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Fishes from the upper Yuruá river, Amazon basin, Peru

We report results of an ichthyological survey of the upper Rio Yuruá in southeastern Peru. Collections were made at low water (July-August, 2008) near the headwaters of the Brazilian Rio Juruá. This is the first of four expeditions to the Fitzcarrald Arch an upland associated with the Miocene-Pliocene rise of the Peruvian Andes with the goal of comparing the ichthyofauna across the headwaters of the largest tributary basins in the western Amazon (Ucayali, Juruá, Purús and Madeira). We recorded a total of 117 species in 28 families and 10 orders, with all species accompanied by tissue samples preserved in 100% ethanol for subsequent DNA analysis, and high-resolution digital images of voucher specimens with live color to facilitate accurate identification. From interviews with local fishers and comparisons with other ichthyological surveys of the region we estimate the actual diversity of fishes in the upper Juruá to exceed 200 species. Introduction The freshwater fish fauna of tropical South America is among the richest vertebrate faunas on Earth, with more than 6,000 species representing about 46% of the world’s 13,000 freshwater fish species, and perhaps 10 % of all known vertebrate species (Vari and Malabarba 1998; Reis et al. 2003). At the core of this region lies the Amazon basin, the greatest interconnected freshwater fluvial system on the planet, discharging approximately 16% of the world's flowing freshwater into the Atlantic Ocean (Goulding et al. 2003). The diversity of South American freshwater fishes is centered on the Amazon basin. The alpha diversity of Amazonian ichthyofaunas is very high, with many floodplain faunas represented by more than 100 locally abundant resident species (e.g., Crampton 1999; Petry et al. 2003; Correa et al. 2008). The Yuruá river rises in the department of Ucayali in Peru and runs into Brazilian territory, where it is known as Juruá river. The Juruá river is a tributary to the Solimões river (Brazil) in the Amazon basin with more than 90 % of its length flowing through Brazilian territory. The river has an extensive number of meanders, a huge floodplain, and is studded with thousands of oxbow lakes. The Juruá contributes about 4% of the total Amazon discharge (Goulding et al., 2003). One of the earliest fish studies in the Rio Yuruá basin was made by La Monte (1935), who presented a fish list with 37 species from the Envira river, an upper tributary to the Juruá in Brazil. Other studies in the upper portions of Juruá river basin include Silvano et al. (2000; 2001) presenting respectively 90 and 111 species from the Brazilian portion of this drainage, and Rengifo (2007), identifying a high diversity of 185 species from the Peruvian portion. Check List 5(3): 673–691, 2009. ISSN: 1809-127X


Introduction
The freshwater fish fauna of tropical South America is among the richest vertebrate faunas on Earth, with more than 6,000 species representing about 46% of the world's 13,000 freshwater fish species, and perhaps 10 % of all known vertebrate species (Vari and Malabarba 1998;Reis et al. 2003). At the core of this region lies the Amazon basin, the greatest interconnected freshwater fluvial system on the planet, discharging approximately 16% of the world's flowing freshwater into the Atlantic Ocean (Goulding et al. 2003). The diversity of South American freshwater fishes is centered on the Amazon basin. The alpha diversity of Amazonian ichthyofaunas is very high, with many floodplain faunas represented by more than 100 locally abundant resident species (e.g., Crampton 1999;Petry et al. 2003;Correa et al. 2008).
The Yuruá river rises in the department of Ucayali in Peru and runs into Brazilian territory, where it is known as Juruá river. The Juruá river is a tributary to the Solimões river (Brazil) in the Amazon basin with more than 90 % of its length flowing through Brazilian territory. The river has an extensive number of meanders, a huge floodplain, and is studded with thousands of oxbow lakes. The Juruá contributes about 4% of the total Amazon discharge (Goulding et al., 2003). One of the earliest fish studies in the Rio Yuruá basin was made by La Monte (1935), who presented a fish list with 37 species from the Envira river, an upper tributary to the Juruá in Brazil. Other studies in the upper portions of Juruá river basin include Silvano et al. (2000; presenting respectively 90 and 111 species from the Brazilian portion of this drainage, and Rengifo (2007), identifying a high diversity of 185 species from the Peruvian portion.
