Ichthyofauna from three streams of the lower Iguatemi River in the upper Paraná river basin , Brazil

The ichthyofauna from 3 streams (Água Boa, Perobão, and Santa Maria) to the lower Iguatemi River were inventoried, which is located in the upper Paraná river basin, in Mato Grosso do Sul state, Brazil. Sites in the upper, intermediate, and lower portions of each stream were quarterly electrofished from March to December 2008. All sampled fish (n = 6,816 individuals) represented 43 species of 5 orders, and 16 families. The most abundant species was Phalloceros harpagos (63.5%), followed by Astyanax aff. paranae (10.6%), Hypostomus ancistroides (5.9%), Gymnotus inaequilabiatus (3.4%), and Knodus moenkhausii (2.7%). Despite the high ichthyofauna richness in the lower portion of Iguatemi River, the need to implement and/or expand soil conservation practices and riparian forest restoration is of utmost importance to maintain these populations in the long term.


Introduction
The South American freshwater fish fauna is the most diverse on earth (Albert et al. 2011), with about 20 orders, 69 families, 739 genera, and 5,160 valid species (Reis et al. 2016).Of these, approximately 310 species, including both native and non-native species, are found in the upper Paraná river basin (Langeani et al. 2007).Small tributar-ies and streams of this basin harbor a great concentration of small-bodied species of fish (Castro 1999, Winemiller et al. 2008), with little or no commercial value, which correspond to around 50% of the richness of freshwater fish species in tropical regions (Lowe-McConnell 1999, Winemiller et al. 2008).
Despite the representativeness of Brazilian streams fish fauna in Neotropical biodiversity and its contribu-tion to the functioning of ecosystems, the composition of fish species in Brazilian streams is still poorly reported in the literature (Castro et al. 2003, Langeani et al. 2007, Winemiller et al. 2008).Although relatively well known compared to elsewhere in South America, the ichthyofauna of the upper Paraná river basin also requires further investigations (Langeani et al. 2007).Such a lack of information on the species composition of fish assemblages is particularly pronounced at the lower portion of the Iguatemi River, a right bank tributary of the upper Paraná river basin (see Súarez and Petrere-Júnior 2003, 2005, 2006).
The Iguatemi River, mainly in its lower section, is located within the limits of the area of influence of flood pulses of the upper Paraná River floodplain.This area corresponds to an extensive floodplain, mainly in the Mato Grosso do Sul state, and represents a very dynamic ecosystem in biotic and abiotic terms (Agostinho et al. 2009), presenting a high environmental heterogeneity and importance for biodiversity maintenance (Thomaz et al. 2007).Since the knowledge on fish species living in a river basin is essential for any measure of management of fishery resources and/or water quality and habitats (Oliveira et al. 2014), we present a list of fish species for 3 first-order streams, tributaries to the Iguatemi River, within the limits of the upper Paraná River floodplain.

