Ecological Indicators 82 (2017) 478–483

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Ecological Indicators
journal homepage: www.elsevier.com/locate/ecolind

Original Articles

Influence of oil palm monoculture on the taxonomic and functional MARK

composition of aquatic insect communities in eastern Brazilian Amazonia
⁎
Ana Luiza-Andradea, , Leandro Schlemmer Brasila, Naraiana Loureiro Benonea, Yulie Shimanoc,
Ana Paula Justino Fariasb, Luciano Fogaça Montaga,b, Sylvain Dolédecd, Leandro Juena,b
a
Programa de Pós-graduação em Zoologia, Instituto de Ciências Biológicas, Universidade Federal do Pará, Rua Augusto Corrêa, N° 1, Bairro Guamá, CEP: 66075-110
Belém, Pará, Brazil
b
Programa de Pós-graduação em Ecologia, Instituto de Ciências Biológicas, Universidade Federal do Pará, Rua Augusto Corrêa, N° 1, Bairro Guamá, CEP: 66075-110
Belém, Pará, Brazil
c
Museu Paraense Emílio Goeldi, Campus de Pesquisa, Av. Perimetral, 1901 – Terra Firme, CEP: 66077-830 Belém, Pará, Brazil
d
CNRS, UMR 5023, LEHNA (Laboratoire d'Ecologie des Hydrosystèmes Naturels et Anthropisés), Biodiversité et Plasticité dans les Hydrosystèmes, Université Claude
Bernard (Lyon I), Villeurbanne, Rhône, France

A R T I C L E I N F O A B S T R A C T

Keywords: Large scale palm oil plantations for the production of vegetable oil are among the most harmful agricultural
Land use activities to biodiversity, especially given their rapid expansion, worldwide. Many cases of species loss have
Freshwater already been recorded in Asian countries, although research is still incipient in the Amazon basin, and the
Ephemeroptera environmental impacts of these monocultures on freshwater ecosystems in the Neotropical region are still poorly
Plecoptera
understood. The present study evaluated the effects of oil palm plantations on the physical structure of stream
Trichoptera
habitats and the resulting changes in the taxonomic and functional composition of aquatic insect communities. A
Functional traits
total of 2100 specimens of the orders Ephemeroptera, Plecoptera and Trichoptera were collected during the
present study, representing 40 genera and 16 families. The hypothesis tested was that the taxonomic and
functional diversity of the orders Ephemeroptera, Plecoptera and Trichoptera (Insecta) decreases in streams
surrounded by oil palm plantations in comparison with those embedded in forested areas. In the plantation
streams, the taxonomic richness and composition, and the functional richness are modified significantly.
Functional composition appeared unaltered despite reduced canopy cover associated with oil palm streams.
These effects emphasize the importance of the riparian vegetation for the protection of the aquatic communities
found in oil palm plantations. The maintenance of the riparian vegetation may mitigate the impacts of plan-
tations, contributing to the conservation of insect communities and associated biodiversity.

1. Introduction
The exotic species Elaeis guineensis Jacq. (common name: oil palm)
has recently become one of the most cultivated equatorial crops (Koh,
2008). Brazil is one of the world’s top producers of oil palm due to the
favorable conditions for this monoculture (e.g., high temperature and
rainfall, low soil pH) in the Amazon rainforest (Muller and Alves, 1997;
Butler, 2011). Yet, oil palm expansion in Amazon may increase the
impact of habitat loss and fragmentation on biodiversity (Butler, 2011;
Foster et al., 2011).
There is compelling evidence of the loss of taxonomic and functional
diversity in the bird and amphibian assemblages associated with oil
palm plantations in eastern Amazonia (Lees et al., 2015; Almeida et al.,
2016; Correa et al., 2015). However, there is little consensus on the
nature of the impact of oil palm plantations on the region’s aquatic
ecosystems. For example, while Cunha et al. (2015), recorded a de-
crease in heteropteran species richness, Shimano and Juen (2016)
found no clear evidence of any change in the species composition of
ephemeropterans. While some studies have addressed the impact of oil
palm on the taxonomic composition of specific groups of organisms,
there has yet to be any systematic analysis of the impact on the func-
tioning of stream ecosystems. Complementary approaches, such as
functional diversity, especially if compared with taxonomic composi-
tion, may reveal distinct community patterns, and provide a better
understanding of the relationship between the impacts of oil palm
plantations and aquatic biodiversity.
The larvae of the orders Ephemeroptera, Plecoptera, and
Trichoptera (EPT) are widely used as ecological indicators due to their

