benthic invertebrate assemblages and species diversity patterns of the upper paraguay river

RIVER RESEARCH AND APPLICATIONS

River Res. Applic. 21: 485–499 (2005)

Published online in Wiley InterScience(www.interscience.wiley.com). DOI: 10.1002/rra.814

BENTHIC INVERTEBRATE ASSEMBLAGES AND SPECIES DIVERSITYPATTERNS OF THE UPPER PARAGUAY RIVER

MERCEDES R. MARCHESE,a* KARL M. WANTZENb and INES EZCURRA DE DRAGOa

a Instituto Nacional de Limnologıa (INALI-CONICET-UNL), Jose Macia 1933, (3016) Santo Tome (Santa Fe), Argentinab Max-Planck-Institut fur Limnologie, Tropical Ecology Work Group, Postfach 165, 24302 Plon, Germany. Current address: University of

Konstanz, Limnology Institute, Postfach M659, 78467 Konstanz, Germany

ABSTRACT

This paper presents the first study of the benthic invertebrate assemblages of the upper section of the Paraguay River, a majortributary to the Pantanal wetland in Brazil. Thirty-eight sites were sampled along a 200 km section below the city of Caceres inNovember 2000. Sixty-nine species and morphospecies were identified, which were dominated by Oligochaeta and Chirono-midae. Mean density of benthic invertebrates varied between 72 and 10 354m�2 in the meandering sector of the river, 3611–49 629m�2 in the straight–transitional sectors, 682–5962m�2 in the floodplain lakes, and 1704–2208m�2 in floodplain chan-nels. Highest densities were attained in sand-gravel sediments dominated by the psammophilous oligochaete Narapa bonettoi.The Shannon diversity index ranged from 0.75 to 2.08 and was highest in floodplain lakes. Statistical analysis (UPGMA andCCA) revealed that benthic assemblages in the floodplain habitats were clearly distinct from the riverine habitats. In the riverchannel, the habitats were distinguished by grain size while the floodplain habitats were mostly determined by current and silt-clay concentration (floodplain channels) or by organic matter concentration (floodplain lakes). Conservation efforts in theUpper Paraguay area should aim to maintain the flood pulse as a permanent source of spatial and temporal habitat heterogeneity.Copyright # 2005 John Wiley & Sons, Ltd.

key words: benthos; functional units; Pantanal; floodplain; biodiversity; Narapa bonettoi

INTRODUCTION

Studies of freshwater benthic communities show a general bias towards investigations on small streams,

whereas the benthos of large floodplain rivers, especially neotropical rivers, is poorly understood. Sampling

of benthos in large, deep, and fast-flowing rivers imposes methodological difficulties (e.g. Humpesch and

Elliott, 1990). However, ecological information on the benthos of large rivers that integrates physical, chemi-

cal, and biological aspects is needed in order for scientific concepts to be tested and to provide a sound database

for conservation and management.

Several concepts have been formulated dealing with the distribution of organisms along the river course or in

habitat patches. The importance of the longitudinal dimension for the serial distribution of benthic diversity and

functional feeding groups is emphasized by the River Continuum Concept (Vannote et al., 1980) and the Serial

Discontinuity Concept (Ward and Stanford, 1983), which are based on data from partly regulated, temperate-zone

rivers. In large, free-flowing floodplain rivers, however, the lateral and temporal dimensions represented by hydro-

logical connectivity (Amoros and Roux, 1988) and the flood pulse (Junk et al., 1989; Junk, 1999) have been

shown to play a key role for organic matter budgets and species traits (Marchese and Ezcurra de Drago, 1992;

Marchese et al., 2002). The vertical (hyporheic) dimension has been studied on large-river benthos (Ward,

1989; Wantzen, 1992; Humpesch and Niederreiter, 1993; Fauvet et al., 2001) and on exchanges between rivers

and groundwater (Stanford and Ward, 1993; Amoros and Bornette, 2002).

Received 1 April 2003

Copyright # 2005 John Wiley & Sons, Ltd. Accepted 26 April 2004

*Correspondence to: Mercedes R. Marchese, Instituto Nacional de Limnologıa, (INALI-CONICET-UNL) Jose Macia 1933, (3016) Santo Tome(Santa Fe), Argentina. E-mail: [email protected]

Species traits of benthic macroinvertebrates, i.e. their life cycle strategies, correspond to the physical and che-

mical characteristics of the habitats (habitat templet; Townsend and Hildrew, 1994). In general, the benthic assem-

blages are gradually replaced in response to changes in the physical–chemical features. However, variation of

geomorphology, hydraulics, and sediment composition can lead to the establishment of discrete benthic assem-

blages within a channel, as observed in a floodplain channel of the Middle Parana River (Marchese et al.,

2002). Physical processes have emerged as architects of habitat heterogeneity in all aquatic systems (Raffaelli

et al., 1994). Organisms, such as beavers (Wright et al., 2002), alligators (Campbell and Mazotti, 2001), and float-

ing macrophyte mats in the Upper Paraguay River (K. M.Wantzen et al., in press), can also contribute considerably

to floodplain landscapes.

