Early Plant Succession in Abandoned Pastures in Ecuador
R. A. Zahawi; C. K. Augspurger
Biotropica, Vol. 31, No. 4. (Dec., 1999), pp. 540-552.
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BIOTROPICA 31 (4): 540-552
1999
Early Plant Succession in Abandoned Pastures in Ecuadori
R. A. Zahawi and C. K. Augspurger
Department of Plant Biology, University of Illinois at Urbana-Champaign, 265 Morrill Hall,
505 South Goodwin Avenue, Urbana, Illinois 61801, U.S.A.
ABSTRACT
We compared early plant succession in four abandoned pastures of differing age since abandonment and a nearby
secondary forest site in northwestern Ecuador. Two "Open" pastures had no tree canopy covering, and two "Guava"
pastures had a well-developed canopy cover of Psidium guajaua. No site had been seeded with pasture grasses. All
pastures were compared in a chronological sequence; nvo were monitored for 18 months. Species richness was consistently higher in Guava sites than in Open sites and it continued to increase over time, whereas it remained static
in Open sites. Species richness was highest in secondary forest. Recruitment of tree saplings in Guava sites was lower
than in secondary forest; however, it was nearly absent in Open sites. The seed bank contained predominantly
herbaceous species at all sites, and was highly dissimilar to aboveground vegetation. Dominance-diversity curves for
Guava sites showed a more equitable distribution of species that increased over time. In contrast, dominance-diversity
curves for Open sites were static and indicated dominance by a few aggressive species. Soil characteristics among sites
were variable; however, a principal components analysis on soils isolated the older Open site from all others. The
older Open site had the lowest species richness and was dominated by Baccharis trineruis, an aggressive shrub species.
The site appears to be in a state of arrested succession and some form of restorative intervention may be necessary to
initiate succession toward a forested condition. Succession in Guava sites appears headed toward secondary forest,
whereas it does not in Open sites.
RESUMEN
La sucesi6n de flora temprana fue comparada en cuatro pasturas abandonadas por el ganado con diferentes periodos
de abandono. Tambit-n se realizaron estudios comparativos en una parcela de selva secundaria ubicada en una localidad
cercana. La experiencia se efectuo en el noroeste de Ecuador. Dos de las pasturas bajo estudio eran "abiertas", es decir,
carecian de cobertura de drboles. El resto de las pasturas eran de "guava" y estaban cubiertas por un canopeo de
Psidium guajaua bien desarrollado. No se realizaron prdcticas de resie~nbraen ninguna de las parcelas bajo estudio
durante el transcurso del experimento. Todas las pasturas fueron comparadas cronosecuencial~nente y dos de ellas
fueron monitoreadas temporariamente durante 18 meses. La riqueza de especies fue consistentemente mayor en las
parcelas de "guava" que en las parcelas "abiertas" y continuo incrementando a lo largo del tiempo. Contrariamente,
en las parcelas "abiertas" la riqueza de especies se mantuvo constante. La mayor riqueza especifica se encontr6 en las
parcelas de selva secundaria. El reclutamiento de plantulas de Brboles en las parcelas de "guava" fue menor que en la
selva secundaria y fue despreciable en las parcelas "abiertas". El banco de semillas en codas las parcelas estaba colnpuesto
predominantemente de especies herbiceas y era significativamente distinto de la vegetacion presente en estratos superiores. Curvas de dominancia y diversidad en parcelas de "guava" evidenciaron una distribuci6n de especies equitativa
que increment6 con el tiempo. Por el contrario, las funciones de dominancia y diversidad calculadas en las parcelas
"abiertas" permanecieron estiticas y indicaron el predominio de unas pocas especies agresivas. Las caracteristicas eddficas
de las parcelas era variable. Sin embargo, un Analisis de Co~nponentesPrincipales en suelos separ6 la parcela "abierta"
Inas antigua del resto de las parcelas bajo estudio. Esta parcela result6 tener la menor riqueza de especies y estaba
do~ninadapor Baccharis trineruis, una especie arbustiva sumamente agresiva. Dicha parcela parece estar en un estado
de sucesi6n latente y por ende, es necesaria alguna forma de intervention restauradora para iniciar el proceso de
sucesi6n hacia una condition forestada. La sucesion en las parcelas de "guava" avanza, aparentemente, hacia un estadio
de selva secundaria, aunque no sucede lo ~nismoen las parcelas "abiertas".
Kejj words: abandoned cattle pastures; arrested succession; Ecuador; forest recovery; natural regeneration; Psidium guajava;
Temnant trees; secondarjj forest; secondary succession; unseededpastures.
MUCHDEFORESTATION
IN THE NEOTROPICS
has taken
place to convert land into pastures for cattle grazing
(Buschbacher 1986, Fearnside 1989, Aide et al.
