Biodivers Conserv (2011) 20:1921–1949
DOI 10.1007/s10531-011-0067-3
ORIGINAL PAPER
Tree changes in a mature rainforest with high diversity
and endemism on the Brazilian coast
Felipe Zamborlini Saiter • Frederico Augusto Guimarães Guilherme
Luciana Dias Thomaz • Tânia Wendt
•
Received: 17 October 2010 / Accepted: 5 May 2011 / Published online: 18 May 2011
Ó Springer Science+Business Media B.V. 2011
Abstract The tree changes of 1.02 ha of montane forest at the Santa Lúcia Biological
Station, southeastern Brazil, were analyzed using two surveys separated by an interval of
11 years with the aim of confirming the patterns of stability of structure and diversity over
time. In the original survey all trees with diameter at breast height C6.4 cm were sampled.
In second survey (this study), dead trees, survivors and recruits in the same forest were
reported. The data suggest a dynamic balance of the forest structure because mortality
(-1.06% year-1 for number of trees and -0.85% year-1 for basal area) was very close to
recruitment (0.89% year-1) and ingrowth (1.05% year-1). The high diversity of the original survey (H0 [ 5.2) was maintained by the turnover species. The main tree populations
also showed stability of number of trees and basal area. This pattern was shared by most of
the 28 local endemic species, ensuring the maintenance of their populations in the plot.
Keywords Tree mortality Tree recruitment Turnover Forest stability
Atlantic rainforest
F. Z. Saiter (&)
Instituto Federal de Educação, Ciência e Tecnologia do Espı́rito Santo, Campus Santa Teresa,
Rodovia ES 080, km 21, Santa Teresa, ES 29660-000, Brazil
e-mail: fsaiter@ifes.edu.br
F. A. G. Guilherme
Departamento de Ciências Biológicas, Universidade Federal de Goiás,
Campus Jataı́, Rodovia BR 364, km 192, Jataı́, GO 75801-615, Brazil
L. D. Thomaz
Departamento de Ciências Biológicas, Universidade Federal do Espı́rito Santo,
Avenida Fernando Ferrari, 514, Vitória, ES 29075-900, Brazil
T. Wendt
Departamento de Botânica, IB, Universidade Federal do Rio de Janeiro,
Rio de Janeiro, RJ 21941-590, Brazil
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Introduction
Mature forests are ecosystems with a recognized ability to maintain both structure and
floristic diversity stable over time through the dynamic balance of mortality, recruitment and
growth of plants (Stephenson and van Mantgem 2005). This balance is based on the growth
cycle of the forests, which consists of three phases of development according to Whitmore
(1988): mature, gap and building. The mature phase has mature trees in various layers and a
closed canopy. Eventually canopy trees die or are damaged, knocking down the smaller trees
surrounding them and forming gaps. In a short time, these gaps are filled with herbs, climbers
and treelets which can arise from exposed roots and stumps or a bank of seeds and seedlings.
The building phase corresponds to the growth of plants until the formation of a new canopy
after many years, restoring the mature stage and all its layers (Whitmore 1988).
The turnover rate (the average of tree mortality and recruitment rate) is important data
that has been used with success to summarize the dynamism of forests. In the case of
tropical forests (admittedly more productive than temperate forests), the turnover rates are
higher because the dynamic balance is accelerated, making losses that are offset by gains
more quickly (Rees et al. 2001; Stephenson and van Mantgem 2005).
In the tropics, long-term research projects that monitor dynamic processes in permanent
sample plots have become a central theme in forest ecology in recent years because they
represent an appropriate strategy for gaining an understanding of how tropical forests maintain
their high diversity and how they are affected by global climate patterns (Picard et al. 2010).
Based on these projects, ecologists recognize that treefall gap dynamics is the key process
which maintains diversity in forests (Rees et al. 2001; Machado and Oliveira-Filho 2010) and
atmospheric changes, such as the increasing CO2 concentration and periods of drought and
intense heat, have made tropical forests more dynamic and changed their composition (Phillips
1996; Lewis et al. 2004a; Laurance et al. 2009; Lingenfelder and Newbery 2009).
The Atlantic rainforest is one of the Earth’s biologically richest and most endangered
terrestrial ecoregions (Mittermeier et al. 2004). In Brazil, the Atlantic rainforest has been
severely damaged during the last 50 years; the few remaining areas are covered by mature
forest and are mostly confined to protected areas (Ribeiro et al. 2009). Some of these areas
have already received initial phytosociological studies, but permanent sample plots and
monitoring of floristic composition and structure have only been maintained in a few. In
reflection of this, only the studies of Melo et al. (2000) and Rolim et al. (2005) have
reported on mature forests of the Brazilian coastline.
This study aims to analyze the changes of the community and the populations of trees
and tree palms in a mature forest on the Brazilian coast using two surveys separated by an
interval of 11 years to confirm the patterns of structure and diversity maintenance over
time, as observed in mature tropical forests. The factors that motivated the realization of
the present study were the lack of research on forest dynamics in the Atlantic rainforest, the
great ecological diversity found in the original survey (one of the highest diversity indexes
ever recorded in the world) and the description of many new and locally endemic species
from botanical materials collected in there since the installation of fotest permanent plots.
Methods
Study site
The Santa Lúcia Biological Station (SLBS) is a small protected area (467.89 ha)
located in Santa Teresa, the montane region of Espı́rito Santo state, southeastern Brazil
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Fig. 1 Location of the Santa
Lúcia Biological Station in the
montane region of the Espı́rito
Santo state, southeastern Brazil
(19°570 1200 –19°590 1000 S; 40°310 1300 –40°320 3200 W, see Fig. 1). The SLBS is supported by
the Museu de Biologia Prof. Mello Leitão and the Universidade Federal do Rio de Janeiro,
but it is not a legally recognized conservation unit. Nevertheless, the SLBS plays an
important role in the fragmented landscape of the region, contributing to the connection (at
least functional) between small surrounding forest fragments (maximum of 100 ha) and the
Augusto Ruschi Biological Reserve (3573 ha), the main protected area in the region.
Recently, important taxonomic and ecology research was undertaken in the SLBS which
identified new plant species of the Atlantic rainforest. Besides this, several research projects
have recorded high levels of local biodiversity in this region (Mendes and Padovan 2000).
The climate is Cfa, according to the Köppen classification, with rainy summers and dry
winters. The average annual temperature at the site is 20°C and the average annual rainfall
(influenced by orographic rainfall) is 1868 mm. November is the wettest month and June is
the only month of the year with precipitation below 60 mm (Mendes and Padovan 2000).
The relief is very undulating forming a valley with several streams that contribute to the
river Timbuı́. There are extensive rocky outcrops at altitudes from 600 to 900 masl.
Shallow dystrophic soil with a high acidity, high levels of exchangeable Al and a low base
saturation dominates the region (Thomaz and Monteiro 1997). According to the classification of the Instituto Brasileiro de Geografia e Estatı́stica (1992), the predominant vegetation is montane rainforest (500–1500 m in altitude).
Study design and forest surveys
The whole sample stand comprises 1.02 ha and was installed in 1992–1993 during the
initial survey of trees and tree palms with a diameter at breast height (dbh) C6.4 cm. The
stand is located on the northeast side of a slope to the right of the bank of the river Timbuı́,
at 650–850 m high, and is subdivided into three transects of 0.34 ha (see Fig. 1) composed
of 34 contiguous permanent plots 100 m2 (10 9 10 m). Transect 1 is at 650–660 m,
transect 2 is at 675–700 m, and transect 3 is at 820–850 m high (Thomaz and Monteiro
1997). In transect 1 the sequence of quadrats was interrupted due to the dense cluster of
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Merostachys sp. new, a woody bamboo species. Because of this, 10 plots were installed
before this cluster and 24 plots were installed after. The stand is not disturbed by flooding
and there are no reports of human disturbance.
In the second survey (this study), carried out between 2003 and 2004, the dead trees,
survivors and recruits were reported. Recruits were considered as trees which had reached
the minimum dbh after 11 years. Moreover, great effort was expended in the last 5 years to
revise and update the floristic list published by Thomaz and Monteiro (1997), which was
composed of 443 species but more than a half of them (54%) were without a complete
identification due to incipient knowledge of the regional flora at that time. For this, taxonomists and the herbarium collections of the Museu de Biologia Mello Leitão Herbarium
(MBML), the Universidade Federal do Espı́rito Santo Herbarium (VIES), the Jardim
Botânico do Rio de Janeiro Herbarium (RB), the Universidade Federal do Rio de Janeiro
Herbarium (RFA), the Missouri Botanical Garden Herbarium (MO) and the New York
Botanical Garden Herbarium (NY) were consulted.
The result of this review was the recognition of 385 species, with only 20% without
complete identification yet (see Table 6 in Appendix). It is noteworthy that 28 of these
species were described as new to science using botanical materials collected in the SLBS
and in its surroundings, and their geographical distributions are only assigned to Santa
Teresa and some adjacent municipalities (totaling only about 3000 km2).