The attempt to incorporate different spatial scales in the classification of river habitats has recently gained

increasing importance (Frissell et al., 1986; Menge and Olsen, 1990; Levin, 1992; Giller et al., 1994; Habersack,

2000). Nested hierarchical habitat classification schemes provide the baseline for the analysis of biodiversity on

different scales: � diversity (local), � diversity (spatial species turnover), and � diversity (regional) (Whittaker,

1972). Recent investigations have documented these components of biodiversity for different taxonomic groups

in the floodplain water bodies of large European rivers (Castella et al., 1991; Tockner et al., 1998, Ward et al.,

1998; Amoros and Bornette, 2002).

Despite the Paraguay River being one of the largest South American rivers that feeds and drains the large Pan-

tanal wetland in its upper reaches, information on benthic communities is limited to studies on the tributaries

(Takeda et al., 2000; Wantzen, 1998; Heckman, 1998) and on the Lower Paraguay River (Ezcurra de Drago

et al., 2004). The goals of this study were (1) to examine the benthic communities in the different habitats units,

and (2) to attribute the species assemblages to a classification of aquatic habitats for the upper section of the Para-

guay River–floodplain system.

MATERIALS AND METHODS

The Paraguay River extends from headwater plateaux north of the city of Caceres in Mato Grosso, Brazil, to its

confluence with the Parana River near Corrientes in Argentina (Figure 1). We studied a c. 200 km section of river

between Caceres and the bifurcation of the river into a main channel and Bracinho channel at Taiama Island.

Floodplain areas occur along the entire stretch. This section is divided into five distinct sectors: (1) a headwater

sector upstream of the confluence of the Sepotuba River, above Caceres city (250 km–not studied here); (2) a

meander floodplain sector from the Sepotuba River outlet to the mouth of the Jauru River, with a bordering mean-

der floodplain (82 km); (3) a straight and moderately braided sector from the Jauru River mouth to the Morro

Pelado hills (83 km); (4) a transition sector, where the main channel is characterized by irregular meanders, from

Morro Pelado to the bifurcation of the Paraguay and Bracinho Rivers (46 km); and (5) a fluvio-lacustrine sector

from the channel bifurcation to Taiama Island (44 km), where the main channel shows alternating reaches of irre-

gular and tortuous meanders (K. M. Wantzen, et al., in press).

The study was conducted in November 2000 at low water levels. The benthic samples in the main channel of the

Upper Paraguay were taken in sectors 2 (from Caceres city), 3 and 4 of the stretch described above (I, II and III in

Figure 1), with five transects in the meandering sector and in two transects each in the straight and transition sectors

(see Table I for abbreviations of the site names). For the analysis of functional classification we adopted the ‘fluvial

unit’ given by Petts and Amoros (1996) in the Fluvial Hydrosystem Concept (FHC) which determined that ‘the

individual functional units are generally arranged in spatial succession along topographic gradient defined, for

example, by water depth, frequency of inundation or duration of period of the desiccation’. Thus, we analysed

three functional units: bank habitats, central channel and floodplain water bodies. The samples in the floodplain

water bodies were taken in two floodplain channels (LAK-GS, LAK-JS), two lakes (LAK-G, LAK-J) with indirect

or direct connection to the main channel of the transition sector, and one lake (LAK-C) in the meandering flood-

plain sector. Samples from the main channel of the Paraguay River (PYR 1–9) and one site in the Jauru River (JAU)

were collected from the central channel (C) and the left (L) and right (R) banks. In the floodplain lakes, samples

were collected at two sites (central and margin). At each of 38 sampling locations, three replicate samples

were collected using a Tamura grab (322 cm2), which were filtered through a 200 mm sieve and preserved in

486 M. R. MARCHESE, K. M. WANTZEN AND I. EZCURRA DE DRAGO

Copyright # 2005 John Wiley & Sons, Ltd. River Res. Applic. 21: 485–499 (2005)

Figure 1. Map of the Upper Paraguay River showing sampling sites 1–9 in the main channel of the Upper Paraguay River. Abbreviations: C, G,J, floodplain water bodies; JAU, Jauru River (tributary); I–III, functional sectors: I, meander floodplain, II, straight and moderately braided, III,

transition

BENTHOS OF THE UPPER PARAGUAY RIVER 487


5% formaldehyde plastic vials. The grab has been shown to be effective in deep, fast-flowing, sand-bottomed rivers

in previous studies (e.g. Ezcurra de Drago 1980; Marchese, 1987; Marchese and Ezcurra de Drago 1992; Marchese

et al. 2002). Additional sediment samples for granulometry and organic matter content analysis were taken at the

same sites. Depth, temperature, water velocity, pH, oxygen, Secchi depth, and turbidity were also measured at each

site using hand-held WTW series 300 probes, a HACH turbidimeter, and a MiniAir2 current meter. The physical

and chemical data are shown in Table I.

In the laboratory, all organisms were hand-picked from samples at 10�magnification using a dissection micro-

scope and were preserved in 70% alcohol for subsequent counting and identification to species or morphospecies

(level of taxonomic precision is indicated in Table II).