⁎
Corresponding author.
E-mail address: andradeanaluiz@gmail.com (A. Luiza-Andrade).

http://dx.doi.org/10.1016/j.ecolind.2017.07.006
Received 23 November 2016; Received in revised form 9 June 2017; Accepted 3 July 2017
Available online 21 July 2017
1470-160X/ © 2017 Elsevier Ltd. All rights reserved.
A. Luiza-Andrade et al.
sensitivity to environmental changes in aquatic habitats, in particular at
the micro-habitat level (Lake, 2000; Péru and Dolédec, 2010; Luiza-
Andrade et al., 2017). Functional redundancy, which determines the
resilience of a community to environmental variation (Petchey and
Gaston, 2002), may also be altered by the impact of human activities.
Communities with a high degree of functional redundancy, for example,
are potentially more tolerant of variation in the environment (Petchey
and Gaston, 2002).
The present study compares the functional and taxonomic responses
of the Ephemeroptera, Plecoptera, and Trichoptera found in streams
located within forested areas and oil palm plantations in eastern
Amazonia. The study analyzed two complementary questions: (1) do
the species richness and the taxonomic and functional composition of
the EPT vary systematically between forest and plantation streams? (2)
Which specific functional traits are related to the environmental vari-
ables found in both types of stream? The taxonomic and functional
diversity is expected to be reduced in plantation areas in comparison
with the forest, given that the oil palm monocultures tend to reduce
environmental heterogeneity, the number of habitat types, and resource
availability.
2. Material and methods
2.1. Study area and sampling design
The present study was conducted in the Agropalma Agroindustrial
Complex, in the municipalities of Tailândia, Acará and Moju, in
northeastern Pará state, northern Brazil. The study area comprises
107,000 ha, of which 39,000 ha are covered with oil palm plantations
and 64,000 ha with forest reserve (Agropalma, 2015). The predominant
vegetation type of the region is Tropical Rainforest. The area is the
largest forest remnant of the Belém Center of Endemism. The climate
corresponds to Köppen’s Af type (Peel et al., 2007), i.e., tropical humid,
with an average temperature of 26 °C and relative humidity of 85%
(Fig. 1).
Sampling was conducted in second and third order streams of the
basin of the Acará River (Strahler, 1957), only in dry season, in
Fig. 1. Distribution of sites in 21 streams distributed in oil palm plantations (circles) and forest fragments (triangles), that were sampled in 2012 and 2013 in Acará, Moju and Tailândia,
Pará, northern Brazil.
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Ecological Indicators 82 (2017) 478–483
November and December 2012, and July and August 2013. The re-
striction of sampling to the dry season was due to the fact that benthic
macroinvertebrates are more abundant during this period (Bispo et al.,
2001; Diniz-Filho et al., 1998), and that samples are thus more re-
presentative of the community structure (Brasil et al., 2016). A total of
21 streams were sampled, eight in native forest and 13 in oil palm
plantation (Fig. 1). One 150 m transect was established in each stream,
and was divided into 10 15 m stretches, each subdivided into three 5 m
segments. The first two segments of each stretch were sampled, while
the third segment was used to gain access to the subsequent stretch. A
total of 20 samples were thus collected in each stream.
Based on the recommendations of Shimano and Juen (2016), the
study focused on the larvae of the orders Ephemeroptera, Plecoptera,
and Trichoptera. The specimens collected were fixed and stored in 85%
ethanol, and identified to the genus level using the identification keys
of Lecci and Froehlich (2007), Pes et al. (2014), and Domínguez et al.
(2006), consultations with experts, and comparisons with material de-
posited in the Zoological Collection of the Federal University of Pará.
2.2. Environmental variables
Environmental variables were measured in each of the 10 stretches
of stream, following Peck et al. (2006). This protocol evaluates various
components of the physical structure of the stream, such as the channel
morphology, substrate flow type, quantity of woody debris in the
stream, the structure of the riparian vegetation, the availability of
