A test of the escape and colonization hypotheses for

Transcription

A test of the escape and colonization hypotheses for
Plant Ecol (2007) 190:245–258
DOI 10.1007/s11258-006-9205-5
ORIGINAL PAPER
A test of the escape and colonization hypotheses for
zoochorous tree species in a Western Amazonian forest
Pablo R. Stevenson
Received: 9 February 2006 / Accepted: 4 August 2006 / Published online: 5 September 2006
Springer Science+Business Media B.V. 2006
Abstract In order to assess the importance of
seed dispersal (escape and colonization hypotheses), I used transplant experiments for seeds and
seedlings of 5–11 plant species with fleshy fruits in
a lowland tropical forest (Tinigua National Park,
Colombia). I controlled seed density, distance to
parental tree, and habitat type. I monitored seed
removal, seedling survival, and seedling growth
during the first year of development for an average of 554 seeds and 169 seedlings for each species. I supplemented the experimental results with
measurements of natural recruitment. I found
little support for the escape hypothesis during the
seed and seedling stages. For six species that
showed differences in seed removal associated
with distance, five showed highest removal away
from, than close to parent trees, suggesting
predator satiation. Seedling survival during the
first year was not consistently associated with low
densities and long distances from parent trees.
For the majority of species, seedlings did not
survive flooding in low basins, and there was
P. R. Stevenson
IDPAS, State University of New York at Stony
Brook, Stony Brook, NY, USA
Present Address:
P. R. Stevenson (&)
Departamento de Ciencias Biológicas, Universidad de
Los Andes, Cr. 1 No. 18a-10, Bogota D.C., Colombia
e-mail: [email protected]
growth advantage for most plant species in canopy gaps. These differences imply advantages for
seed dispersal to adequate habitats, as predicted
by the colonization hypothesis. In contrast to
experiments, strong negative distance-dependent
effects were evident when analyzing natural
recruitment patterns. The ratio between saplings
and seedlings was higher away from parent trees
for the species with enough recruitment to be
analyzed and this suggests that a negative distance-dependent effect may also occur after
seedling establishment. This pattern is suspected
for several other species, but an analysis with
some of the other most common trees showed a
variety of negative, neutral, and positive distance
dependent effects. This study emphasizes the
importance of long-term studies to asses the role
of seed dispersal.
Keywords Janzen–Connell distance effects Æ
Seed clumping Æ Seed dispersal Æ Tinigua Park
Introduction
The great majority of plant species in tropical
forests have specialized mechanisms to disperse
their seeds (Ridley 1930; van der Pijl 1972), suggesting large benefits associated with the process
of seed dispersal. The advantages associated with
seed dispersal have been addressed by three main
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246
hypotheses: escape, colonization and directed
dispersal (Howe and Smallwood 1982). According to the escape hypothesis, dispersed seeds have
a higher probability of survival because they
avoid predation, diseases, and intraspecific competition, which are hypothesized to be strongest
below the parental tree. This theory is part of a
broader idea to explain the importance of seed
dispersal as well as to provide an explanation for
the high diversity of plants in tropical forests,
which is known as the Janzen–Connell hypothesis. The arguments to explain the advantage of
dispersing seeds were based on the presumptions
that below the parental tree it is easier for predators to find seeds or seedlings (Janzen 1970),
there is a high possibility for diseases to propagate (Augspurger 1984), and there is more intraspecific competition between seedlings than there
is away from the tree (Connell 1971). These effects may be caused either by a high density of
seeds and/or seedlings below parental plants
(density effect) or by plant enemies being more
likely located near or are attracted to parental
plants (distance effect; Janzen 1970). The main
prediction of the escape hypothesis is that seeds
falling under or near the parental crown or at high
densities have a lower probability of survival than
dispersed seeds. The colonization hypothesis
states that for some plant species there are places
with adequate conditions for germination,
recruitment and later development (Howe and
Smallwood 1982). According to this hypothesis,
dispersal away from the parental plant enhances
the probability that seeds will arrive at those
adequate sites, which could be associated with
different soil types, light conditions, etc. In some
cases the dispersal agents may carry the seeds
directly to places with particularly good conditions for germination and development, and this
type of advantage is addressed by the directed
dispersal hypothesis. The main prediction from
the colonization hypothesis is that seeds dispersed
to distinct forest conditions will have different
probabilities of success. However, this prediction
is not exclusive of this hypothesis. For example, if
one considers a forest condition to be equal to a
long distance from a parental tree, then both the
escape and the colonization hypotheses would
have similar predictions in terms of plant survival.
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Plant Ecol (2007) 190:245–258
Despite this unavoidable ambiguity between the
hypotheses and for the sake of simplicity, in this
paper I will consider evidence supporting the escape hypothesis to be data showing higher survival of propagules leaving the proximity of the
parents, and evidence for the colonization
hypothesis to be the data showing differences in
survival associated with three different forest
conditions (gaps, terra firme, and flooded forests).
Many studies have shown dispersal advantages
related to strong negative density and distance
effects for a large number of species (Wills et al.
1997; Harms et al. 2000; Hubbell et al. 2001;
Wright 2002; Terborgh et al. 2002 and references
therein). However, more studies are needed because the predictions of the escape hypothesis are
far from being always supported (Hyatt et al.
2003), the precise mechanisms causing the negative effects remain obscure, and the analyses are
still limited to only a few study sites and plant–
animal disperser systems (Russo and Augspurger
2004). This is in part due to the difficulties in
doing integrated studies of plant regeneration,
because such studies must include a variety of
stages in the life history of plant species (Schupp
and Fuentes 1995), and there is temporal variation in the strength of the factors that affecting
plant mortality (Augspurger 1983; Schupp 1990).