Methods
Study area.Água Boa, Perobão, and Santa Maria are first-order streams, which run for about 6.0, 4.3, and 5.3 km, respectively, in rural areas in southern Mato Grosso do Sul, Brazil.Only the headwater of the Santa Maria stream is located in the urban area of the municipality of Mundo Novo.All the 3 streams flow into the right bank of the Iguatemi River, upper Paraná river basin (Fig. 1).These streams are surrounded by poor arboreal riparian forest.The native vegetation is the Atlantic Forest biome (semi-deciduous forest), which has been largely replaced with agriculture and pasture.Deforestation is a remarkable characteristic of the history of regional occupation (Súarez and Petrere-Júnior 2003).Siltation is another anthropogenic stressor.The soil in the region is sandy and frequently impacted by gullies, intensifying the input of sediments into the streams; added to this, rural populations indiscriminately use the water from streams for livestock, which worsens the siltation process due to animal trampling (Mendonça et al. 2014).Garbage accumulation is another impact on the Santa Maria stream given its contact to urban areas.
Data collection.Samplings were conducted quarterly from March to November, 2008 (Brazilian license 146/2007, IBAMA/SISBIO) in the upper (Site 1), intermediate (Site 2) and lower (Site 3) portions of Água Boa, Perobão, and Santa Maria streams.Each sampling site shows distinct characteristics of width, depth, flow, streambed, and riparian vegetation (for more details, see Table 1).Fish were caught using electrofishing (portable generator TOYAMA 1600, 220V, DC).The sampling effort was standardized for each stream and the different months.Each sampled portion length was determined according to Fitzpatrick et al. (1998), wherein we took 5 width measurements in each portion (emphasizing the environmental heterogeneity including the regions of run, riffle, and pool).Later, we calculated the arithmetic mean of these measures and multiplied the result by 20.The length of the upper, intermediate, and lower portion sampled were 82 m, 71 m, and 50 m for the Água Boa stream, 94 m, 57 m, and 61 m for the Perobão stream, and 19 m, 37 m and 63 m for the Santa Maria stream.Blocking nets were installed at the end of each portion (10 m × 2 m and mesh size of 0.5 cm between opposite nodes) to prevent fish from escaping.A single electrofishing pass was used to collect the fish in each portion.
The specimens were euthanized in benzocaine and fixed in 10% formalin.In the laboratory, specimens were sorted and placed in glass vials containing 70% alcohol.Identification followed Graça and Pavanelli (2007) and/or via specialist verification.Taxonomic classification followed Reis et al. (2003), Betancur et al. (2017), andFerraris (2007) particularly for Siluriformes.Voucher specimens were deposited in the fish collection of the Nupélia (NUP: Núcleo de Pesquisas em Limnologia, Ictiologia e Aquicultura), Universidade Estadual de Maringá, Maringá, Paraná (NUP 16119 to NUP 16122, NUP 16138 to NUP 16148, NUP 16151 to 16185, and NUP 16170).The species were categorized by their constancy of occurrence, which was calculated for each stream according to Dajoz (1983).Species with a frequency of occurrence up to 25% were classified as occasional, between 25 and 50% as an accessory, and above 50% as constant.In addition, the species were categorized into autochthonous and allochthonous, respectively, to distinguish native and introduced species to the upper Paraná river basin (Graça and Pavanelli 2007, Langeani et al. 2007, Júlio Júnior et al. 2009).

Moenkhausia australe (Eigenmann, 1908)
Deep body; terminal mouth; inner row of premaxilla with 5 teeth, outer with 3 or 4, dentary with 9-12 and maxilla with 1 or 2 teeth.Lateral line complete, with 19-26 pored scales; longitudinal series with 24-26 scales; transversal series above lateral line with 4, 4½ or 5 scale rows and below with 3, 3½ or 4 scale rows.Dorsal fin with 11, pectoral fin with 11-13, pelvic fin with 8, anal fin with 24-27 and caudal fin with 19, total rays.Ground color silvery; scales with dark-brown border, conferring reticulated pattern to body; 1 dark-brown humeral spot; anterior half of caudal peduncle with light area.Hyaline fins, except caudal fin.Moenkhausia australe is morphologically similar to M. forestii and M. sanctaefilomenae, but can be distinguished from them by having lateral line completely pored, rarely disrupted (vs lateral line incompletely pored, in M. forestii and M. sanctaefilomenae).Benine, Castro & Sabino, 2004 Moenkhausia bonita Benine et al. 2004: 68,  Material examined.Table 2; Figure 5I.Elongated body; terminal mouth; inner row of premaxilla with 5 teeth, outer with 2-5, dentary with 4 and maxilla with 2 or 3 teeth.Lateral line complete, with 29-34 pored scales; transversal series above lateral line with 5 scale rows and below with 3 scale rows.Dorsal fin with 11, pectoral fin with 12-13, pelvic fin with 8, anal fin with 24-26 and caudal fin with 19, total rays (Benine et al. 2004).Ground color silvery to pale yellow; dark-brown longitudinal stripe from opercle (conspicuously from vertical through dorsal-fin origin) to median caudal-fin rays; distal portion of caudal-fin lobes equally dark brown.Deep body; terminal mouth; premaxilla, dentary and maxilla without teeth.Lateral line with 31-36 pored scales; transversal series above lateral line with 5½-7 scale rows and below with 4½-6 scale rows.Dorsal fin with 11 or 12, pectoral fin with 14-16, pelvic fin with 9 or 10, anal fin with 8 or 9 and caudal fin with 19, total rays (Vari 1992).Ground color silvery; dark brown inconspicuous longitudinal band along lateral line to distal margin of median caudal-fin rays, larger on caudal peduncle; hyaline fins.Material examined.Table 2; Figure 5P.Elongated body; terminal mouth; premaxilla, dentary, and maxilla without teeth; palate with irregular glomerular projections.Lateral line with 33-37 pored scales; transversal series above lateral line with 5½-6½ scale rows and below with 4½-5½.Dorsal fin with 10-12, pectoral fin with 11-14, pelvic fin with 9, anal fin with 9 or 10, and caudal fin with 19, total rays (Vari 1991).Ground color silvery; black conspicuous longitudinal stripe along lateral line to distal margin of median caudal-fin rays, larger on caudal peduncle; yellowish fins; dorsal-fin black blotch on the base of median rays, sometimes little conspicuous.