Classification analysis was performed using the Multivariate Statistical Package (MVSP, version 3.1 for Win-

dows, Kovach Computing Services) on log10 (xþ 1)-transformed abundance data. Sites were grouped by cluster

analysis using abundance data of all macroinvertebrate taxa (unweighted pair group average linkage based on the

Bray-Curtis dissimilarity) matrix. Using both species and environmental data, canonical correspondence analysis

(CCA) was performed in order to reveal the most important trends in the relationships of the macroinvertebrates to

Table I. Physical and chemical characteristics of the 38 sampling location in the Upper Paraguay River

Sampling Velocity Turbidity pH Oxygen Conductivity Secchi Depth Temperature Clay Silt Sand Organiclocation* (cm s�1) (NTU) (mg l�1) (mS cm�3) (cm) (m) (�C) (%) (%) (%) matter (%)

PYR-1L 20 68.4 7.2 7.50 30.3 26 0.8 30.0 3 0 97 0.01PYR-1C 99 32.6 7.0 7.48 33.3 26 3.0 29.6 3 0 97 0.01PYR-1R 60 34.7 7.0 8.16 36.6 26 3.0 29.6 3 0 97 0.01PYR-2L 20 55.0 7.0 4.20 150 25 0.3 30.8 3 0 97 0.01PYR-2C 30 29.1 7.2 8.30 31.7 38 3.3 30.2 1 5 94 7.00PYR-2R 40 29.1 7.1 8.20 31.8 36 1.2 30.1 3 1 96 3.00PYR-3L 37 38.8 7.0 7.43 35.5 35 3.5 28.6 3 0 97 0.01PYR-3C 80 38.6 7.1 7.10 35.4 37 4.8 28.6 3 0 97 0.01PYR-3R 14 40.7 6.7 6.90 35.4 32 1.5 28.6 3 0 97 0.01PYR-4L 76 41.3 6.7 7.10 32.6 35 1.8 28.2 3 0 97 5.00PYR-4C 87 41.5 6.7 7.15 32.6 35 4.5 28.2 3 0 97 0.01PYR-4R 76 42.3 7.0 7.33 33.0 35 1.9 28.3 3 0 97 7.00PYR-5L 34 43.7 7.4 7.03 34.2 34 0.8 30.0 17 18 65 1.00PYR-5C 74 42.0 7.4 7.16 32.7 34 3.9 30.0 3 0 97 0.01PYR-5R 53 56.9 7.3 7.07 33.7 34 2.1 30.1 21 4 65 3.00JAU-L 60 38.8 6.9 6.69 47.7 34 2.1 29.9 3 11 97 0.01JAU-C 102 41.0 7.1 6.94 40.1 34 2.1 29.6 3 0 97 0.01JAU-R 95 40.7 7.1 6.79 46.2 34 1.5 29.0 1 1 98 0.01PYR-6L 28 43.9 7.0 6.35 34.5 35 3.6 29.4 1 1 98 1.00PYR-6C 37 47.9 6.8 6.53 33.9 35 3.5 29.2 3 0 97 0.01PYR-6R 35 39.2 6.9 6.29 35.5 34 1.4 29.2 3 0 97 0.01PYR-7L 42 49.1 6.8 6.49 36.6 35 3.9 29.9 3 0 97 0.01PYR-7C 83 50.6 6.7 6.62 33.0 35 1.8 29.2 18 1 81 0.01PYR-7R 28 43.0 7.1 6.62 35.4 35 0.5 29.3 3 0 97 0.01PYR-8L 65 42.0 6.8 6.71 36.6 34 3.7 31.7 8 1 91 1.00PYR-8C 81 41.0 6.8 6.73 33.0 34 4.5 31.7 3 0 97 0.01PYR-8R 81 42.1 6.8 6.68 35.4 34 4.2 31.7 1 1 98 2.00PYR-9L 98 48.4 7.0 6.24 31.3 32 2.0 29.9 1 1 98 0.01PYR-9C 81 48.4 7.0 6.24 31.3 30 3.3 30.1 3 0 97 0.01PYR-9R 61 48.3 7.0 6.24 31.3 35 0.8 30.5 3 0 97 2.00LAK-CS 7 70.8 6.4 3.55 40.9 37 1.2 27.7 24 11 65 7.00LAK-CC 32 65.4 5.6 3.80 33.7 38 0.6 28.2 1 11 88 4.00LAK-GS 2 24.8 6.1 2.73 34.1 45 0.8 28.0 18 11 71 7.00LAK-GM 6 6.1 6.5 4.81 29.1 35 1.3 30.2 35 20 45 4.00LAK-GC 31 12.3 6.4 5.40 30.1 48 1.8 30.2 18 21 61 9.00LAK-JS 2 57.8 6.4 4.14 36.4 25 0.4 33.5 3 0 97 0.01LAK-JM 7 53.5 6.5 5.30 36.4 28 0.3 30.6 1 8 91 5.00LAK-JC 44 52.4 6.5 5.60 36.4 31 1.7 30.5 1 1 98 7.00

*PYR 1–9: main channel sites Paraguay River. Position within channel: C, central; L, left bank; R, right bank. LAK: floodplain lake sites. Firstletter, lakes C, G and J; the second letter: C, lake centre; M, lake margin; S, connecting floodplain channel.



