Ichthyoplankton community structure on the shelf break off northeastern Brazil

JANA R. SANTANA ALEJANDRO E.S.F. DA COSTA DÓRIS VELEDA SILVIA HELENA L. SCHWAMBORN PAULO O. MAFALDA JÚNIOR RALF SCHWAMBORN About the authors

Abstract

Oceanographic features influence the early stages of fish to a high degree. We investigated the influence of continental shelf-slope gradient on the ichthyoplankton composition and distribution off Northeastern Brazil. Two oceanographic campaigns were performed during July-August 2010 and 2012. The samplings were performed along three transects composed by three stations, covering the continental shelf and slope areas. Abiotic data were obtained by an ADCP and a CTD. The ichthyoplankton was sampled through diurnal and nocturnal hauls using a 500-µm bongo net from 200 m to the surface. A total of 1634 larvae and 4023 eggs, representing 91 genera and 76 species, were collected. Higher concentrations of fish eggs were found on the continental shelf, probably because of the North Brazil Undercurrent flux. Higher concentrations of larvae were found at night and could be associated with net avoidance or natural variation. Neritic, oceanic and transition groups of species association were determined. Larvae of neritic, demersal and pelagic fishes prevailed on the continental shelf, while larvae of oceanic, mesopelagic and bathypelagic fishes on the continental slope. Melanostomiidae, Scorpaena sp., Lestidium atlanticum, Lampadena sp. and Diaphus sp. were identified as indicators of the continental slope.

Key words
continental shelf-slope gradient; early life stages of fishes; indicator species; spatial distribution

INTRODUCTION

The ichthyoplankton is composed by fish eggs and larvae and constitutes a major component of the meroplanktonic communities (Ciechomski 1981CIECHOMSKI JD. 1981. Ictioplancton. In: Boltovskoy D (Ed), Atlas del zooplancton del Atlántico Sudoccidental y métodos de trabajo con el zooplancton marino. INIDEP, Mar del Plata, p. 829-860.). The spatial distribution of the ichthyoplanktonic assemblage is highly influenced by mesoscale physical processes commonly occurring over continental shelf break areas, such as eddies or density fronts (Grimes & Finucane 1991GRIMES CB & FINUCANE JH. 1991. Spatial distribution and abundance of larval and juvenile fish, chlorophyll and macrozooplankton around the Mississippi River discharge plume, and the role of the plume in fish recruitment. Mar Ecol Prog Ser 75: 109-119., Sabatés & Olivar 1996SABATÉS A & OLIVAR MP. 1996. Variation of larval fish distributions associated with variability in the location of a shelf-slope front. Mar Ecol Prog Ser 135: 11-20.). Temperature and salinity may also play important roles in the structure of the ichthyoplanktonic assemblages (Osorio-Zúñiga et al. 2018OSORIO-ZÚÑIGA F, LANDAETA MF, ANGULO-AROS J & BALBONTÍN F. 2018. Spatio-temporal variability of ichthyoplankton and its relationship with oceanographic conditions at the shelf break off Chilean Patagonia (43˚S – 51˚S). Mar Biol Res 14: 191-202.).

Studies related to the influence of mesoscale physical processes over biological communities are still inceptive in the South Atlantic waters and concentrate at the southern portion of the Atlantic basin (e.g. Franco et al. 2006FRANCO BC, MUELBERT JH & MATA MM. 2006. Mesoscale physical processes and the distribution and composition of ichthyoplankton on the Southern Brazilian shelf break. Fish Oceanogr 15: 37-43., Acha et al. 2004ACHA EM, MIANZAN HW, GUERRERO RA, FAVERO M & BAVA J. 2004. Marine fronts at the continental shelves of austral South America: physical and ecological processes. J Marine Syst 44: 83-105.). In the Brazilian waters, such studies were mainly performed over continental shelf break areas of the Southern region (e.g. Muelbert & Sinque 1996MUELBERT JH & SINQUE C. 1996. Distribution of Bluefish (Pomatomus saltatrix) larvae along the continental shelf off Southern Brazil. Mar Freshwater Res 47: 311-314., Macedo-Soares et al. 2014MACEDO-SOARES LCP, GARCIA CAE, FREIRE AS & MUELBERT JH. 2014. Large-scale ichthyoplankton and water mass distribution along the South Brazil shelf. PLoS ONE 9: e91241.). The relationships among mesoscale physical processes and biological communities remain poorly understood at the western tropical Atlantic waters off Northeast Brazil.

