niNeotropical IchthyologyNeotrop. ichthyol.1679-62251982-0224Sociedade Brasileira de Ictiologia10.1590/1982-0224-2020-0030Original articleThe deep sea teleost fish fauna of the Brazilian North Coast0000-0002-0029-7639KlautauAlex Garcia Cavalleiro de Macedo10000-0001-5822-454XCintraIsrael Hidenburgo Aniceto20000-0003-1886-5320RotundoMatheus Marcos30000-0002-2903-7355Carvalho-FilhoAlfredo40000-0002-9918-3972CairesRodrigo Antunes50000-0003-4286-0482MarceniukAlexandre Pires6Centro Nacional de Pesquisa e Conservação da Biodiversidade Marinha do Norte, Instituto Chico Mendes de Biodiversidade, Av. Tancredo Neves, 2501, 66077-830 Belém, PA, Brazil. (AGCMK) alex.klautau@icmbio.gov.brInstituto Chico Mendes de BiodiversidadeCentro Nacional de Pesquisa e Conservação da Biodiversidade Marinha do NorteInstituto Chico Mendes de Biodiversidade66077-830BelémPABrazilalex.klautau@icmbio.gov.brInstituto Socioambiental e dos Recursos Hídricos, Universidade Federal Rural da Amazônia, Av. Presidente Tancredo Neves, 2501, 66077-830 Belém, PA, Brazil. (IHAC) israel.cintra@ufra.edu.br.Universidade Federal Rural da AmazôniaInstituto Socioambiental e dos Recursos HídricosUniversidade Federal Rural da Amazônia66077-830BelémPABrazilisrael.cintra@ufra.edu.brAcervo Zoológico da Universidade Santa Cecília, 11045-907 Santos, SP, Brazil. (MMR) mmrotundo@unisanta.br.Acervo Zoológico da Universidade Santa CecíliaAcervo Zoológico da Universidade Santa Cecília11045-907SantosSPBrazilmmrotundo@unisanta.brFish Bizz Ltd., Rua D. Maria D. N. Garcez 39, 05424-070 São Paulo, SP, Brazil. (ACF) alfie@telnet.com.br.Fish Bizz Ltd.Fish Bizz Ltd.05424-070São PauloSPBrazilalfie@telnet.com.brMuseu de Zoologia da Universidade de São Paulo, 04263-000 São Paulo, SP, Brazil. (RAC) rodricaires@yahoo.com.br.Museu de Zoologia da Universidade de São PauloMuseu de Zoologia da Universidade de São Paulo04263-000São PauloSPBrazilrodricaires@yahoo.com.brMuseu Paraense Emílio Goeldi, 66040-170 Belém, PA, Brazil. (APM) a_marceniuk@hotmail.com (corresponding author).Museu Paraense Emílio GoeldiMuseu Paraense Emílio Goeldi66040-170BelémPABrazila_marceniuk@hotmail.com
Fernando Gibran
Alexandre Pires Marceniuk a_marceniuk@hotmail.com
Alex Garcia Cavalleiro de Macedo Klautau : Data curation, Funding acquisition, Supervision.
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.
Resumo
Os dados sobre peixes de profundidade encontrados na costa Norte do Brasil são restritos aos resultados de coletas realizadas pelo RV Oregon, um navio do Serviço Nacional de Pesca Marítima da América do Norte, e do Programa REVIZEE. O Programa REVIZEE Score-Norte teve como foco as espécies de peixes com valor comercial e recursos naturais com potencial para exploração na plataforma continental da costa Norte do Brasil. Contudo, o REVIZEE Score-Norte gerou pouca informação sobre as espécies sem valor comercial, não catalogou o material da biodiversidade inventariada, assim como não gerou listas de espécies. Dada a lacuna no conhecimento sobre os peixes de profundidade da costa norte do Brasil, nós compilamos todos os dados disponíveis e recuperamos registros fotográficos do Programa REVIZEE Score-Norte, incluindo os projetos PRODEMERSAL e PROTUNA. Considerando os registros publicados, espécimes depositados em coleções zoológicas e os registros fotográficos, apresentamos uma lista de 63 espécies de peixes de profundidade na costa Norte do Brasil. Outras 30 espécies encontradas nos registros publicados do PRODEMERSAL e PROTUNA, foram consideradas duvidosas, carecendo de confirmação.