Although the stand design is not ideal, in the present study the three transects were
combined into a single plot. This was enabled by the small distance between transects, the
similarity of soil samples (for details see Thomaz and Monteiro 1997), the small difference
between the richness of the transects in the original survey (208, 203 and 211 species in
transects 1, 2 and 3, respectively), and the high similarity index between the transects
(Sørensen index C0.5, F. Z. Saiter, non-published data).
Data analysis
The Shannon diversity index (H0 ) and the evenness index (J) were calculated for the
original and second surveys according to Magurran (1988). The diversity t test was applied
using the free software PAST (developed by Øyvind Hammer of the University of Oslo and
collaborators; Hammer et al. 2001) to identify possible differences of H0 between surveys
(P B 0.05).
In regard to parameters of forest structure (number of trees and basal area), possible
differences between the two surveys was tested using the Wilcoxon’s signed-rank test
(two-tailed; P B 0.05) according to Zar (1999). This test was applied using the free
software BioEstat 5.0 (developed by Manuel Ayres of the Universidade Federal do Pará
and collaborators; Ayres et al. 2007).
Assuming that changes of communities and tree populations over time are a constant
proportion of their initial conditions, we calculated average annual rates of change (r)
using the exponential equation described by Korning and Balslev (1994):
r ¼ ðCt = C0 Þ1=t 1
For the analysis of the community, r means the average annual rate of death (when r \ 0)
or recruitment/ingrowth (where r [ 0) and C0 is the number of trees or the basal area in the
original survey; Ct is the number or basal area of trees surviving in the second survey
(Ct = C0 - dead trees), in the case of death/loss, and the initial number of trees added by the
number of recruits (Ct = C0 ? recruited trees), in the case of recruitment or the basal area
increasing from initial recruitment and growth of survivors (Ct = C0 ? recruits ? growth
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of survivors trees) in the case of ingrowth/gain. For change (r) of each population, t is the
period of time in years between the two surveys, C0 is the size of the population in the original
survey and Ct is the size of the population after t years.
The average rate of annual turnover (rate at which trees that die are replaced by recruits)
was calculated from the average of the rates of mortality and recruitment. Turnover was
applied to both number of trees and basal area (as in the method of Oliveira-Filho et al. 1997).
Furthermore, based on the rates of mortality, recruitment and ingrowth, values in years of
half-life (t) and doubling time (t2) were obtained, which are, respectively: the time in which
the community will reduce by half (keeping up the rates of mortality), and the time that the
community will double (keeping up the rates of recruitment and ingrowth). According to
Korning and Balslev (1994) the logarithmic expressions for these parameters are:
t1=2 ¼ ln ð0:5Þ=ln ð1 þ rÞ and t2 ¼ ln ð2Þ=ln ð1 þ rÞ
The turnover time and stability time in years were obtained from the mean of t and t2,
and the numerical difference between them, respectively. The turnover time is defined as
the time in years required for the total renovation of the cover in a sample of forest. The
turnover of species and families were presented by the number of species and families
recruited and absent in the second survey.
After the calculations for populations, species were sorted by importance value (IV) in
the second survey, which was obtained from the sum of relative density, relative dominance and relative frequency of each species (Mueller-Dombois and Ellenberg 1974).
The following intervals were used for the analysis of community changes by dbh
classes: 6.4–10, 10–20, 20–40, 40–80 and [80 cm. The classes had increasing intervals in
order to compensate the small number of trees which had dbh[30 cm. For each dbh class,
the number of trees subjected to the following events was obtained: death, ingrowth (given
by the entry of trees into a class by recruitment and growth) and outgrowth (given by the
output of trees of a class by growth). The variations in the rates of mortality, outgrowth and
ingrowth among the dbh classes were tested using the Kolmogorov–Smirnov test (one
sample; P B 0.05) according to Zar (1999).
For analysis of changes of populations the annual rates of change (r), which were
obtained as described above, were classified in thirteen classes (100%; [12 to 24%; [6 to
12%;[3 to 6%;[1.5 to 3%;[0 to 1.5%; 0%;\0 to -1.5%;\-1.5 to -3%;\-3 to -6%;
\-6 to -12%;\-12 to -24%; -100%). The classes ‘100%’ and ‘-100%’ correspond to
recruits and absent species in the second survey, respectively. Spearman’s rank correlation
test (rs; P B 0.05) was used for to identify correlation between annual rates of change and
number of trees recorded for the species which showed changes after 11 years.
The Kolmogorov–Smirnov and the Spearman’s rank correlation tests were carried out
by the software BioEstat 5.0 (Ayres et al. 2007).
Results
Community
Table 1 summarizes the community changes between 1992–1993 and 2003–2004. The
number of trees in 2003–2004 is close to the number of trees in 1992–1993. The difference
in number of trees between the two surveys was small and non-significant (T = 1794;
P = 0.39) because mortality was just a bit higher than recruitment, with 242 dead trees and
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Table 1 Summary of the community changes in 1.02 ha of montane rainforest at the Santa Lúcia Biological Station, Espı́rito Santo, southeastern Brazil. Data were obtained from forest surveys carried out in
1992–1993 (Thomaz and Monteiro 1997) and 2003–2004 (this study)
1992–1993
2003–2004
Loss/Dead
Gain/ingrowth
Survivor
Species
385
384
15
14
370
Families
64
63
2
1
62
Trees
2190
2173
242
225
1948
Basal area (m2)
47.94
49.47
4.28
0.96
48.51
H0
5.27
5.22
J
0.89
0.88
Table 2 Parameters of community changes obtained from forest surveys carried out in 1992–1993
(Thomaz and Monteiro 1997) and 2003–2004 (this study) in 1.02 ha of montane rainforest at the Santa
Lúcia Biological Station, Espı́rito Santo, southeastern Brazil
-1
Mortality rate (% year )
Number of trees
Basal area
-1.06
-0.85
Recruitment rate (% year-1)
0.89
1.05
Turnover rate (% year-1)
0.98
0.95
65.11
81.44
Double time (year)
77.96
66.61
Turnover time (year)
71.54
74.02
Stability time (year)
12.85
14.83
Half life (year)
225 recruits accounted after 11 years. These numbers resulted in average annual rates of
mortality and recruitment being very close and an average annual turnover rate of
0.98% year-1, as shown in Table 2. The basal area increased by 1.53 m2 (0.20% year-1),
but the difference between the two surveys was non-significant (T = 2179; P = 0.14). In
total values, the contribution of the basal area increment by recruits (0.96 m2) was about
five times lower than the growth of survivors (4.85 m2), which would be expected since the
recruitment group was composed of trees with a smaller dbh and the surviving group had
the largest number of trees. The community also showed a very close turnover time and
stability time for both periods for the number of trees and the basal area.
The tree richness changed little after 11 years. Of the 385 species in 1992–1993 (number
obtained after reviewing the list of 443 species originally recorded by Thomaz and Monteiro
1997, see Table 6 in Appendix), 15 had disappeared in 2003–2004. However, 14 new species
were recorded as recruits in 2003–2004 (Table 1). The absent species and the recruited
species each had a low abundance (never more than four trees) and are listed in Table 3. For
the families Solanaceae and Winteraceae, which were represented by only one species each
(Solanum sooretamum and Drimys brasiliensis, respectively) in 1992–1993, were absent in
2003–2004, while the family Linaceae was recorded for the first time with the occurrence of
Roucheria cf. dryadica. Melastomataceae was the family with the largest number of
recruited species while Myrtaceae had the largest number of absent species.
The high ecological diversity of the original survey (H0 [ 5.2) was maintained
(t = 1.189; P = 0.23; non-significant), confirming that the SLBS forest has one of the
highest diversity indices recorded in the world. The evenness index, greater than 0.8 in
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Table 3 Absent and recruited tree species in 1.02 ha of montane rainforest at the Santa Lúcia Biological
Station, Espı́rito Santo, southeastern Brazil, 11 years after the forest survey of Thomaz and Monteiro (1997)
Families
Species absent 2003–2004
ND
Annonaceae
Rollinia laurifolia
1
Aquifoliaceae
Ilex amara
1
Urticaceae
Pourouma bicolor
1
Celastraceae
Salacia nemorosa
1
Erythroxylaceae
Erythroxylum cuspidifolium
1
Euphorbiaceae
Croton floribundus
1
Lauraceae
Licaria guianensis
2
Melastomataceae
Miconia doriana
1
Myrtaceae
Eugenia neoglomerata
1
Myrtaceae
Myrcia pubipetala
2
Myrtaceae
Myrcia racemosa
1
Myrtaceae
Siphoneugena dussii
2
Salicaceae
Banara serrata
4
Solanaceae
Solanum sooretamum
1
Winteraceae
Drimys brasiliensis
1
Families
Species recruited 2003–2004
NR
Annonaceae
Anaxagorea dolichocarpa
1
Annonaceae
Annona cacans
1
Lauraceae
Aniba firmula
2
Lauraceae
Ocotea indecora
2
Melastomataceae
Miconia longicuspis
1
Melastomataceae
Miconia sellowiana
1
Melastomataceae
Miconia sp. new
2
Melastomataceae
Miconia tristis
2
Myrtaceae
Eugenia sp5 new
1
Myrtaceae
Eugenia melanogyna
1
1
Linaceae
Roucheria cf. dryadica
Proteaceae
Panopsis sp.