The shelf break and continental slope regions in northeastern Brazil are dominated by oligotrophic warm waters (Peterson & Stramma 1991PETERSON RG & STRAMMA L. 1991. Upper-level circulation in the South Atlantic Ocean. Progr Oceanogr 26: 1-73.), which leads to low biological productivity (e.g. Lessa et al. 2009LESSA R, BEZERRA JR JL, NASCIMENTO ED, LIMA M & PEREIRA AA. 2009. Oceanografia biológica: Composição, distribuição e abundância do ictioneuston na ZEE da região Nordeste do Brasil. 2009. In: Hazin FHV (Ed), Biomassa fitoplanctônica: Biomassa primária e secundária, macrozooplâncton, ictioplancton, ictioneuston, macrofauna bêntica. Fortaleza: Martins & Cordeiro 2: 166-194., Knoppers et al. 2002KNOPPERS B, EKAU W, FIGUEIREDO JR AG & SOARES-GOMES A. 2002. Zona costeira e plataforma continental do Brasil. In: Pereira RC & Soares-Gomes A (Eds). 2002. Biologia marinha. Rio de Janeiro: Interciência, p. 352-361., Souza et al. 2013SOUZA CS, LUZ JAG, MACEDO S, MANUEL JFM & MAFALDA JR PO. 2013. Chlorophyll a and nutrient distribution around seamounts and islands of the tropical south-western Atlantic. Mar Freshw Res 64: 168-184.) yielding ~ 75 g C m-2 y-1 (Longhurst et al. 1995LONGHURST A, SATHYENDRANATH S, PLATT T & CAVERHILL C. 1995. An Estimate of global primary production in the ocean from satellite radiometer data. J Plan Res 17: 1245-1271.).

Commonly, coastal areas receive nutrients through the influx of rivers in association with mangrove ecosystems (Ekau et al. 1999EKAU W, WESTHAUS-EKAU P & MEDEIROS C. 1999. Large scale distribution of fish larvae in the continental shelf waters off North-East Brazil. Arch Fish Mar Res 47: 183-200.), while oceanic areas are richer in nutrients in places where upwelling occurs, e.g. around islands and seamounts (Ekau et al. 1999EKAU W, WESTHAUS-EKAU P & MEDEIROS C. 1999. Large scale distribution of fish larvae in the continental shelf waters off North-East Brazil. Arch Fish Mar Res 47: 183-200., Knoppers et al. 2002KNOPPERS B, EKAU W, FIGUEIREDO JR AG & SOARES-GOMES A. 2002. Zona costeira e plataforma continental do Brasil. In: Pereira RC & Soares-Gomes A (Eds). 2002. Biologia marinha. Rio de Janeiro: Interciência, p. 352-361.), since this process weakens the stratification of the water column, allowing nutrients in deeper layers to reach surface waters. This enrichment may also occur at the region of the shelf break owing to the dynamics of physical processes, which may interfere in the ichthyoplanktonic biomass (e.g. González-Quirós et al. 2003GONZÁLEZ-QUIRÓS R, CABAL J, ÁLVAREZ-MARQUÉS F & ISLA A. 2003. Ichthyoplankton distribution and plankton production related to the shelf break at the Avilés Canyon. ICES J Mar Sci 60: 198-210., Franco et al. 2006FRANCO BC, MUELBERT JH & MATA MM. 2006. Mesoscale physical processes and the distribution and composition of ichthyoplankton on the Southern Brazilian shelf break. Fish Oceanogr 15: 37-43., Katsuragawa et al. 2014KATSURAGAWA M, DIAS JF, HARARI J, NAMIKI C & ZANI-TEIXEIRA ML. 2014. Patterns in larval fish assemblages under the influence of the Brazil current. Cont Shelf Res 89: 103-117.). Nevertheless, physical processes such as meanders and vortices may transport fish larvae from one area to another, as from the continental shelf to oceanic waters, influencing the abundance and composition of fish larvae assemblages of different areas (Franco et al. 2006FRANCO BC, MUELBERT JH & MATA MM. 2006. Mesoscale physical processes and the distribution and composition of ichthyoplankton on the Southern Brazilian shelf break. Fish Oceanogr 15: 37-43.).