Keywords:InventoryMarine biodiversityPRODEMERSALPROTUNAREVIZEE Score-NortePalabras-chave:Biodiversidade marinhaInventário de faunaPRODEMERSALPROTUNAREVIZEE ScoreNortePrograma de Capacitação Institucional (MCTIC/CNPq)444338/2018-7Programa de Capacitação Institucional (MCTIC/CNPq)300675/2019-4INTRODUCTION
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 km2, 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, 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., 2017, 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 and 1969. 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 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 2000 and 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 2002 and 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 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 km2, 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 km2 (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).
Data Collection. The surveys of the REVIZEE Score-Norte Program were conducted by the Centro Nacional de Pesquisa e Conservação da Biodiversidade Marinha do Norte (CEPNOR), a division of the Instituto Brasileiro de Meio Ambiente e dos Recursos Naturais Renováveis (IBAMA). Exploratory expeditions were based on standard fishing techniques such as bottom trawls, traps, and longlines (Lucena, Asano-Filho, 2006). Most of the information presented here is derived from the photographic records of the samples obtained by bottom trawls (REVIZEE, Fig. 1A), deep-water trawls (PRODERMERSAL, 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).
Brazilian North coast, shaded in grey, with The Great Amazon Reef System, as defined by Moura et al. (2016), shaded in red and collection locations shaded in black (modified from resources and species with potential for exploitation on the continental shelf and slope (Lucena, Asano-Filho, 2006). A. collection locations of Program REVIZEE Score-North, B. collection locations of Program PRODEMERSAL, and C. collection locations of Program PROTUNA.
The species identified here include those found in the photographic records recovered by researchers who participated in the REVIZEE Score-Norte Program (IHAC). Specimens recognized in these photographs were identified by three taxonomists (MMR, RAC, ACF), based on their expertise and data from literature (Nafpaktitis et al., 1977; Uyeno et al., 1983; Whitehead et al., 1984a,b, 1986; Smith, Heemstra, 1986; Böhlke et al., 1989; Cohen et al., 1990; Nielsen et al., 1999; Carpenter, 2002a,b), in addition to records from American ichthyological collections (http://www.fishnet2.net). Species nomenclature follows Fricke et al. (2020), while the supraspecific classification is based on Nelson et al. (2016).
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 selenopsFig. 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 epi-mesopelagic (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 are also found in the eastern Atlantic, and 18 species are considered to be circumglobal (Tab. 1, F column). However, five species are thought to be restricted to the western Atlantic between the Gulf of Mexico and northern Brazil (Tab. 1, F column), Anthias asperilinguis, Anthias nicholsi and Poecilopsetta inermis is thought to be exclusive to the Caribbean and northern South America, Aulotrachichthys argyrophanus and Centrodraco oregonus are assumed to be restricted to the northern and northeastern coast of Brazil, and Neobythites braziliensis is classified as endemic to Brazil.
The deep-sea teleost fish from the Brazilian North coast (bold, species with photographic record or specimens in the zoological collection). A. Specimens collected by the: REVIZEE Score-North (RZ), PRODEMERSAL (PD), PROTUNA (PT), and Centro Nacional de Pesquisa e Gestão de Recursos Pesqueiros do Litoral Norte (CEPNOR). B. Species with material deposited in North American zoological collections (see Supplementary Material). C. Specimens collected by the Program PROTUNA (Asano-Filho et al., 2005), with photographic records or with specimens in zoological collections (X) and specimens without photographic records or specimens in zoological collections (?). D. Life habits. E. Depth range (meters). F. Distribution.
