Rapid assessment of the ichthyofauna of the southern Guiana Shield tributaries of the Amazonas River in Pará, Brazil

ABSTRACT The Northern Pará Drainage System encompasses the left-bank tributaries of the Amazonas River in the southern Guiana Shield region of Pará state, Brazil. Five of the region’s state protected areas are considered strategic for the conservation of its biodiversity. In the present study, we assessed the ichthyofauna of the five state protected areas of the Northern Pará Drainage System. Seven expeditions were conducted between January 2008 and January 2009, which surveyed stretches of the Cuminá, Cuminapanema, Curuá, Jari, Mapuera, Nhamundá, and Paru rivers. These surveys yielded 286 species belonging to 38 families and eight orders, including seven new records of fish species for Brazil, six of which are also new records for the Amazon basin. Our results provide a valuable database for future research and conservation programs in the protected areas of the region.


INTRODUCTION
The Northern Pará Drainage System (NPDS) encompasses the left-bank tributaries of the Amazonas River in the southern Guiana Shield region of Pará state, Brazil. This area encompasses five strictly-protected or sustainable-use conservation units, as defined by the Brazilian National System of Conservation Units (Brasil 2000). Together with other types of federal protected areas, such as indigenous lands, the NPDS forms the Northern Pará Biodiversity Corridor, which connects the Central Amazonian Biodiversity Corridor with the Amapá VOL. 50(1) 2020: 24 -36 ACTA AMAZONICA Biodiversity Corridor, forming the largest biodiversity corridor found anywhere in the world (SEMA 2011a). This corridor encompasses the world's largest complex of protected areas, with a total area of almost 22 million hectares, which corresponds to 78% of the total area of the NPDS (SEMA 2010).
The Northern Pará Drainage System includes a number of important left bank tributaries of the Amazonas, such as the Nhamundá, Trombetas, Paru, Cuminapanema, Cuminá, Curuá, and Jari rivers. These rivers drain from the southern border of the Guiana Shield -a region of relatively high altitudes and aquatic ecosystems with characteristic features, such as rapids and streams with rocky beds -to the lowlands of the lower Amazon basin. This altitudinal gradient and the environmental heterogeneity of the region have been interpreted as important biogeographical and ecological factors that contribute to the high biodiversity of Amazonian fish (Lujan et al. 2013;da Costa et al. 2018).
The ichthyofauna of the Guiana Shield was reviewed by Vari et al. (2009), who listed 1148 species. This geographic region comprises four freshwater ecoregions, delimited by Abell et al. (2008), known as the Orinoco Guiana Shield, Essequibo, the Guianas, and the Amazonas Guiana Shield. The latter ecoregion coincides with the southern portion of the Guiana Shield, and most of the NPDS. Vari et al. (2009) noted that the ichthyofauna of northern Pará is known only from the study of Ferreira (1993), who surveyed the Trombetas River basin intensively. Although the NPDS includes a number of other tributaries of the Amazonas River, its ichthyofauna is still poorly known, and has been referred to by Dagosta and de Pinna (2017;2019) as a under-sampled area that lacks adequate fish inventory data. Given the logistic difficulties of reaching many isolated parts of the Amazon basin, the rapid sampling approach has become an important strategy for the production of preliminary checklists from poorly-known, but potentially diverse ecosystems, such as those of the NPDS, providing essential data for the development of effective conservation policies and management plans (Rapp Py-Daniel et al. 2007;Bernard 2008).
Between 2008 and 2009, the Museu Paraense Emílio Goeldi conducted seven expeditions to the state protected areas located in the NPDS to inventory its fauna and flora. The results were used to develop the management plans of the protected areas (SEMA 2010;2011a, b, c, d). Here, we present the checklist of the fish species sampled in the principal drainages of the five state protected areas of the Northern Pará Drainage System.

Sampled areas
The present study focused on five state protected areas ( Maicuru Biological Reserve (REBIO Maicuru). The FLOTA Faro is the smallest of these conservation units, with an area of 635,936 ha, and is drained primarily by the Nhamundá River, which separates the Brazilian states of Amazonas and Pará (SEMA 2011b). The FLOTA Trombetas covers an area of 3,172,978 ha, and is drained, from west to east, by the Trombetas, Cuminá (also known as the Erepecuru or Paru do Oeste), and Cuminapanema rivers (SEMA 2011c). The ESEC Grão-Pará is the largest of the protected areas, with a total area of 4,245,819 ha, which is drained by the headwaters of the Mapuera River, and parts of the Trombetas, Cuminá, Cuminapanema, Curuá, and Maicuru basins (SEMA 2011a). The REBIO Maicuru has an area of 1,151,761 ha, and is drained partly by the Maicuru, Paru, and Jari river basins (SEMA 2011d), while the FLOTA Paru covers a total area of 3,612,914 ha, and is drained primarily by the Paru River basin (SEMA 2010).
With the exception of FLOTA Faro, which is located in the central Amazonian lowlands, the state protected areas of the NPDS are located in the southern Guiana Shield, at altitudes of 100 to 500 m above sea level, with areas of both Amazonian rainforest and savanna vegetation (Vari et al. 2009). The headwater streams and rivers of these foothills have clear water, with visibility of up to 5 m, as observed in the Trombetas River. Most of the study area has a humid tropical climate (subtype Am in the Köppen classification), except for the northern extreme of ESEC Grão-Pará, which is classified as Aw (Peel et al. 2007).

