Download How human disturbance of tropical rainforest can influence avian

Oikos 000: 000000, 2009
doi: 10.1111/j.1600-0706.2009.17245.x,
# 2009 The Authors. Journal compilation # 2009 Oikos
Subject Editor: Eric Seabloom. Accepted 9 March 2009
How human disturbance of tropical rainforest can influence avian
fruit removal
Kara L. Lefevre and F. Helen Rodd
K. L. Lefevre ([email protected]) and F. Helen Rodd, Dept of Ecology and Evolutionary Biology, Univ. of Toronto, 25 Harbord Street,
Toronto, Ontario, M5S 3G5, Canada. Present address for KLL: Dépt des sciences du bois et de la forêt, Univ. Laval, 2405 rue de la Terrasse,
Québec, QC, G1V 0A6, Canada.
Fruit consumption by birds is an important ecological interaction that contributes to seed dispersal in tropical rainforests.
In this field experiment, we asked whether moderate human disturbance alters patterns of avian frugivory: we measured
fruit removal by birds in the lower montane rainforest of Tobago, West Indies, using artificial infructescences made with
natural fruits from two common woody plants of the forest understory (Psychotria spp., Rubiaceae). Displays were
mounted simultaneously in three forest habitats chosen to represent a gradient of increasing habitat disturbance (primary,
intermediate and disturbed), caused by subsistence land use adjacent to a protected forest reserve. We measured the
numbers of fruits removed and the effect of fruit position on the likelihood of removal, along with the abundances of all
fruits and fruit-eating birds at the study sites. Fruit removal was highly variable and there was not a significant difference
in removal rate among forest habitats; however, the trend was for higher rates of removal from displays in primary forest.
Canopy cover, natural fruit availability, and frugivore abundance were not good predictors of fruit removal. Birds
preferred more accessible fruits (those proximal to the perch) in all habitats, but in disturbed forest, there was a tendency
for distal fruits to be chosen more frequently than in the other forest types. One possible explanation for this pattern is
that birds in disturbed forests were larger than those in other habitats, and hence were better able to reach the distal fruits.
Coupled with differences in bird community composition among the forest types, this suggests that different suites of
birds were removing fruit in primary versus disturbed forest. As frugivore species have different effectiveness as seed
dispersers, the among-habitat differences in fruit removal patterns that we observed could have important implications for
plant species experiencing disturbance; these possible implications include altered amounts of seed deposition and
seedling recruitment in Tobago’s tropical rainforest.
The effects of human disturbance on population dynamics
are relatively well-studied, but less attention has been paid
to potential impacts on species interactions and the basic
functioning of ecosystems (Orians et al. 1996, Kremen
2005). The concern is that, by altering community
structure, anthropogenic disturbances could disrupt complex biotic interactions that maintain ecosystem integrity,
causing a cascade of ecological impacts (Bond 1994). For
example, there is evidence that habitat disturbance can
cause declines in pollination (Kremen et al. 2002), and
changes in the visitation rates of animal fruit-consumers to
rainforest trees (Luck and Daily 2003). Empirical studies
demonstrate that these anthropogenic disruptions can have
important effects on plant populations including declines in
fruit and seed set (Aizen and Feinsinger 1994), increased
inbreeding (Fuchs et al. 2003), altered seed dispersal
patterns (Cordeiro and Howe 2003, Levey et al. 2005),
reduced germination (Bruna 1999), and lower seedling
recruitment (Chapman and Chapman 1995). It has been
hypothesized that potential outcomes of disrupted seed
dispersal could thus include changes in plant species
distributions, community composition, and even species
extinction (Bond 1994, Loiselle and Blake 2002). Altered
patterns of frugivory might have a smaller measurable effect
on plants than altered pollination, because the relationships
between species are not as tightly coupled in seed dispersal.
Instead, plants usually rely on suites of vertebrates for
dispersal (Wheelwright and Orians 1982, Levey et al.
1994), which may be why there is little evidence for the
role of animal dispersers in the diversification of angiosperms (Herrera 1989). However, disturbance impacts on
many seed dispersers simultaneously could interfere with
plant regeneration (Willson and Traveset 2000). Concomitantly, animal dispersers can play a critical role in
maintaining forest plant communities following habitat
loss (Montoya et al. 2008). Thus, studies of patterns of
frugivory in disturbed areas are important for determining
the potential consequences for plant populations and forest
ecosystems.
We investigated how anthropogenic, tropical rainforest
disturbance influences avian frugivory the consumption of
fruit by birds. Species of fruit consumers differ in their
Early View (EV): 1-EV
effectiveness as seed dispersal agents (Schupp 1993), due to
variations in body size, diet composition, feeding behaviour,
digestive physiology, and movement patterns (Levey et al.
1994, Jordano et al. 2007). Frugivore species therefore
generate distinctive seed shadows, resulting in different
effects on plant fitness (Willson and Traveset 2000, Loiselle
and Blake 2002). Changes in avian frugivory could thus
alter plant reproduction, distributions, and forest composition (Levey et al. 1994). In these ways, birdfruit interactions contribute to the structure and biodiversity of tropical
rainforest communities (Snow 1971, Morton 1973, Howe
and Smallwood 1982, Howe 1986, Stutchbury and Morton
2001).
Studies of fruit consumption by birds show that plant
distributions and spatial habitat variables can influence
avian fruit choice and removal rates (Denslow 1987,
Sargent 1990, Levey et al. 1994, McCarty et al. 2002,
Saracco et al. 2005). The position of fruit on plants also
influences frugivory so that, given a choice, birds usually
select fruits closest to a perch because they are more
accessible (Denslow and Moermond 1982, Moermond
and Denslow 1983, Levey et al. 1994). Because human
alteration of forests can influence habitat structure and
plant and bird community composition (reviewed in
Lefevre 2008), important variables that can influence fruit
selection by birds, we postulated that disturbance might also
influence patterns of avian fruit removal.
In this study, we asked whether anthropogenic forest
disturbance affects patterns of fruit removal by birds;
specifically, we asked whether disturbance affected the
numbers of fruit taken and the positions on plants from
which fruits were removed. To do so, we used concurrent
experiments in protected rainforest and in neighbouring,
disturbed rainforest, in Tobago. We consider the subsistence human activity in the disturbed area as moderate,
compared to the more severe, well-studied disturbances
caused by outright habitat loss or fragmentation. Fruit
removal was quantified using standardized displays of
natural rainforest fruits. Despite considerable variation in
fruit removal rates documented in the literature, in general,
previous studies have shown that more fruits are typically
removed near forest edges and in gaps than under closed
canopy (Thompson and Willson 1978, Denslow and
Moermond 1982, Moore and Willson 1982, Restrepo et
al. 1999); this may occur because fruits are discovered more
easily in sunlit patches (Thompson and Willson 1978), or
because frugivores generally forage more in gaps than in
forest interior (Willson et al. 1982, Levey 1988b). We
therefore predicted that fruit removal rates would be higher
in our disturbed sites, because the partial clearing in these
areas might be similar to natural forest openings. We also
considered the effect of natural fruit and frugivore
abundances on fruit removal rates.
