Turkish Journal of Zoology Turk J Zool

(2018) 42: 557-566

http://journals.tubitak.gov.tr/zoology/
© TÜBİTAK
Research Article doi:10.3906/zoo-1801-48

Temporal variability of the macroinvertebrate community associated with

Eichhornia azurea (Swarts) Kunth (Pontederiaceae) in a lake marginal to a tropical river
Natalia Kaori ARAKI, Carolina Vieira da SILVA*, Raoul HENRY
Department of Zoology, Institute of Biosciences, São Paulo State University (UNESP), Botucatu, Brazil

Received: 30.01.2018 Accepted/Published Online: 06.07.2018 Final Version: 17.09.2018

Abstract: Aquatic macroinvertebrates have a close relationship with associated floating macrophytes, especially with the roots. The plant
root mass is an environment favorable to the development of the macroinvertebrate fauna, supplying both food resources and refuge
against predators. The present study aimed to analyze the structure of the macroinvertebrate community associated with the roots of
Eichhornia azurea (Sw.) Kunth (Pontederiaceae) in a lake marginal to a tropical river. Sampling was performed quarterly in three stands
of E. azurea. One plant specimen was selected from each stand and five root mass samples were collected. The study was carried out in an
extremely rainy year, with high rainfall in July, when the river level increased quickly, causing an extreme inundation and an increase in
the root biomass of E. azurea. A higher abundance of macroinvertebrates was found in April, around four to five times the total density
of the other periods. Taxa richness presented no significant temporal differences. Oligochaeta and Chironomidae were the predominant
group of invertebrates in all periods. The extraordinary flood in June–July caused a modification in the macroinvertebrate fauna (an
increase in the abundance and a reduction in the taxon richness), and was apparently a controlling factor for the community structure.

Key words: Eichhornia azurea, extraordinary flood, macrophyte, phytofauna, root biomass.