1
Sapindaceae
Talisia sp.
1
Vochysiaceae
Qualea gestasiana
2
Survey held in 2003–2004 (present study)
ND number of dead species, NR number recruited
both surveys, showed a good uniformity of individual distribution in relation to species.
Indeed, in both surveys just over 70% of species were represented by up to five trees.
Diameter classes
The changes of the community by dbh class are shown in Table 4. The recruits were
almost entirely in the 6.4–10 cm class, with a few occurring in the 10–20 cm class (but
these were no larger than 13.7 cm). The 20–40 cm class accumulated the greatest basal
area, but the largest increase of basal area was in the 40–80 cm class (about 1 m2).
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Table 4 Changes of tree community by diameter class (dbh) in 1.02 ha of montane rainforest at the Santa
Lúcia Biological Station, Espı́rito Santo, southeastern Brazil, surveyed in 1992–1993 (Thomaz and Monteiro
1997) and 2003–2004 (this study)
Dbh classes (cm)
Trees
Deads
Outgrowth
Recruits ? Ingrowth
BA (m2)
6.4–10
10–20
20–40
40–80
[80
Totals
1992–1993
925
880
348
36
1
2190
2003–2004
900
881
349
42
1
2173
Change
-25
1
1
6
0
-17
NT
109
94
38
1
0
242
% year-1
-1.13
-1.02
-1.05
NT
136
52
10
% year-1
-1.44
-0.55
-0.26
-0.26
0.00
-0.86
NT
216
9
0
0
0
225
4
138
49
199
-0.26
1
0.00
-1.06
0
199
8
0
% year-1
1.96
1.41
1.20
1.84
0.00
1.62
1992–1993
4.68
13.73
20.14
7.96
1.43
47.94
2003–2004
4.55
13.81
20.69
8.99
1.44
49.47
KS
0.33 ns
0.27 ns
0.26 ns
NT number of trees, BA basal area, KS Kolmogorov–Smirnov test (one sample), ns non-significant at
P B 0.05
Fig. 2 Distribution of the number of species per classes of annual rates of change, in number of trees (NT),
after 11 years in 1.02 ha of montane rainforest at the Santa Lúcia Biological Station, Espı́rito Santo,
southeastern Brazil. The classes ‘100%’ and ‘-100%’ correspond to recruits and absent species in the
second survey, respectively
Mortality did not occur in the [80 cm class since this class was represented by only one
live tree of Caryocar edule in both surveys. The variations in the rates of mortality,
outgrowth and ingrowth among classes were not significant and, in general, the decline in
the number of trees in a class was accompanied by a decrease in basal area.
Populations
In general, the size of the populations changed little because 56% of species maintained the
same number of trees and 26% showed annual rates B3% after 11 years (see Fig. 2).
Within the group of 169 species which changed in the number of trees, the annual rates of
change were negatively correlated to the number of individuals (rs = -0.885;
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Fig. 3 Distribution of the number of species per classes of annual rates of change, in basal area (BA), after
11 years in 1.02 ha of montane rainforest at the Santa Lúcia Biological Station, Espı́rito Santo, southeastern
Brazil. The classes ‘100%’ and ‘-100%’ correspond to recruits and absent species in the second survey,
respectively
P \ 0.0001). With respect to the basal area, the annual rates of change were small and
positive (between 0 and 3%) in most species (see Fig. 3).
The population changes of the 100 species with the highest importance values (IV) are
presented in Table 5. These species were responsible for 66% of the trees and about 72.5%
of the total basal area in both surveys.
The palm tree Euterpe edulis was the most abundant species in the community and
showed a remarkable imbalance in favor of recruitment, which resulted in an increase of 34
individuals in its population. Ocotea aciphylla, Eriotheca macrophylla, Unonopsis sanctateresae, Ecclinusa ramiflora and Mezilaurus sp. (new species) were others abundant
species of the community. But they did not show major changes in their populations,
following the pattern of most species (see Table 5).
Unonopsis sancta-teresae and Mezilaurus sp. (new species) are distinguished as local
endemic species. Twenty-six other local endemic species were recorded in plot, but the
size of their populations did not differ much in original and second surveys (see Fig. 4).
Endemic species with special situations were Salacia nemorosa, which was absent in
second survey due to the death of a single tree, and Miconia sp. (new species) and Eugenia
sp. 5 (new species) which were recruited.
Ocotea cryptocarpa, Ocotea odorifera and Maytenus obtusifolia presented negative
growth of basal area, because there was decay of some stems of trees with multiple stem.
Ocotea aciphylla presented the largest growth of survivors and had a positive change of
basal area, even with the decrease in the number of trees. Several others populations also
showed positive changes of basal area and negative changes in number of trees. Caryocar
edule although represented by only two trees had the largest total basal area (1.762 m2).
Vochysia rectiflora showed the greatest loss in basal area (0.349 m2), a fact attributed to
the death of only two trees of great size.
Discussion
Community
The data suggest stability of the forest in SLBS after a period of 11 years as a dynamic
balance was found between the losses and gains of trees and basal areas which corresponds
123
Species
IV
Number of trees
1992–1993
D
R
2003–2004
Change
(% year-1)
Basal area
1992–1993
Loss
Gain
2003–2004
Change
(% year-1)
16.62
168
18
52
202
1.69
1.262
0.147
0.333
1.448
Ocotea aciphylla
8.78
85
13
5
77
-0.89
1.079
0.065
0.225
1.240
1.27
Eriotheca macrophylla
7.57
53
8
5
50
-0.53
1.524
0.171
0.154
1.507
-0.10
Euterpe edulis
1930
123
Table 5 Population changes of the 100 species of highest importance value after the second survey in 1.02 ha of montane rainforest at the Santa Lúcia Biological Station,
Espı́rito Santo, southeastern Brazil
1.26
Ecclinusa ramiflora
5.20
41
2
2
41
0.00
0.753
0.027
0.086
0.813
0.70
Unonopsis sancta-teresae
4.55
45
4
3
44
-0.20
0.373
0.041
0.037
0.369
-0.10
4.15
41
2
1
40
-0.22
0.588
0.034
0.012
0.565
-0.36
4.02
21
4
2
19
-0.91
0.930
0.048
0.181
1.063
1.22
Vantanea obovata
4.01
19
1
0
18
-0.49
1.148
0.017
0.058
1.189
0.32
Caryocar edule
3.76
2
0
0
2
0.00
1.743
0.000
0.019
1.762
0.10
Guapira opposita
3.48
26
4
6
28
0.68
0.500
0.121
0.126
0.505
0.09
Virola gardneri
3.40
13
0
2
15
1.31
0.874
0.000
0.081
0.955
0.81
Guapira obtusata
3.30
26
5
5
26
0.00
0.424
0.048
0.085
0.461
0.76
Beilschmiedia taubertiana
3.08
17
0
1
18
0.52
0.634
0.000
0.041
0.676
0.58
Inga capitata
2.99
22
0
3
25
1.17
0.251
0.000
0.056
0.306
1.84
Micropholis venulosa
2.91
15
0
0
15
0.00
0.609
0.000
0.104
0.712
1.44
Pseudoxandra spiritus-sancti
2.90
14
2
1
13
-0.67
0.749
0.012
0.070
0.807
0.68
Guapira venosa
2.83
20
3
6
23
1.28
0.315
0.057
0.068
0.326
0.32
Ocotea sp3
2.54
17
0
0
17
0.00
0.431
0.000
0.078
0.509
1.52
Ormosia cf. friburgensis
2.43
16
3
1
14
-1.21
0.556
0.037
0.036
0.555
-0.02
Ocotea cryptocarpa
2.43
16
2
1
15
-0.58
0.593
0.149
0.004
0.448
-2.51
Sloanea guianensis
2.43
17
1
0
16
-0.55
0.479
0.015
0.040
0.505
0.49
Ocotea divaricata
2.42
12
1
0
11
-0.79
0.618
0.003
0.030
0.645
0.39
Siparuna glossostyla
2.37
17
1
5
21
1.94
0.202
0.019
0.071
0.254
2.10
Biodivers Conserv (2011) 20:1921–1949
