Everton Giachini Tosetto
email: evertontosetto@hotmail.com

Barbara Barkokébas Silva

Xiomara Franchesca

García Díaz

Sigrid Neumann-Leitão

Arnaud Bertrand

E Giachini

E Giachini Tosetto

B Barkokébas

Thaliacean community responses to distinct thermohaline and circulation patterns in the Western Tropical South Atlantic Ocean

Keywords: Pyrosoma atlanticum, Soestia zonaria, Doliolida, North Brazilian undercurrent, South Equatorial current, Gelatinous zooplankton

niveau recherche, publiés ou non, émanant des établissements d'enseignement et de recherche français ou étrangers, des laboratoires publics ou privés.

Introduction

Holoplanktonic organisms of the class Thaliacea (Chordata: Tunicata) have a global distribution and a rich biodiversity with variations in size, morphology and behaviour, reflecting adaptations to their wide range of habitats [START_REF] Harbison | Effects of temperature on the swimming of salps (Tunicata, Thaliacea): Implications for vertical migration1: Temperature effects on salps[END_REF][START_REF] Govindarajan | A molecular phylogeny of the Thaliacea[END_REF][START_REF] Lucas | Gelatinous zooplankton biomass in the global oceans: geographic variation and environmental drivers: Global gelatinous biomass[END_REF].

Abstract

In western boundary current systems, strong currents transport oligotrophic oceanic waters towards the coast. Thaliaceans may have an advantage in these systems due their ability to filter small particles such as the bacterioplankton, typically responsible for the primary production in oligotrophic waters. Here, we evaluated the structure of the thaliacean community present in the tropical South Atlantic Ocean western boundary current system to test the 1 Although some species are restricted to polar regions, the greatest diversity and biomass of thaliaceans is found in tropical and sub-tropical waters [START_REF] Van Soest | Zoogeography and speciation in the Salpidae[END_REF][START_REF] Lucas | Gelatinous zooplankton biomass in the global oceans: geographic variation and environmental drivers: Global gelatinous biomass[END_REF]. Many of these tropical systems are oligotrophic, with primary production typically dominated by bacterioplankton [START_REF] Hagström | Microbial loop in an oligotrophic pelagic marine ecosystem: Possible roles of cyanobacteria and nanoflagellates in the organic fluxes[END_REF][START_REF] Zubkov | High rate of uptake of organic nitrogen compounds by prochlorococcus cyanobacteria as a key to their dominance in oligotrophic oceanic waters[END_REF]. Thaliaceans are efficient filter-feeders, their characteristic barrel-shape body with circular musculature allows them to swim and simultaneously filter pico-and nanoparticles as small as 0.2 µm such as bacteria [START_REF] Piette | Thaliaceans, the neglected pelagic relatives of ascidians: A developmental and evolutionary enigma[END_REF][START_REF] Dölger | Dense dwarfs versus gelatinous giants: The trade-offs and physiological limits determining the body plan of planktonic filter feeders[END_REF]. Thanks to this strategy, they flourish and remove a large portion of primary production from the environment even in oligotrophic systems, particularly in tropical western boundary systems [START_REF] Stone | Salp contributions to vertical carbon flux in the Sargasso Sea[END_REF].

Under specific conditions, such as high temperatures and phytoplankton productivity, upwelling events and/or specific water mass intrusions, the high rates of asexual reproduction of thaliacieans, producing aggregated zooids, allows rapid population growth and occasional blooms [START_REF] Deibel | Laboratory determined mortality, fecundity and growth rates of Thalia democratica Forskal and Dolioletta gegenbauri Uljanin (Tunicata, Thaliacea)[END_REF][START_REF] Gibson | Feeding and growth rates of the doliolid, Dolioletta gegenbauri Uljanin (Tunicata, Thaliacea)[END_REF][START_REF] Henschke | Large vertical migrations of Pyrosoma atlanticum play an important role in active carbon transport[END_REF]. These large aggregations or swarms can compete and overlap other typically more abundant planktonic feeders such as copepods, changing the structure of marine food webs [START_REF] Harbison | The feeding rates of the pelagic tunicate Pegea confederata and two other salps1: Salp feeding rates[END_REF]. Historically, due to the high water content in their tissues and low caloric value, thaliaceans and other gelatinous organisms were considered irrelevant and even dead-ends in marine trophic networks. However, this concept has changed in recent decades as it has been observed that these organism are key components in the diet of groups such as crustaceans, fish and turtles [START_REF] Henschke | Rethinking the role of Salps in the Ocean[END_REF][START_REF] Hetherington | Re-examining trophic dead ends: Stable isotope values link gelatinous zooplankton to leatherback turtles in the California Current[END_REF]. Although their energetic content is indeed lower than other zooplankton organisms, due to their slow motion, predators expend less energy in the capture process making them an efficient food source [START_REF] Henschke | Rethinking the role of Salps in the Ocean[END_REF][START_REF] Hetherington | Re-examining trophic dead ends: Stable isotope values link gelatinous zooplankton to leatherback turtles in the California Current[END_REF]. Additionally, due the combination of the efficient filter-feeding lifestyle and eventual large population blooms, thaliaceans are able to transform small particles they feed, into large faecal pellets, which quickly sink, as well as their carcass after death, promoting an important carbon input to the deep ocean [START_REF] Iseki | Particulate organic matter transport to the deep sea by salp fecal pellets[END_REF][START_REF] Henschke | Rethinking the role of Salps in the Ocean[END_REF][START_REF] Köster | How efficiently can doliolids (Tunicata, Thaliacea) utilize phytoplankton and their own fecal pellets?[END_REF].

In the Western Tropical South Atlantic, the southern South Equatorial Current (sSEC) reaches the continental slope around 10-20°S and bifurcates into two branches. The northern one feeds the strong North Brazil Undercurrent (NBUC), which flows northward along the Brazilian coast [START_REF] Dossa | Near-surface western boundary circulation off Northeast Brazil[END_REF]. Meanwhile, the central South Equatorial Current (cSEC) transposes the Fernando de Noronha Ridge (FNR), composed by a series of islands and seamounts around 5°S, encountering the NBUC when reaching the Brazilian coast [START_REF] Dossa | Near-surface western boundary circulation off Northeast Brazil[END_REF]. Differences in the intensity and direction of these currents affect the thermohaline structure of the Western Tropical South Atlantic and two areas were previously identified [START_REF] Assunção | 3D characterisation of the thermohaline structure in the southwestern tropical Atlantic derived from functional data analysis of in situ profiles[END_REF]: (i) area 1, along the continental slope and under the influence of NBUC, presenting thicker thermocline and weaker stratification, hereafter called Western Boundary Current System (WBCS); and (ii) area 2, offshore in the region of FNR under the influence of cSEC, with high stratification, hereafter called central South Equatorial Current system (SECS). Although nutrient-rich estuarine plumes and uplift may enhance primary production in western boundary systems, continental drainage is low in the Western Tropical South Atlantic, not reaching beyond 16 km offshore, and uplift events due anticyclonic eddies occurring near the shelf break are sporadic [START_REF] Smith | Phytoplankton biomass and productivity in the Amazon River plume: Correlation with seasonal river discharge[END_REF][START_REF] Castro | Multidisciplinary oceanographic processes on the Western Atlantic continental shelf between 4°N and 34°S[END_REF][START_REF] Dossa | Near-surface western boundary circulation off Northeast Brazil[END_REF]. Therefore, the region presents the lowest primary production along the Brazilian Coast [START_REF] Ekau | An introduction to the pelagic system of the Northeast and East Brazilian shelf[END_REF][START_REF] Castro | Multidisciplinary oceanographic processes on the Western Atlantic continental shelf between 4°N and 34°S[END_REF].

Although the particular characteristic of this system may benefit the thaliaceans filter-feeding behaviour on pico-and nanoparticles, knowledge on the species inhabiting the area is scarce [START_REF] De Carvalho | Tunicata, Thaliacea, Pyrosomatidae, Pyrosomella verticillata (Neumann[END_REF][START_REF] Díaz | New record of Thalia cicar van Soest 1973 (Urochordata: Thaliacea) in the Equatorial Atlantic[END_REF][START_REF] Neumann-Leitao | Diversity and distribution of the mesozooplankton in the tropical Southwestern Atlantic[END_REF] and no study evaluated the structure of the thaliacean community. Here, we evaluated the composition, spatial distribution (horizontal and vertical) and abundance of the thaliacean community (Pyrosomatidae, Salpidae and Doliolidae) of the Western Tropical South Atlantic according to the characteristics of the physical environment. In particular, we test the hypothesis according to which differences in the circulation and thermohaline patterns of the WBCS and SECS shape the structure of the thaliacean community in the region.