shelter for the aquatic biota, and human pressures. Physical and che-
mical variables of the water were also measured, that is, the tempera-
ture (°C), turbidity (NTU), dissolved oxygen (mg/L), conductivity (μS/
cm), total dissolved solids (mg/L), and pH at the beginning, middle, and
end of each 150 m transect using a Horiba® multi-parameter probe.
Following Cunha et al. (2015) and Juen et al. (2016), variables with a
Pearson correlation of | > 0.7| were excluded from the analyses to
avoid problems associated with the collinearity of variables (Table 2).
A. Luiza-Andrade et al.
2.3. Functional traits
For the analysis of functional traits, five multi-choice traits related
to the behavior, ecology, and morphology of the insects (respiration,
feeding habits, locomotion, and body size and shape) were selected,
following Poff et al. (2006). The functional traits were quantified based
on the descriptions of South American taxa found in the scientific
(Table S1, Supplementary data). These traits were processed using the
fuzzy coding approach (Chevenet et al., 1994) to determine the affinity
of each species to the trait categories. These affinities were assigned a
score ranging from 0 to 3, where the higher the value, the greater the
affinity of the species to the category.
2.4. Data analysis
Student’s t was used to test for differences in the abundance of in-
dividuals, the genus richness and functional richness between oil palm
and forest streams (Zar, 2010) after first verifying the assumption of the
normality and homogeneity of variance. A Permutation Multivariate
Analysis of Variance (PERMANOVA) was run to test for differences in
the taxonomic and functional composition of the forest and plantation
streams (factor with two levels). The significance was obtained using
the Monte Carlo randomization with 9999 permutations (Anderson and
Walsh, 2013). The PERMDISP (Anderson, 2005) was used to test for the
homogeneity of variances between the factor levels. A Principal Co-
ordinates Analysis (PCoA) was used to visualize the results in a biplot,
based on a distance matrix of the Bray-Curtis (for the taxonomic data)
and Gower (for the functional data) similarity indices (Pavoine et al.,
2009). Functional richness was calculated using the Fric index (Villéger
et al., 2008).
A combination of RLQ (Dolédec et al., 1996) and Fourth-corner
analysis (Legendre et al., 1997), as proposed by Dray et al. (2014), was
used to test which environmental variables influenced the functional
traits of the communities. This approach produces a matrix that de-
scribes the association between traits and environmental variables,
known as a fourth-corner matrix, which summarizes the combined
structure of the three preceding matrices (Legendre et al., 1997). All
analyses were run in the R software, version 3.0.2 (R Development Core
Team, 2016), and the associated packages ade4 (Dray and Dufour,
2007) and vegan (Oksanen et al., 2016).
3. Results
3.1. Effects of the physical habitat on aquatic assemblages
The environmental characteristics of the forest and plantation
streams are summarized in Table 2. Plantation streams were char-
acterized by higher water temperatures (Temp), pH, and the quantity of
roots (PCT_RZ) and fine sediment (PCT_ST), while the forest streams
had larger amounts of woody debris in the channel (NWD), greater
mean riparian canopy cover (XC), and a higher width/depth ratio
(XWD_RAT; Fig. 2b). The taxonomic composition of the EPT was in-
fluenced by environmental variables (RLQ model 2, p = 0.028), while
the functional traits composition were not (RLQ model 4, p = 0.846).
3.2. Taxonomic and functional richness and composition
A total of 2100 specimens of the orders Ephemeroptera, Plecoptera
and Trichoptera were collected during the present study, representing
40 genera and 16 families (Table 1). Just over half (1083) of these
specimens (representing 31 genera) were collected in streams located
within oil palm plantations. The mean number of genera recorded per
stream was significantly higher (t = 3.286, DF = 19, p = 0.003) in
forest streams (15.375 ± 4.657) in comparison with plantation
streams (9.307 ± 3.75), although abundance did not vary system-
atically between habitats (t = 1.787, DF = 19, p = 0.089).
