Ichthyofauna of Marinheiros Island , Patos Lagoon estuary , southern Brazil

Marinheiros is the largest island of the estuarine archipelago of Patos lagoon and is considered an area of biological relevance in the coastal region of the extreme south of Brazil. Aiming to contribute to the knowledge on the biodiversity of this important area, we conducted an ichthyofaunistic inventory in the limnic environments of the island. Twenty-seven field trips were performed between April 2015 and May 2017. A total of 12 sites representative of habitats of an intermittent shallow lagoon, intermittent pools and a perennial artificial channel were sampled. Sampling of 2,436 specimens revealed the occurrence of 30 species, including the non-native piscivorous Acestrorhynchus pantaneiro. Characiformes was the most diverse order (18 species), followed by Cichliformes (four species) and Cyprinodontiformes (three species). Characiformes was also the most numerically abundant order (77%) followed by Cichliformes (17.6%) and Cyprinodontiformes (5.1%). The species richness recorded in Marinheiros Island is is comparable to the richness observed for lotic systems of southernmost Brazilian coastal plain. The fish assemblage is composed mainly of species of limnic habits whereas few taxa of estuarine-marine-limnic and estuarine-limnic habits were recorded. In view of the presence of allochtonous A. pantaneiro and its potential to impact native species, monitoring is recommended to the ichthyofauna of Marinheiros Island and the other estuarine islands, as well as peninsular systems connected to Patos lagoon estuary.


Introduction
Patos lagoon is the world's largest choked lagoon, extending over 240 km on the southernmost Brazilian coastal plain (Kjerfve 1986).The estuarine zone of Patos lagoon is characterized by the presence an archipelago composed by eight main islands and several islets emerged during the Holocene.Marinheiros is the largest island, covering an area of 62 km 2 .It is also the first to emerge from the estuarine submerged flats, at about 5,000 years ago, in a process of lagoon sediment deposition (Vieira 1983).
Studies on vertebrate fauna in Marinheiros Island date back only to the last decade and have already highlighted the island as an important area from the biogeographical and conservation perspectives in southern Brazilian coast.Sampling efforts on anuran (Quintela et al. 2007, 2009, Bernardo-Silva et al. 2012, Dalmolin et al. 2017), reptilian (Quintela et al. 2011) and avian fauna (Gianuca et al. 2007(Gianuca et al. , 2008(Gianuca et al. , 2012) ) in the insular environments have identified the occurrence of some unexpected taxa for the region, including the southernmost and isolated population of the threatened red-bellied toad Melanophryniscus dorsalis (Mertens, 1933) (Quintela et al. 2006, Bernardo-Silva et al. 2012).While some groups such as herpetofauna and avifauna are relatively well-known in the island, the ichthyofauna remained practically unexplored.Meanwhile, Marinheiros shelters a peculiar complex of intermittent shallow lagoons and pools, which consist of potential habitats for the fish fauna.
Marinheiros Island is separated from the mainland by approximately 1.7 km and remained isolated until the year 2004, when the establishment of a bridge linked it to an adjacent island (Leonídeo), which is in turn connected to Rio Grande peninsula.The easy access to Marinheiros resulted in the increase of anthropogenic impacts due to the expansion of settlements and a large increment on tourism and visitation.The insular limnic ecosystems, in particular, also face the threat of pesticides, used in a wide range in the local agricultural production (Quintela et al. 2009(Quintela et al. , 2011)).Thus, pollution and contamination represent potential risks to Marinheiros waterbodies and its associated biota.
Despite the aforementioned importance of Marinheiros for the local biodiversity, the island still lacks an effective plan for the management and conservation of ecosystems, in part due to the gap of knowledge on its biota.Herein, we present the first list of the ichthyofauna occurring in freshwater systems of Marinheiros Island, aiming to contribute to the knowledge on the faunistic diversity in this important area.

