Aquat. Sci. (2009) 71:389398 DOI 10.

1007/s00027-009-0109-z

Aquatic Sciences

RESEARCH ARTICLE

The role of an extreme ood disturbance on macrophyte assemblages in a Neotropical oodplain

Andre Andrian Padial Priscilla Carvalho Sidinei Magela Thomaz Solana Meneghel Boschilia Roberta Becker Rodrigues Josilaine Taeco Kobayashi

Received: 8 January 2009 / Accepted: 10 June 2009 / Published online: 23 July 2009 Birkhauser Verlag, Basel/Switzerland 2009

Abstract Aquatic macrophytes produce large amounts of organic matter and have an essential structuring role in oodplains. This process highlights the importance of this community to aquatic biodiversity maintenance. We investigated the role of a ood disturbance on the response of macrophyte assemblages in regional and local structur ing in the Upper Parana River oodplain. Plant species were recorded before (November 2006) and after (March 2007) an uncommon increase in water level caused by the o El Nin South Oscillation, which is considered a disturbance. Samples were taken in lakes and backwaters located in the oodplain and connected to three distinct rivers (that differentiate three sub-systems). Species richness and the assemblage structure of macrophyte patches underwent signicant changes after the ood disturbance, depending on the specic sub-system (rivers) to which the lakes were connected. In addition, ood disturbance had a strong impact on community organization at the local scale.

However, regionalization with respect to sub-systems remained signicant after the ood disturbance. Our results emphasize the importance of connection to the river on macrophyte community composition and richness, and suggest that ood events in the Upper Parana River oodplain disrupt community organization only at ne (local) scales. Keywords Macrophyte community Flood disturbance Depth gradient River connection Classication strength Upper Parana River oodplain

Introduction Aquatic macrophytes are key components of inland waters because they affect nutrient cycling, produce great amounts of organic matter (Wetzel 2001; Lopes et al. 2007) and contribute to enhancing habitat complexity (Dibble et al. 2006), which increases freshwater biodiversity (Bonecker et al. 1998; Pelicice et al. 2008). These attributes highlight the positive effects that several types of wetlands (including river-oodplain systems), which are highly colonized by macrophytes, have on biodiversity conservation. Different types of macrophytes (i.e. submersed, emergent, free-oating leaved, rooted with oating leaves and free-submersed) usually colonize the same aquatic ecosystem simultaneously. These life forms are affected differently by ood disturbances (van Geest et al. 2005a) and the degree of connectivity in river oodplain systems (Bornette et al. 1994). They are also organized differently along depth gradients within littoral regions (Sculthorpe 1967). Such gradients (or zonation patterns) have been widely described in lakes where the water level is almost constant (Sculthorpe 1967; Wetzel 2001). However,

A. A. Padial Departamento de Biologia Geral, Instituto de Ciencia Biologicas, Universidade Federal de Goias, PO Box 131, Goiania, GO CEP 74001-970, Brazil e-mail: aapadial@gmail.com P. Carvalho S. M. Thomaz (&) R. B. Rodrigues J. T. Kobayashi Nucleo de Pesquisa em Limnologia, Ictiologia e Aquicultura (Nupelia), Universidade Estadual de Maringa, Maringa, PR CEP 87020-900, Brazil e-mail: smthomaz@gmail.com S. M. Boschilia Departamento de Ecologia, Instituto de Biociencias, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS CEP 91.501-970, Brazil e-mail: solbos@gmail.com

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knowledge about depth gradients in more dynamic ecosystems in which water levels uctuate over time is scarce. Depth gradient is important in organizing macrophyte assemblages at local, more restricted scales, but there are several other factors that become more important at larger spatial scales (Lougheed et al. 2001; Baattrup-Pedersen et al. 2006; Lacoul and Freedman 2006). It has been shown that aquatic vegetation richness, composition and abundance in oodplain lakes are affected by several abiotic factors, such as inundation duration, drawdown area and a lakes age and morphometry (van Geest et al. 2003, 2005a, b). These factors interact and their effects should not be viewed separately (van Geest et al. 2003). However, except for lakes not inundated during the growing season (van Geest et al. 2003), the hydrological regime is considered to be the main driving force that determines the structure of several types of aquatic assemblages (Junk et al. 1989; Neiff 1990; Ilg et al. 2008), including macrophyte assemblages (Bornette et al. 1994, 2001; Reid and Quinn 2004; Maltchik et al. 2007; Strausz and Janauer 2007). Vegetation response to oods basically results from nutrient and propagule inputs, scouring effects, suspended matter inputs and depositional processes (Bornette et al. 2008). In conjunction, these factors select specic plant strategies, depending on ood frequency and intensity. For example, plants with opportunistic strategies, such as vegetative reproduction and water dispersal (which increases the opportunity for propagules to reach gaps after a disturbance) are selected in more disturbed habitats within a oodplain (Bornette et al. 2008). Aside from the abovementioned determinants associated with the hydro-regime, the degree of connectivity among oodplain habitats also affects the structure of biotic assemblages (Bornette et al. 1994; Tockner et al. 1999, 2000a; Ward et al. 2002; Thomaz et al. 2007). In a mosaic of lakes connected to different rivers (typical for Neotropical oodplains), those connected to the same river usually share the same source of propagules, have similar limnological features and are located close to each other. Thus, it is expected that lakes connected to the same river have similar macrophyte assemblages (Bini et al. 2001; Thomaz et al. 2004a). Many wetlands in Neotropical regions have been destroyed or are facing severe threats (Agostinho et al. 2004, 2005; Rolon and Maltchik 2006). Moreover, few studies have tried to understand wetland biodiversity and the determinants of community structure in large spatial areas in Neotropical regions (Agostinho et al. 2004; Rolon and Maltchik 2006). The Upper Parana River oodplain is an important area for biodiversity conservation. It has some seasonality in its hydrological regime (with rainy summers, when water levels are usually higher, and dry winters, with predominantly lower water levels), which is considered the