1. Introduction (due to presence of allelochemical components), are factors

Macrophytes present different physiognomic types and
variable morphological and structural complexity. Aquatic
plants from the littoral zone provide a site for colonization
for a rich and abundant macroinvertebrate community
(Takeda et al., 2003; Taniguchi et al., 2003; Poi de Neiff and
Neiff, 2006; Cremona et al., 2008; Silva et al., 2009). The
presence of aquatic plants may also contribute to increased
macroinvertebrate diversity in lentic environment
sediment (Shimabukuro and Henry, 2011).
The high macroinvertebrate fauna abundance
associated with aquatic floating macrophytes can be
attributed to the presence of the dense root mass of plants
that makes up colonization sites for different organisms.
Root macrophytes supply microhabitats (for refuge against
predators and for posture, for example) and resources
(such as food) to the fauna (Takeda et al., 2003; Peiró and
Alves, 2004; Tessier et al., 2004, 2008; Cronin et al., 2006;
Padial et al., 2009).
Macrophyte richness, shaped by species with distinct
morphological architecture, biological types, and substrate
texture and associated periphyton, differs in community
composition. Characteristics of adhered detritus and
particulate matter, as well as macrophyte toxicity levels
* Correspondence: cvscarol@hotmail.com
which directly and indirectly influence macroinvertebrate
community structure (Stripari and Henry, 2002; Poi de
Neiff, 2003; Takeda et al., 2003; Tessier et al., 2004, 2008;
Poi de Neiff and Neiff, 2006; Cremona et al., 2008).
The presence and diversity of invertebrates have
great functional importance in aquatic ecosystems.
These organisms are part of the trophic web, as primary
and secondary consumers of the detritus food chain,
decomposing allochthonous and autochthonous organic
matter, and are important components of nutrient
recycling (Hargeby, 1990; Bouchard, 2004).
Among aquatic macrophytes, Eichhornia azurea
(Sw.) Kunth (Pontederiaceae) is one of the most widely
distributed floating plants in the Neotropical region
(Santos, 1999; Moretti et al., 2003; Padial et al., 2009).
Commonly known as “aguapé” or “camalote” in Brazil,
this species presents dimorphic leaves according to its life
stage; that is, when juvenile, the leaves are straight and
submerged, and when adult, they are emerged and round
(Souza and Lorenzi, 2008), with an invaginating sheath
covering the rhizome. When adult, the long rhizomes are
submersed and develop quickly, forming great floating
stands in lake, lagoon, and reservoir littoral zones (Moretti
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This work is licensed under a Creative Commons Attribution 4.0 International License.
 ARAKI et al. / Turk J Zool
et al., 2003; Souza and Lorenzi, 2008). The flowers are
zygomorphous with a violet color, and appear from
March to May (Santos, 1999; Thomaz and Santos, 2000),
organized as inflorescences in ears (Martello et al., 2008).
When adult, E. azurea can be divided into a sediment-
fixed/rooted part (basal zone) and a floating part (apical
zone) (Melo et al., 2004). Their roots are adventitious, hair-
type, made up of various fine ramifications that develop into
the nodes of each rhizome (Saulino and Trivinho-Strixino,
2014), in different lengths and biomasses according to the
plant development stage (Padial et al., 2009). Variability
of E. azurea stand biomass depends on environmental
conditions, such as depth, turbidity, nutrient contents,
temperature, and water level (Camargo and Esteves, 1996;
Thomaz and Santos, 2000; Milne et al., 2006).
E. azurea was selected as a study model in the present
investigation because of its perennial life cycle and the
morphological aspects of some structures (submerged
roots, rhizomes, and some leaves). The submerged plant
parts make up a large area of the colonization substrate
and different microhabitats for the associated communities
(Poi de Neiff, 2003; Takeda et al., 2003; Henry and Costa,
2003). When compared to other macrophytes, E. azurea
presents a great diversity of associated macroinvertebrates
due to its peculiar morphological structure (Trivinho-
Strixino et al., 2000; Moretti et al., 2003; Martello et al.,
2008). Additionally, the leaf senescence favors the presence
of shredder species (Mormul et al., 2006; Martins et al.,
2012), and the extensive storage of organic detritus on the
roots favors collectors (Trivinho-Strixino et al., 2000).
The aim of this study was to analyze variations in
the biomass of E. azurea’s sampled adventitious roots
and the taxa richness and abundance of the associated
macroinvertebrate community in a lake connected to
a tropical river. Considering that adventitious roots of
E. azurea can present variations in biomass among the
months of the year, we expected a temporal difference in
the structure of macroinvertebrate communities.
2. Materials and methods
2.1. Study area
Three E. azurea stands were sampled in Barbosa Lake,
marginal to the Paranapanema River, located in the zone
of confluence with the Jurumirim Reservoir, São Paulo,
Brazil (Figure 1). The river–reservoir transition zone is a
wetland, formed by permanently connected lakes and by
some isolated from the river. This zone can be classified as
an artificial wetland (Junk et al., 2014). The marginal lakes
fluctuate in volume and depth due to lateral water inflow
dependent on the level variation of the Paranapanema
River and the operational management of the Jurumirim
Reservoir (Henry, 2005; Silva and Henry, 2013).
558
Data on water levels were supplied by the Duke Energy
Generation Paranapanema Company, and the precipitation
values were provided by the Water and Electric Energy
Department’s (Departamento de Água e Energia Elétrica,
DAEE) pluviometric station located approximately 25 km
from Barbosa Lake at Angatuba, São Paulo State, Brazil.
According to the Köppen Climate Classification System,
the region has a tropical climate typical of the altitude
(Setzer, 1966), with rainy summers and dry winters.
2.2. Sampling
Usually, the presence and abundance of macroinvertebrates
associated with E. azurea are examined in the apical part of
the macrophyte in the littoral zone–limnetic zone interface
(Silva and Henry, 2013). Nevertheless, the long rhizomes
with adventitious roots increase in volume and length
in the basal direction of the plant; therefore, limiting
the numeric evaluation of macroinvertebrates solely to
the apical part of the plant can mean subestimations of
richness and abundance.
Macroinvertebrate sampling was performed in April,
July, and October 2013, as well as in January 2014, in one
individual plant each of three distinct E. azurea stands
(Figure 1). From each plant stand, five samples of roots of
the individual were collected in a sequence of increasing
masses (2nd, 5th, 8th, 11th, and 14th root masses) from
the apical (located at the transition of limnetic–littoral
zones) to basal parts of the macrophyte, to ensure a better
representation of the biomass of all of the macrophyte
roots system (Figure 2), based on Melo et al.’s (2004)
sampling methodology. The samples were transferred to
plastic bags and immediately fixed with 4% formaldehyde.
The material was then washed on a 250-µm net screen,
and the organisms were stored in plastic vessels containing
70% alcohol.
2.3. Analysis of the associated macroinvertebrate
community
The organisms were identified at the phylum, class, and
order levels, and at family level for Insecta (except for
Diptera and Trichoptera pupae). For the identification, we
used the Dominguez and Fernandez (2009) and Mugnai et
al. (2010) keys.
Density was expressed as the number of individuals g–1
of dry weight of root mass of each sequentially collected
macrophyte sample. Relative taxon abundance was also
computed for each sample, including juvenile and pupal
stage macroinvertebrates.
2.4. Statistical analysis
Kruskall–Wallis nonparametric variance analysis was
performed to detect differences between sampling
periods in relation to macroinvertebrate community,
taxon richness, and total density, followed by multiple
comparison analysis of means between the periods. All the
community data were log (x + 1) transformed.
 ARAKI et al. / Turk J Zool

