The effects of oil palm plantations on the functional diversity of Amazonian birds

Abstract

Oil palm plantations are rapidly expanding in tropical areas, although the nature of the impacts on the functional roles of the different species in the ecosystem is poorly understood. The present study is the first assessment of how oil palm affects the functional diversity of birds in the Brazilian Amazon and tests the hypothesis that converting forest to oil palm decreases functional diversity of bird communities, selecting species more tolerant to environmental disturbances. We conducted point counts to survey bird communities in 16 plots in the eastern Amazon. We sampled 32 points in riparian forest, 128 in oil palm and 160 in forested habitats. To test whether the conversion of forest into oil palm plantations affects functional diversity of birds we calculated the FD (Functional Diversity) and FRic (Functional Richness) indices. To examine whether oil palm plantations select species functionally more similar than expected by chance we used a null model (SES.FD). FD was significantly higher in the forest plots in comparison with riparian forests and oil palm, and lower in oil palm when compared with riparian forests. FRic, in turn, was greater in forest plots than in oil palm and in riparian forest. These results show that the conversion of forested areas to oil palm represents a great loss of functional strategies. The SES values indicate that in forested habitats bird communities tend to be functionally clustered while in the oil palm they are functionally overdispersed. The functional traits most affected by oil palm were those associated with diet and foraging stratum. In short, oil palm plantations reduced functional diversity of birds, although the presence of riparian forests within the plantations and the fragments of forest adjacent are extremely important for the maintenance of ecosystem services.

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The effects of oil palm plantations on the functional diversity of Amazonian birds
Sara M. Almeida, Larissa C. Silva, Maíra R. Cardoso, Pablo V. Cerqueira, Leandro Juen and Marcos P. D. Santos
Journal of Tropical Ecology / FirstView Article / August 2016, pp 1 - 16
DOI: 10.1017/S0266467416000377, Published online: 05 August 2016
Link to this article: http://journals.cambridge.org/abstract_S0266467416000377
How to cite this article:
Sara M. Almeida, Larissa C. Silva, Maíra R. Cardoso, Pablo V. Cerqueira, Leandro Juen and Marcos P. D. Santos The
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Journal of Tropical Ecology, Page 1 of 16. © Cambridge University Press 2016
doi:10.1017/S0266467416000377
The effects of oil palm plantations on the functional diversity
of Amazonian birds
Sara M. Almeida∗,1, Larissa C. Silva∗,Ma
´
ıra R. Cardoso∗, Pablo V. Cerqueira∗, Leandro Juen∗,†
and Marcos P. D. Santos∗,†
∗Graduate Program in Zoology, Universidade Federal do Par´
a/Museu Paraense Em´
ılio Goeldi, Caixa Postal 479, CEP 66075–110, Bel´
em, Par´
a, Brazil
†Institute of Biological Sciences, Universidade Federal do Par´
a (UFPA), Bel´
em, Par´
a, Brazil
(Received 28 February 2016; revised 27 June 2016; accepted 28 June 2016)
Abstract: Oil palm plantations are rapidly expanding in tropical areas, although the nature of the impacts on the
functional roles of the different species in the ecosystem is poorly understood. The present study is the first assessment
of how oil palm affects the functional diversity of birds in the Brazilian Amazon and tests the hypothesis that converting
forest to oil palm decreases functional diversity of bird communities, selecting species more tolerant to environmental
disturbances. We conducted point counts to survey bird communities in 16 plots in the eastern Amazon. We sampled
32 points in riparian forest, 128 in oil palm and 160 in forested habitats. To test whether the conversion of forest
into oil palm plantations affects functional diversity of birds we calculated the FD (Functional Diversity) and FRic
(Functional Richness) indices. To examine whether oil palm plantations select species functionally more similar than
expected by chance we used a null model (SES.FD). FD was significantly higher in the forest plots in comparison with
riparian forests and oil palm, and lower in oil palm when compared with riparian forests. FRic, in turn, was greater in
forest plots than in oil palm and in riparian forest. These results show that the conversion of forested areas to oil palm
represents a great loss of functional strategies. The SES values indicate that in forested habitats bird communities tend
to be functionally clustered while in the oil palm they are functionally overdispersed. The functional traits most affected
by oil palm were those associated with diet and foraging stratum. In short, oil palm plantations reduced functional
diversity of birds, although the presence of riparian forests within the plantations and the fragments of forest adjacent
are extremely important for the maintenance of ecosystem services.
Key Words: classification tree, ecological corridors, Elaeis guineensis, functional overdispersion, traits
INTRODUCTION
Agricultural expansion caused by the high demand for
food and biodiesel is the principal factor contributing to
deforestation in tropical regions (Malhi et al.2014, Tilman
et al.2001). In recent years, the cultivation of one crop,
oil palm (Elaeis guineensis Jacq.), has been expanding at an
annual rate of 9% worldwide, driven by the demand for
low-cost vegetable oils for food-processing and biofuels
(Fitzherbert et al.2008,Malhiet al. 2014). In Brazil,
the production of palm oil is concentrated in the eastern
Amazon basin, in particular in the state of Par´
a, where in
2014 an estimated total of 329 000 ha was planted with
E. guineensis (Villela et al.2014).
1Corresponding author. Email: salmeida.eco@gmail.com
Most of the research into the effects of oil palm
plantations on local biodiversity has been conducted in
Asia, and shows major impacts on species richness and
the structure of biological communities (Aratrakorn et al.
2006,Azharet al.2013, Fitzherbert et al.2008,Koh
2008, Savilaakso et al.2014). Similarly, in the eastern
Amazon, recent studies show that these plantations
reduce the species richness and alter the composition of
the assemblages of aquatic insects (Heteroptera) (Cunha
et al.2015), frogs (Correa et al.2015) and birds (Lees et al.
2015).
In Par´
a State, oil palm plantations are considered to
be a low-impact land-use and may substitute native
vegetation of riparian forests and legal reserves in
smallholdings (Lees et al.2015). However, this crop
cannot be considered low-impact and cannot substitute

