pilocarpus pennatifolius Lem.
NP
3
0
0.02
0.00
0.80
0.00
Zanthoxylum caribaeum Lam.
NP
3
0
0.30
0.00
1.15
0.00
Zanthoxylum petiolare A.St.-Hil. & Tul.
NP
0
2
0.00
0.01
0.00
0.29
Casearia decandra Jacq.
NP
1
0
0.01
0.00
0.27
0.00
Casearia sylvestris Sw.
NP
2
3
0.09
0.02
0.62
0.50
P
1
4
0.03
0.15
0.30
0.84
Diatenopteryx sorbifolia Radlk.
NP
4
0
2.59
0.00
4.03
0.00
Allophylus edulis (A.St.-Hil. et al.) Hieron. ex
Niederl.
Matayba elaeagnoides Radlk.
NP
0
1
0.00
0.36
0.00
0.58
Chrysophyllum gonocarpum (Mart. & Eichler ex
Miq.) Engl.
NP
9
34
1.06
3.63
2.86
7.37
Chrysophyllum marginatum (Hook. & Arn.)
Radlk.
NP
4
8
0.04
0.31
0.89
1.54
P
0
1
0.00
0.01
0.00
0.22
Solanaceae
Cestrum bracteatum Link & Otto
Solanum argenteum Dunal
P
0
1
0.00
0.03
0.00
0.24
Urticaceae
Cecropia pachystachya Trécul
P
3
7
0.13
0.21
0.74
1.52
Urera baccifera (L.) Gaudich. ex Wedd.
P
0
6
0.00
0.08
0.00
0.89
Violaceae
Hybanthus bigibbosus (A.St.-Hil.) Hassl.
NP
0
1
0.00
0.36
0.00
0.58
518
514
27.08
32.22
100.00
100.00
Total
* Exotic species
Acta bot. bras. 28(4): 569-576. 2014.
573
Darlene Gris, Lívia Godinho Temponi and Geraldo Alves Damasceno Junior
Table 2. Comparision of the parameters for both analyzed areas, as well as the values obtained in other studies conducted in Seasonal Semideciduous Forest remnants. Size of the sampling site in hectares (Area), circumference at breast height (CBH) used as inclusion criteria, bulk density (D) in individuals per hectare,
Shannon-Wiener diversity (H’) and evenness (J’) for the sampling sites.
This work
Local
Area
CBH
D
H’
J’
FSM
0.4
>15
1285
3.36
0.79
INP
0.4
>15
1295
2.71
0.67
D
H’
J’
0.82
Other studies conducted in Seasonal Semideciduous Forest
Local/Reference
Area
Fazenda Santa Irene – SP (IVANAUSKAS et al., 1999)
0.42
>15
2271
3.77
Parque Estadual Mata dos Godoy– PR (BIANCHINI et al., 2003)
0.5
>15
1824
3.44
-
1
>16
2236
3.20
0.76
Zona da Mata Mineira – MG (SILVA et al., 2004)
0.5
>15
2786
3.56
0.74
Estação Ecológica do Caiuá – PR (COSTA-FILHO et al., 2006)
2.25
-
1239
3.32
0.77
1
>15
-
3.47
0.81
Serra do Sudeste – RS (JURINITZ e JARENKOV, 2003)
Reserva Legal da Fazenda Irara – MG (PRADO-JÚNIOR et al., 2011)
areas are expected to show a pattern in which individuals in
the smaller diameter classes are more numerous and there
are fewer large trees. Individuals with a diameter < 15 cm
predominated in the FSM and INP (respectively accounting
for 80% and 86% of the total), this pattern (many individuals
in the smaller diameter classes) being commonly observed
in tropical forests (Meyer 1952). However, we observed a
significant difference in the diameter distribution between
the two sites, individuals with a CBH > 70 cm being found
only in the INP. Although the FSM has a history of human
disturbance, no timber extraction or other type of human
activities has taken place there in the last 60 years. Nevertheless, this lack of large individuals may be due to mortality
of older, larger individuals after intense disturbance or by
CBH
timber extraction, as observed in remnants of Amazon rain
forest (Laurance et al. 2000) and submontane Atlantic Forest
(Carvalho & Nascimento 2009). Therefore, the exclusion
of individuals of the canopy could favor an increase in the
number of small individuals, suggesting that there was a
change in the successional processes and in the current
structural conformation in this forest fragment.