The intense fishery accentuates the necessity of investigations on early stages of fishes, as well as on their relationship with physical and biological processes, to achieve a better comprehension of the variability in the recruitment of fishery resources (Hunter & Alheit 1997HUNTER JR & ALHEIT J. 1997. International GLOBEC Small Pelagic Fishes and Climate Change Program. Implementation Plan. GLOBEC Report 11: 36 p.). Physical and biological processes that occur in the shelf break are primordial to the recruitment of some fish species, granting the regulation of some of its populations (González-Quirós et al. 2003GONZÁLEZ-QUIRÓS R, CABAL J, ÁLVAREZ-MARQUÉS F & ISLA A. 2003. Ichthyoplankton distribution and plankton production related to the shelf break at the Avilés Canyon. ICES J Mar Sci 60: 198-210.). Although the number of studies related to the ichthyoplankton at shelf break areas at the Southern region of Brazil is increasing (e.g. Franco & Muelbert 2003FRANCO BC & MUELBERT JH. 2003. Distribuição e composição do ictioplâncton na quebra de plataforma do sul do Brasil. Atlântica 25: 75-86., Franco et al. 2006FRANCO BC, MUELBERT JH & MATA MM. 2006. Mesoscale physical processes and the distribution and composition of ichthyoplankton on the Southern Brazilian shelf break. Fish Oceanogr 15: 37-43., Katsuragawa et al. 2014KATSURAGAWA M, DIAS JF, HARARI J, NAMIKI C & ZANI-TEIXEIRA ML. 2014. Patterns in larval fish assemblages under the influence of the Brazil current. Cont Shelf Res 89: 103-117.), at the Northeastern region it is only inceptive.

The Northeastern Brazilian continental shelf concentrates many commercially and ecologically important species, such as the catfish, needlefish, tuna fish and others (Nóbrega & Lessa 2007NÓBREGA MF & LESSA RP. 2007. Description and composition of catches from the artisanal fishing fleet in Northeastern Brazil. Arq Cienc Mar 40: 64-74.). In the Northeast, although the fishery is intense, especially in the continental shelf (Nóbrega & Lessa 2007NÓBREGA MF & LESSA RP. 2007. Description and composition of catches from the artisanal fishing fleet in Northeastern Brazil. Arq Cienc Mar 40: 64-74.), there is scarcity of works focusing on the relationship among the ichthyoplankton distribution and physical-biological processes occurring in the region.

Based on this, the present work aims to investigate a potential gradient in the distribution and structure of the ichthyoplanktonic assemblage among the outer continental shelf and the deep continental slope, as well as the influence of the environmental variables over the ichthyoplankton at such domains.

MATERIALS AND METHODS

Study area

The neritic (shelf) and oceanic (slope) areas off the States of Pernambuco (PE), Paraíba (PB) and Rio Grande do Norte (RN) are located at the northwest South Atlantic. The continental shelf in the northeastern region of Brazil is on average 40 – 50 km wide and its depth is under 40 meters in most of its extension. The continental slope is on average 85 – 105 km wide, with a maximum width of 140 km in the adjacencies of the Pernambuco plateau. The continental rise is located between 4800 – 5200 meters’ depth (Coutinho 2009COUTINHO PN. 2009. Levantamento do estado da arte da pesquisa dos recursos vivos marinhos do Brasil. In: Hazin FHV (Ed). 2009. Oceanografia geológica. Fortaleza: Martins & Cordeiro 1: 138.).

The relief of the continental shelf is flat and alternated with a wavy bottom, fields of sandwaves and irregular features of calcareous algae (Coutinho 2009COUTINHO PN. 2009. Levantamento do estado da arte da pesquisa dos recursos vivos marinhos do Brasil. In: Hazin FHV (Ed). 2009. Oceanografia geológica. Fortaleza: Martins & Cordeiro 1: 138.). These areas are under the influence of warm waters belonging to the North Brazil Undercurrent (NBUC). The NBUC is the northern limb of the bifurcation of the south branch of the South Equatorial Current (sSEC), while the south limb becomes the Brazil Current (BC) (Veleda et al. 2012VELEDA D, ARAUJO M, ZANTOPP R & MONTAGNE R. 2012. Intraseasonal variability of the North Brazil Undercurrent forced by remote winds. J Geophys Res 117: 1-10., Stramma et al. 2005STRAMMA L, HÜTTL S & SCHAFSTALL J. 2005. Water masses and currents in the upper tropical northeast Atlantic off northwest Africa. J Geophys Res 110: 1-18.).