Fish sampling and species inventory
We sampled 76 sites during seven expeditions to the five protected areas between January 2008 and January 2009 (Table 1; see Supplementary Material, Appendix S1 for information on each sampling site). The sampling sites included headwater streams, river channels and margins, and lakes ( Figure 2). During the FLOTA Faro expedition, we sampled 11 sites in the Nhamundá River basin, while in the FLOTA Trombetas, we obtained samples from 13 sites in the Cuminá River basin. In REBIO Maicuru, we sampled 10 sites on the Ipitinga River, a tributary of the Jari River basin, while in FLOTA Paru, we sampled nine sites in the Paru River basin. Given the enormous size of ESEC Grão-Pará, three expeditions were conducted in this area, including 14 sites in the Curuá River basin, denominated here as the "ESEC G-P South" sector, 11 sites at the headwaters of the Mapuera River (ESEC G-P North sector), and eight sites in the Cuminapanema basin (ESEC G-P Center sector). The number of points sampled in each type of environment (streams, river channels and margins, and lakes) at each locality is shown in Table 1.
Fish specimens were collected using standard fishing gear (hand nets, seine nets, and gill nets). The hand nets were circular, approximately 60 cm in diameter, with a 3-mm mesh. Seine nets of two sizes were used (2 or 5 m long), both 1.50 m high with a 5-mm mesh. The gill nets varied in length VOL. 50(1) 2020: 24 -36 ACTA AMAZONICA from 10 to 20 m, with heights between 1.8 and 2.5 m, and a range of mesh sizes (20, 40, 50, 60, 70, 80 and 100 mm).
Sampling effort was standardized among the different environments and collection methods. Hand and small (2 m) seine nets were used in streams, while the longer (5 m) seine nets were used in lakes and river margins, and the gill nets were set in lakes and rivers. At each stream, a stretch of 30 m was delimited, and four collectors each conducted 200 sweeps within the stretch, and the seine net was deployed 50 times. The lakes and river margins were also sampled with 50 sweeps of the seine net. The gill nets were set for approximately 24 hours, whenever possible, in lakes and river channels.
Once collected, the specimens were euthanized in a solution of clove oil, and fixed in 10% formalin for at

RESULTS
A total of 286 fish species were collected during the present study, representing 38 families and nine orders ( As already mentioned, ESEC Grão-Pará was surveyed during three expeditions. A total of 47 species were recorded in ESEC G-P South, representing 19 families and five orders. Eighteen of these species (corresponding to 38.3% of the fishes recorded in ESEC G-P South) were collected only in this sector. In ESEC G-P Center, 35 species were recorded, representing 16 families and five orders. Six of these species [Astyanax anterior Eigenmann 1908, Hyphessobrycon cf. agulha In addition to the species recorded in FLOTA Faro, which is located in the lowland Amazon basin, we recorded 179 species from the southern Guiana Shield tributaries of the Amazonas River. These species include 52 (29% of the total) that were recorded in the region for the first time (see Table 2), of which seven had not previously been recorded in Brazil. The species recorded in Brazil for the first time were

DISCUSSION
In general, the composition of the fish fauna of the Northern Pará Drainage System was typical of the Neotropical region, with a predominance of otophysians (Characiformes, Siluriformes and Gymnotiformes) and cichlids (Roberts 1972;Lowe-McConnell 1999;Reis et al. 2016). While the data were not analyzed statistically, the clear variation in the fish diversity of the study areas may be accounted for, at least in part, by the positive relationship between fish diversity and the high productivity of the várzea floodplain ecosystems of the lowland Amazon basin (Forsberg et al. 1993), with decreasing diversity coinciding with the altitudinal gradient (Lujan et al. 2013). At one extreme, FLOTA Faro and FLOTA Paru, which are located in the lowest part of the study area, had the highest fish diversity, whereas the ESEC G-P North, located at the highest altitudes, had the smallest number of fish species. A decline in fish diversity at higher altitudes is typical of the Neotropical region (e.g., Albert et al. 2011;Lima and Ribeiro 2011;da Costa et al. 2018).
In addition to their greater productivity, Dagosta and de Pinna (2019) also discussed the role of the interconnectivity of lowland watercourses, which tend to facilitate the dispersal of taxa with more ample geographic ranges. By contrast, upland areas tend to be more isolated from neighboring watercourses, resulting in higher endemicity and reduced diversity in comparison with lowland areas. The altitudinal gradient may also represent a key environmental filter for the composition of the fish assemblage, reinforcing the complementarity of the features of different aquatic ecosystems in terms of the conservation of fish diversity. For example, loricariid species predominated in areas of higher altitude (FLOTA Trombetas and ESEC G-P North), while these fish were much less diverse in lowland areas. Areas of higher altitude typically have more rocky substrates and faster flowing water, with an abundance of microhabitats, a type of environment that favors some groups of loricariids (Teresa et al. 2016). In the lowland areas, the higher fish diversity recorded in our study may be related to the variety of aquatic ecosystems sampled, including lakes, streams, and large rivers, in contrast with the headwaters streams, that were the only bodies of water available for sampling in the upland areas.
Six species were recorded for the Amazon basin for the first time. Hyphessobrycon georgettae was previously known only from Suriname, while Jupiaba potaroensis and Phenacogaster simulata had only been recorded in Guyana, and J. keithi in French Guiana (Vari et al. 2009). Corydoras guianensis was known to occur in both French Guiana and Suriname, whereas C. oxyrhynchus was previously considered to be endemic to Suriname

CONCLUSIONS
The RAP assessment of the ichthyofauna of the Northern Pará Drainage System provided valuable insights into the fish diversity of the region, contributing an important database for future research and conservation programs. Further expeditions to the NPDS may nevertheless reduce gaps in the ichthyological, taxonomic, and geographic knowledge of this megadiverse group in the Amazon basin. VOL. 50 (1)