Mezilaurus sp. new
Coussapoa microcarpa
Species
IV
Number of trees
1992–1993
D
R
2003–2004
Change
(% year-1)
Basal area
1992–1993
Loss
Gain
2003–2004
Change
(% year-1)
Myrcia laurifolia
2.17
19
1
1
19
0.00
0.191
0.007
0.017
0.201
0.45
Hirtella hebeclada
2.17
14
0
1
15
0.63
0.373
0.000
0.056
0.429
1.27
Trichilia lepidota
2.16
12
2
1
11
-0.79
0.532
0.018
0.028
0.542
0.18
Micropholis guyanensis
2.14
12
0
0
12
0.00
0.465
0.000
0.075
0.539
1.37
Psychotria sessilis
2.11
13
0
2
15
1.31
0.278
0.000
0.096
0.374
2.74
Pouteria sp2
2.10
16
3
0
13
-1.87
0.506
0.098
0.007
0.415
-1.79
Ocotea catharinensis
2.03
18
3
1
16
-1.07
0.330
0.072
0.079
0.338
0.20
Licania micrantha
1.98
14
2
0
12
-1.39
0.332
0.019
0.065
0.378
1.19
Pouteria aff. reticulata
1.97
16
1
0
15
-0.58
0.241
0.005
0.038
0.274
1.17
Maytenus cestrifolia
1.96
15
3
7
19
2.17
0.070
0.016
0.036
0.094
2.75
Diplotropis incexis
1.95
15
1
0
14
-0.63
0.347
0.084
0.023
0.286
-1.74
Eugenia aff. pruniformis
1.91
9
0
0
9
0.00
0.466
0.000
0.026
0.492
0.50
Swartzia apetala
1.89
14
1
0
13
-0.67
0.281
0.019
0.018
0.280
-0.04
Roupala consimilis
1.82
17
3
0
14
-1.75
0.207
0.023
0.041
0.225
0.78
Myrsine umbellata
1.80
11
2
1
10
-0.86
0.490
0.130
0.026
0.386
-2.13
Trichilia silvatica
1.79
13
0
1
14
0.68
0.193
0.000
0.015
0.208
0.68
Eugenia acutata
1.71
14
1
0
13
-0.67
0.239
0.024
0.031
0.245
0.25
Manilkara cf. longifolia
1.69
9
0
0
9
0.00
0.340
0.000
0.043
0.383
1.08
Geonoma schottiana
1.68
16
3
5
18
1.08
0.055
0.010
0.017
0.063
1.23
Trichilia sp. new
1.66
13
3
0
10
-2.36
0.454
0.106
0.025
0.373
-1.77
1.64
13
3
2
12
-0.73
0.248
0.045
0.084
0.291
1.44
1.64
11
0
0
11
0.00
0.254
0.000
0.032
0.285
1.08
Lacistema robustum
1.60
12
0
4
16
2.65
0.135
0.000
0.044
0.180
2.61
Amaioua intermedia
1.57
12
2
1
11
-0.79
0.194
0.008
0.035
0.221
1.18
1931
123
Vochysia santaluciae
Ocotea corymbosa
Biodivers Conserv (2011) 20:1921–1949
Table 5 continued
1932
123
Table 5 continued
Species
IV
Number of trees
1992–1993
D
R
2003–2004
Change
(% year-1)
Basal area
1992–1993
Loss
Gain
2003–2004
Change
(% year-1)
Attalea burretiana
1.52
6
0
0
6
0.00
0.443
0.000
0.008
0.451
Pouteria sp1
1.51
15
0
0
15
0.00
0.097
0.000
0.007
0.105
0.16
0.67
Mouriri cf. regeliana
1.50
5
0
1
6
1.67
0.446
0.000
0.022
0.468
0.44
Pouteria bangii
1.47
6
0
2
8
2.65
0.268
0.000
0.055
0.323
1.71
Tovomita leucantha
1.45
12
2
2
12
0.00
0.188
0.071
0.023
0.141
-2.63
1.38
13
4
1
10
-2.36
0.394
0.208
0.049
0.236
-4.56
1.37
10
0
0
10
0.00
0.176
0.000
0.027
0.203
1.32
Byrsonima variabilis
1.36
11
1
1
11
0.00
0.166
0.013
0.023
0.176
0.53
Tetrastylidium grandifolium
1.33
10
0
0
10
0.00
0.179
0.000
0.032
0.211
1.52
Elvasia capixaba
1.31
13
3
0
10
-2.36
0.249
0.093
0.018
0.174
-3.23
Parinari obtusifolium
1.30
4
0
0
4
0.00
0.422
0.000
0.023
0.444
0.48
Marlierea obscura
1.29
4
0
0
4
0.00
0.393
0.000
0.070
0.463
1.51
Beilschmiedia sp.
1.28
9
0
0
9
0.00
0.167
0.000
0.014
0.181
0.76
Sparattanthelium botocudorum
1.23
3
0
0
3
0.00
0.421
0.000
0.038
0.459
0.80
Schefflera calva
1.21
4
0
0
4
0.00
0.355
0.000
0.042
0.396
1.02
Maytenus obtusifolia
1.21
12
2
0
10
-1.64
0.190
0.044
0.000
0.149
-2.20
-1.92
Ocotea odorifera
1.19
10
2
0
8
-2.01
0.230
0.044
0.000
0.185
Hirtella angustifolia
1.18
10
2
0
8
-2.01
0.192
0.019
0.034
0.207
0.68
Hymenaea aurea
1.14
8
0
0
8
0.00
0.199
0.000
0.016
0.214
0.69
-0.28
Myrcia plusiantha
1.12
10
2
0
8
-2.01
0.187
0.019
0.013
0.181
Chrysophyllum splendens
1.12
11
1
0
10
-0.86
0.134
0.007
0.008
0.136
0.10
Citronella paniculata
1.11
6
1
0
5
-1.64
0.299
0.003
0.004
0.299
0.02
Micropholis sp.
1.07
5
1
0
4
-2.01
0.322
0.000
0.000
0.328
0.18
Barnebya dispar
1.06
9
1
0
8
-1.07
0.167
0.056
0.013
0.124
-2.66
Biodivers Conserv (2011) 20:1921–1949
Coussapoa pachyphylla
Sorocea guilleminiana
Species
IV
Number of trees
1992–1993
D
R
2003–2004
Change
(% year-1)
Basal area
1992–1993
Loss
Gain
2003–2004
Change
(% year-1)
Casearia commersoniana
1.06
7
0
1
8
1.22
0.109
0.000
0.011
0.120
0.90
Eugenia copacabanensis
1.04
4
0
0
4
0.00
0.293
0.000
0.021
0.314
0.64
Pourouma guianensis
1.02
7
1
0
6
-1.39
0.151
0.005
0.056
0.204
2.74
Pouteria gardneri
1.01
7
0
0
7
0.00
0.115
0.000
0.033
0.148
2.31
Myrcia splendens
1.01
8
1
1
8
0.00
0.115
0.007
0.017
0.125
0.78
Eugenia xiriricana
1.00
8
1
1
8
0.00
0.117
0.014
0.015
0.118
0.06
Licania parvifolia
0.98
7
1
0
6
-1.39
0.177
0.005
0.012
0.184
0.34
Micropholis aff. crassipedicellata
0.97
4
0
0
4
0.00
0.255
0.000
0.026
0.281
0.88
Sloanea obtusifolia
0.96
2
0
0
2
0.00
0.341
0.000
0.036
0.377
0.92
Byrsonima sp.
0.95
6
0
1
7
1.41
0.095
0.000
0.051
0.146
3.98
Pouteria sagotiana
0.94
6
0
0
6
0.00
0.176
0.000
0.017
0.193
0.82
Copaifera langsdorffii
0.94
7
1
1
7
0.00
0.228
0.107
0.022
0.142
-4.19
0.94
8
2
1
7
-1.21
0.141
0.010
0.010
0.141
0.05
0.93
8
0
0
8
0.00
0.055
0.000
0.004
0.059
0.62
Gomidesia crocea
0.91
8
0
0
8
0.00
0.061
0.000
0.014
0.075
1.83
Bathysa australis
0.91
6
0
2
8
2.65
0.033
0.000
0.013
0.046
3.05
Calyptranthes sp6
0.90
7
1
0
6
-1.39
0.145
0.018
0.017
0.144
-0.06
Neomitranthes warmingiana
0.89
6
0
1
7
1.41
0.080
0.000
0.010
0.091
1.08
Hydrogaster trinervis
0.89
1
0
0
1
0.00
0.358
0.000
0.031
0.389
0.76
Protium heptaphyllum
0.88
6
1
0
5
-1.64
0.159
0.008
0.032
0.184
1.33
Eugenia rugosissima
0.88
8
1
0
7
-1.21
0.113
0.034
0.002
0.082
-2.91
Symplocos nitens
0.87
4
0
0
4
0.00
0.194
0.000
0.037
0.232
1.60
Ocotea dispersa
0.86
7
1
0
6
-1.39
0.131
0.010
0.004
0.126
-0.37
Ocotea elegans
0.85
4
0
0
4
0.00
0.192
0.000
0.030
0.221
1.31
1933
123
Pouteria bullata
Pouteria cuspidata
Biodivers Conserv (2011) 20:1921–1949
Table 5 continued
1934
123
Table 5 continued
Species
IV
Number of trees
1992–1993
D
R
2003–2004
Change
(% year-1)
Basal area
1992–1993
Loss
Gain
2003–2004
Change
(% year-1)
Ocotea velutina
0.85
6
0
0
6
0.00
0.112
0.000
0.007
0.119
Myrsine venosa
0.85
7
1
0
6
-1.39
0.113
0.008
0.039
0.145
0.55
2.25
Mollinedia salicifolia
0.84
7
0
0
7
0.00
0.087
0.000
0.003
0.090
0.30
Cupania furfuracea
0.84
7
1
0
6
-1.39
0.110
0.021
0.022
0.112
0.15
Sclerolobium densiflorum
0.84
4
0
0
4
0.00
0.210
0.000
0.030
0.240
1.23
IV importance value, D dead trees, R recruits
Biodivers Conserv (2011) 20:1921–1949
Biodivers Conserv (2011) 20:1921–1949
1935
Fig. 4 Balance of the number of trees (NT) of 28 endemic species between the original survey in
1992–1993 (Thomaz and Monteiro 1997) and the second survey in 2003–2004 (this study) in 1.02 ha of
montane rainforest at the Santa Lúcia Biological Station, Espı́rito Santo, southeastern Brazil. The diagonal
line represents the complete balance between original and second surveys. 1—Salacia nemorosa; 2—
Eugenia sp. 5 new; 3—Miconia sp. new; 4—Schefflera kollmannii; 5—Williamodendron cinnamomeum,
Myrcia sp. 6 new; 6—Schefflera grandigemma, Euterpe espiritosantensis, Cryptocarya velloziana, Myrcia
sp. 5 new; 7—Schefflera ruschiana; 8—Myrsine sp. new, Calyptranthes sp. 1 new, Myrcia sp. 3 new; 9—
Xylopia decorticans, Cryptocarya sp. new, Ocotea pluridomatiata; 10—Miconia capixaba; 11—Mollinedia
sp. new; 12—Ocotea sp. 7 new; 13—Eugenia rugosissima; 14—Trichilia sp. new, Elvasia capixaba; 15—
Vochysia santaluciae; 16—Pseudoxandra spiritus-sancti; 17—Ocotea cryptocarpa; 18—Mezilaurus sp.
