Ichthyofauna from the Parque Nacional da Serra dos Órgãos and its surrounding areas , Rio de Janeiro state , Brazil

This study provides a list of freshwater fishes of the Parque Nacional da Serra dos Órgãos (PARNASO; Rio de Janeiro state, Brazil) and its surrounding areas. Fish samplings were performed by electrofishing during the dry season (2010 –2011) in three different areas: 1, inside of the PARNASO (2 sites); 2, in the buffer zone (4 sites); and 3, in adjacent areas (8 sites). A total of 47 fish species in 13 families and six orders were recorded. Fish composition within the limits of the PARNASO differed from that recorded in the adjacent area, with the latter having comparatively higher species richness. The buffer area had intermediate ichthyofauna composition between the two other areas. This study enhanced knowledge on the composition and structure of the fish assemblages in PARNASO, by recording the occurrence of six new species within the park that were not included in the Management Plan of this Conservation Unit.


INTRODUCTION
The Atlantic Rain Forest, located mostly on the eastern Brazilian coast, presents high species richness but it is under heavy anthropogenic pressure that has devastated large forested areas (Ribeiro et al. 2009).This tropical forest was one of the largest biomes in the Americas, covering ca.150 million ha (Ribeiro et al. 2009).The early exploitation of the forest dates from the beginning of the colonization of Brazil, 500 years ago.Nowadays, only 12.9% of its original cover remains forested (Tabarelli et al. 2010).The majority of remaining forest cover are small fragments (<100 ha) while the largest forested areas are located in cliffs and stepped areas that difficult access of humans (Ranta et al. 1998;Silva et al. 2007;Ribeiro et al. 2009).Because heavy vegetation losses and high endemism degree, the Atlantic Rain Forest is considered one the largest hotspots in the world (Myers et al. 2000;Miranda 2012).The Atlantic Rain Forest has a rich ichthyofauna, estimated about 270 species, belonging to 89 genera and 21 families (Abilhoa et al. 2011;Miranda 2012).However, there are several doubts on species descriptions and on the ecological processes such as heavy water turmoil and vegetation influences on fish assemblages (Guimarães et al. 2010).Despite the high biodiversity in the Atlantic Rain Forest, anthropogenic activities have jeopardized this system and there are few studies on streams fish composition and structure (Myers et al. 2000;Miranda 2012).
Conservation Units have been proposed to mitigate human impacts on biodiversity.The Parque Nacional da Serra dos Órgãos (hereafter PARNASO) (Figure 1), one of the oldest Brazilian conservation units, was created in 1939, and nowadays occupies an area of 20,024 ha, covering parts of four municipalities of the Rio de Janeiro state: Petrópolis, Teresópolis, Magé and Guapimirim (ICMBio 2014).This conservation unit is one of the most important areas of environmental preservation of the Atlantic Rain Forest biome, located in a strategic area of the Serra do Mar.However, knowledge on the ichthyofauna from PARNASO is scarce because of the difficulty to access streams and rivers in the area, where headwaters are located in cliffs and steep park areas, with numerous waterfalls.
This study provides a list of freshwater fish species occurring in the PARNASO and surrounding areas.The surrounding areas were divided into two zones: 1, buffer zone, which is subject to specific rules and restrictions to minimize anthropogenic impacts on the surrounding park area; and 2, adjacent area, which is the surrounding the buffer zone where the conservation unit rules do not reach.We also evaluated the role of the environment protection on the fish assemblage, as well as the

Lists of species
the surrounding park area and to reduce damage on the conservation unit.The adjacent area is located near to the park but is not subject to conservation rules.
Fish and habitat surveys were conducted at 14 sites, which drain to Guanabara Bay in the Atlantic Rain Forest biome (Permit n° 17632-2/ICMBio), distributed within the PARNASO limits (2 sites), in the buffer area (4), and in the adjacent area (8) (Figures 1 and 2).The sites were chosen on the basis of accessibility, and they are first to third streams order, with mean stream width ranging from 0.5 to 15 m (Table 1).Fish samplings were carried out during the dry season (May to October) in 2010 (12 sites) and 2011 (2 sites) to standardize the seasonal context.As descripted in Terra et al. (2013), a site was extended upstream for 40 times the mean wetted channel width, or a minimum of 100 m and a maximum of 500 m.
Each site was surveyed by electrofishing, with alternating current generator (3000 W, 110/220 V) provided by two hoop-shaped (440 mm × 300 mm) anodes supporting a net (3 mm mesh).Two people, each with an anode, fished from one edge to the other removing all fishes detected in the electric field.All collected fish were fixed in 10% formalin and, after 48 hours, preserved in 70% ethanol.All individuals were identified to species, counted and weighed (g).Vouchers were deposited in the fish collection of the Laboratory of Fish Ecology, Universidade Federal Rural do Rio de Janeiro and in the Special Teleost an Fish Collection of the Universidade Federal do Rio de Janeiro (Appendix 1).