Table II. Relative abundance* of macroinvertebrates species collected in the functional units of the Upper Paraguay River

Taxon Abb.y Bank habitats Central habitats Tributary Floodplain

Porifera (1 species)Oncosclera navicella 1

Nematoda (3 morphospecies)Tobrilus sp. 2 2 2 1Nematoda I NeI 1 1 1Nematoda II NeII 1 1

Turbellaria (2 morphospecies)Myoretronectes paranaensis Mp 2 2 1Turbellaria I Tu 1 1 2

Oligochaeta (22 species)Narapa bonettoi Nb 3 3 3 1Bothrioneurum americanum Ba 1 1 1Limnodrilus udekemianus 1cf. Rhyacodrilus sp. 1 1Tubifex tubifex Tt 1 1 1Paranadrilus descolei Pd 1 1 2Aulodrilus pigueti Ap 1 1 2Dero (A) hymanae 1 1Dero (A) cf. gravelyi Dg 1 1 2Dero (D) pectinata Dp 1 1 1Dero (D) righii Dr 1 1 1Dero (D) nivea 1Pristina osborni Po 1 1 1Pristina americana Pa 1 1 1Nais shubarti Ns 1 1Nais elinguis 1Stephensoniana trivandrana St 1 1 3 2Slavina evelinae 1Trieminentia corderoi 1Haplotaxis aedeochaeta Ha 1 1 1Brinkhurstia americana Bra 1 1 1 1Enchytraeidae 1

Hirudinea (1 specie) 1 1Helobdella adiastola 1

Chironomidae (20 morphospecies)Lopescladius sp. Lo 2 2 2Nimbocera sp. Ni 2 1Tanytarsini B 1 1Djalmabatista sp. Dj 1 1 1Cryptochironomus sp. Cr 1 1 1Harnischia sp. Har 1 1cf. Pentaneura sp. 1 1 1 1Polypedilum sp. Pol 1 1 1 1Procladius sp. Pro 1 1Coelotanypus sp. 2 1Clinotanypus sp. 1 1Ablabesmyia sp. Ab 1Tanypodinae I 1 1Fissimentum dessicatum Fi 2 1 1 1Axarus sp. Ax 1 1 1Stempellina sp. 1Brundiniella sp. 1Aedokritus sp. 1Stenochironomus sp. 1Parachironomus sp. Par 1 2 2 1

Continues



the different habitats. Environmental variables and species density data were transformed (log10 xþ 1) to achieve

approximately normal distribution of the data. The rare species were removed; only 39 out of 69 species, which

represented more than 1% in any sample, were considered in this analysis (Table II). Pearson correlations calcu-

lated to represent the explanatory variables, and linear regression analyses of CCA axis 1 and 2 sample scores and

individual variables to elucidate the most significant variables, were performed with Systat Statistical Software

(version 5.0).

Beta diversity across sampling points, in meandering and straight–transitional sectors of the Upper Paraguay

River, was calculated using two indices (Harrison et al., 1992): �-1, which allows comparisons between transects

of unequal size, and �-2, which measures the amount by which regional diversity (� diversity) exceeds the max-

imum diversity attained locally (maximum � diversity). Beta-1 ranges from 0 (complete similarity) to 100 (com-

plete dissimilarity). Beta-1 and �-2 for the dominant taxonomic group, oligochaetes and chironomids, were

calculated using the following formulae:

�-1 ¼ ½ð�=�Þ � 1�=½N � 1� � 100

�-2 ¼ ½ð�=�maxÞ � 1�=½N � 1� � 100

where � is the regional diversity (the number of species in a channel type), � (local diversity) is the mean species

number of the sites, �max is the maximum value that � can attain, and N is the number of sampled habitats within

the region.

Table II. Continued

Taxon Abb.y Bank habitats Central habitats Tributary Floodplain

Ceratopogonidae (2 morphospecies)Ceratopogonidae I CeI 1 1 1 1Ceratopogonidae II CeII 1 1

Trichoptera (1 morphospecies) 1 1 1Coleoptera (1 morphospecies) Col 2 1 1 1Ephemeroptera (6 morphospecies)

Campsurus sp. Cam 2 1 1 1Caenidae Cae 1 1 1Baetidae 1Leptohyphidae Lep 1 1 1 1Ephemeroptera I 1Ephemeroptera II 1

Odonata (1 morphospecies)Gomphidae 1 1

Cladocera (1 morphospecies)Ilyocriptus sp. Ily 1 1 1

Copepoda (2 morphospecies)Calanoida 1 1HarpacticoidaPotamocaris sp. Pot 1 1 1

Ostracoda (1 morphospecies) Os 1 1Hydracarina (1 morphospecies) Hy 1 1 1 1

Gastropoda (2 morphospecies)Heleobia sp. 1 1

BivalviaUnionacea 1

*Abundance classes: 1¼ < 100 individuals per square metre (ind. m�2); 2¼ 101–1000 ind. m�2; 3¼ 1001–10 000 ind. m�2.yTaxa with abbreviation (Abb.) exceeded 1% in any sample and were used in CCA analysis.



