DOI: 10.1899/06-12.1
Published online: 16 October 2007
Aquatic macroinvertebrate response along a gradient of lateral connectivity in river floodplain channels
Amael Paillex1, Emmanuel Castella2, AND Gilles Carron3
Laboratoire d’Ecologie et de Biologie Aquatique, Universite´ de Gene`ve, 18 ch. des Clochettes, CH-1206 Gene`ve, Switzerland
Abstract. Large river floodplains potentially include the full range of freshwater ecosystems from permanently flowing channels to temporary pools and springs. Attempts to restore such complex systems require tools adapted to assess restoration success. In an analysis of invertebrate assemblages in the Rhoˆne River floodplain (France), taxonomic-based indices (rarefied richness and assemblage composition) were compared with functional metrics using trait-based ratios as surrogates of ecosystem processes. Their ability to respond to a gradient of hydrological connectivity was assessed in 7 cut-off channels. The sampling design included 2 sites/channel (upstream and downstream), 4 randomly chosen sampling points (0.53 0.5-m quadrats)/site, and 2 sa0.5-mpling seasons (spring and su0.5-m0.5-mer). Water physicoche0.5-mical and habitat variables were recorded when invertebrates were sampled. Environmental variables, including water conductance, [NH3-N], submerged vegetation cover, diversity of sediment grain size, and organic matter content of the sediment, were used to construct a synthetic variable describing the hydrological connectivity of each site with the main river channel. A quadratic regression of rarefied taxonomic richness and the connectivity gradient was not quite significant, but assemblage composition was strongly related to the gradient. Four of 8 trait-based metrics were correlated with the connectivity gradient. Values of metrics that are surrogates for top-down control of assemblage structure and habitat stability (based on functional feeding groups) declined along the gradient from disconnected sites to more connected sites. Values of metrics that are surrogates for voltinism and food supply for water-column-feeding fish increased with connectivity. Top-down control and voltinism surrogates suggested a decline in predator–prey relationships and lower habitat stability, respectively, in the more connected sites. Assemblage composition and some of the trait-based metrics were sensitive to a flood that occurred before one of the sampling dates. Some of the trait-based metrics showed potential for explaining floodplain invertebrate assemblages and for monitoring postrestoration conditions in floodplain water bodies. However, the metrics were developed initially for studies of lotic systems and their use in heterogeneous floodplain water bodies will require further investigation, e.g., delineation of reference conditions for trait-based metrics.
Key words: macroinvertebrates, lateral connectivity, richness, taxonomic composition, functional met-rics, floodplain ecology, Rhoˆne River.
Under natural conditions, the floodplain of a large river can contain the main river channel, secondary channels permanently connected to the main channel (eupotamal), channels connected to the main channel only at their downstream ends (parapotamal), discon-nected channels (plesiopotamal), abandoned meanders (paleopotamal), alluvial spring brooks, tributaries, and temporary wetlands. These water bodies can be arranged along a gradient of decreasing lateral
hydrological connectivity (permanent or episodic links between the main channel of a river and the various water bodies of its alluvial floodplain; Amoros et al.
1987). Lateral connectivity is difficult to measure directly in the field because it integrates various components, such as connection duration, hydraulic stress during flood events, and sediment scouring or deposition, and it can be confounded by local morphological features of the channels and the habitat structure.
Biogeochemical fluxes, biota, and food webs are strongly influenced by the degree of hydrological connectivity between the various types of surface and
1E-mail addresses: amael.paillex@leba.unige.ch
2emmanuel.castella@leba.unige.ch
3gilles.carron@leba.unige.ch
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ground water (Rostan et al. 1987, Tockner et al. 1999a, Amoros and Bornette 2002, Karaus 2004), and lateral connectivity also is responsible for the diversity pattern of floodplain aquatic invertebrates (Castella et al. 1984, Tockner et al. 1999b, Amoros and Bornette 2002, Arscott et al. 2005). Castella et al. (1984) showed that each type of channel in a European floodplain can exhibit distinctive communities of macroinvertebrates, mostly as a consequence of the morphological and hydrological characteristics of the channels. Tockner et al. (1999b) showed that a series of overlapping species richness maxima for different groups of macroinverte-brates was a result of hydrological connectivity across a floodplain. Reckendorfer et al. (2006) observed that the number of mollusc species peaked at a low level of hydrological connectivity. However, few studies have investigated the response of the full macroinvertebrate community to a gradient of lateral connectivity.