main driving force that determines its limnological features on a large spatial scale (Thomaz et al. 2004b). In addition, oods increase similarity among aquatic habitats in riveroodplain systems (Tockner et al. 2000b; Thomaz et al. 2007), particularly in the Upper Parana River oodplain (Thomaz et al. 2004b). Therefore, the ooding regime may have an important role in structuring macrophyte assemblages in this oodplain. In this study, we identied the role of ood disturbance on macrophyte species richness, assemblage structures, zonation patterns and regional organization in the Upper Parana River oodplain. We hypothesized that ood disturbance affects (i) the species richness, assemblage structure and zonation patterns of macrophytes across different sub-systems, and (ii) the regional classication of macrophytes from different sub-systems of the Upper Pa rana River oodplain. As a consequence of (i), we predicted that the species richness and assemblage structure of macrophyte patches will vary depending on the subsystem considered and zonation patterns will be disrupted after the ood. As a consequence of (ii), we predicted that macrophyte assemblages in patches connected to different rivers will become more similar to one another after the ood. To test these hypotheses, we used data collected before and after an extreme ood (with high intensity and o long duration) caused by El Nin South Oscillation in 20062007 in different sub-systems of the Upper Parana River oodplain.

Materials and methods Study area The Upper Parana River and its oodplain (Fig. 1) represent the last stretch of this river that still remains undammed in the Brazilian territory. Several studies have suggested that three distinct sub-systems can be differentiated in this oodplain, considering both biological and limnological features (see Thomaz et al. 2004a, b). These sub-systems are composed of isolated and connected lakes, backwaters and channels that are directly or indirectly connected to three different rivers: the Parana (the main river in this oodplain) and the Ivinheima and Baa Rivers, which drain into the oodplain (see Thomaz et al. 2004b). Upstream from the Upper Parana River oodplain, there is a reservoir cascade that caused profound alterations of the ooding regime, diminishing ood magnitude but increasing ood pulse frequency (Souza Filho et al. 2004). In fact, damming is one of the main anthropogenic impacts on oodplains (Agostinho et al. 2005). However, an uncommon increase in the water level, caused by the El o Nin South Oscillation, occurred in January-February 2007

Flood disturbance and Neotropical macrophytes Fig. 1 The Upper Parana River oodplain, showing the three main sub-systems consisting of the Parana, Ivinheima and Baa Rivers

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(Fig. 2). Long-term data obtained over 34 years (1964 1998) show that oods of similar intensity to the one recorded in our survey, reaching water levels of ca. 600 cm at the gauge of our eld station, for a period of at least 2 months, occurred in the years of 1964, 1965, 1977 and 1980. However, other big oods (600700 cm) with shorter durations (ca. 0.52 months) occurred 16 times in this same period, at irregular intervals. The extreme ood observed in 20062007 was a unique opportunity to evaluate the effects of this type of ood on aquatic macrophyte community stability in the Upper Parana River oodplain.

Data sampling Samples were taken in November 2006 and March 2007 (before and after the ood disturbance; see Fig. 2). Water levels in both sampling periods were similar (Fig. 2). Therefore, we considered that there was no differential effect of depth upon macrophyte assemblages between sampling periods. November represented the end of the low water period. At this time, macrophytes had experienced a long period without oods (ca. 8 months), which made possible a self-organization of these assemblages in oodplain lakes through intra and inter-specic interactions (Neiff 1979; Thomaz et al. 2007). In March 2007, after the ood disturbance, macrophyte patches began recovering their lost biomass from the ood. The richness and composition of macrophyte assemblages of connected lakes, like the ones investigated here, are relatively stable over time, as shown in a long-term study carried out for 6 years in this oodplain (Thomaz et al. 2009). Thus, we suppose that differences before and after the extreme ood could be attributed to a disturbance caused by this specic ood. Macrophytes were surveyed in six lakes connected to the Ivinheima River, ve to the Baa River, ve backwaters and one lake connected to the Parana River. Since backwaters are similar to connected lakes (only differing by having a higher connection with the rivers main channel) and to facilitate communication, we will consider all habitats as lakes from now on. In each lake, we chose from one to four patches of macrophytes and in each patch

Fig. 2 Water level of the Upper Parana River oodplain obtained for the gauge at the University of Maringa Field Station. Solid arrows indicate the two macrophyte surveys, while the dashed arrow indicates the extreme ood recorded in January 2007