The data of the lower stretch (including straight and transitional sectors) were pooled together because the mor-

phology, sedimentology and general habitat characteristics are similar.

RESULTS

A total of 69 species or morphospecies were identified during the study, dominated by oligochaetes (22 species)

and chironomids (20 morphospecies, Table II). Other taxonomic groups (ephemeropterans, microcrustaceans,

nematodes, turbellarians, ceratopogonids, molluscs, hirudineans) comprised fewer morphospecies. Porifera,

Coleoptera, Trichoptera, Odonata and Hydracarina were found in few samples and had only one morphospecies

per order (Table II).

Mean densities of benthic invertebrates varied between 72 and 10 354m�2 in the meandering sector of the main

channel, 3611–49 629m�2 in the straight–transitional sectors, 682–5962m�2 in the floodplain lakes, and 1704–

2208m�2 in the floodplain channels (Figure 2a). In general, highest densities were found in mesohabitats with

sand-gravel sediments. The Shannon index ranged from 0.75 to 2.08 in the floodplain lakes which had the highest

values of all the functional units. Central channel and bank habitats with sand-gravel sediments had markedly

lower values (Figure 2b).

Figure 2. (a) Density (individuals per square metre) of invertebrates at the sampling sites. (b) Species richness and diversity(Shannon-Wiener’s H) at the sampling sites. Abbreviations as in Table I



The meandering sectors of the Upper Paraguay River showed a higher turnover of species (� diversity)

and therefore a higher landscape diversity (� diversity) than the straight–transitional sector (Table III).

Gamma diversity peaked in the bank habitats of the main channel, followed by the floodplain habitats,

and lowest values were obtained in the central channel. Beta diversity (�-1 and �-2) was higher in the

central channel and floodplain water bodies than in the banks of the main channel of the Upper Paraguay River

(Table III).

The � diversity pattern varied among the dominant taxa. Oligochaetes attained their maximum � diversity in

the floodplain water bodies, and chironomids showed similar values in all the functional units. Beta diversity

displayed an inverse pattern of � diversity. At the same time, spatial heterogeneity was higher along the channel

than in the floodplain water bodies. In general, high values of �-2 were found for oligochaetes in all the functionalunits. Low values for chironomids indicate that single sites contained most of the species within each functional

unit type. The ranking of �-1 and �-2 diversity values, taking all species into account, was similar for the central

strip of the main channel and the floodplain water bodies. The bank strip showed the lowest �-1 and �-2 diversity

(Table III).

Cluster analysis of the 38 sampling locations (Figure 3) yielded four major groups at the 60%

dissimilarity level: Group 1 comprised floodplain sites and bank habitats along the main channel

characterized by silt-clay sediments. Paranadrilus descolei, Aulodrilus pigueti, Campsurus sp. were

indicator taxa for this group. Group 2 including floodplain lakes with higher organic matter content and a

dominance of Paranadrilus descolei, Tubifex tubifex, Aulodrilus pigueti, Pristina osborni, and Fissimentum

sp. Groups 3 and 4 consist of riverine habitats, including central channel and bank habitats with patches

of sand and gravel dominated by Narapa bonettoi, Myoretronectes paranaensis, Lopescladius sp.,

Djalmabatista sp., and Parachironomus sp., but densities were much higher in group 3 than in group 4.

Sites PYR-1L and PYR-2L (left bank) were classified separately because the lowest densities were found

there.

Table III. Values of �, � and � diversity in functional sectors and functional units of the Upper Paraguay River

� �-1 �-2 �

OligochaetaFunctional sectorsMeandering 4.4 22.0 4.5 18Straight–transitional 3.0 18.1 4.5 9

Functional unitsBank habitats 3.9 22.7 4.2 19Central habitats 3.4 31.3 9.5 13Floodplain water bodies 7.3 18.9 10.0 17

ChironomidaeFunctional sectorsMeandering 3.4 24.3 4.7 15Straight–transitional 4.4 21.9 3.3 15


All taxaFunctional sectorsMeandering 13.6 20.6 5.0 53Straight–transitional 15.0 18.0 4.1 45




Canonical correspondence analysis clearly showed a gradient from floodplain waterbodies with fine

sediments and high organic matter content to central channel and bank habitats with sand-gravel sediments

(Figure 4). The first two axes of CCA explained 43.91% of the variance. Scores of axis I (29.46% variance,

eigenvalue¼ 0.14) sites were positively correlated with silt (r¼ 0.59, p< 0.001) and organic matter

(r¼ 0.73, p< 0.001) and negatively with water velocity (r¼�0.61, p< 0.001), pH (r¼�0.57, p< 0.001),

sand (r¼�0.42, p< 0.05), oxygen (r¼�0.46, p< 0.05) and depth (r¼�0.44, p< 0.05). Scores of axis II