Order
Family
Species
A
B
C
D
E
F
Notacanthiformes
Halosauridae
Halosaurus guentheri Goode, Bean, 1896
-
-
-
?
bathypelagic
550 – 1600
Atlantic
Anguilliformes
Muraenidae
Gymnothorax conspersus Poey, 1867
Fig. 2A
RZ
-
-
bathydemersal
100 – 310
Western Atlantic
Gymnothorax polygonius Poey, 1875
Fig. 2B
RZ
-
-
reef-associated
10 – 256
Atlantic
Derychthyidae
Coloconger meadi Kanazawa, 1957
Fig. 2C
RZ
-
-
bathydemersal
650 – 925
Western Atlantic
Nettastomatidae
Nettastoma melanura Rafinesque, 1810
-
-
-
?
bathydemersal
320 – 860
Atlantic
Congridae
Ariosoma selenops Reid, 1934
Fig. 2D
RZ
X
-
bathydemersal
348 – 549
Gulf of Mexico, Caribbean, northern South America
Bathycongrus bullisi (Smith, Kanazawa, 1977)
-
-
X
-
bathydemersal
366 – 475
Gulf of Mexico, Caribbean, northern South America
Bathyuroconger vicinus (Vaillant, 1888)
-
-
-
?
bathydemersal
900 – 1000
Circumglobal except Eastern Pacific
Paraconger caudilimbatus (Poey, 1867)
-
-
X
-
reef-associated
35 – 411
Gulf of Mexico, Caribbean, northern South America
Xenomystax congroides Smith, Kanazawa, 1989
-
-
X
-
bathydemersal
140 – 825
Atlantic
Serrivomeridae
Stemonidium hypomelas Gilbert, 1905
-
-
X
-
bathypelagic
175 – 1229
Atlantic and Indo-Pacific
Alepocephaliformes
Platytroctidae
Maulisia mauli Parr, 1960
-
-
-
?
bathypelagic
400 – 1200
Atlantic and Indian Oceans
Alepocephalidae
Talismania homoptera (Vaillant, 1888)
-
-
-
?
bathypelagic
560 – 1700
Tropical Atlantic
Stomiiformes
Stomiidae
Heterophotus ophistoma Regan, Trewavas, 1929
-
-
X
-
bathypelagic
200 – 850
Circumglobal
Stomias affinis Günther, 1887
-
-
-
?
bathypelagic
0 – 3800
Circumglobal
Ateleopodiformes
Ateleopodidae
Ijimaia antillarum Howell Rivero, 1935
Fig. 3A
PD
-
-
bathydemersal
100 – 500
Western Atlantic
Aulopiformes
Synodontidae
Saurida caribbaea Breder, 1927
Fig. 3B
RZ
-
-
demersal
20 – 460
Western Atlantic
Ipnopidae
Bathypterois viridensis (Roule, 1916)
-
-
-
?
bathydemersal
476 –1477
Atlantic
Bathytyphlops marionae Mead, 1958
-
-
-
?
bathydemersal
100 – 1920
Atlantic and Indian Oceans
Chlorophthalmidae
Chlorophthalmus brasiliensis Mead, 1958
-
-
X
-
bathydemersal
366 – ?