The strongest methods to test plant demographic models are based on cohort monitoring
through time (Hubbell et al. 2001). An alternative is to compare different cohorts in the same
population (Clark and Clark 1984; Terborgh et al.
2002), under the assumptions that seed production and mortality patterns are constant over
time. Although these assumptions are not always
valid (DeStevens and Putz 1984; Schupp 1990;
Wright et al. 1999), the approximation to demographic processes from instantaneous vegetation
surveys is the only tool available for some localities. Grouping data into categories containing
plants of similar age (e.g., seedlings and saplings)
may reduce the interannual variation in patterns
of seed production and predation.
In this study, I gathered information on seed
removal rates of seeds on the forest floor and
survival rates of seedlings for a set of plant species
at Tinigua National Park, Colombia. In addition I
made a static analysis of plant demography for
Plant Ecol (2007) 190:245–258
some of the most abundant plant species in the
forest. The goal was to examine the main
hypotheses regarding the importance of seed
dispersal processes in plant recruitment (escape
and colonization). I used an experimental
approach to assess the influence of dispersal distance, seed and seedling density, and habitat type,
as factors determining survival during the first
year of development for 11 plant species. Because
it is difficult to collect long-term demographic
data for tropical trees, I use estimates of seedling
and sapling densities to compare natural establishment patterns below and away from parental
trees.
Methods
Study site
The study site is located in a tropical lowland
forest on the eastern border of Tinigua National
Park (201,875 ha), between the eastern Andes
and the Sierra de La Macarena, Departamento
del Meta, Colombia (240¢ N and 7410¢ W, 350–
400 m above sea level). The study site, Centro de
Investigaciones Ecológicas La Macarena (CIEM)
is on the west margin of the Rı́o Duda. Rainfall is
markedly seasonal in the region, with a
2–3 month dry period occurring between
December and March (Stevenson 2002). Average
annual precipitation at the station for three years
was 2782 mm. Data for this study was collected
between December 1999 and December 2001.
Data collection and analyses
I used transplant experiments for seeds and
seedlings to test the consequences of seed dispersal for 11 animal-dispersed tree species
(Table 1). Plant species were chosen because they
are important elements in the diets of several
frugivores in the Tinigua community, and display
a wide variety of phenological patterns, seed sizes, distributions, and fruit morphologies. These
species are consumed by both birds and primates,
which usually drop intact seeds in their feces
(Stevenson 2002). I included several plant species
with different ecological strategies to allow for
247
broader conclusions regarding the importance of
seed dispersal. However, some analyses were not
possible for all species.
Tests of the escape hypothesis
I set up six transects under each of at least five
different trees for each species, with the bole of
the fruiting tree as the starting point of each
transect. The six transects were uniformly distributed at 60 angles and directed in such a way
that none of them crossed different forest types or
another fruiting tree of the same species. If the
latter occurred, I located additional transects at a
different parental tree. I created three stations
along each transect, each a different distance
from the trunk of the focal tree (2, 10, and 50 m),
which includes the range at which distancedependent effects are known to vary in tropical
forests (Hubbell et al. 2001), including non-dispersed seeds, seeds spat out near the periphery of
the tree crown and seeds dispersed away from the
tree. At each station I placed seeds in an area of
0.3 m2, using one of three density treatments,
varying with seed size. For large seeds (> 1.5 cm
maximum dimension), the densities were 1, 2 and
10 seeds; for medium-sized seeds (1.5–0.7 cm): 2,
5 and 20; and for small seeds (< 0.7 cm): 10, 20
and 60. These densities were chosen because they
reflect seed numbers typically contained in
deposits created by frugivores in this community
(Stevenson 2002). The density of seeds and
seedlings was set at random in such a way that
there was one station at every distance for the
high-density treatment, two for the medium
density treatment, and three for the low-density
treatment. This design with more replicates of
low-density stations was used to reduce the standard error among treatments that is usually very
large for low-density treatments. I used flagging
tape to mark each station at approximately 1.5 m
height. The area around the seeds was initially
cleared of litter, a procedure that may increase
the probability of encounter by rodents (Cintra
1997), but this effect should have affected all
treatments in a similar way.
I checked the seeds every day during the first
week, then once a week during the next 2 months,
and finally at monthly intervals. At each inspection
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Plant Ecol (2007) 190:245–258
Table 1 List of plant species included in the analyses of recruitment patterns at Tinigua National Park, Colombia (data
from Stevenson et al. 2000 and Stevenson 2002, forest types according to Stevenson et al. 2004)
Species
Diaspore
width (mm)
Husk/fruit
(g/g ± SD)
Fruiting period
Density
(ind/ha ± SD)
Forest type
Cecropia membranacea
Hyeronima alchorneoides
Cecropia sciadophylla
Apeiba aspera
Pourouma bicolor
Gustavia hexapetala
Garcinia macrophylla
Hymenaea oblongifolia
Bursera inversa
Virola flexuosa
Spondias mombin
1
2
2
2
7
11
11
11
12
13
16
Unprotected
Unprotected
Unprotected
0.76 ± 0.09
0.16 ± 0.04
0.57 ± 0.07
0.35 ± 0.08
0.60 ± 0.10
0.29 ± 0.01a
0.44 ± 0.05a
Unprotected
Jul–Oct
Dec–Jan
Nov–Mar
Sep–Oct
Dec, Jun
Nov–Mar
Apr
May–Jul
Jul–Oct
Dec–Mar
May–Jul
8.2
2.5
0.6
4.4
4.4
9.3
3.1
2.1
0.9
2.5
4.7
Flooded
Mature
Open
Mature
Mature
Mature
Mature
Mature
Fl & Ma
Mature
Mature
±
±
±
±
±
±
±
±
±
±
±
33.9
3.3
0.5
5.3
4.4
8.6
3.4
2.5
2.6
1.7
7.1
Data on the main frugivorous species that visit each plant can be found in Stevenson 2002 (Table 7.2.2)
a
Dehiscent
the number of removed seeds was recorded, as
well as tracks of potential seed predators or secondary dispersers. I assumed that all removed
seeds were consumed, which was the case in other
studies in Western Amazonia (Notman and
Gorchov 2001; Russo and Augspurger 2004),
where rodents are the main seed predators.