Pyrrhulina australis Eigenmann & Kennedy, 1903
Pyrrhulina australe Eigenmann and Kennedy 1903: 508 [original description].Pyrrhulina australis- Graça and Pavanelli 2007: 107.Material examined.Table 2; Figure 5S.Elongated body; terminal mouth; inner row of premaxilla with 9-12 and outer row with 4-6 teeth, inner row of dentary with 8-12 and outer row with 4-5, and maxilla with 1 or 2 teeth.Lateral line absent; longitudinal series with 20-25 scales; transversal series with 6-8 scale rows.Dorsal fin with 9 or 10, pectoral fin with 11 or 12, pelvic fin with 9 or 10, anal fin with 10 or 11, and caudal fin with 19, total rays.Ground color pale brown; dark brown longitudinal stripe from the anterior portion of the dentary, through orbit, to opercle; yellowish fins; black irregular blotch on the dorsal fin.Some specimens can present few or many dark blotches on body.Material examined.Table 2; Figure 5T.Elongated body; subterminal mouth; premaxilla with 4 or 5, maxilla with 2 or 3 and dentary with no teeth.Lateral line with 39-46 pored scales; transversal series above lateral line with 4½ or 5 scale rows and below with 3 or 4½ scale rows.Dorsal fin with 10-13, pectoral fin with 11-14, pelvic fin with 7-9, anal fin with 7 or 8 rays and caudal fin with 18 or 19, total rays (Pavanelli 1999).Ground color silvery to pale yellow; black longitudinal band along lateral line, from opercle to median caudal-fin rays, without adjacent dark blotches downwards; 6-8 dark brown transversal bars above longitudinal band; hyaline fins or with few scattered dark cromathophores.

Eigenmannia guairaca
Elongated and compressed body; terminal mouth; premaxilla with 9 or 10 teeth distributed in two rows.Lateral line complete, with 110-143 pored scales; transversal series above lateral line with 9-11 scale rows.Pectoral fin with 12 or 13 and anal fin with 151-170, total rays (Peixoto et al. 2015).Ground color pale brown; four dark-brown longitudinal stripes on flank (one superior medial, one lateral line, one inferior medial and one at anal-fin base).
Deep body; terminal mouth; premaxilla with 2 or 3 and dentary with 3 or 4 teeth rows.Upper lateral line with 14-17 pored scales, lower lateral line with 5-8 pored scales and longitudinal series with 22-23 scales.Transversal series above upper lateral with 2½-4 and below lower lateral line with 5-7 scale rows.Dorsal fin with XIII-XV, 10-15, pectoral fin with 12-13, pelvic fin with I,6 and anal fin with III, 8-10 total rays (Kullander 1983).Ground color iridescent green; dark brown transversal bars; dark-brown rounded blotch, slightly below upper lateral line; dark brown blotch on superior portion of caudal peduncle.
Elongated body; terminal mouth; premaxilla and dentary with arranged in several teeth rows.Upper lateral line with 20-22 pored scales, lower lateral line with 7-9 pored scales and longitudinal series with 33-40 scales.
Transversal series above upper lateral with 3-4½ and below lower lateral line with 7-9 scale rows.Dorsal fin with XVI, 14-16, pectoral fin with 14 or 15, pelvic fin with I,5 and anal fin with III, 9-11 total rays (Kullander, 1983).Ground color greyish to greenish; dorsum with dark transversal bars; dark suborbital stripe; dark brown discontinuous longitudinal band, sometimes inconspicuous, from snout to caudal peduncle; black rounded humeral blotch; black rounded ocelli on caudal-fin base.Dorsal, anal and caudal fins with light spots; pectoral and pelvic fins yellowish or hyaline.

