Fish composition ( Teleostei ) of the estuarine region of the Macaé River , southeastern Brazil

The first checklist of fishes of the estuary of the Macae River (Rio de Janeiro State, Brazil) and its adjacent freshwater section is presented. A total of 24,157 specimens belonging to 110 species in 44 families and 21 orders of the Teleostei were collected based on quarterly samplings, between June 2011 and March 2012. The Sciaenidae was the most representative family in species number, whereas the Ariidae, Pristigasteridae, and the invasive Clariidae predominated numerically and/or in terms of biomass. One hundred fifty-seven species of the Teleostei are now recorded in the Macae River, including 68 species previously reported from its upper and middle portions. More than 100 of them permanently or temporarily inhabit the lower 16 km of the river, suggesting that the estuary is relevant to the maintenance of the fish diversity of the region in spite of several human activities that have significantly altered its natural features.


Introduction
Estuaries are relatively well-defined coastal water bodies open to the sea, where the salt content of freshwater is increased by a significant input of marine seawater (Cameron and Pritchard 1963;Pritchard 1967).Seawater intrusion and its pattern of circulation in the estuary are modulated by the amplitude of tides and variations in river discharge, among other geographic and hydrological parameters (Fairbridge 1980;Albaret et al. 2004).Those parameters vary along the length of the estuary, and have a strong influence on its physico-chemical properties (Drinkwater and Frank 1994;Grange and Allanson 1995).Estuaries are also highly relevant in biological terms.They are typically richer in nutrients than rivers or oceans, and thus exhibit a higher secondary production (Elliott et al. 2002).In addition to holding some resident species, estuaries are nursery and refuge grounds for different life-cycle stages of several marine organisms, being also relevant as migration routes for diadromous fishes (Whitfield 1990(Whitfield , 1998;;Blaber 1997;Potter and Hyndes 1999;McLusky and Elliott 2004).
The Macaé River has approximately 130 km from its headwaters, at an altitude of about 1500 m, to its mouth in the coastal plain at the city of Macaé, northern Rio de Janeiro State (Figures 1 and 2).The lower course of the Macaé River was extensively dredged in the 1960's.The naturally meandering estuary was also reshaped into a single, relatively large, straight channel by the federal government at the time in order to drain the floodplain and, supposedly, control tropical diseases such as malaria .As expected, most of the natural riparian vegetation of the estuary and nearby freshwater bodies was replaced by pasture and agricultural crops.

Abstract:
The first checklist of fishes of the estuary of the Macaé River (Rio de Janeiro State, Brazil) and its adjacent freshwater section is presented.A total of 24,157 specimens belonging to 110 species in 44 families and 21 orders of the Teleostei were collected based on quarterly samplings, between June 2011 and March 2012.The Sciaenidae was the most representative family in species number, whereas the Ariidae, Pristigasteridae, and the invasive Clariidae predominated numerically and/or in terms of biomass.One hundred fifty-seven species of the Teleostei are now recorded in the Macaé River, including 68 species previously reported from its upper and middle portions.More than 100 of them permanently or temporarily inhabit the lower 16 km of the river, suggesting that the estuary is relevant to the maintenance of the fish diversity of the region in spite of several human activities that have significantly altered its natural features.Sixty eight species of the Teleostei were recently recorded in the Macaé River (Brito 2007;Jaramillo-Villa 2010), but the fish composition of the estuary is still practically unknown.We therefore present the first comprehensive list of the species of the Teleostei known to temporarily or permanently inhabit the lower 16 km of the Macaé River, which includes the estuary and the freshwater region under its influence.

Study Area
The headwaters of the Macaé River are located in Pico do Tinguá, city of Nova Friburgo, Rio de Janeiro State (22°21′ -22°28′ S, 42°27′ -42°35′ W).The total drainage area of the basin is approximately 1765 km² (SEMADS 2001; Figure 1B).The riparian vegetation is highly variable and mostly related to different land uses.Stretches of relatively well-preserved Atlantic Forest are present on the upper portion of the river, whereas the lower course, where the estuary is located, is mostly characterized by pasture (Bizerril and Primo 2001).
The main channel of the lower 16 km of the Macaé River is relatively narrow and shallow, with a mean depth of approximately 3.0 m, and an average flow of 45.4 m 3 .s - (Weber 2001).In the estuary, tides are usually semidiurnal, ranging from about 1.0 m in spring and 0.5 m during neap tides.The mean annual temperature varies between 22 to 24°C, and the annual rainfall varies between 1000 to 1300 mm (Alvares et al. 2013), being mostly concentrated between November and April.