Methods
Study site and design
Fruit removal experiments were conducted on Tobago,
West Indies (11817?N, 60837?W, Trinidad and Tobago),
a small continental island approximately 120 km from
2-EV
Venezuela. We worked in and near the Main Ridge Forest
Reserve, an area of 3500 ha protected rainforest along the
island’s mountainous backbone, which has been protected
since 1765 and is administered by Tobago’s Dept of
Natural Resources and the Environment (DNRE). The
forest reserve and adjacent Crown Lands were likely never
altered by significant amounts of human interference
because of their inaccessibility, and they do not have a
history of cultivation (Beard 1944). The vegetation is lower
montane rainforest (Beard 1944; premontane wet forest
according to Holdridge et al. 1971), which covers the Main
Ridge from approximately 250 m to 575 m, its highest
elevation. It is characterized by a 1530 m canopy depending on exposure, with abundant lianas and epiphytes, and
was described extensively in past surveys (Beard 1944,
Keeler-Wolf 1982). Seasonality is driven by rainfall: the
dry season occurs roughly from JanuaryMay and the wet
season from JuneDecember. This study took place
from March to May 2004 (experiment dates listed in
Appendix 1), when fruiting diversity peaks in the regions
(Snow 1965).
Experiments were conducted in three types of forest
habitat, chosen to represent an increasing gradient of
habitat disturbance: primary, intermediate and disturbed.
Primary forest
Primary control plots were located in undisturbed forest in
the reserve’s interior. To our knowledge, the only notable
human disturbance is guided nature walks for tourists, and
some wildlife poaching (DNRE pers. comm.). Principal
species in the canopy include Byrsonima spicata (Malpighiaceae), Eschweilera decolorans (Lecythidaceae), Licania
biglandulosa (Chrysobalanaceae), Simarouba amara (Simaroubaceae), Sloanea laurifolia (Eleaocarpaceae), and several
Palmae. The forest understory consists of shrubs and small
trees including numerous members of the Melastomataceae,
Palmae and Rubiaceae.
Disturbed forest
Disturbed forest represented the other end of the disturbance gradient. This habitat was located beyond the
reserve within 1 km of its boundary. To the best of our
knowledge, the area is Crown Land (Beard 1944) with
pockets of private holdings, including small-scale, abandoned cacao plantings that were established in rainforest
by local people, during the first half of the 20th century
(H. Jack pers. comm.). The disturbed forest has significantly less canopy cover than primary forest (Lefevre 2008);
the vegetation is now a mosaic of some large trees,
secondary forest, and openings dominated by pioneer plant
species including Cecropia peltata (Cecropiaceae), Heliconia
spp. (Heliconiaceae) and Piper spp. (Piperaceae). While no
longer actively cultivated, these areas experience subsistence
use at a low intensity by local people, for harvesting fruits
(banana, papaya), grazing goats and cows, and for travel by
foot. For comparison with other studies, we suggest that
this constitutes ‘moderate’ habitat disturbance, a term that
has been applied to activities such as selective logging or
shifting agriculture (Gray et al. 2007).
Intermediate forest
Intermediate forest plots were located in rainforest at the
reserve boundary, directly abutting disturbed areas. Many
large, possibly old-growth trees remained intact in this
habitat. These areas have not had the same small-scale
cultivation as disturbed areas (D. Henry pers. comm.), but
they are not legally protected like the primary forest. An
assessment of plant community composition in the three
habitats showed that intermediate forest includes plant
species characteristic of both protected and disturbed forest,
and that this habitat has a medium amount of canopy cover
(mean 53%, range 1085), compared to the more intact
primary forest (mean cover66%, range 2590) and
the more open disturbed forest (mean cover 43%, range
585; 92.1 SE, n 36 per habitat) (Lefevre 2008). We
emphasize that these levels of disturbance were moderate,
compared to the severe disturbance that might occur in the
case of canopy clearing and other forms of habitat loss or
conversion.
Four study plots (0.75 ha) were established in each of the
three forest types (see Lefevre 2008 for more details).
Locations were chosen based on the availability and
accessibility of suitable habitat. We selected three study
trees in each plot as replicate units for measuring fruit
removal (n 12 trees per forest type). Trees were chosen
depending on the presence of thin horizontal branches ideal
for attaching fruit displays, and the trees selected in each
plot were spaced at least 10 m apart. We chose this
minimum inter-tree distance because field experiments
have shown that fruit displays at least 6.4 m apart are
treated separately by some Neotropical frugivores (Levey
et al. 1984).
Fruit removal experiment
To control for fruit display size and spatial arrangements,
we used artificial infructescences made with natural rainforest fruits that occur in the study area. Medium-gauge
wire (2 mm diameter) was used to create V-shaped ‘twigs’
15 cm long, with 10 small loops to which a single fruit
was attached (Fig. 1). Fruits were collected and sewn onto
loops the day before an experiment began. To create a fruit
Distal fruits (1, 6)
6
1
7
2
8
3
9
4
Proximal fruits (5, 10)
5
10
Tree branch
Figure 1. Schematic drawing of one artificial infructescence
display (‘twig’). Each arm of the twig is 15 cm long. Circles
represent loops made by twisting the wire every 3 cm, to which
fruits were sewn. Numbers indicate positions of fruits, representing five different distances from the main tree branch. The branch
is a potential bird perch.
display, we attached three twigs to each experimental tree,
using duct tape to affix wires upright on a horizontal
branch. Each twig was placed on a different branch, within
50 cm of each other, and 1.52 m above the ground. There
were 30 fruits presented on each tree, for a total of 1080
fruits per replicate experiment (10 fruits per twig3 twigs
per tree36 trees). Displays were mounted at sunrise. We
revisited at sunset to record the number of fruits removed,
and the twig positions from which fruits were removed.
Fruits were presented for 10 to 11 hours, depending on the
time required to hike in to study plots. We assumed that
removals were due largely to birds because they are mostly
diurnal, as opposed to mammals, which are mostly
nocturnal. We frequently observed squirrels Sciurus granatensis active in the day, but observed them feeding only on
large fruits, never on berries similar to those used in this
experiment.