new; 19—Unonopsis sancta-teresae
to the pattern expected for mature tropical forests (Swaine et al. 1987; Ayyappan and
Parthasarathy 2004; Stephenson and van Mantgem 2005).
The rates of mortality, recruitment and ingrowth are close to those found in various
mature tropical forests worldwide (Swaine et al. 1987; Phillips 1996; Ayyappan and
Parthasarathy 2004; Lewis et al. 2004a). The small differences between these rates found
in this study were non-significant and can be attributed to the cyclical rhythms of dynamic
processes, whereby mortality occurs first and opens the way for the establishment and
growth of recruits, creating a small temporary imbalance of these mechanisms (OliveiraFilho et al. 1997).
However, it should be noted that the slight increase in basal area could also be explained
by the CO2 fertilization hypothesis, which relates the increase in atmospheric CO2 concentrations to a greater productivity of forests and a consequent increase in biomass
(Phillips 1996). However, confirmation of a trend of increasing biomass would only be
possible if a sequence of periodic inventories had been carried out, as has been done in
other forests where this trend was analyzed (Laurance et al. 2009; Lewis et al. 2004a).
Thus, the occurrence of cyclical rhythms of dynamic processes was accepted as the best
explanation at the time.
Although balanced, the dynamics of the forest have been slow (a slow forest according
to Lewis et al. 2004a). The turnover time of about 70 years revealed that the replacement
of trees and the basal area of the forest are long processes. The turnover rates for trees or
basal areas were slightly lower than in other mature tropical forests, where normally the
123
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Biodivers Conserv (2011) 20:1921–1949
turnover rates reach 1–3% year-1 (Phillips 1996). However, comparisons among dynamics
studies with different time intervals are inappropriate because, according to Lewis et al.
(2004b), the values of turnover rates tend to decrease when the time intervals increase.
Thus, small differences when compared to other mature forests may only be mathematical
artifacts.
The high ecological diversity remained after 11 years because there was balance between
the numbers of species and families in both surveys and the turnover of floristic composition
was performed by the less abundant (rare) species of the community. This role of less
abundant species in community dynamics has been confirmed by other studies (Ayyappan
and Parthasarathy 2004; Werneck and Franceschinelli 2004; Guedes-Bruni et al. 2009).
The large participation of the family Myrtaceae in the species turnover was surely a
result of its large number of species (N = 83) in the survey, many of which were represented by only one or two trees. In the case of Melastomataceae, the large participation,
especially in species recruitment, can be attributed to the ability of some Melastomataceae
species (named gap-dependent species) to respond with rapid growth in height and width of
the canopy under more intense conditions of natural light caused by the opening of natural
gaps (Daws et al. 2007).
These characteristics of the community show that the natural disturbances (especially
the death of trees by various causes) generally expected in any section of a mature tropical
forest did not modify the structure of the forest SLBS over time. It is true that during the
interval of the study, more precisely in the years 1997 and 1998, various tropical regions
experienced a period of drought and intense heat due to the El Niño Southern Oscillation
(ENSO). Although there are no detailed records of the structure of the SLBS forest during
that period, it is likely that mortality rates increased significantly in the community, as
reported by studies in the Amazon rainforest (Nascimento et al. 2007; Laurance et al.
2009), in southeastern Brazil (Rolim et al. 2005) and in Borneo (Lingenfelder and Newbery 2009). Assuming that these effects did actually occur in the SLBS forest, the results
show that after the ENSO the losses were offset after only 5 years.
Diameter classes
For this study, no relationship was found between mortality rates and diameter class. This
situation also was found in other studies carried out in preserved tropical forests
(Manokaran and Kochummen 1987; Carey et al. 1994; Korning and Balslev 1994). This
contrasts with the higher mortality rates in smaller size classes (usually with dbh between 5
and 20 cm), which has been recorded for tropical forests in regeneration after anthropogenic disturbances (Guilherme et al. 2004; Werneck and Franceschinelli 2004; Higuchi
et al. 2008; Taylor et al. 2008).
In regard to recruitment, it was expected that the recruits would be smaller trees, concentrated in the 6.4–10 cm class. However, this concentration did not result in an increase of
basal area in this class due to the migration of trees to other classes for ingrowth.
Populations
The main populations also showed stability, following the general pattern of balance
between mortality and recruitment for mature tropical forests. As for the community, small
differences in abundance or in the basal area of each population between surveys may also
be the result of dynamic cycles involving the mechanisms of mortality and recruitment/
growth.
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Biodivers Conserv (2011) 20:1921–1949
1937
One of the few species that did not fit into this pattern was the palm Euterpe edulis,
which had expanded its participation due to the large number of recruits. This may be
linked to the reproductive success of this species, as already recorded by Silva-Matos
and Watkinson (1998) and Portela et al. (2010), and the absence of disturbances able to
modify the structure of the community. Euterpe edulis is important in Atlantic rainforest because of its large production of fruit, which constitutes a major food resource
for wildlife at certain periods of the year (Silva-Matos and Watkinson 1998; Portela
et al. 2010). However, it is a species which is still exploited illegally for its edible palm
heart.
In the other cases of species which showed large changes (annual rates above 6%,
positive or negative), the small size of these populations may explain why the death/
recruitment of few trees or the loss/gain of very small portions of basal area resulted in
seemingly high rates.
In the case of local endemic species in particular, the balance of trees in the original and
second surveys was important in ensuring the continuity of its populations in the plots.
However, to say that these species are protected from the risk of extinction is still hasty,
since the time scale of this study may have been inappropriate for this interpretation.
Moreover, since the geographical distribution of these species was limited to a few square
kilometers in region, this shows that their future also depends on the conservation of other
populations located in neighboring forest fragments.
The slight increase in basal area experienced by the total community was also confirmed
in most populations because they had small positive changes. Negative changes occurred in
a small number of species and this was not sufficient to fully balance gains and losses of
the community.
Conclusion
The data on the tree changes in this study showed an affinity with the pattern of dynamic
balance for both structure and diversity expected in mature tropical forests. This is
interesting, mainly because the balance in this study was in a forest with high levels of
diversity and endemism.
In addition, this study provides a basis for further work on the dynamics of the forest
studied. Such investigations may be conducted over the coming years in other surveys,
perhaps with shorter intervals and also considering other components such as lianas and
saplings of trees species, as has been done in various forests throughout the world. Topics
that might be explored are the changes in basal area and turnover rates, changes in the
participation of groups of species with different requirements for light and moisture and
monitoring of the dynamics of local endemic species in order to create support for
conservation.
In fact, the 1.02 ha of this study may seem small when compared with the large plots in
other dynamic studies around the world. But the absence of data on the dynamics of mature
forests in the Atlantic rainforest region is mainly caused by the scarcity of these areas, by
the large amount of time needed to carry out these surveys, which also requires a large
amount of human and financial resources, and by the difficulty in identifying botanical
species within a very rich flora that are still little known. The small number of research
projects to date are the only existing records about the dynamics of this magnificent
neotropical ecoregion.