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Ecological Indicators 82 (2017) 478–483
Ephemeropterans were predominant in the plantation streams, pro-
viding 55% of recorded specimens, whereas Plecoptera and Trichoptera
were more abundant in forest streams, which provided 77% and 54% of
the specimens collected, respectively.
A significant difference was found in the taxonomic composition of
the EPT between plantation and forest streams (PERMANOVA: pseudo-
F = 2.426, DF = 19; p = 0.035). The results of PERMDISP analysis
showed that there was no significant difference (F = 4.043; DF = 19,
p = 0.053) in the variance of the species composition between plan-
tation (0.501 ± 0.072) and forest streams (0.408 ± 0.117). Nine
genera were exclusive to the forest streams (Amazonatolica, Aturbina,
Enderleina, Polyplectropus, Thraulodes, Traveryphes, Tricorythodes,
Tricorythopsis, and Zelusia) whereas only one genus (Cryptonympha) was
unique to the plantation streams (Table 1).
Functional richness was significantly higher (t = 2.155, DF = 19;
p = 0.044) in forest streams (57.559 ± 35.865) than in plantation
streams (29.541 ± 23.965). However, no significant difference was
found in the functional composition between the plantation and forest
streams (PERMANOVA: pseudo-F = 0.219, DF = 73; p = 0.922), and
the variances were homogeneous among treatments (PERMDISP:
F = 3.346; p = 0.880).
4. Discussion
Like most other crops, oil palm plantations impact biodiversity,
although the exact effects depend on how the culture is managed
(Fitzherbert et al., 2008). The cultivated area of oil palm in Brazil is
expected to continue increasing in the near future (Borges et al., 2016)
in response to the growing demand for palm oil. The results of the
present study indicate clearly that taxonomic and functional richness,
as well as the species composition of the ephemeropteran, plecopteran,
and trichopteran larvae were all affected by oil palm plantation, which
makes the ongoing expansion of plantations a major concern. In this
scenario, active conservation measures may be increasingly necessary
to guarantee the diversity of these groups in streams associated with oil
palm plantations.
The taxonomic and functional richness were lower in plantation
streams in comparison with forest streams. Reduced has been recorded
in communities of beetles, bats, lizards, fish (Giam et al., 2015), and
aquatic insects (Rawi et al., 2013) associated with oil palm plantations
in Asia (Foster et al., 2011). Wang and Foster (2015) also found dif-
ferences in ant species richness in oil palm plantations of different ages,
with mature plantations having the lowest richness. In the Neotropics,
similar effects have been recorded for birds (Lees et al., 2015) and
heteropterans (Cunha et al., 2015) in eastern Amazonia. The latter
study also found that the loss of heteropteran diversity was linked to the
loss of environmental integrity.
Fitzherbert et al. (2008) concluded that changes in species compo-
sition may be related to the increase in the more generalist taxa in oil
palm plantations, given that these areas tend to have less canopy cover,
even when the riparian vegetation is preserved. In the present study,
the riparian vegetation of the streams located within the oil palm
plantations was approximately 30 m wide, which is in accordance with
the Brazilian Forestry Code. However, a strip of vegetation this sie is
probably insufficient to guarantee the persistence of species in the en-
vironment. Riparian vegetation minimizes negative impacts on bodies
of water, and is a source of allochthonous organic matter, shelter,
oviposition sites, and habitat for juvenile insects (Valle et al., 2013;
Soininen et al., 2015). In a previous study, Rodrigues et al. (2016)
showed that a buffer zone of 250 m, containing 60% native vegetation,
around streams was required to ensure the retention of dragonfly
community structure. This is almost an order of magnitude larger than
required by the Brazilian legislation.
Despite the significant decrease in functional and taxonomic rich-
ness, and the changes in species composition observed in the plantation
streams in the present study, the results indicated that the functional
A. Luiza-Andrade et al. Ecological Indicators 82 (2017) 478–483