Each replicate experiment took two days to run, with
half of the study trees tested on each day (i.e. 18 trees per
day, six from each forest type). We repeated the experiment
ten times to maximize the chance that birds would respond,
because fruit crops of understory plants may go undetected
by frugivores when crop sizes are relatively small (Murray
1987), search time between patches may be relatively high
(Howe 1986), and frugivorous birds may not visit new food
sources immediately (Restrepo et al. 1999).
We chose two Psychotria species for use in experiments
because members of the family Rubiaceae are generally
bird-dispersed and are relatively common fruiting plants in
the Neotropical rainforest understory (Levey et al. 1994,
Smith et al. 2004). Their ripe fruits were available in
large numbers in the Main Ridge during the dry season.
Psychotria muscosa is a 13 m tall shrub that produces
terminal clusters of 37 white to purple fleshy berries, 0.5
1 cm in size. Psychotria tobagensis is a small tree 37 m tall,
with panicles bearing scores of 0.5 cm oval-shaped orangered berries with a very thin pulp layer. Fruits of both species
contain two seeds. We did five replicates with each species,
running subsequent experiments when a large enough crop
of either species was ripe and accessible for collection.
The average time between replicates was 6 days (range
214 days; Appendix 1). Fruits were gathered in the Reserve
away from study plots, and experiments were not conducted
during heavy rain. In addition, we attempted one replicate
with a fruit species more common to disturbed/edge forest
(Ficus tobagensis), and one with a fruit that does not grow in
the study area (dried cranberries, Vaccinium macrocarpon),
but as birds did not respond to the displays, these data are
not included here.
We also attempted to collect direct observations of fruit
removal by conducting focal watches at natural P. muscosa
and P. tobagensis plants. Removal was not observed during
these periods. This is not surprising since birds removing
fruits in the understory tend to be wary (Howe 1979) and
generally avoid feeding near observers (Murray 1987), and
the fruit crops of these plants were small, compared to large
fruiting trees such as Ficus. However, based on casual
observations and on fecal samples we collected, we know
that P. muscosa was eaten by blue-backed manakins
Chiroxiphia pareola and P. tobagensis was eaten by yellowlegged Platycichla flavipes and white-necked thrushes Turdus
albicollis. Psychotria fruits in Panama are eaten by migrant
3-EV
Empidonax flycatchers (E. S. Morton pers. comm.) and
several other species of the thrush, manakin, flycatcher,
trogon and tanager families (Poulin et al. 1999), so we infer
that these fruits could also be eaten by other frugivores in
our study site.
Environmental variables
We collected data on three environmental variables that we
anticipated would be most likely to influence fruit removal
rates: canopy cover, fruit abundance, and abundance of
fruit-eating birds. To collect data on these variables, we
established three 10 10 m quadrats in each 0.75 ha plot,
with quadrats spaced evenly through the plot (one at each
end and one in the middle). We measured canopy cover
because it influences the level of sunlight that penetrates
into the forest interior and hence fruit abundance. Based
on the spherical densiometer method (Engelbrecht and
Herz 2001), two observers made independent estimates of
percent canopy cover to the nearest 10% at three locations
in each quadrat, using a hand-held, 117 cm mirror
marked with a grid. We took the average of the two
estimates for each location.
We measured natural fruit abundance, because this
influences fruit consumption by animals (Howe and
Smallwood 1982). We censused all fruiting plants in each
quadrat once per month. For every plant bearing fruit, we
recorded the species and estimated the number of ripe and
unripe fruits present. Only ripe fruits were included in the
estimate of fruit available to avian frugivores, because birds
tend to eat ripe fruits except during periods of scarcity
(Moermond and Denslow 1983).
We also quantified the abundance of fruit-eating birds
because temporal variation in their numbers is likely to
affect fruit removal rates (Levey et al. 1994). We used point
counts, a standard method to census birds by sight and
vocal display (Karr 1981): 10 min, unlimited radius counts
at two points per plot, 150 m apart, one morning each
month between sunrise and 11 a.m. Then, we calculated
mean bird abundance (number of individuals) for the pair
of points in each plot, because we were not certain that
points were far enough apart to be considered independent
samples in the more open habitat of disturbed forest. Both
frugivores and fruit-eating omnivores were included in this
calculation, to account for all bird species that regularly
included fruit in their diet. Feeding guild designations were
based on our own field observations and literature reports of
avian feeding ecology in the Neotropics (point count data
along with the references used for guild classification are
detailed in Lefevre (2008)).
Data analysis
First, we asked whether fruit removal rates varied among
habitat types. Removal was calculated as the rate of fruit
removed per twig per hour; we used this standardized
measure because fruits were presented for slightly different
durations in each plot, due to differing times required to
reach locations on foot. Removal rates were not normally
distributed even after transformation. Also, we wanted to
express removal as a rate per twig in order to examine
4-EV
variation within experimental replicates (i.e. trees). Thus,
we calculated the mean removal rate per twig at each
replicate tree species (Hurlbert 1984), across the five
experiments with each fruit type, and performed a separate
one-way, non-parametric analysis of variance (Kruskal
Wallis test) for each Psychotria species, with forest habitat
as the dependent variable. Then we repeated the analyses,
after excluding trees from which no fruit was removed;
again rates were not normally distributed. This second test
accounted for the likelihood of frugivore visitation, an
important component of seed dispersal (Murray 1987).
Next, we wanted to compare fruit removal among
habitats within each replicate experiment, to account for
temporal variation in removal. We did this by analyzing total
fruit removal at the study plot level. Within each replicate
experiment, we compared the total amount of fruit removed
from all interior forest plots to the mean of total fruit
removed from intermediate and disturbed forest plots
(i.e. (intermediatedisturbed)/2)). This enabled a paired
comparison of fruit removed from the forest reserve versus
fruit removed from both habitats experiencing some degree
of disturbance. We transformed the total amount of fruit
removed (square root (x3/8)) to obtain a normal distribution and conducted a paired t-test.
We could not perform a multiple regression with our
environmental data because fruit removal rates were not
normally distributed. Therefore, we used Spearman rank
correlations to test for associations between fruit removal
rates and canopy cover, fruit abundance, and frugivore
abundance. We also asked whether Psychotria removal rates
were higher in plots where the same species was fruiting
naturally, compared to plots where it was absent or not
fruiting, using a Wilcoxon rank sum test.
To determine whether study plots near to each other had
similar patterns of fruit removal, we used hierarchical
clustering. Plots were clustered based on removal rates of
both Psychotria species (complete data sets, including
instances of zero removal), using an unweighted average
distance algorithm (UPGMA). We visually inspected the
resulting dendrogram to see if trees were clustered more by
habitat type or spatial location.