The NBUC flows below 50 m and may reach 900 m (Veleda et al. 2012VELEDA D, ARAUJO M, ZANTOPP R & MONTAGNE R. 2012. Intraseasonal variability of the North Brazil Undercurrent forced by remote winds. J Geophys Res 117: 1-10.). It presents a maximum flow in July and a minimum during the period of October to November, when its mean flow structure is well developed in the latitude of 11˚S (Schott et al. 2005SCHOTT FM, DENGLER M, ZANTOPP R, STRAMMA L, FISCHER J & BRANDT P. 2005. The shallow and deep western boundary circulation of the South Atlantic at 5˚–11˚S. J Am Meteorol Soc 35: 2031-2053.). In the proximities of the Equator, the east branch of the South Equatorial Current (eSEC) overlaps the nuclei of subsurface of the NBUC and forms the North Brazil Current (NBC), intensified at the surface (Stramma & England 1999STRAMMA L & ENGLAND M. 1999. On the water masses and mean circulation of the South Atlantic Ocean. J Geophys Res 104: 20863-20883.).

Collecting methods

The samplings were performed during the period of July and August of 2010 and 2012 aboard of the Brazilian Navy’s NHo Cruzeiro do Sul vessel, during the execution of the Camadas Finas I and II projects. Three transects of profiles perpendicular to the coastline were designed. The transect 1 (south) was located off the borders of the States of Pernambuco and Paraíba; the transect 2 (central) was located off the Paraíba State; and the transect 3 (north) was located off the borders of the States of Paraíba and Rio Grande do Norte. Each transect consisted of three stations positioned over different isobaths (Figure 1). One station was considered neritic and was located on the outer continental shelf (A), with depths varying between 40 – 70 m. The other stations were considered oceanic and were located on the upper continental slope (B), with depths varying between 200 – 500 m, and on the deep continental slope (C), with depths varying between 600 – 900 m. The samplings were performed at each station during the diurnal and nocturnal periods.

Figure 1
(a) Location of the study area in the South America and (b) positioning of the oceanographic stations in the regions of the outer continental shelf (A) and continental slope (B and C) in the western Tropical Atlantic, Brazil.

A Seabird 9 Plus CTD was used to obtain temperature, salinity, dissolved oxygen, fluorescence and water density profiles. Measurements of current flow speed and direction were obtained throughout the whole area among the transects by means of an Ocean Surveyor Broadband/Narrowband ADCP (Acoustic Douppler Current Profiler).

The ichthyoplankton was sampled through diurnal and nocturnal double oblique tows from surface to 200 m on the continental slope or to a depth at 10 m from the bottom on the continental shelf to prevent the equipment from damage. The depth of the Bongo was controlled by calculating the amount of necessary towing cable to be lowered on the water by correcting for the inclination angle using an inclinometer. On the continental slope, the Bongo was lowered once and on the continental shelf the Bongo was lowered twice to increase the volume of water filtered. The Bongo was equipped with nets of 500 µm and 300 µm mesh size and had an opening diameter of 60 cm. A flowmeter was attached to the mouth of the bongo net to assess the total volume filtered by the tow. The samples were fixed in borax-neutralized formaldehyde in a final concentration of 4%. Only the samples collected with the 500 µm net were considered, yielding a total of 36 analyzed unity samples.

All larvae were sorted under the stereomicroscope and identified to the lowest possible taxonomic level with basis on the specialized literature (e.g. Neira et al. 1998NEIRA FJ, MISKIEWICZ AG & TRNSKI T. 1998. Larvae of temperate Australian fishes: laboratory guide for larval fish identification. Nedlands: University of Western Australia Press, 474 p., Leis & Carson-Ewart 2002LEIS JM & CARSON-EWART BM. 2002. In situ settlement behavior of damselfish (Pomacentridae) larvae. J Fish Biol 61: 325-346., Richards 2006RICHARDS WJ. 2006. Early Stages of Atlantic Fishes: An Identification Guide for the Western Central North Atlantic. Florida: CRC Press 1-2: 2640 .). All larvae were deposited in the Ichthyoplankton Collection (COLICT) of the Museu de Oceanografia Petrônio Alves Coelho (MOUFPE) of the Universidade Federal de Pernambuco (UFPE). For all the individuals, a morphometric, meristic and morphologic characterization was performed, and linear dimensions were measured using a micrometric ocular, aiming to help in the identification process. The individuals were sorted in relation to the degree of the notochord flexion (pre-flexion, flexion and post-flexion stages), according to Miller & Kendall Jr. (2009).

