A cascade of dams affects fish spatial distributions and functional groups of local assemblages in a subtropical river

Jaqueline de Bem1 , Josiane Ribolli , Cristhiana Röpke2 , Kirk O. Winemiller3 and Evoy Zaniboni-Filho1

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Abstract​


EN

Dams reduce the longitudinal connectivity of rivers and thereby disrupt fish migration and the spatial distribution of species, impacts that remain poorly studied for some Neotropical rivers from mega-diverse basins. We investigated the spatial distribution of fish species with different trophic and movement/reproductive/size characteristics to assess how functional groups have responded to a cascade of dams on the Uruguai River in southern Brazil. Fish abundance, biomass, and species composition were evaluated at eight locations along the longitudinal gradient. The fish assemblage in the upper stretch was mainly characterized by small and medium-sized species at higher trophic levels, whereas the sites located furthest downstream displayed more medium and large-sized species, including many carnivorous species. Species with high fecundity, seasonal migrants, and catfishes with internal fertilization were common in the river´s middle and lower reaches. Detritivorous species dominated areas distant from the dams. Overall, functional diversity of local fish assemblages was greater in lower reaches. The cascade of dams has impacted the distribution of functional groups of local fish assemblages of Uruguai River. The alteration of functional groups in upper reaches of the river has potential consequences for ecosystem processes and services, such as nutrient cycling and fisheries.

Keywords: Ichthyofauna, Reproductive tactics, Reservoirs, River fragmentation, Trophic groups.

PT

As barragens reduzem a conectividade longitudinal dos rios e interrompem a migração e a distribuição espacial das espécies, configurando impactos pouco estudados para alguns rios Neotropicais megadiversos. Investigamos a distribuição espacial de espécies de peixes com diferentes características tróficas e reprodutivas para avaliar como grupos funcionais responderam a uma cascata de reservatórios no rio Uruguai, sul do Brasil. Abundância de peixes, biomassa e composição de espécies foram avaliadas em oito locais ao longo do gradiente longitudinal. A assembleia de peixes no trecho superior foi caracterizada principalmente por espécies de pequeno e médio porte em níveis tróficos mais elevados, enquanto que os ambientes localizados mais a jusante apresentaram mais espécies de médio e grande porte, incluindo muitas espécies carnívoras. Espécies com alta fecundidade, migradores sazonais e bagres com fertilização interna foram comuns no curso médio e inferior. Espécies detritívoras dominaram áreas distantes das barragens. A diversidade funcional das assembleias de peixes locais foi maior nas partes inferiores. A cascata de barragens impactou a distribuição dos grupos funcionais das assembleias de peixes locais no rio Uruguai. A alteração da diversidade funcional no curso superior do rio tem consequências potenciais para a dinâmica e serviços do ecossistema, como ciclagem de nutrientes e pesca.

Palavras-chave: Fragmentação de rios, Grupos tróficos, Ictiofauna, Reservatórios, Táticas reprodutivas.

Introduction​

Hydropower dams impact river ecosystems by reducing river longitudinal connectivity (Agostinho et al., 2016; Vitule et al., 2017; Barbarossa et al., 2020), hydrology and sediment dynamics (Araújo et al., 2013; Forsberg et al., 2017), and water physicochemistry (Zaniboni-Filho, Schulz, 2003). Dams also impact fish populations by altering in-stream and riparian habitats and blocking migration corridors (Mueller et al., 2011; Granzotti et al., 2018). River fragmentation impacts are both local and regional (Rosenberg et al., 1997), with cumulative effects that can affect regions located hundreds of kilometers downstream and upstream of the dam (Grill et al., 2015). When dams and their associated reservoirs are built in series, i.e., a cascade of dams, impacts to aquatic biota and ecosystem dynamics may be compounded. Hydropower dams constitute one of the main threats to freshwater biodiversity (Vörösmarty et al., 2010), and impacts are particularly devastating for the mega-diverse fish faunas in the tropics (Winemiller et al., 2016; Vitule et al., 2017). Migratory species are especially vulnerable because hydroelectric projects obstruct corridors essential for seasonal movements for reproduction and exploitation of habitats critical for feeding or providing refuge from predation (Carolsfeld et al., 2003; Hoeinghaus et al., 2009; Pelicice et al., 2015). Even for non-migratory fishes, dams cause population fragmentation and reductions in the sizes of local stocks and gene flow among them (Allendorf et al., 2012). As a consequence, river fragmentation compromises the adaptive capacity and the long-term persistence of fish stocks (Allendorf et al., 2012).