Statistical test
We calculated abundance (N), biomass (B) and frequency of occurrence (FO%) to each species for a consequences of impacts from non-protected areas on fish assemblage diversity.Although only the most accessible sites were searched, we also describe fish structure assemblage.We believe this study can contribute to an update of species composition in reference to the management plan estimates and reinforce the importance of conservation unit on fish diversity maintenance.

Sampling design
The streams sampling sites included in this study were distributed inside of the PARNASO area, in its buffer area, and in the adjacent area.The buffer area is defined according to the Brazilian law (n° 9.985/2000) as the area in which human activities are subject to specific rules and restrictions to minimize anthropogenic impacts on  fish assemblage description (Table 2).The frequency of occurrence was calculated from the number of samples in which each species was observed in relation to the total number of sampling sites.The abundance and biomass were calculated based on the total of individuals and weights for each species, respectively.With the objective of identify differences in fish assemblages composition among areas (PARNASO, buffer zone, and adjacent area), we performed a Non-Metric Multidimensional Scaling (MDS).The resemblance matrix was based on Bray Curtis similarity and this analysis was performed in PRIMER 6 with PER-MANOVA+ software (Clarke and Gorley 2006).

RESULTS
We collected a total of 4,617 individuals belonging to 47 species, 13 families and six orders (Table 2).Siluriformes represented 42.6% (20 species) of the total number of species, followed by Characiformes with 32% (15 species).Cyprinodontiformes were represented by six species, Perciformes by three, Gymnotiformes by two and Synbranchiformes by only one species.Characidae was the family with the highest number of species (13 species), followed by Loricariidae (11 species).The Characidae family also had the highest number of individuals (40% of the total number of individuals), followed by Poeciliidae (15% of individuals).
Astyanax taeniatus (Jenyns, 1842) represented 19.2% of the total number of individuals and 22% of total biomass, occurring mainly in streams in the buffer area.Poecilia reticulata Peters, 1859 was the second most abundant species (12% of the total number of individuals); however the second highest biomass was recorded for Rhamdia quelen (Quoy & Gaimard, 1824) (15%).Phalloceros harpagos Lucinda, 2008 was the most frequent species, occurring in 10 of the 14 streams.Poecilia reticulata and Xiphophorus sp.(only one individual in the adjacent area) were the only recorded non-native species.
A total of 12 species was recorded within the PARNASO limiting area (Table 2), therefore doubles the number of species originally recorded in the management plan for the conservation unit.One of the six species previously recorded in the park management plan (Trichomycterus goeldii Boulenger, 1896) was not recorded in this study.We collected Characidium vidali Travassos, 1967 and the management plan listed Characidium sp.n., although we cannot ensure they are the same species.Fish assemblage composition within the PARNASO limits differed from those recorded in streams from the adjacent area (Figure 3).Moreover, streams in the buffer area have intermediary ichthyofauna composition between the PARNASO and the adjacent area.Two species were found only in the sites within the PARNASO limits (Crenicichla lacustris (Castelnau, 1855) and Trichomycterus cf.paquequerense (Miranda Ribeiro, 1943)  2, Hypostomus sp., Astyanax sp., Callichthys callichthys (Linnaeus, 1758), and Kronichthys heylandi (Boulenger, 1900) were collected only in the buffer area, whereas other 11 species were found only in the adjacent area.