Data analysis

The species richness was calculated using the Margalef index (Margalef 1957MARGALEF R. 1957. La teoria de la informacion en ecologia. Mem Real Acad Ciencias Artes Barcelona 32: 373-449.) (DMg ), the specific diversity index (H’) according to Shannon (1948)SHANNON CEA. 1948. Mathematical Theory of Comunication. Bell Syst Tech J 27: 379-423. and the equitability (J’) according to Pielou (1984)PIELOU EC. 1984. The Interpretation of Ecological Data: A Primer on Classification and Ordination. New York: Wiley, 1st ed., 263 p..

The comparisons of the total density of fish eggs and larvae, as well as of the DMg , H’ and J’ between isobaths, years and day period were carried out by means of the Fisher-Pitman permutation test. A total of 4999 permutations were performed using the Monte-Carlo resampling procedure. The Fisher-Pitman permutation test has the advantage of being free of the assumptions underlying the parametric correspondent F test.

The method of the non-parametric permutational multivariate analysis of variance (PERMANOVA) (Anderson 2001ANDERSON MJ. 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecol 26: 32-46.) was used to investigate the existence of differences in the structure of the fish larvae assemblage in relation to the sampled distances (outer continental shelf and continental slope), day period (diurnal and nocturnal periods) and transects (1, 2 and 3). The PERMANOVA was performed with basis on a Hellinger distance matrix, which is the Euclidian distance calculated on the biological matrix transformed by Hellinger, as described in Legendre & Gallagher (2001)LEGENDRE P & GALLAGHER ED. 2001. Ecologically meaningful transformations for ordination of species data. Oecologia 129: 271-280.. This distance was adopted since its use has been recommended for community composition data. A total of 999 permutations were performed. Prior to the PERMANOVA, an analysis of multivariate homogeneity of groups dispersions (Anderson 2006ANDERSON MJ. 2006. Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62: 245-253.) was performed to test if the assumption of homogenous groups dispersions was fulfilled. As the PERMANOVA is sensitive to differences in the dispersion of the observations (Anderson 2001ANDERSON MJ. 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecol 26: 32-46.), the analysis was performed only in those cases in which the groups dispersions were homogenous.

Aiming to investigate the existence of species associated to individual or combinations of isobaths an Indicator Value analysis (IndVal) (Dufrêne & Legendre 1997DUFRÊNE M & LEGENDRE P. 1997. Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol Monogr 67: 345-366.) extended for combination of groups (de Cáceres et al. 2010DE CÁCERES M, LEGENDRE P & MORETTI M. 2010. Improving indicator species analysis by combining groups of sites. Oikos 119: 1674-1684.) was performed. The significance of the associations of the species and isobaths was tested by means of permutation tests based on 999 permutations.

To investigate the existence of groups of species association, a non-hierarchical cluster analysis was performed in R mode using species that occurred at least twice on the samples. The method of the k means partitioning was adopted and different numbers of groups were considered in the analysis. For each number of groups tested, 100 initial random configurations were used. The Calinski-Harabasz criterion was adopted to define the best number of groups of species association and the Kendall coefficient of concordance W was calculated for each group and tested for significance by means of a permutation test (Legendre 2005LEGENDRE P. 2005. Species associations: the Kendall coefficient of concordance revisited. J Agric Biol Environ Stat 10: 226-245.).

All the univariate and multivariate statistical analyses were performed using the R (R Core Team 2016R CORE TEAM. 2016. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at https://www.R-project.org. Accessed on 10th October 2018.
https://www.R-project.org...
) and RStudio Softwares implemented with the packages “coin” (Hothorn et al. 2008HOTHORN T, HORNIK K, WIEL MA & ZEILEIS A. 2008. Implementing a class of permutation tests: the coin package. J Stat Softw 28: 1-23.), “indicspecies” (de Cáceres & Legendre 2009) and “vegan” (Oksanen et al. 2016).