To analyze the effect of fruit position on likelihood of
removal, we conducted a categorical analysis considering
only twigs from which fruit was removed. We used G-tests
to determine whether there was uniform fruit removal
among four possible categories (fruit positions shown in
Fig. 1): distal fruit removed (positions 1 or 6), proximal
fruit removed (position 5 or 10), both terminuses removed
(position 1 and 6, or 5 and 10), or no terminal fruits
removed (i.e. only central positions 24 or 79 removed).
Separate G-tests were conducted for each replicate because
consecutive replicates at the same tree were not independent. This analysis was conducted for P. muscosa experiments only because frequencies of P. tobagensis removal
were too low to allow for valid tests.
To ascertain whether the likelihood of removal increased
at each tree over time, as birds became accustomed to the
fruit displays during subsequent replicate experiments, we
used one-tailed runs tests (Zar 1984) to test for contagion in
the distribution of fruit removals.
All analyses were performed using the statistical software
JMP version 5.0.1a (SAS Inst.), other than runs tests, which
were calculated by hand.
2.0
a
1.5
Forest
Primary
Intermed
1.0
Results
Fruit removal rates and quantity
Mean frequency (/10 replicates)
Removal rates were highly variable for both fruit species,
and their distributions were positively skewed due to the
prevalence of zeros in the data sets. Birds removed more
P. muscosa than P. tobagensis fruits (Appendix 1): at least
one fruit was removed from 35% of P. muscosa displays,
versus 23% of P. tobagensis displays. No fruit was removed
from a study tree 38.4% of the time. When fruit was
removed from a plot during a replicate experiment, it was
taken typically from just one tree (62.2% of trees),
sometimes from two trees (33.8%), and rarely from all
three trees in a plot (4.1%; Fig. 2a). At the twig level, most
often no fruit was taken from a display (70.8% of the time).
When fruit was removed from a tree, it was often taken
from one (48.6%), two (24.8%), or all three twigs (26.7%)
within the tree (Fig. 2b). These removal patterns suggest
that birds were most often feeding at just one tree within a
plot, but from multiple twigs on a tree and, therefore, were
treating trees, rather than twigs, as independent fruit
patches.
We detected no significant difference among forest types
in the rates of fruit removal per display when data for all
replicates at all trees were included in the analysis (Fig. 3a).
This was true for both species: removal rates did not depend
on habitat for P. muscosa (KruskalWallis test, x2 0.32,
n 36 trees, DF 2, p0.85) or P. tobagensis (Kruskal
Wallis test, x2 0.41, n 36 trees, DF 2, p0.81).
Considering only instances when at least one fruit was taken
from a tree during a replicate experiment (Fig. 3b), removal
did not differ with forest type for either P. muscosa
10
a
10
8
8
6
6
4
4
2
2
b
0
0
0
1
2
3
No. of trees with fruit removed
0
1
2
3
No. of twigs with fruit removed
Figure 2. Pattern of Psychotria fruit removal (mean9SE) from
trees and twigs, for ten replicate experiments (all experiments in all
habitats, combined). (a) Number of trees with at least one fruit
removed, of three trees in a plot (n 12 plots). When removed,
fruit was typically taken from only one tree, or sometimes two
trees. (b) Mean number of twigs per tree with at least one fruit
removed, of three twigs on a tree (n 36 trees). When removed,
fruit was taken from one, two, or three twigs on a tree. These plots
show that frequently, no fruits were removed from a twig, or even
an entire tree. When fruits were removed, birds were mainly
feeding at one tree within a plot but from multiple twigs on that
tree.
Mean fruits removed / twig
Disturbed
0.5
0
6
b
4
2
0
Psychotria muscosa
Psychotria tobagensis
Figure 3. Amount of fruit removal for two Psychotria species in
three rainforest habitats. (a) Number of fruit removed per display
(‘twig’) (maximum 10 fruits) from each experimental tree (n 12 trees per forest type, for five replicates with each fruit species).
(b) Number of fruit removed per twig, after twigs from which no
fruit was removed were excluded from the analysis, to account for
the likelihood of frugivore visitation. Bars show actual numbers
of fruit removed (mean9SE) during a 10 h period, to show
standardized results for the minimum amount of time that all
experiments were run. Analyses were conducted on hourly removal
rates to account for small differences in the time fruit was available
to birds.
(KruskalWallis test, x2 1.57, n 34 trees, DF 2, p
0.46) or P. tobagensis (KruskalWallis test, x2 0.58, n 26 trees, DF 2, p 0.75). However the plot-level analysis,
comparing the total amount of fruit removed within each
replicate experiment, showed that fruit removal from
primary forest was greater than from the other two habitats
(paired t-test: t 2.4, n 10 replicates, p 0.04).
No habitat variable was a good predictor of fruit removal
neither canopy cover, ripe fruit abundance, nor frugivore
abundance was clearly related to removal rates (Table 1).
Moreover, experimental fruit removal was not correlated
with the natural abundance of the same Psychotria fruit in
study plots. Nor was fruit removal simply dependent on
whether or not the species used in the experiment was
fruiting naturally in the same study plot, for either
P. muscosa (Wilcoxon rank sum test, Z 0.73, n 9,27,
p0.46) or P. tobagensis (Z 0.23, n 3,33, p0.82).
The clustering analysis of trees, based on removal rates of
both fruit species (i.e. the complete data set including
instances of no removal), suggests that removal patterns
were driven by a combination of forest type and local spatial
effects (Fig. 4). Our study plots did not cluster clearly
according to habitat or spatial location alone. Rather,
clusters on the dendrogram include trees from a mixture
of habitat types and locations.
The likelihood of fruit removal from each tree did not
increase significantly over time. Data for each of 32 trees
were tested separately. Runs tests were not significant in 31
cases (p 0.05). One test was significant for a tree in
interior forest (m2, m0.05(1)3,7 2, pB0.025), where
5-EV
Table 1. Associations between removal rate of two species of Psychotria fruits (mean of five replicates at each tree) and habitat variables
(Spearman rank correlations, n 36 trees).
Habitat variables (measured in each study plot)
Canopy cover (%)
Fruit abundance (all ripe fruits)
Psychotria abundance (only the species being tested)
Frugivore abundance
removal was clustered toward the end of the 10 replicates.
There were too few instances of fruit removal to conduct a
test for the other five trees: fruit was never removed at two
trees, and was removed in only one replicate at three trees.