Gulf of Mexico, Caribbean, northern South America
Parasudis truculenta (Goode, Bean 1896)
Fig. 3C
RZ
-
X
demersal
133 – 181
Western Atlantic
Alepisauridae
Alepisaurus brevirostris Gibbs, 1960
Fig. 3D
PD
-
-
bathypelagic
640 – 1591
Circumglobal
Myctophiformes
Neoscopelidae
Neoscopelus macrolepidotus Johnson, 1863
-
-
-
?
pelagic-oceanic
300 –1180
Circumglobal, except Indian Ocean
Mycophidae
Centrobranchus nigroocellatus (Günther, 1873)
-
-
X
-
bathypelagic
0 – 800
Circumglobal
Diaphus dumerilii (Bleeker, 1856)
-
-
X
-
pelagic-oceanic
50 – 500
Atlantic
Lampanyctus tenuiformis (Brauer, 1906)
-
-
X
-
bathypelagic
40 – 750
Circumglobal
Lepidophanes guentheri (Goode, Bean, 1896)
-
-
X
-
pelagic-oceanic
50 – 800
Atlantic
Notoscopelus resplendens (Richardson, 1845)
-
-
X
-
bathypelagic
50 – 1550
Circumglobal
Polymixiiformes
Polymixiidae
Polymixia lowei Günther, 1859
Fig. 3E
RZ
-
X
bathydemersal
150 – 600
Western Atlantic
Zeiformes
Oreosomatidae
Pseudocyttus maculatus Gilchrist, 1906
-
-
-
?
bathydemersal
900 – 1100
Southern circumglobal
Zeidae
Zenopsis conchifer (Lowe, 1852)
Fig. 3F
PD
-
-
benthopelagic
150 – 300
Circumglobal
Gadiformes
Macrouridae
Coelorinchus occa (Goode, Bean, 1885)
-
-
-
?
bathydemersal
400 – 2200
Atlantic
Gadomus arcuatus (Goode, Bean, 1886)
-
-
-
?
bathydemersal
610 – 1370
Atlantic
Malacocephalus laevis (Lowe, 1843)
Fig. 3G
RZ
-
-
bathydemersal
200 – 1000
Circumglobal
Nezumia atlantica (Parr, 1946)
-
-
-
?
bathydemersal
360 – 1100
Western Atlantic
Nezumia suilla Marshall, Iwamoto, 1973
-
-
-
?
bathydemersal
860 – 920
Western Atlantic
Moridae
Gadella imberbis (Vaillant, 1888)
-
-
-
?
benthopelagic
200 – 800
Atlantic
Laemonema barbatulum Goode, Bean, 1883
-
-
-
?
bathydemersal
50– 1600
Western Atlantic
Physiculus fulvus Bean, 1884
-
-
X
-
bathydemersal
70 – 800
Gulf of Mexico, Caribbean, northern South America
Physiculus kaupi Poey, 1865
Fig. 4A
RZ
-
-
bathydemersal
260 – 365
Western Atlantic
Trachichthyiformes
Diretmidae
Diretmus argenteus Johnson, 1864
-
-
X
-
bathypelagic
0 – 2000
Circumglobal
Trachichthyidae
Aulotrachichthys argyrophanus (Woods, 1961)
-
-
X
-
bathypelagic
228
Brazilian North coast and off NE Brazil
Gephyroberyx darwinii (Johnson, 1866)
Fig. 4B
PD
-
-
benthopelagic
200 – 500
Circumglobal
Hoplostethus occidentalis Woods, 1973
-
-
-
?
bathydemersal
485 – 850
Circumglobal except Eastern Pacific
Beryciformes
Gibberichthyidae
Gibberichthys pumilus Parr, 1933
-
-
-
?
bathypelagic
320 – 1100
Western Atlantic
Ophidiiformes
Ophidiidae
Dicrolene introniger (Goode, Bean, 1883)
-
-
-
?
bathydemersal
1000 – 1600
Atlantic
Monomitopus agassizii (Goode, Bean, 1896)
-
-
-
?
bathydemersal
48 – 1125
Western Atlantic
Neobythites braziliensis Nielsen, 1999
-
-
X
-
bathydemersal
320 – 410
Brazil
Bythitidae
Diplacanthopoma brachysoma Günther, 1887
-
-
-
?
