Benthic invertebrate assemblages and functional feeding groups in the Paraná River floodplain (Argentina)

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Limnologica 38 (2008) 159–171 www.elsevier.de/limno

Benthic invertebrate assemblages and functional feeding groups in the Parana´ River floodplain (Argentina) Florencia Lucila Zilli, Luciana Montalto, Mercedes Rosa Marchese Instituto Nacional de Limnologı´a (Consejo Nacional de Investigaciones Cientı´ficas y Te´cnicas y Universidad Nacional del Litoral), Jose´ Macia´ 1933, Santo Tome´ 3016, Santa Fe, Argentina Received 9 August 2007; received in revised form 13 December 2007; accepted 21 January 2008

Abstract The benthic invertebrate assemblages and functional feeding groups in different mesohabitats of the Middle Parana´ River–floodplain system were analyzed. Benthic invertebrates and bottom sediments were sampled in a secondary channel (center and bank mesohabitats), a temporal marginal fluvial wetland adjacent to the river, an isolated lake and a connected lake during low water level. Cluster analysis of average invertebrate densities based on the Bray Curtis dissimilarity index yielded a group composed by the mesohabitats with higher species richness, the floodplain lakes, banks mesohabitats and the wetland. The center mesohabitat of the main channel characterized by sandy sediments with low organic matter content and the lowest invertebrate densities and species richness was classified separately. Alpha diversity increased from the center mesohabitat (6 taxa) to the adjacent wetland (71 taxa), and were similar between the floodplain lakes (24 and 22 taxa) and the river bank mesohabitat (24 taxa). Gamma and beta diversities (Whittaker index) were 92 and 2.19, respectively. The highest turnover of taxa was between the river and the other mesohabitats and the lowest between floodplain lakes. Detrended correspondence analysis (DCA) showed a clear separation of wetland and banks from other mesohabitats (axis 1 and 2 explained 52.25% variance) explained by shredders and collector-filterers. The other mesohabitats were arranged in a gradient from the main channel mostly related to collector-gatherers to the connected lake and the isolated lake that were mostly characterized by predators and scrapers. The invertebrate assemblage complexity and functional feeding groups composition increased in the lateral dimension, from the center of the main channel to the temporal marginal fluvial wetland due to the influences of the spatial heterogeneity caused by different sources of organic matter inputs. r 2008 Elsevier GmbH. All rights reserved. Keywords: Parana´ River; Benthos; Lateral dimension; Mesohabitats; Beta diversity; Functional feeding groups

Introduction The spatial heterogeneity in the lateral dimension of large free-flowing floodplain rivers is generated and Corresponding author. Tel.: +54 342 4740723; fax: +54 342 4750394. E-mail address: fl[email protected] (F.L. Zilli).

0075-9511/$ - see front matter r 2008 Elsevier GmbH. All rights reserved. doi:10.1016/j.limno.2008.01.001

maintained by hydrological connectivity (Amoros and Roux 1988) and the influence of flood pulse (Junk et al. 1989; Junk 1999), which plays a key role in organic matter budgets and species traits (Marchese and Ezcurra de Drago 1992; Marchese et al. 2002). The Middle Parana´ River floodplain comprises a wide variety of secondary channels, lakes with a connectivity degree ranging from isolated to permanently connected

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with the channels and temporal marginal wetlands regulated by the flood-pulse (Neiff 2001; Neiff and Poi de Neiff 2003). In these habitats, the importance of vegetation (riparian and macrophytes) as a source of allochtonous and autochthonous organic matter and as a structuring factor for macroinvertebrate communities has been well established (Burton et al. 2002; Kelly and Hawes 2005; Marchese et al. 2005; Poi de Neiff et al. 2006). The complexity of macroinvertebrate communities may be studied from the structural or functional perspective, and although many authors have reported the relevance of one or another point of view, it also has been noted that an integrated approach is more appropriate (Walker 1992; Rosenfeld 2002). Thus, to establish the patterns of biodiversity and to understand the variations in the diversity species is a major focus in ecology (Harborne et al. 2006). By this way, beta diversity provides insights into the partition of habitats by species and constitutes a good perspective on analyzing biodiversity in a river–floodplain system (Ward et al. 1999; Amoros and Bornette 2002). Besides, if the goal is to determine the role of species in the ecosystem, the functional feeding groups (FFGs) approach may be appropriate (Merritt et al. 1996, 2002; Cummins et al. 2005). In spite of the high importance of benthic macroinvertebrates in river–floodplain systems, there are few studies on benthic invertebrate assemblages in temporal wetlands (Pacini and Harper 2001; Arscott et al. 2002; Poi de Neiff and Casco 2003; Van der Nat et al. 2003; Montalto and Marchese 2005; Montalto and Paggi 2006) and floodplain lakes of large rivers (Ezcurra de Drago 1980; Heuschele 1969; Junk and Robertson 1997; Bonetto et al. 1978; Bechara and Varela 1990; Ezcurra de Drago et al. 2004), while there is more information on the invertebrates of lotic environments. Despite the high complexity caused by the flood pulse and sources of organic inputs, there is little information about the differences in diversity, assemblages and FFGs among different mesohabitats of Parana´ River system (Ezcurra de Drago et al. 2007). We hypothesize that the macroinvertebrate assemblages and FFGs composition are dissimilar among floodplain mesohabitats of Parana´ River and show a structural and functional complexity gradient from the main channel to the temporary wetland.

