Abstract
The deep sea is the largest and one of the most extreme environments on Earth. It is estimated that 10–15% of all fish species are dwelling in the deep sea, most of which have unique morphological and physiological adaptations. Biological expeditions to sample the deep ocean off Brazil started with the British HMS Challenger Expedition (1872–1876), followed by a few fishery stations made by the German RV Ernst Haeckel (1966) and the North-American MIV Oregon II (1957–1975), the cruises of the French RVs Marion Dufresne (1987) and Thalassa (1999, 2000), the Brazilian RV Atlântico Sul (1996–1999), the FV Diadorim and FV Soloncy Moura (1996–2002), OSB Astro Garoupa (2003), and, more recently, the American RV Luke Thomas and Seward Johnson (2009, 2011), the French RV Antea (2015, 2017), and the Brazilian RV Alpha Crucis. A total of 712 species of deep-sea fishes were recorded, including five species of Myxini, six species of Holocephali, 81 species of Elasmobrachii, and 620 species of Actinopteri. As in other parts of the world, the Brazilian deep-sea ichthyofauna struggles under severe anthropogenic impacts caused by the commercial fishing, and the extraction of oil and gas. The deep ocean is a delicate environment and its recovery is considerably slower than an equivalent in shallow water habitat. Therefore, increasing the research efforts is needed to avoid that part of its diversity disappear without our accurate knowledge.
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7.1 Introduction
The oceans cover 70% of the Earth’s surface, which represents 97% of the water available as fish habitats. The average depth of the oceans is 3800 m and more 50% of their volume below is 3000 m, and 95% is below 200 m, making the deep sea the largest environment available on Earth (Horn 1972; Angel 1997). Even though the oceans are continuous and interconnected, there are well-defined basins limited by the continents, water masses, currents, and a great variety of habitats that range from continental slopes and rises, abyssal plains, trenches, canyons, zones of oxygen depletion, and hydrothermal vents (Tyler 2003).
The deep sea is characterized by extreme conditions of pressure, temperature, and light penetration (Angel 1997; Thistle 2003) that influence fish assemblages. The pressure increases one atmosphere for every 10 m of water depth and can reach up to 1100 atmospheres in the deepest parts of the world’s oceans. The sunlight intensity decreases exponentially with depths, while the long wavelengths of the light spectrum – red, yellow, and orange – only penetrate to approximately 15, 30, and 50 m, respectively, making photosynthesis impossible below depths greater than 250 m. However, the short wavelengths of the light spectrum – violet, blue and green – can penetrate in depths of up to 1000 m, creating the twilight zone. Below 1000 m depth, the sunlight is completely absent and the only light available is produced by bioluminescent organisms, such as cnidarians, fishes, cephalopods, and crustaceans. In the deepest regions, the water temperature is constant between 2 and 3 ° C, but it is extremely variable from 200 to 400 m, with the formation of thermoclines. Gases such as oxygen and carbon dioxide have a higher solubility at greater pressure, making the levels of oxygen similar to the surface waters, with the exception of the zones with oxygen depletion (Brinton 1979; Rogers 2000; Tunnicliffe et al. 2003).
It is estimated that 10–15% of the known diversity of fishes and over 160 families occur in depths greater than 500 m (Weitzman 1997; Priede and Froese 2013). Among the hagfishes (Myxini), more than 50% of the species are from deep waters, 800 m on average. Two myxinid species, Eptatretus deani (Evermann and Goldsborough 1907) and E. fritzi Wisner and McMillan 1990, were reported at 2743 m (Fernholm 1998). More than 50% of chimaeras, sharks, and rays (Chondrichthyes) occur in depths greater than 500 m; however, they become extremely rare at depths over 3000 m. The deepest records for a chimaera belong to the chimaerid Hydrolagus affinis (De Brito Capello 1868) at 3000 m, for the sharks, to the dalatiid Isistius brasiliensis (Quoy and Gaimard 1824) and the somniosid Centroscymnus coelolepis Barbosa du Bocage and de Brito Capello, 1864 at 3700 m, and for a skate, to the rajid Rajella bigelowi (Stehmann 1978) at 4156 m (Priede et al. 2006, Musick and Cotton 2015). The bony fishes (Actinopterygii) comprise the majority of the biodiversity, and the deepest records belonging to the liparid Pseudoliparis amblystomopsis (Andriashev 1955) at 7703 m, and the ophidiid Abyssobrotula galatheae Nielsen 1977, known as the deepest-living known vertebrate, living at 8370 m (Nielsen 1977; Smith Fujii et al. 2010). The two extant species of coelacanth (Sarcopterygii), the latimerids Latimeria chalumnae Smith 1939 and Latimeria menadoensis Pouyaud et al. 1999, are also from deep waters, occurring in depths from 150 to 700 m (Fricke et al. 1991; Pouyaud et al. 1999; Jewett 2001).
7.1.1 Early Discoveries of Deep-Sea Organisms
Historically, the first reports of deep-sea organisms collected with precise depths were the polychaete Lumbriclymene cylindricauda Sars 1872, and an ophiuroid, probably Gorgonocephalus arcticus Leach 1819. Both were brought to the surface from off the northeast coast of Canada on a sounding line deployed at 1095 m, by the British HMS Isabella under the command of Captain Sir John Ross RN (Ross 1819; Anderson and Rice 2006).
