Ichthyofauna of the inner shelf of Paraná , Brazil : checklist , geographic distribution , economic importance and conservation status

Comprehensive species checklists are essential to effectively implementing preservation and recovery measures, and should assess conservation status, vulnerability degree and anthropogenic threats. This checklist was compiled from fish species recorded in surveys conducted over the last 30 years in the shallow inner continental shelf in the State of Paraná, Brazil. Information on biogeography, conservation status, economic importance and degree of species’ vulnerability are provided. A total of 272 fish species were recorded, spanning 25 orders and 88 families. The most speciose family was Sciaenidae (25 species), followed by Carangidae (23), Engraulidae (10), Carcharhinidae (9), Epinephelidae (9) and Paralichthyidae (9). Most species occurring in Paraná’s shallow inner continental shelf are restricted to the West Atlantic. In terms of economic importance, 93% (253) of the species recorded were of fishery, aquaculture or aquaria interest. A notable fraction (39%) of the recorded species was classified as having moderate to very high vulnerability to extinction. In particular, 28 species (10%) were listed as globally endangered, and 34 species (12%) were listed as endangered in the Brazilian territory.


Introduction
The State of Paraná, in southern Brazil, has a 98 km long coastline, and is cut by two large estuarine complexes, namely, the Paranaguá Bay to the north and the Guaratuba Bay to the south.Its continental shelf extends from 175 to 190 km offshore, and is dominated by sandy bottoms, and a few rocky substrates (Brandini 2014).
Paraná's continental shelf harbors a rich fauna, particularly in its inner region which is nutrient enriched by the continental drainage system.Like the estuaries, the inner shelf functions as habitat for reproduction and development of many fish species; therefore, it performs a vital role in their life cycles (Blaber 2000).In addition, the continental shelf contains several fish species of commercial importance.
There have been several studies on the fish fauna in the Paranaguá Estuarine Complex (Hackradt et al. 2009;Félix-Hackradt et al. 2010;Ignácio & Spach 2010;Contente et al. 2011;Passos et al. 2012;Pichler et al. 2015Pichler et al. , 2017;;Possatto et al. 2017) and in the Guaratuba Bay (Chaves & Corrêa 1998;Chaves & Vendel 2001).On the other hand, few studies have focused on the continental shelf region, especially those assessing the taxonomic composition of the ichthyofauna (Santos 2006;Carniel 2008;Schwarz-Junior 2010).Of concern is the threat to the region's fish biodiversity, most notably due to overfishing, deposition of dredged sediments, habitat loss, and deployment of new habitats, such as artificial reefs, whose impact on biodiversity is not yet fully understood.In this study, we have compiled a checklist of fish species inhabiting the shallow inner continental shelf of Paraná.Considerations about geographic distribution, conservation status, economic importance, and degree of vulnerability to extinction are provided.This checklist compiles useful information in a single document that should be of great help in devising measures of preservation and species recovery.