Here we report the result of an expedition to the Rio Yuruá, as part of a four-year survey project funded by NSF called "Proyecto Alto Purus". The goals of this project are to sample the headwaters of four major basins in Peru: Ucayali, Yuruá, Purus and Madre de Dios. These basins have a radial pattern rising in the Fitzcarrald arch, a major structural high of the Andes in the Amazon foreland basin (Espurt et al. 2007).

Materials and methods
Sixteen localities where sampled in the upper portions of the Rio Yuruá, department of Ucayali in Peru (Table 1, Figure 1). Field work was conducted from July 20 to August 11, 2008, for a period of 20 days during the dry season, in the area of the town of Breu (09°31' S, 72° 45' W, 271 m) on the upper Yuruá river in southeastern Peru, by James Albert (University of Louisiana at Lafayette), Roberto Quispe and Isabel Corahua (University of San Marcos, Lima). Three major types of environments where sampled: river channels and beaches (rios), stream runs and pools (quebradas), and oxbow lakes (cochas) (Figure 2). Rios are major rivers (i.e., Yuruá, Breu, Huacapistea), quebradas are small tributary streams, and cochas are oxbow lakes located on the floodplain. All collecting stations were georeferenced using GPS, and habitats were documented with high resolution digital photographs and written descriptions.  Table 1. Collections were made using standard ichthyological gear, including seine nets (5, 10 and 20 m, 5 mm between knots), dip nets, cast nets, traps, and hook and line. Electric fishes were located with the aid of a portable amplifier (Wells and Crampton 2006). A local fish-toxin called huaca (pronounced 'waka') was used in log jams of larger streams. In the upper Rio Yuruá leaves of the shrubby Clibadium remotiflorum (Asteraceae) are crushed and molded into a paste, and then washed through the water where a polyacetylenic compound, ichthyothereol, depletes the oxygen (Cascon et al. 1965;Czerson et al. 1979). After application most fishes float to the surface, except for certain loricariid taxa which tend to burrow deeper into the substrate. Fish mortality using the huaca of the upper Yuruá is very low and most specimens recover in minutes (JSA, pers. obs.). The fishes collected in upper Rio Yuruá were not poisoned; indeed huaca is biodegradable and commonly used by the local Ashininka communities for collecting fish for consumption.
A synoptic reference collection was accumulated in Breu, including one or more representative of all morphospecies encountered. Each lot in this reference collection was assigned a unique field number that was attached to each tissue sample, and accompanying digital photo(s) and unique voucher specimen. Tissue samples were excised using a sterilized scalpel and preserved in 100% ethanol in 1.8 ml vials, and then stored in a cool location at the base camp before transport to the laboratory. All voucher specimens were measured for standard length, individually labeled with plastic tags, fixed in 10% formalin for at least 48 hours in a closed Nalgene container or covered flat plastic tray (for larger specimens), and later transferred to 70 % ethanol in the laboratory.

Results and Discussion
A total of 117 species (Table 2) belonging to 28 families and 10 orders were captured and identified. The list of species and their respective occurrence environment are presented in Table 2. The families with highest species richness were Characidae (33 spp.); Loricariidae (18 spp.); Pimelodidae and Curimatidae (8 spp.). Half of the families (14) were represented by only one species. The most abundant orders were Characiformes (54 spp.) and Siluriformes (44 spp.), representing 46% and 37%, respectively, of the total fishes captured. Less abundant representatives, however, were the orders Perciformes (7 spp., 6%) and Gymnotiformes (5 spp., 4 %). In our study, except for Perciformes, the composition of ostariophysan orders is approximately the same as found throughout the Amazon basin, 43% Characiformes, 39% Siluriformes, 12% Perciformes, and 3% Gymnotiformes (Roberts 1972;Lowe-McConnell 1987). A relatively low diversity of Perciformes is also found in other studies in the upper portions of tributaries of the Amazon basin (4.7% in Anjos et al. 2008;4.4 % in Silvano et al. 2000). Perhaps the low diversity could be explained by the preference of cichlids to occupy lentic habitats within rivers and streams (Kullander 2003).