P1-1
P1-2
D4-3
P2-2
P2-3
I3-1
P2-1
P4-1
I2-1
I3-2
I3-1
I1-3
P4-2
I1-2
D2-1
I1-1
D2-3
D4-1
P3-3
D1-3
I2-2
I4-1
I4-2
D3-2
D1-1
D2-2
P3-2
I2-3
D3-3
D4-2
P4-3
I3-3
I4-3
D1-2
P1-3
D3-1
Figure 4. Dendrogram from hierarchical clustering (algorithm
method average, or UPGMA) of 36 experimental trees, based on
similarities in avian fruit removal of two species of Psychotria.
Alpha-numeric codes identify each tree, for comparison of
locations and habitats: letters denote the forest habitat (P primary, I intermediate, Ddisturbed), the first number is
the replicate study plot in that habitat, and the second number is
the individual tree in the plot. Trees sharing a symbol are in the
same cluster of the diagram.
6-EV
P. muscosa
P. tobagensis
rs
p
rs
p
0.08
0.05
0.18
0.24
0.67
0.79
0.30
0.17
0.07
0.08
0.04
0.09
0.74
0.71
0.80
0.67
Fruit removal position
Fruit position on the twig had a significant influence on the
likelihood of fruit removal in four of five P. muscosa
replicates, with fruits closest to the branch (where birds
would likely perch) being chosen more than distal fruits.
This pattern varied significantly with habitat type in two of
the replicates (G-tests, Table 2). In primary forest, proximal
fruits were the most likely to be removed from displays.
Proximal fruits were also removed more often in intermediate and disturbed forest, but the pattern was less
pronounced in these habitats (Fig. 5). This result could be
due to differences in the feeding ecology of birds that predominate in each forest type, because bird community composition differed among our forest habitats (Appendix 2).
For example, experiments with captive frugivores show that
birds with strong legs (e.g. Thraupinae and Emberizinae:
thrushes and finches) tend to feed from a perched position
and select more accessible fruits, while birds with weaker
legs (e.g. Pipridae, Trogonidae and Tyrannidae: manakins,
trogons and flycatchers) tend to feed on the wing while
hovering and are less restricted by fruit position (Moermond and Denslow 1983, Moermond et al. 1986). To
determine whether such differences in foraging behaviour
might explain our observed fruit removal pattern, we
categorized birds as either ‘perchers’ or ‘hoverers’, and
compared the abundance of individuals in each of these
feeding groups, across forest types. Based on our observed
fruit removal pattern, we would expect perchers to be most
common in primary plots, where fruit removal was most
affected by accessibility. In contrast, we found that perchers
were most common in disturbed plots (ANOVA, F2,9 4.8, p0.04) while hoverers were most common in
interior plots (ANOVA, F2,9 31.5, pB0.001). Thus,
these differences in feeding behaviour alone cannot explain
the removal pattern.
Another possible explanation for the pattern of fruit
removal from displays is frugivore size. For example, a large
percher might easily be able to reach the fruits at the
terminus of our 15 cm infructescences despite its inability
to hover. Thus, to determine if differences in body size
were consistent with fruit removal patterns, we obtained
the body length of frugivores in our data set from the
literature (ffrench 1991), assuming that length determines
how far birds can reach to feed. Based on the observed fruit
removal pattern, we expected to find larger frugivores in
disturbed plots, because relatively more fruits were taken
from the distal position in that habitat. Indeed, mean body
size of frugivores (weighted by the abundance of each
species) was greatest in plots with the least canopy cover
Table 2. Categorical analysis of the relationship between Psychotria muscosa fruit position versus removal frequency. Separate G-tests were
conducted for each repeated experiment.
Replicate
Does fruit position influence
removal? (DF3)
G
p
Depends on habitat type?
(DF6)
G
p
yes
yes
yes
yes
no
22.7
10.2
21.3
7.95
6.22
B0.0001
0.017
B0.0001
0.047
0.10
yes
yes
no
no
no
19.2
23.4
9.76
4.3
3.14
B0.01
B0.01
0.14
0.63
0.79
1
2
3
4
5
(Fig. 6), indicating that larger birds were more common in
disturbed plots (r2 0.37, n 4, p0.035).
Discussion
Patterns of fruit removal by birds in Tobago’s rainforest
were characterized by a high amount of variation, across all
three forest habitats. Removal rates varied dramatically in
both space and time, as has been found in other studies of
40
30
proximal
20
both
distal
neither
10
P
I
D
1.2
b
closer
to branch
Mean fruits removed
1.0
0.8
40
• Primary
0.6
0.4
0.2
0.0
P
I
D
Forest habitat
Figure 5. Influence of fruit position on likelihood of Psychotria
muscosa removal by birds, in primary (P), intermediate (I), and
disturbed (D) forest. (a) Summarized results for all experiments,
illustrating whether fruit was removed close to (proximal) or
furthest from (distal) the tree branch to which infructescences were
affixed. Each count represents one infructescence (twig) including
only those from which fruit was removed. (b) Mean fruit removal
at each of five distances from the tree branch (shown in Fig. 3a),
including instances of zero removal. Within each habitat, the left
bar represents the most distal fruit, and bars to the right are
proximal fruits (i.e. closest to the main branch to which displays
were attached).
Mean frugivore body length (cm)
Frequency of removal
a
frugivory (McCarty et al. 2002). Local spatial effects alone
were not driving fruit removal patterns, as our clustering
analysis rarely grouped trees from the same plot. Also, we
found that the likelihood of fruit removal did not increase
over time, suggesting that birds were not simply responding
more to known fruit locations. We had expected that the
abundance of fruit-eating birds and natural fruit availability
within a plot would be important influences on removal
rates. Other studies have shown that the abundance of fruit
and frugivores typically increases in naturally disturbed and
second-growth forest (Levey 1988a). However, we found no
significant influence of fruit abundance on fruit removal
rates; rates were not correlated with either Psychotria
abundance or the total amount of fruit available in study
plots. We also found no significant influence of fruit-eating
bird abundance on removal rates. This suggests that there
was neither increased frugivory nor increased competition
among plants for seed dispersers in the disturbed areas that
we studied.
Indeed, others have found that fruit removal rates are
difficult to predict (McCarty et al. 2002), because they are
influenced by many complex, interrelated factors in addition to fruit and frugivore abundance. A number of studies
found little or no evidence for a positive relationship
between fruit crop size, frugivore visitation, and the amount
of fruit removal (Moore and Willson 1982, Davidar and
Morton 1986, Denslow 1987, Murray 1987, Laska and
Stiles 1994, Korine et al. 2000). However, Ortiz-Pulido
and Rico-Gray (2000) found that all of these measures were
x Intermed
35
o Disturbed
30
25
20
30
40
50
60
70
80
Percent canopy cover
Figure 6. Relationship between body size of frugivorous birds and
percent canopy cover (r2 0.37, p0.035). Every bird observed
in a study plot was included in the analysis; body size data were
obtained from the literature (Methods). Each symbol represents
the mean for one forest plot (n 4 plots/treatment).