Fig. 1. Map showing the mesohabitats studied. Abbreviations: TVC, Tiradero Viejo River central channel; TVB, Tiradero Viejo River banks; VYL, Vuelta de Yrigoyen lake; LML, La Mira lake; TMFW, temporal marginal fluvial wetlands.

Parana´ River basin (Tiradero Viejo River, in the center: TVC) and the banks mesohabitat (TVB), two lakes with different degree of connection with Parana´ River channel (Vuelta de Yrigoyen lake, VYL: permanently connected; La Mira lake, LML: isolated), and a temporal marginal fluvial wetlands (TMFW) (Fig. 1). The central mesohabitat of the secondary channel (TVC) is characterized by a sandy bed with low organic matter content, and a low current velocity especially during the low water phase. The banks (TVB) with siltclay sediments and higher detritus content show an important development principally of floating meadows during low water. The TMFW selected for this study is a zone flooded by the TVC during high water levels and which remains inundated during the low water phase for approximately 4 months and includes the riverine pioneer forests dominated by Tessaria integrifolia and Salix humboldtiana. This mesohabitat is also covered by floating meadows (Eichhornia crassipes, Pistia stratiotes, Salvinia herzogii), aquatic and pallustrine grasses (Echinochloa spp., Polygonum sp., Panicum spp., Typha sp., Thalia sp., Ludwigia peploides, etc.) and shrubs (Sesbania virgata, Panicum prionites, Solanum sp.) which produce heterogeneous patchiness of decaying litter. The permanently connected lake (VYL) has an irregular shape and is free of floating macrophytes in the center. On the other hand, the isolated lake (LML) is smaller, circular in shape and covered by floating meadows, mainly E. crassipes and submerged rooted species such as Ceratophyllum spp. At low water levels, the growth and decay of primary producers (mainly macrophytes) and the mixing and resuspension of sediments govern lakes metabolism (Drago et al. 2003).

Study area Material and methods The study area is located on the right bank of the Parana´ River basin in the cross-section between Santa Fe city and Parana´ city (311400 S–601300 W and 311460 S–601390 W), Argentina (Fig. 1). The selected mesohabitats included a secondary channel of the

One sampling station in TVC and one in TMFW, two in TVB (including left and right banks) and three in each lake (VYL, LML) mesohabitats were sampled. Three replicates of bottom sediments for benthic invertebrates,

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one sample for bottom organic matter and one for granulometric analysis were collected during low water levels since 2001–2005 with a Tamura grab of 319 cm2 (in the river), Ekman grab of 225 cm2 (in floodplain lakes) and corer of 79 cm2 (in the temporal fluvial wetland). The Tamura grab has been shown to be the most effective in deep, fast-flowing sandy bottom rivers (Marchese and Ezcurra de Drago 1992), the Ekman grab in silt-clay sediment (widely used in lakes) and the corer in flooded soils in temporal wetlands (Montalto and Marchese 2005). The benthic samples were fixed in 10% formaldehyde in the field. In the laboratory, the organisms were handpicked from samples under stereoscopic microscope (4  ) and preserved in 70% alcohol for subsequent counting and identification. All taxa were categorized into FFGs based on available information (Merritt and Cummins 1996; Cummins et al. 2005). Physical and chemical variables such as conductivity (Beckman conductivity meter), depth, transparency (Secchi disk), pH (Hellige), and temperature (standard thermometer) were measured in situ in each sampling station. Bottom water oxygen (Winkler method), percentage of fine particulate organic matter (FPOM o1000 mm), coarse particulate organic matter (CPOM 41000 mm) and granulometric composition (Wentworth 1932) were determined in the laboratory. The organic matter was filtered through a 1000 mm sieve, the two fractions (CPOM and FPOM) were dried at 100 1C to constant mass and the organic matter was obtained by ignition (muffle furnace at 550 1C for 3 h). Alpha diversity (a, local species number) and beta diversity (spatial species turnover) were calculated based on presence–absence data according to Whittaker (1972), using the following formula: bw ¼ (S/¯a)1, where S is the total number of species recorded for the mesohabitats and a¯ is the average species found within mesohabitats. Beta diversity was calculated from the benthic invertebrates found between all pairs of mesohabitats. For the calculation of total beta (among all mesohabitats), analysis was performed in BioDAP. Mesohabitats were grouped by cluster analysis using log10(x+1)-transformed abundance data of all macroTable 1.

