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CITATION Perez, J.A.A., E. dos Santos Alves, M.R. Clark, O. Aksel Bergstad, A. Gebruk, I. Azevedo Cardoso, and A. Rogacheva. 2012. Patterns of life on the southern Mid-Atlantic Ridge: Compiling what is known and addressing future research. Oceanography 25(4):16–31, http://dx.doi.org/10.5670/ oceanog.2012.102.

DOI http://dx.doi.org/10.5670/oceanog.2012.102

COPYRIGHT This article has been published inOceanography , Volume 25, Number 4, a quarterly journal of The Oceanography Society. Copyright 2012 by The Oceanography Society. All rights reserved.

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Patterns of Life on the Southern Mid-Atlantic Ridge

Compiling What is Known and Addressing Future Research

By José Angel A. Perez, Eliana dos Santos Alves, Malcolm R. Clark, Odd Aksel Bergstad, Andrey Gebruk, Irene Azevedo Cardoso, and Antonina Rogacheva

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2.5 mm ABSTRACT. The South Atlantic is one of the youngest of all the major oceans. It has prominent topographic features, in particular, the Mid-Atlantic Ridge. This feature largely determines deepwater circulation patterns that connect this ocean to the North Atlantic, Southern, Indian, and Pacific Oceans. Yet very little is known about biodiversity patterns in the South Atlantic or its connectivity with other deep Fauna collected during the South Atlantic MAR-ECO cruise, October– areas of the world ocean. The South Atlantic MAR-ECO (SA MAR-ECO) project November 2009. (a) Leontocaris was developed as part of the Census of Marine Life to fill such knowledge gaps, smarensis new sp. (b) Parapagurus abyssorum. (c) Parapagurus particularly focusing on the southern Mid-Atlantic Ridge. This article summarizes pilosimanus in symbiosis with and reviews published information on the deep South Atlantic as background zoanthid Epizoanthus sp. Photos: knowledge for the concepts, principal questions, and goals of SA MAR-ECO. It also a–b, Irene Cardoso; c, André Barreto describes the strategies and methodological approaches adopted for a southern Mid-Atlantic Ridge sampling program and the limitations and achievements of the first field survey in November 2009.

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16 Oceanography | Vol. 25, No. 4 INTRODUCTION indicating how mid-ocean ridge com- information on the South Atlantic as Mid-ocean ridges and seamount chains munities are structured (Vecchione background knowledge for the con- are prominent structures of the deep et al., 2010). As with all CoML projects, cepts, major questions, and goals of seafloor that have attracted considerable MAR-ECO necessarily began with a SA MAR-ECO. It also describes the strat- attention for their biodiversity, fisher- data-mining effort to determine what egies and methodological approaches ies, and mineral resources (Clark et al., was known about the area. to be adopted by the proposed southern 2010). The potential for sustainable In 2006, an initiative to expand sam- Mid-Atlantic Ridge sampling program exploration of these ecosystems and the pling activities and studies to the South and the limitations and achievements of need for their conservation have been Atlantic mid-ocean ridge spun off the the first field experience in 2009. issues of increasing concern worldwide MAR-ECO project, supported by the and have motivated modern scientific CenSeam (Census of Marine Life on What Do We Know initiatives such as those within the Seamounts) project (Consalvey et al., About the Deep South scope of the global Census of Marine 2010). This initiative was particularly Atlantic Ocean? Life (CoML) (McIntyre, 2010). One of concerned with addressing biologi- Geological Origins these initiatives, MAR-ECO: Patterns cal questions considering (a) complex The South Atlantic Ocean was formed and Processes of the Ecosystems of the patterns of geological morphology by the separation of the South American Northern Mid-Atlantic, was proposed and deepwater circulation of the ridge, and African Plates 175–90 million years in 2001 as a CoML field project to (b) its connections with the North ago. Its configuration and size are out- study the diversity and ecology of the Atlantic, Pacific, Indian, and Southern comes of two independent spreading northern Mid-Atlantic Ridge (MAR; Oceans, and (c) its recent origin, as it processes: one that formed the North Bergstad and Godø, 2003). Historically, is virtually “the youngest of the major Atlantic in the early Mesozoic nearly this extensive and topographically rough world oceans” (Levin and Gooday, 200 million years ago and another that seafloor spreading area has been poorly 2003). A first field expedition conducted formed the South Atlantic 100 million sampled, except for the chemosynthetic in 2009 to sample pelagic and benthic years later. This latter spreading process ecosystems that lie along small portions biota of the southern Mid-Atlantic Ridge resulted in connections with three other of the ridge. Consequently, there were effectively initiated the “South Atlantic oceans—the Southern, Pacific, and many unanswered questions regarding MAR-ECO” (SA MAR-ECO) project Indian. Also, it included a north-south as the origin and dispersion of the MAR’s focused on improving knowledge about well as an east-west component, which deep-sea fauna and the significance of its the biodiversity patterns of this vast and shaped the sinuous seafloor and defined “comparatively shallow structures in the little known area of the world ocean. most of its features (Figure 1; Fairhead middle of the deep oligotrophic ocean, This article reviews published and Wilson, 2004). Because it is relatively for the distribution and production of biota” (Bergstad et al., 2008). MAR-ECO José Angel A. Perez ([email protected]) is Professor, Centro de Ciências addressed this knowledge gap by com- Tecnológicas da Terra e do Mar, Universidade do Vale do Itajaí, Santa Catarina, Brazil. bining modern technology, an intensive Eliana dos Santos Alves is Research Associate, Centro de Ciências Tecnológicas da Terra and well-planned sampling strategy, and e do Mar, Universidade do Vale do Itajaí, Santa Catarina, Brazil. Malcolm R. Clark the collaborative work of international is Principal Scientist, National Institute for Water and Atmospheric Research, scientific experts (Bergstad and Godø, Wellington, New Zealand. Odd Aksel Bergstad is Principal Scientist, Institute of 2003). Pelagic and benthic habitats were Marine Research, Bergen, Norway. Andrey Gebruk is Head of Laboratory, P.P. Shirshov sampled to a maximum depth of 4,500 m Institute of Oceanology, Russian Academy of Sciences (IORAS), Moscow, Russia. over the North Atlantic mid-ocean Irene Azevedo Cardoso is a researcher in the Setor de Carcinologia, Departamento de ridge, providing well-documented new Invertebrados, Museu Nacional/Universidade Federal do Rio de Janeiro, São Cristóvão, information on previously described Rio de Janeiro, Brazil. Antonina Rogacheva is PhD Candidate, P.P. Shirshov Institute of and undescribed species and models Oceanology, IORAS, Moscow, Russia.