Material and Methods
Data on fish species inhabiting the inner continental shelf of the State of Paraná were compiled from the peer-reviewed literature (Corrêa et al. 1986;Chaves et al. 2003;Godefroid et al. 2004;Costa & Chaves 2006;Gomes & Chaves 2006;Santos et al. 2006;Félix et al. 2007a;Félix et al. 2007b;Bornatowski et al. 2009;Hackradt & Hackradt 2009;Hackradt et al. 2011;Daros et al. 2012;Bornatowski et al. 2014a;Bornatowski et al. 2014b;Rossi-Wongtschowski et al. 2014, Santos et al. 2016) as well as less accessible academic literature (Santos 2006 andCarniel 2008 -master thesis; Schwarz-Junior 2010 and Spier 2016 -PhD thesis) published over the past 30 years.The full extent of Paraná's shallow inner continental shelf was sampled down to the 20 m isobath, including areas near the mouth of the Paranaguá Estuarine Complex and the Guaratuba Bay (Figure 1).Overall, gillnetting, trawling, and underwater visual census were the main sampling methods used in the studies compiled in this work.Further details on sampling methods and sampling areas are provided in Table 1.The taxonomic classification and nomenclature follows Marceniuk (2005), Craig & Hastings (2007), Smith & Craig (2007), Figueiredo & Menezes (2009), Carvalho-Filho et al. (2010), Menezes et al. (2010) and Eschmeyer et al. (2014).Orders and families are listed according to phylogenetic order (Eschmeyer et al. 2014) and the species inside each family are organized in alphabetical order.
To analyze the zoogeographic affinities of the fauna, the species were classified in geographic distribution categories based on Floeter et al. (2008), Luiz Jr et al. (2008), Eschmeyer et al. (2014) and Froese & Pauly (2017).The categories were: CT = Circumtropical, TA = Trans-Atlantic (Western and Eastern Atlantic Ocean), WA = Western Atlantic (Northern and Southern Atlantic Ocean), SWA = Southwest Atlantic (ranging from Northern Brazil to Argentina), SSWA = Southern Southwest Atlantic (Southeastern and Southern Brazil, Uruguay and Argentina), Ca = Caribbean (ranging from Florida to Venezuela), Br = Brazilian Province [ranging from the Orinoco River Delta in Venezuela to the State of Santa Catarina in Brazil (sensu Briggs & Bowen 2012)], and EP = Eastern Pacific.
Regarding species' economic importance in Brazil, we defined four categories, namely, 1) food: referring to human consumption, 2) animal feed, 3) aquarium, and 4) none: referring to species without any identified commercial purpose.Categories 1, 2, and 4 were implemented based on the work of Menezes et al. (2003); Figueiredo & Menezes (2009); Froese & Pauly (2017), as well as on the authors' previous knowledge.Category 3 was implemented based on the technical and scientific bulletin of CEPENE (2005), which lists marine fish species allowed for capture in Brazil.Furthermore, we also indicate which species have economic importance specifically for the State of Paraná, based on the authors' knowledge.
Vulnerability to extinction was categorized as low, low to moderate, moderate, moderate to high, high, high to very high, and very high, following FishBase (Froese & Pauly 2017).These categories were determined based on the life history and ecological characteristics of each species (Cheung et al. 2005).Species were also classified according to the IUCN categories (IUCN 2017) and the national status of conservation proposed by the Brazilian Ministry of Environment (MMA 2014).Conservation status and vulnerability to extinction provide a rough assessment of species' endangerment.

Cynoscion
The geographic distribution of species across the different categories defined in the previous section are illustrated in Figure 2.Many of the recorded species are widely distributed over the Western Atlantic, and can be further separated into two groups with distinct distribution: the first, characteristic of the Caribbean fauna, is also found in the Caribbean and Brazilian Province; and the second, with temperate affinities, is characteristic of the Southern Southwest Atlantic, including Argentina and Uruguay.
In terms of Brazilian economic importance, 156 species (57%) are used for human consumption, 74 species (27%) for aquaria and 30 species (11%) for animal feed.Only 19 species (7%) have no commercial importance in Brazil.In the State of Paraná, on the other hand, only 57% of species of economic interest in Brazil are exploited.In particular, 21 species used for human consumption in other parts of Brazil have no economic importance in Paraná.Moreover, the aquaria and animal feed industries are relatively underdeveloped, with only 9 of 74 potentially viable species used in aquaria, and 4 of 30 potentially viable species commercialized for animal feed.In short, of 253 species of economic interest in Brazil, only 144 are exploited in the State of Paraná (Figure 3).
A total of 61% of species were categorized as having low to moderate vulnerability to extinction, and 39% ranged from moderate to very high vulnerability (Table 2).Most Elasmobranchii (29 species) were highly or very highly vulnerable.Among the Perciformes, 50 of the 146 species were classified as having moderate to very high vulnerability.Considering both red lists, 82% of catalogued species in Paraná's inner shelf were assessed for their risk of extinction.Two hundred and forty-two species occurring in the shallow inner continental shelf of Paraná appear in the red list of the International Union for Conservation of Nature (IUCN 2017), where 185 are listed as least concern, 17 as data deficient, 12 as near threatened, 17 as vulnerable, 8 as endangered, and 3 as critically endangered.The Brazilian Ministry of Environment (MMA 2014) classified substantially less species in the area (85 species), however with higher risk of extinction (12 vulnerable, 7 endangered, 15 critically endangered) (Figure 4).