I gathered and stored seeds in good condition
for < 2 weeks and the experiments were set up
just when the population of the species stopped
producing fruits. By doing this, I minimized the
probability of natural seed rain altering the
counts at the stations. Data on surviving or germinated seeds were summed for each density and
distance treatment per tree to avoid problems of
spatial pseudoreplication that would result from
treating within tree stations as independent sample units. I do not include information on germination rates in this study, because these kinds of
data has been published in other papers (Stevenson 2000; Stevenson et al. 2002). I analyzed
these results using the Kaplan-Meier procedure
for survival analysis in JMP 3.2.2 (SAS Institute
1994). Although this is a powerful tool to compare survival curves of different treatments, the
program does not allow testing for interactions. In
order to assess the existence of distance–density
interactions I analyzed distance effects separately
for each density treatment, and the existence of
strong interactions was noted when the distance
dependent results were opposite and significant
for different density treatments.
123
I used a similar experimental design to test the
effect of density and distance on the survival of
seedlings from the selected species. Seedlings
were transplanted at fixed densities of 1, 2, or 10
to the same stations used in the previous experiment. In this experiment I counted the number of
surviving seedlings at monthly intervals, and
measured the height of the seedling as an
approximation of plant vigor. Causes of seed and
seedling mortality were noted when evident. In
addition to direct observations in the field (e.g.,
presence of insect larvae in seeds, seed remains,
evidence of damping-off, etc.), I used Sherman
traps for small and medium sized rodents with
seeds of the focal plant as bait in order to identify
potential seed predators.
Test of the colonization hypothesis
I carried out transplant experiments for the seeds
and seedlings of eight of the plant species in three
different forest conditions: closed-canopy welldrained forest, canopy gaps in well-drained forest,
and closed-canopy flooded forest. I did not use
gaps in flooded forest because the fast growing
Heliconia spp. in this area usually prevents high
light intensities from reaching the forest floor for
extended periods. Consequently, gaps in the
flooded forest might play a minor role in plant
recruitment. I selected 10 different sites within
the study area for each habitat condition and one
station was set up at each site. For most plant
Plant Ecol (2007) 190:245–258
species, the stations at 50 m from parental trees in
previous experiments were used as the stations
for transplanted seeds and seedlings to closedcanopy well-drained forest.
I monitored seeds until they were all removed,
consumed in place, or germinated. For small seeded species (e.g., Cecropia spp.) it was difficult to
recount seeds; for instance rainfall moved seeds
away from stations and seeds were difficult to recover. For such cases, only one recount was done
at about the time when seeds started to germinate
(ca. after 1 week). On average, I monitored
seedlings monthly for 1-year after the initial
transplant for all species studied. In the cases of
small-seeded plants complete mortality occurred
in gaps within the first month after transplant and
therefore their survival and growth patterns were
not analyzed. I measured seedling height at
monthly intervals. For seedling vigor, I used proportional growth at the end of observation:
249
was defined from the smallest reproductive tree
know in the area, from a database of 7,674 records of fruiting trees in phenological transects or
in the diets of different primate species (based on
Stevenson et al. 1998; Stevenson 2004).
In order to assess if distance-dependent effects
can occur after 1 year, I analyzed the association
between the number of saplings and seedlings,
and the presence of adult plants. I classified all
the seedling and sapling quadrats according to
parental presence, using two different scales. I set
the scales as a parent present within the same
10 · 10 m2 or 30 · 30 m2 quadrant. The results are presented in terms of the sapling/seedling ratios, and the significance of the association
between the number of saplings and seedlings
with the presence of adult trees was assessed by G
tests in 2 · 2 contingency tables.
Results
Growth ¼ ðfinal size - initial sizeÞ= initial size:
Transplant experiments: escape hypothesis
Natural seedling and sapling distribution
In order to assess the probability of recruitment
for the most abundant trees in the forest I used a
static demographic analysis based on the number
of seedlings and saplings in different habitat
conditions. Seedlings were broadly defined,
including young and old seedlings, as plants less
than 1.3 m tall or less than 1 cm diameter at
breast height (DBH). Saplings were defined as
plants between 1 and 5 cm DBH. I counted the
number of seedlings and saplings of all tree species in 463 quadrats, most of them within 5-hectare plots where all woody plants (DBH > 5 cm)
had been identified and mapped in 100
(10 · 10 m2) subplots (Stevenson et al. 2004).
Quadrat size was 4 m2 and 25 m2 for seedlings
and saplings respectively, and I recorded the
presence of parental plants of the focal study
species within or adjacent to the subplot. For
dioecious species, only mature female trees were
included in the analyses, unless I was uncertain
about tree gender. In those cases the trees were
included as parents if they fit in the adult class
category for that species. The adult tree category
I found few effects of distance from parental tree
on seed removal rates (Table 2). In 6 out of the 11
species analyzed I found a significant effect, and
in five of these cases there was lower removal
near the parental tree than far from it, opposite to
the pattern predicted by the escape hypothesis.