Oceanography | December 2012 17 young, the South Atlantic is narrow and linearity of the ridge system and large- transform faults as the ridge axis sub- has a high ratio of margin to deep water scale ocean circulation (Huang and Jin, sided. Seamounts on both rises were also (Levin and Gooday, 2003). 2002; Fairhead and Wilson, 2004). At the formed by intermittent volcanic activity The most prominent ocean floor southern extreme, two seamount chains, that followed this separation (< 80 mil- feature is the Mid-Atlantic Ridge, Walvis Ridge and Rio Grande Rise, form lion years ago); they include the islands of which extends 14,000 km continuously bridges that run from the central ridge the Tristan da Cunha group and Gough from Iceland in the north (87°N) to to the African and South American con- (Fodor et al., 1977; Kumar, 1979; Camboa Bouvet Island (54°S) in the south, and tinental margins, respectively. Kumar and Rabinowitz, 1984). The MAR, the rises 2,000–3,000 m above the seafloor (1979) called them “paired aseismic Equatorial Fracture Zone, and the sea- (Figure 1). The joining of the north- rises” of the South Atlantic and proposed mount ridges surround five basins: Brazil, south spreading centers in the early a common geological origin between Argentine, Guinea, Angola, and Cape mid-Cretaceous resulted in development 100 and 80 million years ago. During (Figure 1). These basins are connected by of a shear zone between West Africa this early phase of the South Atlantic deep channels that include the Vema Sill and the northeastern margin of Brazil. opening, “abnormally intense” volcanism and Hunter Channel on either side of the It produced the Equatorial Fracture along the axis of a MAR segment created Rio Grande Rise, and Kane Gap on the Zone, a large geological feature about a volcanic pile that was subsequently eastern side of the Equatorial Fracture 60 million years old, that affects both the separated by east-west movement of Zone (Murray and Reason, 1999).

Oceanography The counterclockwise “Subtropical Gyre” formed by the interconnected Brazil, Antarctic Circumpolar, Benguela, and South Equatorial Currents dominates the surface circulation of the south- ern Atlantic Ocean. Wind-effect and thermohaline processes determine this circulation pattern, which affects subsurface waters as deep as 1,500 m (Schmid et al., 2000). Below 2,000 m, the interactions between North Atlantic Deep Water (NADW) and Antarctic Bottom Water (AABW), induced by their thermohaline properties and the seafloor topography (Figure 2), drive the main flow path of deep water. In the western basin, NADW flows southward between 1,500 and 4,000 m depth. Below this layer, AABW flows in the opposite direction, penetrating the South Atlantic through the Vema Sill and the Hunter Figure 1. South Atlantic Ocean seafloor and its main topographic features as extracted from ETOPO Channel and into the North Atlantic (http://www.earthmodels.org). Boxes represent target sectors defined for the South Atlantic MAR-ECO project. SPSPS = St. Peter and St. Paul’s Sector. SEMS = South Equatorial Mid-Atlantic Ridge Sector. (Murray and Reason, 1999). At the TMS = Tropical Mid-Atlantic Ridge Sector. SCMS = Subtropical Convergence Mid-Atlantic Ridge Sector. equator, this water mass also branches WRS = Walvis Ridge Sector. RGRS = Rio Grande Rise Sector. The yellow dotted line depicts the track of the twenty-ninth voyage of R/V Akademik Ioffe (Shirshov Institute, Academy of Sciences, Russia) in eastward, flowing through the Kane Gap November 2009, including South Atlantic MAR-ECO predefined “superstations” and extra stations. back into the Southeast Atlantic below

18 Oceanography | Vol. 25, No. 4 4,000 m depth (Stephens and Marshall, The equatorial sector of the MAR, (10°W) between June and December. 2000). That is the main source of AABW including the Equatorial Fracture These authors pointed out that the in the eastern basins because the Walvis Zone, lies under the South Equatorial coastal upwelling system off Namibia Ridge blocks northward flow of this Current System where two provinces and the plume produced by the Congo water mass from the Southern Ocean. are defined as the East Tropical Atlantic River runoff also contributed to such As a result, the Southeast Atlantic basin, and the West Tropical Atlantic (ETRA concentrations. Because all these pro- above 4,000 m, is almost exclusively and WTRA). Phytoplankton blooms in cesses principally influence areas of the NADW that flows in through the frac- eastern equatorial waters, which may Southeast Atlantic, energy input to the ture zones (e.g., Romanche and Chain) represent important sources of energy deep seafloor, and consequently benthic at the equator (Huang and Jin, 2002; input into the MAR region, season- biomass distribution, may be higher Bickert and Mackensen, 2003). ally influence these oligotrophic waters toward the east (Wei et al., 2010). Except for limited areas of hydro- (Longhurst, 1993). During the boreal The South Atlantic Gyral Province is thermal vents and seeps, life patterns summer, the northern displacement delimited by the extension of the South along the Mid-Atlantic Ridge depend of the Intertropical Convergence Zone Atlantic subtropical gyre and may influ- on biological production exported from (ITCZ) tends to intensify the southeast ence a significant portion of the southern the sunlit epipelagic layers (Vecchione trade winds that, in turn, cause deepen- MAR that extends between latitudes et al., 2010). In the South Atlantic, spatial ing of the thermocline in the WTRA and 10° and 37°S. These are stable oligotro- and temporal patterns of production shoaling in the ETRA. Both the thermo- phic waters where mean productivity is are associated with large-scale pelagic cline and the upper mixed layer become less than 35 g C m–2 yr–1 (Berger, 1989). systems, defined by Longhurst (1995) as shallower in the east equatorial Atlantic Between 30° and 60°S, however, the ridge “biogeochemical provinces,” each hav- where primary production is enhanced axis crosses beneath the Subtropical and ing specific “currents, fronts, topography (Figure 2). In this area, Pérez et al. (2005) Sub-Antarctic Frontal Zones (Stramma and recurrent features in the sea surface reported chlorophyll a concentrations and Peterson, 1990) as well as two chlorophyll field” (Figure 2). varying between 0.66 and 1.28 mg m–3 productive biogeochemical provinces,

Figure 2. Schematic representation of South Atlantic Ocean patterns of deepwater circulation (left panel) and pelagic productivity and biogeochemical provinces (right panel) based on Stramma and Peterson (1990), Longhurst (1993, 1995), Murray and Reason (1999), Stephens and Marshall (2000), and Pérez et al. (2005). Red and blue arrows represent the circulation of North Atlantic Deep Water (NADW, 1,500–4,000 m deep) and Antarctic Bottom Water (AABW, > 4,000 m deep), respectively. ETAB = East Tropical Atlantic Bloom. STG = Subtropical Gyre. STC = Subtropical Convergence. SAC = Sub-Antarctic Convergence. The 1,000 and 2,000 m isobaths are displayed in the background.