bathydemersal
460 – 1670
Western Atlantic
Pleuronectiformes
Paralichthyidae
Citharichthys cornutus (Günther, 1880)
-
-
X
-
bathydemersal
140 – 400
Western Atlantic
Pleuronectidae
Poecilopsetta inermis (Breder, 1927)
-
-
X
-
bathydemersal
182 – 793
Caribbean and northern South America
Bothidae
Chascanopsetta lugubris Alcock, 1894
Fig. 4C
RZ
-
-
bathydemersal
60 – 3210
Circumglobal
Monolene antillarum Norman, 1933
-
-
X
-
demersal
0 – 370
Western Atlantic
Monolene atrimana Goode, Bean, 1886
-
-
X
-
bathydemersal
? – 527
Western Atlantic
Engyophrys senta Ginsburg, 1933
-
-
X
-
demersal
35 – 180
Western Atlantic
Callionymiformes
Callionymidae
Synchiropus agassizii (Goode, Bean, 1888)
Fig. 4D
RZ
-
-
bathydemersal
250 – 700
Western Atlantic
Draconettidae
Centrodraco oregonus (Briggs, Berry, 1959)
-
-
X
-
bathydemersal
229 – 411
Brazilian North coast
Scombriformes
Gempylidae
Gempylus serpens Cuvier, 1829
Fig. 4E
PT
-
-
pelagic-oceanic
0 – 600
Circumglobal
Lepidocybium flavobrunneum (Smith, 1843)
Fig. 4F
PT
-
-
pelagic-oceanic
200 – 1100
Circumglobal
Nealotus tripes Johnson, 1865
-
-
-
?
pelagic-oceanic
914 – 1640
Circumglobal
Neoepinnula americana (Grey, 1953)
Fig. 4G
PD
-
-
benthopelagic
184 – 457
Western Atlantic
Nesiarchus nasutus Johnson, 1862
-
-
-
?
pelagic-oceanic
200 – 1200
Western Atlantic
Promethichthys prometheus (Cuvier, 1832)
-
-
-
?
pelagic-oceanic
80 – 800
Circumglobal except Eastern Pacific
Ruvettus pretiosus Cocco, 1833
Fig. 4H
PT/PD
-
X
benthopelagic
100 – 800
Circumglobal
Ariommatidae
Ariomma bondi Fowler, 1930
Fig. 4I
RZ
-
-
demersal
100 – 200
Western Atlantic
Ariomma melana (Ginsburg, 1954)
Fig. 4J
PD
-
X
bathydemersal
180 – 550
Western Atlantic
Perciformes
Epigonidae
Epigonus macrops (Brauer, 1906)
-
-
-
?
bathydemersal
550 – 1300
Circumglobal except Eastern Pacific
Epigonus pandionis (Goode, Bean, 1881)
Fig. 4K
CEP
-
-
bathydemersal
200 – 600
Atlantic
Serranidae
Anthias asperilinguis Günther, 1859
Fig. 4L
PD
X
-
reef-associated
230 – 320
Caribbean and northern South America
Anthias nicholsi Firth, 1933
Fig. 4M
RZ/PD
-
-
reef-associated
90 – 256
Caribbean and northern South America
Hyporthodus niveatus (Valenciennes, 1828)
-
PD
-
-
demersal
30 – 525
Western Atlantic
Bramidae
Brama brama (Bonnaterre, 1788)
Fig. 5A
PD
-
-
pelagic-neritic
0 – 200
Circumglobal
Priacanthidae
Cookeolus japonicus (Cuvier, 1829)
Fig. 5B
PD
-
-
reef-associated
165 – 200
Circumglobal
Lutjanidae
Etelis oculatus (Valenciennes, 1828)
Fig. 5C
PD
-
-
bathydemersal
100 – 450
Western Atlantic
Scorpaeniformes
Scorpaenidae
Pontinus nematophthalmus (Günther, 1860)
-
-
X
-
reef-associated
82 – 410
Western Atlantic
Pontinus rathbuni Goode, Bean, 1896
Fig. 5D
RZ
X
-
reef-associated
73 – 150
Western Atlantic
Setarches guentheri Johnson, 1862
Fig. 5E
RZ/PD
-
X
benthopelagic
150 – 780
Circumglobal
Triglidae
Bellator brachychir (Regan, 1914)
Fig. 5F
RZ
-
-
demersal
35 – 366
Western Atlantic
Prionotus beanii Goode, 1896
-
-
X
-
demersal
35 – 200
Caribbean and South America
Prionotus ophryas Jordan, Swain, 1885
-
-
X
-
reef-associated
1 – 171
Western Atlantic
Prionotus stearnsi Jordan, Swain, 1885
Fig. 5G
RZ
-
-
demersal
70 – 180
Western Atlantic
Peristediidae
Peristedion altipinnis Regan, 1903
-
-
-
?