Figure 1. Study site and sampling stations (P1, P2, and P2) in Barbosa Lake (the circle shows the connection site between the
lake and the river).

Figure 2. Scheme of an adult E. azurea individual showing the sampled root mass in sequential direction from the apical to
the basal parts of the plant.

Nonmetric multidimensional scaling (NMDS) was
performed to assess the structure (density data) and
composition (presence/absence data) similarity of the
associated fauna between sampling periods (Clarke and
Gorley, 2006). The Bray–Curtis dissimilarity coefficient
was used for the computation of the similarity matrix.
Similarity analysis (ANOSIM) was also carried out, and the
similarity percentages (SIMPER) were computed (Clarke,
1993). SIMPER presents the contribution percentage of
each taxon for the similarity between sampling periods.
All the density values were square-root–transformed
(Clarke and Warwick, 2001).
Linear regression between root biomass and
macroinvertebrate density and between root biomass
and macroinvertebrate richness was also computed using
Sigma Plot v.11.0 software (Systat Software, Inc., 2008).
The Kruskal–Wallis analysis and multiple comparison
analysis between means were performed using Statistica
7.0 software (StatSoft, Inc., 2004), while PCA, NMDS,
ANOSIM, and SIMPER were performed using Primer6
software.
For the statistical analysis, juvenile and pupal-
stage macroinvertebrate data, as well as data for
microcrustaceans recorded in the samples, were not

