The deep sea teleost fish fauna of the Brazilian North Coast

Data on the deep sea fishes found off the northern Brazilian coast are restricted to the results of the surveys of the RV Oregon, a research vessel of the North American National Marine Fisheries Service, and the REVIZEE Program. The REVIZEE Score-Norte Program focused on commercial fish species and natural resources with potential for exploitation on the continental shelf and slope off the northern coast of Brazil. In this sense, the REVIZEE Score-Norte Program generated little information on species of no commercial value, did not catalog its inventory in zoological collections, and did not publish species lists. Given this considerable knowledge gap on the deep-sea fish found off the North coast of Brazil, we compiled all the available data on the deep-sea fish of this region and also retrieved photographic records from the REVIZEE Score-Norte Program, including the PRODEMERSAL and PROTUNA projects. Considering the published records, specimens deposited in zoological collections, and the interpretation of photographic records, we compiled a list of 63 species of deep-sea fish from the North coast of Brazil. An additional 30 species were found in the published records from the PRODEMERSAL and PROTUNA, but were considered to be doubtful or pending confirmation.


INTRODUCTION
The northern Brazilian coast comprises the region between the mouths of the rio Oiapoque, which forms the frontier between Brazil and French Guiana, and the rio Parnaíba, which marks the frontier between the Brazilian states of Maranhão and Piauí. Considered to be one of the most productive regions in the Brazilian Exclusive Economic Zone (EEZ), the Brazilian North Coast is part of one of the world's most important fishing grounds, with a total area of approximately 223,000 km 2 , which extends northward to the mouth of the Orinoco River, in Venezuela (Corrêa, Martinelli, 2009). Despite its considerable importance in ecological, biogeographical, and economic terms, the fish fauna of the North Coast is still poorly known (Marceniuk et al., 2013(Marceniuk et al., , 2019. Although some inventories on the coastal fish fauna have been conducted (Eskinazi, Lima, 1968;Rocha, Rosa, 2001;Espírito-Santo, Isaac, 2005;Moura et al., 2016;Marceniuk et al., 2017Marceniuk et al., , 2019, information on the deep-sea fishes is restricted basically to the results of two long-term surveys. One of these surveys was undertaken by the Oregon, a research vessel of the North American National Marine Fisheries Service, while the other was part of the Brazilian National Program for the Assessment of the Sustainable Potential of Natural Resources in the Exclusive Economic Zone (REVIZEE).
The RV Oregon conducted the most complete inventory of marine fishes off the northern coast of Brazil between 1957 and1969. The results of this study indicated that this fish fauna is closely similar to that found off French Guiana, as well as providing the first evidence of the existence of a coral barrier off the mouth of the Amazon River (Collette, Rützler, 1977). The surveys carried out by the National Marine Fisheries Service generated an enormous amount of scientific material, which is deposited in North 3/19 ni.bio.br | scielo.br/ni American zoological collections, as well as the publication of a number of taxonomic studies, including species descriptions, many of deep-water fishes, such as Centrodraco oregonus (Briggs, Berry, 1959), Scorpaena petricola Eschmeyer, 1965, Scorpaena melasma Eschmeyer, 1965, Schroederichthys tenuis Springer, 1966, Malacocephalus okamurai Iwamoto, Arai, 1987, and Neobythites braziliensis Nielsen, 1999 The REVIZEE Score-Norte Program began to survey the northern Brazilian coast in 1996, sampling commercially-valuable natural resources and species with potential for exploitation on the continental shelf and slope (Lucena, Asano-Filho, 2006). However, this program generated little information on species with little or no commercial value, did not catalog specimens in zoological collections or publish species lists. Two distinct projects were developed within the scope of the REVIZEE Score-Norte Program: the PROTUNA, Desenvolvimento Tecnológico para a captura de Grandes Pelágicos Oceânicos na Costa Norte do Brasil, which was operational between 2000and 2002(Asano-Filho et al., 2004; and the PRODEMERSAL, Desenvolvimento Tecnológico para a Captura de Recursos Demersais com Arrasto na região Norte do Brasil, which ran between 2002and 2004(Asano-Filho et al., 2005. These two projects focused on the prospecting of potentially exploitable stocks of large pelagic fish and deep sea demersal species, respectively, and did generate species lists (Asano Filho et al., 2004, 2005. However, both projects presented the same general deficiencies as the REVIZEE Score-Norte Program, and did not contribute to the scientific cataloging of the fish species from the northern coast of Brazil. A single exception is a very rare record of the occurrence of the goblin shark (Mitsukurina owstoni Jordan, 1898) in Brazil, through a specimen that is currently housed in the Univali Oceanographic Museum (MOVI), Santa Catarina, Brazil (see Asano-Filho et al., 2005). No other specimens from the REVIZEE Score-Norte program is available for examination in museums.