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invertebrate taxa (unweighted pair group average linkage based on the Bray–Curtis dissimilarity) matrix. In order to analyze variation in species composition between mesohabitats, we used SIMPER analysis in PRIMER-E package (Version 6.0). Detrended correspondence analysis (DCA) was applied to evaluate the more important trends in the relationships of the FFGs in different mesohabitats (using the MVSP, version 3.1, Kovach Computing Services). The relationship between the number of species within each FFG (y) and the taxonomic richness (x) was analyzed performing regression analysis to determine the model that best fitted (INFOSTAT, version 2.1).

Results Physical and chemical characteristics Temperature and pH had similar values in the different habitats. The highest Secchi disk values were registered in the floodplain lakes (VYL and LML), while similar values were obtained in the other habitats. The highest depth was reached in the center of the main channel and the highest conductivity and the lowest values of bottom-dissolved oxygen were registered in TMFW (Table 1). The bottom sediments of TVC and TMFW were sandy (98% and 82%, respectively) with a low percentage of silt-clay and low organic matter content, 0.02% of FPOM in the central channel and 0.86% CPOM and 0.41% FPOM in the wetland (Fig. 2). The other habitats were characterized as silt-clay sediments (TVB: 76%; VYL: 90%; LML: 94%). The floodplain lakes showed the highest bottom organic matter content (LML: 6% CPOM and 13% FPOM; VYL: 3% CPOM and 10% FPOM) (Fig. 2). The TVC was the more homogeneous mesohabitat, while the banks, lakes and wetland mesohabitats showed higher spatial and temporal heterogeneity because are largely influenced by riparian and aquatic vegetation and by the flood-drying period.

Median values and range of environmental variables in different mesohabitats

Variables

TVC

TVB

pH Temperature (1C) Oxygen (mg l1) Depth (m) Conductivity (mS cm1) Secchi (m)

7.3 24.0 7.6 3.22 130 0.20

7.2 21.0 7.1 1.95 130 0.20

(7–7.3) (16.0–26.0) (7.0–9.0) (2.81–3.82) (100–140) (0.10–0.25)

(7–7.3) (14.0–26.0) (4.4–9.0) (0.50–3.82) (80–140) (0.09–0.27)

VYL

LML

TMFW

7.2 22.0 8.8 2.20 110 0.54

7.2 20.0 9.6 2.67 90 0.84

7.4 18.0 1.0 0.20 310 0.20

(7–7.6) (17.0–23.5) (7.4–8.9) (1.65–5.50) (100–120) (0.16–0.65)

(7.2–7.6) (16.5–24.0) (4.6–11.3) (1.97–2.91) (80–100) (0.60–0.95)

(7.2–7.6) (12.5–18.5) (0.1–4.7) (0.17–0.21) (110–480) (0.17–0.20)

Abbreviations: TVC, TiraderoViejo River central channel; TVB, Tiradero Viejo banks; VYL, Vuelta de Irigoyen lake; LML, La Mira lake; TMFW, temporal marginal fluvial wetland.

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Fig. 2. Granulometric and organic matter composition of bottom sediments from different mesohabitats of the Middle Parana´ River floodplain. The bars show the standard deviation. Abbreviations: TVC, Tiradero Viejo River central channel; TVB, Tiradero Viejo River banks; VYL, Vuelta de Yrigoyen lake; LML, La Mira lake; TMFW, temporal marginal fluvial wetlands.

Fig. 3. Average invertebrate densities (ind m2) from mesohabitats studied. The bars show the standard deviation. Abbreviations: TVC, Tiradero Viejo River central channel; TVB, Tiradero Viejo River banks; VYL, Vuelta de Yrigoyen lake; LML, La Mira lake; TMFW, temporal marginal fluvial wetlands.