1996, Nepstad et al. 1996). Current estimates indicate that ca 20 million ha of Amazonian forest
' Received 27 August 1997; revision accepted 2 June 1998.
have been converted into cattle pastures (Nepstad
et al. 1996). Pastures are usually abandoned after
five to ten years of use due to soil degradation and
a corresponding decrease in pasture productivity
(Buschbacher 1986, Fearnside 1989, SerrSo & Toledo 1990, Nepstad et al. 1991). As tropical lands
increasingly are made up of abandoned pastures, it
Succession in Abandoned Pastures
541
is critical to gain a greater understanding of the locally referred to, can establish within ten years.
patterns of plant succession and the processes af- Once established, these pastures serve a dual purfecting it. In developing a greater understanding of pose for ranchers as the trees provide shade and
these successional processes, we will be able to pre- fruit for the cattle (Somarriba 1985, 1988b). The
dict if pastures are on a successional trajectory to- two remaining pastures did not have canopies of I!
ward secondary (2") forest. Furthermore, we then guajava.
can determine if it is necessary to accelerate the rate
The objectives of this study were to (1) docuof recovery of pastures to forest when they are in ment the patterns of plant succession in both a
a state of arrested succession.
temporal and chronosequential manner; (2) exPrevious studies have shown that forest recovery amine the biotic and abiotic properties of these
rates vary depending upon the type, intensity, and sites that might affect the course of succession; (3)
duration of disturbance (Uhl 1982, Purata 1986, compare succession in pastures with a canopy cover
Uhl et al. 1988, Reiners et al. 1994, Aide et al. to those without cover; and (4) predict whether any
1995, Nepstad et al. 1996). Most studies of succes- of these pastures will revert to 2" forest over time
sion in abandoned moist tropical pastures have fo- or will remain in a state of arrested succession. We
cused on "seeded pastures (Uhl et al. 1988, SerrCo documented changes in species richness and per& Toledo 1990, Nepstad et al. 1991, Reiners et al. cent cover. Species composition, size of the seed
1994, Nepstad et al. 1996, Quintana-Ascencio et al. bank, and recruitment of tree saplings also were
1996). Seeded pastures are established by clearing determined. Ambient air temperature and several
sites of woody vegetation and then seeding them key soil properties were quantified.
with often nutrient-demanding Poaceae species, such
as Paspalum panicuhtum or Panicum maximum (Uhl
METHODS
et al. 1988, Nepstad et al. 1990, SerrCo & Toledo
1990, Nepstad et al. 1991). No known studies, STUDYS I T E . - T ~
study
~ site is located in the Rehowever, have focused on successional processes fol- serva Maquipucuna, a mid-elevational forest prelowing abandonment in "unseeded pastures. Re- serve on the western slopes of the Andes, ca 45 krn
search on these "unimproved or "natural" pastures northwest of Quito, Ecuador. The reserve comhas focused primarily on their inherent pastoral pro- prises ca 4450 ha, ranging in elevation from ca
ductivity, and how it compares to pastoral produc- 1200 to 2600 m. Mean annual rainfall is 3200tivity in seeded pastures (Watson & Whiteman 3500 mm, with a drier season from June through
1981, Somarriba 1988b). In addition, Sarmiento August. Most of the reserve (ca 90%) consists of
(1997) has documented seed rain into unseeded pas- relatively undisturbed montane wet forest; the retures. Unseeded pastures are cleared in the same mainder, mostly at lower elevations, was farmed
manner as seeded pastures but are not seeded with and/or logged during the last 50 years. Most agria specific forage species; thus the ground cover is cultural practices ceased when the reserve was cremade up primarily of native forb and Poaceae spe- ated in 1989, but a few pastures (including two of
cies. Although not the predominant pasture type in the study pastures) continued to be grazed through
tropical regions, unseeded pastures are found in July 1994.
In June 1995, five sites (four pasture and one
small-scale farming communities, and an understanding of their successional processes following 2" forest) were chosen based on their agricultural
history and age since abandonment (Table 1). All
abandonment is important.
This study focused on early patterns of plant pasture sites originally were cleared of all woody
succession in four abandoned unseeded pastures of vegetation. Two pasture sites had developed a unidiffering age compared to a nearby 2" forest site. form canopy (mean ca 80% canopy cover) of I?
Two of the pastures had well developed canopies guajava trees and were designated as "Guava" pasof Psidium guajava. I!guajava groves are established tures; the remaining two pastures were designated
primarily by seed dissemination from cattle, as as "Open" pastures, pastures without a canopy covfarmers often feed the fruits to their herds (So- ering of trees. All pastures had seedlings of I? guamarriba 1985, 1986, Smith et ul. 1992). Because java. It was assumed that seeds of I? guajava were
cattle do not eat the vegetative shoots (Somarriba disseminated into these pastures soon after clearing.
1995), I? guajava seedlings can grow to bear fruit Accordingly, we estimated when these areas were
within five to eight years of germination (Purseglo- cleared based on the diameter of I? guajava trees in
ve 1968, Soetopo 1991, Somarriba 1995). Conse- the pastures (Somarriba 1988a; Table 1). All pasquently, these pastures, or "guayabals" as they are tures are believed to have been subjected to light
542
Zahawi and Augspurger
TABLE 1. Area, elevation, estimated number ofyears since clearing and time since abandonment (in j~ears)$rfourpasture
sites and one Zo$rest site. Dates ofsurveys are in parentheses; two sites were surveyed three times.
Area (ha)
Open site
Open site
Guava site
Guava site
2" Forest
ca
ca
ca
ca
ca
0.10
1.0
0.30
0.15
3.00
Elevation (m)
ca
ca
ca
ca
ca
1500
1320
1350
1350
1380
grazing intensity (C. Rhoades, pers. comm.). The
2" forest site was cleared ca 25-40 years ago. It may
have been farmed briefly; however, it was abandoned soon after clearing and has since been reverting back to forest. No I? guajawa trees were
found in the 2" forest site. All pastures were located
within 1 km of each other and were generally surrounded by a mosaic of 2" forest. Nearest seed
sources were within 100 m of all pasture sites.