7-EV
positively correlated, and suggested that previous results
may be unclear because spatio-temporal variation in fruit
production tends to be overlooked. Also, frugivores are
selective in their choice of fruit (Moermond et al. 1986)
because, in addition to fruit abundance, a vast array of fruit
traits including size, nutritional content, and digestibility
influences the attractiveness of fruit to birds (Denslow
1987, Levey et al. 1994). Extrinsic factors such as habitat
characteristics, neighbourhood effects related to plant
densities and spatial configurations (Sargent 1990, McCarty
et al. 2002, Saracco et al. 2005), predation risk (Howe
1979), and direct or indirect edge effects (Restrepo et al.
1999) also play an important role in avian fruit choice. Any
of these factors could have thus been influencing fruit
removal in our study site, making it more difficult to detect
any underlying patterns among habitats.
We observed no significant difference in the rate of fruits
removed per display, among forest types. In terms of total
fruits removed in each experiment, however, we found that
birds removed significantly more Psychotria fruits from
primary forest, compared to intermediate and disturbed
forest. One explanation could be that birds in primary
forest were more likely to respond to our displays because
fruiting Psychotria plants are more common in that habitat,
making birds there more familiar with the fruits. However,
there was no correlation between fruit removal and the
abundance of the same Psychotria species in study plots.
Alternatively, we suggest that this occurred because disturbance in our study site is altering bird community
composition, including frugivore abundances, which in
turn could influence fruit consumption. Perhaps this is why
we did not find higher rates of fruit removal with
disturbance as some other studies have detected in forest
gaps and near forest edges (Thompson and Willson 1978,
Denslow and Moermond 1982, Moore and Willson 1982),
including at edges created by human activity (Restrepo et al.
1999, Galetti et al. 2003). However, we note that Galetti
et al. (2003) also found that the probability of fruit
consumption declined in smaller forest fragments.
In our study area, a possible implication of lower fruit
removal following disturbance could be a decline in the
dispersal of shade-tolerant plant species and, correspondingly, a lack of seed input from primary forest plants into
disturbed areas. For example, blue-backed manakins, which
frequently eat P. muscosa, and white-necked and yellowlegged thrushes, which eat P. tobagensis, were most common
in our primary forest study plots, and less abundant or
absent from disturbed plots. Given that fewer fruits were
removed from disturbed forest, it seems that other frugivore
species common to disturbed forest (e.g. blue-gray tanagers)
are not simply interchangeable with primary forest frugivores, in terms of fruit consumption and dispersal services
provided to Psychotria plants. Therefore, if disturbance
affects bird species composition (as it has done here), there
can be important implications for plant species that
are dispersed by birds that are sensitive to disturbance.
We did detect some noteworthy patterns in the positions
from which fruits were removed from displays. Fruits
closest to the branch, where some birds presumably
perched, were chosen most frequently. This impact of
accessibility on fruit choice has been demonstrated in other
feeding experiments. Birds that feed while perching prefer
8-EV
fruits that are closest to their perch (Denslow and
Moermond 1982, Moermond and Denslow 1983). However, we found that this preference for proximal fruits was
strongest in primary forest; in disturbed forest, where birds
were generally larger, distal fruits were chosen at a frequency
similar to proximal fruits. This pattern suggests that
differences in bird species composition, due to disturbance,
could be influencing the accessibility of fruits, and hence
fruit selection by birds in this ecosystem. While we cannot
comment on the precise implications in Tobago’s rainforest, because we did not make observations of fruit
consumption and dispersal, other studies have found that
species of animal consumers contribute to seed dispersal in
very different ways. For example, Jordano et al. (2007)
found that larger birds dispersed seeds over greater distances
and into more open microhabitats, affecting seed-mediated
gene flow differently than smaller birds. The increase in
avian body size that we noted in disturbed habitats may
hence be having a direct influence on bird-mediated seed
dispersal patterns. Certainly the exact nature of these
relationships will differ depending on the plant species in
question, the frugivores present, their degree of frugivory
and individual fruit preferences. All of these factors are of
interest for future studies of disturbance impacts on fruit
consumption and seed dispersal.
Despite the complexity of factors influencing fruit
consumption, and the large variation in avian fruit removal
that we found, our results suggest that moderate human
disturbance could be affecting patterns of avian fruit
consumption in Tobago. We found some evidence for
less fruit removal and different patterns of removal from
displays in disturbed forest, and we infer that these changes
may result from the altered bird community composition in
habitats affected by human activity in our study area. These
differences in fruit consumption could indicate some rather
serious, indirect impacts of forest disturbance on plants.
That is, considering the essential role of avian frugivory in
the seed dispersal of forest plants, and considering the
influence that interspecific differences in bird feeding
behaviour and dietary composition can have on seed
shadows and the effectiveness of seed dispersal (Schupp
1993, Loiselle and Blake 2002), we hypothesize that
changes in fruit removal could influence plant reproduction
in our study site. For example, a change in bird community
composition due to disturbance might decrease the likelihood of shade-tolerant plant species being dispersed to
gaps for future regeneration, and might increase the
likelihood of pioneer plant species penetrating into the
periphery of primary forest. The differences in fruit removal
patterns that we observed among rainforest habitats might
therefore have long-term implications for plant populations
experiencing disturbance.
Acknowledgements Tobago’s Dept of Natural Resources and the
Environment (DNRE) authorized use of the Main Ridge Reserve.
We thank their staff for training and logistical support, especially
J. Edwards, N. George, D. Henry, H. Jack and A. Ramsey.
Fieldwork in Tobago was assisted by H. Robert, A. Stephens,
A. Suley and H. Thorpe. J. D. Thomson encouraged us to pursue
this experiment, and M. J. Fortin provided helpful statistical
advice. We thank them, E. S. Morton, and T. C. Moermond for
guidance and comments on the manuscript. D. J. Levey gave
encouraging feedback, N. Cordeiro offered invaluable suggestions
for field methods, and for other helpful advice we thank F. Hayes,
L. Manne, L. Nagel, S. Peters, J. Thaler, K. Whitney, and U of
T’s Evolutionary Ecology Group. D. Montoya and made suggestions that greatly improved the manuscript. This study was funded
by operating grants to FHR (NSERC, PREA) and a Munk Centre
for International Studies travel grant to KLL. NSERC, OGS, and
the Dept of Ecology and Evolutionary Biology at the Univ. of
Toronto provided personal funding for KLL. We declare that to
the best of our knowledge, our experiments complied with the
current laws of the Republic of Trinidad and Tobago.