Similarly, I found significant density effects in
only three species; and removal did not decrease
at low seed densities (Table 2). I found evidence,
from behavioural observations and traps baited
with seeds, that generalist predators, such as small
rodents were the main seed removers. I observed
at least three species of mice consuming Gustavia
hexapetala and Pourouma bicolor seeds. The
plant species with most seed predators reported
was Garcinia macrophylla, which included small
rodents, acouchys (Myoprocta sp.), curassows
(Crax alector and Mitu salvini), and even bees.
Seedling survival was higher away from
parental trees for two of the seven species analyzed (Table 3). Contrary to the predictions of the
escape theory, seedling survival was not lowest in
high-density treatments for any species; in two
species survival was actually greater at high densities.
123
123
2
10
50
2
10
50
2
10
50
2
10
50
2
10
50
2
10
50
2
10
50
2
10
50
2
10
50
2
10
50
2
10
50
Apeiba
aspera*
24.2
19.0
16.7
35.3
36.5
29.9
9.5
12.2
8.5
31.1
23.4
23.8
9.5
9.2
9.7
4.3
5.6
9.1
31.0
21.3
16.8
198.9
180.9
165.3
43.1
37.9
46.9
0.50
0.65
0.64
0.70
0.69
0.62
2.5
2.2
2.2
2.8
2.9
2.8
0.7
1.4
0.9
2.7
2.3
2.3
0.2
0.2
0.2
0.6
1.0
1.0
2.8
2.2
1.8
4.4
6.1
8.8
5.8
6.3
7.9
0.09
0.10
0.09
0.09
0.09
0.10
Mean
time (days
± SE)
0.21
0.74
0.9
6.2
19.0
20.4
1.2
6.5
6.3
2.6
6.3
v2
0.55
0.04
0.04
0.26
0.04
0.81
0.48
0.6
0.04
< 0.0001
< 0.0001
P
82 (1750)
35 (780)
102
256
568
256
780
543
256
256
543
n
High
Medium
Low
High
Medium
Low
High
Medium
Low
High
Medium
Low
High
Medium
Low
High
Medium
Low
High
Medium
Low
High
Medium
Low
High
Medium
Low
High
Medium
Low
High
Medium
Low
Density
10.0
6.7
8.6
34.3
33.0
33.8
10.6
10.1
8.3
21.2
35.2
26.6
9.5
9.5
9.5
5.6
6.6
8.8
24.4
18.5
24.5
134.6
102.7
133.1
47.1
40.5
30.6
0.27
0.66
0.53
0.51
0.66
0.73
1.0
0.9
1.5
2.1
3.4
4.1
0.8
1.2
1.2
1.7
2.9
3.8
0.2
0.2
0.3
0.5
1.2
2.0
1.8
2.3
3.3
4.4
4.6
6.3
5.1
8.1
8.0
0.09
0.10
0.09
0.13
0.09
0.07
Mean
time (days
± SE)
1.1
4.49
3.2
5.5
7.7
1.4
0.2
17.7
4.2
0.31
4.0
v2
0.34
0.02
0.2
0.06
0.02
0.50
0.9
0.0001
0.12
0.86
0.13
P
82 (1750)
35 (780)
102
256
568
256
780
543
256
256
543
n
Flooded
Gap
Mature
Flooded
Gap
Mature
Flooded
Gap
Mature
Flooded
Gap
Mature
Flooded
Gap
Mature
Flooded
Gap
Mature
Flooded
Gap
Mature
Flooded
Gap
Mature
Flooded
Gap
Mature
Forest
0.51
0.55
0.00
0.64
26.1
25.9
9.1
1.8
17.2
11.1
95.2
142.0
165.3
6.9
70.9
46.9
3.7
5.1
8.5
11.0
13.1
17.8
16.5
17.1
6.6
0.19
0.18
0.08
0.07
5.9
5.8
1.0
0.1
3.4
1.0
5.3
10.0
8.8
1.2
3.4
7.9
0.5
1.8
1.2
2.1
2.9
1.5
1.6
1.3
0.9
Mean
time (days
± SE)
2
0.03
38.2
203.4
1.0
69.6
19.4
8.9
8.6
50
v2
0.87
< 0.0001
< 0.0001
0.60
< 0.0001
< 0.0001
0.01
0.01
< 0.0001
P
13 (1260)
20 (1260)
233
126
331
126
252
142
583
n
Data from Stevenson et al. (2005)
F statistics instead of v2
* Strong distance–density interactions (see methods)
b
a
The table shows mean removal time and standard error of seeds remaining in stations varying in distance, seed density, and forest type. The analyses provided v values comparing survivorship
curves among treatments, and significant differences (P < 0.05) are indicated in bold. For Cecropia spp. ANOVA tests were made and the proportion of seeds remaining in stations is shown, as
well as the number of samples and the total number of seeds in parenthesis
Cecropiaa
sciadophylla
Cecropiaa
membranacea
Virola
flexuosa
Spondias
mombin
Pourouma
bicolor
Hymenaea
oblongifolia
Hieronima*
alchorneoides
Gustavia
hexapetala
Garcinia
macrophylla
Bursera
inversa
b
Distance
Species
Table 2 Results of seed removal experiments for 11 plant species at Tinigua National Park, using the Kaplan–Meier method for survival analyses
250
Plant Ecol (2007) 190:245–258
2
10
50
2
10
50
2
10
50
2
10
50
2
10
50
2
10
50
2
10
50
Garcinia