The results obtained in the present study seem to agree
with some premises of the intermediate disturbance theory,
showing, as expected, an increase in diversity in the area
with a known history of disturbance (the FSM) in relation
to a more conserved one (INP). It would be useful to investigate a third area, with very high disturbance, to have
a comparative that could confirm the hypothesis, because
other potential determinants were not evaluated. In the
FSM, the increased diversity is related to the increase in species richness. The FSM also showed a pattern of individuals
in the smaller diameter classes, which is likely attributable to
the extraction of large individuals during the anthropogenic
process of forest modification.
Acknowledgments
Figure 1. Rarefaction curves for the private nature reserve Fazenda Santa Maria
(FSM) site and the Iguaçu National Park (INP) site, showing the relationship
between the number of tree species and number of individuals sampled.
Continuous lines indicate observed values, whereas dotted lines represent the
upper and lower limits of the confidence interval.
574
We are grateful to the researchers at the Curitiba
Municipal Botanical Museum, for their assistance in the
identification of specimens, to Adaíldo Policena, for the
assistance in the fieldwork, and to Dr. Arnildo Pott, for
reviewing the English. This study received financial support from the Parque Tecnológico Itaipu Ciência, Tecnologia
e Inovação da Fundação Parque Tecnológico Itaipu – Brasil
(PTI C&T/FPTI-BR, Itaipu Technology Park for Science,
Technology and Innovation via the Itaipu Technology
Park Foundation of Brazil; master’s scholarship to DG); the
Araucaria Foundation (Grant no. 223/2010); the Fundação
de Amparo à Pesquisa do Estado de São Paulo (FAPESP, São
Paulo Research Foundation; Grant no. 2010/17400-3); the
Brazilian Conselho Nacional de Desenvolvimento Científico
Acta bot. bras. 28(4): 569-576. 2014.
Structure and floristic diversity of remnant semideciduous forest under varying levels of disturbance
Figure 2. Diameter class distribution at intervals of 5 cm at the two sampling sites: a) Iguaçu National Park (INP) and b) the private nature reserve Fazenda Santa
Maria (FSM).
Table 3. Number of species for successional groups: pioneers and non-pioneers; number of individuals for successional groups: pioneer and non-pioneer for Iguaçu
National Park (INP) and Fazenda Santa Maria RPPN sites. According to values obtained by chi-square and p. Numbers followed by * differed significantly from the
number in the same column with p<0.05 using the chi-square (χ²) test.
Pioneers species
Non-pioneers species
Pioneers individuals
Non-pioneers individuals
INP
9
49
15
481
FSM
15
55
51*
463
χ²
1.50
0.35
19.63
0.34
p
0.22
0.56
0.93-5
0.56
e Tecnológico (CNPq, National Council for Scientific and
Technological Development; Grant no. 562240/2010-1); and
the Centro de Ciências Biológicas e da Saúde-Universidade
Estadual do Oeste do Paraná (CCBS-Unioeste, Western
Paraná State University Center for Biological and Health
Sciences).
References
Alves, L.F. & Santos, F.A.M. 2002. Tree allometry and crown shape of
four tree species in Atlantic rain forest, south-east Brazil. Journal of
Tropical Ecology 18: 245–260.
APG III. 2009 An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Botanical
Journal of the Linnean Society 161: 105-121.
Bertoncini, A.P. & Rodrigues, R.R. 2008. Forest restoration in an indigenous
land considering a forest remnant influence (Avai, São Paulo State,
Brazil). Forest Ecology and Management 255: 513–521.
Acta bot. bras. 28(4): 569-576. 2014.
Bhering, S.B. & Santos, H.G. (Orgs.). 2008. Mapa de Solos do Estado do
Paraná – Legenda Atualizada. Rio de Janeiro, Embrapa Florestas,
Embrapa Solos, IAPAR.