The first reports of deep-sea fishes were made even before their formal description by Linnaeus (1758) – for instance, the velvet belly lanternshark Etmopterus spinax (Linnaeus 1758) (Etmopteridae) appeared in Willughby (1686), Ray (1713), and Artedi (1738), however, without a precise depth record. By 1775, 26 species of deep-demersal fishes were known from the Atlantic (Haedrich 1996) and, in the early nineteenth century, Risso (1810, 1820a, b) compiled a primary summary of the bathymetric distributions of fishes in the Mediterranean, including myctophids [e.g., Gasteropelecus humboldti Risso 1810 (now valid as Myctophum punctatum Rafinesque, 1810) and Lampanyctus crocodilus (Risso 1810)] and alepocephalids [e.g., Alepocephalus rostratus Risso 1820)].
“The shape of these fish [Alepocephalus rostratus Risso 1820a, b], their extraordinarily large eyes, the dark hues, and little variations which cover them, reveal that they are from the deep abyssal pelagic, which make their home, and their habits and habitats will remain, for the naturalists, long buried in these profound regions.” [Translated from Risso 1820b].
Ignoring these data, Forbes (1844) reportedly proposed the azoic hypothesis, which predicted a decrease of abundance and diversity of marine animals with depth, which would cease to exist at a depth of 300 fathoms, about 550 m. Surprisingly, the azoic theory became widely accepted among the scientific community (Anderson and Rice 2006). A few years later, James Clark Ross (1847) and Michael Sars (1872, 1875) obtained several specimens of deep-sea invertebrates at depths of up to 700 m from the Antarctic, and between 360 and 500 m from deep areas off Norway, respectively. Nevertheless, it was only after the expeditions coordinated by the Scottish naturalist Charles W. Thomson onboard of the British HMS Lightning (1868) and HMS Porcupine (1869, 1870) that the azoic theory was finally dismissed (Thomson 1873; Levin and Gooday 2003; Anderson and Rice 2006).
Thomson used the results of those expeditions to convince the British Royal Navy to allow the use of the HMS Challenger in a worldwide expedition to explore the deep sea. The Challenger Expedition took place between December 7th, 1872 and May 24th, 1876, traveling 68,890 nautical miles (=127,584 km) across the Atlantic, Pacific, and Indian Oceans. It was the first oceanographic expedition to obtain biological, chemical, and physical samples from around the world, collecting data from 362 stations, in depths of up to 8183 m – the majority between 1800 and 5400 m (Thomson 1880). The outcome of the Challenger Expedition was published in a series of reports between 1885 and 1895, that includes four volumes on botany, one volume on deep-sea deposits, and an introduction plus 83 volumes on zoology, with the descriptions of astonishing 715 genera and 4417 species of marine organisms, most of which are still valid nowadays (Murray 1895). The fishes were studied by the German ichthyologists Albert Günther (1877, 1878a, b, 1880, 1887), which recognized 385 species living below 180 m and 230 species below 550 m.
The western South Atlantic deep-sea ichthyofauna remained unstudied until the two passages of the Challenger Expedition off Northeastern Brazil (1873) and off Uruguay and Argentina (1976). In Brazil, the deep sea had not been further explored for almost a century, until the passages of the German RVs Ernst Haeckel (1966) between Southern Brazil and Argentina and the American MIV Oregon II (1957–1976) in northern South America. The first expedition focused exclusively on Brazilian waters was carried out much later, onboard the French RV Marion Dufresne (1987), and the most important contributions were made during the REVIZEE years (1996–2002), especially with the cruises of the French RV Thalassa (1999, 2000), the Brazilian RV Atlântico Sul (1996–1999), and the Brazilian FVs Diadorim and Soloncy Moura (1996–2002). The Brazilian oil company Petróleo Brasileiro S.A. – Petrobras hired the Brazilian OSB Astro Garoupa (2001, 2007) and the American RVs Luke Thomas and Seward Johnson (2009, 2011) to evaluate the deep-sea biodiversity on the oil basins. The most recent expeditions were made onboard the French RV Antea (2015, 2017) and the Brazilian RV Alpha Crucis (2019), as part of the ABRACOS (Acoustics along the BRAzilian COaSt) and the DEEP-OCEAN (Diversidade E Evolução de Peixes de Oceano Profundo) projects, respectively. In this chapter, we provide a historical overview about the discoveries of deep-sea fishes in the Brazilian Economic Exclusive Zone (EEZ), including a summary of the results obtained by either the major scientific expeditions or the additional fisheries exploratory surveys of interest (Table 7.1, Fig. 7.1).
The search for the taxonomic records was initially made in Catalog of Marines Fishes of Brazilian Coast (Menezes et al. 2003) and the Catálogo Taxonômico da Fauna do Brasil (Boeger et al. 2015) and restricted to those species that occur in depths greater than 200 m. To minimize the chance of error and update taxonomic status, each record was double-checked in the Eschmeyer’s Catalogue of Fishes (Fricke et al. 2020), literature reviews, and the original descriptions, and only those records with a voucher specimen obtained in the Brazilian EEZ were considered. Reports of species that had been substantiated by material deposited in museums were confirmed or excluded from the account by accessing the online databases of the Museum of Comparative Zoology of Harvard University, the National Museum of Natural History of the Smithsonian Institution, and the Zoologisches Institut und Zoologisches Museum der Humboldt Universität, and also examining material in the Museu de Zoologia da Universidade de São Paulo, and the Museu Nacional da Universidade Federal do Rio de Janeiro.