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we recorded all species within a 1 m2 quadrat close to the shore (herein shallower quadrat) and another one closer to the limnetic region (herein deeper quadrat). Larger environments, which had more macrophyte patches, required more surveys. When necessary, submersed species were sampled with a rake held by a four-meter long pipe. The objective of using shallower and deeper quadrats was to analyze the effect of ooding on local macrophyte organization (i.e. the zonation pattern, considering the depth gradient of macrophyte species). For other purposes, we used the presence of macrophytes recorded in shallower plus deeper quadrats (herein considered a macrophyte patch) as replicates. A total of 92 macrophyte patches (40 in Ivinheima River, 25 in Baa River and 27 in Parana River) were analyzed in each period (November 2006 and March 2007). We always surveyed the same location in both periods. Since we had a small number of patches per lake (210), we used them (but not lakes) as replicates to compare different sub-systems. Data analysis A factorial ANOVA was applied to assess the effects of ood disturbance and river connection on the species richness of macrophyte patches from different rivers, as well as their interactions. For that, we used the species richness recorded in macrophyte patches as replicates. This analysis indicates whether the ood event and/or sub-system affects macrophyte species richness in each patch. A detrended correspondence analysis (DCA), applied to presence/absence data recorded in the patches of macrophytes, was used to summarize biological data (Hill and Gauch 1980). In ordination, we downweighted rare species and reported the k values (eigenvalues) of each axis on the graphs. Three ordinations were done in order to visualize assemblage structures, using total species composition collected before and after the ood disturbance in patches of each sub-system. For this analysis, we used PC-Ord software, version 4.1 (McCune and Mefford 1999). To test the effect of ooding on zonation patterns, the classication strength (CS) was calculated using shallower and deeper quadrats as the two classes (i.e. zonation patterns), with data from lakes connected to the same river (i.e. belonging to the same sub-system). This technique, based on the mean similarity approach, allowed one to measure the strength of an a priori classication scheme (see van Sickle and Hughes 2000; Heino and Mykra 2006). CS is calculated as the difference between the mean of all within-class similarities (W) and mean between-class similarity (B) (CS = W - B). Large values of CS thus indicate strong classication (high within-class and low between-class similarity). For that, we used Jaccards similarity coefcients to construct a similarity matrix. We

carried out these analyses before and after the disturbance to evaluate the disturbances role on local organization, using only the species composition recorded within the shallower or deeper quadrats. If a local organization is found before the ood, but not after, zonation patterns are disrupted by ood disturbance. At a regional (broader) scale, we considered that patches connected to each one of the three rivers belonged to three different classes: patches from Baa, Ivinheima and Parana Rivers (i.e. three different sub-systems sensu Bini et al. 2001; Thomaz et al. 2004a, b). Again, two analyses were carried out: before and after the ood disturbance using the total species composition of macrophyte patches (i.e. the species composition recorded in shallower and deeper quadrats). If regionalization is signicant before the ood and no longer signicant after the ood, then patches connected to different rivers are more similar among each other after the ood. The signicance of CS was determined after 1,000 random permutations of the data. We used the free-software R-project (R Development Core Team 2007) for these analyses. For all analyses, signicant values were considered when the type I error was less than 0.01. Graphs were done in STATISTICA software (Statsoft 2005).

Results A total of 42 species of aquatic macrophytes were recorded in November 2006 (25, 33 and 21 species at the Ivinheima, Baa and Parana River habitats, respectively). The most frequent species were Eichhornia azurea, Salvinia auriculata, Salvinia minima, Oxycaryum cubense and Eichhornia crassipes (Fig. 3). The less frequent species were Pistia stratiotes, Ludwigia cf. decurrens, Commelina sp., Cyperus giganteus and Potamogeton cf. pusillus. In March 2007, after the ood disturbance, 38 species of aquatic macrophytes were recorded (21, 33 and 21 species in the Ivinheima, Baa and Parana River habitats, respectively). The most frequent species were E. azurea, S. auriculata, E. crassipes, S. minima and O. cubense. Despite the ood disturbance, the frequency of occurrence of most species was roughly similar between both months (Fig. 3). However, some species such as Egeria najas and Cabomba furcata became almost extinct locally after the ood (Fig. 3). Two-way ANOVA showed a signicant effect of river (F = 13.34; P \ 0.001) and period (F = 22.48; P \ 0.001) on species richness per patch and a signicant interaction between both variables (F = 62.56; P \ 0.001) (Fig. 4). Species richness per patch varied across the habitats of each river depending on the period (before and after the ood disturbance). In fact, the highest mean