The functional characteristics of fish can be useful for assessing the impacts of dams on river ecology (Hoeinghaus et al., 2009; Mouillot et al., 2013; Pendleton et al., 2014; Santos et al., 2017, 2020; Zhang et al., 2020). Traits, such as morphology associated with modes of swimming and use of habitat, exploitation of various types of food resources and how food is obtained, defense tactics, reproductive strategies, and other aspects of performance that affect fitness, can be used to group species into functional groups or niches (Violle et al., 2007; Winemiller et al., 2015). These attributes can be used to assess how fish assemblages respond to human impacts and predicting the fish community’s responses to anthropic impacts (Angermeier, Winston, 1998; Arantes et al., 2019; Dias et al., 2020).

Impacts from dams differentially affect species and locations along the fluvial gradient. Rheophilic species, feeding specialists and species that depended on seasonal access to floodplain habitats generally are excluded from impounded areas (Agostinho et al., 2008). Ecological generalists and species adapted for lentic conditions may prosper in modified habitats (Arantes et al., 2019). Evaluation of assemblage functional groups facilitates comparative study of natural communities as well as impact assessment for dams and other human disturbances (Hoeinghaus et al., 2007; Cella-Ribeiro et al., 2017; Pelicice et al., 2018). These impacts can be more intense in cascade reservoirs system, in which changes in physical and biological characteristics have a substantial influence on trait compositions of fish communities (Santos et al., 2017, 2020; Arantes et al., 2019). Here, we assess the distribution of fish functional groups across a dam/reservoir cascade system in the Uruguai River within the subtropical region of South America.

Functional groups of aquatic organisms are expected to be longitudinally distributed in relation to fairly predictable riverscape characteristics, according to the assumptions of the River Continuum Concept (RCC; Vannote et al., 1980). For example, greater proportions of insectivorous fishes should occur in the upper river reaches where the riparian vegetation canopy covers the channel and provides allochthonous inputs in the form of terrestrial invertebrates and leaf litter that supports aquatic insects. In lower river reaches, where the channel is broader and sunlight and nutrients fuel autochthonous primary production, omnivorous and detritivorous fishes should comprise greater proportions of fish assemblages. However, this theory applies well to unobstructed rivers. Impoundments disrupt longitudinal connectivity and therefore should alter many predictions of the RCC (Vannote et al., 1980). The Serial Discontinuity Concept (SDC; Ward, Stanford, 1995) and Cascading Reservoir Continuum Concept (CRCC; Barbosa et al., 1999) predict how reservoir cascades alter physical and biodiversity patterns and processes described by the RCC.

We make several predictions about how the cascade of dams and reservoirs in the Uruguai River should affect the functional composition of local fish assemblages. Areas unaffected by dams with relatively natural flow regimes and habitats with fast-flowing water should retain the full complement of native fishes, including species that are rheophilic, trophic specialists and migratory species (Schork, Zaniboni-Filho, 2018). In areas directly impacted by dams, fish assemblages should be dominated by small and medium-sized fishes with opportunistic life-history strategies (Schork, Zaniboni-Filho, 2017). We further predict that the river’s altered longitudinal gradient (with dams blocking fish migration, lentic conditions in reservoirs, modified flow regimes in stretches downstream from dams, and transition zones in between (Thornton et al., 1990; Monaghan et al., 2019; Dias et al., 2020) has not only affected functional composition of local fish assemblages, but also functional diversity, numerical abundance, and biomass.


Material and methods

Sampling. The study was conducted along an approximately 600 km reach of the Upper Uruguai River where three hydroelectric dams have been constructed: Barra Grande (Upper stretch – completed in 2005), Machadinho (Middle stretch – completed in 2002), and Itá (Lower stretch – completed in 2000). Barra Grande has an area of 94 km2 and 90.6 days of the water residence time, while these values are 79 km2 and 54 days for Machadinho, and 141 km2 and 55 days for Itá. All of these reservoirs are formed by dams that are more than 100 m height. The spatial distribution of fish functional groups was investigated in eight locations, listed here from upstream to downstream: distant environment upstream from the uppermost dam [Distant Upstream – DU]; Barra Grande Reservoir [R1]; immediately downstream from Barra Grande Dam [Downstream Barra Grande DR1]; Machadinho Reservoir [R2]; immediately downstream from Machadinho Dam [Downstream Machadinho – DR2]; Itá Reservoir [R3]; immediately downstream from Itá Dam [Downstream Itá – DR3]; and distant downstream from the last dam [Distant Downstream – DD] (Fig. 1; Tab. 1). The environments Downstream R1, R2 and R3 were located approximately 250 m downstream from the dams, and the DD is a comparatively long and unimpeded stretch where several free-flowing tributaries join the river.