VEGETATION
SAMPLING.-A~
each pasture site, eight
2- X 10-m transects were surveyed in June 1995
for species richness and percent cover. Sixteen transects were sampled in the 2" forest because eight
transects could not account for its higher species
diversity adequately. Plants were identified to species level whenever possible (Appendix 1). Percent
cover for each species in each transect was determined using a modified version of Daubenmire's
cover classes (0-5, 5-10, 10-25, 25-50, 50-75,
75-95 and 95-100%; Daubenmire 1959). Median
cover values for each species at each site were then
grouped into five relative height classes: ground,
vine, shrub, sub-canopy and canopy (sub-canopy
was only considered for the 2" forest in which there
was often > 1 canopy layer). Thus, tree species at
differing life stages were found in all height classes
except for the vine "height" category. The two
younger pasture sites were surveyed a second time
in June 1996 and again in January 1997 using the
same transects (Table 1). Therefore, the study included temporal successional sequences (1, 2, and
2.5 yr since abandonment, at the same site), as well
as chronological sequences (2.5, 5-8, and 25-40
yr [2" forest] since abandonment, at different sites)
for both Open and Guava pastures.
Recruitment of tree species was quantified for
all sites in June 1996. For each site, thirty 1-m2
quadrats were randomly located and all individuals
ranging from 0-180 cm in height were counted.
To determine species number and composition of
the soil seed bank, ten randomly located soil samples (four subsamples in each sample, mean volume
Cleared
(611995)
2-5
2-5
12-15
30-40
25-40
1
5-8
1
5-8
25-40
(611996)
(111997)
2
2.5
-
-
2
2.5
-
-
-
-
per sample ca 340 cm3, depth 0-10 cm) were collected from each of the five sites ( N = 50 total) in
June 1996. Soil samples were placed in shallow
plastic containers and watered daily in a growth
chamber programmed to simulate light, temperature, and humidity ranges that were typical of a
gap in the 2" forest. All individuals were counted
and identified weekly for the first two months and
bimonthly thereafter. Samples were stirred three
times during the six-month study. Individuals were
identified to species level whenever possible, and
were removed with tweezers to minimize soil disturbance.
SAMPLING.-TOdetermine the average perABIOTIC
cent moisture of the soil, ten soil samples per site
were collected on the same day ( N = 50). The
procedure was repeated twice in July 1996. Samples were weighed, dried at 105°C for 24 hr, and
then reweighed. Bulk density was determined for
two depths: 0-5 cm and 5-15 cm. Twenty soil
sampleslsite (ten at each depth) were collected using three cylindrical aluminum rings of known volume and placed in airtight bags. Due to oven space
limitations, two smaller subsamples from each entire bag sample were weighed and dried as indicated above; their mean dry weight was used to estimate the dry weight and bulk density for the entire
soil sample in the bag.
Additional soil samples (ten samples per site,
depth 0-10 cm) were randomly collected and analyzed at the University of Illinois, Urbana, Illinois,
for texture, percent carbon, and pH. A calibrated
p H meter was used to determine the p H of a mixture of soil and distilled water on a 1:l ratio. Texture (percent sand, silt, and clay) was analyzed following the procedure of Gee and Bander (1986).
Percent carbon was analyzed using a LECO instrument, model CNS-2000 (LECO, St. Joseph, Michigan).
Repeated air temperature readings were taken
at 0 cm for all five sites using soil thermometers
that were taped to a stick. Measurements were tak-
Succession in Abandoned Pastures
12.5
lli
I Open sites
I
I Guava sites
10
Habit
3
Grass
v
Herb
g 7.5
1
543
Vine
N Shrub
2.5
Tree
0
1
2
2.5
5-8
2'
1
2
2.5
5-8
2O
FIGURE 1. Mean species richness for five habits at each of five sites contrasting Open and Guava pastures and 2"
forest. Pastures are arranged in temporal (1, 2, and 2.5 yr since abandonment, same site) and chronological (2.5, 58 yr, and 2" forest, different sites) order. Age represents years since abandonment. Values represent mean i 1 SD.
en every hour ( i 1 0 min) between 0700-1200 h
on clear days during July 1996. Five replicate temperature readings were taken for each hour at each
site.
ANALYSIS.-All results were analyzed using SAS
(SAS 1995). Repeated measures ANOVAs for species richness of the younger pasture sites (temporal
sequence) and soil moisture were done using
PROC MIXED. Two-way simple ANOVAs for all
other analyses were done using PROC GLM. It is
important to note that transects were used as replicates and sites were compared to each other; however, in this case, sites cannot represent treatments
(N = 1) and, as such, significant differences among
sites can only be interpreted as trends.
RESULTS
Results of a repeated measures ANOVA on the two
younger sites (temporal sequence) indicated that
mean species richness changed significantly over
time (df = 2, P < 0.001). Mean species richness
(mean number of species per transect) increased at
the Guava site, most notably for tree and vine species; the Open site showed a decrease in herbaceous
species (Fig. 1). A comparison between the two
sites of the distribution of habits was also significant (df = 4, P < 0.001), and changed over time
(df = 8, P < 0.01; Fig. 1). A LS Means analysis
(comparing younger Open and Guava sites)
showed that the Guava site had significantly higher
numbers of herb and tree species ( P < 0.001 and
P < 0.05, respectively), while the Open site had
greater numbers of grass and vine species ( P < 0.01
and P < 0.001).
