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http://journals.tubitak.gov.tr/zoology/

Turkish Journal of Zoology Turk J Zool(2018) 42: 557-566© TÜBİTAKdoi:10.3906/zoo-1801-48

Temporal variability of the macroinvertebrate community associated withEichhornia azurea (Swarts) Kunth (Pontederiaceae) in a lake marginal to a tropical river

Natalia Kaori ARAKI, Carolina Vieira da SILVA*, Raoul HENRYDepartment of Zoology, Institute of Biosciences, São Paulo State University (UNESP), Botucatu, Brazil

* Correspondence: cvscarol@hotmail.com

1. IntroductionMacrophytes 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

(due to presence of allelochemical components), are factors 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

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.

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

Research Article

This work is licensed under a Creative Commons Attribution 4.0 International License.

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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 methods2.1. Study areaThree 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).

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. SamplingUsually, 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 communityThe 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 analysisKruskall–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.

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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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included in the community values of richness, density, and composition. 3. ResultsPrecipitation 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).

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

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.

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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. DiscussionUsually, 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,

Figure 4. Means and standard deviations of root biomass of E. azurea (g.DW–1) in Barbosa Lake during the study period.

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Platyhelminthes Nematoda Oligochaeta Hirudinea Gastropoda Bivalvia Ostracoda Conchostraca Hydracarina Dicteriadidae Coenagrionidae Libellulidae Caenidae Baetidae Polymitarcyidae Pleidae Corixidae Crambidae Ceratopogonidae Chironomidae Polycentropodidae Hydroptilidae Leptoceridae Outros

Bivalvia Ostracoda Conchostraca Hydracarina Dicteriadidae Coenagrionidae Libellulidae Caenidae Baetidae Polymitarcyidae Pleidae Corixidae Crambidae Ceratopogonidae Chironomidae Polycentropodidae Hydroptilidae Leptoceridae Outros

Libellulidae Caenidae Baetidae Polymitarcyidae Pleidae Corixidae Crambidae Ceratopogonidae Chironomidae Polycentropodidae Hydroptilidae Leptoceridae Outros

Crambidae Ceratopogonidae Chironomidae Polycentropodidae Hydroptilidae Leptoceridae Others

Relative abundance (%)

0 20 40 60 80 100

January

October

July

April 12,772 ind.gDW-1

3,467 ind.gDW-1

2,387 ind.gDW-1

2,867 ind.gDW-1

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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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

Figure 7. NMDS diagram of macroinvertebrates in the sampled periods. (A) NMDS: structure; (B) NMDS: composition.

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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

the macroinvertebrates’ presence.Biomass depends on the substrate area and the

morphological complexity of the plants and influences the abundance of the associated fauna (Taniguchi et al., 2003; Tessier et al., 2004; Thomaz et al., 2008). This probably occurred in July in Barbosa Lake, since the high root biomass value and low macroinvertebrate density associated with the extraordinary flooding led to a great reduction in density in the following months. Another factor that can affect community density is root complexity, but it was not measured in the present study.

Studies on plant decomposition also showed a negative relationship between an increase in density and a decrease in root biomass (Mormul et al., 2006; Fulan and Henry, 2007), an indication that the extraordinary flood promoted a greater decomposition of E. azurea stands and a rise in environmental heterogeneity, favoring an increase in communities’ richness.

AcknowledgmentsNKA is grateful to FAPESP (proc. 2013/09144-5) for the scholarship. The authors are also grateful to Hamilton Antonio Rodrigues, Lucio Miguel de Oliveira, and Joaquim Nunes da Costa for their help in the fieldwork, and to Laerte José da Silva for revising the English of the manuscript.

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