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2ALMEIDA ET AL.
native forest vegetation for large property owners,
because it affects communities as intensively as cattle
pasture (Lees et al.2015). Oil palm plantations are
homogeneous environments characterized by a less
complex structure (Fitzherbert et al.2008), while natural
forest is heterogeneous and capable of supporting a
greater variety of niches, which support a more complex
local biodiversity (Tews 2004).
Functional diversity is considered to be one of the most
ecologically relevant measures of biodiversity (Tilman
2001), due to the fundamental role of this parameter
in the maintenance and functioning of community-level
ecological processes (D´
ıaz & Cabido 2001, Petchey &
Gaston 2006, Tilman 2001). This measure estimates
the differences among organisms directly, based on
their functional characteristics, and incorporates the
ecological similarities among the species that coexist in
a given community (Petchey & Gaston 2006, Tilman
2001).
Understanding the implications of land-use change
for functional diversity of birds is essential, given that
these animals contribute a range of ecosystem services,
including pollination (Bawa 1990,Lucket al.2013), seed
dispersal (Pizo & Galetti 2010) and predation (Perfecto
et al.2004),as well asoccupying a widerange of ecological
niches (S¸ekercio˘
glu 2012). Thus, the objective of the
present study was to verify the functional structure of
bird communities in forested habitats and in oil palm
plantations in the eastern Brazilian Amazon region. Our
hypothesis is that the bird communities in plantations
are functionally more similar than expected by chance
due to low niche variability in this habitat, while in
forested areas bird communities are functionally more
different than expected by chance. In addition, we test the
hypothesis that the functional diversity of birds in areas
of forest is higher than in plantations, given that forested
habitats support bird assemblages with diverse functional
characteristics.
METHODS
Study area
The study area was located within the Agropalma agro-
industrial complex (02º3618S, 48º4706W; Figure 1),
which consists of 64 000 ha of legal reserve (fragments
of rain forest) and 39 000 ha of oil palm plantations. The
company has Roundtable on Sustainable Palm Oil (RSPO)
certification, which implies that the production process
respects various environmental requirements. The forest
fragments were between 5000 and 17 000 ha, and were
dominated by unflooded (terra firme) forests (Bolfe &
Batistella 2011, Portes et al.2011). The fragments can
be considered well-preserved since they are protected and
monitored by the company and no logging and hunting
is allowed.
The present study focused on 16 plots, eight of which
were located in oil palm plantations, and eight in adjacent
fragment of native forest. The plantation plots were
established within the areas planted exclusively with
Elaeis guineensis and all oil palm plots included at least
one stream (Figure 1). The inclusion of watercourses in
the study plots was based on the fact that riparian forest is
a protected type of habitat under Brazilian legislation and
provides potential corridors for dispersal between forest
fragments(Develey & Pongiluppi2010,Hawesetal.2008,
Lees & Peres 2008). The portion of each plot that included
the stream margins comprises a buffer zone of natural
vegetation, with a width of 10–30 m on each side of the
stream. Outside this zone, the plot is composed entirely of
oil palm plantation (10–15 y).
Sampling of the birds
The bird fauna was sampled using an adapted point count
method (Blondel et al.1970, Vielliard et al.2010), in May
and December 2012, with all the plots sampled during
each campaign. At each plot a set of 10 sample points was
established, separated by a distance of 200 m from one
another, at which 10-min counts were conducted. In the
plantation areas, eight point counts were conducted in
oil palm plantations and two point counts next to each of
the margins of the stream. In total, we sampled 32 points
in riparian forest, 128 in oil palm plantations and 160 in
forested habitats.
The number of individuals of each species observed
and/or heard within a radius of 50 m of the observer
was recorded between 05h00 and 10h30. Considering
the narrow width of the riparian buffer and the risk of
double counting, our experienced ornithologists (PVC
and MPDS) recorded only the species within the limits
of the riparian forest. Despite the difference in the
number of point counts, the species accumulation curves
indicated asymptotic tendency for the three treatments
(Appendix 1).
Functional traits
To quantify functional diversity, 17 functional traits were
used for each species, following Wilman et al.(2014).
Theywererelatedtodiet(1–invertebrates;2–mammals,
birds; 3 – reptiles, amphibians; 4 – fish; 5 – vertebrates –
general or unknown (for species where it was not clear
what kind of vertebrates were being eaten), 6 – scavenge,
garbage, carcasses, carrion; 7 – fruit, drupes; 8 – nectar,
pollen, plant exudates, gums; 9 – seed, maize, nuts, spores,
grains; 10 – other plant material), foraging stratum