Materials and methods

Data were collected during the ABRACOS 2 survey (Bertrand, 2017) on board the French R/V Antea from 9 April to 6 May 2017 (rainy season) in the Western Tropical South Atlantic Ocean along the continental slope of Northeastern Brazil (5-9°S) and around the Fernando de Noronha Ridge (between 3°S, 37°W and 5°S, 31°W; Fig. 1). Fifty samples were collected in 32 stations at day and night using a micronekton mesopelagic trawl (body mesh: 40 mm, cod-end mesh: 10 mm) at depths ranging from the surface to 1170 m, selected according to the presence of sound scattering layers detected with an echosounder (organisms were also captured during net descent and ascent phases). The net was hauled at 2-3 knots during approximately 30 min once the targeted depth was reached. Additional samples were obtained with a finer mesh (body mesh: 30 mm, cod-end mesh: 4 mm) around Fernando de Noronha. Specimens collected in these samples were used to improve species composition, only. Thaliaceans were sorted from the entire trawl sample on board and fixed with 4% formaldehyde buffered with sodium tetraborate (0.5 g L -1 ).

At each station, vertical profiles of temperature (°C), salinity, pressure and fluorescence were obtained with a CTD-O2 profiler Seabird SBE911 + . Conductivity, temperature and pressure accuracies were estimated at 0.0003 S m -1 , 10 -3 °C and 0.7 dbar, respectively. Along-track current profiles were recorded with an 'Ocean Surveyor' ship-mounted acoustic Doppler current profiler (SADCP) operating at a frequency of 75 kHz with a depth range of 15-700 m. SADCP data were processed and edited using the Common Ocean Data Access System (CODAS) software package developed at the University of Hawaii (http:// curre nts. soest. hawaii. edu). The relative velocities were rotated from the transducer to the Earth reference frame using the ship gyrocompass. The global positioning system (GPS) was used to retrieve the absolute current velocities. The orientation of the transducer relative to the gyroscopic compass and the amplitude correction factor for the SADCP were determined by standard calibration procedures. Finally, velocity profiles were averaged hourly, providing profiles in the 19-600 m range. SADCP data located over the shelf (bathymetry shallower than 70 m) were often affected by spurious reflections on the bottom, so the data coverage was only partial in these shallow areas. To describe current patterns, data from the upper (0-70 m depth) and mesopelagic (70-350 m) layers were integrated and averaged each 0.1 square degree.

To estimate the abundance of organisms, the volume of water filtered by the net was estimated from the distance covered and the area of the net's mouth. In the laboratory, samples with more than 200 thaliaceans were fractionated. The organisms of each subsample were identified (mainly following [START_REF] Esnal | Pyrosomatida[END_REF]Esnal & Daponte, 1999a, 1999b) and counted. The type of zooid was identified by differentiating oozoids (asexual solitary zooids) and blastozooids (hermaphrodite aggregated zooids) based on the number and arrangement of the body muscle bands, the position and form of the digestive tract and the shape of the tunic [START_REF] Tavares | Occurrence of doliolios and salps during 1958, 1959, and 1960 off the São Paulo coast[END_REF]. For Doliolidade, only unidentified rigid transparent tunics were recorded. Abundances were standardized in number of individuals or colonies per 10 5 m -3 .

Laboratory analyses were performed at the Laboratório de Ecologia Aquática Tropical (LECAT-UFRA, Belém-Brazil) and Laboratorio de Zooplâncton of Museu de Oceanografia of Universidade Federal de Pernambuco (LABZOO-UFPE, Recife-Brazil). After laboratory analyses, samples and specimens were deposited at the Museu de Oceanografia of Universidade Federal de Pernambuco.

Data analysis

For data analysis, the 32 stations were aggregated according to [START_REF] Assunção | 3D characterisation of the thermohaline structure in the southwestern tropical Atlantic derived from functional data analysis of in situ profiles[END_REF] in two areas with distinct thermohaline structure (Fig. 1): the WBCS, along the continental slope, corresponds to the western boundary current system dominated by the NBUC [START_REF] Dossa | Near-surface western boundary circulation off Northeast Brazil[END_REF], while the SECS encompasses the Rocas Atoll and part of Fernando de Noronha ridge seamounts and corresponds to the cSEC [START_REF] Silva | Surface circulation and vertical structure of upper ocean variability around Fernando de Noronha Archipelago and Rocas Atoll during spring 2015 and fall 2017[END_REF]. For practical purpose, station 39, which was in the transition zone, was included in the SECS. To dampen effects of dominant species, abundance data were transformed by log (x + 1) in all analysis. A bi-factorial Permutational Multivariate Analysis of Variance (PERMANOVA; [START_REF] Anderson | Permanova For Primer: Guide to Software and Statiscal Methods[END_REF] was used to test for spatial (WBCS and SECS) differences among the thaliacean community structure. Additionally, bi-factorial Analysis of Variance (ANOVA) was performed to test for spatial differences among the dominant thaliacean species. Spatial patterns in thaliacean community abundance were identified by hierarchical cluster analysis using Bray-Curtis similarity matrix. The validity of the groups defined by this analysis was tested though SIMPROF test (5% significance level). A Similarity Percentage (SIMPER) analysis was performed to identify representative species and their contribution to similarity within the groups defined by the cluster analysis.

We performed a constrained ordination analyses to identify associations between the thaliacean species and the environmental variables. The following continuous explanatory variables were used: (i) sea surface temperature (SST), (ii) sea surface salinity (SSS), (iii) maximum value of fluorescence (as an indirect measure of primary productivity) from the surface to maximum sampling depth in each station, (iv) bottom depth, (v) relative presence of Tropical Surface Water (σ 0 < 25.6), South Atlantic Central Water (σ 0 between 25.6 and 27) and Antarctic Intermediate Water (σ 0 > 27) from the surface to maximum sampling depth in each station, (vi) the zonal component (westward/eastward) of ADCP data integrated over the first 70 m depth and between 70 and 350 m depth and (viii) the meridional component (southward/northward) of ADCP data integrated over the first 70 m depth and between 70 and 350 m depth. Detrended Canonical Correspondence Analyses (DCCA) revealed short length of variable gradients (< 3), indicating that a linear method was more appropriate to use on this occasion, and thus Redundancy Analysis (RDA) was selected [START_REF] Lepš | Multivariate Analysis of Ecological Data using CANOCO[END_REF].

Environmental and distribution maps were produced in Ocean Data View 5.0 [START_REF] Schlitzer | Ocean Data View[END_REF] and QGIS 3.4 (QGIS Development Team, 2022). ANOVA was performed in Statistica 10 (Stat-Soft Inc., 2011). Cluster, SIMPROF, SIMPER and PERMANOVA analyses were performed in Primer v.6 + PERMANOVA [START_REF] Clarke | PRIMER 6 + PERMANOVA[END_REF]. DCCA and RDA were performed in CANOCO 4.5 [START_REF] Lepš | Multivariate Analysis of Ecological Data using CANOCO[END_REF].

Results

Environmental background

SST ranged from 28.6 to 29.3 °C through the area. Shallower stations over the continental slope in the WBCS presented higher surface salinity ranging from 36.5 to 37.5, particularly over the Pernambuco Plateau in the south of the study area, where the highest values were observed (Fig. 2). In the open ocean (SECS), SSS was slightly lower and more stable, ranging from 35.7 to 36 with exception of station 39, in the transition zone. The region of seamounts in the north of the WBCS presented intermediate values around 36 (Fig. 2). Although the SECS presented higher values of maximum fluorescence in the water column, it was quite variable, with both areas presenting high and low values. In the WBCS, it ranged from 0.56 to 1 and in the SECS from 0.5 to 1.1 (Fig. 2). For a detailed description of patterns of the thermohaline structure and phytoplankton biomass in the area, see [START_REF] Assunção | 3D characterisation of the thermohaline structure in the southwestern tropical Atlantic derived from functional data analysis of in situ profiles[END_REF] and [START_REF] Farias | Uncoupled changes in phytoplankton biomass and size structure in the western tropical Atlantic[END_REF], respectively.

SADCP data integrated from 0 to 70 m depth showed the cSEC flowed westward over the open ocean (with its core around Fernando de Noronha Ridge), feeding the NBUC and surface currents (both flowing north/northwestward) when reaching the slope and continental shelf (Fig. 3). Overall, in the surface waters (0 to 70 m depth) cSEC and NBUC were much more intense north of 7.5°S, where they spread over the continental shelf. South of 7.5°S, surface current speed weakened over the slope and almost dissipated over the continental shelf where some eastward flow was observed (Fig. 3). However, from 70 to 350 m depth, NBUC was intense all over the slope and seamounts of the WBCS (Fig. 3). In contrast, in the open ocean, cSEC almost dissipated in this depth and eastward flow of the South Equatorial Undercurrent SEUC was observed in the area (Fig. 3). For detailed description of the circulation in the study area see [START_REF] Stramma | Ocean oxygen minima expansions and their biological impacts[END_REF], [START_REF] Stramma | On the water masses and mean circulation of the South Atlantic Ocean[END_REF], [START_REF] Dossa | Near-surface western boundary circulation off Northeast Brazil[END_REF] and Costa da [START_REF] Silva | Surface circulation and vertical structure of upper ocean variability around Fernando de Noronha Archipelago and Rocas Atoll during spring 2015 and fall 2017[END_REF].