FIGURE 1 | Sampling locations in the Upper Uruguai River, Brazil. The symbols indicate survey sites: circles represent sites within the reservoirs (R1 = site 3 to 5; R2 = site 7 to 9; R3 = site 11 to 14); squares indicate sites located just below dams [Downstream R1 (DR1) = 6, Downstream R2 (DR2) = 10, Downstream R3 (DR3) = 15], and triangles indicate sites that are most distant from dams [Distant Upstream (DU) = 1 and 2; Distant Downstream (DD) = 16 and 17].

TABLE 1 | Characteristics of survey sites within eight locations along the Upper Uruguai River, Brazil. DU (distant location upstream of the most upstream dam), DD (distant and downstream of the most downstream dam), R1 (Barra Grande Reservoir), R2 (Machadinho Reservoir), R3 (Itá Reservoir), DR1 (immediately downstream from Barra Grande Dam), DR2 (immediately downstream from Machadinho Dam), DR3 (immediately downstream from Itá Dam).

LocationsSample SitesUTM Coordinate (X)UTM Coordinate (Y)Distance downstream from the first sample site (km)Distance between river banks (km)
DU1529400687328800.15
DU2523534688097311.490.22
R13512252689851349.460.39
R14496769691211479.060.58
R154817536926735105.550.74
DR164807796927650106.880.11
R274540486946672156.220.34
R284385146956148189.550.51
R294219246955590224.340.96
DR2104220476954598225.760.33
R3114109686957484250.040.40
R3124022726971232288.400.54
R3133909456978846311.010.67
R3143673116981165367.480.77
DR3153619556981341382.300.20
DD162994657002554514.810.28
DD172644807001424583.480.56

Fish assemblage data from surveys conducted at 17 sites were grouped into eight study locations (Distant Upstream – DU; Reservoirs – R1, R2, R3; Downstream Reservoirs – DR1, DR2 and DR3; and Distant Downstream – DD). Those sites are grouped considering similarities in geographical location and abiotic characteristics. Field work was done during January–February, April–May, July–August and October–November from 2006 to 2010, totaling 290 survey events successfully concluded. At each site during each survey seven different nets set were used, totaling 2,145 net samples. During each survey, fishes were caught along a stretch of shoreline with a set of four gill nets and three trammel nets with mesh sizes ranging from 1.5 to 5.0 cm between adjacent knots, nets height ranging from 1.6 to 1.8 m and the length ranging from 10 to 40 m. Nets were placed in the evening and removed in the following morning (set for approximately 12 h). All captured fish were counted and identified at the species level, weighed (in grams) and measured (total length in cm). Collecting license was provided by Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis – IBAMA (52/2007 and 145/2009). The nomenclature of the species list was based on Fricke et al. (2021) and in consultation with taxonomic experts. Vouchers of all species were deposited in the fish collection of Museu de Zoologia da Universidade Estadual de Londrina, Paraná, Brazil (MZUEL) (S1).

Abundance of each fish species was estimated from of numerical Catch Per Unit Effort (CPUE) (sum of individuals per 100 m2 net area/12 h – CPUEN) and biomass (sum of grams per 100 m2 net area/12 h – CPUEB), for each sampling unit (for each sampling site and period). Then, fish species were grouped according to functional groups, and CPUEN and CPUEB.

Defining functional groups. Functional groups were defined with an emphasis on characteristics predicted to affect responses to damming and reservoir formation: trophic niche, body size, and reproductive strategy (Arantes et al., 2019). Information on feeding and reproductive biology of species analyzed in this study were based on the scientific literature (e.g., Vazzoler, 1996; Hahn et al., 1998; Zaniboni-Filho et al., 2004; Reynalte-Tataje, Zaniboni-Filho, 2008; Araújo et al., 2009; Gubiani et al., 2012), including accounts for congeneric species when no information was available, and body size was recorded as the largest specimen captured from the Upper Uruguai River during regular surveys conducted by our research group from 1995 to 2014.