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Birds in oil palm plantations 3
Figure 1. Map of Brazil showing the state of Par´
a (hatched), sampled sites in Agropalma agro-industrial complex (a) and survey experimental design
(b). Squares represent sites in forest and triangles are those located in oil palm plantations.
(water, ground, understorey, mid to high levels, canopy,
aerial) and body mass (geometric mean of average values
provided for both sexes). Diet and foraging stratum were
based on estimated percentage usage of each category as
determined by the literature (Wilman et al.2014).
Additionally, four biometric parameters were estab-
lished for each species (length, height, and width of the
beak, and the length of the tarsus), given their relationship
with the foraging strategies adopted by the species and the
types of resource it exploits. These measurements were
obtained from the ornithological collection of the Goeldi
Museum in Bel´
em, Par´
a, Brazil. Three male specimens
of each species were measured using a digital caliper
with a precision of 0.1 mm, and three readings of each
measurement were taken from each specimen, with the
mean of these three values being used for analysis. The
specimens were selected based on the proximity of their
collecting localities to the geographic location of the
present study.
Data analysis
A matrix presenting the 21 functional characteristics
of each species was constructed and converted into a
similarity matrix using Gower’s measure of distance
(Pavoine et al.2009). Then a functional dendrogram
was produced using the UPGMA clustering approach.
Values of functional diversity (FD), which are the sum
of the branches of the functional dendrogram, were
calculated in the pd function of the FD package in the
R environment (Lalibert´
e & Legendre 2010). To test
whether oil palm plantations affect functional diversity of
birds the FRic (functional richness) was also calculated,
which quantifies the volume of functional space occupied
by the community irrespective of the species richness
(Cornwell et al.2006, Mouchet et al. 2010, Vill´
eger et al.
2008).
Species richness, FD and FRic were compared among
treatments (forest, riparian forest and plantation) using
one-way ANOVA test with intervals followed by a Tukey
post hoc test to check for significant pairwise differences.
FD is one of the best parameters for the detection
of the rules of composition under different scenarios of
simulation (Mouchet et al.2010), and has been widely
used for the evaluation of the structural patterns of
bird assemblages (Devictor et al.2010). To evaluate
whether the species that make up an assemblage are
functionally more similar to one another than expected
by chance the standardized effect size (SES) of FD
was calculated. This model (SES.FD) is the difference
between the observed value of FD and the mean value
of randomized assemblages, divided by the respective
standard deviation of the 999 randomized values
(see Sobral & Cianciaruso 2015 for similar application).
The analysis and the randomizations were run in the

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4ALMEIDA ET AL.
picante package of the R environment using ses.pd with
the taxa.label argument for the null models (Kembel et al.
2010).
To test whether the SES values calculated for the
bird communities in the forests, riparian forest and
plantation were higher (i.e. functional overdispersion)
or lower (i.e. functional clustering) than expected by
chance Fisher’s P was used (Whitlock 2005), through
function combine.test in survcomp package (Schroeder
et al.2011). This analysis combines the probabilities
(P-values) from several independent tests upon the same
null hypothesis (Whitlock 2005). Then, to verify the
relationship between richness and functional diversity,
a Pearson’s correlation between SES values and species
richness was conducted.
To identify which functional characteristics were most
associated to forested and plantation sites a classification
tree using the traits was constructed (Breiman et al.
1984). The species recorded in the forest but absent
in the plantation (absences) and the species present at
plantation (presences) were considered. Thus, we can
verify the functional attributes more strongly affected by
oil palm plantations. In this case, we did not consider
species recorded in riparian forest. The classification of the
guilds was based on Wilman et al.(2014), who classified
species that prefer 50% or more of a particular item of diet
or foraging stratum to be specialists. Species that used the
foraging stratum or dietary items in proportions smaller
than 50% were classified as generalists. For diet items,
the species were grouped according to dietary preference:
fruits-nectar, invertebrates, seeds-plants, vertebrates and
omnivores. Considering the foraging stratum, the species
were classified in ground, understorey, mid to high levels,
canopy, aerial, water and generalist.
Classification tree models were performed in rpart
package of the R environment. Gini’s impurity function
was used as a division criterion, thus terminal nodes have
the maximum homogeneity among all the possible traits.
Cross-validation (10-fold cross-validation) was used to
decide how much of the tree model to retain, i.e. the
optimal tree size. For plotting rpart tree we used the
rpart.plot package.
Spatial autocorrelation of bird composition was
evaluated using Mantel’s statistic (permutations =999),
performed in ade4 R package (Dray & Dufour 2007), and
there was no significant spatial autocorrelation of bird
assemblages within (r =0.009, P =0.35) or between
sites (r =0.02, P =0.40).
RESULTS
We recorded 248 bird species, including 185 species in
the forested habitat, 116 in riparian forests and 58 in
the oil palm plantations (for a full list see Appendix 2).
Figure 2. Parameters of diversity recorded for the bird assemblages
observed in forest habitats and oil palm plantations in eastern Amazon,
state of Par´
a, Brazil: SR – Species richness (a), FD – Functional diversity
(b), and FRic – Functional richness (c). The middle line represents
median, lower and upper bounds of box plots represent 25th and
75th percentiles (first and third quartiles, respectively), whiskers shows
minimum and maximum values. Values indicated with different letters
are significantly different (according to a Tukey test 95%).
The mean species richness was 87.2 ±28 in the forest
plots (N =8, range =71–106), 40.2 ±8.7 in riparian
forests (N =8, range =28–54), and 25.8 ±5.7 in
oil palm plantation (N =8, range =19–34), and
these differences were significant between all treatments
(F=102, df =21, P <0.001; Figure 2a). The functional
diversity (FD), in turn, was 2.1 and 1.7 times higher in the
forest plots (mean =7.41 ±1.83, range =6.43–8.18)
in comparison with the plantation (mean =3.43 ±0.42,
range =2.78–4.05) and riparian forests (mean =4.37
±0.78, range =3.09–5.57), respectively. Furthermore,
the FD was lower in the plantations when compared with
riparian forest (F=89.7, df =21, P <0.001; Figure 2b).