demersal
100 – 200
Southwestern Atlantic
Peristedion ecuadorense Teague, 1961
-
-
-
?
bathydemersal
392 – 910
Western Atlantic
Peristedion sp.
Fig. 5H
RZ
-
-
bathydemersal
Peristedion truncatum (Günther, 1880)
-
-
-
?
bathydemersal
150 – 900
Western Atlantic
Caproiformes
Caproidae
Antigonia capros Lowe, 1843
Fig. 5I
PD
-
-
demersal
100 – 300
Circumglobal
Antigonia combatia Berry, Rathjen, 1959
Fig. 5J
RZ/PD
X
-
bathydemersal
115 – 585
Western Atlantic
Lophiiformes
Lophiidae
Lophius gastrophysus Miranda Ribeiro, 1915
Fig. 5K
PD
-
-
bathydemersal
40 – 700
Western Atlantic
Sladenia shaefersi Caruso, Bullis, 1976
Fig. 6A
PD
-
-
bathydemersal
900 – 1200
Western Atlantic
Chaunacidae
Chaunax pictus Lowe, 1846
-
-
-
?
bathydemersal
220 – 1060
Atlantic and Mediterranean
Chaunax suttkusi Caruso, 1989
Fig. 6B
RZ
-
-
bathydemersal
200 – 980
Atlantic
Ogcocephalidae
Dibranchus atlanticus Peters, 1876
Fig. 6C
RZ
-
X
bathydemersal
300 – 820
Atlantic
Diceratiidae
Bufoceratias wedli (Pietschmann, 1926)
-
-
-
?
bathypelagic
300 –1500
Atlantic
Species of the order Anguilliformes, family Muraenidae, A. Gymnothorax conspersus, photograph by Revizee Score-North, B. Gymnothorax polygonius, photograph by Revizee Score-North, family Derychthyidae, C. Coloconger meadi, photograph by Revizee Score-North, and family Congridae, D. Ariosoma selenops, photograph by Revizee Score-North.
DISCUSSION
The history of the biological exploration of Brazil’s deep sea environments began with the visit of H.M.S. Challenger to the waters off the country’s northeastern coast, in 1873, but it took almost another 100 years for the first Brazilian surveys to take place, with those conducted by the Almirante Saldanha, an oceanographic vessel of the Brazilian 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).
Species of the order Ateleopodiformes, family Ateleopodidae, A. Ijimaia antillarum, photograph by PRODEMERSAL, Order Aulopiformes, family Synodontidae, B. Saurida caribbaea, photograph by Revizee Score-North, family Chlorophthalmidae, C. Parasudis truculenta, photograph by Revizee Score-North, family Alepisauridae, D. Alepisaurus brevirostris, photograph by PRODEMERSAL, order Polymixiiformes, family Polymixiidae, E. Polymixia lowei, photograph by Revizee Score-North, order Zeiformes, family Zeidae, F. Zenopsis conchifer, photograph by PRODEMERSAL, and order Gadiformes, family Macrouridae, G. Malacocephalus laevis, photograph by Revizee Score-North.