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Fig. 3 Frequency of occurrence of species recorded before (November 2006) and after (March 2007) the disturbance by a severe ood. BAC = Bacopa sp.; CAB = Cabomba furcata; ECA = Eichhornia azurea; ECC = Eichhornia crassipes; EGN = Egeria najas; ELO = Eleocharis sp.; HYD = Hydrilla verticillata; LMB = Limnobium laevigatum; LWP = Ludwigia peruviana, LWT = Ludwigia cf. decurrens; NYM = Nymphaea amazonum; OXC = Oxycaryum cubense; PIS = Pistia stratiotes; PLF = Polygonum ferrugineum; PLH = Polygonum hydropiperoides; PLM = Polygonum meisnerianum; PLS = Polygonum stelligerum; PSR = Paspalum repens; RCC = Ricciocarpus natans; SAU = Salvinia auriculata; SHZ = Salvinia herzogii; SMN = Salvinia minima; UTF = Utricularia foliosa; UTG = Utricularia gibba; WSP = Wolfella sp.

species richness per patch was found at the Ivinheima River before the ood disturbance (mean = 6.5 species per patch) and at the Baa River lakes after the ood disturbance (mean = 10 species per patch) (Fig. 4). Ordinations summarized the major patterns of the species of patches connected to the same river before and after the ood disturbance (Fig. 5). Patches connected to the Ivinheima River were not clearly separated between sampling periods (Fig. 5a), whereas those connected to the Baa and Parana rivers were clearly separated before and

after the ood (Fig. 5b, c). Patches from the Baa River lakes were characterized by a mix of different life forms in both periods, such as Najas sp. (rooted submersed) and Echinodorus grandiorus (emergent) before the ood and Lemna sp. (free-oating) and Cyperus giganteus (emer gent) after the ood (Fig. 5b). In the Parana River, patches were dominated mainly by submersed species (e.g., Egeria densa and Hydrilla verticillata) before the ood disturbance and by emergent and amphibian species (e.g., Pontederia cordata and Limnobium laevigatum) after the ood (Fig. 5c). DCA also clearly showed that patches in the Baa and Parana Rivers were more similar among each other after the ood, as indicated by a low dispersion of scores along axis 1 in this sampling period. Considering patches connected to the Ivinheima River, CSs based on quadrat depth (as a surrogate for local macrophyte organization along a depth gradient) were signicant and similar between periods (Table 1). On the other hand, CSs at this local scale substantially decreased in those patches that were connected to the Baa and Parana Rivers between periods, presenting low and non-signicant values after the ood disturbance (Table 1). This shows that local organization was disrupted after the ood only in these two rivers. Therefore, the ood homogenized macrophyte assemblages of shallower and deeper quadrats in both the Baa and Parana River patches, whereas, the local organization of macrophytes in the Ivinheima River patches was independent of the ood disturbance. Classication strengths based on a regional perspective (i.e. considering rivers in which patches were connected as classes) were signicant (but weak) both before and after the ood disturbance (Table 1). This shows that intragroup similarity (i.e. the mean similarity of patches from the same river) is considerably higher than inter-group similarity (i.e. the mean similarity of patches from different rivers). Therefore, patches can be classied according to the sub-systems described here. In addition, CS values were similar between periods (Table 1), indicating that the strength of this classication is independent of ood disturbance.

Discussion The number of species recorded in this survey (a total of 42 taxa) is ca. 66% of the total species richness recorded for the Upper Parana oodplain (Thomaz et al. 2004a). This low number of species can be explained by the reduced sampling effort, since samplings in previous surveys were carried out at longer time periods (ca. 5 years) and in other habitats not surveyed here, such as the river main channel and isolated lakes (Souza et al. 2002). However, an important feature of our survey as compared with those

Fig. 4 Mean (SE) species richness per patch measured before (November 2006) and after (March 2007) the ood disturbance in the lakes connected to the Ivinheima, Baa and Parana rivers. Shared letters show similar values according to the Tukey post-hoc test

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A. A. Padial et al. Table 1 Results of classication strengths: the mean intra-group similarities (W), the mean inter-group similarity (B) and the classication strengths (CS: W - B) of the two classication schemes (quadrat depth and rivers in which lagoons are connected) before (b.f.) and after ooding (a.f.) Classication scheme Ivinheima River Quadrat depth b.f. Quadrat depth a.f. Baa River Quadrat depth b.f. Quadrat depth a.f. Parana River Quadrat depth b.f. Quadrat depth a.f. Regionalization Rivers b.f. Rivers a.f. 0.289 0.263 0.276 0.252 0.150 0.284 0.258 0.321 0.225 0.180 0.075 0.224 0.094 0.283 0.179 0.228 0.064 0.083 0.201 0.028 0.056 0.001 0.079 0.093 <0.001 <0.001 <0.001 0.019 NS <0.001 0.398 NS <0.001 <0.001 W B CS p