Material examined. Table 2
Deep body; terminal mouth terminal with dentigerous tooth plates in both premaxilla and dentary.Dorsal fin with I,6, pectoral fin with I,7, pelvic fin with 7 or 8 and anal fin with 21-24, total rays.Adipose fin present.
Ground color pale yellow to orange with several darkbrown irregular blotches as well as fins.

Material examined. Table 2.
Elongated body; terminal mouth.Lateral line with 4-6 pores on upper series of plates.Dorsolateral series with 25-27 and ventrolateral with 22-24 plates.Dorsal fin with I,7, pectoral with I,9 or 10, pelvic fin with 6 and anal fin with 8, total rays (Reis 1997).Ground color dark gray, lighter ventrally; dark fins.Coracoid bone exposed; maxillary barbel long, surpassing gill opening; dorsalfin spine short, smaller than half of its first unbranched ray; caudal fin bifurcated; maxillary barbel not reaching pelvic-fin base.

Material examined. Table 2.
Elongated body; terminal mouth; premaxilla and dentary with several diminute and viliform teeth.Dorsal fin with 7, pectoral fin with 8-11, pelvic fin with 6 and anal fin with 11-14, total rays.First dorsal fin ray shorter than the second one; adipose-fin base short, not extending to caudal fin.Ground color beige; few scattered dark brown on body, except on ventral region of head and abdomen; dark brown transversal bars on dorsum; dark brown conspicuous longitudinal stripe along lateral line; yellowish or hyaline fins.

Discussion
The taxonomic composition of the 3 studied streams was not different from the pattern described for the South America freshwater fish fauna, given the predominance of Characiformes and Siluriformes orders (Albert et al. 2011, Hulsey andLópez-Fernández 2011), which included 83% of the captured species.In addition, the record of 18 of the 34 families listed by Buckup (1999) for Brazilian streams draws attention to the high richness of the Iguatemi river fish fauna, considering that only 3 streams were sampled.The families with the highest number of species in our study (Characidae, Heptapteridae, and Loricariidae) were also reported by Langeani et al. (2007) as the most species-rich in the upper Paraná river basin.Similarly, several studies have indicated the prevalence of these families in other streams of this basin (Casatti et al. 2001, Cunico et al. 2009, Súarez and Lima-Júnior 2009, Felipe and Súarez 2010, Pereira et al. 2014, Frota et al. 2016, Bifi et al. 2017).In addition, the most representative species in number of individuals, P. harpagos, A. aff.paranae, H. ancistroides, G. inaequilabiatus, and K. moenkhausii, were also numerically important in other surveys conducted in streams of the upper Paraná river basin (Casatti et al. 2001, Castro et al. 2004, Casatti 2005, Ferreira 2007, Daga et al. 2012, Mendonça et al. 2014).
It is also important to emphasize that the species richness of Água Boa and Santa Maria streams (both with 31 species) are well above those recorded in other streams of the upper Paraná river basin (see Casatti 2004, Rocha et al. 2009, Felipe and Súarez 2010), even including pristine streams (see Casatti et al. 2001).This finding once again highlights the role of the Iguatemi river basin in harboring a diverse fish fauna in its streams.In fact, the number of species recorded in the three streams inventoried here, accounts for 29% of the representativeness of ichthyofauna of the upper Paraná River floodplain presented by Graça and Pavanelli (2007), and 15% of the species of the Mato Grosso do Sul state recorded by Froehlich et al. (2017).Therefore, we advocate that the sampled area is intimately associated with maintaining the biodiversity of fish species in the floodplain, serving as refuges, and encompassing a good percentage of fish species of the state within a small area.
The high fish species richness of streams could be related to 3 main factors.The first concerns about the small body size of individuals inhabiting streams; the speciation rate is assumed to be inversely related to body size (Marzluff andDial 1991, Brown 1995).These habitats may contain more niches for small organisms than large ones; therefore, in principle, small-bodied species would be less prone to extinction (Purvis et al. 2003).The second factor is related to the environmental complexity of streams (Castro et al. 2003, Copatti andCopatti 2011) as the mosaic of pools, runs, and riffles clearly delimit different combinations of flow, depth, and substrate (Angermeier and Schlosser 1989); thus, it is expected that every mesohabitat hold unique species given the resources and conditions available.The third factor has to do with the degree of conservation of riparian vegetation, as fish species richness is positively associated with surrounding vegetation integrity (Ferreira and Casatti 2006).The deleterious effects caused by the removal of this vegetation bordering streams include: increased solar radiation and consequent rise in water temperature, reducing fish tolerance to toxic gases such as ammonia; development of toxic Cyanophyceae; the silting-up of the bed; reduced leaf, trunk, and branch inputs that shelter and provide substrate for the development of organisms consumed by the fish (Pusey andArthington 2003, Casatti 2010).These impacts can substantially alter the composition and abundance of fish assemblages inhabiting streams (Agostinho et al. 2007, Casatti et al. 2010).Whereas the riparian vegetation surrounding these streams is poor, due to anthropogenic action, the fish assemblages may already be under such deleterious effects.
This conception of constancy of species can illustrate the spatial occupation of fish assemblages (Begon et al. 2007), discriminating migrant and resident populations (Dajoz 1983, Langeani et al. 2005).The greatest number of accessory and occasional species recorded in Água Boa and Santa Maria suggests a high exchange of species between these streams and Iguatemi River, as long as fish may use these environments in the search for resources.Súarez and Petrere-Júnior (2006) drew similar inferences for Jogui region, Iguatemi river basin and Viana et al. (2013) for Bonito region, Ivaí river basin.
In addition, the fish fauna of the sampled streams was primarily composed of autochthonous species, following the pattern described for the species of the upper Paraná River (Langeani et al. 2007).Regarding the 5 allochthonous species, we may report that K. moenkhausii and S. brevipinna reached the upper Paraná river basin after the construction of Itaipu Reservoir (Júlio-Júnior et al. 2009).In turn, B. aff.gauderio and H. unitaeniatus were introduced by fishing activities, possibly as live bait, while the origin of G. inaequilabiatus in the basin is unknown (Langeani et al. 2007).Therefore, the presence of these 5 species in the streams highlights their dispersal abilities and success in the occupation of low order rivers.
In general, our study shows that streams of the lower portion of the Iguatemi river basin encompass a diverse fish fauna, in contrast to the anthropogenic impacts affecting the microbasins.This calls the attention to the urgency of primary management measures in the studied microbasins, such as the implementation and/or extension of soil conservation practices and riparian vegetation restoration, to help the maintenance of fish populations.