Given the knowledge gap that exists on the deep-sea fish fauna of the northern coast of Brazil, we compiled all the available data on the region's deep-sea fish, including the identification of species observed in photographic records recovered from the REVIZEE Score-Norte program, including the PRODEMERSAL and PROTUNA projects.

MATERIAL AND METHODS
Study area. The northern coast of Brazil, which includes the sedimentary basins of the Amazon and Parnaíba Rivers, was formed during the Paleozoic and reactivated between the late Jurassic and early Cretaceous (Martins et al., 1979). This highly diverse coastline has a total extension of some 2,500 km (Floriani et al., 2004). The hydrological dynamics of this area, in particular at the mouth of the Amazon River, are intensely seasonal, being influenced primarily by the discharge of the Amazon, trade winds, and the North Brazil (or Guianas) current, which transport the waters of the external shelf and slope toward the northwest (Richardson et al., 1994). The highly turbid Amazon plume may stretch up to 500 km to the northwest and more than 200 km into the Atlantic off the mouth of the river (Curtrin, 1986). The sediments adjacent to the mouth of the Amazon are formed primarily by silts, while the northeastern sector is rich in clays, a feature that is probably determined by tidal currents (Coutinho, Morais, 1970;Kowsmann, Costa, 1979). The region is also influenced by the Orinoco River, through the formation of 4/19 ni.bio.br | scielo.br/ni Amazon-Orinoco Plume, which creates unique oceanographic conditions (Hu et al., 2004;Grodsky et al., 2014). The surface temperatures of the water may reach 31°C near the coast, and 27°C on the continental shelf. A thermocline is found at depths of around 120 m in the adjacent oceanic waters, with temperatures of approximately 17°C at depths of up to 200 m. The salinity of the coastal and estuarine waters is strongly influenced by the fluvial discharge, increasing toward the open sea, and reaching 36.9% in the adjacent oceanic waters (Oliveira et al., 2007;Grodsky et al., 2014).
The northern continental shelf covers a wide area and is relatively flat, whereas the internal portion of the shelf, between the Parnaíba and Pará rivers, undulates considerably, forming ridges of coarse quartz sand that reach heights of up to 10 m. The inner continental shelf off Amapá is covered with deposits of fluvial mud, interspersed with relict areas of transgressive quartz sands, which were deposited during the periods of marine regression, on the coasts of the states of Pará and Maranhão. The internal shelf also has deposits of fluvial sand off the mouths of the Amazon and Pará rivers (Kowsmann, Costa, 1979). The Amazon Cone, which is adjacent to the mouth of the Amazonas, is formed by the accumulation of sediments from the Amazon River, which extend offshore beyond the outer limit of the Exclusive Economic Zone. The Amazon Cone does not have a typical continental elevation or slope, with varying depth gradients, but rather, a continuous slope, which extends all the way to the abyssal plain, being interrupted by paleochannels and other constructive or erosive geological features of non-tectonic origin. The external portion of the shelf is very rugged, with innumerable troughs and canyons, and an abrupt change in slope at a depth of around 80 m. Between the depths of 60 m to 120 m, three carbonatic facies are found, constructed of mollusks, benthic foraminifers, and Holocenic algae typical of shallow coastal zones, as well as biodetritic sands (Kowsmann, Costa, 1979;Lana et al., 1996;Oliveira et al., 2007). The slope of the shelf tends to decrease as its width increases towards the extremes of the Amazon Gulf.