For the chronological sequence (2.5 yr, 5-8 yr
Open and Guava pastures, 2" forest), mean species
richness among sites was significantly different (df
= 4, P < 0.001). Mean species richness was highest in the 2" forest and lowest in the 5-8 yr Open
site (Fig. 1). A p~iori comparisons between sites
indicated that Open sites (both sites combined)
had significantly lower mean species richness compared to both 2" forest (df = 1, P < 0.001) and
Guava (df = 1, P < 0.001). Mean species richness
in Guava sites was not significantly different from
2" forest (df = 1, P = 0.082). In terms of habit,
the distribution of species in Guava sites approached that of 2" forest with increasing site age,
whereas Open sites showed a strong discontinuity
in the older Open site (Fig. 1).
Total species richness (sum of species in all
transects) for both Guava sites was greater relative
to mean species richness values, but remained essentially the same for Open sites. A twofold increase was noted for all habits in Guava sites, except for vine and grass habits which remained the
same. As expected, the 2" forest site had a much
higher total number of species compared to any
pasture site (fourfold increase for all habits except
grass), and represented the largest proportion of the
total number of species in the study (Appendix 1).
Total soecies richness for the 2" forest did not level
off, indicating that the number of transects surveyed did not account adequately for the high species richness of the site.
Median values for percent cover of different
height classes in Guava sites approached those of
2" forest over time (Fig. 2). Although proportionally lower than the 2" forest, sub-canopy and canopy height classes were present in the older Guava
site. In contrast, Open sites did not show this
trend. The younger Open site appeared static and
-
544
Zahawi and Augspurger
100
90
80
$
70
60
8
40
30
u
Height class
Ground
Vine
Shrub
50
61 Sub-Canopy
20
10
ea
canopy
0
FIGURE 2. Median percent cover for five height classes and five sites contrasting Open and Guava pastures and 2"
forest. Sites are ordered and described as in Figure 1. With the exception of "vine," height classes represent relative
height categories and do not necessarily correspond to plant habit. Cover values for Aidium guajava trees in the Guava
sites are excluded from the figure.
was highly dissimilar to the height class distribution
of the older Open site.
Sorensen's similarity indices (Mueller-Dombois
& Ellenberg 1974), based on presence and comparing pasture sites to 2" forest, revealed great dissimilarities among communities (Table 2). Few
species were shared between the 2" forest and any
pasture. Guava sites, however, increased in similarity to 2" forest over time, with the oldest Guava
site (5-8 yr) having the highest similarity index. In
contrast, the similarity indices of Open sites to 2"
forest showed little change over time.
Dominance-diversity curves for Guava sites
showed an increase in the number of rare species
(defined as least-dominant species or species with
the lowest percent cover values) over time as well
as an increase in the overall number of species (Fig.
3). Open sites were static or possibly regressive.
TABLE 2.
Species dominance (based on mean percent cover
for each species) also became more evenly distributed in Guava sites over time, whereas it again appeared static or regressive in Open sites. In comparison to both pasture types, the 2" forest site had
a more equitable dominance distribution of species
and a much greater number of rare species.
Total number of recruited tree saplings (0-180
cm) was highest in the 2" forest site, especially for
the smallest height class (0-30 cm; Fig. 4). Guava
sites had a much lower number of tree recruits
compared to 2" forest, whereas tree recruits in
Open sites were minimal. Therefore, while the
number of tree recruits in Guava sites was distinctly
lower than the 2" forest, tree species were a component of plant succession in Guava sites and were
not in Open sites.
Species richness of the seed bank was higher in
Similarip indices (coefients of communiq) comparingfour pasture sites (see Table 1) and one Z0forest site
using the Sorensen index for species presence. Values range from 0 to I . Higher values indicate more similar
species assemblages among sites. k r s indicate time since abandonment.
Open
Guava
2 Yr
2.5 yr
5-8 yr
I Yr
2 Yr
2.5 yr
5-8 yr
2" Forest
0.8986
0.7429
0.7606
-
0.2553
0.2917
0.3673
-
0.4483
0.4407
0.4667
0.3243
0.4474
0.4416
0.4615
0.3273
0.3908
0.3864
0.4494
0.2121
0.475
0.5185
0.5122
0.3729
0.0909
0.1053
0.1194
0.1081
-
0.6364
-
0.5455
0.7789
-
0.5429
0 5455
0.5051
-
0.0656
0.1143
0.1854
0.2778
Open
I Yr
2 yr
2.5 yr
5-8 yr
Guava
1 Yr
2 Yr
2.5 yr
5-8 yr
-
Succession in Abandoned Pastures
1
loo open sites
- lyr'
------- 2yr
........-.
I
2.5~1
---- 54yr
*
\-
----
1
I
I Guava sites
.-8
40
-,5
30
$G
-
(----,
I
5
I
Herb
Vine
20
1
10
8
----------,
I
Habit
Grass
aJ
Z0
'---,
I
0
545
I
Shrub
El Tree
0
2 yr 5-8 yr 2 yr 5-8 yr
I
Open sites
2'
Guava sites
FIGURE 5.
Total species richness in the seed bank for
five habits at each of five sites. Year is time elapsed since
pasture abandonment.
o
Species rank
FIGURE 3. Dominance-diversity curves
the
log mean percent cover of each species against its rank.
Species are arranged from left to right in decreasing rank
order of importance. Figure legends are as in Figure 1.
1676), and was lowest for the 2" forest ( N = 84).
Similarity indices comparing the species presence
of the seed bank to aboveground species were exceedingly low, due mainly to the large number of
unknowns in the seed bank.