(14.35% variance, eigenvalue¼ 0.07) sites were correlated to clay (r¼�0.25, p< 0.05). Regression of CCA

axis 1 and 2 sample scores with environmental variables and the abundance data for the most common species

demonstrated significant relationships with four physical and three chemical variables and the abundance of

sixteen species for CCA axis 1 but only eight species for CCA axis 2 (Table IV). Sediment grain size, organic

matter content and water velocity were the principal factors controlling faunal variation between functional

units (r2> 0.35, p¼ 0.0001). Thus, CCA axis 1 separated the sites according to a gradient. One end of this

gradient is represented by sites of floodplain lakes, floodplain channels, and those sites of the bank habitats

of the main channel with silt-clay sediments and high organic matter content. At the other end of the gradient,

sites comprised central channel and bank habitats, and the tributary sites with coarse sediments, high water

velocity, depth, and oxygen levels and low organic matter content. Along this habitat gradient from slow-

flow/organic-rich/fine-sediment to fast-flow/organic-poor/coarser-sediment conditions, the species assemblage

followed a sequence from Dero (A) cf. gravelyi, Aulodrilus pigueti, Paranadrilus descolei, Pristina americana

Stephensoniana trivandrana, Tubifex tubifex, Botrhioneurum americanum, Pristina osborni and Ostracoda to

Myoretronectes paranaensis, Narapa bonettoi, Haplotaxis aedeochaeta, Pristina americana, Djalmabatista

sp., Lopescladius sp., Parachironomus sp. Potamocaris sp. and Ceratopogonidae II. CCA axis 2 (r2> 0.36,

p¼ 0.0001) isolated sites of bank habitats with sandy sediments and clay patches characterized by the

assemblage composed of Brinkhurstia americana, Polypedilum sp., Nimbocera sp., Campsurus sp., Caenis

sp., Ceratopogonidae I, Hydracarina and Coleoptera (Figure 4, Table IV).

Figure 3. Cluster analysis (using the Bray-Curtis index) of the 38 sampling locations using abundance of macroinvertebrate taxa (which weretransformed using log10 (xþ 1). Sampling location abbreviations are given in Table I



DISCUSSION

Benthic assemblages in the floodplain habitats were clearly distinct from the riverine habitats, described by sedi-

ment size and organic matter content, water velocity, depth, oxygen and pH. Patches in the channel functional units

were distinguished by the presence or absence of coarse sand and gravel while differences in the floodplain habitats

were determined by current and silt-clay sediments (mostly floodplain channels) or by high organic matter content

Figure 4. Ordination of the sampling sites and invertebrate data with environmental variables using canonical correspondence analysis (CCA).(A) Ordination of sampling locations. (B) Ordination of the species abundance (abbreviations as in Table II) and significant environmentalvariables are represented by arrows: c, clay percentage; s, silt percentage; sn, sand percentage; O, oxygen concentration; OM, organic matter;

V, water velocity, pH; Z, depth.



(mostly floodplain lakes). Each functional unit was characterized by a typical benthic macroinvertebrate commu-

nity that is indicative of the habitat condition at the sites (cf. Petts and Amoros, 1996). The species assemblages of

benthic invertebrates in the main channel of the Upper Paraguay River revealed a similar pattern to those studied in

different sections of the Parana River (see studies by Varela et al., 1983; Marchese 1987; Marchese and Ezcurra de

Drago, 1992; Montanholi-Martins and Takeda, 1999; Marchese et al., 2002) and the lower section of the Paraguay

River (I. Ezcurra de Drago et al., unpublished manuscript). The psammophilous oligochaete Narapa bonettoi is the

most typical species of this assemblage, accompanied mainly by Haplotaxis aedeochaeta, Myoretronectes para-

naensis, Potamocaris sp., and Tobrilus sp. and secondarily by Lopescladius sp., Djalmabatista sp. and Parachir-

onomus sp. These are rheophilous species typically found in sandy and organic-matter-poor sediments of fast-

flowing habitats. Therefore, we suggest that this pattern is predictable for other large South American rivers with

similar characteristics. Within this general pattern, the abundance ratio of chironomids to oligochaetes was higher

in studies from Brazil (Montanholi-Martins and Takeda, 1999) than from Argentina (Marchese and Ezcurra de

Drago, 1992; Marchese et al., 2002; I. Ezcurra de Drago et al., unpublished work), presumably because of higher

temperature and lower water conductivity in Brazilian rivers.

The biodiversity patterns of river systems can only be fully understood through studies at different spatial

(Tockner and Ward, 1999) and temporal (Habersack, 2000) scales. There are few studies of large rivers that cover

Table IV. Variables having a significant regression with canonical correspondenceanalysis (CCA) axis 1 and 2 scores

Variables r2 p

CCA Axis 1Water velocity 0.37 0.0001pH 0.33 0.0001Oxygen 0.22 0.0030Depth 0.21 0.0050Silt 0.35 0.0001Sand 0.18 0.0080Organic matter 0.53 0.0001Myoretronectes paranaensis 0.51 0.0001Narapa bonettoi 0.89 0.0001Haplotaxis aedochaeta 0.27 0.0001Pristina osborni 0.45 0.0001Pristina americana 0.46 0.0001Dero (A) cf. gravelyi 0.62 0.0001Stephensoniana trivandrana 0.63 0.0001Aulodrilus pigueti 0.73 0.0001Paranadrilus descolei 0.64 0.0001Tubifex tubifex 0.19 0.0070Bothrioneurum americanum 0.12 0.0300Lopescladius sp. 0.51 0.0001Parachironomus sp. 0.39 0.0001Djalmabatista sp. 0.28 0.0001Ceratopogonidae II 0.23 0.0020Potamocaris sp. 0.16 0.0100

