Lanternfish ( Myctophidae ) from eastern Brazil , southwest Atlantic Ocean

Twenty-nine species from 11 genera of Myctophidae were taken in daytime midwater and bottom trawl hauls off eastern Brazil (11-22S). Trawls were performed aboard the French R/V Thalassa to depths from 19 to 2271 m, including samples from shelf, slope and in the vicinity of oceanic banks and seamounts. Diaphus garmani was the most abundant species, accounting for 84% of all identified individuals and with four other species (D. dumerilii, D. brachycephalus, D. perspicillatus and Myctophum obtusirostre) accounted for >95% of all myctophids caught. Regarding longitudinal distribution patterns, 16 species are broadly tropical, seven tropical, three subtropical, two temperate and one amphi-Atlantic. For the most abundant and frequent species, highest abundances were associated mainly with cold waters, either South Atlantic Central Water or Antarctic Intermediate Water. Non-metric multidimensional scaling based on species presence-absence in the samples and oceanographic conditions was used to identify spatial distribution of myctophid assemblages. Three assemblages were identified in the studied area: north of Abrolhos Bank, south of Abrolhos Bank, and seamounts.


INTRODUCTION
Myctophids are typically pelagic fish of the open ocean (Hartel & Craddock, 2002) and, together with members of Sternoptychidae, Gonostomatidae, Chauliodontidae and the suborder Stomiatoidei, represent the characteristic families in mesopelagic depths (Haedrich, 1997).Among these, Myctophidae is the dominant family (Nafpaktitis et al., 1977) and the most speciose, including almost 250 species referred to as lanternfish due to a variety of luminous organs, among which photophores are the most characteristic (Nelson, 2006).Lanternfish range from arctic to antarctic waters, and from the surface at night to depths exceeding 2000 m (Nafpaktitis et al., 1977).The family also includes species known as pseudoceanic, associated with continental shelf and slope regions and in the neighbourhood of oceanic islands (Hulley, 1981).Continental slopes are particularly important due to the topographic and hydrographic gradients, and are considered areas of dynamic tension (Merrett & Haedrich, 1997).Continental slopes also encompass a wider set of physical niches, and provide an environment for the development of a recognizable and trophicallydependent community of benthic and benthopelagic fish (Haedrich et al., 1980).Down-slope zonation of lanternfish may result from the combined effects of depth and water column structure (Hulley, 1992).
The present study provides knowledge about southwestern Atlantic lanternfish, including samples from Vitória-Trindade chain, an area understudied (Clark et al., 2010), adjacent to a transition zone between tropical Atlantic and temperate South America biota.We report the occurrence and distribution of lanternfish in relation to oceanographic conditions and attempt to examine whether species associations are spatially different.

Study area
The eastern coast of Brazil is a typical oligotrophic system (Gaeta et al., 1999), and the most important oceanic surface feature is the southward flowing Brazil Current (BC: 22-27 o C, 36.5-37.0psu), the warm western boundary current of the subtropical gyre (Silveira et al., 2001).The continental shelf of the study area (11-22ºS) extends for only 8 km off Salvador (França, 1979) and widens to the south to form the Royal Charlotte Bank (RCB, 16 o S) and the Abrolhos Bank (AB, 18 o S).The Vitória-Trindade chain that extends along 20.5ºS comprises seamounts that have shallow summits at depths of 34-76 m (Miloslavich et al., 2011).These topographic barriers produce a complex hydrographic structure including vortices, upwellings and vertical mixing processes, which alter the oligotrophic condition mainly south of AB (Ciotti et al., 2007;Valentin et al., 2007).The subsurface layer beneath the BC is occupied by the cold and nutrient-rich South Atlantic Central Water (SACW: 6.0-18.5 o C, 34.5-36.0psu) flowing north, between 400-700 m (Schmid et al., 1995).Periodic upwelling of SACW beyond the deep thermocline (80-120 m) enhances primary production (Nonaka et al., 2000).In the subthermocline region there are three major water masses, Antarctic Intermediate Water (AAIW) near 800-900 m, North Atlantic Deep Water (NADW) centered at about 2500 m, and Antarctic Bottom Water (AABW) below about 3500 m (Hogg & Owens, 1999).