macrophylla
2.0
2.8
3.2
4.7
6.3
3.0
5.2
5.8
3.1
4.2
5.2
5.0
1.8
1.4
2.3
23.5
44.1
2.9
41.2
52.9
5.9
0.4
0.4
0.4
0.5
0.6
0.3
0.4
0.4
0.3
0.3
0.4
0.4
0.2
0.2
0.3
6.9
8.7
1.7
13.9
12.1
9.0
Mean time
(month ± SE)
4.0
1.0
9.3
1.7
12.2
3.8
8.5
v2
0.03
0.4
0.01
0.42
0.002
0.15
0.01
P
34
34
255
255
255
255
180
n
High
Medium
Low
High
Medium
Low
High
Medium
Low
High
Medium
Low
High
Medium
Low
High
Medium
Low
High
Medium
Low
Density
10.6
8.3
10.1
5.1
5.8
6.4
4.8
4.7
5.2
24.4
24.5
18.5
1.9
1.5
2.1
33.3
8.3
11.1
30.0
37.5
38.9
0.8
1.2
1.2
0.4
0.7
0.8
0.3
0.5
0.5
1.8
3.3
2.3
0.2
0.2
0.3
17.4
5.6
7.6
14.4
12.5
11.8
Mean time
(month
± SE)
0.1
8.7
2.9
3.2
1.52
2.0
16.7
v2
0.89
0.0009
0.23
0.20
0.47
0.37
0.0002
P
34
34
255
255
255
255
204
n
a
Flooded
Gap
Mature
Flooded
Gap
Mature
Flooded
Gap
Mature
Flooded
Gap
Mature
Flooded
Gap
Mature
Forest
2.5
4.3
2.7
3.2
3.7
5.5
2.9
5.2
4.9
1.6
5.4
4.8
0.6
7.1
1.9
Mean
time
(month
± SE)
F statistics instead of v2. Forest type analyses are not shown because all seedlings in canopy gaps died before the first census
Column headings are the same as in Table 2, except for the time scale that corresponds to months in this table
Cecropiaa
sciadophylla
Cecropiaa
membranacea
Spondias
mombin
Pourouma
bicolor
Hymenaea
oblongifolia
Gustavia
hexapetala
Distance
Species
0.5
0.7
0.2
0.2
0.4
0.3
0.3
0.3
0.2
0.2
0.4
0.2
0.1
0.5
0.1
201.6
103.7
25.6
26.5
11.1
v2
0.004
< 0.0001
< 0.0001
< 0.0001
< 0.0001
P
Table 3 Results of seedling transplant experiments for seven plant species at Tinigua National Park, using the Kaplan–Meier method for survival analyses
455
455
455
455
263
n
Plant Ecol (2007) 190:245–258
251
123
252
Plant Ecol (2007) 190:245–258
Transplant experiments: colonization
hypothesis
Differences in seed removal were associated with
forest type for the majority of the species. The
most common pattern was high removal rates in
flooded forests (e.g., Ga. macrophylla, G. hexapetala, P. bicolor and Virola flexuosa). The seedlings of all seven species that could be analyzed
showed low survival rates in the flooded forests,
and seedling survival was especially low at periods of flooding in the forests on low basins. Only a
few seedlings of Ga. macrophylla and G. hexapetala were able to survive flooding periods (as
resprouting seeds in the former case). Higher
seedling survival in gaps was observed in three
species (Table 3), and expected in two others
(Cecropia spp.), but a period of drought combined with high solar irradiation killed all the
small Cecropia seedlings soon after they were
transplanted to gaps.
For three out of five species available for
growth analyses, I found greater growth rates in
canopy gaps (Table 4). For two shade tolerant
species there was no significant effect of forest
type on growth (G. hexapetala and Ga. macrophylla). The only case of significant density or
distance effects on seedling growth was found in
P. bicolor. However, higher growth at a distance
from the parental tree was due only to the formation of a large canopy gap adjacent to a highdensity station during the study.
Natural seedling and sapling distribution
Considerable numbers of seeds fall below their
tree crowns (Stevenson 2002), and some seeds
experience no negative density or distance effects
on survival until the seedling stage. Several species (such as G. hexapetala, P. bicolor, Hymenaea
oblongifolia, and Cecropia membranacea) showed
larger seedling densities under parental crowns
than away from them (Fig. 1a). This pattern was
observed at both small and medium scales,
though the differences were usually accentuated
at the smallest scale. For the remaining species
seedling densities were low, and for none of the
remaining species was I able to detect differences
associated with parental presence.