DISCUSSION
The predominance of Siluriformes and Characiformes as main components of the ichthyofauna of the Atlantic Rain Forest streams was expected because they are the dominant orders in Neotropical freshwater systems (Lowe-McConnell 1999;Abilhoa et al. 2011) and were also observed in Atlantic Rain Forest streams (Casatti et al. 2001;Sarmento-Soares et al. 2007;Ferreira and Petrere 2009).The opportunist species Astyanax taeniatus and Poecilia reticulata that had the highest total number of individuals colonized several types of habitats.Characins inhabit several aquatic habitats such as streams, rivers, lagoons and reservoirs in different levels of environmental quality, whereas the poecilids are known for their capacity to colonize a wide range of degraded habitats tolerating low water quality where other species cannot tolerate (Araújo et al. 2009;Teixeira et al. 2005).
From species that were exclusively collected within PARNASO limits, Crenicichla lacustris is a widely distributed species over coastal drainages of the Southeastern and Eastern Brazil (FishBase 26/11/2014).However, T. cf.paquequerense that was considered endemic for the Paquequer River basin (also located within the PARNASO limiting area) was recorded for the first time in this study for the Soberbo River.This species is typical of cold and turbulent waters with special habitat requirements.
In the buffer zone, we found both, species more sensible to environmental disturbance (e.g., sewage discharges, channelization, lack of riparian cover) such as R. transfasciatus, and more tolerant species to environmental degradation such as the non-native P. reticulata, the characins of Astyanax genera and the siluriformes Rineloricaria sp. 2. In the adjacent area where human interference such as residences near the stream margins, small dams for recreation, poultry activities, small plantation, among others we recorded species typical of lowland areas that inhabit sites with comparatively high temperature and with high pool availability.
Altitude has been reported as an important environmental variable determining fish assemblage structure in streams (Ferreira and Petrere 2009).However, fish responses to altitudinal gradient can be confounding with anthropogenic impacts that are more common in low altitudes.Streams within the PARNASO limits and in its buffer area have comparatively higher altitude and have comparatively lower species richness that are associated with fast waters (rapids and runs), higher dissolved oxygen and comparatively lower temperature (River Continuum Concept, Vannote et al. 1980).Species of Trichomycterus and the Characidium vidali are typical representative of such areas.On the other hand, decreasing slope, increasing temperature and high availability of pools contribute to changes in the substrate type of downstream sites favoring the occupation of the stream habitat by other species adapted to these conditions as we found in the adjacent area of the PARNASO.
This study contributed to enhanced knowledge on the fish assemblage composition and structure in the PARNASO streams, recording six new species for the area that were not included in the management plan of this conservation unit.Knowledge on the community's composition and distribution is a main concern considering the high pressure of human activities on several of the world aquatic ecosystems (Duncan and Lockwood 2001;Aquino et al. 2009).This is a main step to elaborate and to establish management plans aiming conservation and recovery of aquatic ecosystems.

Figure 1 .
Figure 1.Map of the study area, indicating the 14 Atlantic Forest stream sites, in the Parque Nacional da Serra dos Órgãos (PARNASO) and its surrounding areas, southeastern Brazil.BA= Buffer area.Map given by Parque Nacional da Serra dos Órgãos (adapted).The altitude of the sites is given inTable 1.

Figure 2 .
Figure 2. Stream pictures indicating the 14 Atlantic Rain Forest stream sites arranged according to their position in relation to Parque Nacional da Serra dos Órgãos.Numbers in each picture indicates their code.Odd numbers correspond to first distance from top to bottom.The arrow with numbers indicates the distance in meters from the park boarder.
Camilo et al. | Ichthyofauna from the Parque Nacional da Serra dos Órgãos

Figure 3 .
Figure 3. MDS plots of fish assemblages at each of the 14 Atlantic Rain Forest sites based on Bray-Curtis similarity measures.The species associated with the sites were shown in the bottom of the figure.The distance from each site sample to the PARNASO is shown using scaled bubbles.Scale of bubbles 0 -4000 meters.A= adjacent area and B= buffer zone.

Table 1 .
Physical characteristics of the 14 Atlantic Forest stream sites sampled in the Parque Nacional da Serra dos Órgãos and its surrounding areas, southeastern Brazil.

Table 2 .
List of species collected in the 14 Atlantic Rain Forest stream sites sampled in the Parque Nacional da Serra dos Órgãos, buffer zone and its adjacent areas.N = Number of individuals.B = Biomass in grams.FO% = Frequency of occurrence.X = Species recorded in the PARNASO Management Plan.Gray color indicates species sampled in within the area.Camilo et al. | Ichthyofauna from the Parque Nacional da Serra dos Órgãos