RESULTS

Hydrography

There was little variation in temperature and salinity among the different transects, which characterizes a general pattern of warm surface waters with a thermocline beginning at 75 – 100 m at the continental slope areas. On the continental shelf, no thermocline was found.

The amplitude variation of the fluorescence values was narrower at the outer continental slope area (with minimum values varying between 0.07 and 0.31 µg L-1 and maximum values varying between 0.11 and 0.95 µg L-1). At the continental slope areas, minimum values of fluorescence between 0.00 and 0.12 µg L-1 and maximum values of fluorescence between 0.40 and 1.05 µg L-1 were detected. At most of the stations over the continental slope areas, the fluorescence peaks coincided with the depth of onset of the thermocline (75 – 100 m). In a few cases, the fluorescence peak was slightly above or under the depth of onset of the thermocline. At the continental shelf area, the fluorescence maximum was always close to the bottom (45 – 58 m).

Two water masses were found throughout the sampled isobaths, the Tropical Surface Water (TSW), which presents temperature values higher than 20˚C and salinity higher than 36, and the South Atlantic Central Water (SACW), which presents temperature values between 6 and 20˚C and salinity between 34.5 and 36. On the continental shelf stations, only the TSW was found and it extended from the surface to the bottom. At the continental slope stations, the TSW and SACW were present. The TSW extended from the surface to a depth of 115 – 177 m and the SACW occurred from a depth ranging between 123 and 179 m and extended to the deepest sampled depths (200 m).

The surface circulation pattern has not varied throughout the transects and isobaths. Comparing the years, however, there was a slight variation on the intensity and direction of the current. In 2010, the surface current flowed northward-northwestward with a small inclination angle in relation to the magnetic north (i.e., alongshore) and slightly stronger flux, with speeds of approximately 0.5 m s-1 (Figure 2). In 2012, the surface current flowed basically westward towards the coastline (i.e., onshore), throughout the whole study area, with a mean current speed of 0.3 m s-1.

Figure 2
Surface circulation pattern (30 m) in the area between the transects during the sampling periods of 2010 and 2012.

Ichthyoplanktonic assemblage and spatial distribution

A total of 4023 fish eggs and 1634 fish larvae were collected and these represented 59 families, 91 genus and 76 species (Table I). Regarding the stage of notochord flexion, most of the larvae were in the flexion stage (62.4%), followed by the pre-flexion stage (33.3%) and post-flexion stage (1.3%). A portion of 3% of the larvae were damaged and could not be classified according to the stage of notochord flexion. Most of the larvae in the flexion stage were found on the deep continental slope (45.5%), and on the upper continental slope (40.3%), with the remaining 12.2% on the outer continental shelf. In the pre-flexion stage, the pattern was the same with 45.5% on the deep continental slope, and 35.4% on the upper continental slope and 19.1% on the outer continental shelf. In relation to the post-flexion stage, most of the larvae concentrated on the deep continental slope (55%), followed by the outer continental shelf (25%) and upper continental slope (20%).

Table I
List of taxonomic groups, frequency of occurrence (%) and mean density in the isobaths A (outer continental shelf), B (upper continental slope) and C (deep continental slope). FO – frequency of occurrence; – average density (ind. 100 m-3); MD – maximum density (ind. 100 m-3); n.i. – non-identified at the species level.

The most frequent species were Diaphus sp. 1 (82.4%), Diaphus sp. 2 (67.7%), Decapterus punctatus (41.2%), Lampadena sp. 2 and Sparisoma sp. (35.3%). The species Diaphus sp. 1 was the most abundant in the transects 1 (31%) and 2 (30%), while the family Sciaenidae was the most abundant in the transect 3 (18.7%).

At the outer continental shelf, the taxonomic groups that prevailed were mainly demersal and pelagic fishes belonging to families such as Sciaenidae (max. of 28.8 larvae 100 m-3), Serranidae (average 0.9 larvae 100 m-3; max. of 6.3 larvae 100 m-3), Mullidae (max. of 6.3 larvae 100 m-3), among other families associated to coral reefs (Holocentridae, Sygnathidae, Apogonidae) and species associated to estuaries such as Opisthonema oglinum and Dormitator maculatus. However, oceanic and bathypelagic species belonging to the genera Diaphus and Lampadena (Myctophidae) also occurred.