Oceanography | December 2012 19 the South Subtropical Convergence the faunal groups most widely studied, Zone (e.g., Pasternak, 1968; Parin and Province and the Sub-Antarctic Province principally from collections obtained Andriyashev, 1972; Andriyashev et al., (Longhurst, 1995). Mean surface produc- by large-scale expeditions and fishery 1974; Malyutina, 1999, 2004). tivity nearly doubles (71.4 g C m–2 yr–1) surveys around oceanic islands and sea- Novel biological data have been and also exhibits a moderate seasonal mounts (e.g., Krefft, 1976; Pakhorukov, produced from the recently discovered fluctuation pattern (Moore and Abbot, 1976, 1980; Shcherbachev et al., 1985, MAR hydrothermal vent sites 3–7° south 2000), the implication being that deep- 1995; Trunov, 1981; Parin et al., 1995). of the equator, the hottest reported to water habitats (benthic and pelagic) of Air-breathing vertebrates, such as turtles, date, with temperatures up to 407°C the southern MAR to the north and to seabirds, and mammals, have been stud- (Devey et al., 2005; Koschinsky et al., the south of ~ 30°S may obtain surface ied by regional surveys around oceanic 2006; German et al., 2008). A detailed food supply at low/constant and high/ islands (e.g., St. Peter and St. Paul’s Rocks taxonomic description of most groups seasonally varying rates, respectively. and Ascension) and in some fishing is still unavailable in the literature, but Such a latitudinal pattern parallels that grounds, where these animals interact visual assessments indicate that the described in the North Atlantic (Gordon with commercial fishing activities. southern fauna may be similar to north- et al., 2008), although both primary pro- Records of deepwater macrofauna ern MAR vent fauna; for example, the duction rates and seasonal fluctuations diversity largely concentrate on the mussel Bathymodiolus puteoserpentis, seem more important in the Northern South American and African continen- the vesicomyd clam Abyssogena Hemisphere (Moore and Abbot, 2000; tal margins and the Southern Ocean. southwardae, and the alvinocarid shrimp Levin and Gooday, 2003). The deep central South Atlantic is one Rimicaris exoculata (German et al., of the least-studied areas of the world 2011) are dominant in both habitats. Biological Information ocean (OBIS, 2011). Much of the data A. southwardae inhabits both hydro- Biological information available for available from the South Atlantic MAR thermal vents and cold seeps in the South Atlantic oceanic areas compiled derive from large-scale expeditions Atlantic, including those on the eastern as background for the SA MAR-ECO conducted by North Atlantic countries and western continental margins and in project includes more than 720 records since the late nineteenth century (Wüst, the mid-ocean system (Krylova et al., to date (for a complete reference list, 1964). The first and highly significant 2010). R. exoculata is endemic to the see http://www.mar-eco.no; Table 1). contribution was the HMS Challenger MAR, and no genetic differences were Biological studies have generally Expedition between 1873 and 1876, the found between individuals sampled to focused on (a) the epipelagic environ- first worldwide effort to describe deep- the north and to the south of the equator ment around oceanic islands such as sea macrofauna biodiversity (Murray, (Teixeira et al., 2012). The Rimicaris- St. Peter and St. Paul’s Rocks, Ascension, 1895). In particular, during the ship’s associated copepod Stygiopontius St. Helena, Tristan da Cunha group, return trip to England, in March 1876, cladarus was also observed at southern Gough, and Bouvet (e.g., Duhamel et al., this vessel set a straight track along the MAR vent sites (Ivanenko et al., 2007). 1983; Edwards and Glass, 1987; Andrew top of the ridge, from Tristan da Cunha These faunal similarities are inconsistent et al., 1995; Floeter and Gasparini, 2000; to Ascension Island, conducting benthic with the hypothesized role of equato- Trunov, 2006), and (b) the epipelagic dredge tows at 2,200–3,600 m depths rial fracture zones and the MAR as and mesopelagic environments over sea- and recording over 80 taxa (e.g., Agassiz, barriers for the dispersal of vent fauna mount chains associated with the central 1881; McIntosh, 1885; Busk, 1886). north-south and east-west, respectively ridge. They were focused primarily on Other historical contributions were pro- (German et al., 2011). species occurrence and/or description, vided by the former USSR’s expeditions Further knowledge is derived from taxonomic reviews, and biogeography. in the second half of the twentieth cen- benthic diversity studies on non­ Data on vertical distribution patterns, tury, although most published data refer chemosynthetic ecosystems off Bouvet population dynamics, and ecological to trenches and oceanic basins, and only Island and Spiess Seamount (100–600 m processes of macrofauna are scarce or a few samples were obtained from ridge depths) at the southernmost end of the absent. Pelagic and demersal fishes were habitats such as the Romanche Fracture South Atlantic MAR system (see Polar

20 Oceanography | Vol. 25, No. 4 Table 1. Themes and marine environments examined by studies conducted inSA MAR-ECO target areas and other deep areas of South Atlantic. Sunlit Levels: Studies on epipelagic or intertidal/infratidal environments. Deep Sea: Studies on meso/bathypelagic or abyssal/bathyal environments. All Depths: Studies on a wide range of depths or where it was not possible to identify the depth range.