Figure 4 .
Figure 4. Percentages of number of specimens of each species with more than 100 individuals captured.

Figure 3 .
Figure 3. Percentages of the total number of sampled species in each family.

Table 1 .
Environmental features and sampled area at Água Boa, Perobão and Santa Maria streams.Site 1 = upper portion; Site 2 = intermediate portion; Site 3 = lower portion.Minimums and maximums are shown for width and depth.
Figure 2. Percentages of the total number of sampled species in each order.

Depth (cm) Flow conditions Stream bed Riparian vegetation Principal impacts
Stream Site Latitude (S) Longitude (W) Width (m) rapids & pools Rocky & sandy; slightly sinuous, with steep bank & limited downstream by a waterfall (about 3 m)

Table 2 ;
Astyanax paranae-Hoffmann et al. 2015: 4, fig.A1.H. Figure 5D.Elongated body; terminal mouth; inner row of premaxilla with 5 teeth, outer with 4 or 5, dentary with 8-13, and maxilla with 1 tooth.Complete lateral line with 38 or 39 pored scales; transversal series above lateral line with 5 or 5½ scale rows and below with 4 or 4½ scale rows.Dorsal fin with 11, pectoral fin with 15 or 16, pelvic fin with 9, anal fin with 17-23 and caudal fin with 19, total rays.Ground color silvery; dark vertically elongated humeral blotch followed by another similar dark humeral blotch, smaller than the first.Reddish fins.

Table 2 ;
Figure5W.TL); in larger specimens stripes can be broken or disappear, resulting in color pattern with darkbrown rounded or irregular blotches, especially on dorsal region of body; dark-brown bars wider than light bars.Hyaline fins, with scattered dark-brown spots.Body with 21 or 22 pairs of obliquely dark bands from the tail tip to nape.Pectoral and anal fins are uniformly dark gray, and the posterior part of the anal fin is pale.

Table 2 .
fig.A3.I.Elongated body; terminal mouth.Lateral line with 4 pores on upper series of plates.Dorsolateral series with 26-29 and ventrolateral series with 24-27 plates.Dorsal fin with I,7 or 8, pectoral with I,6, pelvic and anal fins with 6, total rays.Ground color pale brown to dark grey; dark fins with dark spots.Coracoid bone, between pectoral fins, covered by skin.
Material examined.