Temperatures were highest for the younger
Open site (Fig. 6). The older Open site had lower
temperatures than both Guava sites. As expected,
temperatures were consistently lowest in the 2" forest. Soil texture values between Guava sites and the
2" forest were not significantly different (Table 3).
the pasture sites compared to the 2" forest, and was
predominantly herbaceous (Fig. 5). All sites had
low tree species richness. The number of seedlings
established from the seed bank was highest in the
Open sites, especially for the younger site ( N =
Height class
0-30 cm
30-60 cm
12.5
60-90 cm
11
90 cm+
2 yr 5-8 yr 2 yr 5-8 yr 2'
Open sites Guava sites
FIGURE 4. Total number of recruited tree individuals
grouped into four height categories at each of five sites.
Year represents time since pasture abandonment.
1
7
8
9
10
12
Time (h)
FIGURE 6. Comparisons of mean morning temperatures at 0 cm for five sites in which the open square =
2 yr Open, open circle = 5-8 yr Open, solid square =
2 yr Guava, solid circle = 5-8 yr Guava, and solid diamond
=
2' forest.
546
Zahawi and Augspurger
TABLE 3. Mean valuesfor soil variables i I SD (N = 10). Results of Least Signzjcant D{fererzce (LSD) arznlyses,6om
one-way ANOVAs for each variable are indicated by small letters. Dzffereizt letters denote signzfictirzce values
of P < 0.05. BD = Bulk Density /g/cm3); soil moisture has a range Porn 0 to I .
2 yr Open
Percent sand
Percent silt
Percent clay
Moisture
BD (0-5 cm)
BD (5-15 cm)
pH
Percent carbon
58.92
15.26
16.86
0.68
0.80
0.95
4.97
5.38
6.01"
5.32"
i 0.97"
i 0.13"
i 0.05"
i 0.04"
i 0.22ab
2 0.95"b
k
k
5-8 yr Open
58.60
9.09
32.31
0.66
0.67
0.94
5.03
6.00
2 yr Guava
2.38"
64.90 k 3.89b
i 2.21b
16.97 -C 4.09"'
i 2.6Gb
18.13 -C 1.08"
0.70 2 0.09"
i 0.07"
0.74 i 0.08ab
i 0.05~
1.02 i O.Obb
i 0.05"
i 0.31a
4.53 2 0.13b
i 0.59"
5.89 k 0.62ab
2
Overall, the two Open sites were significantly distinct from the remaining sites. The older Open site
had the most distinct texture values, perhaps a
component of the steeper inclination of the site (ca
15"). Soil moisture values were not significantly different from each other. Bulk density values for the
0 -5 cm depth were variable and showed no distinct
patterns, whereas bulk densities for the 5-15 cm
depth were highest in the Guava sites (Table 3). In
general, Open sites had bulk density values resembling those of the 2" forest, although the reasons
for this are not known. Soils were acidic and p H
values were similar to each other with the exception
of the younger Guava site (pH = 4.53). No clear
patterns, however, emerged when p H values of pasture types were compared to each other and to the
2" forest.
A principal components analysis (PCA) com-
Principal component 1
FIGURE 7. Principal components analysis for all soil variables at five sites. Site symbols are described in Figure 6.
5-8 yr Guava
63.76
19.59
16.65
0.64
0.87
1.08
5.20
5.84
i 3.59b
i 3.3lC
i 0.6ga
2" Forest
65.09
16.70
18.23
0.67
k 0.06a
0.68
i 0.07'
i 0.06~
0.94
4.87
i 0.97"
5.17
i 0.85"~
k
7.21b
i 4.32"'
i 3.35"
i 0.13"
i O.llb
2 0.09"
i 0.30ab
i l.llb
bining all soil variables separated the older Open
site from all other sites (Fig. 7). The three main
variable loadings that contributed to the first principal component were bulk density at 0-5 cm and
5-15 cm, and percent clay. For the second component, the main variable loadings were percent
carbon, soil moisture, and percent clay. The two
components explained 31 and 20 percent of the
data, respectively. Thus, in terms of overall soil
characteristics, the most divergent site was the older
Open site.
DISCUSSION
Species richness in Guava pastures (sites with a canopy cover of I? guajava trees) was consistently
greater than in Open pastures (sites with no canopy
cover), and this disparity increased over time. Most
importantly, the number of tree species in Guava
sites increased over time and was much greater than
the number encountered in Open sites. The number of individual tree saplings was also much greater in Guava pastures compared to Open pastures.
In a previous study, Somarriba (198813) found little
difference in floristic composition between shaded
(with I? guajava trees) and unshaded, unseeded pastures. These pastures, however, were being grazed
by cattle and were manually weeded and sprayed
with herbicide on an annual basis. Results from the
study also found that growth rates of pasture grasses in shade were 49-63 percent of that in open
pastures. A study by Guariguata et al. (1995) comparing recruitment of woody individuals in plantations to pastures in Costa Rica found significantly
higher numbers of woody recruits in plantations.
Recruits in pastures were essentially absent and the
authors concluded that establishment was inhibited
by aggressive pasture grasses. Thus, the presence of
a canopy cover may give forest species an advantage
by reducing competition with grass species.
Succession in Abandoned Pastures
Purata (1986) determined that proximity to
seed source was an important factor affecting the
rate of succession in old fields; however, all pasture
sites were within 100 m of 2" forest, and distance
from seed source was considered to have minimal
impact on differences in succession. Studies also
have found that the number of seeds of tree soecies
dispersed by birds was often much lower in open
areas compared to 2" forest, due to the tendency
of frugivores to avoid clearings (Aide & Cavelier
1994, Da Silva et al. 1996, Nepstad et al. 1996,
Sarmiento 1997). Remnant trees and snags in pastures, however, have been shown to attract birds
that forage or perch; the birds then dispersed seeds
through defecation or regurgitation (Uhl et al.