Species composition

Seven species of thaliaceans were observed in pelagic waters of the Weastern Tropical South Atlantic, corresponding to six species from the order Salpida and one from the order Pyrosomatida (Table 1). Only tunics from the order Doliolida were found, which were grouped in a single taxon as Doliolida spp. (Table 1). Overall, the most frequent and abundant species was Pyrosoma atlanticum Péron, 1804, which was present in 56.4% of the samples and represented 97.1% of the total specimens collected (Table 1). Although Doliolida spp. was present in 43.6% of the samples, it always occurred in low abundance, representing 2.2% of the total catch (Table 1). The most frequent and abundant species among Salpida was Soestia zonaria (Pallas, 1774) which was present in 30.8% of the samples and represented 0.7% of the total catch (Table 1).

Spatial, vertical and diel distribution patterns

Overall, the thalicean community presented highly significant differences according to the areas (PER-MANOVA Pseudo-F = 27.455, P = 0.001). The dominant species, P. atlanticum, presented higher abundance over the continental slope and around oceanic seamounts (WBCS), reaching 700 col. 10 5 m -3 (Fig. 4, Table 1). Although also present in oceanic stations of the Fernando de Noronha Ridge (SECS), P. atlanticum was significantly (ANOVA F = 18.33, p = 0.0001) less abundant there (max: 3.4 col. 10 5 m -3 ; Fig. 4, Table 1). At daytime, the abundance of P. atlanticum was even in the different depths of the sampled water column. Contrastingly, at night, higher abundances were observed in the first 200 m (Figs. 4,5). Doliolida spp. occurred in low abundances in both areas, except for station 42A in the SECS, where it reached 27 ind. 10 5 m -3 (Fig. 4, Table 1). No significant differences among areas were observed (ANOVA = 0.069, P = 0.79); however, Doliolida spp. was absent from most stations over the slope in the WBCS (Fig. 4). During the day, it was more abundant in deeper waters (400 to 850 m) while at night, higher abundances occurred in the first 200 m (Figs. 4,5).

Table 1 Species composition and basic statistics of thaliaceans from two areas [START_REF] Assunção | 3D characterisation of the thermohaline structure in the southwestern tropical Atlantic derived from functional data analysis of in situ profiles[END_REF] Soestia zonaria was significantly more abundant in the WBCS (ANOVA F = 8.66, P = 0.005), particularly in the south of the study area where it reached 7.4 ind. 100 km -3 . Only occasional catches were observed in the SECS. It was more abundant in stations sampled at night where it peaked in the first 200 m of the water column. During the day, S. zonaria was more abundant in samples with target depth between 400 and 600 m (Fig. 5). Other Salpida species occurred almost exclusively in the first 100 m of water column in stations over the slope in the south of the WBCS (Figs. 4,5). It is noteworthy that mesh selectivity is a potential drawback in these results since the coarse aperture may have lost smaller species and early life stages.

Community structure

The cluster analysis depicted three groups: A, B and C, with low similarity between each other (Fig. 6). SIMPROF analysis performed on the results of the cluster analysis considered the three groups as valid.

Group A, with 76.3% similarity within group, included most stations located in the WBCS (Fig. 6). High abundances of P. atlanticum were the main responsible for the similarity in the group. S. zonaria was also present in the samples of the group, but with a much lesser abundance (Table 2). Group B included only offshore stations from the SECS (Fig. 6). The group had 64.7% similarity and Doliolida spp. contributed for 90% of the similarity within the group (Table 2), although P. atlanticum was also present in low abundance. Group C was represented by samples from both areas (although more frequent in the SECS) where thaliaceans were found in very low abundances or completely absent (Figs. 4,6,Table 2).

Species responses to environmental gradient

The two first canonical axes of the RDA explained 64.3% of species variance (Table 3). Monte Carlo test showed that the first (F-ratio = 40.110, P = 0.002) and all canonical axes together (F-ratio = 4.902, P = 0.002) were significant. Axis 1 explained 60.7% 3). Axis 2 explained additional 3.6% and was positively related to SSS and the relative presence of SACW and AIW in the portion of the water column sampled and negatively related to the relative presence of TSW, SST and bottom depth (Fig. 7, Table 3).

Pyrosoma atlanticum and S. zonaria were positively related to axis 1, indicating these species were more abundant in shallower samples under the influence of the NBUC with lower fluorescence and higher salinity. Doliolida spp. was related to the negative portion of axis 2, indicating the taxa was more abundant in deeper stations, and related to higher SST and relative presence of TSW (Fig. 7).

Discussion

Our results reveal that in the Western Tropical South Atlantic off Northeast Brazil, the thaliacean community structure presents different patterns according to the current system and associated thermohaline structure. This was not necessarily expected since in other gelatinous organisms, such as planktonic cnidarians, Fig. 5 Average relative abundance (individuals and aggregates per 10 5 m -3 ) per target depth strata (including net descent and ascent phases) and day period of Pyrosoma atlaticum, Doli-olida spp. and Salpida species in the Western Tropical South Atlantic. x = Depth strata not sampled the spread of oligotrophic oceanic waters over the coast led to typically homogeneous oceanic communities in the study area and other regions [START_REF] Thibault-Botha | Siphonophore assemblages along the east coast of South Africa; mesoscale distribution and temporal variations[END_REF][START_REF] Tosetto | Spatial patterns in planktonic cnidarian distribution in the western boundary current system of the tropical South Atlantic Ocean[END_REF].

In the WBCS, P. atlanticum and in a lesser extent S. zonaria were the most representative thaliacean species. These species were highly related to the NBUC, the strong western boundary subsurface current that reaches up to 1.2 ms -1 and flows parallel to the coast [START_REF] Dossa | Near-surface western boundary circulation off Northeast Brazil[END_REF]. In this area, P. atlanticum reached the highest abundances observed in the study (up to 700 col. 10 5 m -3 ). Massive occurrences of P. atlanticum were reported previously in areas with sloping topography under the influence of strong currents, such as the Northern California current and Guinea current. These studies associated the massive occurrences of the species with local changes in water temperature and salinity [START_REF] Lebrato | Mass deposition event of Pyrosoma atlanticum carcasses off Ivory Coast (West Africa)[END_REF][START_REF] Miller | Distribution of pelagic thaliaceans, Thetys vagina and Pyrosoma atlanticum, during a period of mass occurrence within the California current[END_REF][START_REF] Schram | Abundance, distribution, and feeding ecology of Pyrosoma atlanticum in the Northern California Current[END_REF], but the relation of P. atlanticum with water circulation was not addressed properly by the authors. Tunic tissues of P.

atlanticum are typically thicker than other thaliaceans [START_REF] Hirose | Tunic morphology and cellulosic components of pyrosomas, doliolids, and salps (Thaliacea, Urochordata)[END_REF]. This trait, associated with the larger sizes of the colonies, may grant them resistance to survive in strong boundary currents and the possibility to take advantage from local conditions of water and additional food supply. These organisms may also have been pushed by the coastward currents and accumulated over the slope. Although this process was never observed in thaliaceans, many studies reported the aggregation of other planktonic organisms in sloping topography induced by oceanic currents and species vertical behaviour [START_REF] Cotté | Formation of dense krill patches under tidal forcing at whale feeding hot spots in the St. Lawrence estuary[END_REF][START_REF] Sourisseau | Krill aggregation in the St. Lawrence system, and supply of krill to the whale feeding grounds in the estuary from the gulf[END_REF][START_REF] Hazen | Fine-scale prey aggregations and foraging ecology of humpback whales Megaptera novaeangliae[END_REF]. Additionally, P. atlanticum and S. zonaria were negatively related to fluorescence. Fluorescence is an indirect proxy of primary production and food availability. These species are efficient filter-feeders consuming pico-and nanoparticles including the bacterioplankton typically responsible for most primary production in oligotrophic systems such as the Western Tropical South Atlantic. Thus, the large abundance of P. atlanticum observed in this study may have contributed to the reduction of the chlorophyll stocks as previously observed in other ocean basins [START_REF] Drits | Pyrosoma atlanticum (Tunicata, Thaliacea): Grazing impact on phytoplankton standing stock and role in organic carbon flux[END_REF][START_REF] Perissinotto | Grazing by Pyrosoma atlanticum (Tunicata, Thaliacea) in the south Indian Ocean[END_REF].