Depth Range Target Area/Theme Sunlit Levels Deep Sea All Depths Totals

Southern Mid-Atlantic Ridge Plankton 1 1 - 2 Benthos 28 21 - 49 Nekton 50 2 - 52 Various Zoological Groups 9 - - 9 Environmental Setting 84 St. Peter and St. Paul’s Rocks Plankton 5 - - 5

eas Benthos 20 1 - 21

al Ar Nekton 42 - - 42 c

o Various Zoological Groups 8 - - 8 g L Environmental Setting 28 rin e

v Rio Grande Rise Nekton 4 5 2 11 es Co i Various Zoological Groups 1 1 tud S Environmental Setting 19 Walvis Ridge Benthos 1 5 2 8 Nekton 5 4 2 11 Microbiology - 1 - 1 Various Zoological Groups - 1 - 1 Environmental Setting 14 Totals 173 42 6 366

South Atlantic

Plankton 36 - - 36 g

rin Benthos 4 35 1 40 e eas v Nekton 29 3 5 37 de Ar

es Co Microbiology - 2 - 2 i i

W Various Zoological Groups 9 3 - 12 tud S Environmental Setting 117 Totals 78 43 6 244

Other South Atlantic Deep Water 111

Total 721

Oceanography | December 2012 21 Biology, 2006:29, special issue). These on megafauna diversity and ecology C. profunda) were at the likely southern studies show that the megabenthic fauna on the Walvis Ridge and Rio Grande and northern limits of their distribution of these relatively “young” (~ 1 million Rise seamount chains adjacent to the ranges, respectively. The Valdivia Bank years old), small (~ 800 km2 above the MAR. Catches and biological data are was also shown to be a potential step- 500 m isobath), and isolated environ- available from these areas for alfon- ping-stone for west-east dispersion of the ments can be remarkably diverse and are sino (Berix splendens), orange roughy benthic octopod Scaeurgus unicirrhus probably influenced by their exposure (Hoplostethus atlanticus), southern (Sánchez and Alvarez, 1988) in the South to the Antarctic Circumpolar Current, boarfish (Pseudopentaceros richardsoni), Atlantic and to provide unique Atlantic which connects them with other bathyal cardinalfishes (Epigonus spp.), bluenose outposts for fish (Parapercis roseoviridis, habitats in the Patagonian and Antarctic (Hyperoglyphe antarctica), Patagonian Chrionema chlorotaenia) and crus- continental margins, sub-Antarctic toothfish (Dissostichus eleginoides), and tacean (Benthesicimus investigatoris, islands, and the South Pacific Ocean red crab (Chaceon spp.) (see Clark et al., Projasus parkeri) species only known to (Arntz, 2006). A total of 217 taxa were 2007, and Rogers and Gianni, 2010, occur in the Indian and Pacific Oceans identified by video transects, Agassiz for reviews). Russian and Spanish fish- (McPherson, 1983; Melville-Smith, 1990; trawls, and baited traps around Bouvet ing surveys undertaken in the Valdivia Bañon et al., 2000, 2001). Investigations Island and on the summit of Spiess Bank (Walvis Ridge) have also provided on diversity and benthic ecology of Seamount (Arntz et al., 2006; Gutt benthic and benthopelagic diversity the Walvis Ridge seamounts have et al., 2006). Echinoderms, in particular inventories and community struc- recently resumed through initiatives of ophiuroids (e.g., Ophionotus victoriae ture data (McPherson, 1987; Fedorov, countries such as Spain and Namibia, and Ophiurolepis sp.), were the most fre- 1991; Fedorov and Karamyshev, 1991). motivated by the need to identify vul- quently recorded taxon around Bouvet Decapod crustacean fauna was studied nerable marine ecosystems and support Island. Diversity was found to be much by McPherson (1984), who described the ecosystem-based fishing manage- higher than previously reported, with 28 species (20 benthic, eight pelagic, ment measures adopted by the South dramatic increases in species records of seven new to science), extending the Atlantic Fisheries Organization (SEAFO) molluscs (16 to 45 species), cheilostome geographic distribution of most of (Durán Muñoz et al., 2012). bryozoans (20 to 34 species), and espe- them to the Southeast Atlantic. On the Much less information is available cially amphipods (5 to 62 species) (Arntz same seamount, Zibrowius and Gili from the Rio Grande Rise, except for et al., 2006; Barnes, 2006; Linse, 2006). (1990) reported nine species of scler- fish fauna records produced by Russian Many of these records were new to sci- actinian cold-water corals, two of them exploratory fishing. Parin et al. (1995), ence, including the Opisthobranchia (Lophelia pertusa and Caryophyllia examining bottom-trawl collections from Tritonia dantari (Ballesteros and profunda) occurring on the summit 1974 and 1988–1989, reported 65 species Avila, 2006), the amphipod Atyloella (230–250 m), one (Enallopsammia of benthic, benthopelagic, and bathy- tribinicuspidata (Rauschert, 2006), and rostrata) on the upper flanks pelagic fish, nearly half of them (34) the crab Paralomis elongata (Spiridonov (511–586 m), and the remaining spe- belonging to the families Macrouridae, et al., 2006). An analysis combining cies (Fungyaciathus hydra, Caryophyllia Alepocephalidae, Synaphobranchidae, stable isotopes and feeding relation- balaenacea, C. valdiviae, Stephanocyathus and Chlorophthalmidae. One species, ships showed that the benthic ecosystem campaniformes, Deltocyathus conicus Gaidropsarus pakhorukovi (Family around Bouvet Island is dominated by a and Truncatoflabellum sp.) on the lower Gadidae), was described as new to sci- variety of suspension feeders and mobile flanks (882–1,230 m). The geographic ence, and nine species were reported for benthic predators and scavengers, par- distribution of most species is probably the first time in the Southwest Atlantic. ticularly peracarid crustaceans (but not limited to the Southeast Atlantic, but The reported ichthyofauna was basically fishes, which were rare in the samples; two species (L. pertusa and E. rostrata) composed of equal shares of subtropical- Jacob et al., 2006). were found to be widely distributed in temperate water species, mostly of the Commercial and exploratory fish- the North Atlantic, Indian, and Pacific Southern Hemisphere, and tropical ing have also been sources of data Oceans, and two species (D. conicus and species distributed in the Atlantic and