Benthic invertebrates assemblages The total average densities varied from 350 ind m2 (TVB) to 5220 ind m2 (TMFW), while in TVC the density was 1947 ind m2, and reached similar values in

lakes: 3016 ind m2 (LML) and 3442 ind m2 (VYL) (Fig. 3). Cluster analysis of the average invertebrates densities of each mesohabitats, yielded a group formed by floodplain lakes (LML: isolated and VYL: connected),

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Table 2. (continued )

Fig. 4. Dendrogram resulting of UPGMA clustering method based on Bray Curtis index, after log10(x+1) invertebrates densities transformation. Abbreviations: TVC, Tiradero Viejo River central channel; TVB, Tiradero Viejo River banks; VYL, Vuelta de Yrigoyen lake; LML, La Mira lake; TMFW, temporal marginal fluvial wetlands.

Table 2. Percentage contribution of taxa (ffi50%) differentiation between mesohabitats (SIMPER analysis) TVC with

LML

VYL

TVB

Narapa bonettoi Aulodrilus pigueti Trieminentia corderoi Chaoborus sp. Limnodrilus hoffmeisteri Chironomus gr. decorus Campsurus violaceus Nematoda Parachironomus spp. Corynoneura sp. Axarus sp.

13.60 10.82 8.64 7.55 6.73 6.60 – – – – –

15.83 9.59 6.20 – 7.66 – 7.10 6.10 – – –

26.07 – – – – – – 6.98 8.11 5.91 4.37

Cum. %

53.94

52.48

51.44

TVB with

LML

VYL

VYL with LML

A. pigueti T. corderoi Chaoborus sp. C. gr. decorus L. hoffmeisteri Nematoda Hirudinea spp. C. violaceus Corbicula spp. Ablabesmyia spp.

10.29 9.09 7.98 6.98 6.93 6.63 5.16 – – –

9.86 6.68 – – 8.11 6.29 4.49 6.65 4.13 4.12

6.37 6.95 5.80 7.75 6.13 6.54 5.43 6.11 – –

Cum. %

53.06

50.33

51.08

TMFW with

VYL

N. bonettoi Ostracoda Polypedilum spp. Pristina leidyi Tanytarsus spp.

– 3.98 3.92 3.28 3.14

LML 2.49 4.09 3.37 3.15

TVB

TVC

4.06 2.96 3.75 3.32

4.56 3.98 3.40 3.32 3.18

TMFW with

VYL

LML

TVB

TVC

Ablabesmyia spp. Pristina americana Monopelopia sp. Hirudinea Slavina evelinae Aphylla sp. A. pigueti Hyalella curvispina Nematoda T. corderoi Ceratopogonidae spp. Dero hymanae Dero multibranchiata Curculionidae sp. L. hoffmeisteri C. violaceus Harpacticoida spp. C. gr. decorus Dero sawayai Chaoborus sp. Paranadrilus descolei

2.21 3.05 2.90 – 2.34 2.56 2.23 2.33 1.86 1.70 2.87 2.15 1.93 1.65 2.33 2.33 1.65 1.64 – – –

3.23 3.14 2.98 – 2.40 2.45 1.74 2.39 – 1.72 2.95 2.17 1.90 1.69 2.27 – 1.68 1.63 1.58 2.63 –

3.03 2.71 3.23 2.12 2.63 2.13 2.17 2.49 2.33 2.15 2.96 1.95 1.90 1.88 – – 1.74 – – – 1.64

3.10 3.10 2.95 2.90 2.40 2.39 2.36 2.27 2.24 2.13 2.04 1.95 1.90 1.80 – – – – – – –

Cum. %

52.05

51.65

51.15

51.97

Abbreviations: TVC, TiraderoViejo River central channel; TVB, Tiradero Viejo banks; VYL, Vuelta de Irigoyen lake; LML, La Mira lake; TMFW, temporal marginal fluvial wetland.

which linked to the banks mesohabitats (TVB) and TMFW. The TVC was classified separately to the other mesohabitats (Fig. 4). Narapa bonettoi, only recorded in TVC, showed the highest contribution to this mesohabitat differentiation and also Paranadrilus descolei sp. contributed to its differences with the banks mesohabitats (TVB). The wetland (TMFW) was characterized by many taxa with similar contribution (Ostracoda spp., Polypedilum spp., Pristina leidyi, Tanytarsus spp. Ablabesmyia spp., Monopelopia sp., Pristina americana) to its differentiation of other mesohabitats. On the other hand, Aulodrilus pigueti, Limnodrilus hoffmeisteri, Trieminentia corderoi, Campsurus violaceus and Chaoborus sp. were the taxa that mostly contributed to the differentiation of lakes from the other mesohabitats and Chironomus gr. decorus was only registered in the isolated lake (LML) (Table 2).