Biological sampling
The studied material was obtained with midwater and demersal trawls, both performed only during the day, on the continental shelf, continental slope and near oceanic banks and seamounts off eastern Brazil (Fig. 1).During the midwater cruise, the collections were obtained using a large midwater net (292 m circumference and 191 m long).During operations, maximum horizontal and vertical opening was 56 and 25 m, respectively.Mesh sizes were 8000 mm in the wings and 20 mm in the cod-end.A total of 62 pelagic midwater trawls were towed at depths from 19 to 910 m, among which 50 had myctophid catches (n = 28,645).Hauls were undertaken on acoustically detected fish aggregations.
During the demersal cruise, the individuals were obtained using a bottom-trawl net with a 26.8 m head rope and 47.2-m foot rope, equipped with 40 rubber bobbins (rockhoppers) attached to the foot-rope.Mesh sizes were 110 mm for the wings and 20 mm for the cod-end.During the fishing operations, the horizontal and vertical mouth openings ranged between 28.0 and 45.5 m and from 3.0 to 10.6 m, respectively.
Demersal trawls were decided based on the availability of trawlable bottoms.A total of 58 stations yielded more than 45,000 specimens, from which 2,720 specimens of myctophids were recorded in 47 stations, ranging in depth from 100 to 2,271 m.On both cruises, trawl depth was acoustically controled using SCANMAR system, which was also used to access trawl geometry, including the horizontal opening and distance from net to bottom.The vertical opening and its distance in relation to the bottom was controled by the Ossian Trawl-Eye 49 KHz transducer fixed in the headrope.These systems allowed maintaining the net operating at specific depths during fishing and further classify the stations into different depth strata.

Water mass distribution in the study area
Temperature and salinity profiles (n = 116) recorded during the midwater cruise were used to analyse the horizontal distribution of temperature contours at the 200 m isobath (e.g., beginning of the mesopelagic zone), throughout the studied area (11-22 o S).Water masses distribution was inferred from a T-S diagram using data compiled from the National Oceanographic Data Centre (Brazilian Navy), including CTD profiles down to 5,000 m.These data was sorted from the same geographic area and period (May-July) and processed using Ocean Data View (ODV) software.

Distribution
The distribution of myctophid assemblages was analysed with non-metric multidimensional scaling (Clarke & Warwick, 2001) using the Sorensen similarity index calculated with species presenceabsence in the samples.The final matrix used in the ordination was composed by 29 species and 53 samples (9 midwater and 44 demersal trawls).Stations with only one species (n = 11) were excluded from the matrix.A non-quantitative index was chosen due to differences in net sizes and sampling strategies between midwater and demersal fishing.

Water mass distribution in the study area
The thermal structure of the water column during the two cruises, both during winter, was similar.The water temperature ranged from 24-28ºC at surface, 20-24ºC at 100 m depth, 15.7-16.1ºCat 200 m, 8-9.5ºC at 500 m, and was always <3ºC beyond 1,000 m depth.Tropical Water (TW) from BC (T > 20 o C; S > 36.2 psu) was present at surface (29-68 m), and the subtropical SACW with lower temperatures (6-18.5 o C) and salinities (34.6-36.0psu) occuppied the subsurface layer (118-624 m) (Fig. 2).
The horizontal distribution of the water temperature at 200 m (Fig. 3) showed that this depth was occuppied by SACW throughout the studied area, with an east-west gradient of decreasing temperatures.The lowest temperatures (14-15ºC) were identified between 13-15 o S off Salvador, and near RCB, AB and the Vitória Channel, reflecting the upwelling of SACW as a result of BC meandering along the shelf edge and seamounts.
The number of species/trawl ranged from 1-13 (Fig. 5), but captures of more than 5 species/trawl were more frequent in demersal trawls (21%) than in midwater trawls (17%).The maximum number of species per trawl (13) was similar in demersal and midwater trawls.Midwater trawls near seamounts south of Abrolhos Bank yielded the highest number of species (Vitória: 13 spp.;Davis: 7 spp.).Demersal trawls that yielded the highest number of species occurred at the southernmost part of the area at 624.5 m (13 spp.) and at 2,126 m off Salvador (10 spp.).Nine trawls yielded 6-9 species trawl -1 .Among these, six were performed between 13-14ºS at depths from 522 to 1,929 m, and three were performed between 19-20ºS at depths from 895 to 1,649 m.