Interestingly, the Salpida species Iasis cylindrical (Cuvier, 1804), Salpa aspera Chamisso, 1819, and Cyclosalpa pinnata (Forskål, 1775) occurred almost exclusively in stations in the south of the WBCS, where the Pernambuco Plateau is located [START_REF] Buarque | Post-rift volcanic structures of the Pernambuco Plateau, northeastern Brazil[END_REF]. The particular topography and circulation in the region reduces the influence of western boundary currents over the shelf and oceanward transport of coastal water is observed (Dossa et al., Tosetto et al., 2021). This hydrographic configuration has significant implications in the structure of pelagic communities and possibly the entire ecosystem [START_REF] Eduardo | Identifying key habitat and spatial patterns of fish biodiversity in the tropical Brazilian continental shelf[END_REF][START_REF] Tosetto | Spatial patterns in planktonic cnidarian distribution in the western boundary current system of the tropical South Atlantic Ocean[END_REF]. Doliolida spp. dominated stations from group B, located exclusively in the SECS. Unfortunately, only tunics were found in our samples; thus, identification to species level was not possible. However, common doliolid species in waters of the Western Tropical South Atlantic are Dolioletta gegenbauri (Uljanin, 1884), Dolioloides rarum (Grobben, 1882), Doliolum denticulatum Quoy & Gaimard, 1834, and Doliolum nationalis Borgert, 1893 (Esnal & Daponte, 1999a;[START_REF] Díaz | Biodiversidade e dinâmica espaço-temporal do zooplâncton[END_REF]. These are typical epipelagic warm water species (Esnal & Daponte, 1999a); thus, the close positive relation of doliolid species observed in this study with tropical surface water mass (Fig. 7) is expected.

Although we did not perform depth stratified samples, our results suggest the three more frequent and abundant taxa performed diel vertical migrations. Higher abundances of P. atlanticum occurred in samplings carried out at night between 100 and 200 m depth. At daytime, this species was steadily abundant in the sampled water column. Since no tows were made below 1170 m depth, we cannot infer whether during daytime these organisms were aggregated in deeper waters or were distributed evenly throughout the water column. Both hypotheses are possible since P. atlanticum is known to undertake large vertical migrations below 1000 m depth [START_REF] Andersen | Pyrosoma atlanticum (Tunicata, Thaliacea): diel migration and vertical distribution as a function of colony size[END_REF][START_REF] Henschke | Large vertical migrations of Pyrosoma atlanticum play an important role in active carbon transport[END_REF]. Both Doliolida spp. and S. zonaria were more abundant in samplings carried out down to 200 m depth during night, and below 400 during daytime. S. zonaria vertical migration was not studied previously; however, this is a common behaviour in other Salpida species (e.g. [START_REF] Wiebe | Diel vertical migration by Salpa aspera and its potential for large-scale particulate organic matter transport to the deep-sea[END_REF][START_REF] Madin | Distribution and vertical migration of salps (Tunicata, Thaliacea) near Bermuda[END_REF][START_REF] Nishikawa | Diel vertical migration of the tunicate Salpa thompsoni in the Southern Ocean during summer[END_REF] and thus expected for S. zonaria. Differently, large vertical migration, as suggested by the larger abundances occurring in distinct depths during day and night, was never observed for doliolids, which often are reported in epipelagic waters (Esnal & Daponte, 1999a). Vertical migration is an important mechanism transporting carbon assimilated in the surface by epipelagic phytoplankton to deeper water masses across the thermocline, particularly when considering large swarms as observed herein for P. atlanticum. Thus, future studies should use closing net devices to better describe the vertical migration of thaliacean species and quantify carbon fluxes.

Mesh selectivity is always a potential drawback when sampling pelagic organisms. While a coarse mesh may lose smaller species and early life stages, a small mesh may filter high rates of unwished particles, obstructing water passage and rapidly clogging the mesh [START_REF] Riccardi | Selectivity of plankton nets over mesozooplankton taxa: Implications for abundance, biomass and diversity estimation[END_REF][START_REF] Tosetto | Sampling planktonic cnidarians with paired nets: Implications of mesh size on community structure and abundance[END_REF]. Studies focussing on thaliancean communities use wide range of mesh sizes, from fine plankton nets to large micronekton meshes (e.g. [START_REF] Li | Distribution and abundance of thaliaceans in the northwest continental shelf of South China Sea, with response to environmental factors driven by monsoon[END_REF][START_REF] Henschke | Large vertical migrations of Pyrosoma atlanticum play an important role in active carbon transport[END_REF][START_REF] Miller | Distribution of pelagic thaliaceans, Thetys vagina and Pyrosoma atlanticum, during a period of mass occurrence within the California current[END_REF]. In this study, we used a relatively coarse mesh to sample the thaliacean community (40 mm in the main body and 10 mm in the cod-end). Still, with this gear, we could filter a large volume of water reaching deeper strata. The coarse meshes also reduce clogging and Fig. 7 RDA relating the thaliacean species to environmental gradients in the Western Tropical South Atlantic Ocean bow wave effect, enabling the catch of large specimens and colonies [START_REF] Vannucci | Loss of organisms through the meshes Zooplankton sampling[END_REF]. Thaliacea encompasses species with a wide range of sizes and no single method would allow a sampling all of them. The additional trawls we performed with the finer mesh (30 mm in the main body and 3 mm in the codend) collected two additional salp species (Table 1). Unfortunately, few tows were performed with this mesh, and we could not properly compare the effects of mesh selectivity on the structure and abundance of the thaliacean community in the Western Tropical South Atlantic, an important subject to be addressed in the future studies. Additionally, studies carried out with samples collected with a 300-μm mesh size from 200 m depth to surface at the Archipelago of Saint Peter and Saint Paul, close to FNR, recorded eight thaliaceans species: P. atlanticum, D. rarum, D. denticulatum, I. cylindrica (as Weelia cylindrical), Thalia democratica (Forskål, 1775), Thalia cicar van Soest, 1973, Pegea socia (Bosc, 1802) and Thalia sp. [START_REF] Díaz | Biodiversidade e dinâmica espaço-temporal do zooplâncton[END_REF]. Thus, at least three of the species collected with the finer mesh in Saint Peter and Saint Paul were not present in our samples.

In conclusion, we observed clearly distinct patterns in the thaliacean community in the Western Tropical South Atlantic likely related to the circulation and thermohaline structure in the area. Over the continental slope, where the strong NBUC flows northward, high abundances of P. atlanticum, and, to a lesser degree, S. zonaria were observed. Over the Pernambuco plateau, in the South of this area and where current intensity was lower, other less abundant salp species, such as I. cyilndrica, C. pinnata and S. aspera, were present as well. Meanwhile, offshore around the Fernando de Noronha Ridge, Doliolida spp. were the dominant thaliacean, co-occurring with P. atlanticum in lower abundance.

Funding We are grateful to the French oceanographic fleet for funding the survey ABRAÇOS 1 and the officers, crew and scientific team of the R/V Antea for their contribution to the success of the operations. The present study was not possible without the support of all members from LABZOO and other laboratories from UFPE and UFRPE. We thank to CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Supe-

Fig. 1

 1 Fig. 1 Geographic location of the study area in the Western Tropical South Atlantic, showing the sampled stations

Fig. 2 Fig. 3

 23 Fig. 2 Sea surface temperature (SST, °C), sea surface salinity (SSS) and maximum fluorescence (mg.m -3 ) during autumn 2017 in the Western Tropical South Atlantic

Fig. 4

 4 Fig. 4 Geographic distribution of the abundance of Pyrosoma atlaticum, Doliolida spp. and Salpida species. s-solitary individuals, a-aggregates. Values standardized in number of individuals or aggregates per 10 5 m -3 ▸

Fig

  Fig. 6 a Cluster analysis dendrogram of data indicating three groups samples with similar thaliacean communities in the Western Tropical South Atlantic Ocean, dashed lines are significant groups in the SIMPROF analysis. b Map indicating distribution of the groups arranged in the cluster analysis

  rior) and CNPq (Brazilian National Council for Scientific and Technological Development), which provided Research Scholarships to E.G.T., B.B.S. and S.N.L. This work is a contribution to the LMI TAPIOCA (www. tapio ca. ird. fr), CAPES/ COFECUB program (88881.142689/2017-01), the European Union's Horizon 2020 projects PADDLE (Grant agreement No. 73427) and TRIATLAS (Grant agreement No. 817578).

  in the Western Tropical South Atlantic Ocean off Northeast Brazil Mean abundance (colonies or individuals 10 5 m -3 ) per station and standard deviation, range of abundance, frequency of occurrence (f; considering both areas). X = Species present only in the additional samples and not included in the analysis