22 Oceanography | Vol. 25, No. 4 other oceans. A high level of similarity includes the southern extreme of the Schlacher et al., 2010). For example, was found between this fauna and that South Atlantic mid-ocean ridge and sea- seamounts, ridges, canyons, and slope reported for similar depths around the mount chains mostly south of 30°S. In areas on continental margins may share Walvis and Madagascar Ridges in the the abyssal depth zone (3,500–6,500 m), similar patterns of faunal composition Indian Ocean. The Rio Grande Rise has four provinces are proposed in the South (e.g., Rowden et al., 2010; Menot et al., also been subject to current biodiver- Atlantic, as delimited by the extent of 2010), but can differ in structure and sity investigation, particularly due to its major deep basins: Brazil, Angola-Sierra relative abundance (e.g., McClain et al., potential for cobalt-rich ferromanganese Leone, Argentine, and East Antarctic- 2009). Along the North Atlantic mid- crust exploration and the need to pro- Indian. In the hadal depth zone ocean ridge, there are notable latitudinal duce comprehensive “environmental (> 6,500 m), a “Romanche” province is discontinuities in deep fauna composi- baseline” studies as recommended by defined at the Romanche trench (a com- tion in association with productivity gra- the International Seabed Authority (ISA, ponent of the Romanche Fracture Zone) dients in the epipelagic layers (Vecchione 2007; recent work of author Perez). in the Equatorial Atlantic. This study et al., 2010). These findings highlight the It is clear from the examples outlined also includes an independent province importance of understanding biogeo- above that existing knowledge on bio- classification for hydrothermal vent envi- graphic patterns as well as mechanisms diversity of the southern MAR is frag- ronments. A “Mid-Atlantic Ridge South” of dispersal and connectivity whereby mented and concentrated on its northern province was hypothesized, although faunal communities in such habitats are and southern extremes as well as the recent biological data from vent fields linked across a range of spatial scales adjacent seamount chains. An extensive south of the equator have generally sup- (Clark et al., 2012). Therefore, as the area between 10° and 50°S still remains ported a connection with North Atlantic geological history of the South Atlantic undersampled and much less understood vent sites (see above). basin and its complex interactions with than the northern MAR. deepwater circulation patterns are taken Defining Priorities into consideration, a number of scientific Biogeography for Understanding questions about deep-sea biodiversity Combining the available information Diversity Patterns of patterns of the South Atlantic arise: on biodiversity with bathymetry and the Southern MAR • Are the faunal communities of the the geographical distribution of bot- Sampling efforts within the umbrella of Mid-Atlantic Ridge and seamounts tom temperature, salinity, oxygen, and the CoML significantly enhanced diver- related to and part of broader deep organic matter flux, a set of benthic sity inventories in the world ocean in South Atlantic environments? biogeographical provinces has been pro- general (Snelgrove, 2010). Yet, they also • Is the southern Mid-Atlantic Ridge posed (through an expert workshop) for revealed how incomplete our knowledge fauna different from that of the different depth zones in the deep South is on what lives in the deep environ- bathyal sectors of the South American Atlantic Ocean (UNESCO, 2009). The ments that are particularly critical in and African continental margins? lower bathyal depth zone (800–3,500 m) some areas, such as the Southeast Pacific • What are the environmental drivers of includes a wide “South Atlantic” prov- and the South Atlantic. Hence, deter- faunal composition and abundance? ince that extends from the equator to the mining faunal composition of deep-sea (e.g., is there a relationship between Antarctic Convergence and encompasses benthic and pelagic fauna associated surface production and abundance? the lower continental margins of Africa with the southern MAR constitutes a Do the physical ridges in the South and South America, isolated seamounts, major goal to be addressed by any ridge- Atlantic such as the Romanche and seamount chains (e.g., Rio Grande oriented sampling program. Fracture Zone, Rio Grande Rise, and Rise, Walvis Ridge), oceanic island CoML studies also emphasize that Walvis Ridge provide linkages or slopes, and the southern Mid-Atlantic deep-sea habitats are not isolated, but obstacles to faunal communities?) Ridge. Also a “sub-Antarctic” province rather are both connected in hori- • Are the MAR diversity patterns dif- delimited by Antarctic and Subtropical zontal space and dynamically linked ferent from other ridge systems in the Convergences encircles the globe and to the water column (McIntyre, 2010; Southern Hemisphere?

Oceanography | December 2012 23 These descriptive aspects of benthic and ecological complexities of the deep The former comprises a massive flat- and pelagic faunal composition denote South Atlantic. Relevant to such sam- topped structure that rises approximately priorities toward understanding the pat- pling are (a) target areas for concentra- 3,000 m from the ocean basin and is terns of life in the southern MAR and tion of sampling activity, (b) the range of bordered on the eastern side by ridges define a knowledge basis with which biota and ridge habitats to be sampled, and seamounts. The Walvis Ridge is a more complex questions about deep (c) spatial strategy and technology seamount chain that extends obliquely ecosystem processes can be addressed in to be adopted in sampling plans, and from the Namibia-Angola continental the future. They also define major goals (d) sampling platforms. margin to the Tristan da Cunha island for the development of a field project to: group, at the MAR (Figure 1). Seamount (a) describe and understand the patterns Target Areas fisheries surveys have been conducted of diversity, distribution, and abun- Practical limitations of time and effort on Walvis Ridge seamounts (Clark et al., dance of the organisms inhabiting the mean that sampling efforts should focus 2007), an area managed by SEAFO southern MAR and adjacent seamounts, on a few representative sectors of the (Rogers and Gianni, 2010). and (b) explore the role of these deep- ridge system. Six target sectors were ocean features in faunal dispersal pro- initially defined (Figure 1, Table 2). Targeted Fractions of Marine cesses between the coasts of Africa and Two of them, St. Peter and St. Paul’s Biota and Ridge Habitats South America and among the North Sector (SPSPS) and South Equatorial A comprehensive study on biodiversity Atlantic, Pacific, Indian, and Southern MAR (SEMS), are located on equato- patterns and processes of the MAR eco- Oceans. They would also contribute to rial fracture zones and include an array systems, as proposed by the MAR-ECO the sustainable use of natural resources of benthic habitats mostly formed by project, involves macrofauna sampling (e.g., mining, fishing, biotechnology) and ridge crests and trenches. At the surface, in benthopelagic and benthic habitats conservation of unique deep-sea ecosys- these habitats are under the influence of on the flanks and summits of the ridge, tems, as required by both governmental the seasonal eastern equatorial Atlantic as well as in the overlying pelagic zone and nongovernmental agencies in the primary production blooms (Longhurst, (Bergstad and Godø, 2003). The South South Atlantic. These include regional 1993), which may be a critical source of Atlantic MAR-ECO initiative incorpo- fisheries management organizations, energy to the deep habitats. rates the same focus with microbial sam- principally SEAFO (Southeast Atlantic Two sectors were identified at the pling in both the water column and sedi- Fisheries Organization) and ICCAT central axis of the MAR: (1) the Tropical ments added, not only to address a major (International Commission for the MAR Sector (TMS) located beneath the component of deepwater communities Conservation of Atlantic Tuna) as well as core of the South Atlantic Subtropical (Snelgrove, 2010) but also to include other international forums such as CBD Gyre and under the influence of an bioprospecting as a potential economic (Convention on Biological Diversity), oligotrophic and stable water column, by-product of the project. Sampling is ISA (International Seabed Authority), and (2) the Subtropical Convergence structured as follows: and FAO (United Nations Food and MAR Sector (SCMS) that crosses under- • Microbiology: Focused on prokary- Agriculture Organization). neath the Subtropical Convergence and otic (e.g., bacteria and Archaea) and extends into the sub-Antarctic zone eukaryotic (e.g., phytoplankton, Sampling Southern (Figure 1). Surface waters are highly protozooplankton, and benthic pro- MAR Habitats productive in the latter sector (Moore tists) microbial diversity. Capacity for In order to address the goals outlined and Abbot, 2000), and geologically, it producing certain enzymes such as above, a sampling strategy needs to includes an area where the MAR, Walvis lipases and cellulases is also included incorporate spatial and operational con- Ridge, and Rio Grande Rise converge. in this theme as preliminary steps cepts and technology developed for the The remaining sectors are located to toward further bioprospecting. North Atlantic MAR-ECO (Bergstad the west and the east of the MAR and • Zooplankton: Including meso-, macro-, et al., 2008; Wenneck et al., 2008) while enclose the Rio Grande Rise (RGRS) and and megaplankton inhabiting meso- considering the area and the geological Walvis Ridge Sectors (WRS) (Figure 1). and bathypelagic layers associated