Fourteen functional groups were classified considering trophic and movement/reproductive/size categories. There were five trophic groups, based on diet: i) detritivore (species which fed on detritus, organic layer, periphytic algae and mud), ii) omnivore (defined as species with a generalist diet without predominance of either plant or animal tissue), iii) invertivore (species which fed on invertebrates), iv) carnivore (i.e., invertivore with a tendency for piscivore), and v) piscivore (species which fed mainly on fish). Movement/reproductive/size groups were nine combinations of this three characteristics: movement – considering fish with Sedentary habits or Short Migration (S/SM) or Long Migration (LM); reproductive strategy – with Parental Care (PC), Internal Fertilization (IF) or neither (No Parental Care – NPC); and body size – Small, maximum total length < 20 cm (S); Medium, total length between 20 and 40 cm (M); and Large, total length > 40 cm (L). These characteristics (movement, reproductive strategy and body size) were grouped based on their assumed functional and evolutionary interdependence. Thus, the nine movement/reproductive/size groups were: LNL (LM-NPC-L), SIM (S/SM-IF-M); SIS (S/SM-IF-S), SNL (S/SM-NPC-L), SNM (S/SM-NPC-M), SNS (S/SM-NPC-S), SPL (S/SM-PC-L), SPM (S/SM-PC-M), and SPS (S/SM-PC-S).

Numerical abundance and biomass of each functional group were determined from the sum of CPUEN and CPUEB of species for each sampling unit.

Data analysis. The CPUEN and CPUEB of the fourteen functional groups were log-transformed (log (x+1)) and nonmetric multidimensional scaling (NMDS) using the Bray-Curtis index was applied to evaluate dissimilarity in abundance (CPUEN) and biomass (CPUEB) of the functional groups between the sampled environments. Analysis were performed separately for trophic groups and movement/reproduction/size categories. The differences of functional assemblage structures (based on both trophic and movement/reproductive/size) among the eight locations were tested by Permutational Multivariate Analysis of Variance (PERMANOVA; Anderson, Walsh, 2013; Anderson, 2014), followed by post hoc tests performed with PERMANOVA pairwise comparisons, and Bonferroni method. The multivariate data were analyzed using the Bray-Curtis index generated from the transformed data with 9.999 permutations.

An analysis of homogeneity of multivariate dispersions (PERMDISP, Anderson et al., 2006) using the Bray-Curtis dissimilarity index was applied to evaluate if the eight locations had different degrees of homogeneity of assemblage structures based on different to CPUEN and CPUEB of functional groups. All analyzes were performed in software R (Version 3.2.4; http://cran.r-project.org), with Vegan, Mass, Car and RVAideMemoire packages.


Results​


Surveys conducted at the eight locations in Upper Uruguai River yielded 77 fish species from 49 genera and 24 families (S1), distributed into eight study locations (S2). PERMANOVA analyses with adonis function revealed a significant difference between fish assemblage structures in the different habitat categories based on trophic (numerical abundance R = 0.27, p = 0.001; biomass R = 0.23, p = 0.001) and movement/reproductive/size categories (numerical abundance R = 0.32, p = 0.001; biomass R = 0.27, p = 0.001). Results of the PERMANOVA pairwise comparisons for eight environmental presents no differences between DUxR2, DUxDD, DR1xDR2, DUxR3 and DDxR3 for trophic categories (p > 0.05), and DUxR2 for movement/reproductive/size categories (p > 0.05), but with significant differences for the others comparisons.

The results of ordination (NMDS; Fig. 2) indicated that piscivorous fishes were predominant in most upstream reservoir (R1), long-distance migratory and carnivorous fishes were most common immediately downstream from reservoirs (DR), and detritivorous fishes and those with internal fertilization were most common in the location Distant and Downstream from the lowest dam in the cascade (DD).

 Approximately half of the total fish abundance and biomass in the assemblage at the location most Distant Downstream (DD) and the assemblage most Distant Upstream (DU) was composed of detritivorous species (Tab. 2).

The assemblage from the uppermost reservoir of the cascade (R1) had the lowest numerical abundance and biomass of detritivores, invertivores and carnivores. R1 had the highest numerical abundance and biomass of piscivores (41% and 65% of total fish abundance and biomass, respectively). Omnivorous fish were abundant in R1, DR1, and DR3 (44%, 68% and 47%, respectively; Tab. 2). The high abundance of omnivores immediately downstream from Barra Grande Dam (DR1) was due to an extraordinary abundance of a single species (Psalidodon aff. fasciatus).

FIGURE 2 | Ordination plots produced by the non-metric multidimensional scaling analysis (NMDS) using the Bray-Curtis index, considering the abundance (CPUEN) of movement/reproductive/size (A) and trophic categories (B), and biomass (CPUEB) of movement/reproductive/size categories (C) and trophic categories (D), among survey locations. [DU (red triangle), DD (yellow triangle)] = Sampling points away from the dams; [R1 (red circle), R2 (green circle), R3 (orange circle)] = sampling points located in the reservoirs; [DR1 (green square), DR2 (orange square), DR3 (red square)] = locations downstream from dams. Labels are for Detritivores, Invertivores, Carnivores, Omnivores, and Piscivores; S/SM = sedentary/short migration, NPC = no parental care, PC = parental care, IF = internal fertilization, and LM = long migration; and Small, Medium, and Large body sizes.