References
Aizen, M. A. and Feinsinger, P. 1994. Forest fragmentation,
pollination and plant reproduction in a chaco dry forest,
Argentina. Ecology 75: 330351.
Beard, J. S. 1944. The natural vegetation of the island of Tobago,
British West Indies. Ecol. Monogr. 14: 135163.
Bond, W. J. 1994. Do mutualisms matter? Assessing the impact of
pollinator and disperser disruption on plant extinction.
Philos. Trans. R. Soc. Lond. B 344: 8390.
Bruna, E. M. 1999. Seed germination in rainforest fragments.
Nature 402: 139.
Chapman, C. A. and Chapman, L. J. 1995. Survival without
dispersers: seedling recruitment under parents. Conserv.
Biol. 9: 675678.
Cordeiro, N. J. and Howe, H. F. 2003. Forest fragmentation
severs mutualism between seed dispersers and an endemic
African tree. Proc. Natl Acad. Sci. USA 100: 1405214056.
Davidar, P. and Morton, E. S. 1986. The relationship between
fruit crop sizes and fruit removal rates by birds. Ecology 67:
262265.
Denslow, J. S. 1987. Fruit removal rates from aggregated and
isolated bushes of the red elderberry, Sambucus pubens. Can.
J. Bot. 65: 12291235.
Denslow, J. S. and Moermond, T. C. 1982. The effect of
accessibility on rates of fruit removal from tropical shrubs: an
experimental study. Oecologia 54: 170176.
Engelbrecht, B. M. J. and Herz, H. M. 2001. Evaluation of
different methods to estimate understorey light conditions in
tropical forests. J. Trop. Ecol. 17: 207224.
ffrench, R. 1991. A guide to the birds of Trinidad and Tobago.
Comstock Publ. Ass.
Fuchs, E. J. et al. 2003. Effects of forest fragmentation and
flowering phenology on the reproductive success and mating
patterns of the tropical dry forest tree Pachira quinata.
Conserv. Biol. 17: 149157.
Galetti, M. et al. 2003. Effects of forest fragmentation, anthropogenic edges and fruit colour on the consumption of
ornithocoric fruits. Biol. Conserv. 111: 269273.
Gray, M. A. et al. 2007. The response of avian feeding guilds to
tropical forest disturbance. Conserv. Biol. 21: 133141.
Herrera, C. M. 1989. Seed dispersal by animals a role in
Angiosperm diversification. Am. Nat. 133: 309322.
Holdridge, L. R. et al. 1971. Forest environments in tropical life
zones. Pergamon.
Howe, H. F. 1979. Fear and frugivory. Am. Nat. 114: 925931.
Howe, H. F. 1986. Seed dispersal by fruit-eating birds and
mammals. In: Murray, D. R. (ed.), Seed dispersal. Academic
Press Australia, pp. 123187.
Howe, H. F. and Smallwood, J. 1982. Ecology of seed dispersal.
Annu. Rev. Ecol. Syst. 13: 201208.
Hurlbert, S. H. 1984. Pseudoreplication and the design of
ecological field experiments. Ecol. Monogr. 54: 187211.
Jordano, P. et al. 2007. Differential contribution of frugivores to
complex seed dispersal patterns. Proc. Natl Acad. Sci. USA
104: 32783282.
Karr, J. R. 1981. Surveying birds in the tropics. In: Ralph, C. J.
and Scott, J. M. (eds), Estimating numbers of terrestrial birds.
Studies in avian biology, No. 6. Allen Press, Inc., pp. 548
553.
Keeler-Wolf, T. H. 1982. Reduced avian densities in Tobago
lower montane rain forest: a resource-based study. PhD thesis.
Univ. of California, Santa Cruz.
Korine, C. et al. 2000. Fruit characteristics and factors affecting
fruit removal in a Panamanian community of strangler figs.
Oecologia 123: 560568.
Kremen, C. 2005. Managing ecosystem services: what do we need
to know about their ecology? Ecol. Lett. 8: 468479.
Kremen, C. et al. 2002. Crop pollination from native bees at risk
from agricultural intensification. Proc. Natl Acad. Sci. USA
99: 1681216816.
Laska, M. S. and Stiles, E. W. 1994. Effects of fruit crop size on
intensity of fruit removal in Viburnum prunifolium (Caprifoliaceae). Oikos 69: 199202.
Lefevre, K. L. 2008. The influence of human disturbance on avian
frugivory and seed dispersal in a neotropical rainforest. PhD
thesis. Univ. of Toronto.
Levey, D. J. 1988a. Spatial and temporal variation in Costa Rican
fruit and fruit-eating bird abundance. Ecol. Monogr. 58:
251269.
Levey, D. J. 1988b. Tropical wet forest treefall gaps and
distributions of understory birds and plants. Ecology 69:
10761089.
Levey, D. J. et al. 1984. Fruit choice in Neotropical birds: the
effect of distance between fruits on preference patterns.
Ecology 65: 844850.
Levey, D. J. et al. 1994. Frugivory: an overview. In: McDade,
L. A. et al. (eds), La Selva: ecology and natural history of a
Neotropical rain forest. Univ. of Chicago Press, pp. 282294.
Levey, D. J. et al. 2005. Effects of landscape corridors on seed
dispersal by birds. Science 309: 146148.
Loiselle, B. A. and Blake, J. G. 2002. Potential consequences of
extinction of frugivorous birds for shrubs of a tropical wet
forest. In: Levey, D. J. et al. (eds), Seed dispersal and
frugivory: ecology, evolution and conservation. CABI Publishing, pp. 397406.
Luck, G. W. and Daily, G. C. 2003. Tropical countryside bird
assemblages: richness, composition, and foraging differ by
landscape context. Ecol. Appl. 13: 235247.
McCarty, J. P. et al. 2002. Spatial and temporal variation in fruit
use by wildlife in a forested landscape. For. Ecol. Manage.
164: 277291.
Moermond, T. C. and Denslow, J. S. 1983. Fruit choice in
Neotropical birds: effects of fruit type and accessibility on
selectivity. J. Anim. Ecol. 52: 407420.
Moermond, T. C. et al. 1986. The influence of morphology on
fruit choice in neotropical birds. In: Estrada, A. and
Fleming, T. H. (eds), Frugivores and seed dispersal. Dr. W.
Junk Publishers, pp. 137146.
Montoya, D. et al. 2008. Animal versus wind dispersal and the
robustness of tree species to deforestation. Science 320:
15021504.
Moore, L. A. and Willson, M. F. 1982. The effect of microhabitat,
spatial distribution, and display size on dispersal of Lindera
benzoin by avian frugivores. Can. J. Bot. 60: 557560.