Studies incorporating the biological or ecological traits of benthic invertebrate species have been widely developed in Europe (e.g., Statzner et al. 1994, Dole´dec et al. 1999, Usseglio-Polatera et al. 2000, Gayraud et al.
2003). They are based upon the assumption that, depending on the habitat characteristics, variations in trait composition have the potential to indicate processes acting at the ecosystem level and structuring macroinvertebrate assemblages (Lamouroux et al.
2004). The trait approach has the advantages of circumventing taxonomic and biogeographic varia-tions and allowing comparisons across environmental conditions. Several authors also demonstrated that specific combinations of trait profiles could be related to the intensity and nature of river degradations or stressors (Usseglio-Polatera et al. 2000, Archaimbault 2003, Dole´dec et al. 2006). Merritt et al. (2002) proposed several functional-group metrics as surro-gates to assess ecological functions in remnant oxbows in southwest Florida. These metrics had their origin in the long-established use of functional feeding groups in running waters (Cummins and Klug 1979) and were based upon ratios of numbers of individuals belonging to biological or ecological groupings, such as func-tional feeding groups, modes of attachment to the substrate and locomotion, life-history patterns, and drift propensity. The metrics provide information about the type of organic matter, the physical stability of the habitat, and the availability of invertebrates to higher trophic levels. To our knowledge, our work is the only case of application of such trait-based metrics to the assessment of floodplain aquatic biotopes, of which one salient feature is a sharp gradient in hydraulic conditions from permanently flowing side channels to stagnant, disconnected cut-off channels (Amoros and Petts 1993, Cummins et al. 2005).
Statzner et al. (1994) tested the congruence between the distribution of species traits in the Upper-Rhoˆne River and expectations derived from a habitat templet for river systems (Townsend and Hildrew 1994).
However, this attempt had no direct implications for the assessment of floodplain condition. Reckendorfer et al. (2006) showed linkage between a hydrological connectivity gradient and variations in the trait composition of mollusc assemblages. Species domi-nating in isolated sites were characterized by a higher resistance to desiccation, a preference for higher plants as food, and a preference for less shaded habitats.
Various forms of river regulation have disrupted hydrological connectivity in many of the world’s rivers by modifying the natural disturbance regimes that maintained a level of connectivity across the floodplain landscape. Reduction in river dynamics also has caused fragmentation of the river continuum and enhancement of floodplain terrestrialization. Reconnection and reju-venation of cut-off channels as a means to restore more natural hydrological conditions have become a central purpose of river restoration projects (Schiemer et al.
1999, Amoros 2001). Macroinvertebrate assemblages and, more precisely, changes in their richness, compo-sition, and traits have been used to assess the prerestoration condition of ecosystems and the efficien-cy of hydrological and ecological restoration measures (Schiemer et al. 1999, Merritt et al. 2002). Understanding relationships between hydrological connectivity and various biodiversity metrics clearly is needed to monitor the alterations of riverine floodplain biota induced by river regulation and to formulate sound restoration recommendations. However, few studies have compared the sensitivity of various biotic metrics to hydrological connectivity and its alterations.
The goal of our study of benthic macroinvertebrate assemblages in the Rhoˆne River floodplain was to compare the responses along a gradient of lateral connectivity of: 1) taxonomic richness, 2) taxonomic composition, and 3) a set of functional trait-based metrics proposed by Merritt et al. (2002) as surrogates for ecosystem processes. We hypothesized that all 3 groups of metrics would react to the connectivity gradient. In accordance with the intermediate distur-bance hypothesis (IDH) (Connell 1978), we expected taxonomic richness to be at a maximum for an intermediate level of connectivity. Along the lateral dimension of the floodplain, high connectivity with the main channel implies frequent and intense disturbance by floods, leading to reduced species richness (Town-send et al. 1997b). Richness also is expected to be low at the other end of the connectivity gradient, where flood disturbance is extremely reduced or absent, because of the dominance of competitively superior
taxa (Townsend et al. 1997b). Early studies of floodplain water bodies recognized the role of con-nectivity with the river in shaping the composition of zoobenthic assemblages, either at the single-channel scale (Richardot-Coulet et al. 1983) or at the sector scale (Castella et al. 1984). Therefore, we also expected that changes in lateral connectivity would be reflected in changes in taxonomic composition.