TABLE 2 | CPUEN and CPUEB of five trophic categories within samples of fish assemblages from eight locations along Upper Uruguai River obtained between 2006–2010. DU (distant upstream from the most upstream dam), DD (distant downstream from the most downstream dam), R1 (Barra Grande Reservoir), R2 (Machadinho Reservoir), R3 (Itá Reservoir), DR1 (immediately downstream from Barra Grande Dam), DR2 (immediately downstream from Machadinho Dam), DR3 (immediately downstream from Itá Dam).

 Trophic categoryDU%R1%DR1%R2%DR2%R3%DR3%DD%
AbundancePiscivorous281085419485416104192610315115
Carnivorous2110101413110420310
Omnivorous501890448016899292294110839285475729
Invertivorous7928221116514129389116301185143116
Detritivorous12143941141054161292310137183309950
BiomassPiscivorous581721136436517165226997372126635340325747312150213
Carnivorous4192203134254486384015664159131081
Omnivorous28471048162319214255353289062153927292601142361130
Invertivorous27351048521331117278715648611958727274166014
Detritivorous156185717418232263032151723817394853352482640502342

Fish assemblages at DR1 and Machadinho Reservoir (R2) had highest biomass and numerical abundance, respectively, of invertivorous fishes (Tab. 2). The fish assemblage at Itá, the most downstream reservoir of the cascade (R3), had the greatest numerical abundance and biomass of carnivorous fishes (4%; Tab. 2). Assemblages at the location immediately downstream from R3 (DR3) and the location furthest downstream (DD) had the lowest numerical abundance and biomass of fish categorized as piscivores.

Sedentary or short migratory species (S/SM) were abundant with large biomass at all eight locations (Tab. 3). Long-distance migratory fishes, including Prochilodus lineatus and Salminus brasiliensis, were absent in samples from the first reservoir (R1) and location immediately downstream (DR1) (S2). However, at Downstream R3 (DR3) and the most distant downstream location (DD) the numerical abundance and biomass of long-distance migrants were relatively high at 10% and 9%, respectively (Tab. 3).

The fish assemblage at the distant downstream location had greater numerical abundance and biomass of species with internal fertilization, but only four species were in this category. No species with internal fertilization were captured from Machadinho Reservoir (R2) or locations upstream. Functional categories with small-bodied species without parental care, stood out immediately downstream of R1, and medium-size species (without parental care – NPC), had greater numerical abundance and biomass at Barra Grande and Machadinho Reservoirs (R1 and R2). The assemblage at the location immediately downstream from Itá Reservoir (DR3) had the highest numerical abundance and biomass of medium-size species with parental care, and the most Distant Downstream location (DD) had the greatest abundance of large-size species with parental care (Tab. 3).

TABLE 3 | CPUEN and CPUEB of nine movement/reproductive/size categories within samples of fish assemblages from eight locations along Upper Uruguai River obtained between 2006–2010. Values are presented by annual mean number and percentage, S/SM = Sedentary/Short Migration, LM = Long Migration, PC = Parental Care, NPC = No Parental Care, IF = Internal Fertilization, S = small, M = medium, and L = large. Movement/reproductive/size groups: LNL (LM–NPC–L), SIM (S/SM–IF–M); SIS (S/SM–IF–S), SNL (S/SM–NPC–L), SNM (S/SM–NPC–M), SNS (S/SM–NPC–S), SPL (S/SM–PC–L), SPM (S/SM–PC–M), and SPS (S/SM–PC–S). DU (distant upstream from the most upstream dam), DD (distant downstream from the most downstream dam), R1 (Barra Grande Reservoir), R2 (Machadinho Reservoir), R3 (Itá Reservoir), DR1 (immediately downstream from Barra Grande Dam), DR2 (immediately downstream from Machadinho Dam), DR3 (immediately downstream from Itá Dam).