Bianchini, E.; Popolo, R.S.; Dias, M.C. & Pimenta, J.A. 2003. Diversidade
e estrutura de espécies arbóreas em área alagável do município de
Londrina, Sul do Brasil. Acta Botanica Brasilica 17(3): 405-419.
Bongers, F.; Poorter, L.; Hawthorne, W.D. & Sheil, D. 2009. The Intermediate Disturbance Hypothesis applies to tropical forests, but disturbance
contributes little to tree diversity. Ecology Letters 12(8): 798-805.
Bridson, D.M. & Forman, L. 2004. The Herbarium Handbook. 3rd ed.
Kew, Royal Botanic Gardens.
Brokaw, N. 1985. Gap-phase regeneration in a tropical forest. Ecology
66: 682-687.
Campos, J.B. 2006. A fragmentação de ecossistemas, efeitos decorrentes
e corredores de biodiversidade. Pp. 165-174. In: Campos, J.B., Tossulino, M.G.P. & Muller, C.R.C (Eds.). Unidades de Conservação:
ações para a valorização da biodiversidade. Curitiba, Instituto
Ambiental do Paraná.
Carvalho, F.A. & Nascimento, M.T. 2009. Estrutura diamétrica da comunidade e
das principais populações arbóreas de um remanescente de Floresta Atlântica Submontana (Silva Jardim-RJ, Brasil). Revista Árvore 33(2): 327-337.
575
Darlene Gris, Lívia Godinho Temponi and Geraldo Alves Damasceno Junior
Colwell, R.K. & Coddington, J.A. 1994. Estimating terrestrial biodiversity
through extrapolation. Philosophical Transactions of the Royal
Society (Series B) 345: 101-118.
Connell, J.H. 1978. Diversity in Tropical Rain Forests and Coral Reefs.
Science 199(4335): 1302-1310.
Costa-Filho, L.V.; Nanni, M.R. & Campos, J.B. 2006. Floristic and Phytosociological Description of a Riparian Forest and the Relationship
with the Edaphic Environment in Caiuá Ecological Station – Paraná –
Brazil. Brazilian Archives of Biology and Technology 49(5): 785-798.
Gomes, A.P.C.; Souza, A.L. & Meira Neto, J.A.A. 2004. Alteração estrutural de uma área florestal explorada convencionalmente na bacia do
Paraíba do Sul, Minas Gerais, nos domínios de Floresta Atlântica.
Revista Árvore 28(3): 407-417.
Gotelli, N.J. & Colwell, R.K. 2001. Quantifying biodiversity: procedures
and pitfalls in the measurement and comparison of species richness.
Ecology Letters 4: 379-391.
Hammer, O.; Harper, D.A.T. & Ryan, P.D. 2001. PAST: Paleontological
statistics software package for education and data analysis. Palaeontologia Electronica 4(1): 1-9.
Hatschbach, G.G. & Ziller, S.R. 1995. Lista vermelha de plantas ameaçadas
de extinção no estado do Paraná. Curitiba, Secretária de Estado do
Meio Ambiente.
Hernandez-Stefanoni, J.L. 2005. Relationships between landscape patterns
and species richness of trees, shrubs and vines in a tropical forest.
Plant Ecology 179: 53-65.
Hill, J.L. & Curran, P.J. 2003. Area, shape and isolation of tropical forest
fragments: effects on tree species diversity and implications for conservation. Journal of Biogeography 30: 1391-1403.
Hunter, M.L. 1996. Fundamentals of conservation biology. Cambridge,
Blackwell Science.
Hutcheson, K. 1970. A test for comparing diversities based on the Shannon
formula. Journal of Theoretical Biology 29: 151-154.
IBGE – Instituto Brasileiro de Geografia e Estatística. 1992. Manual Técnico da Vegetação Brasileira. Rio de Janeiro, IBGE.
IUCN - International Union for Conservation of Nature. 2009. IUCN Red
List of Threatened Species. Available from: http://www.iucnredlist.
org. Cited 2013 Aug 01.
Ivanauskas, N.M.; Rodrigues, R.R. & Nave, A.G. 1999. Fitossociologia de
um trecho de Floresta Estacional Semidecidual em Itatinga, SP, Brasil.