However, the differences in seedling density
vanished when looking at sapling densities and
parental distributions (Fig. 1b). Only for one
species, C. membranacea, was there a considerable density of saplings close to adult trees, and
those were from plots restricted to river margins,
where saplings can occur at high densities very
Table 4 Differences in the proportional growth of seedlings from different plant species at Tinigua National Park, which
were transplanted in three different treatments of distance to parental trees, seedling density, and forest type
Species
Factor
6 months
F
Gustavia hexapetala
Pourouma bicolor
Spondias mombin
Garcinia macrophylla
Hymenaea oblongifolia
Distance
Density
Forest type
Distance
Density
Forest type
Distance
Density
Forest type
Distance
Density
Forest type
Distance
Density
Forest type
2.8
0.4
12.1
3.9
0.4
(29.5)
0.2
0.3
11.9
0.5
(3.2)
2.2
2.8
0.41
12.1
End of study
P
<
<
<
<
0.06
0.66
0.001
0.02
0.66
0.001
0.86
0.88
0.001
0.6
0.2
0.12
0.06
0.66
0.001
N
F
92
92
147
96
96
141
16
16
81
27
27
53
92
92
147
0.34
0.05
(1.7)
(8.4)
(2.0)
1.88
0.27
0.81
0.58
7.16
0.37
4.1
P
N
0.72
0.95
0.19
0.02
0.36
0.07
0.87
0.37
0.56
< 0.001
0.69
0.02
73
73
79
19 > height at 50 m
19
42 > height in gaps
> height in gaps
12
12
25
67
67
98 > height in gaps
Two sets of ANOVA were made at different times after transplantation (6 months and at the end of the study which was
about a year for most species). Numbers in paranthesis indicate the results of non-parametric tests. In case of significant
differences, the main effect is included in the last column
123
5
(a)
Without (10 m x 10 m)
4
With parent (10 m x 10 m)
Without (30 m x 30 m)
3
With parent (30 m x 30 m)
2
1
Virola flexuosa
Cecropia
sciadophylla
Cecropia
membranacea
Apeiba aspera
Spondias
mombin
Garcinia
macrophylla
Hymenaea
oblongifolia
(b)
Without (10 m x 10 m)
0.4
With parent (10 m x 10 m)
Without (30 m x 30 m)
0.3
With parent (30 m x 30 m)
0.2
0.1
close to adult trees (usually young adult individuals about 6-year-old). C. membranacea saplings
were never found below parental trees in closed
canopy conditions.
In the most accentuated case, the densities of
G. hexapetala seedlings changed from being
highly positively correlated with the presence of
parents, to being negatively correlated with adult
trees when they reached the sapling stage (Fig. 1,
Table 5). This pattern was apparent for some
other species (P. bicolor, H. oblongifolia, Ga.
macrophylla, Apeiba aspera, and V. flexuosa), but
in these cases the low abundance of saplings did
not allow statistical analysis.
Based on the results, seedling densities were in
general low in the flooded forests (except for
C. membranacea) (Fig. 2a). Consistent with the
patterns of seed production in the forest
(Stevenson 2004), and with relatively high seedling survival rates, I found high seedlings densities
Virola flexuosa
Cecropia
sciadophylla
Cecropia
membranacea
Apeiba aspera
Spondias
mombin
Garcinia
macrophylla
Hymenaea
oblongifolia
Pourouma
bicolor
0.0
Gustavia
hexapetala
Sapling density (Ind./25 m2)
0.5
Pourouma
bicolor
0
Gustavia
hexapetala
Fig. 1 Seedling (a) and
sapling densities (b) for
nine plant species at
Tinigua National Park,
comparing plots with and
without adult trees. The
analyses were made for
two different scales for
each species (10 · 10 m2
and 30 · 30 m2
quadrats). The error bars
represent one standard
error
253
Seedling density (Ind./4m2)
Plant Ecol (2007) 190:245–258
of G. hexapetala in non-flooded forests. For two
small-seeded species (A. aspera and Cecropia
sciadophylla), I found the highest seedling densities in canopy gaps, suggesting that light or
Table 5 Correlation coefficients between the abundance
of adult trees and the density of both saplings and
seedlings of the major studied species, at large spatial
scales (hectares) in Tinigua National Park, Colombia
Species
Gustavia hexapetala
Pourouma bicolor
Hymenaea oblongifolia
Garcinia macrophylla
Spondias mombin
Apeiba aspera
Cecropia membranacea
Cecropia sciadophylla
Virola flexuosa
Adults versus
seedlings
0.81
0.65
0.51
0.31
0.57
– 0.22
0.80
– 0.18
0.53
Adults versus
saplings
– 0.20
0.11
0.05
0.00
0.14
0.94
0.99
– 0.22
– 0.03
Bold numbers indicate significant coefficients (P < 0.05)
123
Fig. 2 Seedling (a) and
sapling densities (b) of
nine plant species in
different forest types in
Tinigua National Park.
Error bars represent one
standard error
Plant Ecol (2007) 190:245–258
Seedling density (No./ 4 m2)
254
3
(a)
Mature
Open-degraded
2
Flooded on bars
Flooded on basins
Gaps
1
Virola flexuosa
Cecropia
sciadophylla
Cecropia
membranacea
Cecropia
membranacea
Spondias
mombin
Garcinia
macrophylla
Hymenaea
oblongifolia
Pourouma
bicolor
Apeiba aspera
0.25
Apeiba aspera
Sapling density (No / 25 m2)
Gustavia
hexapetala
0
(b)
Mature
0.20
Open-degraded
Flooded on bars
0.15
Flooded on basins
Gaps
0.10
0.05
temperature are very important triggers of the
germination of seeds for these species. The other
small-seeded species analyzed, C. membranacea,
was unable to establish in small canopy gaps
though it recruited on newly formed beaches and
in very large gaps. The relatively large density of
seedlings of this species in flooded forests seemed
to be related to a seasonal germination episode,
but it does not reflect the real patterns of regeneration in flooded forest on low basins because
the saplings only recruit when they are directly
exposed to sunshine (as on beaches).
I estimated sapling/seedling ratios for all common species in the forest in each subplot
(10 · 10 m and 30 · 30 m). Twenty species
were analyzed because they had high numbers of
seedlings and saplings, which allowed for G tests
(Sokal and Rohlf 1995); only one species was included for which transplant experiments were
also done. In this case (G. hexapetala), there was
123
Virola flexuosa
Cecropia
sciadophylla
Spondias
mombin
Garcinia
macrophylla
Hymenaea
oblongifolia
Pourouma
bicolor
Gustavia
hexapetala
0.00
a significantly higher sapling to seedling ratio far
from parental crowns at both scales (Table 6).