Sampling
Four quarterly campaigns were performed between June 2011 and March 2012 at five sampling non-equidistant stations (Figure 1C; Table 1), which include the salt wedge in the estuary (P0, P1 and P2; Figure 2A, 2B and 2C), and the freshwater section of the river under the influence of the estuary (P3 and P4; Figure 2D and 2E).Fishing equipment consisted of two sets of gill nets (mesh sizes 15, 20, 25, 30, 35, 40, and 45 mm), casting nets (mesh sizes 10, 20 and 25 mm), and a seining net (mesh size 5 mm) that was operated either with the aid of a motor boat on the deeper portions of the river, or manually at the margins of the river and at the beach.Sampling was complemented with sieves and dip nets at the vegetated banks and under macrophyte stands.Depth, salinity and temperature were recorded during sampling (Table 1).Fishes collected were fixed in a 10% solution of formalin immediately after collection, and later preserved in 70% alcohol.They were identified with the aid of several taxonomic guides and keys (e.g., Figueiredo and Menezes 1978, 1980, 2000;Menezes andFigueiredo 1980, 1985), original species descriptions, and comparisons with previously identified specimens deposited in fish collections, especially those of the Museu Nacional, Universidade Federal do Rio de Janeiro (MNRJ) and of the Núcleo em Ecologia e Desenvolvimento Socioambiental de Macaé, Universidade Federal do Rio de Janeiro (NPM).Names of genera and species follow Eschmeyer (2014).Suprageneric classification follows Wiley and Johnson (2010).Biometric data of specimens, including total length (TL, cm) and total weight (TW, g) were also recorded.The most representative species were considered as those that comprised 95% and 90% of total abundance and biomass, respectively.Selected specimens representing all species recorded in the estuary were deposited in NPM (Appendix).

Results
A total of 24,157 specimens (297 kg) was collected, which corresponds to 110 species in 44 families and 21 orders of the Teleostei (Table 2).The number of species in a single locality ranged from 25 to 69.When only the region identified as the main estuary is considered (P0, P1 and P2), 22,620 specimens belonging to 78 species were collected.Forty-one specimens of 8 species were exclusively recorded in P3 and P4.Only the bluefish Pomatomus saltatrix (Linnaeus, 1766) was recorded both at the upper and lowermost sampling stations (P4 and P0).
Species richness varied positively with salinity, but was inversely related to the distance from the sea.There was an abrupt reduction of 50% of the species number between P1 and P2, which are inside the estuary, where the greatest differences in water salinity between consecutive sampling stations were recorded (Figure 3, Table 1).When all stations are considered, species of the Sciaenidae, Engraulidae and Ariidae represented 30.0% of the total richness, with 13.64%, 8.18% and 8.18%, respectively, of the species recorded.Lower species richness were recorded in stations P2, P3 and P4.Species in those stations belong mostly to the Characidae, Cichlidae and Poeciliidae, families that basically include fishes of the Primary and Secondary Divisions of Myers (1938).The abundance of species among the three stations located farther from the sea (P2, P3 and P4) was more equitable when compared to stations P0 and P1.
The number of species recorded was higher in stations close to the sea (P0 and P1), but those stations were also characterized by few species that numerically dominated the catches (Table 2).Dominant species were the ariids Cathorops spixii (Agassiz 1829) and Genidens genidens (Cuvier 1829), which was by far the most abundant species in those stations, the engraulids Anchovia clupeoides (Swainson 1839), Anchoa tricolor (Spix & Agassiz 1829) and Lycengraulis grossidens (Agassiz 1829), the pristigasterid Pellona harroweri (Fowler 1917), and the haemulid Conodon nobilis (Linnaeus 1758) (Figure 4A; Table 2).A few species of the Centropomidae, Gobiidae, Mugilidae, Engraulidae and Syngnathidae were collected in four sampling stations, but no species were recorded in all five stations (Table 2).Together, species of the Ariidae, Engraulidae, Sciaenidae and Pristigasteridae comprised 89.76 % of the total abundance.The sum of the weights of all specimens of those families combined with those of the North African catfish Clarias gariepinus (Burchell 1822) (Clariidae) corresponds to 74.64% of the total biomass (Figure 4B).