	Species	WBCS		SECS		f (%)
		Mean ± SD	Range of non-zero abundances	Mean ± SD	Range of non-zero abundances
	Pyrosoma atlanticum (colony)	206.42 ± 209.67	27.65-699.96	0.36 ± 0.79	0.2-3.38	56.41
	Doliolida spp.	2.06 ± 4.17	0.33-12.42	2.5 ± 5.89	0.37-27.04	43.59
	Soestia zonaria (aggregate)	1.01 ± 1.44	0.54-4.7	0.04 ± 0.11	0.33-0.39	25.64
	Soestia zonaria (solitary)	0.39 ± 0.81	0.18-2.69	0.02 ± 0.09	0.43	17.95
	Iasis cyllindrica (solitary)	0.08 ± 0.22	0.28-0.9	-	-	7.69
	Salpa aspera (solitary)	0.01 ± 0.04	0.18-0.18	0.02 ± 0.09	0.43	5.12
	Salpa aspera (aggregate)			X
	Cyclosalpa pinnata (solitary)	0.02 ± 0.08	0.36-0.36	-	-	2.56
	Salpa fusiformis (solitary)			X
	Cyclosalpa polae (solitary)			X

Table 2

 2 Results of SIMPER analysis, showing the relative contribution of thaliaceans taxa in the formation of the groups defined in the Cluster analysis

	Species	A	B	C
	Pyrosoma atlanticum	93.1	9.4	30.5
	Doliolida spp.		89.8	45.7
	Soestia zonaria	4		23.8

Table 3

 3 Summary of the RDA performed between the thaliacean taxa and environmental explanatory variables from the Western Tropical South Atlantic

		Axis 1	Axis 2
	Eigenvalues	0.607	0.036
	Species-environment correlations	0.843	0.578
	Cumulative variance (%)
	Of species data	60.7	64.3
	Of species-environment relationships	92.9	98.3
	Correlations of explanatory variables
	0-70 m currents zonal component	-0.3304	0.1006
	0-70 m currents meridional compo-nent	0.6625	0.0678
	70-350 m currents zonal component	-0.6243	0.0347
	70-350 m currents meridional com-ponent	0.7143	0.1054
	Bottom depth	-0.1959 -0.1299
	Sea surface temperature	0.1365 -0.3367
	Sea surface salinity	0.3739	0.2105
	Fluorescence	-0.6734 -0.0143
	% of Tropical surface water	0.0506 -0.1276
	% of South Atlantic Central water	-0.028	0.099
	% of Antarctic intermediate water	-0.0608	0.1115

Data availability

The data that support the findings of this study are available from the corresponding author, upon reasonable request.

Conflict of interest

The authors declare they have no conflict of interests.


F A Alves-Júnior

L F Andrade

A Ber Trand

S Neumann-Leitão

Alves Coelho

Pelágicas O Gênero

Thysanopoda H Milne Edwards

(Euphausiacea, Euphausiidae) from the Southwestern Atlantic: with comments on morphological variations

Keywords: Krill, Brazil, zooplankton, pelagic habitat, Abraços Project

Euphausiids are a diverse order of crustaceans that play a key role in pelagic food webs. The genus Thysanopoda H. Milne Edwards, 1830 is composed of 14 valid species, widely distributed in all oceans. However, some gaps remain in our knowledge of the geographic distribution of Thysanopoda cristata G. O. Sars, 1883, and its actual occurrence in Brazil. This study aims to expand the knowledge on krill diversity in Brazilian waters, confirming the occurrence of T. cristata and providing illustrations of its morphological variations. Four specimens, two males and two females, were collected on board R/V "Antea" in October 2015, using a micronekton net with 1 mm mesh size, at depths ranging between 10 and 1660 m. Before this study, reports of T. cristata from Brazil were provided only in species lists or unpublished data. Our study confirms the presence of the species from the southwestern Atlantic and brings new information on its morphology.

INTRODUCTION

Zooplanktonic organisms are widely studied worldwide to assess their biodiversity, biology and role in the pelagic energy transport, food webs, carbon and nitrogen flow and indications of environmental conditions [START_REF] Bonecker | Horizontal and vertical distribution of mesozooplankton species richness and composition down to 2,300 m in the southwest Atlantic Ocean[END_REF]. Among these organisms, holoplanktonic crustaceans of the order Euphausiacea Dana, 1852, composed by organisms, commonly known as krill [START_REF] Ramirez | Eufáusidos de algunos sectores del Atlántico sudoccidental[END_REF][START_REF] Ramirez | Eufáusidos de la Campaña Oceanográfica "Walter Herwig[END_REF][START_REF] Ramirez | Planktonic indicators or Argentine shelf and adjacent areas[END_REF][START_REF] Montú | Eufausidos de la plataforma Argentina y adyacencias I[END_REF], play an important role in the dynamics of pelagic communities, participating in both top-down and bottom-up controls (Rissik et al., 1997;[START_REF] Verity | Status, trends and the future of the marine pelagic ecosystem[END_REF][START_REF] Champalbert | Zooplankton spatial and temporal distribution in a tropical oceanic area off West Africa[END_REF].

Krill is indeed the main prey for a large number of cephalopods, fishes, seabirds, sea lions and whales, due to its great abundance and rich source of energy and nutrients (Mauchline & Fisher, 1969;[START_REF] Gibbons | Euphausiacea[END_REF][START_REF] Letessier | Drivers of euphausiid species abundance and numerical abundance in the Atlantic Ocean[END_REF][START_REF] Vereshchaka | A phylogenetic study of krill (Crustacea: Euphausiacea) reveals new taxa and co-evolution of morphological characters[END_REF]. Krill is also used in the production of feed for the aquaculture industry, the production of pharmaceuticals, and has been used as human food in some regions of Antarctica, Russia and Japan, due to the high concentration of fatty acids, lipids, vitamin A, Omega-3 and fluorine [START_REF] Gibbons | Euphausiacea[END_REF][START_REF] Atkinson | Oceanic circumpolar habitats of Antarctic krill[END_REF]. For several regions of the world, e.g., subtropical, subpolar and polar regions, krill can be a potential indicator of water masses, associated with their occurrence and migration only in specific masses (Montú & Cordeiro, 1986;[START_REF] Atkinson | Oceanic circumpolar habitats of Antarctic krill[END_REF]Sutton & Beckley, 2017).

To date, the order Euphausiacea is composed of two families: (i) Bentheuphausiidae [START_REF] Colosi | Crostacei. Part II, Eufausiacei. Raccolte Planctoniche fatte dalla R. Nave 'Liguria[END_REF], which is monospecific, comprising only the genus Bentheuphausia G. O. [START_REF] Sars | Report on the Schizopoda collected by H.M.S. Challenger during the years 1873-1876[END_REF], represented by B. amblyops G. O. Sars, 1885;and (ii) the family Euphausiidae Dana, 1852, comprising 11 genera and86 valid species (WoRMS, 2022), which is widely distributed in all oceans including high latitudes, occurring in pelagic habitats from the surface to the deep ocean (>5000 m) (Boden et al., 1955;Antezana & Brinton, 1981;[START_REF] Gibbons | Euphausiacea[END_REF][START_REF] Vereshchaka | A phylogenetic study of krill (Crustacea: Euphausiacea) reveals new taxa and co-evolution of morphological characters[END_REF].

Around 60 species of krill are reported in the South Atlantic, from neritic to oceanic zones, including islands, archipelagos and atolls [START_REF] Montú | Eufausidos de la plataforma Argentina y adyacencias I[END_REF][START_REF] Muxagata | Euphausiacea diversity in a transoceanic transect through the South Atlantic Ocean: the first Atlantic record of Thysanopoda astylata Brinton[END_REF]. In Brazilian waters, 22 species are currently recorded, distributed among Euphausia Dana, 1850 (6 species), Nematobrachion Calman, 1905 (3 species), Nematoscelis G. O. Sars, 1883 (4 species), Stylocheiron G. O. Sars, 1883 (4 species) and Thysanopoda (5 species) [START_REF] Ramirez | Eufáusidos de algunos sectores del Atlántico sudoccidental[END_REF]Antezana & Brinton, 1981;Montú & Cordeiro, 1986;[START_REF] Gibbons | Euphausiacea[END_REF]Lansac-Tôha & Freire, 1999). Large parts of these records are concentrated in only a few regions of Brazil, such as: the Saint Peter and Saint Paul as well as the Fernando de Noronha archipelagos and in the states of Espírito Santo, Rio de Janeiro (Campos Basin), São Paulo, Paraná and Rio Grande do Sul [START_REF] Ramirez | Eufáusidos de algunos sectores del Atlántico sudoccidental[END_REF][START_REF] Gibbons | Euphausiacea[END_REF].