Species data
From a total of 31,365 myctophids examined, all but 278 (0.9%) were identifiable to species.Table 2 lists the species grouped according to abundance, along with their totals and frequency of occurrence in midwater and demersal trawls, depth of occurrence and size range.The identified material comprised 11 genera and 29 species.The top five most abundant species comprised approximately 95% of the total number of individuals.Only one species was extremely abundant, 4 were abundant, 5 were common, 8 were uncommon and 11 were rare.Diaphus dumerilii was the most frequent species, both in demersal (62%) and midwater (66%) trawls.The majority of species (79%) had broadly tropical and tropical affinities (as indicated by Hulley, 1981), while species with subtropical and temperate affinities were poorly represented and occurred in very low numbers (1-17 ind).
Although NAB and SAB did not significantly differ (P = 0.255), a change in dominance was evident when mean densities (ind h -1 ) of the nine most abundant and frequent species in midwater trawls were compared (Fig. 7).Diaphus garmani and D. dumerilii were caught throughout the area, though mostly abundant at RCB and Minerva seamount.M. obtusirostre occurred associated to the four seamounts sampled (Minerva, Hotspur, Vitória, and Davis).At Vitória seamount, except for D. garmani, the eight remaining species occurred together in catches, with yields that ranged from 4.2 to 110.2 ind h -1 .A monospecific school of D. brachycephalus caught at 15ºS yielded 1,115 ind h -1 .