Discussion
Eighty-nine species of the Teleostei were herein recorded for the first time in the Macaé River.A total of 157 species of that group is now reported for the river, including species previously identified by Brito (2007) and Jaramillo-Villa (2010).Species of the Ariidae, Engraulidae, Clupeidae, Pristigasteridae, Sciaenidae, Gerreidae, Sparidae and Haemulidae, which were numerically expressive in the catches, are also well represented in fish communities of estuaries of the tropical western Atlantic (e.g., Vieira and Musick 1994;Andrade-Tubino et al. 2008;Marceniuk et al. 2013).Those species are typically eurytopic and are therefore able to cope with a wide range of environmental conditions, especially salinity, which is considered as the main limiting factor regulating the occurrence of fishes in estuaries (Vieira and Musick 1993).
Species that live exclusively in tropical and temperate estuaries represent less than 13% of the total species richness of those environments (Day Jr. et al. 1989).As in other temperate and tropical estuaries, most species recorded in the estuary of the Macaé River might be regarded as opportunists or seasonally migrants.If that is the case, then the relevance of the estuary of the Macaé River to the maintenance of populations of several marine fishes that are probably using that environment for growth and development is reinforced.
The lower values of species richness recorded in stations P2, P3 and P4 might actually reflect the presumably smaller population sizes in the estuary and in the region under its influence of the more stenohaline freshwater species.Despite the environmental modifications that the lower Macaé River has been subjected to, rheophilic and relatively rare large species, such as the prochilodontid Prochilodus vimboides Kner 1859 and the anostomid Leporinus copelandii Steindachner 1875, were recorded.However, the region under study is now overrun by the North African catfish C. gariepinus, an exotic generalist predator that can reach up to 150 cm TL (Teugels 2003).That species was collected in all sampling occasions, at  least in one of the stations P2-P4.Clarias gariepinus is also frequently caught by local fishermen, usually in high quantities and sometimes in large sizes (Figure 5), strongly indicating that a viable population of the species is now established in the lower Macaé River.The occurrence of that highly resilient species in the region represents an additional threat to the indigenous ichthyofauna of the river, such as the fat sleeper Dormitator maculatus (Bloch 1792).Three juvenile specimens of that species, which exclusively inhabits the lower portion of Atlantic coastal drainages between southern North America and Uruguay (Volcan et al. 2010;Bastos et al. 2013;Duarte et al. 2013), were collected in one occasion in station P2 (

Figure 1 .
Figure 1.(A) Map of South America, study area indicated by the rectangle; (B) Macaé River drainage basin (dark grey), including the original configuration of rivers in light blue and the modern configuration of the channel of the Macaé River and some of its main tributaries in dark blue; (C) Location of sampling stations P0 -P4, with the urban portion of the city of Macaé in light brown.

Figure 2 .
Figure 2. Sampling stations, city of Macaé, Rio de Janeiro State: (A) P0, mouth of the estuary of the Macaé River; (B) P1 and (C) P2, inside the estuary, within city limits; (D) P3, downstream the confluence of the Rivers Macaé (left) and São Pedro (right); (E) P4, lower Macaé River, Serra do Mar escarpment in the foreground.

Figure 3 .
Figure 3. Variation in fish species richness (left axis, bars) and salinity (right axis, dots) in sampling stations P0 -P4 in the estuarine region of the Macaé River, Rio de Janeiro State, between June 2011 and March 2012.The distance from the sea is 0, 2, 5, 12 and 16 km for the sampling stations P0, P1, P2, P3 and P4, respectively.

Figure 4 .
Figure 4. Species that comprise (A) 95% of the numerical abundance and (B) 90% of the biomass collected in stations P0 -P4 in the estuarine region of the Macaé River, Rio de Janeiro State, between June 2011 and March 2012.

Figure 5 .
Figure 5. Local fisherman with a 65 cm SL specimen of the North African catfish Clarias gariepinus (NPM 1575) fished in the estuary of the Macaé River in June 2009, at station P2.

Table 1 .
Geographic coordinates of sampling stations and physico-chemical parameters measured during the study, between June 2011 and March 2012.Values represent the mean ± standard deviation of the quarterly samplings.

Table 2 .
List of species collected in the estuarine region of the Macaé River, northern Rio de Janeiro State, between June 2011 and March 2012.New records (NR), total length (TL, in cm) of the specimens, and numerical abundance in each sampling stations are presented.