Diversity and functional feeding groups (FFGs) Taxa recorded in each mesohabitat, their relative abundances and FFGs assigned are shown in Table 3. Alpha (a) increased from TVC (6 taxa) to TMFW (71 taxa), being similar between the floodplain lakes (LML: 24 taxa and VYL: 22 taxa) and the bank mesohabitat

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Table 3.

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Relative abundance of taxa and functional feeding groups at the different mesohabitats

Taxa Turbellaria Nematoda Oligochaeta Enchytraeidae sp. Trieminentia corderoi Harman Pristina leidyi Smith P. prosboscidea Beddard P. americana Cernosvitov P. menoni Aiyer P. osborni Walton D. (D.) multibranchiata Steiren D. (D.) palmata Aiyer D. (D.) digitata Mu¨ller D. (D.) obtusa d’Udekem D. (D.) sawayai Marcus D. (D.) nivea Aiyer Dero (A.) furcatus Mu¨ller D. (A.) hymanae Naidu D. (A.) vagus Leidy D.(D.) righii Varela Allonais paraguayensis Michaelsen Slavina evelinae Marcus S. isochaeta Cernosvitov Nais communis Piguet Limnodrilus udekemianus Clapared L. hoffmeisteri Clapared Aulodrilus pigueti Kowalewski Bothrioneurum americanum Bebbard Paranadrilus descolei Gavrilov Narapa bonettoi Rigui & Varela Eiseniella tetraedra Savigny Hirudinea

Sites TVC

TVB

VYL

LML

TMFW

FFG

1

1

2

2

1 2

P P

2

2

1 1 2 1 2

C-g C-g C-g C-g C-g C-g C-g C-g C-g C-g C-g C-g C-g C-g C-g C-g C-g C-g C-g C-g C-g C-g C-g C-g C-g C-g C-g C-g

1 1 1 1 1 1

1

Insecta Entomobryidae spp. Ephemeroptera Leptophlebiidae spp. Campsurus violaceus Needham & Murphy Caenidae spp.

1 1

1 1

1 1 1 1 1 1 1 1

1 1 2 1 1 1 1 1

2 3

2 3

1 1 2 1

1

1

1

2

1

P

1 1

1 1

1

C-f C-f C-f Scr Scr Scr Scr Scr Scr

1 2 2 1

C-f C-g Shr Shr

1

C-g

1

C-g C-g C-g

1 3 1 1

Mollusca Limnoperna fortunei Dunker Corbicula Megerle sp. Pisidium Pfeiffer spp. Pomacea canaliculata Lamarck Asolene d0 Orbigny spp. Heleobia guaranitica Doering Gundlachia Pfeiffer spp. Planorbidae spp. Omalonix unguis d’Orbigny Crustacea Harpacticoida spp. Ostracoda spp. Hyalella curvispina Shoemaker Trichodactylus borelianus Nobili

1 1 1

2

1 2

1 1 1 1

1

1

1

1

1

1

1 1

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Table 3. (continued ) Taxa

Sites TVC

TMFW

FFG

1 1 1 1

P P P P

Heteroptera Hebrus Curtis sp. (L) Lipostemmata mayor Ashlock (L)

1 1

P P

Coleoptera Hydrochus Leach sp. (L) Hydrochus Leach sp. (A) Berosus Leach sp. (L) Anacaena cordobana Knish (A) Enochrus (M.) circumcinctus Buch (A) Tropisternus (T.) carinispina Orhymont (A) Gymnoshthebius sp. (A.) Heterocerus similis Grouvelle (A) Tropicus Pacheco sp. (A) Staphylinidae sp. (A) Cyphon Paykull sp. (L) Curculionidae sp.(L)

1 1 1 1 1 1 1 2 1 1 1 1

P C-g P C-g C-g C-g C-g C-g C-g P C-g Shr

2 1

1 1

P P P P P P P P P P C-g C-g C-g C-g P Shr C-g C-g Shr C-f C-g C-g C-g P

1 1

C-f P

Odonata Telebasis willinki Frasser Aphylla Selys sp. Erythrodiplax Brauer sp. Perithemis Hagen sp.

Diptera Tipulidae spp. Ceratopogonidae spp. Chaoborus Lichtenstein sp. Clinotanypus Kieffer spp. Coelotanypus Kieffer spp. Ablabesmyia Johannsen spp. Labrundinia Fittkau spp. Monopelopia Fittkau sp. Djalmabatista Fittkau spp. Tanypus Meigen sp. Axarus Roback sp. Chironomus Meigen gr. decorus spp. Parachironomus Lenz spp. Goeldichironomus Fittkau spp. Cryptochironomus Kieffer spp. Phaenopsectra Kieffer sp. Harnischia Kieffer spp. Saetheria Jackson sp. Polypedilum Kieffer spp. Tanytarsus Epler spp. Pseudochironomus Saeter sp. Corynoneura Winnertz sp. Stratyiomidae spp. Dolichopodidae spp. Trichoptera sp. Hydroptilidae spp.