Bold face numbers indicate signicant values. NS non-signicant CS values

Fig. 5 Score distributions of patches connected to the Ivinheima River (a), Baa River (b) and Parana River (c), along the rst two DCA axes before (BF) and after (AF) the ood disturbance. ALT = Alternanthera sp.; AZO = Azolla sp.; CYG = Cyperus giganteus; ECG = Echinodorus grandiorus; EGD = Egeria densa; ELO = Eleocharis sp.; HYD = Hydrocotyle cf. ranunculoides; HYL = Hydrilla verticillata; LMB = Limnobium sp.; LMN = Lemna sp.; LWP = Ludwigia peruviana; LWT = Ludwigia sp.; NAJ = Najas sp.; PLA = Polygonum acuminatum; PLM = Polygonum meisnerianum; PLP = Polygonum punctatum; PLS = Polygonum stelligerum; PON = Pontederia cordata; RCC = Ricciocarpus natans; UTG = Utricularia gibba

carried out previously (Thomaz et al. 2004a) is the presence of Hydrilla verticillata. This species, native to Asia, was recorded for the rst time in June 2005 in the ood plain and it is spreading quickly, especially in the Parana River main channel and in its lateral channels (Thomaz et al. 2009). The water level regime and its associated abiotic characteristics (e.g., turbidity, ow and nutrients) is considered the main factor affecting macrophyte composition and diversity in oodplain habitats (e.g., Tockner et al. 2000b; Ward et al. 2002; Thomaz et al. 2004a; Maltchik et al. 2005, 2007; van Geest et al. 2005a). In fact, our results showed that the ood disturbance affected macrophyte species richness, assemblage structure and zonation patterns. The ood also increased the similarity of macrophyte assemblages at both coarser (among patches of sub-sys tems) and ner (different depths) scales in the Baa and Parana sub-systems, as shown by DCA and the classication analysis. The homogenization of biota is a pattern described in several other river oodplain systems (Thomaz et al. 2007). However, responses to the ood pulse depended on the sub-system that was examined (the Ivinheima, Baa or Parana River sub-system). There are several non-mutually exclusive reasons for this. First, these three rivers are conspicuously different in terms of their limnological features (Thomaz et al. 2004b), and thus macrophytes experience local driving forces in addition to the ood, which represents a regional driving force. Second, propagules from the upstream cascade of reservoirs reach habitats connected to the Parana and Baa rivers easier than

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those of the Ivinheima River, given that this last system is located downstream and its oodplain is more isolated from the Parana River main channel (see Fig. 1). The transport of propagules by river ow and the limnological features have been considered important determinants in the structure of macrophyte assemblages in backwaters (Bornette et al. 1998, 2001; van Geest et al. 2005a; Strausz and Janauer 2007). Third, lakes are less connected to the Baa and Ivinheima Rivers than the backwaters associated with the Parana River, which are directly connected to this river through their downstream ends. As mentioned, these habitats suffer from frequent water level uctuations (caused by upstream reservoirs), which may select different species from those colonizing lakes connected to the other two rivers. The patches of Ivinheima River lakes showed a slight decrease in species richness after the ood disturbance, despite not showing a substantial change in assemblage structure and local organization. The decrease in frequency of free-oating macrophytes (that are easily carried by oodwaters) can be one explanation for the decline in species richness. In fact, the preference of free-oating species for habitats with low water velocity has been demonstrated by others (e.g., Makkay et al. 2008). Moreover, given that water bodies in this sub-system have high turbidity and low transparency (Thomaz et al. 2004b, 2009), submersed macrophytes rarely colonize and develop, which reduces the successful colonization of propagules coming from reservoirs after a ood disturbance. Finally, the fact that the ood disturbance had no effect on the local organization of macrophytes in the Ivinheima River sub-system suggests that, by being localized far from the Parana River main channel (see Fig. 1), biological communities in this sub-system are less dependent on the ooding regime of this river. Distance from the main river has been considered important for the organization of communities in river-oodplain systems (Ward et al. 2002; Strausz and Janauer 2007).

As opposed to the patches from the Ivinheima lakes, those connected to the Baa River had a signicant increase in species richness per patch (see Fig. 4) and a conspicuous change in assemblage structure after ooding (see Fig. 5b). One reason for the increasing diversity and changing assemblage structure after the ood disturbance in the Baa River could be that periodic emersion may limit competitive exclusion of littoral vegetation, which promotes the local diversity of aquatic plant communities (Bornette et al. 2001; Ward et al. 2002; van Geest et al. 2005b). Moreover, all environments in the Upper Parana River oodplain (including habitats in the Baa River) are located immediately downstream from a reservoir cascade (Thomaz et al. 2004b). These reservoirs are highly colonized by macrophytes (Martins et al. 2005, 2008; Thomaz et al. 2009) and they represent a continuous source of propagules for lakes. Thus, species that are common in the reservoirs have a high chance of increasing their relative abundance after a ood, when local dominance within macrophyte patches is reduced. Finally, some mechanisms of facilitation can also occur in these environments that promote species richness, change assemblage structure and disrupt zonation patterns after a ood. For instance, free-oating species benet from the colonization of species such as Eichhornia azurea (which is highly resilient to ooding; Fig. 3), making the local environment more favorable by reducing water velocity (Boschilia et al. 2008). Nevertheless, relationships between species diversity and resilience in habitats in the Upper Parana River oodplain require further study. The common ood perturbations, together with nutrient poor waters of the Parana River (with a total P \10 lg/L; Thomaz et al. 2004b) may be reasons for the low species richness per patch in the Parana lakes (Fig. 4). In fact, most backwaters studied in this environment have a direct con nection to the main channel of the Parana River, enhancing the negative effect of any disturbance caused by ood pulses upon species richness. The excessive connectivity

Fig. 6 Theoretical framework showing the responsesand their probable causesof the macrophyte assemblages to the ood disturbance in the different rivers in the oodplain

