Ichthyofauna from floodplain lakes of Reserva de Desenvolvimento Sustentável Piagaçu-Purus (RDS-PP), lower rio Purus

The ichthyofauna of the rio Purus has been little investigated, especially in its lower portion, characterized by diverse aquatic environments, especially in flooded areas. We inventoried the ichthyofauna of floodplain lakes with different management efforts in Reserva de Desenvolvimento Sustentável Piagaçu-Purus (RDS-PP), which represent important resource for commercial fishing in North region, in the first illustrated inventory of the fish fauna from lower rio Purus. We surveyed 20 lakes, classified as open access (eight lakes) and protected (12 lakes) during 2009 low water levels. A total of 2,299 individuals were collected, represented by seven orders, 25 families and 74 species. Characiformes was the most representative order in number of species and families, followed by Siluriformes, Cichliformes, Gymnotiformes, Clupeiformes, and Osteoglossiformes. Most abundant and frequent species were Pygocentrus nattereri, Triportheus angulatus, Serrasalmus sp. “2n=58”, Pterygoplichthys gibbiceps, and Osteoglossum bicirrhosum. Protected lakes presented higher species richness compared to open access lakes. Similarly, protected lakes possessed 26 species occurring exclusively, with emphasis on Colossoma macropomum, an important species for fisheries due to its commercial importance. We added 44 new records of fish species for the lower rio Purus. Our results indicate the potential efficiency of zoning systems of open access and protected lakes established by local population and ruled by RDS-PP for fisheries management. Therefore, we strongly suggest its maintenance for conservation of ichthyofauna of floodplain lakes of lower rio Purus.


Introduction
The Amazon basin is the largest and most diverse hydrographic system on Earth (Goulding et al. 2003), covering an area of over 8,000,000 km 2 (Sioli 1984), comprising almost 20% of the total river water in the world (Reis et al. 2016). Diversity of ichthyofauna inhabiting the Amazon basin comprises 60 families, 529 genera, and almost 2,720 described species, from which more than 60% are endemic to the basin (Dagosta & de Pinna 2019). However, this number might be underestimated, because new species descriptions are increasing fish species richness abruptly (Hoorn & Wesselingh 2010, Dagosta & de Pinna 2017. The Western Amazon (or Lowland Amazon) is drained by whiteor muddy-water rivers with headwaters in the Andes (i.e., Solimões, Madeira and Japurá) and by tributaries draining the western lowlands as Purus and Juruá (Lima & Ribeiro 2011), composing the floodplains popularly known as várzeas (Sioli 1984). This region is characterized by elevated load of sediments and dissolved inorganic solids (Sioli 1984, Goulding et al. 2003. The fish species richness in Lowland Amazonia is directly related to the exceptional diversity of the floodplains (Crampton 2011) and might also be influenced by the tributary effect that enriches the species diversity of Amazon mainstream, especially the white water tributaries from the Western region (Fernandes et al. 2004).
The rio Purus is one of the largest tributaries of the rio Solimões, with an extension of 2,765.65 km (Melo 2012) from its sources in Peru until its confluence on rio Solimões, at Amazonas State. It represents the largest fishing productivity of Amazon basin compared to other major white-water tributaries (Petrere 1978, Batista 1998, 2003, however, the efforts are concentrated in a few species, from which only 12 represent 80% of the fish landed in the main ports of Amazonas State (Barthem & Fabre 2003). Despite this potential, few studies were conducted in order to investigate the ichthyofauna of this basin. Most focused on the upper portion of the river, with 48 species recorded in the río Macauhan (tributary of río Yaco) (La Monte 1935), 86 species in Caeté and Macapá rivers (Anjos et al. 2008), and 94 species in rio Acre (Claro-García et al. 2013). The investigations in lower rio Purus registered higher number of species: 180 by Rapp Py-  in flooded areas, and approximately 110 species in two sandy beaches of Reserva Biológica de Abufari and Reserva de Desenvolvimento Sustentável Piagaçu-Purus (RDS-PP) (Duarte et al. 2010).
The RDS-PP was created in 2003 by the Amazonas State Government, to conciliate usage of natural resources with socioenvironmental sustainability. The region was deeply exploited for terrestrial and aquatic resources during the first half of twentieth century (Vieira et al. 2015). Activities as fishing, hunting, and practice of small-scale agriculture and extractivism are allowed to approximately 60 communities with 4,000 residents , IPI 2010. Fishing rules agreement determining management practices and fisheries areas were established in 2008 by local population and signed in agreements. Floodplain lakes were divided in a zoning model into two categories: open access and protected. In open access lakes subsistence and commercial fishing are allowed, while in protected lakes commercial fishing is prohibited (IPI 2010). The zoning model adopted in RDS-PP is similar to the model pioneered in RDS-Mamirauá (Queiroz & Crampton 1999).
The reserve is comprised of both upland terra firme landscapes and flooded forests, the latter representing 45% of its area, more concentrated on its North region, on the interfluve of Solimões and Purus rivers IPI 2010). The confluence of Purus and Solimões rivers generates a large floodplain area in the lower portion of the basin, with many environments still unexplored, which require huge sampling efforts to improve the fish fauna knowledge and fisheries consequences in natural sources. In this study, we sampled, for the first time, floodplain lakes in RDS-PP, with different management efforts, that represent important resources for commercial fishing in North region. Therefore, the main goals of this study were: (i) register the composition of fish species that occur in the RDS-PP floodplain lakes of different zoning model categories: open access and protected; and (ii) provide the first illustrated inventory of the ichthyofauna from floodplain lakes of lower rio Purus basin.