TVB

VYL

LML

1

1 1 1 1

1 1

2 1 1

1 1

1 2 1 2 1 1

1 2 1

1 1 1

1

1 1 1 1

1

1 1

1

3 2

1 1

Abbreviation: TVC, TiraderoViejo River central channel; TVB, Tiradero Viejo banks; VYL, Vuelta de Irigoyen lake; LML, La Mira lake; TMFW, temporal marginal fluvial wetland; FFG, functional feeding group; P, predators; C-g, collectors-gatherers; C-f, collectors filterers; Scr, scrapers; Shr, shredders; A, adults; L, larvae. Abundance classes: 1 ¼ 1–100 ind m2; 2 ¼ 101–1000 ind m2 3: X1001 ind m2.

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(TVB: 24 taxa) as is showed in Table 4. Although the sampled areas were comparatively similar, the highest local diversity found in TMFW included the 77% of the regional diversity, where gamma diversity (g) was 92 taxa. Beta diversity (bw) among all the mesohabitats was 2.129, with a 53% taxa turnover in the system. The pairwise beta indicated a high turnover between mesohabitats, with the highest replacement of taxa between the main channel of the TVC and the other mesohabitats. On the other hand, bw between lakes was the lowest, showing the high similarity in taxa composition (Table 4). Table 4. Alpha (a) and beta diversity (bw) between mesohabitats (performed in BioDAP) and gamma diversity (g)

Alpha (a) Beta (bw) TVC TVB VYL LML

TVC

TVB

VYL

LML

TMFW

6

24

22

24

71

0.800

0.929 0.652

0.933 0.667 0.435

0.922 0.663 0.763 0.684

Beta among mesohabitats (bw): 2.129 (BioDAP) Gamma (g): 92 Abbreviation: TVC, TiraderoViejo River central channel; TVB, Tiradero Viejo banks; VYL, Vuelta de Irigoyen lake; LML, La Mira lake; TMFW, temporal marginal fluvial wetland

The most represented FFG was collector-gatherers in all mesohabitats; however, the taxonomic unit richness was different within each mesohabitats showing more spatial variability than scrappers, shredders and collector-filterers. There was an increment in the number and relative importance of taxa in the FFGs from the lotic environment (TVC) to the marginal wetland (TMFW) (Figs. 5 and 6 and Table 3). The lotic habitat (TVC) presented the lowest number of FFGs, and was dominated by collector-gatherers (N. bonettoi, Bothrioneurum americanum, Parachironomus spp. and Corynoneura sp.). The predators (Nematoda and Ceratopogonidae) were very scarce, with the lowest number of taxonomic units for each group. The river banks (TVB) were dominated by collector-gatherers (16 taxonomic units, such as P. descolei, C. violaceus, Axarus sp. and Parachironomus spp.), and showed a low abundance of predators (7 taxa, such as Coelotanypus spp., Ablabesmyia spp., Djalmabatista spp. and Aphylla sp.) and shredders (Polypedilum spp.) (Figs. 5 and 6 and Table 3). In the floodplain, lakes the relative abundances of FFGs were similar. The collector-gatherers (13 taxa in VYL and 12 taxa in LML) were represented by Oligochaeta with a dominance of A. pigueti, L. hoffmeisteri and T. corderoi, and in the connected lake P. descolei was also found. C. violaceus and Chironomidae, with a dominance of C. gr. decorus spp. in LML and Harnischia spp. in VYL, also were recorded. The predators (6 taxa in each lakes) were very important in

Fig. 5. Relative abundances of the functional feeding groups at studied mesohabitats. Abbreviations: TVC, Tiradero Viejo River central channel; TVB, Tiradero Viejo River banks; VYL, Vuelta de Yrigoyen lake; LML, La Mira lake; TMFW, temporal marginal fluvial wetlands.

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Fig. 6. Functional feeding groups taxonomic units and organic matter content (%) in studied mesohabitats. Abbreviations: TVC, Tiradero Viejo River central channel; TVB, Tiradero Viejo River banks; VYL, Vuelta de Yrigoyen lake; LML, La Mira lake; TMFW, temporal marginal fluvial wetlands.