Regarding Euphausiidae, the genus Thysanopoda H. Milne Edwards, 1830 is composed of 14 valid species with a broad distribution in all oceans (including Arctic and Antarctic regions), especially in meso-and bathypelagic zones (∼200 to 4000 m) [START_REF] Brinton | The distribution of Pacific euphausiids[END_REF][START_REF] Baker | A practical guide to euphausiids of the world: 1-96[END_REF][START_REF] Gibbons | Euphausiacea[END_REF]. According to Lansac-Tôha & Freire (1999) and [START_REF] Muxagata | Euphausiacea diversity in a transoceanic transect through the South Atlantic Ocean: the first Atlantic record of Thysanopoda astylata Brinton[END_REF], only five species of Thysanopoda have been recorded in the South Atlantic (T. aequalis [START_REF] Hansen | Further notes on the Schizopoda[END_REF]T. monacantha Ortmann, 1893;T. obtusifrons G. O. Sars, 1883;T. orientalis Hansen, 1910;and T. tricuspidata H. Milne Edwards, 1837). However, reports of T. cristata G. O. Sars, 1883 from the South Atlantic can only be found as elements in species lists in grey literature, and in [START_REF] Silva | Diet composition of bigeye tuna (Thunnus obesus) and yellowfin tuna (Thunnus albacares) caught on aggregated schools in the western equatorial Atlantic Ocean[END_REF]. In view of that surprisingly basic condition, this study aims to improve knowledge on krill diversity in Brazilian waters with the confirmation of T. cristata collected during the Acoustic Along the Brazilian Coast 1 (Abraços 1) survey in 2015, providing illustrations, morphological variations and deposited material.

MATERIAL AND METHODS

The specimens of Thysanopoda cristata were collected in October 2015 during the Abraços 1 survey, covering Northeastern Brazil between the states of Alagoas and Rio Grande do Norte and encompassing the Fernando de Noronha Archipelago, Rocas Atoll and the Fernando de Noronha Chain [START_REF] Bertrand | ABRACOS cruise[END_REF]. Sampling was performed in the water column, using a micronekton trawl net with a 1 mm mesh at depths ranging between 10 and 1170 m.

After sampling, specimens were sorted out. In the laboratory, all individuals were measured with a digital calliper (0.01 mm) for total length (TL) and carapace width (CW), and were next preserved in formalin 4% and thereafter identified to species level according to Boden et al. (1955) and[START_REF] Lozano Soldevilla | A record of the euphausiid Thysanopoda monacantha Ortmann, 1893 from the coast of Tenerife (Canary Islands)[END_REF][START_REF] Lozano Soldevilla | A record of the euphausiid Thysanopoda monacantha Ortmann, 1893 from the coast of Tenerife (Canary Islands)[END_REF]. The appendages were dissected and mounted on semipermanent excavated glass slides with glycerin and observed under an optical microscope Leica DM E and a stereomicroscope Nikon SMZ 800, both with camera lucida, for illustration. The drawings were digitized with CorelDRAW ® Graphics Suite 2018. All specimens examined were deposited in the Museum of Oceanography Prof. Petrônio Alves Coelho of the Federal University of Pernambuco, Recife, Brazil (MOUFPE).

RESULTS AND DISCUSSION

Specimens collected

Four specimens of Thysanopoda cristata, 2 females and 2 males, were collected from Rocas Atoll, "Abraços 1" Station 22/ Leg. 1, initial trawl coordinates: 4°07 ′ S 33°47 ′ W, final trawl coordinates: 4°07 ′ S 33°48 ′ W, 8 October 2015, at a depth of 525 m, MOUFPE 20050.

Descriptive notes

The specimens' size (TL) ranged from 51.5 to 67.8 mm, while the carapace width (CW) ranged between 15 and 21 mm. T. cristata is characterized by a rostrum with an acute main spine and a shorter one above it (fig. 1A); carapace with a longitudinal groove above the inferior margin and a posterolateral denticle on the inferior margin (fig. 1A); first segment of the peduncle of first antenna bearing a hood-like lappet with dorsal setae, second segment dorsally produced as an acute spine (fig. 1B,C); fourth and fifth abdominal somites with a dorsal spine (fig. 1D,E); sixth abdominal somite slightly longer than fifth (fig. 1F); petasma with spinous process almost straight to curved, terminal process curved, proximal process longer than terminal and tapering distally, lateral process long and very curved distally, additional process short and somewhat rounded (fig. 1G); uropod extending beyond distal end of telson, protopod bearing short lateral plumose setae, with a produced dorsal spine, exopod with plumose setae, smooth on the lateral margin and slightly serrate on medial margin, bearing a distolateral projection forming an acute spine, endopod shorter than exopod, with plumose setae, margins slightly crenulate (fig. 1H); telson with up to 10 pairs of stout dorsal setae (fig. 1I). Thoracopods 1-8 with regular shape and structurally similar, bearing plumose, pectinate and/or serrate setae on the endopods and densely plumose setae on exopods (fig. 2A-H); seventh thoracopod (fig. 2G) like the sixth thoracopod (fig. 2F); eighth thoracopod (fig. 2G) with rudimentary endopod.

Remarks and general discussion

The individuals of T. cristata analysed herein present some morphological differences from others described in the literature, such as: inferior margin of carapace with a denticle (vs. carapace without inferior denticle in G. O. Sars' (1883) original description). Boden et al. (1955) and[START_REF] Lozano Soldevilla | A record of the euphausiid Thysanopoda monacantha Ortmann, 1893 from the coast of Tenerife (Canary Islands)[END_REF][START_REF] Lozano Soldevilla | A record of the euphausiid Thysanopoda monacantha Ortmann, 1893 from the coast of Tenerife (Canary Islands)[END_REF] provided an identification key in which the denticle is present, leading us to suppose that this character was overlooked by [START_REF] Sars | Preliminary notices on the Schizopoda of H.M.S. Challenger Expedition[END_REF] as it can be often shortened. Additionally, the denticle does not exceed the carapace inferior margin, while it does in the illustration by Boden et al. (1955). The rostrum in our individuals has the main spine slightly longer than the shorter one and is weakly curved upwards, whereas it seems to be longer and deflexed in the description by [START_REF] Sars | Preliminary notices on the Schizopoda of H.M.S. Challenger Expedition[END_REF], and straight in that of Boden et al. (1955). The sixth abdominal somite of our individuals presents a strong notch near the posterodistal corner, not observed, nor reported, in other literature. In our specimens, it is also possible to see the telson with up to 10 pairs of stout dorsal setae (vs. 6 pairs and 7 pairs described, respectively, in the works of [START_REF] Sars | Preliminary notices on the Schizopoda of H.M.S. Challenger Expedition[END_REF]Boden et al., 1955).

Thysanopoda cristata was described by Sars ( 1883) based only on one adult male from off Mindanao in the Philippines (Pacific Ocean) (Station 213 at 3750 m), but it is known to be widely distributed in the Indo-Pacific (between 30°N and 40°S), South Africa (Natal coast), Baja California in Mexico, and in the Polar Arctic and Antarctic oceans (Boden, 1955;[START_REF] Brinton | The distribution of Pacific euphausiids[END_REF]Grindley & Penrith, 1965;[START_REF] Taniguchi | Mysids and euphausids in the eastern Indian Ocean with particular reference to invasion of species from the Banda Sea[END_REF][START_REF] Youngbluth | The vertical distribution and diel migration of euphausiids in the central waters of the eastern South Pacific[END_REF]. For the Atlantic Ocean, this species was reported only in the Sargasso Sea, Azores and possible observations in the tropical western Atlantic (covering the North and South Atlantic) [START_REF] Gibbons | Euphausiacea[END_REF]Lansac-Tôha & Freire, 1999;[START_REF] Muxagata | Euphausiacea diversity in a transoceanic transect through the South Atlantic Ocean: the first Atlantic record of Thysanopoda astylata Brinton[END_REF]. However, several of these records were provided in unpublished reports (dissertations and theses) containing only species lists, without taxonomic descriptions, and specimens not deposited in a zoological collection, nor included an estimate of a possible region of occurrence for the T. cristata found. Based on those data, some geographic information included in the literature may contain dubious records from some marine areas around the world.