The arrangement of Classes, Orders, and Families follows Fricke et al. (2020) for Myxini and Chondrichthyes, which are divided into the Classes Elasmobranchii and Holocephali; Betancur-R et al. (2017) was used for the ranks within the Class Actinopteri. Prefixes of vessels used along text are as follows: FV, fishery vessel; MV or MIV, motor vessel; RV research vessel; HMS, His/Her Majesty’s Ship; OSV, offshore supply vessel.
The habitat definition adopted herein is adapted from Briggs (1960) and Gaither et al. (2016): (A) shallow benthopelagic, species that live on or near to the bottom and are typically found on the continental shelf in shallower waters and mesophotic reefs, which were also reported in depths greater than 200 m (e.g., muraenids, serranids); (B) epipelagic, species that generally inhabit the upper 200 m of the water column, but also visit deeper waters (e.g., lamnids and scombrids); (C) deep benthopelagic, species that live on or near to the bottom at depths greater than 200 m (e.g., chimaerids and synaphobranchid eels); (D) mesopelagic, species that are encountered in the water column at depths between 200 and 1000 m (e.g., etmopterids, myctophiforms, and stomiiformes), and (E) bathypelagic, species that occur in the water column in depths great than 1000 m (e.g., dalatiids, ceratioids, and eurypharyngids). All the records were organized considering the cruise and presented along with the existing information on habitat occupation.
7.2 Records of Deep-Sea Fishes in Brazilian EEZ
7.2.1 HMS Challenger Expedition (1872–1876)
In Brazil, the Challenger Expedition passed through the Saint Paul Rocks (August 28–29th, 1873) and the Fernando de Noronha Archipelago (September 1s–8th, 1873), but only obtained biological collections between Pernambuco and Bahia States (September 9–14th, 1873) (Thomson 1880). Those specimens were used by Günther (1877, 1878a, b, 1880, 1887) for the descriptions of the first Brazilian deep-sea fishes, including the grenadier Coryphaenoides leptolepis Günther 1877 (Macrouridae), the tripod fish Bathypterois quadrifilis Günther 1878, the grideye Ipnops murrayi Günther 1878 (Ipinopidae), the serranid Bathyanthias roseus Günther 1880 (Serranidae), the flatfish Citharichthys cornutus (Günther 1880) (Paralichthyidae), the armored-searobin Peristedion truncatum (Günther 1880) (Peristediidae), the viviparous brotula Diplacanthopoma brachysoma Günther 1887 (Bythitidae), the clusk eel Neobythites ocellatus Günther 1887 (Ophidiidae), and the bigscale Poromitra crassiceps (Günther 1878a, b) (Melamphaidae).
The Challenger Expedition also visited other parts of South America, obtaining samples from Punta Arenas, Chile to the Falkland Islands (January 20th–February 3rd, 1976), from the Falkland Islands to off the Rio de la Plata mouth, at the border between Argentina and Uruguay (February 8–26th, 1876), and from the Rio de la Plata mouth to the Tristan da Cunha Islands (February 28th–March 14th, 1876) (Thomson 1880). Those stations in adjacent waters resulted in the descriptions of additional five species that also occur in the Brazilian EEZ: the gadiforms Coryphaenoides affinis Günther, 1878, Laemonema longifilis Günther 1880 [valid as Urophycis brasiliensis (Kaup 1858) (Lemes et al. 2016)] (Phycidae), and Antimora rostrata; the tripodfish Bathypterois longipes Günther 1878 (Ipnopidae); and the viviparous brotula Cataetyx messieri ) (Bythitidae).
7.2.2 Fishery Surveys in the Nineteenth Century (1950–1970)
In 1966, the western German RV Ernst Haeckel made a cruise to the southern part of South America between Brazil and Argentina (32°–51° S), resulting in records of 85 species of Actinopterygii, nine from deeper waters, and the description of the flathead Cottunculus granulosus Karrer 1968 (Psychrolutidae) (Krefft 1968a, Lima and Mincarone 2004).
Between 1957 and 1975, the United States National Oceanic and Atmospheric Administration MIV Oregon II conducted several expeditions to Northern Brazil, off the mouth of the Rio Amazonas. Most part of the samples was taken from up to 80 m, on the continental shelf; however, a few stations were made on the continental slope, in depths of up to 411 m (Cohen 1958, Collette and Rützler 1977). Those stations resulted in the discovery of a deep-reef of sponges and rhodoliths, and the descriptions of the slender catshark Schroederichthys tenuis Springer 1966 (Scyliorhinidae), the shortspine boarfish Antigonia combatia Berry and Rathjein 1958, a slope dragonet Centrodraco oregonus (Briggs and Berry 1959) (Draconettidae), the Atlantic green eye Chlorophthalmus brasiliensis Mead 1958 (Chlorophthalmidae), a grenadier Malacocephalus okamurai Iwamoto and Arai 1987 (Macrouridae), an argentine Glossanodon pygmaeus Cohen 1958 (Argentinidae), a clusk eel Neobythites braziliensis Nielsen 1999 (Ophidiidae), the anguilliforms Bathycongrus bullisi (Smith and Kanazawa 1977) (Congridae) and Chlorophthalmus brasiliensis Mead 1958 (Chlorophthalmidae), and the western luminous roughy Aulotrachichthys argyrophanus (Woods 1961) (Trachichthyidae) (Mead 1958; Briggs and Berry 1959; Woods 1961; Springer 1965; Smith and Kanazawa 1977; Iwamoto and Arai 1987; Gadig et al. 1996; Nielsen 1999).