24 Oceanography | Vol. 25, No. 4 with the southern MAR summits. • Macrobenthos: Including large-sized sectors, aligned across the ridge axis, to • Pelagic Nekton: Including micronekton epibenthic organisms inhabiting both address bathymetric gradients of benthic forming the deep sound scattering hard and soft substrates of the ridge and benthopelagic fauna and the effects layer (e.g., larval, juvenile, and small and seamounts. Also, sediment layers of summit vs. slope areas on the pelagic pelagic crustaceans, fishes, and cepha- sampled over the MAR for microbiol- communities. Each superstation consists lopods) as well as meso- and bathy- ogy screening will allow meiofauna to of several stations where different sam- pelagic fishes and cephalopods occur- be opportunistically addressed. pling gear is operated to record the range ring over the ridge and seamount of biota and environments. Second, summits. It also includes large preda- Sampling Strategy and Technology surveys targeted particular sectors of tors such as tuna, elasmobranchs, sea- Sampling was planned with two kinds St. Peter and St. Paul’s Rocks, Rio Grande birds, and marine mammals that may of surveys. First, large-scale surveys Rise, and Walvis Ridge. These surveys visit the epipelagic layers in the vicin- were conducted along the ridge axis and address seamount biodiversity as well as ity of the MAR and seamount ridges. adjacent structures following the model current resource management questions. • Demersal Nekton: Defined by the used by the MAR-ECO project in the For example, benthic community struc- mobile megafauna, mostly bentho­ North Atlantic (Wenneck et al., 2008). In ture in relation to seafloor morphology pelagic fishes and cephalopods, that these surveys, previously defined “super- and mineral composition is a specific inhabit the Benthic Boundary Layer. stations” were placed within the target issue in the Rio Grande Rise sector due

Table 2. Summary of the South Atlantic MAR-ECO target areas

Lat/ Surface Oceanographic Target Area Geological Features Biodiversity Knowledge Human Threats Long Regime

South Equatorial Current Mostly epipelagic and St. Peter and Ridge crests and trenches; pelagic system and sea- Mining interest 3°N–3°S associated with the islet St. Paul’s Sector St. Peter and sonal primary production (polymetallic sulfides and 26°–32°W coasts; Deep benthic areas (SPSPS) St. Paul’s islets cycles of the eastern equa- cobalt crusts) unsampled torial Atlantic Ocean South Equatorial Current Mostly epipelagic and South Equatorial pelagic system and sea- associated with the coast Mining interest 2°N–10°S Ridge; MAR Sector sonal primary production of Ascension Island; (polymetallic sulfides and 12°–22°W Ascension Island (SEMS) cycles of the eastern equa- Some deep benthic cobalt crusts) torial Atlantic Ocean sampling Tropical South Atlantic 17°–25°S Some deep benthic Mining interest MAR Sector Ridge Subtropical Gyre; 10°–20°W sampling (cobalt crusts) (TMS) Oligotrophic waters Ridge; Mostly epipelagic and Subtropical Point of convergence Subtropical Convergence associated with the coast Convergence 36°–43°S with Walvis Ridge and system extending into of Tristan da Cunha group Fished area MAR Sector 9°–18°W Rio Grande Rise; sub-Antarctic zone; and Gough Islands; (mostly spiny lobster) (SCMS) Tristan da Cunha group, Highly productive waters Some deep benthic and Gough Islands sampling Fished area Rio Grande Rise 28°–36°S Seamounts South Atlantic Some benthic and (mostly alfonsinos); Sector 28°–39°W (guyots) Subtropical Gyre benthopelagic sampling Mining interest (RGRS) (cobalt crusts) South Atlantic Subtropical Gyre; Fished area Walvis 20°–33°S Seamount chain Bounded by productive Some benthic and (mostly orange roughy, Ridge Sector 5°W–10°E (some are guyots) waters of the Benguela benthopelagic sampling toothfish, (WRS) Current System and the deepwater crabs) Subtropical Convergence