Movement/reproductive/sizeDU%R1%DR1%R2%DR2%R3%DR3%DD%
AbundanceSNS4616 8240 79968 10531 20136 13750 19532 4824 
SNM12243 10450 23220 18254 21338 5420 11018 4020 
SNL1011392943148814 7
SPS0<1 00001<1 00<1 
SPM8932 346186812 2610 19132 3116 
SPL147676284015 176633 
SIS000000<1 00<1 
SIM00001105
LNL<1000<13<1 0<1 4<1 1<1 
BiomassSNS103819441285017 210711 3027254419 2821121810 
SNM952135 1147655 2126028 890447 2393639 279120 4734231119 
SNL2581307815 1033114 438123 672611 244518 2335637 185416 
SPS200001303
SPM886632 44349201405849914 185814 2181835 203417 
SPL526919 394619 2698135 200911 1703628 370327 3390317027 
SIS000001023
SIM0000754613210
LNL16000322172306649510 1082

PERMDISP analysis indicated that all locations had different degrees of heterogeneity of assemblage functional groups structure (trophic numerical abundance: F(7,282) = 9.74, P < 0.0001; trophic biomass: F(7,282) = 9.06, P < 0.0001; movement/reproductive/size numerical abundance: F(7,282) = 8.95, P < 0.0001; movement/reproductive/size biomass: F(7,282) = 6.19, P < 0.0001). Overall, for both functional groups (trophic and reproductive/movement/size) and metrics (numerical abundance and biomass), pairwise differences were consistent, the locations DU and R1 had the highest heterogeneity (larger distance from centroid) compared to the others, and DR2 the lowest heterogeneity. The location DD had a higher movement/reproductive/size heterogeneity compared to locations from the middle stretch of the Uruguai River (Figs. 3A–D; Tabs. 4–5; S3).

FIGURE 3 | Analysis of multivariate homogeneity of group dispersions (PERMIDISP) by betadisper boxplot, using the Bray-Curtis index, considering the abundance (CPUEN) of movement/reproductive/size (A) and trophic categories (B), and biomass (CPUEB) of movement/reproductive/size categories (C) and trophic categories (D). The data was based on sampling sites, and presented by environment groups: [DU, DD] = Sampling points away from the dams; [R1, R2, R3] = sampling points located in the reservoirs; [DR1, DR2, DR3] = locations downstream from dams. Greater distance to spatial median indicates larger dispersion and therefore a more diverse/heterogeneous environment. Box lower and upper endpoints represent the 25th and 75th quartiles, respectively. The horizontal bar and plus symbol inside each box represent median, excluding outliers, which are presented by open circles. See Tabs. 4 and 5 for P values from environments comparisons.

TABLE 4 | Summary of PERMDISP permuted P values for comparisons of heterogeneity in movement/reproductive/size structure among locations. Above diagonal p values for numeric abundance and below diagonal for biomass movement/reproductive/size structure. Statistically significant P values (P < 0.05) are highlighted in bold.

LocationDUR1DR1R2DR2R3DR3DD
DU 0.1770.0020.0010.0010.0010.0030.989
R10.801 0.0230.0030.0010.0280.0430.128
DR10.0880.043 0.8680.0390.2800.7580.001
R20.0010.0010.785 0.0460.1870.8780.001
DR20.0190.0070.6520.778 0.0020.0220.001
R30.0180.0040.3920.0700.104 0.4420.001
DR30.4530.3100.1360.0130.0100.247 0.001
DD0.2930.4150.0010.0010.0010.0010.019 

TABLE 5 | Summary of PERMDISP permuted P values for comparisons of heterogeneity in trophic assemblage structure among locations. Above diagonal p values for numeric abundance and below diagonal for biomass trophic structure. Statistically significant P values (P < 0.05) are highlighted in bold.

LocationDUR1DR1R2DR2R3DR3DD
DU
0.5720.0010.0010.0010.0010.0010.023
R10.710
0.0040.0030.0010.0010.0010.076
DR10.0190.003
0.2600.0010.1340.8240.035
R20.0010.0010.366
0.0010.8280.1700.286
DR20.0020.0010.3410.026
0.0010.0030.001
R30.0010.0010.7960.3580.200
0.0650.284
DR30.0050.0010.8020.2000.6660.529
0.020
DD0.0890.0120.1110.1260.0070.0230.060

Discussion​

The fish assemblage in the lowest reach (R3, DR3 and DD) and the upper portion (DU), within the dam and reservoir cascade of the Upper Uruguai River, had greater functional group diversity, and this might indicate that environmental impacts were lower compared to upstream locations in the reservoirs cascade. Although this pattern also could reflect a legacy of a natural longitudinal gradient of fish diversity during the period preceding construction of the hydroelectric dams (Lowe-McConnell, 1975; Araújo et al., 2009), the high diversity and presence of piscivorous in the upstream portion may corroborate with the reservoir cascade environmental impact. Piscivorous fishes were relatively abundant in the uppermost reach and the location downstream from the Machadinho Reservoir. Overall, fish assemblages at all locations surveyed in the Upper Uruguai River were dominated by small and medium-sized species that lack parental care. Medium-sized and large carnivorous species dominated assemblages in lower reaches between Itá Reservoir and the most Distant Downstream location, and these assemblages included diverse life history attributes, such as internal fertilization, parental care, and long-distance migratory behavior. The presence of medium-sized and large-sized fish and species with a diversity of life history attributes was associated with habitats less affected by human impacts resulting from dams, but another influence could have been the natural tendency for fish species richness to increase in the downstream direction along longitudinal river gradients (Araújo et al., 2009).