This pattern was also found for a few other species (e.g., Protium sagotianum at the 10 · 10 m2
scale), but the majority of analyses did not show
significant associations and in one case there was
a lower sapling/seedling ratio far from parental
crowns at the small scale (e.g., Dalbergia sp.).
Discussion
Escape hypothesis
Several studies have emphasized the importance
of the first stages of plant establishment to
understand recruitment patterns (Connell 1971)
because seeds and seedlings suffer the highest
rates of mortality. The results of this study confirmed high seed removal and seedling mortality
Plant Ecol (2007) 190:245–258
255
Table 6 The ratio of sapling to seedling densities were compared between plots with and without adults at each spatial
scale, using log-likelihood tests, for which G-statistics and associated probability values are reported
Small scale (10 · 10 m)
Alibertia cf. hadrantha
Castilla ulei
Dalbergia sp.
Euterpe precatoria
Gustavia hexapetala
Hybanthus prunifolius
Mabea maynensis
Oenocarpus bataua
Oxandra mediocris
Protium glabrescens
Protium robustum
Protium sagotianum
Pseudomalmea diclina
Psudolmedia laevigata
Psudolmedia laevis
Quararibea cf.witti
Rinorea lindeniana
Siparuna cuspidata
Talisia intermedia
Medium scale (30 · 30 m)
Without
With parent
G
P
Without
With parent
G
0.30
0.08
0.30
0.28
0.07
0.80
1.18
0.75
0.24
0.75
1.32
0.32
0.50
0.49
1.67
0.50
11.65
1.20
1.07
0.18
0.00
0.79
0.08
0.00
0.70
1.00
0.65
0.22
0.50
3.33
0.07
0.33
1.00
0.31
0.80
12.71
1.20
3.00
0.39
3.00
3.94
1.43
10.62
0.29
0.05
0.49
0.01
0.06
1.82
4.92
0.23
2.39
0.14
0.92
0.04
0.00
1.52
0.53
0.08
0.04
0.23
0.001
0.59
0.82
0.49
0.93
0.81
0.18
0.03
0.63
0.12
0.71
0.34
0.85
0.99
0.22
0.29
0.09
0.36
0.16
0.12
0.69
0.75
0.98
0.32
0.72
1.24
0.63
0.56
0.47
0.27
0.47
3.64
0.92
1.58
0.27
0.02
0.38
0.32
0.01
0.82
1.10
8.17
0.02
0.14
1.00
2.86
0.11
1.32
0.35
0.45
1.66
1.39
3.75
0.02
2.89
0.01
0.88
35.85
0.55
0.33
3.26
4.29
2.65
1.60
6.61
1.24
0.41
2.35
0.39
9.29
0.63
2.12
P
<
0.89
0.09
0.91
0.35
< 0.01
0.46
0.57
0.05
0.04
0.10
0.21
0.01
0.27
0.52
0.13
0.53
0.002
0.81
0.16
Shown in bold are cases where density ratios differed significantly (P < 0.05)
rates at these plant life stages, but suggest that
strong negative density-dependent effects may
occur in older plant stages rather than in these
initial stages. In fact, contrary to the predictions
of the escape hypothesis, there was for some
species, an early advantage for seeds dropping
underneath parental trees, where per capita seed
removal was in general lower than or similar to
removal away from parental trees. Although I can
not be sure about the fate of all removed seeds
and it is possible that some seeds were dispersed
by synzoochory (Forget et al. 1998), the predation
patterns in the stations, the type of seed predators
captured in traps baited with seeds of the focal
species and sporadic observations, all suggest that
most seeds were eaten by rodents. For example,
few seeds of G. hexapetala were attached to a
nylon wire, and half of them were destroyed by
rodents and the remaining were not found, because they were taken deep in the soil (> 20 cm),
where they would not be able to reach the top
soil. Future studies should address the fate of
seeds in order to confirm whether or not seed
mortality by rodents is the fate of most removed
seeds in western Amazonian forests (Notman and
Gorchov 2001).
Neither distance- nor negative-density dependent effects were commonly found after seed
dispersal and during the first year of seedling
development. However, for the species that could
be included in the analysis of plots, recruitment of
saplings was negatively associated with the location of adult trees. Given that for the majority of
the species studied about half of the seed rain falls
below parental trees (Stevenson 2002), an independent or negative distribution of saplings in
space with respect to parent location indicates
much lower per capita probability of recruitment
near parents. The results clearly suggest an
advantage in long-term survivorship for dispersed
seeds, which is likely to occur at intermediate
plant life stages (i.e., saplings) for the species
studied. Similar recruitment patterns have been
documented in other tropical communities (e.g.,
Clark and Clark 1984; Houle 1995; Gavin and
Peart 1997; Wills and Condit et al. 1999; Terborgh
et al. 2002).
The positive correlation between adult trees
and seedling abundance (Table 5), and the lack of
negative distance and density effects in the
majority of the experiments could be explained
by several factors. For example, when territorial
123
256
rodents are the main seed predators in a community, it is possible that the animals living near a
tree that drops many seeds are not going to be
able to eat the entire seed crop. This satiation
effect could thus be the cause for the positive
correlation of adult trees and seedling abundance
in this study. Although, only forests in South–East
Asia are known to be highly synchronized in
terms of fruit production at the community level
(Janzen 1967; Curran and Webb 2000), the existence of annual fruiting peaks commonly seen in
Neotropical forests have been associated with
satiation effects (van Schaik et al. 1993), and the
data from this study support this idea.