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Birds in oil palm plantations 5
Figure 3. Classification tree showing the functional characteristics most associated with the presence and absence of bird species in oil palm plantation
in eastern Amazon, state of Par´
a, Brazil. The values in the terminal branches represent the proportion of species persisting or absent in plantation,
considering the total number of species with the functional characteristics of the branch, and the percentage (%) of species that have the functional
features of each of the terminal groups.
The functional richness (FRic) was greater in forest plots
(mean =102 ±56.2, range =37.6–213) in comparison
with the plantation (mean =7.28 ±5.71, range =2.34–
19.9) and riparian forest (mean =30.7 ±27.6, range
=2.74–78.1) (F=11.9, df =21, P =0.01; Figure 2c).
Nonetheless, FRic was not significantly different between
plantation and riparian forest (P =0.48).
The most important variables associated with the
presence or absence of forest birds in the palm
plantation were diet (44%) and foraging stratum (19%).
Therefore, these variables were used in the model. Other
characteristics (body mass, length of tarsus, length of
beak, height of beak and width of beak) contributed with
10%, 9%, 8%, 8% and 2%, respectively. According to this
model, the species that feed on fruits, nectar, invertebrates
or have a varied diet (omnivorous) had a 14% probability
of being absent in the oil palm. On the other hand, those
that eat seeds (granivorous), vertebrates and feed on the
ground had a 100% probability of occurring in oil palm
plantation. However, those with similar diet (seeds and
vertebrates), but foraging in the understorey, in the water,
in the middle and high stratum, or being a generalist for
foraging strata had a 41% probability of being absent from
oil palm (Figure 3).
Bird communities in forest areas returned values of
functional diversity equal to that expected by chance
indicating random functional structure (Fisher’s P =
0.24). Riparian forests, in turn, showed random structure
to both clustering (Fisher’s P =0.45) and functional
overdispersion (Fisher’s P =0.11). By contrast, the
indices recorded for the plantation indicated functional
overdispersion (Fisher’s P <0.001), that is, the
species had functional characteristics more different than
Figure 4. Relationship between species richness of birds in forest, oil
palm plantation and riparian forest and their respective standardized
effect size of functional diversity (SES.FD) in eastern Amazon, state of
Par´
a, Brazil. Values greater than zero indicate functional overdispersion
while values lower than zero indicate functional clustering.
expected by chance. In general, bird communities with
higher species richness (forested habitats) had a tendency
to be functionally clustered, namely, the species were
more similar to each other in relation to the set of traits
(R =−0.81, P <0.001, Figure 4).
DISCUSSION
The Amazon rain forest in Brazil is highly threatened
by illegal logging, mining and agriculture, including oil
palm plantations (Lees et al.2015, Vieira et al.2008,
Villela et al.2014). Although it is known that in eastern