Study area
Marinheiros Island (31º58'-32º02'S; 52º05'-52º12'W) is located in the southern portion of Patos lagoon estuary, Rio Grande municipality, Rio Grande do Sul state, southern Brazil.The island is distant about 1.4 km from the adjacent Leonídeo island, 1.7 km from peninsular mainland (Rio Grande), and about 16 km from the estuarine mouth (Figure 1).The climate in Rio Grande municipality is classified as subtropical temperate (Cfa of Köppen), with temperatures varying from 9.5ºC (mean minimum) in midwinter to 27.2ºC (mean maximum) in midsummer.The average annual rainfall is 1,252 mm and the rainiest period is from July to September (Vieira 1983).
Hydrographically, Marinheiros Island is characterized mainly by a set of shallow lagoons and pools, strongly influenced by rainfall regime.Some systems can dry completely during periods of high evaporation although heavy rainfall periods can promote the interconnection of systems.Heavy rainfall may also result in the interconnection between internal systems and estuarine waters due to flooding of the peripheral areas of the island.The largest lagoon, locally know as "Lagoa do Rey", can extended over 3.3 km during rainy period while smaller lagoons range from ca. 150 to 700 m long.The coverage of marginal areas varies from sandy bottom to dense patches of emergent macrophytes Typha dominguensis Pers., Schoenoplectus californicus (C.A. Mey.) Soják and Scirpus spp.and deeper sections are colonized by the submerged rooted Cabomba caroliniana A. Gray.Bottom varies from sandy in marginal areas to muddy in deeper sections.A set of around 20 pools ranging from 7 to 20 m in length is located in the eastern portion of the island, know as "Marambaia".The marginal coverage of pools varies from sandy bottom to dense patches of emergent vegetation (mainly T. dominguensis and Scirpus spp.) and some systems are colonized by Nymphoides indica (L.) Kuntzae, Myriophyllum sp. and C. caroliniana.Both pools and lakes do not exceed 2.5 m in depth and have bottoms varying from sandy to muddy.In addition to these natural hydrographic elements, a pluvial channel extends along the 28 km of the island perimeter.This artificial system has an average depth of 0.8 m, muddy bottom, and can be densely covered by floating macrophytes (Azolla filiculoides Lam., Eichornia spp., Salvinia spp.) mainly in the warmer periods.

Sampling
Twenty-seven random samplings were conducted between April 2015 and May 2017.A total of 12 sites were sampled, covering environments of the shallow lagoon "Lagoa do Rey", the set of pools "Marambaia" and the pluvial channel (Table 1, Figure 2).Fishes were captured using the following gear: seine net 5 x 2 m, mesh size 5 mm; gillnet 20 x 2.5 m, mesh size 7 mm; hand net 0.60 x 0.40 m, mesh size 2 mm; funnel traps (length 0.74 m, diameter 0.38 m, mesh size 25 mm; length 0.60 m, diameter 0.32 m, mesh size 15 mm).Captured individuals were euthanized in clove oil solution, fixed in 10% formalin and preserved in 70% ethanol in the Fish Reference Collection of the Instituto de Ciências Biológicas at the Universidade Federal do Rio Grande (CIFURG) (Appendix).Specimens were identified with the help of specialized literature (Reis et al. 2003, Lucinda 2008, Malabarba et al. 2013).Collection was authorized by the Brazilian environmental agency ICMBio through license number 56947-1.Nomenclature of species and higher taxa follows Bertaco et al. (2016).

Results
A total of 2,436 specimens belonging to 30 species, 21 genera, 11 families and six orders was collected (Table 2).Characiformes was the order with the highest species richness (18 species), followed by Cichliformes (four species) and Cyprinodontiformes (three species).Characiformes was the most numerically abundant order (77%), followed by Cichliformes (17.6%) and Cyprinodontiformes (5.1%).Characidae was the most rich family (14 species) and also the most abundant family (74.8%).Cichlidae was the second most diverse (four species) and abundant family (17.6%).All species except Acestrorhynchus pantaneiro Menezes, 1992 (Figure 3) are native to Patos lagoon basin (Saccol-Pereira et al. 2006, Assumpção et al. 2016).The set of pools was the systems with the highest richness recorded (25 species), followed by the pluvial channel (13 species) and the shallow lagoon "Lagoa do Rey" (11 species).The characids Astyanax eigenmanniorum (Cope, 1894) and Hyphessobrycon luetkenii (Boulenger, 1887) were the most abundant species in the pools set and the shallow lagoon, respectively.The poeciliid Phalloceros caudimaculatus (Hensel, 1868) was the most abundant species in the pluvial channel.The number of collected specimens and the relative abundance of recorded species in each sampled system are given in Table 2.