Study area
The Reserva de Desenvolvimento Sustentável Piagaçu-Purus (4°03'-5°25'S and 61°40'-63°30'W) comprises 834,245 ha situated along the lower rio Purus basin (Fig. 1), 223 km upstream from Manaus, capital of Amazonas State (Vieira et al. 2015). Surveys were carried in 20 floodplain lakes of the RDS-PP between October and November 2009, during low water levels on lower rio Purus (Tab. 1). Lakes were chosen according to access availability, and were previously classified by the zoning model as eight open access and 12 protected (Fig. 1).

Data Collection
Sampling efforts were standardized for all lakes. Fishing gear consisted in a set of stationary gillnets (10 m length) with mesh sizes 40, 60, 80, 100 and 120 mm between opposite knots, exposed for 24 hours starting at 6:00 AM, with harvests at fours hours. The exposure time was defined in order to minimize the damage caused by piscivorous fish, dolphins and alligators to gillnet and fish caught.

Fishfauna
The classification of families and subfamilies were presented in alphabetical order due to the many changes in the current classifications, and the lack of congruence or resolution regarding the relationships between them. The nomenclatural arrangement and classification of groupings in levels higher than family and family names followed Betancur-R. et al. (2017). Sub-families of Characidae followed Mirande (2018), and of Loricariidae followed Armbruster (2004), with the exception of Rhinelepinae, which is according to Lujan et al. (2015). Identification follows Menezes & Géry (1983), Kullander & Ferreira (2006), Santos et al. (2006), Bristki & Birindelli (2008)