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between backwaters and river channels was also pointed out as a possible reason for the low species richness of macrophytes in cut-offs of the Rhone River in France (Bornette et al. 1998). Despite not having an effect upon species richness, the signicant effect of the ood disturbance upon the assemblage structure of macrophytes is due, in part, to the disappearance of submersed species (Fig. 3), which were very common in the Parana lakes before the ooding (see Fig. 5c and Thomaz et al. 2004a), followed by the colonization of more resilient species. The probable causes of the disappearance of submersed species are increases in turbidity during oods (Thomaz et al. 2004a) together with scouring, as shown in other oodplains (van Geest et al. 2005a). Accordingly, high connectivity and the consequent disappearance of submersed macrophytes is also the probable reason for the disruption of local community organization in the Parana River sub-system. A conceptual model summarizing the above discussion and showing the possible responses (and their probable causes) of macrophyte assemblages to ood disturbances in the different rivers of the Upper Parana River oodplain is shown in Fig. 6. The classication strength results highlighted the differentiation among the three rivers. In addition, this regionalization seems to be resistent to the ood disturbance, given that CS values were not substantially affected by the ood (see Table 1). In general, this pattern, obtained in samples using a ner grain (macrophyte patch as the unit) is congruent with the one obtained previously by using much coarser grains (lakes as units; Bini et al. 2001). Similarly, Lougheed et al. (2001), studying wetlands in the Great Lakes basin, showed that species richness and community structure of aquatic macrophytes are related mainly to the geographic location of the wetland to which a lake is associated. In general, the strengths of classications, considering both regional and local perspectives, were low (see Table 1). This pattern was also observed using data from other freshwater biota at different scales of classications (Hawkins et al. 2000; Sandin and Johnson 2000; van Sickle and Hughes 2000; Heino et al. 2002; Snelder et al. 2004; Heino and Mykra 2006). Working with macroinvertebrates in streams, Heino and Mykra (2006) argue that even weak classications provide a preliminary approach for conservation planning of aquatic biodiversity. For instance, even if the values of regional classications were low both before and after the ood disturbance, they would be signicant after 1,000 random permutations. This shows that the macrophyte communities in the Upper Parana River can be classied in three different sub-systems independent of the ooding regime. Moreover, divisions combining terrestrial landscape characteristics and associated patterns of terrestrial biodiversity to those of aquatic biodiversity can enhance the

predictability of biological assemblages for conservation efforts. In this sense, further studies using other classi cation schemes should be carried out in the Upper Parana River oodplain to support biological assessments aiming at conservation. In fact, when we used quadrat depths as a classication scheme for each sub-system, we found that local organization is disrupted by ood disturbances in the Parana and Baa River lakes. This showed the particular role that the water level regime played in macrophyte zonation at the ne grain (quadrats) level in these two subsystems. On the other hand, other factors may be related to the local organization of the Ivinheima lakes, such as the characteristics of the surrounding landscape. For example, considering the total area of the Upper Parana River oodplain, habitats in the Ivinheima River are the most conserved (Agostinho et al. 2000). In summary, our results show that despite the extreme o ood caused by the El Nin South Oscillation in 2007, which affected all habitats in the oodplain simultaneously, species richness and the assemblage structure of patches in lakes connected to different rivers responded quite differ ently. The distance from the Parana main channel (leading to ow differences) and the degree of connection of lakes, together with the inuence of the upper reservoirs may be factors causing these ndings. It is also important to note that this extreme ood disrupted community organization at a local perspective (between different depths) only in the Parana and Baa lakes. This scenario suggests that further studies evaluating the effects of hydrological regime control should focus at a small spatial resolution in these two subsystems, and biological assessments should consider the existence of regional organization considering the three rivers. Finally, it is worth emphasizing that the different responses of macrophytes from each sub-system to the ood contribute to maintaining high species (gamma) diversity of macrophytes, and probably also of other aquatic assem blages in the Upper Parana River and its active oodplain.
Acknowledgments We thank A. Bozza and T.A. Boni for eld support. We are also grateful to Dr. Klement Tockner and two anonymous reviewers for valuable suggestions in previous drafts of this manuscript. A.A. Padial and R.B. Rodrigues received student fellowships from Coordenacao de Aperfeicoamento de Pessoal de Nvel Superior (CAPES) during the elaboration of this manuscript. P. Carvalho is supported by the PDTA program (Fundacao Parque Tecnologico ItaipuFPTI-BR) and S.M. Boschilia received a student fellowship from CNPq (National Counsel of Technological and Scientic Development). S.M. Thomaz is a researcher from the Brazilian Council of Research (CNPq) and thanks this agency for its long-term funding.