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Biodivers Conserv (2011) 20:1921–1949
Acknowledgments This study is part of the Master’s dissertation of Felipe Z. Saiter. The authors thank the
National Council for Scientific and Technological Development (CNPq) for financial support (grant n.
690149/01-8) and for a productivity grant to T Wendt and FAG Guilherme, the Museu de Biologia Prof.
Mello Leitão for research permits and logistical support, and FR Scarano, MT Nascimento and two
anonymous reviewers for their helpful suggestions. They also thank the biologists who helped with the field
work: T Senna, V Demuner, R Vervloet, J Tomasini, FA Obermüller, GM Tobón, TS Cóser, ML Dan and
MAS Godinho.
Appendix
See Table 6.
Table 6 List of 399 species (with 28 local endemic) recorded in two successive surveys (1992–1993 and
2003–2004) of trees with dbh C6.4 cm carried out in a stand of 1.02 ha in Santa Lúcia Biological Station,
Santa Teresa, southeastern Brazil. Presence (1) and absence (0) of species in each survey are listed
separately
No.
Family
Species
Presence/absence
1992–1993
2003–2004
1
Anacardiaceae
Tapirira guianensis
1
1
2
Annonaceae
Anaxagorea dolichocarpa
0
1
3
Annonaceae
Annona cacans
0
1
4
Annonaceae
Guatteria australis
1
1
5
Annonaceae
Guatteria glabrescens
1
1
6
Annonaceae
Guatteria sellowiana
1
1
7
Annonaceae
Oxandra nitida
1
1
8
Annonaceae
Pseudoxandra spiritus-sanctia
1
1
9
Annonaceae
Rollinia dolabripetala
1
0
10
Annonaceae
Unonopsis sancta-teresaea
1
1
11
Annonaceae
Xylopia decorticansa
1
1
12
Apocynaceae
Aspidosperma melanocalyx
1
1
13
Apocynaceae
Aspidosperma parvifolium
1
1
14
Apocynaceae
Himatanthus bracteatus
1
1
15
Apocynaceae
Lacmellea pauciflora
1
1
16
Apocynaceae
Rauvolfia grandiflora
1
1
17
Aquifoliaceae
Ilex amara
1
0
18
Aquifoliaceae
Ilex paraguariensis
1
1
19
Araliaceae
Schefflera calva
1
1
20
Araliaceae
Schefflera grandigemmaa
1
1
21
Araliaceae
Schefflera kollmanniia
1
1
22
Araliaceae
Schefflera ruschianaa
1
1
23
Arecaceae
Attalea burretiana
1
1
24
Arecaceae
Euterpe edulis
1
1
25
Arecaceae
Euterpe espiritosantensisa
1
1
26
Arecaceae
Geonoma schottiana
1
1
27
Arecaceae
Syagrus pseudococus
1
1
28
Asteraceae
Vernonia discolor
1
1
29
Bignoniaceae
Jacaranda microcalyx
1
1
123
Biodivers Conserv (2011) 20:1921–1949
1939
Table 6 continued
No.
Family
Species
Presence/absence
1992–1993
2003–2004
30
Bignoniaceae
Tabebuia roseo-alba
1
1
31
Boraginaceae
Cordia sp.
1
1
32
Boraginaceae
Cordia trachyphylla
1
1
33
Burseraceae
Protium brasiliense
1
1
34
Burseraceae
Protium heptaphyllum
1
1
35
Cardiopteridaceae
Citronella paniculata
1
1
36
Caricaceace
Jacaratia heptaphylla
1
1
37
Caryocaraceae
Caryocar edule
1
1
38
Celastraceae
Cheiloclinium cognatum
1
1
39
Celastraceae
Maytenus cestrifolia
1
1
40
Celastraceae
Maytenus obtusifolia
1
1
41
Celastraceae
Salacia elliptica
1
1
42
Celastraceae
Salacia nemorosa
1
0
43
Celastraceae
Tontelea martiana
1
1
44
Chrysobalanaceae
Couepia grandiflora
1
1
45
Chrysobalanaceae
Couepia macrophylla
1
1
46
Chrysobalanaceae
Couepia venosa
1
1
47
Chrysobalanaceae
Hirtella angustifolia
1
1
48
Chrysobalanaceae
Hirtella hebeclada
1
1
49
Chrysobalanaceae
Licania kunthiana
1
1
50
Chrysobalanaceae
Licania leptostachya
1
1
51
Chrysobalanaceae
Licania micrantha
1
1
52
Chrysobalanaceae
Licania octandra
1
1
53
Chrysobalanaceae
Licania parvifolia
1
1
54
Chrysobalanaceae
Licania salzmannii
1
1
55
Chrysobalanaceae
Parinari aff. littoralis
1
1
56
Chrysobalanaceae
Parinari obtusifolium
1
1
57
Clusiaceae
Clusia intermedia
1
1
58
Clusiaceae
Garcinia brasiliensis
1
1
59
Clusiaceae
Garcinia gardneriana
1
1
60
Clusiaceae
Kielmeyera occhioniana
1
1
61
Clusiaceae
Tovomita brasiliensis
1
1
62
Clusiaceae
Tovomita leucantha
1
1
63
Clusiaceae
Tovomitopsis saldanhae
1
1
64
Connaraceae
Connarus detersus
1
1
65
Cunoniaceae
Lamanonia ternata
1
1
66
Dichapetalaceae
Stephanopodium blanchetianum
1
1
67
Elaeocarpaceae
Sloanea aff. garckeana
1
1
68
Elaeocarpaceae
Sloanea obtusifolia
1
1
69
Elaeocarpaceae
Sloanea guianensis
1
1
70
Elaeocarpaceae
Sloanea monosperma
1
1
71
Elaeocarpaceae
Sloanea nitida
1
1
123
1940
Biodivers Conserv (2011) 20:1921–1949
Table 6 continued
No.
Family
Species
Presence/absence
1992–1993
2003–2004
72
Elaeocarpaceae
Sloanea sp.
1
1
73
Erythroxylaceae
Erythroxylum aff. macrophyllum
1
1
74
Erythroxylaceae
Erythroxylum cuspidifolium
1
0
75
Erythroxylaceae
Erythroxylum pulchrum
1
1
76
Erythroxylaceae
Erythroxylum squamatum
1
1
77
Euphorbiaceae
Alchornea triplinervia
1
1
78
Euphorbiaceae
Aparisthmium cordatum
1
1
79
Euphorbiaceae
Croton floribundus
1
0
80
Euphorbiaceae
Maprounea guianensis
1
1
81
Euphorbiaceae
Pausandra morisiana
1
1
82
Euphorbiaceae
Pera leandri
1
1
83
Fabaceae
Abarema cf. obovata
1
1
84
Fabaceae
Andira fraxinifolia
1
1
85
Fabaceae
Copaifera langsdorffii
1
1
86
Fabaceae
Dalbergia foliolosa
1
1
87
Fabaceae
Dalbergia miscolobium
1
1
88
Fabaceae
Diplotropis incexis
1
1
89
Fabaceae
Hymenaea aurea
1
1
90
Fabaceae
Hymenaea courbaril
1
1
91
Fabaceae
Hymenolobium janeirense
1
1
92
Fabaceae
Inga capitata
1
1
93
Fabaceae
Inga cylindrica
1
1
94
Fabaceae
Inga densiflora
1
1
95
Fabaceae
Inga dulcis
1
1
96
Fabaceae
Inga flagelliformis
1
1
97
Fabaceae
Inga lenticellata
1
1
98
Fabaceae
Inga subnuda
1
1
99
Fabaceae
Inga tenuis
1
1
100
Fabaceae
Inga thibaudiana
1
1
101
Fabaceae
Inga vestita
1
1
102
Fabaceae
Melanoxylon brauna
1
1
103
Fabaceae
Ormosia cf. friburgensis
1
1
104
Fabaceae
Peltogyne angustiflora
1
1
105
Fabaceae
Pithecellobium cochliocarpum
1
1
106
Fabaceae
Pseudopiptadenia contorta
1
1
107
Fabaceae
Sclerolobium densiflorum
1
1
108
Fabaceae
Sclerolobium striatum
1
1
109
Fabaceae
Senna multijuga
1
1
110
Fabaceae
Swartzia acutifolia
1
1
111
Fabaceae
Swartzia apetala
1
1
112
Fabaceae
Swartzia myrtifolia
1
1
113
Fabaceae
Zollernia ilicifoia
1
1
123
Biodivers Conserv (2011) 20:1921–1949
1941
Table 6 continued
No.
Family
Species
Presence/absence
1992–1993
2003–2004
114
Fabaceae
Zollernia magnifica
1
1
115
Hernandiaceae
Sparattanthelium botocudorum
1
1
116
Humiriaceae
Vantanea compacta
1
1
117
Humiriaceae
Vantanea obovata
1
1
118
Hypericaceae
Vismia brasiliensis
1
1
119
Lacistemataceae
Lacistema robustum
1
1
120
Lamiaceae
Vitex orinocensis
1
1
121
Lamiaceae
Vitex sp.