According to [START_REF] Vereshchaka | A phylogenetic study of krill (Crustacea: Euphausiacea) reveals new taxa and co-evolution of morphological characters[END_REF], T. cristata is reported from mesopelagic zones, performing nictemeral migration between the depths of 800 and 2000 m, in addition, the occurrence of this species in shallow waters can be associated with upwelling regions, especially around oceanic islands. In this context, many species of krill are used as indicators of fish stocks, due to their direct predation by commercial fish [START_REF] Champalbert | Zooplankton spatial and temporal distribution in a tropical oceanic area off West Africa[END_REF]. For example, in oceanic waters near the Saint Peter and Saint Paul Archipelago, the distribution of T. cristata displays seasonal movements that are indicative of the presence of Thunnus albacares [START_REF] Bonnaterre | Tableau encyclopédique et méthodique des trois règnes de la nature[END_REF] and T. obesus [START_REF] Lowe | A supplement to a synopsis of the fishes of Madeira[END_REF] [START_REF] Silva | Diet composition of bigeye tuna (Thunnus obesus) and yellowfin tuna (Thunnus albacares) caught on aggregated schools in the western equatorial Atlantic Ocean[END_REF].

In Brazil, knowledge on krill diversity is still far from complete, with the main papers published between 1971 and 1999 [START_REF] Ramirez | Eufáusidos de algunos sectores del Atlántico sudoccidental[END_REF][START_REF] Ramirez | Eufáusidos de la Campaña Oceanográfica "Walter Herwig[END_REF][START_REF] Ramirez | Planktonic indicators or Argentine shelf and adjacent areas[END_REF]Antezana & Brinton, 1981;Montú & Cordeiro, 1986;[START_REF] Gibbons | Euphausiacea[END_REF]Lansac-Tôha & Freire, 1999). However, new surveys along the Brazilian oceanic waters are providing new materials for new records of known species. Thus, the new record of T. cristata increases the knowledge on krill diversity in the southwestern Atlantic, thereby providing an insight that the species might be widespread in the region.

Fig. 1 .

 1 Fig. 1. Thysanopoda cristata G. O. Sars, 1883, (MOUFPE 20050). Female, 67.8 mm in length: A, carapace; D, fourth abdominal somite; E, fifth abdominal somite; F, sixth abdominal somite; H, uropod; I, telson. Male, 52.1 mm in length: B, first antennal peduncle in lateral view; C, first antennal peduncle in dorsal view; G, petasma. Scale bars = 10 mm for A; 1 mm for B-C; 5 mm for D-F and I; 0.5 mm for G; 2 mm for H.

Fig. 2 .

 2 Fig. 2. Thysanopoda cristata G. O. Sars, 1883, (MOUFPE 20050). Female, 67.8 mm in length: A-H, thoracopods 1-8, respectively. Scale bars = 0.05 mm.

ACKNOWLEDGEMENTS

The authors would like to thank the French oceanographic fleet for funding the ABRACOS1 survey (http://dx.doi.org/10.17600/17004100) and the officers and crew of the R/V "Antea" for their contribution to the success of the operations. This work is a contribution to the LMI TAPIOCA (www.tapioca.ird.fr). LFA is supported by Fundação de Amparo à Ciência e Tecnologia do Estado de Pernambuco (FACEPE), process number BFP-0106-1.08/21. The authors would like to thank the anonymous reviewers for their precious comments, additionally, Dr. Johanna Weston for her important suggestions throughout the text. The first author would, especially, like to thank Dr. J. C. von Vaupel Klein for his support and friendship.


Ellen Pikitch
email: ellen.pikitch@stonybrook.edu

P Dee Boersma

Ian L Boyd

David O Conover
email: dconover@uoregon.edu

Philippe Cury
email: philippe.cury@ird.fr

Timothy E Essington

Selina S Heppell
email: selina.heppell@oregonstate.edu

Edward D Houde
email: ehoude@umces.edu

Marc Mangel
email: msmangel@ucsc.edu

Daniel Pauly
email: d.pauly@oceans.ubc.ca

Eva Plaganyi
email: eva.plaganyi-lloyd@csiro.au

Keith Sainsbury
email: ksainsbury@netspace.net.au

Robert S Steneck
email: steneck@maine.edu

à la diffusion de documents scientifiques de niveau recherche, publiés ou non, émanant des établissements d'enseignement et de recherche français ou étrangers, des laboratoires publics ou privés.

The strong connection between forage fish and their predators: A response to Hilborn et al. (2017)

We are pleased to see that in the years since the publication of our report, Little Fish, Big Impact: A Report from the Lenfest Forage Fish Task Force [START_REF] Pikitch | Little Fish, Big Impact: Managing a Crucial Link in Ocean Food Webs[END_REF], researchers continue to study forage fish and to reach conclusions similar to ours. [START_REF] Hilborn | When does fishing forage species affect their predators?[END_REF] recommended, as we did, that forage fish management be tailored to individual species and ecosystems where possible. [START_REF] Hilborn | When does fishing forage species affect their predators?[END_REF], however, mischaracterized our work in several respects, presented selective analyses that are not widely representative of forage fish, and made claims not fully supported by their results.

In the interests of furthering science and the management of forage fish, we first briefly address the mischaracterizations, then discuss the selective analysis and unsupported conclusions that reduce the usefulness of the Hilborn et al. paper. We close by suggesting a path forward for forage fish management in light of the current state of the science.

Mischaracterizations of the Lenfest forage fish task force's work

The most important mischaracterization of our report by [START_REF] Hilborn | When does fishing forage species affect their predators?[END_REF] is their oversimplification of our approach and recommendations. Hilborn et al. often conflate our report with a single modeling approach, Ecopath with Ecosim (EwE), and present our recommendations as one-sizefits-all. For example, [START_REF] Hilborn | When does fishing forage species affect their predators?[END_REF] state " [START_REF] Pikitch | Little Fish, Big Impact: Managing a Crucial Link in Ocean Food Webs[END_REF] argued forcefully that their analysis provided general conclusions that should be broadly applied. However, relevant factors are missing from the analysis contained in their work…" This is simply not the case. Our recommendations are tailored to the level of uncertainty and data availability of each system, not broadly and uniformly applied. Furthermore, the statement above, and the subsequent focus on the shortcomings of EwE, ignores the multiple, independent lines of evidence we used in formulating our recommendations. In addition to modeling results, we relied upon evidence obtained during site visits, detailed case studies, analysis of the impacts of different harvest strategies in specific systems, and a comprehensive review of the literature. Our thorough and comprehensive approach considered all the relevant factors that [START_REF] Hilborn | When does fishing forage species affect their predators?[END_REF] [START_REF] Essington | Pitfalls and guidelines for recycling models for ecosystem-based fisheries management: evaluating model suitability for forage fish fisheries[END_REF] and in five cases the modeling was not conducted at the species level…" This is incorrect. Five of the 10 (not 11) EwE models we used in simulations considered age structure. These models received the highest score for "forage detail" in the separate study that [START_REF] Hilborn | When does fishing forage species affect their predators?[END_REF] cite in putative support of their statement, which was authored by two of us [START_REF] Essington | Pitfalls and guidelines for recycling models for ecosystem-based fisheries management: evaluating model suitability for forage fish fisheries[END_REF]. Furthermore, all of our models included species-level forage fish groups. Some models aggregated a subset of the forage species, but this in no way supports the assertion that "modeling was not conducted at the species level." [START_REF] Hilborn | When does fishing forage species affect their predators?[END_REF] also incorrectly presented the findings of [START_REF] Essington | Pitfalls and guidelines for recycling models for ecosystem-based fisheries management: evaluating model suitability for forage fish fisheries[END_REF] as a blanket rejection of the practice of model "recycling" (i.e., applying existing models to new questions or policy concerns). In fact, it is a guide on how to recycle models thoughtfully, which the Task Force didfor example by considering possible distorting effects of aggregating species groups.

Selective analyses and unsupported claims

In addition to mischaracterizing our report, Hilborn et al. based their general statements about forage fish on a small group of species that are not representative of forage fish as defined by [START_REF] Pikitch | Little Fish, Big Impact: Managing a Crucial Link in Ocean Food Webs[END_REF]. They examined 11 prey species in their paper, and some analyses considered as few as 6 of these species. They focused only on U.S. species, excluding many of the world's largest and best-studied forage fish fisheries. The majority of forage fish species they selected (Pacific hake, chub mackerel, Atlantic mackerel, and three squids) do not meet the [START_REF] Pikitch | Little Fish, Big Impact: Managing a Crucial Link in Ocean Food Webs[END_REF] definition of "forage fish." Given this difference, the results of the two studies are not comparable.