References
Agostinho AA, Thomaz SM, Minte-Vera CV, Winemiller KO (2000) Biodiversity in the high Parana River oodplain. In: Gopal B,

Flood disturbance and Neotropical macrophytes Junk WJ, Davis JA (eds) Biodiversity in wetlands: assessment, function and conservation. Backhuys Publishers, Leiden, pp 89 118 Agostinho AA, Gomes LC, Verssimo S, Okada EK (2004) Flood regime, dam regulation and sh in the Upper Parana River: effects on assemblage attributes, reproduction and recruitment. Rev Fish Biol Fish 14:1119 Agostinho AA, Thomaz SM, Gomes LC (2005) Conservation of the biodiversity of Brazils inland waters. Conserv Biol 19:646652 Baattrup-Pedersen A, Szoszkiewicz K, Nijboer R, OHare M, Ferreira T (2006) Macrophyte communities in unimpacted European streams: variability in assemblage patterns, abundance and diversity. Hydrobiologia 566:179196 Bini LM, Thomaz SM, Souza DC (2001) Species richness and betadiversity of aquatic macrophytes in the Upper Parana River oodplain. Arch Hydrobiol 151:511525 Bonecker CC, Lansac-Toha FA, Rossa DC (1998) Planktonic and non-planktonic rotifers in two environments of the Upper Parana River oodplain, State of Mato Grosso do Sul, Brazil. Braz Arch Biol Technol 41:447456 Bornette G, Henry C, Barrat MH, Amoros C (1994) Theoretical habitat templets, species traits and species richness: aquatic macrophytes in the Upper Rhone River and its oodplain. Freshw Biol 31:487505 Bornette G, Amoros C, Lamouroux NL (1998) Aquatic plant diversity in riverine wetlands: the role of connectivity. Freshw Biol 39:267283 Bornette G, Piegay H, Citterio A, Amoros C, Godreau V (2001) Aquatic plant diversity in four river oodplains: a comparison at two hierarchical levels. Biodivers Conserv 10:16831701 Bornette G, Tabacchi E, Hupp CR, Puijalon S, Rostan JC (2008) A model of plant strategies in uvial hydrosystems. Freshw Biol 53:16921705 Boschilia SM, Oliveira EF, Thomaz SM (2008) Do aquatic macrophytes co-occur randomly? An analysis of null models in a tropical oodplain. Oecologia 156:203214 Dibble ED, Thomaz SM, Padial AA (2006) Spatial complexity measured at a multi-scale in three aquatic plant species. J Freshw Ecol 21:239247 Hawkins CP, Norris RH, Gerritsen J, Hughes RM, Jackson SK, Johnson RK, Stevenson RJ (2000) Evaluation of the use of landscape classications for the prediction of freshwater biota: synthesis and recommendations. J North Am Benthol Soc 19:541556 Heino J, Mykra H (2006) Assessing physical surrogates for biodiversity: do tributary and stream type classications reect macroinvertebrate assemblage diversity in running waters? Biol Conserv 129:418426 Heino J, Muotka T, Paavola R, Hamalainen H, Koskenniemi E (2002) Correspondence between regional delineations and spatial patterns in macroinvertebrate assemblages of boreal headwater streams. J North Am Benthol Soc 21:397413 Hill MO, Gauch HG (1980) Detrended correspondence analysis: an improved ordination technique. Plant Ecol 42:4758 Ilg C, Dziock F, Foeckler F, Follner K, Gerisch M, Glaeser J, Rink A, Schanowski A, Scholz M, Deichner O, Henle K (2008) Longterm reactions of plants and macroinvertebrates to extreme oods in oodplain grasslands. Ecology 89:23922398 Junk WJ, Bayley PB, Sparks RE (1989) The ood pulse concept in rivers systems. Can Spec Publ Fish Aquat Sci 106:110127 Lacoul P, Freedman B (2006) Environmental inuences on aquatic plants in freshwater ecosystems. Environ Rev 14:89136 Lopes CA, Benedito-Ceclio E, Martinelli LA (2007) Variability in the carbon isotope signature of Prochilodus lineatus (Prochilodontidae, Characiformes) a bottom-feeding sh of the Neotropical region. J Fish Biol 70:16491659