Oceanography | December 2012 25 to Brazil’s interest in mineral explora- Sampling Platforms and New Zealand embarked in Gran tion and the environmental assessments A detailed and comprehensive survey Canaria Island (Spain) and ended field recommended by the ISA. Similarly, the of a wide range of biota in such a com- work in Cape Town (South Africa) description of benthic and benthopelagic plex and remote environment neces- after 34 days at sea (from October 25 to community structure is a requirement sarily requires sophisticated, multitask November 29, 2009). for the definition of vulnerable marine research vessels capable of enduring long ecosystems (e.g., FAO, 2009), critical journeys in the open sea and preferably Methods for the development of environmentally with advanced technology to operate Sampling was planned along the vessel’s sound fisheries management by the precise and safe sampling procedures original route through the South Atlantic SEAFO convention on the Walvis Ridge (e.g., dynamic positioning, multibeam Ocean during a nine-day work period. seamounts. By designing sampling strat- sonars). Research vessels operating Sampling design was based on the overall egies to combine fundamental scientific under the flag of South Atlantic coastal plan described above. Ten “superstations” objectives with those of resource use and countries seldom have these features and combining sampling procedures for conservation initiatives, a wider funding are mostly designed or equipped to oper- microbiology, zooplankton, pelagic nek- base might become available to enable ate near continental margins. Therefore, ton, and macrobenthos were distributed greater sampling opportunities. important options for the SA MAR-ECO along the ship’s track in order to cover The use of modern tools to observe initiative include: (a) research vessels the largest number of defined target sec- life in the ocean has been central to from non-South Atlantic countries tors (Figure 1). Four superstations were MAR-ECO, CenSeam, and other field that can operate in the region, and located within SEMS, two at the north- projects within the umbrella of the CoML (b) research vessels that operate in other ern and two at the southern extremes. (Boyle, 2009; Snelgrove, 2010). In par- oceans but could provide sampling time Two superstations were placed at the ticular, the combination of acoustic and along their routes (vessels of opportu- TMS and four over the WRS. In each optical instruments with capture gear nity). Because the Southern Ocean is the sector, superstations were organized to has increased the range of information target of concentrated research activity cover 1,000–2,000 m and 2,000–3,000 m extracted from deepwater organisms and by several countries during the austral depth strata (Table S2). There were also their dynamic distribution and habitats, summer months, a range of research extra stations in intermediate areas and and allowed researchers to reach, in a vessels transit through the central South continuous observations of marine mam- noninvasive way, areas formerly inacces- Atlantic. The first field expedition in mal and Sound Scattering Layer (SSL) sible to conventional samplers (e.g., nets). 2009 arose from such an opportunity. acoustic records. Table S1 presents the array of available Because this was an opportunistic technology used for measuring physical, The R/V Akademik Ioffe survey, sampling was determined by chemical, and biological properties of Expedition to the the gear and methodology adopted by deep-sea habitats as well as for sampling Southern MAR the Shirshov Institute science team, the deep pelagic, benthopelagic, and benthic The first opportunity to sample the operational capabilities of the vessel, and biota. These technologies have permit- southern MAR under the framework logistic limitations of the non-Russian ted comprehensive analyses of diversity of the SA MAR-ECO project came science team. Micronekton was sampled patterns associated with ridge habitats in about through a consortium estab- with a 6 m² opening and 25 m long the North Atlantic Ocean (see Bergstad lished between MAR-ECO and the Isaacs-Kidd Midwater Trawl (IKMT), as et al., 2008, and Vecchione et al., 2010, for P.P. Shirshov Institute of Oceanology modified by Samyshev-Aseev (Figure 3). reviews). Together with similar and com- (Russian Academy of Sciences). Planktonic and micronektonic organ- plementary approaches developed for A multihabitat sampling plan was isms were collected in stepped oblique seamount ecological studies by CenSeam adapted to the twenty-ninth annual tows. Trawl duration at each step was (Consalvey et al., 2010; Clark et al. 2012), voyage of R/V Akademik Ioffe to the 5–10 minutes, while the vertical dis- they define survey parameters to be repli- Antarctic Continent. MAR-ECO sci- tance between neighboring steps was cated in the southern MAR. entists from Russia, Brazil, Uruguay, 25–200 m. At each superstation, two

26 Oceanography | Vol. 25, No. 4 IKMT tows were conducted consecu- tively, one at depths as close as possible b to the ridge and another down to the a lower depth of the SSL (Kobylianski et al., 2010). The same procedure was repeated at six extra stations placed in intermediate areas along the ship’s track. Macrobenthos was sampled with 2.5 m and 1.5 m wide Sigsbee Trawls (Figure 3). Bottom contact was determined with c the winch tension meter, or, in some Figure 3. South Atlantic cases, with a Benthos acoustic pinger MAR-ECO cruise, October– November 2009. (a) Isaac-Kidd attached to the wire ~ 300 m from the Midwater Trawl. (b) Sigsbee trawl. Trawls were conducted in a drift- Trawl. (c) Benthic catch at ing regime; the Aquamaster 360° thruster the Romanche Fracture Zone. Photos: André Barreto was used when needed. Tow distance varied depending on depth and trawl- ing conditions from 0.5 to 2 nm (0.92 to 3.7 km). All trawls were conducted after an initial acoustic survey of the topog- raphy with a single-beam echosounder. Microbiology samples were collected from the water column in Niskin bottles oligotrophic subtropical gyre, and the made on the northern and southern set on a rosette array and also from the border of the subtropical convergence, base of the seamount between 4,120 and sediment collected by benthic trawls and respectively (Figure 4). The seafloor was 4,703 m depths. The latter, particularly, piston corers. Conductivity-temperature- typically gently sloping and sediment included part of the Cape Abyssal Plain, depth (CTD) data were obtained in covered on the summit (893 m) and which is covered by high concentra- four 0–2,000 m casts in the vicinity of northern slope (1,360 m) regions of the tions of ferromanganese nodules—over the superstations. Surface temperature Romanche Fracture Zone where the first a metric ton of these nodules were and chlorophyll distribution during the two benthic trawls were conducted. Two caught in one trawl. survey were extracted from the SeaWiFS subsequent trawls were made on the In total, 63 samples were obtained Satellite database (available at http:// ridge south of the Romanche Fracture during the trip: 12 macrobenthos, oceancolor.gsf.nasa.gov; Figure 4). Zone (~ 3,080 m and ~ 1,875 m), where 26 micronekton, 19 plankton, and the seafloor was rough and covered with 15 microbiology (Table S2). Preliminary Preliminary Results volcanic fragments, including ferro- identification was conducted onboard The cruise track was mostly between manganese crusts. The same seafloor and included 175 species of fish the ITCZ and the subtropical highs composition characterized the TMS (~ 5,700 specimens), 50 species of (~ 30°S). Permanent thermoclines ridge area sampled, where a 3,800 m cephalopods (~ 262 specimens), and were 700–1,000 m deep, and surface deep trawl was conducted south of a at least 192 benthic invertebrate spe- thermoclines (~ 30–40 m deep) were transform fault. Walvis Ridge sampling cies (~ 1,980 specimens). Kobyliansky present in the profiles from the equato- was conducted on a large guyot rising et al. (2010) presented a complete list rial area. SEMS, TMS, and WRS super- ~ 4,000 m from the seafloor and oriented of fish species, and Table S3 provides stations were influenced by different in a north–south direction. Three trawls a provisional list of the remaining oceanographic regimes: the seasonal were conducted on the flat summit taxa. The latter was summarized from eastern equatorial bloom (ETRA), the (997–1,401 m deep), and two trawls were a total of 1,120 records submitted to