Migratory fishes were largely restricted to middle-lower reaches of the cascade system where several free-flowing tributaries, including the Ligeiro and Peixe rivers (located between DR2 and R3), join the Uruguai River (Reynalte-Tataje et al., 2012). The connectivity provided by these rivers is crucial for migratory fishes that undergo seasonal long-distance migrations (Agostinho et al., 2002; Cote et al., 2009; Silva et al., 2017). Dams in a cascade system create insurmountable barriers to migratory fish species, both in terms of upstream and downstream movement (Vörösmarty et al., 2010; Pelicice et al., 2018). The absence of large migratory fishes, such as Salminus brasiliensis from the upper stretches (DU, R1 and DR1) have the potential to alter top-down trophic dynamics structuring local fish assemblages (Taylor et al., 2015).

Habitats within reservoirs and immediately downstream from them often have hydrological regimes that vary more as a function of dam releases than seasonal precipitation and runoff (Graf, 2006; Räsänen et al., 2012). Consequently, the magnitude and timing of changes in hydrology and water quality tend to be lower and less variable and predictable compared to the natural flow regime (Vannote et al., 1980; Link et al., 2008). These conditions likely are not conducive to fish species that are seasonal spawners with recruitment dependent upon access to flooded riparian areas or other habitats formed in special hydrological conditions that serve as nurseries (Winemiller, 1989; Winemiller et al., 2008). Daily water-level fluctuations in nearshore areas of reservoirs and in tailraces are disruptive to fishes that deposit eggs in nests and guard them (Agostinho et al., 2008). It is unclear why auchenipterid catfishes with internal fertilization were absent in upper reaches of the dam/reservoir cascade. These fishes have a relatively equilibrium-type life history strategy of relatively large egg size and low fecundity (sensu Winemiller, Rose, 1992). Like cichlids and other brood-guarding fishes that also would be considered equilibrium strategists, these catfishes should be adapted for relatively stable environments (Tedesco et al., 2008).

High percentages of small and medium-sized sedentary and short-migration fishes throughout the Upper Uruguai River suggests that these species are ecological generalist in terms of feeding and habitat requirements. Neotropical fishes in these categories have been shown previously to dominate fish assemblages within reservoirs (Agostinho et al., 2007; Pelicice et al., 2018). Many of the fishes in these categories are omnivorous with broad diets that vary in response to food availability (Agostinho et al., 2007). It is notable that distributions for these fishes contrast with those of detritivorous (Agostinho et al., 2016; Dias et al., 2020) and long-distance migratory fishes (Agostinho et al., 2002; Cote et al., 2009; Silva et al., 2017) that were uncommon at locations most strongly impacted by dams and reservoirs.

Following dam construction, the reservoir filling phase generally produces a marked increase in aquatic primary production (trophic upsurge, Baranov, 1961) and availability of food resources for fishes, especially for small omnivorous and invertivorous fishes, which in turn often leads to an eventual increase in the abundance of piscivores that exploit them as prey (Agostinho et al., 2007). The trophic upsurge and abundant prey may explain the high abundance of piscivorous fishes in the most recently created reservoir (R1). In contrast, the relatively low abundance of large piscivores within reservoirs in the lower stretch of the cascade system might account for the greater abundance of smaller carnivorous species, owing to lower predation mortality as well as competition for some of the same food resources (Petry, Schulz, 2006; Araújo et al., 2009). Detritivorous fish can play an important role in nutrient cycling in both rivers (Taylor et al., 2015) and reservoirs (Vanni et al., 2005), and therefore could influence food web structure and other trophic guilds along river longitudinal gradients. However, this trophic guild is known to be negatively impacted by creation of reservoirs (Santos et al., 2020), and was not abundant in the deep reservoirs of the Upper Uruguai River. Fish in reservoirs avoid deep areas where thermal stratification reduces dissolved oxygen concentrations, which can result in a loss of nutritional quality of detritus (Santos et al., 2020) and places much of the phytoplankton-derived detritus out of reach for detritivores (Baumgartner et al., 2020). Detritivorous fishes were most common at the Distant-Upstream and Distant-Downstream locations, the two areas with flow regimes that were least affected by dams. They also were common in river reaches downstream from dams, where they likely exploit phytoplankton-derived detritus in water released from dams (Hoeinghaus et al., 2007).