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6ALMEIDA ET AL.
Amazon these plantations retain impoverished avian
communities (Lees et al.2015), the present study is
the first assessment of how oil palm plantations affect
functional diversity in the Brazilian Amazon. Here we
found that oil palm plantations negatively affect the
functional diversity of birds. This result is supported
by similar studies in Australia, Borneo and the New
World, which showed that agriculture is the land use
that most reduces functional diversity in birds (Edwards
et al.2013,2014;Flynnet al.2009,Lucket al.2013),
dung beetles (Edwards et al.2014) and mammals (Flynn
et al.2009), while logging (Edwards et al.2013)and
wildfire (Hidasi-Neto et al.2012) did not cause significant
declines.
We found that forest fragments and riparian forests had
higher functional diversity (FD) and functional richness
(FRic) than plantations. Similarly, in Colombia, FD and
FRic were higher in remnant forests than in oil palm
plantation and in pasture (Prescott et al.2016). These
results indicate that conversion of forest to oil palm
plantations represents a great loss of functional strategies
(Azhar et al.2013). This could be explained by the lower
complex structure and lower niche variability in oil palm
plantations (Fitzherbert et al. 2008), thus accommodating
bird assemblages with limited functional characteristics
(Edwards et al. 2013,Hutchinson1957).
The conversion of the forest into monocultures may
result in a series of changes in the functional structure and
interspecific interactions of a community (S¸ekercio˘
glu
2012). In the present study, the functional traits most
affected by oil palm were those related to diet and
foraging stratum. Oil palm plantations did not support
species that use different foraging stratum (for example,
the understorey) while in forested habitats vertical
stratification allowed the coexistence of many bird
species (Lovejoy 1974). Besides that, tropical forest birds
exhibit a high degree of specialization (Rosenberg 1990).
For example, frugivorous and nectarivorous birds (e.g.
Trogonidae, Psittacidae and Trochilidae) and understorey
insectivorous birds (e.g. Thamnophilidae, Formicariidae)
are more closely associated with the forested habitats
and are highly sensitive to changes in the environment
(Galetti & Aleixo 1998,S¸ekercio˘
glu 2006, Zanette
et al. 2000). Granivorous birds, in turn, are favoured
in open areas where grasses proliferate, providing an
important and accessible feeding resource (Wiens &
Johnston 1977). In natural habitats, omnivorous birds
can contribute to ecosystem stability given their ability
to vary feeding strategies, and their role as additional
predators prevents the rapid population expansion of the
prey (Fagan 1997, Namba et al.2008,S¸ekercio˘
glu et al.
2004).
Although the functional richness did not differ between
plantation and riparian forests, we found that these
forested areas helped to maintain the functional diversity
of Amazonian birds. By contrast, Edwards et al.(2010)
studied taxonomic diversity of birds in fragments of logged
forest (0.7–87 ha) surrounded by oil palm, contiguous
logged forest, and oil palm plantations in Borneo, and
they verified that fragments had a species composition
more similar to that of oil palm than of contiguous forest.
Furthermore, the spatial juxtaposition of fragments and
oil palm in the landscape had little effect on the bird
diversity (Edwards et al. 2010).
Other studies showed that forest remnants found in the
vicinity of oil palm plantations constitute an important
refuge for some forest-dwelling birds in the oil palm
matrix (Azhar et al.2013,Koh2008, Prescott et al.
2016). In this case, the connectivity between the riparian
forests and adjacent forest fragments is essential for the
maintenance of the ecosystem services in Amazonian
forests, buffering the effects of the frequent changes in
land use.
Here, we observed that the negative SES values
indicated small functional distances between the species
that coexist in the forest areas, though the functional
structure of these communities was random (Fisher’s
P>0.05). In addition, an increase in the number of
species can promote functional clustering in Amazonian
forest birds. This may be accounted by the greater
environmental complexity of forested habitats and the
consequent increase in the availability of resources
allowing the coexistence of ecologically similar species
(Cornwell et al.2006,Tewset al.2004). In this case, the
random loss of some of the species found in these areas of
forest may not necessarily result in any loss of functional
diversity or alterations in ecosystem function (Edwards
et al.2013, Elmqvist et al. 2003,Lucket al.2013, Petchey
et al. 2007).
The tendency towards functional redundancy (high
functional similarity) was also found for dung beetles
within primary forest in Borneo (Edwards et al.2014),
as well as in Amazonian birds (Hidasi-Neto et al.
2012) and forest bird assemblages in Brazilian savanna
(Sobral & Cianciaruso 2015). Prescott et al.(2016)also
found higher levels of functional redundancy of bird
assemblages in forests than in oil palm. On the other hand,
bird assemblages from forests disturbed by wildfires and of
oil palm plantations have the tendency to be functionally
overdispersed (Edwards et al.2013, Hidasi-Neto et al.
2012).
Nevertheless, in oil palm plantations bird assemblages
were functionally overdispersed because the reduction of
resources may have promoted the occurrence of more
functionally unique species. Functional redundancy is
low when many of the species found in the community
are functionally unique (that is, their traits do not overlap)
and, in the case of this study, the loss of species has major
implications for the functioning of the ecosystem (Luck
et al.2013).

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Birds in oil palm plantations 7
It is important to consider that despite the knowledge
that many bird species are dependent on riparian forest
(Develey & Pongiluppi 2010), the proximity between
plantation and riparian forest may have enabled spillover
of forest birds at the edge and these were recorded within
the plantations. Land-use intensification has led to a
landscape mosaic that juxtaposes human-managed and
natural areas and the probability of spillover effect will
only increase, especially in systems that differ in resource
availability (e.g. oil palm plantation vs. riparian forest)
(Blitzer et al.2012). In this context, Prescott et al.(2016)
found that there was spillover of FD and FRic from forest
fragments into oil palm and pasture. Thus, in a landscape
that has no forest fragments near the plantations, we
would expect to see lower functional diversity values
(Prescott et al.2016).
We found that oil palm plantation causes great losses in
FD and FRic and affects functional groups that are more
sensitive to environmental perturbation. Thus, it would
be better to produce oil palm in areas where there is no
risk of forest conversion (e.g. abandoned cattle pasture)
(Bastos et al.2001). As a mitigation measure, we suggest
the creation of forested buffer zones around the oil palm
plantation and protection of the remnant forest patches in
the landscape, because the tropical landscape needs to be
designed in recognition of its biodiversity, economic and
livelihood needs (Koh 2008,Kohet al.2009).
Overall, the results of the present study indicate that
the layout of oil palm plantations in the Amazon basin
should include the maintenance of tracts of forest in
areas adjacent to the plantations, as well as riparian
forests within the plantation, as a means of connecting
these tracts. In addition, future studies must consider
the functional groups most affected when evaluating
the response of communities to modifications in the
environment, given that the potential for a more refined
analysis will be lost when the species are considered to be
equivalent to one another.
ACKNOWLEDGEMENTS
This study was supported financially by Conservation
International, the Agropalma Group, the U.S. Agency
for International Development (USAID) – Biodiversity
and Socio-Economic Impacts of Palm Oil Bioenergy
Development in the Brazilian Amazon, and the Fundac¸ ˜
ao
Amazˆ
onia Paraense de Amparo `
a Pesquisa (FAPESPA).
We are grateful to CAPES (the Brazilian Higher Education
Training Program) for providing a doctoral stipend to
SMA, a master’s stipend to MRC and LCS, and Propesp-
UFPA for manuscript translation. The Brazilian National
Research Council (CNPq) provided PVC with a graduate
stipend, and LJ (process 303252/2013-8) with research
fellowships.
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10 ALMEIDA ET AL.
Appendix 1. Species rarefaction curves per point count
considering avian assemblage in riparian forest (a), oil palm
plantation (b) and forest habitats (c) in eastern Amazon, state of
Par´
a, Brazil.