Discussion
The vastness of the Brazilian coast and its large ecosystem and biodiversity contributed to a false perception of inexhaustible fishing resources, and the misguided adoption of policies that neglected resource sustainability and focused primarily on species of commercial importance (Nahum et al. 2009).A necessary step towards implementing better informed policies is to obtain an accurate assessment of species occurrence, and their respective economic importance and vulnerability to extinction.Such comprehensive assessment is still lacking for Paraná's shallow inner continental shelf, in Southern Brazil, home to several threatened species.In an attempt to remedy this situation, this study compiled the results of surveys of Paraná's shallow inner continental shelf performed over the past 30 years, providing a comprehensive checklist of fish species, along with information on biogeography, conservation status, economic importance and degree of species' vulnerability.
Extracting correlations between the various factors that could influence species to extinction, and hence pinpointing its causes, is beyond the scope if this work.Nonetheless, we believe that our checklist provides valuable information for future studies on the ecology and conservation of the fish fauna of the area.
In our study, we have confirmed a rich fauna of Elasmobranchii in the continental shelf of Paraná, comprising 24% of Brazilian's elasmobranch fauna (Rosa & Gadig 2014).Several elasmobranchs that occur in Paraná seem to use the southern coast of Brazil for reproduction (Bornatowski & Abilhoa 2012).Vooren et al. (2005) recorded 21 species that use areas on the southern continental shelf for reproduction.It is suspected that several species also use Paraná's coast as parturition and nursery grounds, such as Carcharhinus limbatus, Rhizoprionodon lalandii, Sphyrna lewini, Narcine brasiliensis, Rioraja agassizi, Pseudobatos percellens and Zapteryx brevirostris.
According to Castello (1994), the coastal fish fauna in Southeastern and Southern Brazil is composed of a mixture of species with tropical to subantarctic affinities, explaining the richness of the fish fauna in Paraná's inner shelf.Among the Actinopterygii, Sciaenidae was the most representative family in other continental shelves of Brazil (Rocha & Rossi-Wongtschowski 1998;Muto et al. 2000;Moraes et al. 2009) and its occurrence in Paraná's inner continental shelf is associated with Coastal Water (Muto et al. 2000).Sciaenidae and Carangidae were also the most speciose families in both estuaries of the region: the PEC (Passos et al. 2012) and the Guaratuba Bay (Chaves & Corrêa 1998;Chaves & Vendel 2001).In Brazilian waters, there are 37 species of Sciaenidae and 25 species of Cynoscion, with 25 species of Sciaenidae and 9 of Cynoscion occurring in Paraná (Nelson et al. 2016).That means that only three species of Cynoscion do not occur, or were not registered, in the State of Paraná.Cynoscion guatucupa, for instance, is not listed in this checklist, but its range of occurrence goes from southeastern Brazil to Uruguay.The other two Cynoscion species (C.similis and C. steindachneri) only occur in the Northern Brazilian coast (Nelson et al. 2016).

Figure 1 .
Figure 1.Map of the shallow inner continental shelf of Paraná, Brazil, showing the Paranaguá Estuarine Complex and the Guaratuba estuary.The contour represents the 20-meter isobath.

Figure 3 .
Figure 3. Number of catalogued species with economic importance in the State of Paraná only, versus the number with economic importance in Brazil overall.

Table 1 .
Details on methods and sampling areas of the different sources consulted."x"indicates absence of depth data.

Table 2 .
Taxonomic classification of the ichthyofauna recorded in the shallow inner shelf of Paraná, Brazil.Geographic Distribution: CT = Circuntropical, TA = Trans-Atlantic, WA = Western Atlantic, SWA = Southern West Atlantic, SSWA = Southern Southwest Atlantic, Ca = Caribbean, Br = Brazilian Province and EP = Eastern Pacific.Global conservation status according to IUCN (2010) and national conservation status according to MMA (2014): NE= not evaluated, LC= least concern, NT = near threatened, DD = data deficient, VU = vulnerable, EN= endangered, CR = critically endangered.Economic importance in Brazil.Asterisk indicate which species have economic importance specifically for the State of Paraná.