1982, Guevara et al. 1986, Aide & Cavelier 1994,
Nepstad et al. 1996). A study by Sarmiento (1997)
at the same reserve found that seed rain was significantly greater in Guava pastures than in Open
pasture. Thus Guava pastures, with a "perch" canopy of I! guajava trees, enhanced representation of
bird-dispersed tree species such as Nectandra sp.,
whereas they were scarce in open sites due to frugivores avoiding open sites.
Additionally, seeds may arrive in Open pastures
but fail to survive due to the greater abiotic stresses
in the pastures. Previous studies have shown that
higher temperatures and drought decreased survival
of tree seedlings in open pastures, where drought
stress was often greater than in 2" forest (Nepstad
et al. 1990, Gerhardt 1993, Nepstad et al. 1996).
Air temperatures and exposure to direct sunlight
were much greater in the younger Open site. Rhoades et al. (1998) found that light intensity passing
through I! guajava trees in a nearby pasture was 18
percent of that in the open (at 1 m). Furthermore,
tree seedlings transplanted under the shade of those
pasture trees had survival rates of over 90 percent
compared to almost 100 percent mortality in the
open (G. Eckert, pers. comm.).
Species diversity was dominated by a few competing grass, vine, and shrub species in the younger
Open site and by the shrub Baccharis trinervis in
the older Ooen site. In contrast. Guava sites had a
much more equitable distribution of species that
ranged across all habits. Furthermore, the younger
Guava site showed an increase in the number of
rare species over time. This change was in part due
to a decrease in the abundance of certain extant
species, but was also a result of the influx of new
species into the site. In contrast, the younger Open
site had no net increase in the number of species,
although there were more rare species over time
due to a decrease in the abundance of certain species. Aide et al. (1996), in a chronosequential study
547
on abandoned pastures in Puerto Rico, found that
species equitability increased over time. Dominance-diversity curves for Guava pastures were
similar to results found by Aide et al. (1996); however, an increase in equitability was not evident in
Open pastures.
Similarity indices comparing pastures to the 2"
forest were highest for the Guava pastures; these
indices increased over time in the younger Guava
site. In contrast, a comparison of the younger
Open site to the secondary forest showed little
change over time, implying that the site was not
acquiring 2" forest species. Moreover, a comparison
of the younger Open site to its older counterpart
showed a trend toward increased similarity over
time. This trend suggests that the younger Open
site may be headed toward a community assemblage similar to that found in the older Open site;
B. trinervic was present in the younger site and its
mean percent cover increased from 1.8 percent in
the 1 yr survey to 7.5 percent in the 2.5 yr survey.
Comparisons of Guava sites to each other showed
no distinct change in similarity over time.
Soil moisture levels were not significantly different between sites, although the two sampling
times may not have accounted for the potential
variation expected between Open and Guava sites.
Soil properties varied across sites; however, the
PCA separated the older Open site from all others.
Thus, the older Open site was distinct not only in
terms of its aboveground vegetation, but also in
terms of its soil properties. This difference in soil
properties, most notably in the lower percent silt
value and the markedly larger percent clay content
of the soil, may be affecting the aboveground vegetation at the site.
Results suggest that the older Open site is in a
state of arrested succession. The site had the lowest
species richness of all sites and ca 85 percent of the
site was covered by B. trinervis. Although the site
was surveyed only once (summer of 1995), there
was no notable visual change in the composition
of the plant community in subsequent years. Baccharis trinervis forms a dense 1- to 2-m high shrub
cover that appears to inhibit the establishment of
other species by means of a dense litter layer (up
to 0.5 m) and suppressed light levels. It is not
known if the litter has allelopathic properties that
may further prevent establishment of other species.
The shrub, however, is very shade intolerant; it was
present around the open perimeter of Guava sites
but not under the I?guajava canopy. When it was
found in shade, it was strongly etiolated and was
more vine-like in habit (R. Zahawi, pers. obs.).
Therefore, it is possible that encroachment of the
548
Zahawi and Augspurger
forest from the perimeter of the older Open site
may eventually take over the site by shading out B.
trinervis; however, that process would take a long
time. Cohen et al. (1995) conducted manipulative
experiments in abandoned farmlands of Sri Lanka
that were dominated by the fern Dicranopteris linearis. D. linearis, much like B. trinervis, forms a
dense 1- to 2-m high cover, suppressing the establishment of other species. Removal of D. linearis
increased species richness at the site and initiated
early succession of herbaceous and grass species, although tree species were poorly represented. Removal of B. trinervis had similar effects (R. Zahawi,
pers. obs.). Therefore, it appears that manipulation
of such sites may be necessary to accelerate forest
succession.
Previous studies also have shown that forest regeneration often was spurred by tree sprouts, depending on the prior intensity of pasture use and
pasture age (Uhl et al. 1982, 1988; Nepstad et al.
1990); however, all woody material (including tree
stumps) appeared to have been removed from these
pastures. No tree sprouts were observed at any site,
including Open pastures which had short histories
of use as pasture prior to abandonment. The soil
seed bank also has been shown to play an important role in forest regeneration in the tropics
(Young et al. 1987, Ganvood 1989, Quintana-Ascencio et al. 1996). A review by Ganvood (1989),
however, concluded that seed banks in pastures
tend to be dominated by herbs and grasses with
few tree species. A study by Quintana-Ascencio et
al. (1996) found similar results in a variety of disturbed habitats ranging from pastures to old fields.
Results from this seed bank study concur with
those findings, and it appears that the seed bank
in these pastures contributes little to the overall
woody regeneration of the sites.