I found little evidence of high rates of infestation by insect seed predators, which were postulated as the main players in the original
formulation of Janzen (1970). I noted the effect of
insect predation for only a few species (i.e.,
V. flexuosa and S. mombin), but during the study
the influence of invertebrate seed predation was
relatively low even for these species. Other plant
enemies that have been documented as important
agents for seedling dynamics, such as damping-off
fungi (Augspurger 1984), were observed in several
species. It is possible that some of the advantages
of growing in a canopy gap (such as in S. mombin),
could be attributed to low incidence of dampingoff in high light conditions. This study confirms
that the factors that benefit plant fitness actually
vary in importance for different species. I observed
that mortality causes were different between
seedlings and saplings, at least for some of the
species studied. For example, the presence of galls
in the apical buds and main stems of G. hexapetala
saplings (Cecidomyiidae: Diptera), were not
observed in younger plants. Similarly, miners
eating the soft leaf tissues of several Cecropiaceae
species were observed only on saplings and adult
trees. Further studies will be necessary to test the
effect of these pathogens and herbivores as the
determinants of the negative distance-dependent
patterns suggested in this study.
Colonization hypothesis
The habitat type to which seeds were dispersed
was important for most of the species studied,
as predicted by the colonization hypothesis.
123
Plant Ecol (2007) 190:245–258
Furthermore, seedling survival probabilities were
low in flooded forests, and growth rates were high
in gaps. Even for seeds, for most species I found
differences in seed removal rates between forest
conditions, suggesting spatial heterogeneity in
seed predation patterns. The only recurrent event
was higher seed removal rates in flooded forests
for Ga. macrophylla, G. hexapetala, P. bicolour,
and V. flexuosa, four species that usually produce
seeds in the dry period, when seed rain and fruit
production is minimal in that forest type
(Stevenson 2004). Several studies have demonstrated high predation rates during times of low
seed abundance (e.g., Schupp 1990). These results
stress the effects of temporal variations and spatial heterogeneity of seed rain on seed predation
rates. Similarly, recent studies have shown that
seed fate is more affected by habitat characteristics than from population densities (Chauvet et al.
2004), and the differences may occur at very small
scales, such as the assemblage of seed species in a
frugivore’s dropping (Russo 2005).
The results also indicate clear differences in
life history and recruitment rates among species,
and none of the species could be grouped as
showing similar recruitment strategies. For
example, although I found evidence that all smallseeded species require canopy gaps for seedling
establishment, the two Cecropia species studied
showed differences in the type of light requirements; C. membranacea was much more lightdemanding than C. sciadophylla. Furthermore, C.
membranacea seeds rely more on bats for dispersal (Foster et al. 1986, pers. obs.) than the
other small-seeded species. In fact, the well-protected fruits of A. aspera, the other gap specialist
according to the patterns of seedling recruitment,
were only seen dispersed by primate species, in
contrast to the remaining species. For a gap specialist dispersed mainly by primates, who rarely
defecate seeds in clearings (Stevenson 2002),
there should be a strategy of seed dormancy, as
has been found for other species (Venable and
Brown 1993). For example, primates heavily
consume fruits of C. sciadophylla whose seeds are
in the size range typically buried by dung beetles
(Shephard and Chapman 1998; Andresen 2002). I
have observed that buried seeds of this species
remain dormant for at least 6 months.
Plant Ecol (2007) 190:245–258
I also observed several differences in life history parameters among large-seeded species. Although Spondias mombin has a large diaspore, it
should be classified as small seeded, and requires
canopy gaps for development. The small seed is
protected by a wide corky tissue, which also helps
in seed buoyancy in a complex dispersal system
involving primates, tapirs, and water as dispersal
agents (Stevenson et al. 1997). Other large-seeded species showed better growth in gap conditions (e.g., H. oblongifolia), but for some species
like G. hexapetala and Ga. macrophylla, there
was not a clear advantage for the first year seedlings in canopy gaps. These results suggest that for
these large-seeded primate-dispersed species,
which are usually dispersed under closed canopy
forests, there are tradeoffs that reduce the possibility of high photosynthetic rates in good irradiation conditions.
In summary, the results do not support the
predictions of the escape hypothesis during the
first year for seeds and seedlings, while most predictions of colonization hypothesis were supported. Support for the escape hypothesis was
found only from the static analyses between saplings and seedlings. Although, the interpretation
of this analysis is not as straightforward as the
results from the experiments, the results suggest
that demographic studies at these plant stages
older than 1 year are also important to understand
the importance of distance-dependent processes.
Acknowledgements I would like to thank all the field
assistants who helped in gathering information, especially
Alicia Medina, Carolina Garcı́a, Monica Pineda, Tatiana
Samper, Javier Cajiao, and Andrés Link. I thank Charles
Janson, Patricia Wright, John G. Fleagle, Anthony DiFiore, Maria Clara Castellanos, Nicole Gibson, and several
anonymous reviewers for their comments. This study was
possible thanks to logistic support from Centro de Investigaciones Ecológicas La Macarena (CIEM) and the permits from Unidad de Parques Nacionales. Financial
support came from the following institutions: La Fundación
para la Promoción de la Investigación y la Tecnologı́a
(Banco de la República), Margot Marsh Foundation, Lincoln Park Zoo, Primate Conservation Inc., and IdeaWild.
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