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Birds in oil palm plantations 11
Appendix 2. Systematic list (following Piacentini et al. 2015) of bird species recorded in the forest
(For), riparian forests (RF) and oil palm plantation (Pla) in Agropalma agro-industrial complex,
state of Par´
a, Brazil.
Taxon Name For RF Pla
Tinamiformes
Tinamidae
Tinamus guttatus White-throated tinamou 1
Crypturellus cinereus Cinereous tinamou 1
Crypturellus soui Little tinamou 1
Crypturellus strigulosus Brazilian tinamou 1
Crypturellus variegatus Variegated tinamou 1
Anseriformes
Anatidae
Cairina moschata Muscovy duck 1
Galliformes
Cracidae
Penelope superciliaris Rusty-margined guan 1
Ortalis superciliaris Buff-browed chachalaca 1
Pelecaniformes
Threskiornithidae
Mesembrinibis cayennensis Green ibis 1
Cathartiformes
Cathartidae
Coragyps atratus Black vulture 1
Accipitriformes
Accipitridae
Elanoides forficatus Swallow-tailed kite 1 1
Harpagus bidentatus Double-toothed kite 1
Geranospiza caerulescens Crane hawk 1
Heterospizias meridionalis Savanna hawk 1
Rupornis magnirostris Roadside hawk 1 1
Buteo nitidus Gray hawk 1
Harpia harpyja Harpy eagle 1
Spizaetus tyrannus Black hawk-eagle 1
Gruiformes
Rallidae
Laterallus viridis) Russet-crowned crake 1
Laterallus exilis Grey-breasted crake 1
Charadriiformes
Charadriidae
Vanellus chilensis Southern lapwing 1
Columbiformes
Columbidae
Columbina passerina Common ground-gove 1 1
Columbina minuta Plain-breasted ground-dove 1
Columbina talpacoti Ruddy ground-dove 1 1
Patagioenas cayennensis Pale-vented pigeon 1
Patagioenas plumbea Plumbeous pigeon 1 1
Patagioenas subvinacea Ruddy pigeon 1
Leptotila verreauxi White-tipped dove 1 1
Leptotila rufaxilla Grey-fronted dove 1
Geotrygon montana Ruddy quail-dove 1
Cuculiformes
Cuculidae
Coccycua minuta Little cuckoo 1
Piaya cayana Squirrel cuckoo 1 1
Coccyzus melacoryphus Dark-billed cuckoo 1
Crotophaga ani Smooth-billed ani 1 1
Tapera naevia Striped cuckoo 1
Strigiformes
Strigidae
Megascops usta Austral screech-owl 1
Pulsatrix perspicillata Spectacled owl 1
Glaucidium hardyi Amazonian pygmy-owl 1

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12 ALMEIDA ET AL.
Appendix 2. Continued.
Taxon Name For RF Pla
Nyctibiiformes
Nyctibiidae
Nyctibius griseus Common potoo 1
Caprimulgiformes
Caprimulgidae
Nyctiphrynus ocellatus Ocellated poorwill 1
Antrostomus rufus Rufous nightjar 1 1
Lurocalis semitorquatus Short-tailed nighthawk 1
Nyctidromus albicollis Pauraque 1 1
Apodiformes
Apodidae
Chaetura spinicaudus Band-rumped swift 1
Chaetura brachyura Short-tailed swift 1
Trochilidae
Glaucis hirsutus Rufous-breasted hermit 1 1
Phaethornis ruber Reddishhermit 1 1 1
Phaethornis superciliosus Long-tailed hermit 1 1
Campylopterus largipennis Grey-breasted sabrewing 1 1
Florisuga mellivora White-necked jacobin 1 1
Topaza pella Crimson topaz 1 1
Thalurania furcata Fork-tailed woodnymph 1 1
Amazilia fimbriata Glittering-throated emerald 1 1 1
Trogoniformes
Trogonidae
Trogon melanurus Black-tailed trogon 1
Trogon viridis White-tailed trogon 1 1
Trogon ramonianus Amazonian trogon 1
Trogon rufus Black-throated trogon 1
Coraciiformes
Alcedinidae
Megaceryle torquata Ringed kingfisher 1
Chloroceryle aenea American pygmy kingfisher 1
Chloroceryle americana Green kingfisher 1
Momotidae
Momotus momota Amazonian motmot 1 1
Galbuliformes
Galbulidae
Galbula cyanicollis Blue-cheeked jacamar 1 1
Galbula dea Paradise jacamar 1
Jacamerops aureus Great jacamar 1
Bucconidae
Notharchus hyperrhynchus White-necked puffbird 1
Notharchus tectus Pied puffbird 1
Bucco tamatia Spotted puffbird 1
Bucco capensis Collared puffbird 1
Nystalus torridus Eastern striolated-puffbird 1
Malacoptila rufa Rufous-necked Puffbird 1
Monasa nigrifrons Black-fronted nunbird 1 1
Monasa morphoeus White-fronted nunbird 1 1
Piciformes
Ramphastidae
Ramphastos tucanus White-throated toucan 1 1
Ramphastos vitellinus Channel-billed toucan 1 1
Selenidera gouldii Gould’s Toucanet 1
Pteroglossus inscriptus Lettered aracari 1
Pteroglossus bitorquatus Red-necked aracari 1
Pteroglossus aracari Black-necked aracari 1 1
Picidae
Picumnus exilis Golden-spangled piculet 1
Melanerpes cruentatus Yellow-tufted woodpecker 1
Veniliornis affinis Red-stained woodpecker 1
Piculus flavigula Yellow-throated woodpecker 1 1