The time it takes for abandoned pastures to
return to a forested state is variable. Aide et al.
(1995) found that forest regeneration in abandoned pastures in Puerto Rico was slow for the first
10 to 15 years following abandonment, with sites
being dominated by grasses and herbs. Regeneration increased rapidly thereafter, and sites more
than 40 years since abandonment were indistinguishable from the surrounding 2" forest. Uhl et
al. (1988) estimated that it would take ca 100 years
for pastures with a history of light use to return to
a forested state, with severely degraded pastures requiring a considerably longer period of time. Results from this study indicate that Guava pastures
are on a successional trajectory toward a forested
condition, perhaps within the next 20 to 30 years.
In contrast, Open sites give little indication that
they are headed toward a forested state.
It is yet unclear if the younger Open site is
developing a community assemblage similar to its
older counterpart; as mentioned previously, B. trinervis is present in the younger Open site and the
two sites have become more similar. It is possible
that the widespread colonization of the older Open
site by B. trinervis was a random occurrence under
highly favorable conditions, without which this
Open site might have taken a different successional
course. More monitoring time of Open pastures,
however, would be necessary to determine that.
Tree seedlings (up to 0.5 m height) of I? guajava were present in both Open sites although they
were being outcompeted by B. trinervis and Poaceae species. Therefore, it is possible that Open
pastures could have developed into Guava pastures
had grazing been continued until I? guajava seedlings were well established-a period of perhaps 10
to 15 years. Once abandoned, the successional trajectory then presumably would have followed that
of Guava pastures. Regardless, results of this study
strongly support the role of trees in pastures as facilitators to succession following abandonment.
Without these tree "islands," it seems apparent that
the rate of succession from abandoned pastures to
secondary forest would be greatly impeded.
ACKNOWLEDGMENTS
This study was supported by grants from Sigma Xi, the
Center for Latin American and Caribbean Studies, and
the Department of Plant Biology at the University of 11linois. Jake Gerlie provided help with field data collection.
We thank Michelle Wander for the use of her lab to perform soil analyses. Statistical advice and interpretation
were provided by Susan Aref, Jeff Brawn, and Sophia
Gehlhausen. We thank Danilo Chinea and Steve Frankel
for reviewing final drafts of this manuscript, and Roberto
Barreiro for translating the abstract into Spanish. KJe also
thank Grady Webster for assistance in plant identification
and all the employees at the Reserva Maquipucuna and
those involved in Proyecto PIES for their support and
help during this research.
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APPENDIX 1. A listing of all species collected during the study. Specimens were identjfied
to the species level whenever
possible. Habit codes are G = Grass, H = Herb, V = Kne, S = Shrub, and T = Pee Sites are
arranged as follozus: 1 = Younger Open, 2 = Older Open, 3 = Younger Guava, 4 = Older Guava,
and 5 = 2"Forest site.
Family
Acanthaceae
Amaranthaceae
Amaryllidaceae
Apiaceae
Apocynaceae
Aracaceae
Araceae
Araliaceae
Arecaceae
Asclepiadaceae
Aspleniaceae
Asteraceae
Begoniaceae
Boraginaceae
Clusiaceae
Cucurbitaceae
Cyatheaceae
Cyclanthaceae
Species
Blechzlm pyramidatum
Dicliptera sp.
Hygrophila gzlianensis
Jzlstjcja pectoralis
J. secunda
Unknown sp.
Alternathera porrigens
Cyathula achyranthoides
Hypoxis decum bens
Hydrocogle lez~cocephala
Mesechites sp.
Geonoma undata
Unknown sp.
Anthurizlm ochreatum
Anthurium sp. 1
Anthurium sp. 2
Anthzlrizlm sp. 3
Dieffenbachia sp.
Philodendron ventricosum
Oreopanax sp.
Sheflera pen tundra
Prestoea trichoclada
Fischeria sp. 1
Fireheria sp. 2
Diplazium sp. 3
AgeratumiFleischmannia sp.
Baccharis trinervis
Elephantopus mollis
Hebeclinium sp.
Heterocondylus vitalbae
Mikania cordifolia
Aeudelephantopus spicatus
Wrnonia patens
Begonia parvjjora
Cordia cylindrostachya
Chrysochlamys dependens
Clusia sp. 1
Cltlsia sp. 2
Vismia baccj$ira
Callisia gracilis
Commelina obliqua
Commelina sp.
Gipogandra serrulata
Melothria pendula
Psiguria pedata
I? triphylla
Cyathea sp.
AsplundiaiSphaeradenia sp.
Cyclanthus sp.
Authority
Nees.
Jacq.
Vahl
(Jacq.) Kuntze
Moq. DC.
L. Chain. & Schl Madison
Harms.
(Lamarck) Persoon
H.B.K.
(DC.) King & Rob.
(L. f.) Willdenow (Jussieu ex Aubl.) Rohr H.B.K. Poeppig & End. (R. & P.) Roem. & Sch PI. & Tr. (L.) Triana & Planch.
Habit
Site presence
Succession in Abandoned Pastures
551
APPENDIX 1. Continued.
Family
Cyperaceae
Euphorbiaceae
Fabaceae
Lamiaceae
Lauraceae
Melastomataceae
Meliaceae
Moraceae
Musaceae
Myristicaceae
Myrsinaceae
Myrtaceae
Onagraceae
Oxalidaceae
Piperaceae
Species
Cyperus dtfSUsus
C. hermaphroditus
C. lz~zz~lae
Kyllingia pz~mila
Acalypha diuers@lia
Hyeronima cf. duquei
Phyllanthz~sniruri
Sapium stylare
Sapium sp.