On the middle continental shelf, the penetration of sunlight is related directly to the influence of the Amazon plume and the tropical waters of the North Brazil Current. The Great Amazon Reef System (GARS) is a complex, consolidated bottom environment constituted by living organisms (Moura et al., 2016;Francini-Filho et al., 2018). Current knowledge indicates that the GARS has an area of 9,500 km 2 , composed of typical mesophotic reefs, at depths of 70-220 m, formed principally of coralline algae and scleractinian corals, which may cover a total area of approximately 56,000 km 2 (Moura et al., 2016). The enormous diversity of habitats, which include algae, rhodoliths, sponges, and soft coral and black coral, is influenced by the discharge of sediments and suspended matter from the Amazon River, and the strong local maritime currents (Francini-Filho et al., 2018).  Fig. 1B), and pelagic longlines (PROTUNA, Fig. 1C). As part of the REVIZEE Score-Norte Program, the RV Paulo Moreira trawled for fish and shrimp at 101 trawls between 25 and 639 m depths (Fig. 1A), including 36 at depths below 100 m (Lucena, Asano-Filho, 2006). The PRODEMERSAL project consisted of four exploratory cruises, with a total of 176 days at sea and 592 trawls between depths of 236 to 1,246 m ( Fig. 1B) conducted by the fishing vessels Mar Maria and Noé (Asano-Filho et al., 2005). The PROTUNA project involved 12 exploratory cruises, involving boats of the northern tuna fleet (Asano Filho et al., 2004), which spent a total of 193 days at sea, with 99 pelagic longline operations (Fig. 1C).

RESULTS
The lists compiled by the PROTUNA and PRODEMERSAL projects include a total of 36 species of deep-sea fish (Asano Filho et al., 2004, 2005, see Tab. 1, C column and also Tab. S1). A total of 28 species were identified based on material deposited in North American zoological collections (ANSP, CAS, MCZ, KU, UF, USNM and TU), most of which was collected by the RV Oregon (Tab. 1, B column). Based on the photographic records made during the REVIZEE Score-Norte Program (22 species) and associated projects, PROTUNA (3 species) and PRODEMERSAL (17 species), we identified a total of 37 species (Tab. 1, A column), in a recent collection effort in the Great Amazon Reef System by CEPNOR (Alexandre Marceniuk et al., 2020 pers. comm.). Only four of these species (Ariosoma selenops Fig. 2D, Anthias asperilinguis, Pontinus rathbuni, and Antigonia combatia) are represented in zoological collections by specimens from the study area (Tab. 1, A and B column). Five others (Parasudis truculenta, Polymixia lowei, Ruvettus pretiosus, Ariomma melana, Setarches guentheri, and Dibranchus atlanticus) were included in the species list of the PROTUNA project (Tab. 1, A and C column).