Scientia Forestalis 56: 83-99.
Jurinitz, C.F. & Jarenkow, J.A. 2003. Estrutura do componente arbóreo de
uma floresta estacional na Serra do Sudeste, Rio Grande do Sul, Brasil.
Revista Brasileira de Botânica 26(4): 475-487.
Laurance, W.F.; Delamônica, P.; Laurance, S.G.; Vasconcelos, H.L. & Lovejoy, T.E. 2000. Rainforest fragmentation kills big trees. Nature 404: 836.
Laurance, W.F.; Fernside, P.M.; Nascimento, H.E.M.; Laurance, G., Andrade, A.C.; Ribeiro, E.L. & Capretz, R.L. 2006. Rain forest fragmentation
and the proliferation of successional trees. Ecology 87(2): 469–482.
Lista de Espécies da Flora do Brasil. Jardim Botânico do Rio de Janeiro.
2013. Available from: http://floradobrasil.jbrj.gov.br. Cited 2013 Apr 03.
Lopes, A.V.; Girão, L.C.; Santos, B.A.; Peres, C.A. & Tabarelli, M. 2009.
Long-term erosion of tree reproductive trait diversity in edge-dominated
Atlantic forest fragments. Biological Conservation 142: 1154–1165.
Lorenzi, H. 2002a. Árvores Brasileiras: manual de identificação e cultivo
de plantas arbóreas do Brasil, v. 1. São Paulo, Nova Odessa.
Lorenzi, H. 2002b. Árvores Brasileiras: manual de identificação e cultivo
de plantas arbóreas do Brasil, v. 2. São Paulo, Nova Odessa.
Lorenzi, H. 2010. Árvores Brasileiras: manual de identificação e cultivo de
plantas arbóreas do Brasil, v. 3. São Paulo, Nova Odessa.
Maack, R. 2012. Geografia física do estado do Paraná. 4th ed. Ponta
Grossa, Editora UEPG.
Meyer, H.A. 1952. Structure, growth and drain in balanced uneven-aged
forest. Journal of Forestry 50: 85-92.
Mori, S.A.; Mattos-Silva, L.A.; Lisboa, G. & Coradin, L. 1989. Manual de
manejo do herbário fanerogâmico. 2nd ed. Ilhéus, CEPLAC.
Nunes, Y.R.F.; Mendonça, A.V.R.; Botezelli, L.; Machado, E.L.M. & Oliveira-Filho, A.T. 2003. Variações da fisionomia, diversidade e composição
de guildas da comunidade arbórea em um fragmento de Floresta
Semidecidual em Lavras, MG. Acta Botanica Brasilica 17(2): 213-229.
576
Oliveira, M.A.; Grillo, A.S. & Tabarelli, M. 2004. Forest edge in the Brazilian Atlantic forest: drastic changes in tree species assemblages. Oryx
38: 389–394.
Oliveira, M.A.; Santos, A.M.M. & Tabarelli, M. 2008. Profound impoverishment of the large-tree stand in a hyper-fragmented landscape of the
Atlantic forest. Forest Ecology and Management 256: 1910–1917.
Prado-Júnior, J.A.; Vale, V.S.; Oliveira, A.P.; Gusson, A.E.; Neto, O.C.D.; Lopes,
S.F. & Schiavini, I. 2011. Estrutura da comunidade arbórea em um fragmento de Floresta Estacional Semidecidual, localizada na reserva legal
da Fazenda Irara, Uberlândia, MG. Bioscience Journal 26(4): 638-647.
R Core Team. 2013. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available
from: http://www.R-project.org/. Cited 2013 Aug 02.
Ramos, V.S.; Durigan, G.; Franco, G.A.D.C.; Siqueira, M.F. & Rodrigues,
R.R. 2008. Árvores da Floresta Estacional Semidecidual. Guia de
identificação de espécies. São Paulo, EDUSP – FAPESP.
Ribas, L.L.F.; Zanette, F.; Kulchetscki, L. & Guerra, M.P. 2003. Estabelecimento de culturas assépticas de Aspidosperma polyneuron. Ciência
Florestal 13(1): 115-122.