7.2.3 RV Marion Dufresne (1987)
In 1987, the expedition MD-55 was conducted onboard of the French RV Marion Dufresne, as part of a collaboration between the Universidade Santa Úrsula, Brazil, and the Muséum National d’Histoire Naturelle, France (Guille and Ramos 1988; Tavares 1999). A total of 33 stations using bottom trawls were made on the continental shelf and slope between northern Rio de Janeiro and Espírito Santo States, and on the Vitória-Trindade Seamount Chain (23°36′40″–18°49′00″ S and 42°10′–28°20′ W), in depths of 200 to 5092 m. The MD-55 expedition produced 500 specimens, comprising 81 species and 39 families of Osteichthyes and four Elasmobranchii (Séret and Andreata 1992). The specimens were split between the two leading institutions, but more recently the fish specimens deposited at the Universidade Santa Úrsula were transferred to the Museu Nacional/UFRJ.
7.2.4 The REVIZEE Years (1994–2004)
In 1994, the Brazilian Government launched the Program Evaluation of the Sustainable Potential of Living Resources in the Exclusive Economic Zone (REVIZEE), a 10 years long project which objective was to evaluate the marine resources in the Brazilian Exclusive Economic Zone. The Brazilian EEZ was divided into four scores, according to their oceanographic and biological characteristics, and dominant seabed type: North, Northeast, Central, and Southeast-South (Ministério do Meio Ambiente 2006; Serafim 2007).
During the REVIZEE program, the French RV Thalassa of the Institut Français de Recherche pour l’Exploitation de la Mer (IFREMER) was hired to explore the continental slope. Two cruises were conducted in 1999 and 2000, between Bahia and Rio de Janeiro States (11°–22° S and 34o40’–40°30’ W), formerly named as Bahia-1 and Bahia-2, respectively. The goal of the Bahia-1 cruise was to explore the epipelagic (0–200 m) and mesopelagic (200–1000 m) resources. The samples were obtained from 51 stations, from depths between 14 and 910 m and resulted in the capture of 96 species of Osteichthyes from 38 families (Madureira et al. 2004, Braga et al. 2007). During the Bahia-2 cruise, focused on the demersal and benthopelagic organisms, samples were obtained from 58 stations between 195 and 2137 m and resulted in the capture of 208 species from 61 families of Actinopteri, and 14 species sharks from eight families (Costa et al. 2000, 2007; Nunan et al. 2007). The collections made by the RV Thalassa served as base for descriptions of nine new species: the angelshark Squatina varii Vaz and Carvalho 2018 (Squatinidae); the catsharks Scyliorhinus cabofriensis Soares et al. 2016 and S. ugoi Soares et al. 2015 (Scylirhinidae); the dogsharks Squalus bahiensis Viana et al. 2016 and S. albicaudus Viana et al. 2016 (Squalidae); the skates Dipturus mennii Gomes and Paragó 2001 and Malacoraja obscura Carvalho et al. 2005 (Rajidae); the swallower Kali colubrina Melo 2008 (Chiasmodontidae); the clusk eel Neobythites monocellatus Nielsen 1999 (Ophidiidae); the eelpout Pachycara alepidotum Anderson and Mincarone 2006 (Zoarcidae); and, in part, the bald cutthroat eel Synaphobranchus calvus Melo 2007 (Synaphobranchidae) (Anderson and Mincarone 2006; Carvalho et al. 2005; Melo 2007, 2008; Melo et al. 2009; Nielsen et al. 2009; Soares et al. 2015, 2016; Soares and Carvalho 2016; Viana et al. 2016; Vaz and Carvalho 2018).
For the Southeast-South score, three cruises were made onboard of the RV Atlântico Sul from the Fundação Universidade Rio Grande, between Rio de Janeiro and Rio Grande do Sul States (22°–34° S and 40°–53° W), formerly named as REVIZEE I, II, and III. Most samples were obtained using pelagic nets mainly from 100 to 500 m, but a single station at 675 m during the cruise REVIZEE I, eight stations from 500 to 1480 m during REVIZEE II, and 12 stations from 500 to 1457 m, during REVIZEE III. Those materials collected during those cruises resulted in records of 171 species from 71 families of Actinopterygii and the description of the chimaera Hydrolagus matallanasi Soto and Vooren 2004 (Chimaeridae) (De Figueiredo et al. 2002; Soto and Vooren 2004; Bernardes et al. 2007 and Rossi-Wongtschowski 2007).
For the demersal fauna, the samples were obtained onboard of the Brazilian FVs Diadorim and Soloncy Moura, both from the Centro de Pesquisa e Extensão Pesqueira das Regiões Sudeste e Sul (CEPSUL/IBAMA). Different types of fishing gear were used, including fish traps launched to depths of up to 500 m, long lines to depths between 100 and 1200 m, and bottom trawls made between 100 and 600 m. From these samplings, two species of Myxini, 37 species of Elasmobranchii, and 184 species of Actinopteri were collected (Bernardes et al. 2005a, b; Haimovici et al. 2008). The hagfish Eptatretus menezes Mincarone 2000 (Myxinidae) and the catshark Schroederichthys saurisqualus Soto 2001 (Scyliorhinidae) were described based on specimens collected by the RV Diadorim (Mincarone 2000; Soto 2001).
