The deep sea teleost fish fauna of the Brazilian North Coast

Alex Garcia Cavalleiro de Macedo Klautau1, Israel Hidenburgo Aniceto Cintra2, Matheus Marcos Rotundo3, Alfredo Carvalho-Filho4, Rodrigo Antunes Caires5 and Alexandre Pires Marceniuk6

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Abstract​


EN

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.

Keywords: Inventory; Marine biodiversity; PRODEMERSAL; PROTUNA; REVIZEE Score-Norte

PT

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.

Palavras-chave: Biodiversidade marinha; Inventário de fauna; PRODEMERSAL; PROTUNA; REVIZEE ScoreNorte

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 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, 1968Rocha, Rosa, 2001Espírito-Santo, Isaac, 2005Moura et al., 2016Marceniuk et al., 20172019), 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., 20042005). 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, 1970Kowsmann, 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., 2004Grodsky 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., 2007Grodsky 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, 1979Lana et al., 1996Oliveira 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., 2016Francini-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).

FIGURE 1| 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., 1977Uyeno et al., 1983Whitehead et al., 1984a,b1986Smith, Heemstra, 1986Böhlke et al., 1989Cohen et al., 1990Nielsen et al., 1999Carpenter, 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 asperilinguisPontinus rathbuni, and Antigonia combatia) are represented in zoological collections by specimens from the study area (Tab. 1, A and B column). Five others (Parasudis truculentaPolymixia loweiRuvettus pretiosusAriomma melanaSetarches 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 asperilinguisAnthias 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.

TABLE 1 | 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

 

FIGURE 2| Species of the order Anguilliformes, family Muraenidae, AGymnothorax conspersus, photograph by Revizee Score-North, BGymnothorax polygonius, photograph by Revizee Score-North, family Derychthyidae, CColoconger meadi, photograph by Revizee Score-North, and family Congridae, DAriosoma selenops, photograph by Revizee Score-North.

Discussion​


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, 1988Tavares, 1999), followed 10 years later by the major expeditions of the French RV Thalassa and Brazilian vessels Diadorim and Atlântico Sul (Figueiredo et al., 2002Madureira et al., 2004Bernardes 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, 2010Lins 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., 2015Lins Oliveira et al., 2015Nóbrega 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 pandionisFig. 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 bullisiParaconger caudilimbatus, and Physiculus fulvus, Tab. 1, F column).

FIGURE 3| Species of the order Ateleopodiformes, family Ateleopodidae, AIjimaia antillarum, photograph by PRODEMERSAL, Order Aulopiformes, family Synodontidae, BSaurida caribbaea, photograph by Revizee Score-North, family Chlorophthalmidae, CParasudis truculenta, photograph by Revizee Score-North, family Alepisauridae, DAlepisaurus brevirostris, photograph by PRODEMERSAL, order Polymixiiformes, family Polymixiidae, EPolymixia lowei, photograph by Revizee Score-North, order Zeiformes, family Zeidae, FZenopsis conchifer, photograph by PRODEMERSAL, and order Gadiformes, family Macrouridae, GMalacocephalus laevis, photograph by Revizee Score-North.

FIGURE 4| Species of the order Gadiformes, family Moridae, APhysiculus kaupi, photograph by Revizee Score-North, order Trachichthyiformes, family Trachichthyidae, BGephyroberyx darwinii, photograph by PRODEMERSAL, order Pleuronectiformes, family Bothidae, CChascanopsetta lugubris, photograph by Revizee Score-North, order Callionymiformes, family Callionymidae, DSynchiropus agassizii, photograph by Revizee Score-North, order Scombriformes, family Gempylidae EGempylus serpens, photograph by PROTUNA, FLepidocybium flavobrunneum, photograph by PROTUNA, GNeoepinnula americana, photograph by PRODEMERSAL, HRuvettus pretiosus, photograph by PRODEMERSAL, family Ariommatidae, IAriomma bondi, photograph by Revizee Score-North, JAriomma melana, photograph by PRODEMERSAL, order Perciformes, family Epigonidae, KEpigonus pandionis, photograph by CEPNOR, and family Serranidae, LAnthias asperilinguis, photograph by PRODEMERSAL, MAnthias nicholsi, photograph by PRODEMERSAL.

FIGURE 5| Species of the order Perciformes, family Bramidae, ABrama brama, photograph by PRODEMERSAL, family Priacanthidae, BCookeolus japonicus, photograph by PRODEMERSAL, family Lutjanidae, CEtelis oculatus, photograph by PRODEMERSAL, order Scorpaeniformes, family Scorpaenidae, DPontinus rathbuni, photograph by Revizee Score-North, ESetarches guentheri, photograph by PRODEMERSAL, family Triglidae, FBellator brachychir, photograph by Revizee Score-North, GPrionotus stearnsi, photograph by Revizee Score-North, family Peristediidae, HPeristedion sp., photograph by Revizee Score-North, order Caproiformes, family Caproidae, IAntigonia capros, photograph by PRODEMERSAL, JAntigonia combatia, photograph by PRODEMERSAL, and order Lophiiformes, family Lophiidae, KLophius gastrophysus, photograph by PRODEMERSAL.

FIGURE 6| 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, 1976Sazonov, Williams, 2001Lavrado, Brasil, 2010) and stomiids (e.g. Leptostomias and MelanostomiasBigelow 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, 1984Foroshchuk, 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 cirrataUrophycis mystacea and some Peristedion species (Caires, 2014Lemes, 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.

Acknowledgments​


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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Authors


Alex Garcia Cavalleiro de Macedo Klautau1, Israel Hidenburgo Aniceto Cintra2, Matheus Marcos Rotundo3, Alfredo Carvalho-Filho4, Rodrigo Antunes Caires5 and Alexandre Pires Marceniuk4

[1]    Centro 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.br.

[2]    Instituto 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.

[3]    Acervo Zoológico da Universidade Santa Cecília, 11045-907 Santos, SP, Brazil. (MMR) mmrotundo@unisanta.br.

[4]    Fish Bizz Ltd., Rua D. Maria D. N. Garcez 39, 05424-070 São Paulo, SP. (ACF) alfie@telnet.com.br.

[5]    Museu de Zoologia da Universidade de São Paulo, 04263-000 São Paulo, SP, Brazil. (RAC) rodricaires@yahoo.com.br.

[6]    Museu Paraense Emílio Goeldi, 66040-170 Belém, PA, Brazil. (APM) a_marceniuk@hotmail.com (corresponding author).

Authors’ Contribution


Alex Garcia Cavalleiro de Macedo Klautau: Data curation, Funding acquisition, Supervision.

Israel Hidenburgo Aniceto Cintra: Conceptualization, Project administration, Writing-original draft, Writing-review & editing.

Matheus Marcos Rotundo: Formal analysis, Investigation, Writing-original draft, Writing-review & editing.

Alfredo Carvalho-Filho: Formal analysis, Investigation, Writing-original draft, Writing-review & editing.

Rodrigo Antunes Caires: Formal analysis, Investigation, Writing-original draft, Writing-review & editing.

Alexandre Pires Marceniuk: Conceptualization, Formal analysis, Investigation, Supervision, Writing original draft, Writing-review & editing.

Ethical Statement​


Not applicable.

Competing Interests


The authors declare no competing interests.

How to cite this article


Klautau AGCM, Cintra IHA, Rotundo MM, Carvalho-Filho A, Caires RA, Marceniuk AP. The deep sea teleost fish fauna of the Brazilian North Coast. Neotrop Ichthyol. 2020; 18(3):e200030. https://doi.org/10.1590/1982-0224-2020-0030


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