The spatial distribution of fish functional groups in the dam/reservoir cascade of the Upper Uruguai River suggests that the downstream area (R3, DR3 and DD) have retained more the natural environmental characteristics that support riverine fish diversity. The DD location lies within an extensive unimpeded reach where several free-flowing tributaries enter the river and contribute to fluvial connectivity and a more natural flow regime compared to river reaches directly downstream from reservoirs. Consequently, this location has greater fluvial connectivity and a more natural flow regime compared to upstream locations that are more impacted by dams. Dams cause profound changes in not only the taxonomic structure of river fish assemblages (Freedman et al., 2014), but also the functional groups of aquatic communities with likely effects on food-web dynamics. Our findings contribute to understanding the effects of reservoir cascades on the distribution and abundance of fish with diverse ecological characteristics. Tributaries appear to have fundamental importance for maintaining a high diversity of fish reproductive groups, and reservoir cascades create large-scale environmental heterogeneity that apparently determines the distribution of fish trophic guilds and food web structure. Future management actions should prioritize the maintenance of fluvial habitat connectivity and environment conditions to facilitate fish migration, reproduction and life cycle completion by species spanning diverse life history strategies, and food web dynamics that allow persistence of the full complement of native species.


Acknowledgments​


The authors acknowledge Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Engie (Tractebel Energia), Consórcio Itá, and Consórcio Machadinho for financial support. This study was also supported by SISBIOTA – Top predator network (CNPq 563299/2010–0 and Fundação de Amparo à Pesquisa do Estado de São Paulo – FAPESP 2010/52315-7). JB acknowledge scholarships provided by CAPES and PhD exchange process number 99999.004990/2014–05. JR acknowledge scholarships provided by Programa Nacional de Pós-Doutorado PNPD/CAPES. EZF thanks CNPq, grant 302860/2014–2. We are grateful to the technicians from Laboratório de Biologia e Cultivo de Peixes de Água Doce (LAPAD) for data collection and Dr. Tiago Pires for his contribution to statistical analysis. This study was financed in part by CAPES – Finance Code 001. Collecting license was provided by Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis – IBAMA (52/2007 and 145/2009) and this study did not require permission from Ethical Committee for Animal Use in Experiments. The authors also thank the anonymous reviewers who improved the manuscript.

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Authors


Jaqueline de Bem1 , Josiane Ribolli , Cristhiana Röpke2 , Kirk O. Winemiller3 and Evoy Zaniboni-Filho1

[1]    Laboratório de Biologia e Cultivo de Peixes de Água Doce, Departamento de Aquicultura, Universidade Federal de Santa Catarina, 88066-260 Florianópolis, SC, Brazil. (JDB) jaquedebem@gmail.com (corresponding author), (JR) josianeribolli@gmail.com, (EZF) evoyzaniboni@gmail.com.

[2]    Instituto Nacional de Pesquisas da Amazônia, Coordenação em Biodiversidade, 69067-375 Manaus, AM, Brazil. crisropke@gmail.com.

[3]    Department of Ecology and Conservation Biology, Texas A&M University, 77843-2258 College Station, TX, USA. k-winemiller@tamu.edu.

Authors Contribution


Jaqueline de Bem: Conceptualization, Formal analysis, Investigation, Methodology, Writing-original draft.

Josiane Ribolli: Conceptualization, Supervision, Writing-review and editing.

Cristhiana Röpke: Formal analysis, Supervision, Writing-review and editing.

Kirk O. Winemiller: Conceptualization, Supervision, Writing-review and editing.

Evoy Zaniboni-Filho: Conceptualization, Funding acquisition, Project administration, Supervision, Writing-review and editing.

Ethical Statement​


Collecting license was provided by Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis – IBAMA (52/2007 and 145/2009).

Competing Interests


The authors declare no competing interests.

How to cite this article


de Bem J, Ribolli J, Röpke C, Winemiller KO, Zaniboni-Filho E. A cascade of dams affects fish spatial distributions and functional groups of local assemblages in a subtropical river. Neotrop Ichthyol. 2021; 19(3):e200133. https://doi.org/10.1590/1982-0224-2020-0133

Copyright​


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Diversity and Distributions Published by SBI

Accepted May 24, 2021 by Andrea Bialetzki

Submitted November 25, 2020

Epub Sept 17, 2021