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 ARAKI et al. / Turk J Zool
included in the community values of richness, density, and
composition.
3. Results
Precipitation had an atypical pattern during the study
period (2013), as the comparative analysis of the mean
accumulated monthly values of the last 16 years shows
(Figure 3a). According to the historical series, no dry
period occurred in 2013; only one month had very
low precipitation (August, 3.7 mm), and the highest
precipitation value was observed in June (175.5 mm),
during the dry season (Figure 3b).
Water level varied from 563.11 m (February) to
567.38 m (August) during the study period (February
2013 to January 2014), and the annual range was 4.27 m
(Figure 3c). Potamophase was the only pattern recorded
on Barbosa Lake during the entire study, since the water
level was always higher than 563.60 m, the threshold
level between the lacustrine environment connection and
isolation of the Paranapanema River (Henry 2005).
Figure 3. Means and standard deviations of monthly cumulated precipitation values (mm) recorded from 1996 to 2012 (A);
monthly accumulated precipitation (mm) (B) and daily water level values (m) (C) recorded in the study site between February
2013 and January 2014.
560
3.1. E. azurea adventitious root biomass and
macroinvertebrate community
In general, the biomass mean values of each root mass
varied according to the sampling period. The highest
values were recorded in April and July (0.59 g.DW–1 and
0.73 g.DW–1, respectively), and the lowest values in January
(0.083 g.DW–1, Figure 4).
Thirty-eight taxa were recorded during the study, and
richness ranged from 24 (July) to 34 (April). From the
seven taxa classified as rare, three were recorded only in
April and two only in October.
Several taxa were observed in all macrophyte stands
and periods, as for example Platyhelminthes, Nematoda,
Oligochaeta, Ostracoda, Conchostraca, Hydrachnida,
Caenidae, Chironomidae, Polycentropodidae, and
Hydroptilidae. Some taxa, such as Gomphidae,
Leptophlebiidae, Dytiscidae, Noteridae, Belostomatidae,
Mesoveliidae, and Veliidae, were rare, occurring only in
one of the studied periods.
In relation to the relative contribution (%) of each
taxon to the community total abundance (expressed in
 ARAKI et al. / Turk J Zool
Figure 4. Means and standard deviations of root biomass of E.
azurea (g.DW–1) in Barbosa Lake during the study period.
ind.gDW–1), Oligochaeta presented the highest abundance,
followed by Chironomidae (Figure 5).
The total density of macroinvertebrates recorded in
each sampling period presented a significant difference (P
< 0.05) according to the Kruskal–Wallis analysis. However,
the community richness did not differ significantly
between months (Figure 6).
Structural and compositional NMDS and ANOSIM
of the macroinvertebrate community showed significant
differences among samples and study periods (Figure 7).
SIMPER analysis showed that Oligochaeta was the
most representative taxon in all months, contributing to
a similarity from 28.72% (October) to 36.76% (January)
of total abundance of the community. Chironomidae
was the taxon with the second highest contribution to
similarity in all periods (from 24.81% in April to 29.92%
in July). According to the SIMPER analysis, the greatest
dissimilarity in macroinvertebrates was recorded between
April and January (50.45), and the smallest between July
and October (36.03).
Linear regressions between root biomass and total
density and macroinvertebrate richness showed a trend
towards a reduction in the density with an increase in
root biomass of E. azurea (R2 = 0.34), and an increase in
richness with an increase in root biomass (R2 = 0.18).
4. Discussion
Usually, shallow lakes marginal to a river such as Barbosa
Lake are subject to the influence of the alteration on water
level. The study area is a wetland located in the confluence
zone of Paranapanema River with Jurumirim Reservoir
and thus is also subject to the operational management
of the dam. Water accumulates in the reservoir, and
its management affects the upstream water level of
Paranapanema River and the connected marginal lakes,
acting as a buffer and weakening the inundation pulse
effect (Henry, 2005; Granado and Henry, 2008). The level
variation is a controlling factor for the water’s physical
and chemical characteristics and can also affect the biota
of lakes marginal to Paranapanema River, near the mouth
zone into Jurumirim Reservoir (Granado and Henry,
2008).
The extraordinary flood recorded in June and July
resulted in a significant increase in the mean depth of
Barbosa Lake due to the overflowing of Paranapanema
River (a quick rise in water level in 30 days). In July, during
the extraordinary flood period, a low number of taxa and
a significant reduction in community total density were
recorded. Regarding an environmentally similar situation,
Silva and Henry (2013) commented that in August 2009, a
typical dry season month, as the historical series showed,
an atypically high water level occurred that resulted
in a reduction in the macroinvertebrate total density
associated with E. azurea in Barbosa Lake. However,
the authors showed that richness increased probably
due to an increase in the environmental heterogeneity
resulting from alterations in the lake water’s physical
and chemical characteristics. Fulan and Henry (2006)
recorded similar results—an increase in richness and a
decrease in density—when they examined the structure of
the Odonata community after an extreme inundation in
the same area. Similar results were presented by Stenert et
al. (2003), who showed an increase in macroinvertebrate
richness and density after a disturbance period (i.e., a
flood). The results of the present study are similar to those
reported by Stenert et al. (2003) and Fulan and Henry
(2006), since there was a rise in richness in October after
the extraordinary flood. This rise probably occurred due
to the increased availability of microhabitats and resources
for the community during the macrophyte senescence
process, as well as due to the introduction of different taxa
derived from the river and adjacent areas in Barbosa Lake
(Silva and Henry, 2013). Conversely, the diminution in
total organism density in October may have been related
to stress caused by the flood (Benke et al., 2000; Stenert et
al., 2003).
Therefore, we can infer that richness increase can be
related to an increase in environmental heterogeneity
resulting from the detritus produced during the aquatic
plant degradation process (Silva and Henry, 2013). In
relation to the density, another situation was observed.
Although environmental factors can, in some cases,
be a trigger for the macroinvertebrate reproductive
process (involving emergency, copulation, and posture,
depending on the biology of each taxon), community
abundance is probably related to taxon colonization stage,
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Bivalvia Libellulidae Crambidae