Morton, E. S. 1973. On the evolutionary advantages and
disadvantages of fruit eating in tropical birds. Am. Nat.
107: 822.
Murray, K. G. 1987. Selection for optimal fruit-crop size in birddispersed plants. Am. Nat. 129: 1831.
9-EV
Orians, G. H. et al. (eds) 1996. Biodiversity and ecosystem
processes in tropical forests. Springer.
Ortiz-Pulido, R. and Rico-Gray, V. 2000. The effect of spatiotemporal variation in understanding the fruit crop size
hypothesis. Oikos 91: 523527.
Poulin, B. et al. 1999. Interspecific synchrony and asynchrony in
the fruiting phenologies of congeneric bird-dispersed plants in
Panama. J. Trop. Ecol. 15: 213227.
Restrepo, C. et al. 1999. Anthropogenic edges, treefall gaps and
fruit-frugivore interactions in a neotropical montane forest.
Ecology 80: 668685.
Saracco, J. F. et al. 2005. Crop size and fruit neighborhood effects
on bird visitation to fruiting Schefflera morototoni trees in
Puerto Rico. Biotropica 37: 8187.
Sargent, S. 1990. Neighbourhood effects on fruit removal by
birds: a field experiment with Viburnum dentatum (Caprifoliaceae). Ecology 71: 12891298.
Schupp, E. W. 1993. Quantity, quality and the effectiveness of
seed dispersal by animals. Vegetatio 107/108: 1529.
Smith, N. et al. (eds) 2004. Flowering plants of the Neotropics.
Princeton Univ. Press.
10-EV
Snow, D. W. 1965. A possible selective factor in the evolution of
fruiting seasons in tropical forest. Oikos 15: 274281.
Snow, D. W. 1971. Evolutionary aspects of fruit-eating by birds.
Ibis 113: 194202.
Stutchbury, B. J. M. and Morton, E. S. 2001. Behavioral ecology
of tropical birds. Academic Press.
Thompson, J. N. and Willson, M. F. 1978. Disturbance and the
dispersal of fleshy fruits. Science 200: 11611163.
Wheelwright, N. T. and Orians, G. H. 1982. Seed dispersal by
animals: contrasts with pollen dispersal, problems of terminology and constraints on coevolution. Am. Nat. 119: 402413.
Willson, M. F. and Traveset, A. 2000. The ecology of seed
dispersal. In: Fenner, M. (ed.), Seeds: the ecology of
regeneration. CABI Publishing, pp. 85110.
Willson, M. F. et al. 1982. Avian frugivore activity in relation to
forest light gaps. Caribb. J. Sci. 18: 16.
Zar, J. H. 1984. Biostatistical analysis. Prentice-Hall.
Appendix 1. Pattern of removal through time for two species of Psychotria fruits, from three rainforest habitats, in 10 replicate experiments
during the 2004 dry season on Tobago. During each replicate, 360 fruits were presented in each habitat (m P. muscosa and t P.
tobagensis). Dates are the first day of a two-day replicate experiment. Values are standardized as the number of fruits removed in a 10 h
period, the minimum amount of time all displays were presented.
Date
Mar 26
Apr 3
Apr 17
Apr 21
Apr 26
Apr 29
May 1
May 4
May 11
May 20
Fruit species
Total fruits removed from forest type
t
m
m
m
t
t
t
t
m
m
Primary
Intermediate
Disturbed
1
39
54
49
15
15
9
32
74
26
1
55
24
44
5
4
12
13
41
6
3
29
11
31
20
7
14
16
75
6
Appendix 2. Presence () and absence (0) of fruit-eating birds censused in the study area on Tobago (Lefevre 2008), during the time period
of fruit removal experiments (MarMay 2004). Letters in brackets denote feeding guilds (f frugivore, o omnivore). Numbers 15 indicate
the five most abundant species in each habitat (duplicate numbers are ties) based on point count censuses. Mist netting data (Lefevre 2008)
were also used to complete this species composition list. Frugivores were defined as species that regularly include fruit in their diet. Although
they are among the most abundant frugivores in all three habitats, rufous-vented chachalaca and orange-winged parrot are not included in
the rankings, because they tend to stay high in the canopy, and may be over-represented in counts due to their loud, frequent calls (Lefevre
unpubl.).
Avian frugivore species
Common name
Rufous-vented chachalaca (f)
Pale-vented pigeon (f)
White-tipped dove (f)
Orange-winged parrot (f)
Collared trogon (o)
Blue-crowned motmot (o)
Red-crowned woodpecker (o)
Golden-olive woodpecker (o)
Barred antshrike (o)
Blue-backed manakin (f)
Ochre-bellied flycatcher (f)
Fuscous flycatcher (o)
Yellow-bellied elaenia (o)
Yellow-breasted flycatcher (o)
Brown-crested flycatcher (o)
Venezuelan flycatcher (o)
Streaked flycatcher (o)
Tropical kingbird (o)
Yellow-legged thrush (f)
Bare-eyed thrush (f)
White-necked thrush (f)
Chivi vireo (o)
Scrub greenlet (o)
Northern waterthrush (o)
Bananaquit (o)
Red-legged honeycreeper (o)
Violaceous euphonia (f)
Blue-gray tanager (f)
Palm tanager (f)
White-lined tanager (f)
Black-faced grassquit (o)
Carib grackle (o)
Shiny cowbird (o)
Crested oropendola (o)
Smooth-billed ani (o)
Rainforest habitats
Latin name
Primary
Intermediate
Disturbed
Ortalis ruficauda
Columba cayennensis
Leptotila verreauxi
Amazona amazonica
Trogon collaris
Momotus momota
Melanerpes rubricapillus
Piculus rubiginosus
Thamnophilus doliatus
Chiroxiphia pareola
Mionectes oleagineus
Cnemotriccus fuscatus
Elaenia flavogaster
Tolmomyias flaviventris
Myiarchus tyrannulus
Myiarchus venezuelensis
Myiodynastes maculatus
Tyrannus melancholicus
Platycichla flavipes
Turdus nudigenis
Turdus albicollis
Vireo chivi
Hylophilus flavipes
Seiurus noveboracensis
Coereba flaveola
Cyanerpes cyaneus
Euphonia violacea
Thraupis episcopus
Thraupis palmarum
Tachyphonus rufus
Tiaris bicolor
Quiscalus lugubris
Molothrus bonariensis
Psarocolius decumanus
Crotophaga ani
total no. species35
4
4
0
1
0
0
0
0
0
0
3
2
0
0
0
0
0
0
22
4
0
2
3
0
0
5
1
0
0
0
0
0
27
3
5
2
0
0
1
0
0
4
31
11-EV