Oceanography | December 2012 27 the Ocean Biogeographic Information MAR sectors, respectively, suggesting Eight species of this genus are described System (OBIS; http://www.iobis.org) potential influence of surface biological worldwide, all of them living on deep in 2011. Species numbers will certainly productivity in meso- and bathypelagic coralline habitats of the Southern increase, as a large number of specimens, communities over the ridge (Figure 4). Hemisphere (Cardoso and Fransen, particularly of the macrozooplankton, This influence seems to have also 2012). In addition, three deep-sea hermit are yet to be examined by taxonomic affected cephalopod and benthic inver- crabs of the genus Parapagurus were specialists. There were 23 sightings of tebrate catches (recent work of author reported (Cardoso and Lemaitre, 2012): cetaceans along the MAR and Walvis Perez and colleagues). Gordeeva (2011) P. abyssorum and P. pilosimanus were Ridge, with seven species positively iden- found intraspecific genetic structure in caught at the base (3721 m) and summit tified. Nearly 300 bacteria were isolated four species of mesopelagic lanternfish (997 m) of a seamount on the Walvis from deep sediment and water samples, (Myctophidae) and suggested that some Ridge (Figure 4), and P. nu du s was 50 of them showing potential for widely distributed species may be locally caught south of the Romanche Fracture biotechnological use (Odisi et al., 2012). isolated. This could result from circula- Zone (2,014–3,342 m). Known from The first published study derived tion patterns locally induced by sea- North Atlantic deep areas, P. abyssorum from the cruise addressed meso- and mounts and ridges. and P. nu du s were reported from this bathypelagic fish collected by the IKMT Studies conducted on the benthic cruise for the first time on the South trawls. Kobyliansky et al. (2010) showed crustaceans revealed one new species of Atlantic MAR; P. pilosimanus was pre- that mesopelagic fish assemblages dif- caridean shrimp Leontocaris smarensis viously reported for both the North fered geographically in accordance (Cardoso and Fransen, 2012; see photo a and South Atlantic. These three spe- with oceanographic regimes of the on page 16) collected on the Romanche cies were found living with anthozoans South Atlantic. However, in the lower Fracture Zone (902 m depth) in asso- (Actiniaria) in gastropod shells and in mesopelagic and bathypelagic layers, ciation with live stony (Enallopsammia large colonies of Epizoanthus sp. (see assemblages were more geographi- rostrata and Corallium cf. bayeri) and soft photo c on page 16). cally homogeneous. Highest and lowest (Narella alvinae) corals (Débora Pires, diversity (and abundance) occurred in National Museum, Federal University of Concluding Remarks the south equatorial MAR and tropical Rio de Janeiro, pers. comm., July 2010). The Census of Marine Life program attempted to describe the known and unknown biodiversity and life patterns in the deep ocean. A large (and difficult Figure 4. Chlorophyll a to predict) number of species remain concentration to be found and described, especially in (mg m–3) during South Atlantic MAR- poorly sampled parts of the world ocean ECO Cruise #1_2009 (McIntyre, 2010). It is clear that deep-sea (November 26–20, communities are neither isolated nor 2009). Numbers repre- sent superstation posi- static, but dynamically connected over a tions. Crosses represent range of spatial scales through dispersal extra-station positions. processes and dynamic interactions with Images from SeaWiFS Satellite database avail- the pelagic ecosystem (Snelgrove, 2010). able at http://oceancolor. The rough morphological and topo- gsf.nasa.gov graphic features in the South Atlantic Ocean determine deepwater circulation patterns that connect it to the North Atlantic, Southern, Indian, and Pacific Oceans. We know that surface biologi- cal production patterns differ on both

28 Oceanography | Vol. 25, No. 4 north-south and east-west sides of the Fonseca for supporting the develop- Berger, W.H. 1989. Global maps of oceanic produc- tivity. Pp. 429–455 in Productivity of the Ocean: southern MAR, but abundance and dis- ment of this project beyond the CoML. Present and Past. W.H. Berger, V.S. Smetacek, and tribution patterns of the deep-sea fauna Thanks also to the master and the crew G. Wefer, eds, Dahlem Workshop Reports, Life Sciences Research Report 44, Wiley, Chichester. are largely unknown. The South Atlantic of R/V Akademik Ioffe for great help and Bergstad, O.A., and O.R. Godø. 2003. The pilot proj- MAR-ECO project has been conceived to support onboard during the 29th Cruise ect “patterns and processes of the ecosystems of the northern Mid-Atlantic”: Aims, strategy and address these important unknowns. The (2009). The senior author is supported status. Oceanologica Acta 25:219–226, http:// CoML MAR-ECO and CenSeam proj- by a National Council for Scientific and dx.doi.org/10.1016/S0399-1784(02)01203-3. Bergstad, O.A., T. Falkenhaug, O.S. Astthorsson, ects have posed a set of principal ques- Technological Development (CNPq) I. Byrkjedal, A.V. Gebruk, U. Piatkowsky, tions and set high standards for optimal research grant (Process 309837/2010-3). I.G. Priede, R.S. Santos, M. Vecchione, P. Lorance, and J.M.D. Gordon. 2008. Towards sampling strategies and technologies improved understanding of the diversity and to be used for investigating seamounts Supplemental Tables abundance patterns of the mid-ocean ridge macro- and megafauna. Deep Sea Research and ridges. Preliminary sampling by The supplemental tables for this Part II 55:1–5, http://dx.doi.org/10.1016/​ R/V Akademik Ioffe (P.P. Shirshov article (Tables S1–S3) are available at j.dsr2.2007.10.001. Bickert, T., and A. MacKensen. 2003. Last gla- Institute of Oceanology, Russian http://www.tos.org/oceanography/ cial Holocene changes in South Atlantic deep Academy of Sciences) in November 2009 archive/25-4_perez_supp.pdf. water circulation. Pp. 671–695 in The South Atlantic in the Late Quaternary: Reconstruction highlighted constraints, including long of Material, Budgets and Current Systems. distances, deep and rough topography, References G. Wefer, S. Mulitza, and V. Ratmeyer, eds, Springer-Verlag, Berlin. time, and technology, that limit sam- Agassiz, A. 1881. Report on the Echinoidea dredge by H.M.S. Challenger during the years 1873– Boyle, P.R. 2009. Life in the Mid-Atlantic. Bergen pling the southern Mid-Atlantic Ridge. 1876. Report of Scientific Results of the Voyage Museum Press, 244 pp. Busk, G. 1886. Report on the Polyzoa collected by However, the overwhelming number of H.M.S. Challenger During the Years 1873–76: Zoology Part IX, 321 pp. H.M.S. 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