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Birds in oil palm plantations 13
Appendix 2. Continued.
Taxon Name For RF Pla
Piculus paraensis Belem golden-green woodpecker 1
Celeus undatus Waved woodpecker 1
Celeus elegans Chestnut woodpecker 1
Celeus flavus Cream-coloured woodpecker 1
Celeus torquatus Ringed woodpecker 1
Dryocopus lineatus Lineated woodpecker 1 1
Campephilus rubricollis Red-necked woodpecker 1 1
Falconiformes
Falconidae
Caracara plancus Southern caracara 1
Milvago chimachima Yellow-headed caracara 1
Herpetotheres cachinnans Laughing falcon 1 1
Micrastur ruficollis Barred forest-falcon 1 1
Micrastur mintoni Cryptic forest-falcon 1
Psittaciformes
Psittacidae
Ara macao Scarlet macaw 1
Ara chloropterus Red-and-green macaw 1
Pyrrhura coerulescens Pearly parakeet 1
Pyrrhura amazonum Santarem parakeet 1
Brotogeris versicolurus Canary-winged parakeet 1
Brotogeris chrysoptera Golden-winged parakeet 1 1
Pionites leucogaster White-bellied parrot 1 1
Pyrilia vulturina Vulturine parrot 1
Pionus menstruus Blue-headed parrot 1 1
Pionus fuscus Dusky parrot 1
Amazona farinosa Mealy parrot 1 1
Amazona amazonica Orange-winged parrot 1 1 1
Deroptyus accipitrinus Red-fan parrot 1
Passeriformes
Thamnophilidae
Pygiptila stellari Spot-winged antshrike 1
Myrmotherula axillaris White-flanked antwren 1 1
Myrmotherula longipennis Long-winged antwren 1 1
Myrmotherula menetriesii Gray antwren 1 1
Formicivora grisea White-fringed antwren 1 1
Isleria hauxwelli Plain-throated antwren 1 1
Thamnomanes caesius Cinereous antshrike 1 1
Dysithamnus mentalis Plain antvireo 1
Herpsilochmus rufimarginatus Rufous-winged antwren 1 1
Thamnophilus palliatus Chestnut-backed antshrike 1 1
Thamnophilus aethiops White-shouldered antshrike 1 1
Thamnophilus amazonicus Amazonian antshrike 1 1
Taraba major Great antshrike 1
Hypocnemoides maculicauda Band-tailed antbird 1
Sclateria naevia Silvered antbird 1 1
Pyriglena leuconota White-backed Fire-eye 1 1
Cercomacra cinerascens Grey antbird 1 1
Cercomacra laeta Willis’s antbird 1 1
Willisornis vidua Xingu scale-backed antbird 1 1
Phlegopsis nigromaculata Black-spotted bare-eye 1
Conopophagidae
Conopophaga roberti Hooded gnateater 1
Grallariidae
Grallaria varia Variegated antpitta 1
Formicariidae
Formicarius colma Rufous-capped antthrush 1
Formicarius analis Black-faced antthrush 1
Scleruridae
Sclerurus macconnelli Tawny-throated leaftosser 1

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14 ALMEIDA ET AL.
Appendix 2. Continued.
Taxon Name For RF Pla
Dendrocolaptidae
Dendrocincla fuliginosa Plain-brown woodcreeper 1
Deconychura longicauda Long-tailed woodcreeper 1
Glyphorynchus spirurus Wedge-billed woodcreeper 1 1
Xiphorhynchus spixii Spix’s woodcreeper 1 1
Xiphorhynchus obsoletus Striped woodcreeper 1
Xiphorhynchus guttatus Buff-throated woodcreeper 1 1
Dendroplex picus Straight-billed woodcreeper 1 1
Lepidocolaptes layardi Layard’s woodcreeper 1 1
Dendrocolaptes medius Todd’s woodcreeper 1
Xenopidae
Xenops minutus Plain xenops 1
Furnariidae
Automolus paraensis Para foliage-gleaner 1 1
Anabacerthia ruficaudata Rufous-tailed foliage-gleaner 1
Philydor erythrocercum Rufous-rumped foliage-gleaner 1
Synallaxis albescens Pale-breasted spinetail 1
Synallaxis rutilans Ruddy spinetail 1
Synallaxis gujanensis Plain-crowned spinetail 1 1
Pipridae
Tyranneutes stolzmanni Dwarf tyrant-manakin 1
Pipra fasciicauda Band-tailed manakin 1
Ceratopipra rubrocapilla Red-headed manakin 1 1
Manacus manacus White-bearded manakin 1 1
Dixiphia pipra White-crowned manakin 1 1
Onychorhynchidae
Onychorhynchus coronatus Royal flycatcher 1
Terenotriccus erythrurus Ruddy-tailed flycatcher 1
Tityridae
Schiffornis turdina Thrush-like schiffornis 1
Iodopleura isabellae White-browed purpletuft 1
Tityra inquisitor Black-crowned tityra 1
Tityra cayana Black-tailed tityra 1
Tityra semifasciata Masked tityra 1
Pachyramphus marginatus Black-capped becard 1 1
Cotingidae
Lipaugus vociferans Screaming piha 1 1
Xipholena lamellipennis White-tailed cotinga 1
Querula purpurata Purple-throated fruitcrow 1
Phoenicircus carnifex Guianan red-cotinga 1
Pipritidae
Piprites chloris Wing-barred piprites 1
Platyrinchidae
Platyrinchus saturatus Cinnamon-crested spadebill 1
Platyrinchus platyrhynchos White-crested spadebill 1
Rhynchocyclidae
Mionectes macconnelli McConnell’s flycatcher 1
Rhynchocyclus olivaceus Olivaceous flatbill 1
Tolmomyias sulphurescens Yellow-olive flycatcher 1
Tolmomyias assimilis Yellow-margined flycatcher 1
Tolmomyias poliocephalus Gray-crowned flycatcher 1 1
Tolmomyias flaviventris Yellow-breasted flycatcher 1 1
Todirostrum cinereum Common Tody-flycatcher 1 1
Poecilotriccus sylvia Slate-headed tody-flycatcher 1 1
Myiornis ecaudatus Short-tailed pygmy-tyrant 1
Lophotriccus galeatus Helmeted pygmy-tyrant 1
Tyrannidae
Zimmerius gracilipes Slender-footed tyrannulet 1
Camptostoma obsoletum Southern Beardless-Tyrannulet 1 1
Elaenia flavogaster yellow-bellied elaenia 1
Myiopagis gaimardii Forest elaenia 1 1
Tyrannulus elatus Yellow-crowned tyrannulet 1 1