397 Lougheed VL, Crosbie B, Chow-Fraser P (2001) Primary determinants of macrophyte community structure in 62 marshes across the Great Lakes basin: latitude, land use, and water quality effects. Can J Fish Aquat Sci 58:16031612 Makkay K, Pick FR, Gillespie L (2008) Predicting diversity versus community composition of aquatic plants at the river scale. Aquat Bot 88:338346 Maltchik L, de Oliveira GR, Rolon AS, Stenert C (2005) Diversity and stability of aquatic macrophyte community in three shallow lakes associated to a oodplain system in the south of Brazil. Interciencia 30:166170 Maltchik L, Rolon AS, Schott P (2007) Effects of hydrological variation on the aquatic plant community in a oodplain palustrine wetland of southern Brazil. Limnology 8:2328 Martins D, Marchi SR, Costa NV (2005) Estudo da movimentacao de plantas aquaticas imersas presentes no reservatorio da UHE Eng. Souza Dias - Jupia. Planta Daninha 23:351358 Martins D, Costa NV, Terra MA, Marchi SR (2008) Characterization of the aquatic plant communities of 18 reservoirs of ve watersheds in Sao Paulo, Brazil. Planta Daninha 26:1732 McCune B, Mefford MJ (1999) PC-ORD: multivariate analysis of ecological data, version 4. MjM Software Design, Gleneden Beach Neiff JJ (1979) Fluctuaciones de la vegetacion acuatica en ambientes del valle de inundacion del Parana medio. Physis 38:4153 Neiff JJ (1990) Ideas para la interpretacion ecologica del Parana. Interciencia 5:424441 Pelicice FM, Thomaz SM, Agostinho AA (2008) Simple relationships to predict attributes of sh assemblages in patches of submerged macrophytes. Neotrop Ichythyol 6:543550 R Development Core Team (2007) R: a language and environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org Reid MA, Quinn GP (2004) Hydrologic regime and macrophyte assemblages in temporary oodplain wetlands: implications for detecting responses to environmental water allocations. Wetlands 24:586599 Rolon AS, Maltchik L (2006) Environmental factors as predictors of aquatic macrophyte richness and composition in wetlands of southern Brazil. Hydrobiologia 556:221231 Sandin L, Johnson RK (2000) Ecoregions and benthic macroinvertebrate assemblages of Swedish streams. J North Am Benthol Soc 19:462474 Sculthorpe CD (1967) The biology of aquatic vascular plants. St. Martins Press, New York, 610 pp Snelder TH, Cattaneo F, Suren AM, Biggs BJ (2004) Is the river environment classication and improved landscape-scale classication of rivers? J North Am Benthol Soc 23:580598 Souza DC, Thomaz SM, Bini LM (2002) Species richness and betadiversity of aquatic macrophytes assemblages in three oodplain tropical lagoons: evaluating the effects of sampling size and depth gradients. Amazoniana 17:213225 Souza-Filho EE, Rocha PC, Comunello E, Stevaux JC (2004) Effects of Porto Primavera Dam on physical environment of the downstream oodplain. In: Thomaz SM, Agostinho AA, Hahn NS (eds) The upper Parana River and its oodplain: physical aspects, ecology and conservation. Backhuys Publishers, Leiden, pp 5574 Statsoft Inc. (2005) STATISTICA (data analysis software system) version 7.1 for Windows: statistics. STATSOFT, Inc., Tulsa, USA Strausz V, Janauer GA (2007) Impact of the 2002 extreme ood on aquatic macrophytes in a former channel of the River Danube (Austria). Belg J Bot 140:1724 Thomaz SM, Bini LM, Pagioro TA, Murphy KJ, Santos AM, Souza DC (2004a) Aquatic macrophytes: diversity, biomass and

398 decomposition. In: Thomaz SM, Agostinho AA, Hahn NS (eds) The upper Parana River and its oodplain: physical aspects, ecology and conservation. Backhuys Publishers, Leiden, pp 331 352 Thomaz SM, Pagioro TA, Bini LM, Roberto MC, Rocha RRA (2004b) Limnological characterization of the aquatic environments and the inuence of hydrometric levels. In: Thomaz SM, Agostinho AA, Hahn NS (eds) The upper Parana River and its oodplain: physical aspects, ecology and conservation. Backhuys Publishers, Leiden, pp 75102 Thomaz SM, Bini LM, Bozelli RL (2007) Floods increase similarity among aquatic habitats in river-oodplain systems. Hydrobiologia 579:113 Thomaz SM, Carvalho P, Padial AA, Kobayashi JT (2009) Temporal and spatial patterns of aquatic macrophyte diversity in the Upper Parana River oodplain. Braz J Biol 69:617625 Tockner K, Pennetzdorfer D, Reiner N, Schiemer F, Ward JV (1999) Hydrological connectivity, and the exchange of organic matter and nutrients in a dynamic river-oodplain system (Danube, Austria). Freshw Biol 41:521535 Tockner K, Malard F, Ward JV (2000a) An extension of the ood pulse concept. Hydrol Process 14:28612883 Tockner K, Baumgartner C, Schiemer F, Ward JV (2000b) Biodiversity of a Danubian oodplain: structural, functional and

A. A. Padial et al. compositional aspects. In: Gopal B, Junk WJ, Davis JA (eds) Biodiversity in wetlands: assessment, function and conservation. Backhuys Publishers, Leiden, pp 141159 van Geest GJ, Roozen FCJM, Coops H, Roijackers RMM, Buijse AD, Peeters ETHM (2003) Vegetation abundance in lowland oodplain lakes determined by surface area, age and connectivity. Freshw Biol 48:440454 van Geest GJ, Coops H, Roijackers RMM, Buijse AD, Scheffer M (2005a) Succession of aquatic vegetation driven by reduced water-level uctuations in oodplain lakes. J Appl Ecol 42:251 260 van Geest GJ, Wolters H, Roozen FCJM, Coops H, Roijackers RMM, Buijse AD, Scheffer M (2005b) Water-level uctuations affect macrophyte richness in oodplain lakes. Hydrobiologia 539:239248 van Sickle J, Hughes RM (2000) Classication strengths of ecoregions, catchments, and geographic clusters for aquatic vertebrates in Oregon. J North Am Benthol Soc 19:370384 Ward JV, Tockner K, Arscott DB, Claret C (2002) Riverine landscape diversity. Freshw Biol 47:517539 Wetzel RG (2001) Limnology: lakes and river ecosystems. Academics Press, San Diego, 679 pp