Results
A total of 2,299 individuals were collected, distributed in seven orders, 25 families and 74 species (Tab. 2, Figs. 2-4). Characiformes was the most representative order in number of species and families (44 and 14, respectively), followed by Siluriformes with 20 species and six families ( Fig. 5), Cichliformes, with only one family but five species, and Gymnotiformes (two species in two families). Clupeiformes, Osteoglossiformes and Perciformes were less representative, with only one species each.
Characiformes and Siluriformes presented major number of species. The families with higher species richness were Serrasalmidae (12 species), Curimatidae and Pimelodidae (7 species), and Loricariidae (5 species) (Fig. 6). Highest abundances were also observed for Characiformes and Siluriformes with 1,888 and 279 individuals respectively.
Protected lakes presented higher species richness (62 species) compared to open access lakes with 48 species collected (Table 3). Similarly, protected lakes possessed 26 species occurring exclusively in this category (e.g., Brycon spp., Colossoma macropomum, Curimata inornata, Hypophthalmus spp., and Pseudoplatystoma spp.), while in open access lakes this number was reduced to 12 species (e.g. Loricariichthys acutus, Mylossoma aureum, and Semaprochilodus taeniurus). However, beyond the dominance of Characiformes and Siluriformes in both type of lakes, Cichliformes did not occur in protected lakes, while in open access lakes five species were collected, including commercially important as (Astronotus ocellatus and Cichla monoculus). Open access lakes presented higher abundance of Characiformes than protected lakes, mainly due to the participation of P. nattereri (Tab. 3).
Species accumulation curve is concerned with accumulation rates of new species over the sampled area and depends on species identity. Considering all lakes sampled, the species accumulation curve did not completely reach the asymptote (Fig. 7). Species richness expectation obtained by nonparametric estimators indicated that was collected 72% of the species expected to lakes by Jacknife estimate 1 (Jack1 = 107.4), 60% by Jacknife estimate 2 (Jack2 = 12, 5), 57.5% by Chao estimate (Chao = 133.89) and 85.8% according to the Bootstrap estimator.