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Birds in oil palm plantations 15
Appendix 2. Continued.
Taxon Name For RF Pla
Phaeomyias murina Mouse-colored tyrannulet 1 1
Attila cinnamomeus Cinnamon attila 1 1
Attila spadiceus Bright-rumped attila 1
Legatus leucophaius Piratic flycatcher 1 1
Ramphotrigon ruficauda Rufous-tailed flatbill 1
Myiarchus tuberculifer Dusky-capped flycatcher 1
Myiarchus ferox Short-crested flycatcher 1 1 1
Rhytipterna simplex Grayish mourner 1
Pitangus sulphuratus Great kiskadee 1 1
Myiodynastes maculatus Streaked flycatcher 1
Megarynchus pitangua Boat-billed flycatcher 1 1
Myiozetetes cayanensis Rusty-margined Flycatcher 1
Myiozetetes similis Social flycatcher 1
Tyrannus melancholicus Tropical Kingbird 1 1
Empidonomus varius Variegated flycatcher 1 1
Vireonidae
Cyclarhis gujanensis Rufous-browed peppershrike 1 1 1
Vireo chivi Chivi vireo 1 1
Hylophilus semicinereus Gray-chested greenlet 1 1
Hylophilus pectoralis Ashy-headed greenlet 1 1
Tunchiornis ochraceiceps Tawny-crowned greenlet 1
Troglodytidae
Microcerculus marginatus Scaly-breasted wren 1
Troglodytes musculus Southern house wren 1 1 1
Pheugopedius genibarbis Moustached wren 1 1
Polioptilidae
Ramphocaenus melanurus Long-billed gnatwren 1 1
Polioptila plumbea Tropical gnatcatcher 1
Turdidae
Turdus leucomelas Pale-breasted thrush 1 1
Turdus fumigatus Cocoa thrush 1
Turdus albicollis White-necked thrush 1
Passerellidae
Arremon taciturnus Pectoral sparrow 1 1
Icteridae
Psarocolius viridis Green oropendola 1 1
Psarocolius decumanus Crested oropendola 1
Psarocolius bifasciatus Olive oropendola 1
Cacicus haemorrhous Red-rumped cacique 1 1
Cacicus cela Yellow-rumped cacique 1 1
Icterus cayanensis Epaulet oriole 1
Sturnella militaris Red-breasted blackbird 1 1
Mitrospingidae
Lamprospiza melanoleuca Red-billed pied tanager 1
Thraupidae
Coereba flaveola Bananaquit 1 1 1
Saltator maximus Buff-throated saltator 1 1
Saltator grossus Slate-coloured grosbeak 1 1
Tachyphonus rufus White-lined tanager 1
Ramphocelus carbo Silver-beaked tanager 1 1 1
Lanio surinamus Fulvous-crested tanager 1
Tangara gyrola Bay-headed tanager 1
Tangara mexicana Turquoise tanager 1
Tangara punctata Spotted tanager 1
Tangara episcopus Blue-grey tanager 1 1 1
Tangara palmarum Palm tanager 1 1 1
Tangara cayana Burnished-buff tanager 1 1
Cissopis leverianus Magpie tanager 1
Dacnis cayana Blue dacnis 1
Cyanerpes caeruleus Purple honeycreeper 1
Volatinia jacarina Blue-black grassquit 1
Sporophila americana Wing-barred seedeater 1 1

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16 ALMEIDA ET AL.
Appendix 2. Continued.
Taxon Name For RF Pla
Sporophila lineola Lined seedeater 1
Sporophila nigricollis Yellow-bellied seedeater 1 1
Sporophila minuta Ruddy-breasted seedeater 1
Sporophila angolensis Chestnut-bellied seed-finch 1 1
Cardinalidae
Granatellus pelzelni Rose-breasted chat 1
Caryothraustes canadensis Yellow-green grosbeak 1
Periporphyrus erythromelas Red-and-black grosbeak 1
Cyanoloxia rothschildii Rothschild’s blue grosbeak 1
Fringillidae
Euphonia chlorotica Purple-throated euphonia 1
Euphonia violacea Violaceous euphonia 1
Euphonia cayennensis Golden-sided euphonia 1