The areas of the continental slope, on the other hand, were more characterized by the presence of oceanic mesopelagic and bathypelagic taxonomic groups. The species Diaphus sp. 1 (max. of 26.7 larvae 100 m-3) and Lampadena spp. (max. of 1.5 larvae 100 m-3), in addition to non-identified myctophids (max. of 24.2 larvae 100 m-3), presented an increase in density towards the oceanic areas. Furthermore, several oceanic species occurred exclusively in the continental slope areas, such as Lestidium atlanticum, Cyclothone braueri, Hygophum reinhardtii, Myctophum asperum, Chiasmodon niger, Katsuwonus pelamis, Ranzania laevis, among other. The number of taxonomic groups occurring in the continental slope was considerably higher than the number occurring in the outer continental shelf and this trend was statistically confirmed.

The species richness (DMg ) was significantly higher at the continental slope areas (Fisher-Pitman permutation test, p < 0.05). At these areas, the DMg values varied between 0.75 and 13.7 with averages of 5.7 and 6.6 at the upper and deep continental slope, respectively. At the outer continental shelf, it varied between 0 and 7.7, with an average of 3.1. The period of day and the year of sampling had no effect on the species richness. No difference in the values of species diversity (H’) and equitability (J’) was found among the outer continental shelf and the upper and deep continental slope areas. The day period, as well as the year of sampling had also no effect on H’ and J’.

The spatial distribution of the fish eggs was not homogenous throughout the outer continental shelf and continental slope areas and considerably higher values were found on the outer continental shelf (Fisher-Pitman permutation test, p < 0.05; Figure 3). An average of 182.5 eggs 100 m-3 (median of 167 eggs 100 m-3) was found on the outer continental shelf, with minimum and maximum values of 9.7 and 428 eggs 100 m-3, respectively. On the upper continental slope, an average of 47.2 eggs 100 m-3 (median of 20.4 eggs 100 m-3), with minimum of 0.3 and maximum of 249.4 eggs 100 m-3 was found. On the deep continental slope, an average of 7.7 eggs 100 m-3 (median of 5 eggs 100 m-3), with minimum of 0 and maximum of 25.7 eggs 100 m-3 was found.

Figure 3
Spatial distribution of fish eggs and larvae (100 m-3) across the outer continental shelf – deep continental slope areas during 2010 (left) and 2012 (right). The empty circles represent the diurnal period and the gray-filled circles represent the nocturnal period. The area of the circles is proportional to the density values. The x represents missing data (damaged net).

This pattern of decrease in density values from the outer continental shelf towards the continental slope was not observed for the fish larvae (Fisher-Pitman permutation test, p > 0.05; Figure 3). Nevertheless, higher values of total density of fish larvae were observed during the nocturnal period (Fisher-Pitman permutation test, p < 0.05), as well as different community structures during the diurnal and nocturnal periods (PERMANOVA, p < 0.05). An average of 12.8 larvae 100 m-3 (median of 11.2 larvae 100 m-3) was found during the diurnal period, with a minimum of 1.5 and maximum of 37.2 larvae 100 m-3. During the nocturnal period, an average of 23.2 larvae 100 m-3 (median of 15 larvae 100 m-3), with a minimum of 1.5 and maximum of 76.8 larvae 100 m-3 was found.

Species association and indicator value

Three groups of species association were found and could be described as a neritic, an oceanic and a transition group (Table II). The transition group was composed by neritic and oceanic species. All the groups were significant (permutation test, p < 0.01), which means that within all groups there were species positively correlated among each other.

Table II
Groups of species association found with the k means partitioning.

The indicator value analysis (IndVal) revealed the existence of five ecological indicators for the upper and deep continental slope areas (Table III). Melanostomiidae and Scorpaena sp. were specifically related to the upper continental slope (isobath B), while Lestidium atlanticum and Lampadena sp. were specifically related to the deep continental slope (isobath C). The species Diaphus sp. 1 was related to both continental slope areas (isobaths B + C).

Table III
Ecological indicators of the continental slope area. IndVal – statistic value of the test; p – permutation p value.