Last, we considered that the trait-based metrics used by Merritt et al. (2002) in a riparian marsh system could be applicable to a mid-European floodplain and made predictions for each surrogate; we assumed that each trait-based metric is indicative of an ecosystem attribute. In accordance with the river continuum concept (Vannote et al. 1980) and its transposition to the floodplain lateral dimension (Amoros and Petts 1993), we predicted that an increase in connectivity with the main river channel would be detected as a decrease of macroinvertebrates feeding upon coarse particulate organic matter and an augmentation of those feeding upon transported organic matter (surro-gate metrics: shredder ratio and collector ratio, respectively; Table 1). In lotic environments, predators tend to be late settlers after a disturbance (Mackay 1992); therefore, we predicted that an increase in connectivity with the main river channel would be detected as a decline in the top-down control of predators on prey (surrogate metric: predator ratio;
Table 1). In accordance with the IDH (Connell 1978), we predicted that communities in unstable habitats (i.e., with high connectivity) would be dominated by efficient colonizers like plurivoltine species (surrogate metric: voltinism ratio; Table 1). We expected prey availability to be higher in habitats with low structural complexity (Heck and Crowder 1991). As a conse-quence, we predicted that an increase in connectivity with the main river channel would be detected as an increase of the macroinvertebrates representing a food supply to higher trophic levels, such as fish (surrogate metrics: drifter ratio and benthic ratio; Table 1). In accordance with the spatiotemporal habitat templet of Townsend and Hildrew (1994), we predicted that an increase in connectivity with the main river channel would be detected as a decline of macroinvertebrates requiring stable surfaces for feeding and attachment (surrogate metrics: functional feeding group [FFG]
ratio and functional habit group [FHG] ratio, respec-tively; Table 1).
Methods Study sector
The French Rhoˆne River is 522 km long and drains 90,630 km2 from the Swiss border to the
Mediterra-nean Sea (Bravard 1987). The Rhoˆne River biota is typical of a mid-European river, comparable to the Rhine and the Danube (Roux et al. 1989). In the study sector located near the town of Belley, the Rhoˆne River had a braided pattern and an average annual discharge of 430 m3/s. The river system was strongly influenced by the construction of embankments to facilitate navigation at the end of the 19thcentury and later by the construction of a hydroelectric power plant that was completed in 1982 and diverts a part of the main flow into a head-race canal parallel to the old riverbed (Fig. 1) (Dessaix et al. 1995, Dole´dec et al.
1996). The by-passed river sustains nearly natural geomorphologic conditions and receives a minimum base flow of 25 m3/s from December to March, 28 m3/ s from April to June and from October to November, and 60 m3/s from July to September. Discharge into the by-passed section increases during floods, when the capacity of the head-race canal is exceeded.
The study was done in 6 cut-off channels (BEAR, MOIR, LUIS, ENIL, FOUR, and LUCE) along the by-passed section and 1 cut-off channel (CHAN) down-stream of the junction of the tail-race and the by-passed section (Fig. 1, Table 2). The 7 channels are braided and belong to the parapotamal type defined by Amoros et al. (1982), i.e., they remain permanently connected with the main river channel at their downstream end. During periods of average water levels, the upstream sections of the channels are disconnected from the main river channel and are composed of isolated, mostly groundwater-fed pools.
CHAN has lateral permanent connections with the Rhoˆne and, therefore, a more lotic character in its downstream section. LUCE has a permanent connec-tion with the Rhoˆne and permanent flow from the upstream to the downstream part of the cut-off channel. During periods of high water levels, the 7 channels can become connected to the main river channel at their upstream ends. Flood scouring is sufficient to maintain gravel- and pebble-dominated substrate and a relatively low hydrophyte cover (Table 2).