Ribeiro, M.C.; Metzger, J.P.; Martensen, A.C.; Ponzoni, F.J. & Hirota, M.M.
2009. The Brazilian Atlantic Forest: how much is left, and how is the
remaining forest distributed? Implications for conservation. Biological
Conservation 142: 1141–1153.
Rodrigues, R.R. & Gandolfi, S. 2004. Conceitos, Tendências e Ações para
a Recuperação de Florestas Ciliares. Pp. 235-247. In: Rodrigues, R.R.
& Leitão-Filho, H.F. (Eds.). Matas Ciliares: Conservação e Recuperação. São Paulo, EDUSP – FAPESP.
Salamuni, R.; Salamuni, E.; Rocha, L.A. & Rocha, A.L. 2002. Parque
Nacional do Iguaçu, PR – Cataratas de fama mundial. Pp. 313-312.
In: Schobbenhaus, C.; Campos, D.A.; Queiroz, E.T.; Berbert-Born,
M.L.C. (Eds.). Sítios Geológicos e Paleontológicos do Brasil.
Brasília, DNPM/CPRM - Comissão Brasileira de Sítios Geológicos e
Paleobiológicos (SIGEP).
Santos, L.J.C.; Oka-Fiori, C.; Canali, N.E.; Fiori, A.P.; Silveira, C.T.; Silva,
J.M.F. & Ross, J.L.S. 2006. Mapeamento geomorfológico do Estado do
Paraná. Revista Brasileira de Geomorfologia 7: 3-11.
Santos, B.A.; Peres, C.A.; Oliveira, M.A.; Grillo, A.; Alves-Costa; C.P. &
Tabarelli, M. 2008. Drastic erosion in functional attributes of tree
assemblages in Atlantic forest fragments of northeastern Brazil. Biological Conservation 141: 249–260.
Shepherd, G.J. 2010. FITOPAC 2.1.2: Manual do usuário. Campinas,
UNICAMP.
Silva, N.R.S.; Martins, S.V.; Meira-Neto, J.A.A. & Souza, A.L. 2004. Composição florística e estrutura de uma floresta estacional semidecidual
montana em Viçosa, MG. Revista Árvore 28(3): 397-405.
SIMEPAR- Sistema Meteorológico do Paraná, 2011. Daily data of rainfall
and temperature for the town of Foz do Iguaçu for the period of
01/01/2010 to 01/01/2011.
Soares, C.P.B.; Paula-Neto, F.; Souza, A.L. 2006. Dendrometria e inventário
florestal. Viçosa, Editora UFV.
Tanizaki-Fonseca, K. & Moulton, T.P. 2000. A fragmentação da Mata
Atlântica no Estado do Rio de Janeiro e a perda de biodiversidade.
Pp. 23-35. In: Bergallo, H. G., Rocha, C. F. D., Alves, M. A. S. & Sluys
M. V. (Eds.). A fauna ameaçada de extinção do Estado do Rio de
Janeiro. Rio de Janeiro, Editora UERJ.
Veloso P.H.P.; Rangel Filho, A.L.R.R. & Lima, J.C.A. 1991. Classificação
da Vegetação Brasileira, Adaptada a um Sistema Universal. Rio
de Janeiro, IBGE – Departamento de Recursos Naturais e Estudos
Ambientais.
Villela, D.M.; Nascimento, M.T.; Aragão, L.E.O.C. & Gama, D.M. 2006.
Effect of selective logging on forest structure and nutrient cycling in
a seasonally dry Brazilian Atlantic forest. Journal of Biogeography
33: 506-516.
Wilson, E.O. 1997. A situação atual da diversidade biológica. Pp. 3-24.
In: Wilson E.O. & Peter, F.M. (Eds.). Biodiversidade. Rio de Janeiro,
Nova Fronteira.
Young, T.P. & Hubbell, S.P. 1991. Crown asymmetry, treefalls, and repeat
disturbance of broad-leaved forest gaps. Ecology 72(4): 1464-1471.
Zar, J.H. 1999. Biostatistical analysis. 4th ed. New Jersey, Prentice-Hall.
Acta bot. bras. 28(4): 569-576. 2014.