Platyhelminthes Ostracoda Caenidae Ceratopogonidae
Nematoda Conchostraca Baetidae Chironomidae
Oligochaeta Hydracarina Polymitarcyidae Polycentropodidae
Hirudinea Dicteriadidae Pleidae Hydroptilidae
Gastropoda Coenagrionidae Corixidae Leptoceridae
Bivalvia Libellulidae Crambidae Others
Ostracoda Caenidae Ceratopogonidae
Conchostraca Baetidae Chironomidae
Hydracarina Polymitarcyidae Polycentropodidae
Dicteriadidae Pleidae Hydroptilidae
April
Coenagrionidae Corixidae Leptoceridae 12,772 ind.gDW -1
Libellulidae Crambidae Outros
Caenidae Ceratopogonidae
Baetidae Chironomidae
July
Polymitarcyidae Polycentropodidae 3,467 ind.gDW -1
Pleidae Hydroptilidae
Corixidae Leptoceridae
Crambidae Outros
Ceratopogonidae
October 2,387 ind.gDW -1
Chironomidae
Polycentropodidae
Hydroptilidae
Leptoceridae
January
Outros 2,867 ind.gDW -1

0 20 40 60 80 100
Relative abundance (%)

Figure 5. Relative contribution (%) of taxa to the total density (expressed in ind.gDW–1) of the macroinvertebrate
community associated with E. azurea in Barbosa Lake during the study period. The group “Others” corresponds to
Gomphidae, Leptophlebiidae, Dytiscidae, Noteridae, Belostomatidae, Mesoveliidae, and Veliidae.

Figure 6. Box-plots of macroinvertebrates community richness

(expressed in log values).

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 ARAKI et al. / Turk J Zool

Figure 7. NMDS diagram of macroinvertebrates in the sampled periods. (A)

NMDS: structure; (B) NMDS: composition.

resistance, and resilience (Stenert et al., 2003). When an
extraordinary flood occurred, the community structure
was modified; the intrinsic characteristics determined
the time necessary to attain a new dynamic equilibrium
(Odum and Barrett, 2007). The ecological attributes of
the “new” macroinvertebrate community may be different
from those observed before the disturbance due to
organisms’ resistance (Stenert et al., 2003). The present
study showed that the variation in community attributes
during the year was affected by the extraordinary flood, a
natural event that caused a modification in the structure
of the macroinvertebrate community associated with E.
azurea.
The extraordinary increase in the water level resulted in
the submersion of E. azurea stands in July, which accelerated
the macrophyte decomposition process. After this event,
the macroinvertebrate richness and total density increased
slowly in October and January. Stripari and Henry (2002)
observed that E. azurea decomposes faster in rainy periods
than in dry periods. This is probably because the dead
leaf biomass is positively correlated to the hydrometric
level (Thomaz and Santos, 2000). Silva and Henry (2013)
recorded a similar environmental situation (an atypical
flood) in August 2009, when E. azurea was in the senescent
stage. According to Silva and Henry (2013), microhabitat
availability increased during plant decomposition due to
the appearance of detritus of different sizes, which may
have resulted in a richness rise in October.
Conversely, a reduction in the total density of
macroinvertebrates, approximately 30% between July
and October, may have been related to a high demand
for oxygen in the lake. Degradation of allochthonous
material, especially macrophytes, including E. azurea,
demands a high consumption of oxygen in lake water

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during extraordinary flooding (Shimabukuro and Henry,
2011). According to Hepp (2002), oxygen concentrations
below 4 mg.L–1 can limit the presence of some taxa in
the community because of the intolerance of various
invertebrates to low concentrations of oxygen dissolved
in water; however, in our study, the oxygen presented a
concentration lower than this value only in October.
In relation to the E. azurea root biomass annual
variation, both Camargo and Esteves (1996) and Thomaz
and Santos (2000) concluded that water level and
temperature affect biomass. The former reported higher
root biomass in September (a low water temperature,
hydrologic level, and electric conductivity period) and
lower values in January (a high water temperature,
hydrologic level, and electric conductivity period). The
latter showed that biomass presented a negative correlation
with temperature. Our data showed a weak relationship
between floating macrophyte root biomass and water level.
The relationship between biomass and macroinvertebrate
total density in the present study diverged from the
literature (Poi de Neiff and Neiff, 2006; Fulan and Henry,
2007), since an increase in fauna abundance was negatively
related to root biomass. Root biomass increases from
apical to basal parts on the rhizome of E. azurea; near the
fixation site of plant on sediment, the high oxygen demand
for degradation of organic matter could negatively affect
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