Discussion
The ichthyofauna of floodplain lakes of RDS Piagaçu-Purus on lower rio Purus, as remaining freshwater regions of the world, is composed mostly by Ostariophysi, representing 88.2% of total richness. Characiformes presented higher families representativeness from which Serrasalmidae and Curimatidae composed 25% of all diversity surveyed by us. The predominance of these two families is different from previous results registered for lower rio Purus. From the 90 species inventoried using gillnets by Rapp Py- , mostly belong to Anostomidae (10), Serrasalmidae (8) and Hemiodontidae (6), whereas only Hemiodus sp. "rabo de fogo" and five species of anostomids were captured in the present study. The former study was developed during high water levels (June) and fish were sampled in different types of environments (lakes, paranás, igarapés and river channel), while the present investigation was performed in low water levels (October and November) strictly in lakes.
The lower rio Purus, next to its confluence with rio Solimões generates a large floodplain. Flooded areas are known by suffer seasonally dramatic changes in landscapes, modeled by the flood pulse (Junk et al. 1989). During wet period flooded forest consists an important feeding source of fruits and seeds, providing a wider diversity of habitat options, decreasing the density of possible predators (Winemiller & Jepsen 1998, Lowe-McConnell 1999. In low water ichthyofauna migrates to available habitats, including main river channel and permanent lakes, increasing predators occurrence in consequence of the reduction of suitable occupancy areas (Goulding 1980). These environmental differences are essential to the maintenance of life cycle of many fish species and biological interactions (Duarte et al. 2010). Despite the efficiency and selectivity of the use of a unique sampling effort (gillnet) we reached a representative number of species (74) and complemented available information of ichthyofauna from lower rio Purus, surveying for  2,7,9,12,15,17,18 32078, 48866 Continuation Table 2. the first time flooded lakes from RDS-PP during the dry season. As expected, composition of ichthyofauna changed significantly, with 44 new species recorded by us for this region.
The most abundant and frequent species, occurring in more than 60% of sampled lakes, including open access and protected, were Pygocentrus nattereri, Triportheus angulatus, Serrasalmus sp. 2n=58, Pterygoplichthys gibbiceps, and Osteoglossum bicirrhosum, all consumed by local population of RDS-PP. Similarly, in floodplain lakes of another reserve (RDS Mamiraua) in Solimões river, piranhas (Serrasalmus spp. and P. nattereri) and aruanã (Osteoglossum bicirrhosum) were the main collected species (Silvano et al. 2009). Osteoglossum bicirrhosum is a relevant artisanal fisheries resource in the entire Amazon (Lowry et al. 2005), and is also used as ornamental in aquarium trades (Santos et al. 2006). Apart from its intense exploitation, the aruanã was the third most abundant with the second highest biomass registered by us. This success can be attributed to the generalist feeding behavior, hunting along lake borders and flooded forests, allied to capacity of exploiting allochthonous food items during the high-water season (Saint-Paul et al. 2000, Lowry et al. 2005, Castillo et al. 2012, by leaping from the water to seek allochthonous prey, including terrestrial invertebrates (Aragão 1984, Goulding 1980) and small vertebrates (Verba et al. 2018).
In the comparison between the two lakes categories, open access presented less number of species (48 vs. 62 in protected). Nevertheless, from the 12 exclusively captured in these lakes, several possess elevated importance for artisanal and commercial fisheries, as Pellona flavipinnis, Semaprochilodus taeniurus, Mylossoma aureum, and the cichlids Astronotus ocellatus and Cichla monoculus, indicating the efficacy of choice of these lakes for fish exploration. On the other hand, the exclusive capture of Colossoma macropomum in protected lakes in RDS Piagaçu-Purus, indicates the efficiency of fishing management model adopted, that had already registered a major probability of capture and higher abundance of this species in protected lakes of RDS Mamirauá (Silvano et al. 2009).     However, this can be a consequence of the overexploitation of C. macropomum in open access lakes due to its relevance as feed source of protein for entire Amazon population, but not necessarily mean that such management actions have been ineffective. In marine systems, for example, the main goal of major management is to improve fisheries, allowing some fish landings in managed areas (common-based management), without affecting fish species diversity and ecological integrity (Mcclanahan et al. 1997). Though, the model of integral protection of the lakes adopted in RDS-PP focuses in whole habitat protection, preserving ecological patterns and complexity, and seems to be the factor supporting the ecological stability, beyond providing the local population the most appreciated species for feed consumption.
RDS Piagaçu-Purus provides legal context for monitoring wildlife along with the local population, gathering data and developing strategies for sustainable use. Additionally, it forms a mosaic of protected areas ruled by several different regimes, with two indigenous reserves (Terra Idígena Lago Ayapuá and Itixi Mitari), Reserva Biológica Abufari (REBIO) and Parque Nacional Nascentes do Lago Jari (PARNA), consisting an important region for conservation of ichthyofauna, especially considering fishing productivity of rio Purus. However, recent models of future deforestation in Amazonia predict an increase in the loss of vegetation cover for the RDS-PP, related to the reactivation of the road BR-319 (Manaus -Porto Velho), which percuss the interfluve between Madeira and Purus rivers (Soares-Filho et al. 2006, Fearnside et al. 2009, Vieira et al. 2015. Considering all registers published for the rio Purus basin (i.e. La Monte 1935, Rapp Py-Daniel & de Deus 2003, Fernandes et al. 2004, Anjos et al. 2008, Duarte et al. 2010Claro-García et al. 2013, and the present) 360 currently valid species compose the ichthyofauna of this river basin. Still, we strongly believe that this number is underestimated, with much of the basin still unexplored or only sparsely sampled. Our surveys beyond assessing and illustrating for the first time the ichthyofauna composition of floodplain lakes of RDS Piagaçu-Purus, revealed the occurrence of at least three new species for science in rio Purus, Hemiodus sp. "rabo de fogo", Myloplus aff. asterias (under description by RPO et al.), and Serrasalmus sp. 2n=58. Principally, our results indicate the potential efficiency of zoning systems of open access and protected lakes established by local population and ruled by RDS-PP for fisheries management. Therefore, we strongly suggest its maintenance for conservation of ichthyofauna of floodplain lakes of lower rio Purus.

Author Contributions
Bruno Ferezim Morales: Substantial contribution in the concept and design of the study, contribution to data collection, analysis and interpretation, contribution to manuscript preparation, contribution to critical revision, adding intellectual content.
Rafaela Priscila Ota: Substantial contribution in the concept and design of the study, contribution to data collection, analysis and interpretation, contribution to manuscript preparation, contribution to critical revision, adding intellectual content.
Victória Dandara Pereira e Silva: Contribution for data collection, analysis and interpretation, contribution to critical revision, adding intellectual content.
Cláudia Pereira de Deus: Substantial contribution in the concept and design of the study, contribution for data collection, contribution to critical revision, adding intellectual content.