7.2.5 The Petrobras Expeditions (2000–2011)
Since 2000, the Brazilian oil company Petróleo Brasileiro S.A. – Petrobras started to invest in projects to increase the knowledge of the deep-water fauna (Morais 2013). During the projects OCEANPROF – Oceano Profundo (2001–2007) and HABITATS – Heterogeneidade Ambiental da Bacia de Campos (2008–2015), two expeditions were conducted onboard the Brazilian OSV Astro Garoupa to the continental slope off northern Rio de Janeiro State. Using a bottom trawl, the OSV Astro Garoupa obtained samples from 40 stations on the continental slope, between 1059 and 1640 m. Two species of Elasmobranchii and 80 species of Actinopteri were reported; including part of the specimens used in the description of the cutthroat eel Synaphobranchus calvus (Synaphobranchidae) (Melo 2008; Lavrado and Brasil 2010).
During the Projeto de Monitoramento Ambiental Marinho da Bacia Potiguar (2009–2011), two expeditions were made onboard of the North American RVs Luke Thomas and Seward Johnson off the Rio Grande do Norte State. The samples were obtained using bottom trawl, from depths between 150 and 2000 m, and resulted in the capture of five species of Elasmobranchii and one Holocephali and 159 species of Actinopteri (Oliveira et al. 2015), and was used for the description of Barathronus linsi (Nielsen et al. 2015).
7.2.6 FRV Antea (2015, 2017)
The Acoustics along the BRAzilian COaSt (ABRACOS) is an integrated program between the French Institut de Recherche pour le Développement and the Brazilian institutions Universidade Federal do Rio de Janeiro, Universidade Federal de Pernambuco, and Universidade Federal Rural de Pernambuco, with the goal to monitor the tropical marine ecosystems between oceanic islands and the continental margin in Northeastern Brazil. Two cruises were carried out onboard the French RV Antea (2015, 2017) using micronekton and mesopelagic nets for deep-pelagic organisms in depths of up to 1113 m (Bertrand 2015, 2017;s Eduardo et al. 2018a, b). A bottom trawl was also used in 2017, but focused on the continental shelf, therefore not included in this account (Melo et al. 2020). So far, the results of the two expeditions resulted in new records in the Brazilian EEZ of a trichiurid, two howeliids and four caristiids, and regional accounts for 11 mesopelagic species (Eduardo et al. 2018a, c, 2019, Mincarone et al. 2019).
7.2.7 RV Alpha Crucis (2019–Present)
The Projeto Diversidade E Evolução de Peixes de Oceano Profundo – DEEP-OCEAN, hosted at the Instituto Oceanográfico da Univsersidade de São Paulo, has the goal to study the diversity and evolution of deep-sea fishes in the western South Atlantic. The first cruise to the Brazilian EEZ was conducted onboard the Brazilian RV Alpha Crucis in September 2019 using a bottom trawl between 400 and 1500 m. Preliminary, unpublish data indicates the capture of 88 species of Elasmobranchii (11), Holocephali (1), and Actinopteri (76). Two additional cruises are planned for 2020/2021.
7.2.8 Additional Contributions
Since 2006, the Projeto TAMAR systematically carry out deep-sea fishing off Praia do Forte, Bahia, using the MV Teahupoo adapted to deploy longline and traps. The specimens collected are regularly destined to scientific collections and served for the new records of nine species of Actinopterygii in the Brazilian EEZ (Carvalho-Filho et al. 2009, 2010a, b, 2011a, 2011b, 2012, 2020).
Several projects developed at the Universidade Federal Rural de Pernambuco obtained samples from the Saint Peter and Saint Paul Archipelago (ASPSP) and the continental slope off Pernambuco. According to Nunes (2016), the fishing boat FV Transmar I was used between 2012 and 2014 to deploy longlines and fish traps at depths from 200 to 700 m in the ASPSP, resulting on records of 11 species of Actinopterygii, one of which was recently described by Pires et al. (2019) as Physiculus cirm Carvalho-Filho and Pires 2019 (Moridae).
Partnership with commercial fishing boats also are a good source of scientific material, serving the base for new records of nine species of Actinopterygii in Northeastern Brazil and the description of a new genus and species, Leucogrammolycus brychios Anderson and Mincarone 2008 (Zoarcidae) (Anderson and Mincarone 2008; Caires et al. 2008; de Paiva et al. 2011).
7.3 Important Expeditions to Other Parts of the Western South Atlantic
After the scientific achievements of the Challenger Expedition, there was a considerable increase in oceanographic expeditions across the world to obtain physical, chemical, and biological samples (Wust 1964; Hopper 1995). Several fisheries expeditions were conducted off South America that improved the taxonomic knowledge of the deep-sea ichthyofauna in the western South Atlantic, thus providing additional records for several species that occur in the Brazilian EEZ.
Beginning in the 1960s, the German Institute of Sea Fisheries (Institut für Seefischerei, Hamburg, Germany) conducted several expeditions across the Atlantic Ocean, and off Argentina and Uruguay, using the FRV Walther Herwig (1960–1971) and FRV Walther Herwig II (1973–1985). The results included descriptions of several deep-sea species and extensive taxonomic reviews (Krefft 1968a, b, 1974, 1976; Stehmann and Hulley 1994; Stein 2010).