Fig. 2. a) Distribution of 40 EPT genera per stream. acronyms for species available in Table 1. b) Environmental characteristics of the streams in plantation and forest habitats, acronyms
for environmental variables are listed in Table 2.

composition of the EPT communities was not affected significantly by communities. This functional redundancy would ensure the resilience
the oil palm plantations. This indicates a high degree of functional re- of stream function in the face of the loss of species (Petchey and Gaston
dundancy in the study communities, reflecting the occupation of similar 2002; Bihn et al., 2010), given that the persisting species are able to
ecosystem functions by species with similar traits in the different play the ecological role of the extirpated ones. By contrast, previous

Table 1
Abundance of EPT collected in eight forest streams and 13 plantation (oil palm) streams.

Order Family Genus Abr. Abundance

F P

Ephemeroptera Baetidae Americabaetis Kluge, 1992 Amer 1 1

Aturbina Lugo-Ortiz and McCafferty, 1996 Atur 3 0
Cloeodes Traver, 1938 Cloe 6 3
Cryptonympha Lugo-Ortiz and McCafferty, 1998 Cryp 0 2
Waltzoyphius McCafferty and Lugo-Ortiz, 1995 Walt 1 1
Zelusia Lugo-Ortiz and McCafferty, 1998 Zel 7 0
Caenidae Brasilocaenis Puthz, 1975 Bra 1 3
Coryphoridae Coryphorus Peters, 1981 Cor 1 1
Euthyplociidae Campylocia Needham and Murphy, 1924 Cpl 165 311
Leptohyphidae Amanahyphes Salles and Molineri, 2006 Amn 1 3
Traveryphes Molineri, 2001 Trav 1 0
Tricorythodes Ulmer, 1920 Tric 2 0
Tricorythopsis Traver, 1958 Trip 5 0
Leptophlebiidae Askola Peters, 1969 Ask 1 1
Farrodes Peters, 1971 Far 2 5
Hagenulopsis Ulmer, 1920 Hag 1 3
Microphlebia Savage and Peters, 1983 Mph 1 2
Miroculis Edmunds, 1963 Mir 333 268
Simothraulopsis Demoulin, 1966 Simo 2 3
Thraulodes Ulmer, 1920 Thra 1 0
Ulmeritoides Traver, 1959 Ulm 3 90
Polymitarcyidae Campsuru sEaton, 1868 Cps 12 12
Plecoptera Perlidae Anacroneuria Klapálek, 1909 Anc 33 23
Enderleina Jewett, 1960 End 2 0
Macrogynoplax Enderlein, 1909 Mgx 44 16
Trichoptera Calamoceratidae Phylloicus Müller 1880 Phy 55 45
Glossosomatidae Mortoniella Ulmer, 1906 Mor 10 1
Helicopsychidae Helicopsyche Siebold 1856 Hel 32 16
Hydropsychidae Leptonema Guérin 1843 Lept 20 12
Macronema Pictet 1836 Mne 72 75
Macrostemum Kolenati 1859 Macr 20 27
Smicridea McLachlan 1871 Smc 7 23
Leptoceridae Amazonatolica Holzenthal and Pes, 2008 Amz 1 0
Nectopsyche Müller 1879 Nec 13 4
Oecetis McLachlan 1877 Oec 20 6
Triplectides Kolenati 1859 Tps 85 97
Odontoceridae Marilia Müller 1880 Mar 18 4
Philopotamidae Chimarra Stephens 1829 Chi 19 2
Polycentropodidae Cernotina Ross 1938 Cer 13 23
Polyplectropus Curtis 1835 Pol 3 0
TOTAL 1017 1083

Abr. = taxon abbreviation; F = forest streams; P = plantation streams.