DISCUSSION
In this study, myctophids were more frequent in demersal than in midwater trawls, possibly as a result of our exclusive daytime sampling, since under the normal diel vertical migration pattern these fishes hide from visual predators at depth during the day and forage on abundant plankton in upper waters at night (Pearre, 2003).Also, a number of specimens could have been caught during retrieval and/or deployment of the bottom trawl (the nets used were devoid of open/close mechanisms) and, for this reason, fish density estimates were not compared between midwater and demersal trawls.Moreover, the presence of myctophids in demersal trawls could represent the adoption of an adult benthopelagic life strategy, as indicated by Vinnichenko (1997).Gartner et al. (2008) suggested that persistent high-density near-bottom aggregations (NBAs) are a normal part of the life history of several species traditionally considered to be mesopelagic.These NBAs would enhance the probability of feeding success, as fishes could explore  food supplies in a two dimensional search area (i.e., near bottom).
Among the 29 myctophid species captured in this study, tropical and broad tropical distribution patterns dominated.Species with temperate and subtropical affinities were restricted to hauls that sampled depths below 700 m, which is the upper limit of AAIW in the area (Hogg & Owens, 1999).Although this number is Table 2. Lanternfish catch in midwater and demersal trawls off eastern Brazil (frequency in parentheses).Tropical: distributed only in tropical waters, Subtropical: distributed between 20 o and 35 o in the western South Atlantic, Broadly Tropical: distributed in both tropical and subtropical waters, Amphi-Atlantic: restricted to warm subtropical waters.Biogeographical definitions according to Hulley (1981).lower than that recorded off southeastern and southern Brazil between 22-34ºS (41 species: Figueiredo et al., 2002;Bernardes et al., 2005), if larval occurrence is considered (Bonecker & Castro, 2006), ten more species could be added (Benthosema suborbitale, Centrobranchus nigroocelattus, Diaphus anderseni, Diogenichthys atlanticus, Hygophum macrochir, Hygophum taaningi, Lampanyctus nobilis, Lepidophanes gaussi, Nannobrachium cuprarium, Notolychnus valdiviae) and the numbers be similar.All myctophids spend their larval stages in the productive epipelagic zone (Sassa et al., 2004), moving to the mesopelagic zone after reaching the juvenile stage (Clarke, 1973).
A tendency of increasing species number with depth was observed, and since temperature correlates to lanternfish distribution (Brandt, 1983), this result could be associated with the marked thermal structure of the water column.During hauls that sampled depths higher than 1,500 m between 11º-22ºS, the net was towed through four waters masses (BC, SACW, AAIW, NADW), possibly increasing the probability of catching a higher number of species.Hulley (1992) also observed an increase in lanternfish species richness and in the complexity of the distributions across the slope, possibly as the result of a higher structuring of the water column.
The presence of a variety of reliefs between 11-22ºS adds topographic complexity, causing islandinduced disturbance, in which upwelled nutrients promote primary and secondary production in the island wake (Bonecker et al., 1992(Bonecker et al., , 1993) ) and probably act to affect the distribution of the mesopelagic fauna.Our hydrographic results showed the occurrence of SACW at 200 m between 13-15ºS, and near RCB, AB and the Vitória Channel; this possibly reflects the permanent cyclonic eddy that Schmid et al. (1995) detected to be formed south of the AB from the meandering movement of the BC after passing through the Vitória Channel.The spatial distribution of the SACW in the area studied seems to explain the distribution of the more speciose trawls and, for some species, the highest densities associated with seamounts and banks.
While D. dumerilii was the most frequent and second most abundant species in our study, it was dominant between 22-34ºS (47%; Figueiredo et al., 2002) and seemed to be important in the trophic relation on the slope, once it was found in the stomach contents of several demersal bony fish of STC ecosystem (Haimovici et al., 1994).Near RCB this species was most abundant in rather shallow depths (25-34 m), indicating a certain degree of land association, as it was observed by Wienerroither et al. (2009).Diaphus dumerilii dominated both the water column (deep scattering layer) and the bottom (NBAs) on deep coral banks off Cape Lookout middle slope, North Carolina (Gartner et al., 2008).
The occurrence of mesopelagic species in shallow waters is ascribed to the abrupt depth changeover around islands of volcanic origin (Uiblein & Bordes, 1999), and the direct interaction between pelagic and demersal organisms at the interfaces between submerged bottom features establishes and important link between epipelagic waters and the deep benthos (Marshall & Merrett, 1977).Lanternfish may be an important prey item for large pelagic species, abundant in longline catches from Vitória-Trindade seamounts (Olavo et al., 2005).Future research in the area should address the study of oceanic food webs.crew of the R/V Thalassa for their collaboration.Special thanks are given to the Chief Scientists and coordinators of the Brazilian cruises aboard R/V Thalassa, for the facilitation of logistics and successful integration of the multidisciplinary teams during cruises Bahia-1 and Bahia-2.Two anonymous reviewers made numerous comments to improve the manuscript.

Figure 1 .
Figure 1.Study area and location of the sampling stations.

Figure 2 .
Figure 2. Water masses recorded in the present study, according to depth.TW: Tropical Water, SACW: South Atlantic Central Water, AAIW: Antartic Intermediate Water, NADW: North Atlantic Deep Water, AABW: Antartic Bottom Water.

Figure 3 .
Figure 3. Distribution of temperature contours at 200 m isobath in the study area.

Table 1 .
Number of stations, depth range, effort and characteristics of nets used in midwater and demersal sampling off eastern Brazil and details of myctophids catch.