From the 1970s to the early 2000s, the Japanese Marine Fisheries Research and Development Center (JAMARC) and the Japan Deep-Sea Trawlers Association (JDSTA) performed several fisheries surveys in South America to evaluate the fishery stocks along the coasts of Patagonia (1976–1979), French Guiana and Suriname (1979–1983), and Peru (Uyeno et al. 1983; Nakamura et al. 1986; Nakaya et al. 2009). Off French Guiana and Suriname, bottom trawling was conducted onboard by the whaler MV Nisshin-Maru No. 201 to explore the resources on the continental shelf and slope, between 90 and 1000 m. A total of 453 species were recorded, including two species of Myxini, 45 Chondrichthyes and 406 Actinopteri (Uyeno et al. 1983). Off Patagonia, the Japanese expeditions were conducted by the MVs Akebono Maru No. 72 and Shinkai Maru focused on the continental shelf and slope off Argentina and the Atlantic Chilean coast, between 20 and 1200 m. The results include a single species of Chondrichthyes and 130 species of Actinopteri (Nakamura et al. 1986).
Between 1970s and 1980s, the Ministry of Fishing Industry of the then Soviet Union promoted an expansion of the deep-sea fisheries in the Southern Atlantic, as a part of a global program. Scientific and commercial explorations were conducted on the Victoria-Trindade Seamount Chain (1982) and on the Rio Grande Rise (1982–1984, 2000) using several fisheries vessels equipped with different types of gear. Those expeditions resulted in reports and species descriptions of about 70 species of fish, including the rare goblin shark Mitsukurina owstoni Jordan 1898 (Parin et al. 1995; Shcherbachev 1995; Clark et al. 2007; Prokofiev and Kukuev 2009).
7.4 The Diversity of Deep-Sea Fishes in the Brazilian EEZ
Hitherto, 712 species from 145 families and 37 orders of deep-sea fishes had been recorded in the Brazilian EEZ (Table 7.2). Those records include five species from a single family of Myxiniformes (Table 7.3), six species from three families of Holocephali, 81 species from 23 families and eight orders of Elasmobranchii, and (Table 7.4), and 620 species from 118 families and 27 orders of Actinopteri (Table 7.5). Additionally, 51 species previously mentioned in the area did not have their occurrence confirmed and, therefore, were excluded from this account (Table 7.6).
Among the Brazilian deep-sea ichthyofauna, 40.4% are deep-benthopelagic (e.g., Bathyuroconger vicinus, Coelorinchus caribbaeus, and Bathyraja schroederi), 20.2% are mesopelagic (e.g., Isistius brasiliensis, Argyropelecus aculeatus, and Diaphus adenomus), and 21.6% are bathypelagic (e.g., Barbourisia rufa, Gigantactis verhoeffeni, and Kali indica) (Fig. 7.2). Noteworthy, several species classified herein as bathypelagic are not restricted to greater depths and frequently occur in the mesopelagic zone (Rofen 1966; Melo 2008; Pietsch 2009).
The shallow benthopelagic species represent 12.8% (e.g., Callorhinchus callorynchus, Merluccius hubbsi, and Polyprion americanus), and only 4.9% are epipelagic (e.g., Characarodon carcharias, Mola mola, and Xiphias gladius).
The deep-benthopelagic fishes are the most diversified, including 288 species (Fig. 7.3). All five species of hagfishes (Myxinidae) are benthopelagic. The Elasmobranchii are represented by 41 species from 11 families and six orders: Rajiformes, with 16 species from the families Rajidae (15) and Arhynchobatidae (1); Carcharhiniformes, with 11 species from the families Pseudotriakidae (1) and Scyliorhinidae (11); Squaliformes, with ten species from the families Somniosidae (4), Centrophoridae (2), Dalatiidae (2), Echinorhinidae (1), and Squalidae (1); Hexanchiformes, with two species from the family Hexanchidae (2); Squatiniformes, with a single species in the family Squatinidae; and Torpediniformes, with a single species in the family Narcinidae. The Holocephali is represented by three species from the two families of Chimaeriformes, Chimaeridae (2) and Rhinochimaeridae (1).
Most deep-benthopelagic fishes are actinopterygians, with 237 species from 51 families from 18 orders. Gadiformes is the most diversified order, with 48 species from the families Macrouridae (32), Moridae (12), Mercluciidae (2), Gadidae (1), and Melanonidae (1); followed by Ophidiiformes, with 37 species from the families Ophidiidae (26), Bythitidae (4) Carapidae (4), and Aphyonidae (3); Anguilliformes, with 35 species from the families Congridae (15), Synaphobranchidae (14), Nettastomatidae (5), and Colocongridae (1); Perciformes, with 22 species from the families Bembropidae (5), Scorpaenidae (6), Zoarcidae (4), Serranidae (3), Peristediidae (2), Psychrolutidae (1), and Setarchidae (1); and Alepocephaliformes, with 21 species from the families Alepocephalidae (18) and Platytrocidae (3).
Other deep-benthopelagic fishes includes the Aulopiformes (15), Notacanthiformes (10), Pempheriformes (10), Lophiiformes (7), Pleuronectiformes (7), Syngnathiformes (6), Beryciformes (6), Scombriformes (5), Caproiformes (2), Polymixiiformes (2), Zeiformes (2), Ateleopodiformes (1), and Tetraodontiformes (1).