Fig. 7. Detrended correspondence analysis performed for functional feeding groups densities in each sampling site. Abbreviations: TVC, Tiradero Viejo River central channel; TVB, Tiradero Viejo River banks; VYL, Vuelta de Yrigoyen lake; LML, La Mira lake; TMFW, temporal marginal fluvial wetlands.

both lakes and were represented by Nematoda, Hirudinea, Chaoborus sp. (mainly in the isolated lake), and Chironomidae (Coelotanypus spp., Ablabesmyia spp.). The scrapers Asolene sp., Heleobia guaranitica, and Planorbidae were found (LML: 3 taxa and VYL: 1 taxa) as well as the collector-filterers (2 taxa in each lake) Corbicula sp. and Pisidium spp. with higher abundance in the isolated lake (Figs. 5 and 6 and Table 3). In the isolated lake, shredders were represented only by Polypedilum spp. In the TMFW, all the FFGs were well represented. Among the collector-gatherers (35 taxa), the Oligochaeta

(Pristina spp., Dero spp., A. pigueti, T. corderoi, Enchytraeidae sp. and B. americanum), Chironomidae (C. gr. decorus spp.) and adults of Coleoptera reached greatest abundance. Predators, collector-filterers and shredders were more abundant in TMFW than in the other mesohabitats. The predators were the richest (23 taxa), mainly Chironomidae (Ablabesmyia spp., Monopelopia spp., Djalmabatista spp., Labrundinia spp., Tanypus sp.), Nematoda, Turbellaria, Odonata (Aphylla sp., Perithemis sp., Erythrodiplax sp.) and Coleoptera (Berosus spp. larvae, Hydrochus sp. larvae and adult Staphylinidae sp.). The collector-filterers (4 taxa) were

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Discussion

Fig. 8. Regression plots of the relationship between number of (A) collector-gatherers and accumulative richness and (B) predators and accumulative richness.

represented by Bivalvia (Limnoperna fortunei) and Chironomidae (Tanytarsus spp.). The shredders (5 taxa) were mainly represented by Polypedilum spp. and in lower densities Hyalella curvispina, Phaenopsectra spp. and Trichodactyllus borelianus. The scrapers (4 taxa) were molluscs (Asolene sp., Gundlachia sp. and Omalonix unguis) (Figs. 5 and 6 and Table 3). DCA showed a clear separation of wetland (TMFW) and banks (TVB) from other mesohabitats (axis I and II explained the 52.25% of the variance) explained by shredders and collector-filterers (Fig. 7). The other mesohabitats were arranged in a gradient from the lotic channel (TVC) mostly related to collector-gatherers to the connected lake (VYL) and the isolated lake (LML) that were mostly characterized for predators and scrapers. Also, some TVB samples were included in this gradient, showing its intermediate arrange. The regression with the best fits obtained for collector-gatherers was curvilinear with the equation y ¼ 27.385+(1.03427.385)/[1+(x/28.789)1.391], R2 ¼ 0.937, po0.0001 (Fig. 8A). On the other hand, the curve for predators was linear, with equation y ¼ 0.187+0.335x, R2 ¼ 0.935, po0.0001 (Fig. 8B). The regression analyses performed with the other feeding groups were not significant and did not show any pattern.

Beta diversity indicates the taxa turnover level between habitats, but also the existence of a comparatively heterogeneous habitat patchiness (Koleff et al. 2003; Stendera and Johnson 2005), which could strongly influence population and community dynamics (Tokeshi 1993). Among the elements of this complexity, the substrate, depth, current velocity and the pathways of organic matter play a key role in the distribution of organisms at small spatial scales (Frissel et al. 1986; Hieber et al. 2005), acting as filters for the species of the regional pool, impacting on the distribution of the organisms and finally on the composition of the local assemblages (Poff 1997; Hieber et al. 2005). In our study, bottom sediment composition, deciduous forest in the riparian zone, macrophytes litter, coarse and fine detritus were important factors describing the habitat heterogeneity and contributed to the highest turnover of taxonomic units between the main channel of TVC and the other mesohabitats. In the TMFW, the dominant species were Oligochaeta Naidinae and Chironominae, mainly r-strategists which present traits that enhance their resistance to water loss, such as diapause, cysts, and physiological tolerance to the drying phase (Laddle and Bass 1981; Montalto and Marchese 2005). In addition, the high biodiversity in these mesohabitats may be due to the environmental instability (flooding-drought). On the other hand, in the floodplain lakes and in the river, the dominant species were Oligochaeta Tubificinae and Mollusca, because the more stable environmental conditions favor the K-strategist (Marchese and Ezcurra de Drago 1992; Ezcurra de Drago et al. 2007). The few differences in diversity between the isolated and connected floodplain lakes were unexpected, as the connectivity with the stream often generates high habitat heterogeneity and optimal environmental conditions (e.g. more oxygen). Although interactions between taxa has not been analyzed in our study, it is important to stress that in the studied habitats, mainly in the isolated floodplain lake and in the temporary wetland, the biotic interactions are also important in structuring the communities, mainly by predation (fish and amphibians) (Oliveros 1980; Lajmanovich 2000; Peltzer and Lajmanovich 2004). Many studies have emphasized the importance of biotic interactions in structuring communities at both small and large spatial scales (Englund 1991; Hildrew et al. 2004). In all the aquatic ecosystems, detritus constitutes a multiple resource for benthic macroinvertebrates (Polis and Strong 1996), acting as habitat, food source and refuge to avoid predators (Holomuzki and Hoyle 1990; Reice 1991; Dudgeon and Wu 1999). In the floodplain habitats of the Middle Parana´ River, there is a constant