Hilborn et al. also ignored a large body of literature that contradicts their conclusions about predator dependencies on prey. For example, many empirical studies have demonstrated a strong connection between forage fish and the abundance of predators in southern Africa, Norway, Peru, and Antarctica [START_REF] Roux | Jellyfication of marine ecosystems as a likely consequence of overfishing small pelagic fishes: lessons from the Benguela[END_REF][START_REF] Erikstad | Seabird fish interactions: the fall and rise of a common guillemot Uria aalge population[END_REF][START_REF] Cury | Global seabird response to forage fish depletion-one-third for the birds[END_REF][START_REF] Crawford | Comparison of trends in abundance of guano-producing seabirds in Peru and southern Africa[END_REF]. Others trace the link between forage abundance and breeding success, both through field data (e.g. [START_REF] Boersma | Foraging distance affects reproductive success in Magellanic penguins[END_REF] and global analysis of existing data [START_REF] Cury | Global seabird response to forage fish depletion-one-third for the birds[END_REF]Hilborn et al. cite but dismiss this study). [START_REF] Cury | Global seabird response to forage fish depletion-one-third for the birds[END_REF] provide a comprehensive analysis, which demonstrates that marine birds require the long-term mean forage fish abundance, an evolutionary stable strategy. Hilborn et al. provide an incomplete and therefore potentially biased picture of predator-prey dependencies by emphasizing fishes in their selection of predator species.

In addition, [START_REF] Hilborn | When does fishing forage species affect their predators?[END_REF] made several methodological choices that reduced their ability to detect an impact on predators. One line of analysis looked at relationships between time series of predators and prey. Yet this work did not look at the broader food web context to investigate whether a strong relationship should be expected. For instance, [START_REF] Hilborn | When does fishing forage species affect their predators?[END_REF] included predator-prey combinations where the prey species made up as little as 20 percent of the predator's diet. And they used estimated population levels generated by stock assessment models to identify correlations between predators and prey. The "data" from these models are not empirical measurements, but synthetic estimates predicated on model assumptions. These assumptions include holding constant the values of key demographic rates of predators that are likely to be sensitive to prey abundance.

Insufficient evidence to support the claims

We now address areas where [START_REF] Hilborn | When does fishing forage species affect their predators?[END_REF] provide insufficient evidence to support their broad generalizations. [START_REF] Hilborn | When does fishing forage species affect their predators?[END_REF] compare selectivity by the fishery with the actual sizes of prey eaten by predators to support their claim that "predators often take small forage fish that are unaffected by fishing." However, a more appropriate evaluation would be to use the sizes of prey actually caught by the fishery, as selectivity is a measure of preference, not catch. Examination of their Fig. 3 suggests that predators target a wide range of prey sizes, and that one or more predators eat almost every size of prey. Furthermore, their Fig. 3 shows many instances where the preferred sizes in the fishery are quite similar to the average size in predator diets, and, for apex and many meso-predators, fishery selectivity and average size of prey eaten are very similar (e.g., Atlantic Bluefin tuna feeding on Atlantic menhaden; blacktooth and finetooth sharks feeding on Gulf menhaden; and harbor porpoise, Atlantic Bluefin tuna, harbor seal, spiny dogfish, and Atlantic cod feeding on Atlantic herring). Thus, [START_REF] Hilborn | When does fishing forage species affect their predators?[END_REF] do not provide sufficient evidence to support their assertion. Counter to their claim, and looking outside the limited sample they examined, one finds many examples where there is strong overlap between the sizes eaten by predators and the sizes taken by the fishery. Fig. 1 here (redrawn from [START_REF] Muck | The Peruvian Anchoveta and Its Upwelling Ecosystem: Three Decades of Change[END_REF] illustrates this point for species in the Peruvian and California Current ecosystems. [START_REF] Hilborn | When does fishing forage species affect their predators?[END_REF] show (their Fig. 2) that the sensitivity of forage fish to fishing, particularly for the smallest size classes of forage fish, depends critically on whether spawning biomass affects average recruitment. Yet, for many of the populations [START_REF] Hilborn | When does fishing forage species affect their predators?[END_REF] analyzed, there is weak or inconclusive evidence for the hypothesis that spawning stock does not affect recruitment. For the 7 species examined (their Fig. 4), two indicate recruitment is best explained by a B-H stock-recruitment or hockey stick model (i.e. stock size more important), 3 species show regime shift as the most likely hypothesis, and for 2 species (Pacific hake and Gulf menhaden) the AIC scores are essentially identical across hypotheses (Hilborn et al. Table 2). Three of the species show a breakpoint for which recruitment is reduced below a given stock size, lending further evidence for the importance of stock size on recruitment.

The claim that "spatial distribution of forage species may be more important than their abundance" is not supported by any spatial analysis. Hilborn et al. consider spatial distribution "only qualitatively" and provide no citations or analysis to support the contention that it is more important than abundance. They highlight only the possibility that spatial distribution may trump abundance and not the equally plausible hypothesis that abundance may be more important than spatial distribution.

It should also be noted that a high level of environmentally driven fluctuation in forage fishes does not mean that fishing is unimportant [START_REF] Shelton | Fluctuations of fish populations and the magnifying effects of fishing[END_REF]. [START_REF] Essington | Fishing amplifies forage fish population collapses[END_REF] detected the fingerprint of fishing (in the troughs of population cycles) despite large fluctuations in recruitment and showed that fishing amplifies population collapses. This is particularly relevant for predators that are most sensitive to changes in prey availability. [START_REF] Pikitch | Stop-loss order for forage fish fisheries[END_REF] discussed how the [START_REF] Essington | Fishing amplifies forage fish population collapses[END_REF] finding strengthens the case for minimum biomass thresholds for forage fish fisheries. [START_REF] Muck | The Peruvian Anchoveta and Its Upwelling Ecosystem: Three Decades of Change[END_REF]. A: Overlap between the size of anchoveta (Engraulis ringens) ingested by Peruvian cormorants (Phalacrocrorax bougainvilli) and the size of anchoveta caught in the Peruvian reduction fishery (based on [START_REF] Jordan | El fenomeno de las regurgitaciones en el guanay (Phalacrocorax bougainvilli) y un metodo para estimar la ingestion diaria[END_REF]; B: the same, for boobies (Sula variegata) (based H. Tovar, IMARPE, unpublished data and [START_REF] Fuentes | Las aves marinas en la zona sur del Peru, en Marzo de 1984[END_REF]; C and D: the same for Northern anchovy (Engraulis mordax), pelicans (Pelecanus occidentalis californicus) and a reduction fishery in California, in two different months . (based on data in [START_REF] Sunada | The brown pelican as a sampling instrument of age group structure in the northern anchovy population[END_REF]

A path forward

We agree with Hilborn et al. that fisheries management should be tailored to individual species and ecosystems where possible. However, while Hilborn et al. advocate for a "case by case" analysis, they do not provide guidance for managers in the many circumstances where detailed information is lacking. In contrast, we [START_REF] Pikitch | Little Fish, Big Impact: Managing a Crucial Link in Ocean Food Webs[END_REF] provide default recommendations for such situations based on a comprehensive account of forage fish and their ecosystems. Here, we reiterate our support for these recommendations and urge that they be used as an interim measure, in light of strong evidence that current management approaches are not designed to take into account the variability in forage fish stocks, their unusual lifehistory characteristics, and the role they play in the ecosystem.

In the five years since our report was released, research on forage fish and their role within ecosystems has grown. Recently, an integrated approach to assess the magnitude and consequences of fisheries-seabird resource competition has been proposed that will contribute to implementing best practices for moving towards ecosystem-based fisheries management [START_REF] Sydeman | Best practices for assessing forage fish fisheries-seabird resource competition[END_REF]. Given the importance of forage fish from ecological, economic, and social perspectives, we welcome further advances. We believe an approach that recognizes the strengths and weaknesses of various methods and seeks to use them in a complementary manner will be more effective than one that mischaracterizes and selectively interprets the work of others.

Fig. 1 .

 1 Fig.1. Examples of the commonly observed overlap between the size of forage fish consumed by seabirds and the sizes caught by commercial fisheries (redrawn from Fig.1-3 in[START_REF] Muck | The Peruvian Anchoveta and Its Upwelling Ecosystem: Three Decades of Change[END_REF]. A: Overlap between the size of anchoveta (Engraulis ringens) ingested by Peruvian cormorants (Phalacrocrorax bougainvilli) and the size of anchoveta caught in the Peruvian reduction fishery (based on[START_REF] Jordan | El fenomeno de las regurgitaciones en el guanay (Phalacrocorax bougainvilli) y un metodo para estimar la ingestion diaria[END_REF]; B: the same, for boobies (Sula variegata)(based H. Tovar, IMARPE, unpublished data and Fuentes, 1984); C and D: the same for Northern anchovy (Engraulis mordax), pelicans (Pelecanus occidentalis californicus) and a reduction fishery in California, in two different months . (based on data in[START_REF] Sunada | The brown pelican as a sampling instrument of age group structure in the northern anchovy population[END_REF]

  claim we ignored. Another mischaracterization by Hilborn et al. (2017) is that "None of the 11 EwE models used by Pikitch et al. considered the size or age structure of the forage fish

Declaration of interest

The authors declare that they have no competing interests.

Contributors

All authors have approved the final letter.