These results are part of a four-year project to survey and document the aquatic fauna of the upper Purus National Park, a poorly known, species rich and vulnerable region of tropical moist forests and flooded savannas in the Peruvian Amazon. From a biogeographic perspective, the upper Purus is located on the Fitzcarrald Arch, an upland associated with the Miocene-Pliocene rise of the Peruvian Andes (Campbell et al. 2001). The Fitzcarrald Arch contains the headwaters of four of the largest tributary basins in the western Amazon-Ucayali, Juruá, Purús and Madeira. Importantly, the upper reaches of these rivers are hydrologically isolated from one another. Analyses of radiometric and biostratigraphic data indicate that the Fitzcarrald Arch changed from a depositional to an erosional setting during the Late Miocene to Pliocene (c. 9-3 Ma.) (Potter 1997;Campbell et al. 2001;Harris and Mix 2002;Campbell et al. 2006;Westaway 2006) providing minimum age estimates for the genetic divergence of populations/species inhabiting these isolated basins (Sivasundar et al. 2001;Hrbek et al., 2002;Montoya-Burgos 2003;Albert et al. 2006;Hrbek et al., 2006;Lovejoy et al. 2006;Weir 2006). The Fitzcarrald Arch therefore represents an exceptional biogeographic setting: it is the only geological region contained entirely within the Amazon Basin for which we have reliable estimates of the timing of headwater basin separation.
Given the goals of the Alto Purus project to compare patterns of diversity and taxa across the Fitzcarrald Arch, the Alto Yuruá expedition was scheduled for the period of maximum low water. During this time fishes and other aquatic animals are concentrated in lakes and channels, and not dispersed onto the floodplain. Also the lack of rain and mud greatly facilitates transportation, by air, water and foot. In other words it would not have been possible to sample as many localities during the rainy season in the same number of field days, and each station sampled would have produced fewer specimens and species (Silvano et al. 2000). However, interviews with local fishermen suggest that several fish taxa are present or even abundant in the Alto Yuruá during the rainy season, that were not collected in our survey: e.g., potamotrygonids, Lepidosiren, Pellona, Semaprochilodus, Myleus, Brycon, Hydrolicus, cetopsids, auchenipterids, Eigenmannia, Rhamphichthys, and Colomesus. Much of the upper Yuruá traverses a relatively narrow and water-scourged channel (about 30 -50 m wide and 1-2 m deep at low water), with steep high banks (10 -20 m), sandy or muddy beaches, and little aquatic vegetation. These conditions are not favorable to many fish groups specialized to inhabit lowland Amazonian floodplains and deep river channels.
The diversity reported here compares with 111 species reported by Silvano et al. (2001) on two MacArthur Foundation supported expeditions (1993 and 1994) to adjacent areas of the upper Juruá in Brazil, and 133 species reported by Rengifo (2007) for two expeditions to the Peruvian region of the upper Yuruá in 2005 and 2006. In the ecologically similar upper Purus basin, Anjos et al. (2008) reported 86 species of fishes with just 22 of them being identified in our survey, indicating a very different fauna between these two Amazon tributaries. However, the main peril in comparing species list is the accuracy of the taxonomic identification between different studies. Most of the problems occur in groups widely distributed and those without recent taxonomic reviews in the Amazon basin (e.g. in Loricariidae: Ancistrus, Loricariichthys, Loricaria, Hypostomus, Hypoptopoma, and others), which make the diversity and distribution within these groups almost incomparable. In an effort to reduce this problem, we provided a complete album of the fish species in this paper (Appendix 1). By comparing our species list (with photos) with those presented in Silvano et al. (2001), we identify at least 50 morphospecies that were not captured in our survey. This brings to 167 the total number of fish species known from the upper rio Juruá basin. Taking into account the species presented by Rengifo (2007), we estimate that the ichthyofauna in the upper portions of Rio Juruá should surpass 200 species. Table 2. List of 117 fish species collected in the upper Yuruá river and their respective capture environment.
x x Loricarichthys sp.