Sampling design
Two sites were sampled in each cut-off channel: one upstream (up), usually in an isolated pool, and one downstream (do), close to the connection with the main river channel. These sites represented the 2 extremes of the habitat conditions classically described for such parapotamal cut-off channels (Amoros 1980, Richardot-Coulet et al. 1983). In each site, 4 sampling quadrats, delimited by a 0.530.5-m metal frame, were randomly chosen along a 30-m stretch. Prior to
TABLE1.Metricsbaseduponinvertebratefunctionalgroupsthatwereusedassurrogatesofecosystemattributes(adaptedfromMerrittetal.2002)andtheir predictedresponsealongagradientofincreasinglateralconnectivitywiththemainriver.FFG¼functionalfeedinggroup,FHG¼functionalhabitgroup,CPOM¼ coarseparticulateorganicmatter,FPOM¼fineparticulateorganicmatter. Functionalgroupratios(metrics)TermusedintextEcosystemattribute
Termusedfor ecosystemattribute intextPredictedresponse ofthemetric Shredders/totalcollectorsShredderratioRatioofCPOMtoFPOMCPOM/FPOMDecrease Filteringcollectors/gatheringcollectorsCollectorratioRatioofFPOMintransport(suspended) toFPOMstoredinsediments (depositedinbenthos)
TFPOM/BFPOMIncrease Predators/totalallotherFFGsPredatorratioTop-downcontrolofinvertebrate predatorsonpreyTop-downcontrolDecrease Plurivoltine/(univoltineþsemivoltine)VoltinismratioShortlifecyclevslonglifecycle;capacity ofacommunitytoreachmaturity quickly
VoltinismIncrease Behavioraldrifters/accidentaldriftersDrifterratioPredictablefoodsupplyforwater-column- feedingfishDriftingfoodIncrease Sprawlers/(clingersþclimbersþ burrowersþswimmers)BenthicratioPredictablefoodsupplyforhigher trophiclevels,suchaswadingbirds andbenthic-feedingfish BenthicfoodIncrease (Scrapersþfilteringcollectors)/ (shreddersþgatheringcollectors)FFGratioAvailabilityofstablesurfacesand nonshiftingsedimentsforfeeding,based onfunctionalfeedinggroup(FFG)
FFGhabitatstabilityDecrease (Clingersþclimbers)/(burrowersþ sprawlersþswimmers)FHGratioAvailabilityofstablesurfacesand nonshiftingsedimentsforattachment, basedonfunctionalhabitgroup(FHG)
FHGhabitatstabilityDecrease
invertebrate sampling, habitat characteristics were recorded at the quadrat and site levels. Water specific conductance (lS/cm) was measured using a portable conductivity meter in each quadrat (WTW 330i;
Wissenschaftlich-Technische Werksta¨tten, Weilheim, Germany). The cover of each of 4 sediment categories (silt and clay, sand, gravel, pebble and larger) and vegetation was assessed in each quadrat. Cover was quantified as: 0 (absence of cover), 1 (0–5%), 2 (5–25%), 3 (25–50%), 4 (50–75%), or 5 (75–100%). One water sample was collected in winter at each site to measure
the concentration of NH3-N (method according to HACH, Loveland, Colorado). At the same time, the benthic particulate organic matter (BPOM) in the sediment was quantified according to Rostan et al.
(1987). A corer was used to take a sediment sample of 28 cm2 3 5 cm depth. Organic matter content was determined by combusting the material at 5608C for 90 min. Macroinvertebrates were sampled as completely as possible in each quadrat with a hand net (opening:
14.53 9.5 cm, mesh size: 500 lm) and preserved in 70% ethanol. Sampling was repeated in summer (July 2003 for all sites except CHAN [July 2004]) and spring (April 2004) to account for invertebrate seasonality.
The 112 individual samples were sorted, and inverte-brates were identified in the laboratory to the finest taxonomic level possible (usually genus or species) depending on the size of the individuals. Diptera were identified to family level, and Oligochaeta, Turbellaria, and Hydrachnidia were not identified further.
Data analysis
Connectivity gradient.—Water levels were not moni-tored continuously in the cut-off channels, and the duration and intensity of the actual hydrological connection (i.e., drag forces) between the cut-off channels and the main river channel were not known.
Moreover, the simple distance between a site and the river does not reflect connectivity. For example, 19th -century embankments can decrease the connection frequency of sites that are close to the river. Therefore, surrogate variables were used to describe the lateral connectivity gradient in an approach similar to those of Townsend et al. (1997a), Burgherr et al. (2002), or Ilg and Castella (2006). Five environmental variables known to integrate the level of connectivity of the floodplain sites with the main river channel were used.
Three variables were expected to decrease with increasing hydrological connectivity: water conduc-tance (Carrel 1986, Cellot et al. 1994), organic content of the sediment upper layer (Rostan et al. 1987), and average cover by aquatic vegetation (Chambers et al.
1991, Amoros et al. 2005). Two variables were expected to increase: diversity of the sediment grain size measured with a Simpson index and NH3-N concen-tration (Cellot et al. 1994, Amoros and Bornette 2002).
The 5 connectivity variables were summarized with a centered principal component analysis (PCA) with the goal of producing synthetic variables (the factorial axes) that could be used as surrogates for the level of connectivity between the main river channel and the cut-off channels.