1
1
122
Lauraceae
Aniba firmula
0
1
123
Lauraceae
Beilschmiedia sp.
1
1
124
Lauraceae
Beilschmiedia taubertiana
1
1
125
Lauraceae
Cinnamomum riedelianum
1
1
126
Lauraceae
Cinnamomum sp.
1
1
127
Lauraceae
Cryptocarya saligna
1
1
128
Lauraceae
Cryptocarya sp. newa
1
1
129
Lauraceae
Cryptocarya vellozianaa
1
1
130
Lauraceae
Endlicheria paniculata
1
1
131
Lauraceae
Endlicheria sp.
1
1
132
Lauraceae
Licaria armeniaca
1
1
133
Lauraceae
Licaria guianensis
1
0
134
Lauraceae
Ocotea aciphylla
1
1
135
Lauraceae
Ocotea catharinensis
1
1
136
Lauraceae
Ocotea corymbosa
1
1
137
Lauraceae
Ocotea cryptocarpaa
1
1
138
Lauraceae
Ocotea daphnifolia
1
1
139
Lauraceae
Ocotea dispersa
1
1
140
Lauraceae
Ocotea divaricata
1
1
141
Lauraceae
Ocotea domatiata
1
1
142
Lauraceae
Ocotea elegans
1
1
143
Lauraceae
Ocotea indecora
0
1
144
Lauraceae
Ocotea lancifolia
1
1
145
Lauraceae
Ocotea longifolia
1
1
146
Lauraceae
Ocotea odorifera
1
1
147
Lauraceae
Ocotea puberula
1
1
148
Lauraceae
Ocotea pulchra
1
1
149
Lauraceae
Ocotea silvestris
1
1
150
Lauraceae
Mezilaurus sp. newa
1
1
151
Lauraceae
Ocotea sp1
1
1
152
Lauraceae
Ocotea sp2
1
1
153
Lauraceae
Ocotea sp3
1
1
154
Lauraceae
Ocotea sp4
1
1
155
Lauraceae
Ocotea sp5
1
1
123
1942
Biodivers Conserv (2011) 20:1921–1949
Table 6 continued
No.
Family
Species
Presence/absence
1992–1993
2003–2004
156
Lauraceae
Ocotea sp6
1
1
157
Lauraceae
Ocotea sp7 newa
1
1
158
Lauraceae
Ocotea pluridomatiataa
1
1
159
Lauraceae
Ocotea spixiana
1
1
160
Lauraceae
Ocotea teleiandra
1
1
161
Lauraceae
Ocotea tenuiflora
1
1
162
Lauraceae
Ocotea velutina
1
1
163
Lauraceae
Persea caesia
1
1
164
Lauraceae
Persea sp.
1
1
165
Lauraceae
Williamodendron cinnamomeuma
1
1
166
Linnaceae
Roucheria cf. dryadica
0
1
167
Loganiaceae
Strychnos sp.
1
1
168
Malphigiaceae
Barnebya dispar
1
1
169
Malphigiaceae
Byrsonima sp.
1
1
170
Malphigiaceae
Byrsonima variabilis
1
1
171
Malvaceae
Bombacopsis calophylla
1
1
172
Malvaceae
Eriotheca macrophylla
1
1
173
Malvaceae
Hydrogaster trinervis
1
1
174
Melastomataceae
Meriania tetramera
1
1
175
Melastomataceae
Miconia budlejoides
1
1
176
Melastomataceae
Miconia capixabaa
1
1
177
Melastomataceae
Miconia cinnamomifolia
1
1
178
Melastomataceae
Miconia dodecandra
1
1
179
Melastomataceae
Miconia doriana
1
0
180
Melastomataceae
Miconia latecrenata
1
1
181
Melastomataceae
Miconia lepidota
1
1
182
Melastomataceae
Miconia longicuspis
0
1
183
Melastomataceae
Miconia octopetala
1
1
184
Melastomataceae
Miconia polyandra
1
1
185
Melastomataceae
Miconia prasina
1
1
186
Melastomataceae
Miconia pusilliflora
1
1
187
Melastomataceae
Miconia sellowiana
0
1
188
Melastomataceae
Miconia sp. newa
0
1
189
Melastomataceae
Miconia tristis
0
1
190
Melastomataceae
Mouriri cf. regeliana
1
1
191
Melastomataceae
Mouriri doriana
1
1
192
Melastomataceae
Mouriri glazioviana
1
1
193
Meliaceae
Cabralea canjerana
1
1
194
Meliaceae
Guarea macrophylla
1
1
195
Meliaceae
Trichilia emarginata
1
1
196
Meliaceae
Trichilia lepidota
1
1
197
Meliaceae
Trichilia silvatica
1
1
123
Biodivers Conserv (2011) 20:1921–1949
1943
Table 6 continued
No.
Family
Species
Presence/absence
1992–1993
2003–2004
1
198
Meliaceae
Trichilia sp. newa
1
199
Monimiaceae
Mollinedia stenophylla
1
1
200
Monimiaceae
Mollinedia aff. engleriana
1
1
201
Monimiaceae
Mollinedia fruticulosa
1
1
202
Monimiaceae
Mollinedia heteranthera
1
1
203
Monimiaceae
Mollinedia salicifolia
1
1
204
Monimiaceae
Mollinedia sp. newa
1
1
205
Moraceae
Brosimum cf. glaziovii
1
1
206
Moraceae
Ficus citrifolia
1
1
207
Moraceae
Sorocea guilleminiana
1
1
208
Myristicaceae
Virola gardneri
1
1
209
Myrsinaceae
Myrsine lancifolia
1
1
210
Myrsinaceae
Myrsine sp. newa
1
1
211
Myrsinaceae
Myrsine umbellata
1
1
212
Myrsinaceae
Myrsine venosa
1
1
213
Myrtaceae
Blepharocalyx eggersii
1
1
214
Myrtaceae
Calyptranthes aff. clusiifolia
1
1
215
Myrtaceae
Calyptranthes aff. grandifolia
1
1
216
Myrtaceae
Calyptranthes pauciflora
1
1
217
Myrtaceae
Calyptranthes pulchella
1
1
218
Myrtaceae
Calyptranthes sp1 newa
1
1
219
Myrtaceae
Calyptranthes sp2
1
1
220
Myrtaceae
Calyptranthes sp3
1
1
221
Myrtaceae
Calyptranthes sp4
1
1
222
Myrtaceae
Calyptranthes sp5
1
1
223
Myrtaceae
Calyptranthes sp6
1
1
224
Myrtaceae
Calyptranthes sp7
1
1
225
Myrtaceae
Calyptranthes sp8
1
1
226
Myrtaceae
Calyptranthes sp9
1
1
227
Myrtaceae
Calyptranthes widgreniana
1
1
228
Myrtaceae
Campomanesia aromatica
1
1
229
Myrtaceae
Campomanesia guaviroba
1
1
230
Myrtaceae
Campomanesia laurifolia
1
1
231
Myrtaceae
Eugenia acutata
1
1
232
Myrtaceae
Eugenia aff. platysema
1
1
233
Myrtaceae
Eugenia aff. pruniformis
1
1
234
Myrtaceae
Eugenia aggregata
1
1
235
Myrtaceae
Eugenia candolleana
1
1
236
Myrtaceae
Eugenia cerasiflora
1
1
237
Myrtaceae
Eugenia cf. martiusiana
1
1
238
Myrtaceae
Eugenia cf. neomooniana
1
1
239
Myrtaceae
Eugenia copacabanensis
1
1
123
1944
Biodivers Conserv (2011) 20:1921–1949
Table 6 continued
No.
Family
Species
Presence/absence
1992–1993
2003–2004
240
Myrtaceae
Eugenia egensis
1
1
241
Myrtaceae
Eugenia excelsa
1
1
242
Myrtaceae
Eugenia itapemirimensis
1
1
243
Myrtaceae
Eugenia melanogyna
0
1
244
Myrtaceae
Eugenia neoglomerata
1
0
245
Myrtaceae
Eugenia neolanceolata
1
1
246
Myrtaceae
Eugenia oblongata
1
1
247
Myrtaceae
Eugenia persicifolia
1
1
248
Myrtaceae
Eugenia piloensis
1
1
249
Myrtaceae
Eugenia platyphylla
1
1
250
Myrtaceae
Eugenia rostrata
1
1
251
Myrtaceae
Eugenia rugosissimaa
1
1
252
Myrtaceae
Eugenia sp1
1
1
253
Myrtaceae
Eugenia sp2
1
1
254
Myrtaceae
Eugenia sp3
1
1
255
Myrtaceae
Eugenia sp4
1
1
256
Myrtaceae
Eugenia sp5 newa
0
1
257
Myrtaceae
Eugenia tinguyensis
1
1
258
Myrtaceae
Eugenia xiriricana
1
1
259
Myrtaceae
Gomidesia cf. palustris
1
1
260
Myrtaceae
Gomidesia cf. pubescens
1
1
261
Myrtaceae
Gomidesia cf. schaueriana
1
1
262
Myrtaceae
Gomidesia crocea
1
1
263
Myrtaceae
Marlierea cf. ovata
1
1
264
Myrtaceae
Marlierea excoriata
1
1
265
Myrtaceae
Marlierea obscura
1
1
266
Myrtaceae
Marlierea regeliana
1
1
267
Myrtaceae
Marlierea silvatica
1
1
268
Myrtaceae
Marlierea sp.