Considering only the documented records (specimens deposited in zoological collections or with photographic record), a total of 63 species of deep-sea fish from the North coast of Brazil were recorded. A further 30 records from the literature were considered to be doubtful here, and are pending confirmation. The 63 confirmed species represent 11 orders, 25 families and 55 genera of deep-sea fish (Tab. 1). The most speciose families are Gempylidae (seven species), and Congridae, Myctophidae, and Macrouridae, with five species each. Thirty-seven of the species are bathydemersal, eight are bathypelagic, five benthopelagic, eight from deep reefs and five are epimesopelagic (Tab. 1, D column), ranging over depths up to 3,200 m (Tab. 1, E column). Twenty eight species are widely distributed in the western Atlantic, seven 6/19 ni.bio.br | scielo.br/ni       Navy, in 1967(Eskinazi, Lima, 1968). There was a second foreign expedition in 1987, with the voyage of the French research vessel RV Marion Dufresne (Guille, Ramos, 1988;Tavares, 1999), followed 10 years later by the major expeditions of the French RV Thalassa and Brazilian vessels Diadorim and Atlântico Sul (Figueiredo et al., 2002;Madureira et al., 2004;Bernardes et al., 2005). Subsequent surveys were funded by the Brazilian Oil company Petrobras (Petróleo Brasileiro S.A.) and focused on the northeastern Brazilian coast and the central Brazilian EEZ. These surveys were conducted by the Brazilian vessel N/RB Astro Garoupa and the American research vessels Luke Thomas, and Seward Johnson (Lavrado, Brasil, 2010;Lins Oliveira et al., 2015). Most of the research expeditions in the Brazilian EEZ at the end of the 20th century was conducted within the scope of the REVIZEE Program, whose principal objective was to inventory the commercially exploitable natural resources of the zone, and consolidate efforts to expand its limits (CIRM, 1994). The recovery of photographic records from this program, together with the analysis of published data and the material in zoological collections, provided the baseline evidence for the present study, and the first comprehensive inventory of the deep-water fish fauna of the northern coast of Brazil. The 63 deep-water teleost fish species reported here from northern Brazil represent only 8.2% of the total number of marine bony fish species found in the Brazilian North coast, estimated to be approximately 770 species (Alexandre Marceniuk et al., 2020 pers. comm.). In other regions of Brazil and adjacent waters, deep sea species make up a much larger proportion of the total teleost diversity: (a) in São Paulo, represent 42.6% of the total of the 481 teleost species recorded by Menezes (2011), (b) in the Potiguar basin, Rio Grande do Norte, represent 30.8% of the known fauna of 373 species (Garcia Jr. et al., 2015;Lins Oliveira et al., 2015;Nóbrega et al., 2015), (c) 30.4% of 1,155 deep water species in Brazil as a whole (Menezes et al., 2003), (d) 44.4% of 405 species in Suriname and French Guyana (Uyeno et al., 1983), and (e) 38% of 129 species in Patagonia (Nakamura, 1986). This would appear to imply that many other deep-sea species are yet to be reported from the Brazilian North Coast. In particular, it seems likely that many of the species found in the waters of neighboring areas, as Suriname and French Guyana (see Uyeno et al., 1983), will be confirmed in Brazil, when new surveys are conducted off the northern coast.
Most deep sea species are thought to have a wide distribution, either circumglobal (e.g. Alepisaurus brevirostris, Fig. 3D, and Zenopsis conchifer, Fig. 3F), in the Atlantic (e.g. Epigonus pandionis, Fig. 4K) or the western Atlantic (Ariomma bondi and A. melana, Figs. 4I, J). However, some species have a more restricted distribution, either in northern and northeastern coast of Brazil (Aulotrachichthys argyrophanus and Centrodraco oregonus), endemic from Brazil (Neobythites braziliensis) or including the Caribbean or the Gulf of Mexico (Anthias asperilinguis, Fig. 4L, Anthias nicholsi, Fig. 4M, Bathycongrus bullisi, Paraconger caudilimbatus, and Physiculus fulvus, Tab. 1, F column). These differences in distribution patterns may reflect oceanographic and geographic processes, such as the establishment of the transcontinental flow of the Amazon River to the Atlantic Ocean in the mid to late Miocene, and the isolation of the Caribbean in the Tertiary-Quaternary, which implies that they influenced not only the coastal species, but also the deep sea fauna. This is especially true for some deep-water taxa, such as alepocephalids (Sazonov, 1976;Sazonov, Williams, 2001;Lavrado, Brasil, 2010) and stomiids (e.g. Leptostomias and Melanostomias;Bigelow et al., 1964), although more data will be necessary to confirm these conclusions.
The paucity of specimens of deep sea fish species from the northern Brazilian coast in ichthyological collections is a fundamental problem for the understanding of the teleost diversity of this region. Despite the enormous efforts of the REVIZEE program, almost no data on the region's deep sea fish fauna are available, given that most, of the material collected during these surveys cannot be located or examined. Clearly, investment is required for basic research (surveys) and the cataloging and storage of material to guarantee the development of more systematic study on the taxonomy, ecology and distribution of the fauna of the Brazilian Exclusive Economic Zone, in particular, that of the North Coast.