CCA Axis 2Brinkhurstia americana 0.41 0.0001Campsurus sp. 0.55 0.0001Caenis sp. 0.36 0.0001Nimbocera sp. 0.49 0.0001Polypedilum sp. 0.49 0.0001Ceratopogonidae I 0.36 0.0001Coleoptera 0.71 0.0001Hydracarina 0.59 0.0001



broad spatial and temporal scales (e.g. Ezcurra de Drago, 1980; Marchese and Ezcurra de Drago, 1992; Marchese

et al., 2002). Even though the study in the Upper Paraguay River did not detail temporal variations, we propose that

the species assemblage found in the central channel habitats exhibits persistence despite the physical instability of

this functional unit, with its mobile bed and dunes of variable amplitude. A study exceeding 20 years of the Parana

River floodplains, which have very similar benthic assemblages, supports this hypothesis (Marchese et al., 2002).

Narapa bonettoi attained the highest density in the Parana River as well as in the Paraguay River. As a typical r

strategist, it might be able to reach high densities in the mobile bed because of its reproductive strategies, with

asexual and sexual reproduction occurring at the same time (Marchese, 1994). Its small body size allows fast

(re-)colonization of mobile sandbeds in the central channel and bank strips; however, it may also occur in flood-

plain channels if they meet its ecological requirements (see Table II and Marchese et al., 2002).

In contrast to the homogeneity of the main channel, the species assemblages found among the floodplain func-

tional units varied largely depending on their degree of connectivity, water level, sediment patches, and macro-

phyte composition. Therefore, the benthic structure in these habitats may present differences between low and high

water levels. Their biodiversity followed a gradient of increasing biocomplexity (Amoros and Bornette, 2002) of

the functional units: main channel) floodplain channel) floodplain lakes with indirect connection. Typical spe-

cies were Tubifex tubifex, Paranadrilus descolei, Aulodrilus pigueti, Dero pectinata, Pristina americana, Botrhio-

neurum americanum, Stephensoniana trivandrana in the finer sediments with higher organic matter content, and

Pristina osborni, Dero righii, Ilyocriptus sp., Ostracoda, Fissimentum sp., Polypedilum sp., Procladius in the coar-

ser sediments. Tubificids, naidids, chironomids and ephemeropterans were dominant in the benthic assemblages in

floodplains of the Upper and Lower Paraguay Rivers and the Parana River (Takeda et al., 2000; Marchese and

Ezcurra de Drago, 1992; Marchese et al., 2002; Ezcurra de Drago et al., 2004).

In the floodplain habitats of the Pantanal, oxygen content plays a major role in the microdistribution of benthic

invertebrates. Qualitative samples have shown that large accumulations of black organic matter were often anoxic

and invertebrates were rare or absent. Drifting macrophyte mats locally reduce the oxygen content due to shading

and decomposition. Additionally, large amounts of organic matter become leached when the water levels begin to

rise. Their decomposition involves high oxygen demand and carbon dioxide release, and can cause large fishkills in

the Pantanal (Calheiros and Hamilton, 1998). The effect of this ‘dequada’ phenomenon on invertebrates has not yet

been studied in the Pantanal; however, studies on lake benthos in Amazonia (summarized by Junk and Robertson,

1997) and in the Middle Parana River (Marchese et al., 2002) strongly indicate a periodical absence of benthic

invertebrates in neotropical floodplain lakes during anoxic phases.

Nearness to the extensive floodplains in the lower sections of the study did not significantly influence biodiver-

sity of the river habitats in terms of species richness (Figure 3). Density, however, increased along the river profiles

PYR 7 to PYR 9 relative to the upstream sampling sites, mainly because of the high densities and strong dominance

of Narapa bonettoi which reached densities of 127 720m�2 in a single sample at PYR 9. Besides the input of

medium to coarse sands delivered by the Jauru River which represents a suitable substrate for this species, we

suggest that the close distance between main channel and floodplain lakes in the fluvio-lacustrine section goes

along with an increase in food quality for benthic filter feeders in the main channel.

In spite of the large densities, the small oligochaetes, nematodes and harpacticoids represent very low biomasses

in the moving sandbeds. On the other hand, mass emergences of Campsurus sp. frequently seen in the Pantanal

(Heckman, 1998; K. M.Wantzen, personal observation) indicate the attainment of a large biomass in the functional

units of the floodplain, especially in the channels (K. M.Wantzen and C.M. Butakka, unpublished work). However,

we found only low numbers of Campsurus sp. and few representatives of other invertebrate taxa larger than 1 cm in

body length, although we could count high numbers of Ephemeroptera and Trichoptera (cf. Leptonema) larvae in

bank areas with extense Campsurus burrows. We also identified wooden logs as key habitats for invertebrate colo-

nization, especially for the larger taxa. On three branches (diameter c. 10 cm, total length c. 1.3m) we found insects

(Odonata, Corydalidae, Ephemeroptera (mostly Polymitarcyidae), Trichoptera, Chironomidae, Simuliidae,

Elmidae) in high numbers. In sandy rivers, logs and snags can contribute considerably to benthic productivity

(Benke et al., 1984; Haden et al., 1999). Therefore, secondary channels joining lakes or lakes and channels and

bare clay banks should receive high priority in conservation plans.