Species of the order Gadiformes, family Moridae, A. Physiculus kaupi, photograph by Revizee Score-North, order Trachichthyiformes, family Trachichthyidae, B. Gephyroberyx darwinii, photograph by PRODEMERSAL, order Pleuronectiformes, family Bothidae, C. Chascanopsetta lugubris, photograph by Revizee Score-North, order Callionymiformes, family Callionymidae, D. Synchiropus agassizii, photograph by Revizee Score-North, order Scombriformes, family Gempylidae E. Gempylus serpens, photograph by PROTUNA, F. Lepidocybium flavobrunneum, photograph by PROTUNA, G. Neoepinnula americana, photograph by PRODEMERSAL, H. Ruvettus pretiosus, photograph by PRODEMERSAL, family Ariommatidae, I. Ariomma bondi, photograph by Revizee Score-North, J. Ariomma melana, photograph by PRODEMERSAL, order Perciformes, family Epigonidae, K. Epigonus pandionis, photograph by CEPNOR, and family Serranidae, L. Anthias asperilinguis, photograph by PRODEMERSAL, M. Anthias nicholsi, photograph by PRODEMERSAL.
Species of the order Perciformes, family Bramidae, A. Brama brama, photograph by PRODEMERSAL, family Priacanthidae, B. Cookeolus japonicus, photograph by PRODEMERSAL, family Lutjanidae, C. Etelis oculatus, photograph by PRODEMERSAL, order Scorpaeniformes, family Scorpaenidae, D. Pontinus rathbuni, photograph by Revizee Score-North, E. Setarches guentheri, photograph by PRODEMERSAL, family Triglidae, F. Bellator brachychir, photograph by Revizee Score-North, G. Prionotus stearnsi, photograph by Revizee Score-North, family Peristediidae, H. Peristedion sp., photograph by Revizee Score-North, order Caproiformes, family Caproidae, I. Antigonia capros, photograph by PRODEMERSAL, J. Antigonia combatia, photograph by PRODEMERSAL, and order Lophiiformes, family Lophiidae, K. Lophius gastrophysus, photograph by PRODEMERSAL.
Species of the order Lophiiformes, family Lophiidae, A. Sladenia shaefersi, photograph by PRODEMERSAL, family Chaunacidae, B. Chaunax suttkusi, photograph by Revizee Score-North, and family Ogcocephalidae, C. Dibranchus atlanticus, photograph by Revizee Score-North.
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.
Taxonomic limitations still hamper our understanding of the occurrence and distribution patterns of many offshore fishes, including some of the lesser-known species identified in the present study. For example, we identified one deep sea flounder as Chascanopsetta lugubris, although the limits of the occurrence of this species have been questioned by some authors, in addition to the validity of Chascanopsetta danae, from the western Atlantic (Amaoka, Yamamoto, 1984; Foroshchuk, 1991). Inaccuracies in the taxonomic identification may also have occurred in some cases, such as Chaunax suttkusi (Fig. 6B) and Epigonus pandionis (Fig. 4K, Tab. 1), which were identified in Asano-Filho et al. (2005) as Chaunax pictus and Epigonus macros (Tab. 1). Other species, including Urophycis cirrata, Urophycis mystacea and some Peristedion species (Caires, 2014; Lemes, 2017) have been recorded previously in the Gulf of Mexico and southern Brazil, but not in northern Brazil.
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.
ACKNOWLEDGEMENTS
We wish to express our thanks to Projeto Áreas Marinhas e Costeiras Protegidas - GEF Mar of the Federal Government, responsible for all material examined. APM is grateful for the Programa de Capacitação Institucional (MCTIC/CNPq, Process 444338/2018-7 and 300675/2019-4). To Marcelo Roberto Souto de Melo for the confirmation of the identity of Coloconger meadi and Wagner Santos Rosa by Figure 1 preparation.
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