Tetrorchidizlm andinum
Cassia bacillaris
Desmodium adscendens
D. canum
E. megistophy/la
lnga denszjora
I quaternata
lnga sp.
Hyptis atrorubens
H. obtus$lia
Hyptis sp.
Salwia macrophylla
Nectandra obtzlsa
Nectandra sp. 1
Nectandra sp. 2
Ocotea sp.
Unknown sp. 1
Unknown sp. 2
Eschweilera sp.
Cuphea racemosa
Cuphea strigulosa
Unknown sp.
Pavonia castanaefolia
Sida sp.
Urena lobata
Blakea qzladrzj'lora
Conostegia szperba
Miconia aeruginosn
Ossaea micrantha
Tibozlchina IongEfolia
7: ovalzfolit~m
Gzlarea sp.
Cecropia monostachya
Clarisia bzj'lora
Firus sp.
Morus insignis
Sorocea sp.
Heliconid sp.
Otoba gordonifolia
Ardisia zuebsteri
Ardisia sp.
Weigeltia cf. gozldotiana
Unknown sp.
Eugenia dibrachiata
Myrcia sp.
MyrciantheslEugenia sp.
Psidium guajava
Fzlchsia sp.
Oxalis latifolia
Peperomia bicolorlangularis
Peperomia sp.
Piper bzrllost~m
Authority
Habit
S ~ t epresence
Vahl
(Jacq.) Standl.
(L.) Retzius
Michaux
Jacq.
Cuatr.
L.
Muell. Arg.
Muell. Arg.
L. f.
(Gmelin) Schinz & Thell.
Diels
Bentham
Poeppig
Poiteau
Benth.
T
T
T
(L. f.) Sprengel
H.B.K.
St. Hilaire & Naudin
L.
D . Don ex Naud.
Naud.
(Swartz) Mac. ex Cog.
(Vahl) Baillon
R. & I?
Bureau
H
H
v
S
S
S
v
1
1
1
3
4
3
3
4
4
3
4
4
4
1
3
S
H
H
3
3
5
5
5
5
5
5
5
5
5
5
5
5
5
5
5
5
T
T
T
T
T
T
S
3
S
S
SIT
S
McVaugh
v
v
v
L.
T
5
5
5
5
T
T
T
Pipoly
5
5
5
1
2
3
4
H.B.K.
HIE
H
C. DC.
v
3
5
5
552
Zahawi and Augspurger
APPENDIX 1.
Family
Poaceae
Polygalaceae
Ranunculaceae
Rubiaceae
Scrophulariaceae
Selaginellaceae
Solanaceae
Tiliaceae
Ulmaceae
Urticaceae
Valerianaceae
Verbenaceae
Vitaceae
Zingiberaceae
Continued
Species
I? fiiedrichstahlii
I? mareqzlitense
I? phytolaccaefolium
I? sqzlamuloszlm
Piper sp.
Andropogon bicornis
Axonopus scoparizls
Oplismenzls hirtellus
Paniczlm polygonatum
Panicum sp.
Paspalurn conjzlgatum
I? panicz~latum
L' saccharoides
Aeudechinolaena polystachya
Setaria sphacelata
Sporobolus indiczls
Monnina patula
Clematis sericea
Borreria laevis
Faramea eurycarpa
H o f i a n n i a sp.
Laden bergia macrocarpa
Palicozlrea sp.
Psychotria brachiata
I? gentryi
I? racemosa
I? steyermarkii
Sabicea villosa
Unknown sp.
Castilleja arvensis
Selaginella geniculata
Capsicum lycanthoides
Cestrzlm megalophyllum
C. peruvianzlm
Cestrum sp.
Solanum acerz~olizz
S. oval~oliz~m
Triumfetta grandiflora
Trema mic~antha
Boehmeria cazldata
Clibadium laxus
Pilea anteocensis
I? pu bescenslcostata
Urera b a c c ~ r a
kleriana scandens
Aeg@hila alba
Cornutia odorata
Lantana camara
Stachytarpheta cayennensis
Verbena littoralis
Cissus sp.
Renealmia dilicocalyx
Authority
C. DC.
Habit
S
S
Opiz
S
SIT
S
L.
G
(Fluegge) Kuhl.
G
(L.) Beauvois
G
Schrader
G
G
Bergius
G
L.
G
Nees. ex Trinius
G
H.B.K.
G
(Schumach.) Stapf & C . E. G
Hubb
(L.) Brown
G
Chod.
S
DC.
V
(L.) Grisebach
V
S
H
Vahl
T
V
Swartz
S
(Dwyer) C. M . Taylor
S
S
S
Will. ex Roem. & Sch.
V
S
Schlecht. & Cham.
H
H
S
Dunal
S
S
S
Dunal
S
H
Vahl
S
(L.) Blu~ne
T
Swartz
T
S. F. Blake
S
H
H
(L.) Guadichaud
S
V
Mold.
T
Poeppig ex Scha.
T
S
L.
(Richard) Vahl
H
H.B.K.
H
V
S
Site presence
1
2
3
3
4
5
2
3
3
4
4
5
5
3
3
3
4
3
3
4
4
3
3
3
4
4
1
1
5
1
1
1
1
2
5
1
1
1
1
1
5
5
5
5
5
5
5
5
3
1
3
4
5
1
5
5
3
3
1
4
4
4
5
5
2
4
4
5
5
5
5
3
1
3
1
3
3
3
4
4
5
5
5
5
4
5
5