481
A. Luiza-Andrade et al.
Table 2
Mean and standard deviation of the environmental variables measured in the eight forest
streams and 13 plantation (oil palm) streams analyzed in the present study.
Variable Code Forest Oil palm
Width/depth ratio XWD_RAT 13.09 ± 6.59 9.055 ± 2.29
Amount of wood debris NWD 5.75 ± 3.34 3.28 ± 2.54
(diameter > 30 cm,
length > 5 m) in and over
the stream channel.
Fine sediment (%) PCT_ST 6.49 ± 3.73 15.89 ± 8.68
Mean riparian canopy cover XC 82.13 ± 28.63 77.29 ± 14.28
Water temperature Temp 25.42 ± 0.96 26.11 ± 0.58
pH pH 4.71 ± 0.25 5 ± 0.20
studies have found a reduction in the number of feeding modes of ants
in oil palm plantations in Malaysia (Luke et al., 2014), and of birds in
both Southeast Asia (Edwards et al., 2013) and eastern Amazonia
(Almeida et al., 2016). However, Giam et al. (2015) found no alteration
in the diversity of Neotropical fish, due to the minimization of pesticide
runoff by the preserved riparian vegetation.
The effects of oil palm plantations on the EPT community were
related to changes in water temperature and pH, and the amount of
organic debris and vegetation cover of the streams. The increase in
water temperature under more open canopies favors the occurrence of
genera that are more resistant to environmental change (Shimano and
Juen, 2016). These authors found that Ulmeritoides and Campylocia
(Ephemeroptera) were relatively common in plantation streams with
sandy substrates, and high pH and temperature. High water tempera-
tures and pH also favor the proliferation of microbes, providing the
ephemeropteran larvae with more resources (Boyero et al., 2012).
Generally, the distribution of aquatic insects (especially those of the
EPT) in the Amazon is associated with streams with riparian vegetation
(Hamada et al., 2014).
The maintenance of the riparian forest associated with the steams
found within oil palm plantations favors the accumulation of organic
(woody) debris and the maintenance of the environmental conditions
necessary for a diverse aquatic biota, given that the presence of wood
debris increases the complexity of stream flow patterns. By contrast, a
reduced quantity of debris limits the availability of habitats and refuges
for aquatic organisms, increasing their vulnerability to predators
(Faustini and Jones, 2003). Despite the similarity in the functional di-
versity between forest and plantation streams, the oil palm affected
taxonomic and functional richness, as well as species composition.
These findings emphasize the need for the conservation of riparian
forests to guarantee the ecosystem functions provided by resident spe-
cies, as well as the control of water quality. Future studies should in-
vestigate in more detail how oil palm plantations affect the aquatic
biota over a broad spatial scale, given that the functional response of
the community is probably most affected by the intensity and duration
of the impact. Similarly, the effects of plantations of other types of crop
should also be investigated, for the comparative analysis of the effects
of changes in land use on the functional diversity of aquatic insects and
ecosystem services. In that respect, the responses of EPT communities
may provide a key criterion for the conservation planning and man-
agement of oil palm plantations in the Amazon region.
Acknowledgements
We would like to thank Conservation International (CI) and the
Agropalma Group for their financial and logistic support. We are also
grateful to the Brazilian National Council for Scientific and
Technological Development (CNPq) for granting research productivity
fellowships to LFAM (301343/2012-8) and LJ (307597/2016-4), as
well as master’s and PhD’s stipends to ALA (1401991/2016-0), LSB
(140111/2015-8), and NLB (161350/2013-5), and to the Coordination
482
Ecological Indicators 82 (2017) 478–483
for the Improvement of Higher Education Personnel (CAPES) for
granting a PhD stipend to APJF (23038.016839). This manuscript was
funded by the projects “Influência dos diferentes tipos de uso do solo
sobre a biodiversidade na Amazônia Oriental” (CNPq no. 449314/
2014-2), “Zoneamento bioenergético do plantio de palma e os impactos
a biodiversidade no Estado do Pará” (FAPESPA/CNPq) and
“Biodiversity and Socio-Economic Impacts of Oil Palm Bioenergy
Development in the Brazilian Amazon” (USAID/PEER). We are grateful
to Lenize Batista Calvão, Fernando Geraldo Carvalho, Erlane Rodrigues
Cunha, Bruno Prudente, Tiago Begot, and Márcio Cunha Ferreira for
their assistance during field trips.
Appendix A. Supplementary data
Supplementary data associated with this article can be found, in the
online version, at http://dx.doi.org/10.1016/j.ecolind.2017.07.006.
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