The 144 species of mesopelagic fishes are included in only a single order of Elasmobranchii and four orders of Actinopteri (Fig. 7.4). The elasmobranchs are represented by four species of Squaliformes from the families Etmopteridae (3) and Dalatiidae (1). The actinopterygians are represented by 79 species of Myctophiiformes from the families Myctophidae (77) and Neoscopelidae (2), followed by 49 species of Stomiiformes from the families Gonostomatidae (16), Sternoptychidae (14), Stomiidae (10), and Phosichthyidae (9). Other mesopelagic fishes are the scombriform families Chiasmodontidae (6) and Caristiidae (4), and the gadiform family Bregmacerotidae (2).
The bathypelagic fishes include 147 species (Fig. 7.4). The Elasmobranchii are represented by only seven species of deep-sea sharks from the orders Laminiformes, families Cetorhinidae (1), Megachasmidae (1) and Mitsukurinidae (1), and Squaliformes, families Dalatiidae (2) and Etmopteridae (2). Among the Actinopteri, the most diversified groups are the Aulopiformes, with 32 species from the families Paralepididae (14), Scopelarchidae (6), Notosudidae (5), Evermannellidae (4), and Alepisauridae (3); followed by Stomiiformes, with 28 species from the family Stomiidae, Scombriformes, with 18 species from the families Chiasmodontidae (6), Trichiuridae (5), Gempylidae (4), Caristiidae (1), Centrolophidae (1), and Nomeidae (1); Lophiiformes with 17 species from the families Oneirodidae (4), Ceratiidae (3), Himantolophidae (3), Gigantactinidae (2), Melanocetidae (2), Chaunacidae (1), Diceratiidae (1), and Neoceratiidae (1); and Anguilliformes, with 14 species from the families Nemichthyidae (5), Serrivomeridae (3), Nettastomatidae (2), Cyematidae (1), Derichthyidae (1), Eurypharyngidae (1), and Saccopharyngidae (1). Other bathypelagic fishes belong to the orders Beryciformes (12), Argentiniformes (11), Lampridiformes (8), Pempheriformes (3), Zeiformes (3), and Perciformes (1).
Within the two groups of shallow water fishes that can be occasionally be found in the deep sea, the epipelagic fishes are represented by two species of the lamniform sharks families Lamnidae (2) and Alopidae (1); and 31 species of the orders Scombriformes families Bramidae (10), Scombridae (6), Nomeidae (4), Ariommatidae (2), Gempylidae (2), Centrolophidae (1), and Trichiuridae (1), followed by the orders Tetraodontiformes (3), Acanthuriformes (1), and Istiophoriformes (1).
The shallow benthopelagic fishes are composed by 91 species from 36 families. Holocephali is represented by a single species of Callorhinchidae, and the Elasmobranchii by 25 species, including seven species of Rajiformes from the families Arhynchobatidae (4) and Rajidae (3); five species of Carcharhiniformes, families Triakidae (4) and Scyliorhinidae (1); and five species of Squaliformes, family Squalidae (5). The additional species belong to the orders Lamniformes (3), Squatiniformes (2), Torpediniformes (2), and Hexanchiformes (1).
Among the Actinopteri, Perciformes is the most diverse group, with 23 species from the families Serranidae (12), Peristediidae (4), Priacanthidae (3), Triglidae (3), and Scorpaenidae (1), followed by the Anguilliformes, with ten species from families Muraenidae (3), Ophichthidae (3), Chlopsidae (2), Congridae (1), and Muraenesocidae (1); Pleuronectiformes, with nine species from the families Cynoglossidae (4), Bothidae (3), and Paralichthyidae (1); and Aulopiformes, with six species from the families Synodontidae (5) and Aulopidae (1). Other shallow benthopelagic fish groups include the Lutjaniformes (2), Beryciformes (2), Gadiformes (2), Pempheriformes (2), Lophiiformes (3), the families Malacanthidae (2) and Emmelichthyidae (1), which are incertae sedis in Eupercaria, and Opistognathidae (1), incertae sedis in Ovolentaria.
7.5 Anthropogenic Impacts and Major Treats
Recent accounts of the Brazilian fauna at risk of extinction include 16 species of deep-sea fishes (ICMBIO/MMA 2018a, b). Five species were categorized as vulnerable, including the Soto’s hagfish (Myxine sotoi), the great white shark (Carcharodon carcharias), the argentine torpedo (Tetronarce puelcha), the snowy grouper (Hyporthodus niveatus), and the tile fish (Lopholatilus villarii). Three species are categorized as endangered, the dusky smooth-hound (Mustelus canis), the spotback skate (Atlantoraja castelnaui), and the warsaw grouper (Hyporthodus nigritus). Seven species are categorized as critically endangered, the picked dogfish (Squalus acanthias), two angelsharks (Squatina argentina and S. occulta), two houndsharks (Galeorhinus galeus and Mustelus fasciatus), the broadnose-sevengill shark (Notorynchus cepedianus), and the Atlantic wreckfish (Polyprion americanus). Major treats for those species are related to overfishing causing considerable populational decline in the past 20 years.
Fishing operations targeting deep-sea species on the Brazilian EEZ have been conducted by international vessels since the late 1990s, focusing on both fishes and crustaceans from the continental slopes off Northern and Southern Brazil, the Ceará Plateau, and the Fernando de Noronha Chain (Athiê and Rossi-Wongtschowski 2005; Alvarez Perez et al. 2009; Kitahara 2009). Targeted stocks of several deep-sea species such as the blackfin goosefish (Lophius gastrophysus), Argentine hake (Merluccius hubbsi), and Atlantic wreckfish (Polyprion americanus) are currently depleted (Perez and Haimovici 1998; Perez and Wahrlich 2005; Pezzuto et al. 2006). The ecological impacts of deep-sea fisheries are similar to the impacts in shallow systems and may result on the removal of habitat-formers, decline in diversity, changes in abundance and biomass, reduction in distribution, and changes in the community structure; however, the rates of recovery are much slower and difficult to estimate (Clark et al. 2016).