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supply of energy coming partly from the riparian vegetation but mainly from the macrophytes, with abundant leaf litter decaying at the bottom (Capello et al. 2004; Poi de Neiff et al. 2006). In our study, varying amounts and supplies of detritus were found with low percentages of organic matter content in bottom sediments of the channel and formed only by the smallest fractions (FPOM). On the other hand, the largest quantities of organic compounds were obtained in floodplain lakes with the highest contribution from water hyacinth (E. crassipes). Finally, the marginal wetland as well as the banks of the river had a more diverse contribution from the riparian vegetation, with participation of trees (S. humboldtiana, T. integrifolia, Erhythrina crista-galli), macrophytes (E. crassipes, P. stratiotes, Azolla spp.) and grasses (Paspalum spp., Eryngium spp., Echinochloa spp.). Moreover, wetlands mesohabitats are optimal places for colonists not only from benthos but also from pleuston communities. In temperate northern streams, abundances of shredders and decay rates of leaves are positively correlated (Wallace et al. 1982; Jonsson et al. 2001; Cummins et al. 2005), whereas in the tropics, breakdown of leaves is driven more by microbial action than by insect shredding (Maltby 1992; Irons et al. 1994; Wantzen and Wagner 2006). The characteristics of our studied area could be determining the fact that, although the collector-gatherers prevail in species-richness and density, the contribution of shredders may be variable on food webs depending on the diversity and quality of vegetation sources. Many taxonomic groups that represent typical shredders from temperate zones are not represented in the Parana´ River system. In this study, the shredders were principally chironomids and decapods, and were only well represented in marginal fluvial wetland. We observed Polypedilum spp., and Phaenopsectra sp. chewing leaves, and Hyalella sp. was considered a shredder according to Cummins et al. (2005), although Wantzen and Wagner (2006) have suggested that is predator and Poi de Neiff et al. (2006) that is collector-gatherer. Different assignments of invertebrate to FFG are commonly found in the literature because there are few studies based on gut analysis and the food-spectra can change during life cycle (Motta and Uieda 2004). The curvilinear pattern found between the cumulative species number and the richness obtained in collectorgatherers suggests that this FFG may be saturated (according to the term proposed by Cornell and Lawton 1992), while the linear relation obtained for predators indicates an unsaturated FFG. The collector-gatherers saturation in the Parana´ River floodplain may be explained by the high richness of taxonomic units with low population densities that may indicate competition and trophic niche overlap. On the other hand, the unsaturated predators pattern could be explained

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because includes few species of small size (o2 cm). This interpretation depends on the scale used to define a local community as reported by Loreau (2000), at small spatial scales a diversity contributes less to total diversity because of the direct interactions common at small scales. However, in our study the TFMW mesohabitats contribute with the 77% of the regional diversity. All the other FFGs were represented in each mesohabitat analyzed, although the number of species within and among mesohabitats were different. Naeem (1996) suggested that the apparent redundancy of species is due to the fact that most small changes in species composition are likely to involve species within functional groups rather than entire functional groups. According to the redundancy model (Walker 1992), the taxa that belong to the same functional group should have similar effects on ecosystem processes. The marginal wetland supports more taxonomic units with equivalent feeding functions because of its spatial and temporal habitat heterogeneity. The invertebrate assemblage complexity and FFGs composition increased in the lateral dimension, from the center of the main channel to the temporal marginal fluvial wetland (TVC–TVB–VYL–LML–TFMW), principally due to the influences of the spatial heterogeneity caused by different sources of organic matter inputs and the location of mesohabitats into the river–floodplain system.

Acknowledgments This study was supported by a grant from Universidad Nacional del Litoral (UNL) and Consejo Nacional de Investigaciones Cientı´ ficas y Te´cnicas (CONICET). We thank the Asia Science Editing for revising the English. We thank the constructive comments of two anonymous reviewers.

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