1
1
269
Myrtaceae
Myrcia crocea
1
1
270
Myrtaceae
Myrcia laurifolia
1
1
271
Myrtaceae
Myrcia montana
1
1
272
Myrtaceae
Myrcia plusiantha
1
1
273
Myrtaceae
Myrcia pubipetala
1
0
274
Myrtaceae
Myrcia racemosa
1
0
275
Myrtaceae
Myrcia sp1
1
1
276
Myrtaceae
Myrcia sp2
1
1
277
Myrtaceae
Myrcia sp3 newa
1
1
278
Myrtaceae
Myrcia sp4
1
1
279
Myrtaceae
Myrcia sp5 newa
1
1
280
Myrtaceae
Myrcia sp6 newa
1
1
281
Myrtaceae
Myrcia sp7
1
1
123
Biodivers Conserv (2011) 20:1921–1949
1945
Table 6 continued
No.
Family
Species
Presence/absence
1992–1993
2003–2004
282
Myrtaceae
Myrcia splendens
1
1
283
Myrtaceae
Myrcia subrugosa
1
1
284
Myrtaceae
Myrciaria disticha
1
1
285
Myrtaceae
Myrciaria floribunda
1
1
286
Myrtaceae
Neomitranthes glomerata
1
1
287
Myrtaceae
Neomitranthes warmingiana
1
1
288
Myrtaceae
Pimenta pseudocaryophyllus
1
1
289
Myrtaceae
Plinia cf. involucrata
1
1
290
Myrtaceae
Plinia renatiana
1
1
291
Myrtaceae
Plinia rivularis
1
1
292
Myrtaceae
Psidium sp1
1
1
293
Myrtaceae
Psidium sp2
1
1
294
Myrtaceae
Siphoneugena cf. kiaerskoviana
1
1
295
Myrtaceae
Siphoneugena dussii
1
0
296
Nyctaginaceae
Guapira laxa
1
1
297
Nyctaginaceae
Guapira obtusata
1
1
298
Nyctaginaceae
Guapira opposita
1
1
299
Nyctaginaceae
Guapira venosa
1
1
300
Ochnaceae
Elvasia capixabaa
1
1
301
Ochnaceae
Ouratea cuspidata
1
1
302
Olacaceae
Heisteria cf. silvianii
1
1
303
Olacaceae
Heisteria perianthomega
1
1
304
Olacaceae
Tetrastylidium grandifolium
1
1
305
Oleaceae
Chionanthus micranthus
1
1
306
Pentaphyllacaceae
Ternstroemia brasiliensis
1
1
307
Pentaphyllacaceae
Ternstroemia sp.
1
1
308
Phyllanthaceae
Hyeronima alchorneoides
1
1
309
Phyllanthaceae
Hyeronima oblonga
1
1
310
Phyllanthaceae
Margaritaria nobilis
1
1
311
Polygonaceae
Coccoloba confusa
1
1
312
Polygonaceae
Coccoloba declinata
1
1
313
Proteaceae
Panopsis sp.
0
1
314
Proteaceae
Roupala aff. rhombifolia
1
1
315
Proteaceae
Roupala consimilis
1
1
316
Putranjivaceae
Drypetes sessiliflora
1
1
317
Quiinaceae
Quiina glaziovii
1
1
318
Rosaceae
Prunus brasiliensis
1
1
319
Rosaceae
Prunus sellowii
1
1
320
Rubiaceae
Alibertia sp.
1
1
321
Rubiaceae
Amaioua intermedia
1
1
322
Rubiaceae
Amaioua pilosa
1
1
323
Rubiaceae
Bathysa australis
1
1
123
1946
Biodivers Conserv (2011) 20:1921–1949
Table 6 continued
No.
Family
Species
Presence/absence
1992–1993
2003–2004
324
Rubiaceae
Bathysa stipulata
1
1
325
Rubiaceae
Faramea oligantha
1
1
326
Rubiaceae
Faramea pachyantha
1
1
327
Rubiaceae
Ixora sp.
1
1
328
Rubiaceae
Posoqueria acutifolia
1
1
329
Rubiaceae
Posoqueria latifolia
1
1
330
Rubiaceae
Psychotria carthagenensis
1
1
331
Rubiaceae
Psychotria sessilis
1
1
332
Rubiaceae
Rudgea recurva
1
1
333
Rubiaceae
Simira glaziovii
1
1
334
Rubiaceae
Simira sampaioana
1
1
335
Rubiaceae
Stachyarrhena krukovii
1
1
336
Rutaceae
Hortia brasiliana
1
1
337
Sabiaceae
Meliosma chartacea
1
1
338
Salicaceae
Banara serrata
1
0
339
Salicaceae
Casearia arborea
1
1
340
Salicaceae
Casearia commersoniana
1
1
341
Salicaceae
Casearia decandra
1
1
342
Salicaceae
Casearia sp1
1
1
343
Salicaceae
Casearia sp2
1
1
344
Sapindaceae
Allophylus laevigatus
1
1
345
Sapindaceae
Allophylus petiolulatus
1
1
346
Sapindaceae
Cupania crassifolia
1
1
347
Sapindaceae
Cupania emarginata
1
1
348
Sapindaceae
Cupania furfuracea
1
1
349
Sapindaceae
Cupania scrobiculata
1
1
350
Sapindaceae
Matayba arborescens
1
1
351
Sapindaceae
Matayba cf. guianensis
1
1
352
Sapindaceae
Talisia cf. cerasina
1
1
353
Sapindaceae
Talisia cupularis
1
1
354
Sapindaceae
Talisia sp.
0
1
355
Sapotaceae
Chrysophyllum flexuosum
1
1
356
Sapotaceae
Chrysophyllum gonocarpum
1
1
357
Sapotaceae
Chrysophyllum sp1
1
1
358
Sapotaceae
Chrysophyllum sp2
1
1
359
Sapotaceae
Chrysophyllum splendens
1
1
360
Sapotaceae
Diploon cuspidatum
1
1
361
Sapotaceae
Ecclinusa ramiflora
1
1
362
Sapotaceae
Manilkara cf. longifolia
1
1
363
Sapotaceae
Micropholis aff. crassipedicellata
1
1
364
Sapotaceae
Micropholis aff. gardneriana
1
1
365
Sapotaceae
Micropholis compta
1
1
123
Biodivers Conserv (2011) 20:1921–1949
1947
Table 6 continued
No.
Family
Species
Presence/absence
1992–1993
2003–2004
366
Sapotaceae
Micropholis guyanensis
1
1
367
Sapotaceae
Micropholis sp.
1
1
368
Sapotaceae
Micropholis venulosa
1
1
369
Sapotaceae
Pouteria aff. reticulata
1
1
370
Sapotaceae
Pouteria bangii
1
1
371
Sapotaceae
Pouteria bullata
1
1
372
Sapotaceae
Pouteria caimito
1
1
373
Sapotaceae
Pouteria cf. coelomatica
1
1
374
Sapotaceae
Pouteria cf. guianensis
1
1
375
Sapotaceae
Pouteria cuspidata
1
1
376
Sapotaceae
Pouteria gardneri
1
1
377
Sapotaceae
Pouteria grandiflora
1
1
378
Sapotaceae
Pouteria macahensis
1
1
379
Sapotaceae
Pouteria sagotiana
1
1
380
Sapotaceae
Pouteria sp1
1
1
381
Sapotaceae
Pouteria sp2
1
1
382
Sapotaceae
Pradosia lactescens
1
1
383
Simaroubaceae
Simarouba amara
1
1
384
Siparunaceae
Siparuna glossostyla
1
1
385
Solanaceae
Solanum sooretamum
1
0
386
Symplocaceae
Symplocos celastrinea
1
1
387
Symplocaceae
Symplocos frondosa
1
1
388
Symplocaceae
Symplocos nitens
1
1
389
Thymaelaceae
Daphnopsis martii
1
1
390
Urticaceae
Cecropia hololeuca
1
1
391
Urticaceae
Coussapoa cf. glaberrima
1
1
392
Urticaceae
Coussapoa microcarpa
1
1
393
Urticaceae
Coussapoa pachyphylla
1
1
394
Urticaceae
Pourouma bicolor
1
0
395
Urticaceae
Pourouma guianensis
1
1
396
Vochysiaceae
Qualea gestasiana
0
1
397
Vochysiaceae
Vochysia rectiflora
1
1
398
Vochysiaceae
Vochysia santaluciaea
1
1
399
Winteraceae
Drimys brasiliensis
1
0
a
Local endemic species
123
1948
Biodivers Conserv (2011) 20:1921–1949
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