Our study allowed the grouping of the sites within three functional units, two in the main channel of the

Paraguay River—central and bank habitats—and one in the floodplain—lakes and their linking channels.



Buffagni et al. (2000) classified five functional habitats and their characteristic macroinvertebrate species assem-

blages in the Ticino River based on hydraulic characteristics, substratum composition, and presence/absence of

aquatic macrophytes. Anderson and Day (1986) classified four habitats in the Mississippi River: one with macro-

phytes, one with coarse particle substrates and high water velocity, and two with fine particle substrates. Patches

with silt and clay sediments had a richer biodiversity than sandy sediments.

The meandering sectors of the riverscape, including a large number of mesohabitats in an erosion–deposition

pattern, caused a higher turnover of species (� diversity) and � diversity than the straight sectors. Our study spe-

cifically revealed higher � diversity and higher substrate heterogeneity in the meandering sector than in the straight

sector as reported by Tockner and Ward (1999). We attribute the differences in the sediment grain size between the

sectors to large tributary inputs of coarse sand and gravel into the straight sector.

Investigations of biodiversity pattern in alluvial floodplains emphasize the importance of different degrees

of connectivity for different taxonomic groups (Tockner et al., 1998; Tockner and Ward, 1999; Amoros and

Bornette, 2002). Different patterns of � diversity and �-1 diversity occurred between taxonomic groups.

Oligochaeta exhibited the highest � diversity and the lowest �-1 diversity in floodplain water bodies.

Chironomids showed a similar pattern, but when all species were pooled, �, �-1 and �-2 diversities

peaked in connected floodplain water bodies. The highest diversity (all groups combined) reported by Tockner

et al. (1998) in the Austrian Danube riverscape was recorded in a channel with an intermediate degree of

connectivity. Castella et al. (1991) observed a higher � diversity of macroinvertebrates in the water

bodies of the Ain floodplain with high fluvial dynamics, but a higher �-1 diversity in the more disconnected

Rhone floodplain. Tockner et al. (1998) found the highest �-1 diversity in isolated and fragmented floodplain

channels.

Beta-2 diversity can be regarded as an indicator of nestedness (Tockner et al., 1998). Oligochaetes were char-

acterized by high values of �-2 diversity, particularly in floodplain water bodies and in the central channel strip of

the main channel, exceeding the local diversity by one order of magnitude. Chironomids showed a different pat-

tern: the high values of �-2 diversity were obtained in the bank strip of the main channel, and a value of 0 was

obtained in the connected floodplain water bodies.

The highest diversity (Shannon index) was found in floodplain lakes with macrophytes as reported by Buffagni

et al. (2000) for the Ticino River. The intensity, frequency and amplitude of the flood and drought phases also can

alter the relationship between connectivity and biodiversity. According to the Intermediate Disturbance Hypothesis

(Connell, 1978), higher species diversity is expected in water bodies that connect with intermediate frequency

(Amoros and Bornette, 2002; Ward et al., 1998) and also intermediate amplitude. Isolated water bodies, during

extended drought, show a reduced benthic diversity in response to an increase in the necromass of macrophytes

that produce anoxia at the bed and high H2S concentrations. On the other hand, a long duration of hydrological

connectivity acts to unify effects on the physical and biological characteristics of neighbouring water bodies in

river–floodplain systems (Marchese et al., 2002).

Therefore, conservation efforts in the Upper Paraguay area should aim to maintain the floodpulse as a permanent

source of spatial and temporal habitat heterogeneity. Maintenance of floodplain channel structure is important,

both for the conservation of filter-feeding organisms and for the genetic connectivity between populations in dif-

ferent water bodies.

ACKNOWLEDGEMENTS

This is publication No. 106 of the Pantanal Ecology Project, resulting from the cooperation of the Bioscience Insti-

tute of the Federal University of Mato Grosso (UFMT), Cuiaba, Brazil, the Working Group of Tropical Ecology of

the Max-Planck-Institute for Limnology (MPIL), Plon, Germany, and the National Institute of Limnology (INALI-

CONICET), Santa Fe, Argentina. Financial and technical support has been given by the German Ministry of

Science and Technology (BMBF), project no. 0339373B, and the Brazilian Research Council (CNPq, reg. no.

690001/97-5); travelling grants were given by the PROALAR program of the Deutsche Akademische Austausch-

dienst (DAAD, reg. nr. D99 15373) and the Argentinian National Agency of Scientific and Technical Promotion

(SECYT reg. nr. 99-00010).



We thank Dr W. J. Junk for discussions and two anonymous reviewers for valuable suggestions to improve the

presentation. We also thank S. Meier for editing the manuscript, E. Bustorf for graphical design, and K. A. Brune

for improving the English of an earlier version of the manuscript. Special thanks to A. Olivera Amorin, C. de

Oliveira Neves and the students of the Master Course in Ecology and Conservation Biology at the UFMT for their

help with field work.

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