Additionally, the deep-sea species have been consistently affected by human activities as disposal of litter and waste in sea beds, residuals from sewage, discards from fishing activities and transport of livestock, chemical contamination such as oil spills and pharmaceuticals, mining, ocean acidification, and fisheries (Koslow et al. 2000; van den Hove and Moreau 2007; Ramirez-Llodra et al. 2011; White et al. 2012).
The exploration oil and gas obtained from deep waters in Brazil started back in 1979, and, nowadays, Brazil is one of the world leaders in the exploration of oil and gas in deep (500–1500 m) and ultra-deep (>1500 m) waters. Major fields of explorations include the pre-salt layers of the Bacia de Campos and Bacia de Santos, which extends for about 800 km from the Espírito Santo and Santa Catarina States, and the Bacia Potiguar, located off the Rio Grande do Norte and Ceará States (Trindade et al. 1992; van den Hove and Moreau 2007; Morais 2013). There are substantial risks associated with this kind of activity, including light and acoustic disturbance, disposal of wastes produced during the drilling process, produced water, mechanical impacts caused by anchors, control cables, pipelines and risers, change of habitats by seabed infrastructures, mass hydrocarbon release caused by oil and gas spill, and mass dispersant and chemical amplificant release applied to oil spills (White et al. 2012; Cordes et al. 2016).
7.6 Challenges and Perspectives
The Brazilian deep-sea known unknowns include large areas of the continental slope in Northern and Northeastern Brazil and, in South and Southern Brazil, depths below 500 m, specially from the southern part of Rio de Janeiro to Rio Grande do Sul.
Besides the continental slope, key areas for further exploration are seamounts and oceanic islands, such as the North Brazilian ridge, the Fernando de Noronha ridge, including the oceanic islands of the Fernando de Noronha Archipelago and Atol das Rocas, the Victoria-Trindade Seamount Chain with the Trindade and Martin Vaz archipelago, and the isolated Saint Peter and Saint Paul archipelago, and Rio Grande Rise. Those remote areas are particularly challenging to sample, because of the difficult access and adverse oceanographic conditions of the strong currents, the steep and rocky bottom, and frequent inclement weather in the Rio Grande rise area.
The many efforts to obtain samples from greater marine depths since the beginning of the twenty-first century are contributing to cover such gaps and boosting significant gains to better understand the biodiversity of deep-sea fishes in the western South Atlantic. In the past years, a number of scientific contributions were published focusing on the deep-sea fish fauna, including general inventories and books (De Figueiredo et al. 2002; Madureira et al. 2004; Bernardes et al. 2005b; Costa et al. 2007; Lavrado and Brasil 2010; Oliveira et al. 2015), ecological data on distribution and abundance (Bernardes and Rossi-Wongtschowski 2007; Braga et al. 2014), comprehensive taxonomic reviews (Mincarone et al. 2008; Santos and Figueiredo 2008; Melo 2009, 2010; Lima et al. 2011), and descriptions of sixteen new taxa (see above).
Indeed, only with the development of long-term projects to sample the deep ocean, the deposit of specimens in well-established natural history collections, and extensive public outreach will ensure fantastic discoveries, the appropriate monitoring of anthropogenic impacts on deep-sea communities, and inspire new generations of scientists.
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Acknowledgements
We are deeply indebted to Paulo Sumida and Alexandre Turra (IOUSP) for the opportunity and comments, and the crew of the RV Alpha Crucis under the commandment of José H. M. Rezende, for assistance during the DEEP-OCEAN project. We also would like to thank Paulo A. Buckup, Marcelo R. de Britto and Cristiano R. Oliveira (MNRJ), Alessio D. Silva, Mario C. C. de Pinna, José L. de Figueiredo, Michel D. Gianetti and Osvaldo T. Oyakawa (MZUSP) for allowing access to scientific collections; Polyana Roque (UFRPE), Alfredo Carvalho-Filho (Fish Bizz), Flavia L. Frédou (UFRPE) Cristiano R. Moreira (MNRJ) for providing informations about several scientific projects; Amanda A. Gomes, Flavia T. Masumoto, Barbara B. Bouquerel, and Rayane S. França (IOUSP) for helping to review the species lists, and to the librarians Maria Pureza and Isair de Souza (IOUSP), Dione Seripierri (MZUSP) and the Biodiversity Heritage Library (https://www.biodiversitylibrary.org/) for making available the literature necessary for this work. Financial support was provided to MRSM by FAPESP (#2017/12909-4) and CNPq (#433050/2016-0).
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de Melo, M.R.S., Caires, R.A., Sutton, T.T. (2020). The Scientific Explorations for Deep-Sea Fishes in Brazil: The Known Knowns, the Known Unknowns, and the Unknown Unknowns. In: Sumida, P.Y.G., Bernardino, A.F., De Léo, F.C. (eds) Brazilian Deep-Sea Biodiversity. Brazilian Marine Biodiversity . Springer, Cham. https://doi.org/10.1007/978-3-030-53222-2_7
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