Discussion
The limnic enviroments of Marinheiros Island house an ichthyofaunistic diversity within the range observed for lotic systems in southernmost Brazilian coastal plain, which is between 22 (Fortaleza lagoon; Schifino et al., 2004) and 67 species (Peixe lagoon ;Loebmann & Vieira 2005).It is clear the taxonomic and numerical dominance of order Characiformes, with family Characidae encompassing around 46% of the species richness and 75% of all specimens collected.The high diversity of Characiformes corroborates the general pattern found in Neotropical region (Reis et al. 2003), as well as the regional patterns observed in all of the limnic systems of the southernmost Brazilian coastal plain studied so far, where Characidae stands out as the richest family (Assumpção et al. 2016).The shallow depths of island systems are favorable to the occurrence of characids, which are referred as inhabitants mainly of shallow waters (Lowe-McConnell 1987).However, the most speciose order in Rio Grande do Sul state (Bertaco et al. 2016), Siluriformes, was poorly represented in the insular systems, with only two recorded species (Pimelodella australis Eigenmann, 1917 and Rhamdia aff.quelen Quoy & Gaimard, 1824).It is possible that the great predominance of shallow zones in the systems acts limiting the occurrence of species of this order, usually benthic and inhabitants of deeper zones (Malabarba et al. 2013).Cichlidae, the second most diverse family in Marinheiros, is also among the most rich fish groups in Neotropical region (Kullander 2003) and it is well represented in limnic environments of Rio Grande do Sul coastal plain (Assumpção et al. 2016).Moreover, the insular systems of Marinheiros present physiognomic characteristics such low depths, abundance of aquatic macrophytes and sandy bottoms, which are considered suitable for the cichlids occurrence (Malabarba et al. 2013).
Except by Jenynsia multidentata (Jenyns, 1824), Ctenogobius shufeldti (Jordan & Eigenmann, 1887) (both estuarine-limnic) and Dormitator maculatus (Bloch, 1792) (marine-estuarine-limnic), all the remain recorded species exhibit limnic habits (see Assumpção et al. 2016).Marinheiros Island, as well as the other estuarine islands in Patos lagoon estuary, is strongly subject to flooding during the periods of high precipitation and consequent high discharge of Patos-Mirim basin.Under this condition, estuarine waters overrun a considerable stretch of the borders of the island, including the peripheral freshwater systems.Thus, it was expected a higher representativeness of coastal marine and estuarine-related species which also inhabit freshwater coastal environments of the region, such as Atherinella brasiliensis (Quoy & Gaimard, 1825), Mugil spp., Micropogonias furnieri (Desmarest, 1823), Odontesthes argentinensis (Valenciennes, 1835), O. bonariensis (Valenciennes, 1835), Platanichthys platana (Regan,1917) and others (see Tagliani 1994, Loebmann & Vieira 2005, Garcia et al. 2006, Artioli et al. 2009, Bastos et al. 2013), were absent in our sampling.It should be noted that the insular systems were also sampled subsequently to the heavy rainfall period associated to last El Niño (2015-2016), when Patos Lagoon estuarine archipelago experienced severe flooding events.This fact can be related to the strong influence of the precipitation in the insular systems, which may decrease the salinity in short time after estuarine floods, making the environments little attractive for the coastal and estuarine-related species.
In the southernmost Brazilian state of Rio Grande do Sul, A. pantaneiro is considered autochthonous solely for Uruguay basin (Menezes 2003, Saccol-Pereira et al. 2006).About a decade, it also has been found in Patos-Mirim and Tramandaí basins (Saccol-Pereira et al. 2006, Leal et al. 2009, Artioli et al. 2013, Rocha and Hartz 2013, Einhardt et al. 2014, Corrêa et al. 2015, Neuhaus et al. 2016), where it is considered an invasive species in rapid expansion (Neuhaus et al. 2016).Nevertheless, our record is the first in the estuarine zone of Patos lagoon.Considering that Patos lagoon estuary was systematically sampled in the last decade (Garcia et al. 2003, Garcia et al. 2004, Burns et al. 2006), it is possible that the species settled this area only recently.
Piscivorous invasive fish species show a tendency for establishment, promoting disturbances in trophic cascades and populations of native species (Pusey et al. 2006). Neuhaus et al. (2016) verified a high food niche overlap between invasive A. pantaneiro and native Oligosarcus robustus Menezes, 1969 in Jacuí and Sinos rivers, northern Patos Lagoon basin, were both species predated predominantly on small characids.Thus, if A. pantaneiro became an established invasive species in Marinheiros Island, populations of O. robustus and other native species may be directly affected by resource competition and predation.In view of this, we recommend the monitoring of A. pantaneiro and the ichthyofauna of limnic systems of Marinheiros in general, as well as other estuarine islands and systems of the peninsular systems of the coastal plain connected to the estuary of Patos lagoon.This procedure could detect new areas of occurrence of A. pantaneiro and collect data for the analysis on the relationships between this invasive species and the native ichthyofauna.

Figure 1 .
Figure 1.Location of Marinheiros Island, and the sites of collection of the ichthyofauna, Patos Lagoon estuary, southern Brazil.

Table 1 .
Characteristics and locations of the sites sampled in Marinheiros Island, Patos Lagoon estuary, southern Brazil, and fishing gear applied in each site.

Table 2 .
Number of collected specimens and relative abundance (in parentheses) of fish species recorded in three types of limnic systems in Marinheiros Island, Patos Lagoon estuary, southern Brazil.