Relationships between the connectivity gradient and the macroinvertebrate metrics (density, macroinverte-FIG. 1. A.—Europe, with a focus on the study area
(France). B.—Locations of the 7 cut-off channels in the sector of Belley. The 7 cut-off channels studied are indicated by their codes (see Table 2). Empty circles represent the sampling sites.
brate composition, and functional diversity) were investigated using regression analyses. The relation-ships between functional metrics and the connectivity gradient were explored using 1st-order linear regres-sions followed by quadratic or exponential regression models. Quadratic models were tested for the metrics that were predicted to increase or peak along the gradient of connectivity. Negative exponential models were tested for the metrics that were predicted to decrease along the gradient of connectivity. For each metric, the model with the highest significant coeffi-cient of determination (R2) was selected. Bonferroni-adjusted probabilities were applied to account for multiple tests, and thea-value was reduced to account for the number of tests being done (2 regressions/
metric). Ifpa/n(a¼0.05;n¼2), the observed effect was considered statistically significant, the null hy-pothesis was rejected, and the alternative hyhy-pothesis validated. Analysis of covariance (ANCOVA) was used to test whether the intercept of the relationship between the metrics and the connectivity gradient differed between seasons (season effect) or the slope of the relationship differed between seasons (connectivity 3season effect).
Invertebrate density and taxonomic richness.—Inverte-brate density was expressed as ind./m2and calculated as an average per site based on 4 samples (except MOIR-up in spring, wheren¼3). Taxonomic richness per site or per channel and the associated standard errors were based on the 4 samples/site or 8 samples/
channel pooled together (except MOIR-up in spring) and calculated by rarefaction (Hurlbert 1971, Heck et al. 1975) using 1000 draws in the Vegan function package (Vegan, version 1.6–10. Available from:
http://cc.oulu.fi/;jarioksa/) for the R statistical free-ware (Ihaka and Gentleman 1996). Invertebrate densi-ty and rarefied richness per channel were calculated from the 2 sites pooled per channel. We used 2-sided paired Wilcoxon tests to assess differences in
inverte-brate density and taxonomic richness between sites, channels, and seasons.
Macroinvertebrate composition.—Densities were log(x þ1)-transformed prior to analyses, and only those taxa represented by .2 individuals in all samples com-bined were used. We used between-class correspon-dence analysis (bCA) (Dole´dec and Chessel 1989) to compare the taxonomic composition of the cut-off channel and site assemblages. bCA is an ordination technique in which the variables of interest (in our case, the table containing the abundance of each taxon per sample) are linked to a categorical variable grouping the observations into classes (the sites or cut-off channels). Between-class ordinations are a special case of constrained ordination methods in which the constraining variable is categorical, not continuous. Therefore, bCA ordinates sites under the constraint that the ordination maximally separates sites in the various classes of the constraining variable (Chessel et al. 2004, Baty et al. 2006). This technique is similar to methods known under various names, including partial canonical correspondence analysis, discriminant analysis, and redundancy analysis (ter Braak and Prentice 1988, Legendre and Legendre 1998, Dray et al. 2003). Sabatier et al. (1989) and Lebreton et al. (1991) highlighted the mathematical unity of these techniques and proposed to group them under the name PCA with instrumental variables, following the original description by Rao (1964). Graphical outputs
Macroinvertebrate composition.—Densities were log(x þ1)-transformed prior to analyses, and only those taxa represented by .2 individuals in all samples com-bined were used. We used between-class correspon-dence analysis (bCA) (Dole´dec and Chessel 1989) to compare the taxonomic composition of the cut-off channel and site assemblages. bCA is an ordination technique in which the variables of interest (in our case, the table containing the abundance of each taxon per sample) are linked to a categorical variable grouping the observations into classes (the sites or cut-off channels). Between-class ordinations are a special case of constrained ordination methods in which the constraining variable is categorical, not continuous. Therefore, bCA ordinates sites under the constraint that the ordination maximally separates sites in the various classes of the constraining variable (Chessel et al. 2004, Baty et al. 2006). This technique is similar to methods known under various names, including partial canonical correspondence analysis, discriminant analysis, and redundancy analysis (ter Braak and Prentice 1988, Legendre and Legendre 1998, Dray et al. 2003). Sabatier et al. (1989) and Lebreton et al. (1991) highlighted the mathematical unity of these techniques and proposed to group them under the name PCA with instrumental variables, following the original description by Rao (1964). Graphical outputs