DISCUSSION

This study investigated the ichthyoplankton community structure in western Tropical Atlantic areas close to the shelf break (outer continental shelf and continental slope), as well as its relationship with the abiotic variables. It was possible to observe that there was a higher concentration of fish eggs and a predominance of larvae at pre-flexion and flexion stages of notochord development at the outer continental shelf, which indicates a possible spawning process in this area. The NBUC flowed towards the coast, which may have contributed to the movement of these organisms towards the outer continental shelf.

Ichthyoplankton distribution

In general, the waters in tropical regions were characterized by the presence of a permanent thermocline (Travassos et al. 1999TRAVASSOS P, HAZIN FHV, ZAGLAGIA JR, ADVÍNCULA R & SCHOBER J. 1999. Thermohaline structure around seamounts and islands off North-Eastern Brazil. Arch Fish Mar Res 47: 211-222.) caused by the high solar incidence throughout the year, making these waters warm and oligotrophic (Ekau et al. 1999EKAU W, WESTHAUS-EKAU P & MEDEIROS C. 1999. Large scale distribution of fish larvae in the continental shelf waters off North-East Brazil. Arch Fish Mar Res 47: 183-200.).

The study area is characterized by presenting low values of biological productivity, as indicated by the low chlorophyll-a concentrations (ranging from 0.46 to 1.65 µg L-1) previously observed (Souza et al. 2013SOUZA CS, LUZ JAG, MACEDO S, MANUEL JFM & MAFALDA JR PO. 2013. Chlorophyll a and nutrient distribution around seamounts and islands of the tropical south-western Atlantic. Mar Freshw Res 64: 168-184.). Unfortunately, the western South Atlantic remain poorly known and no estimate of primary production for the study area using 14C technique is available. According to Longhurst et al. (1995)LONGHURST A, SATHYENDRANATH S, PLATT T & CAVERHILL C. 1995. An Estimate of global primary production in the ocean from satellite radiometer data. J Plan Res 17: 1245-1271., the study area is characterized by a low value of 75 g C m-2 y-1. However, in areas of continental shelf break, the development of mesoscale physical mechanisms – such as meanders and eddies – is possible and may allow a higher retention of the plankton leading to a higher concentration of planktonic density and biomass (e.g. Franco et al. 2006FRANCO BC, MUELBERT JH & MATA MM. 2006. Mesoscale physical processes and the distribution and composition of ichthyoplankton on the Southern Brazilian shelf break. Fish Oceanogr 15: 37-43., Okazaki & Nakata 2007OKAZAKI Y & NAKATA H. 2007. Effect of the mesoscale hydrographic features on larval fish distribution across the shelf break od East China Sea. Cont Shelf Res 27: 1616-1628., Katsuragawa et al. 2014KATSURAGAWA M, DIAS JF, HARARI J, NAMIKI C & ZANI-TEIXEIRA ML. 2014. Patterns in larval fish assemblages under the influence of the Brazil current. Cont Shelf Res 89: 103-117.). In addition, processes such as the formation of eddies, as an example, may retain fish larvae at its surrounding and transport the larvae to other areas influencing the assemblage abundance and composition (Franco et al. 2006FRANCO BC, MUELBERT JH & MATA MM. 2006. Mesoscale physical processes and the distribution and composition of ichthyoplankton on the Southern Brazilian shelf break. Fish Oceanogr 15: 37-43.).

There was a significantly higher concentration of fish eggs at the outer continental shelf and this may be associated with the predominant current – NBUC – which was flowing towards the coast and could have contributed to the transport of these eggs towards the continental shelf. The swimming capability of the yolk-sac larvae is low and absent for eggs (Purcell & Arai 2001PURCELL JE & ARAI MN. 2001. Interactions of pelagic cnidarians and ctenophores with fish: A review. Hydrobiologia 451: 27-44.), leaving the latter completely dependent upon the movement of the current. Although no spatial distribution pattern for the larvae could be statistically determined, most of these might also have been under influence of the current, since most of the larvae were in the first stages of flexion of the notochord and deprived of much swimming capability, which increases with age (Fisher 2005FISHER R. 2005. Swimming speeds of larval coral reef fishes: impacts on self-recruitment and dispersal. Mar Ecol Prog Ser 285: 223-232., Fisher et al. 2000FISHER R, BELLWOOD DR & JOB SD. 2000. Development of swimming abilities in reef fish larvae. Mar Ecol Progr Ser 202: 163-173.). Alternatively, the mixture of larval fish taxa may have obscured the spatial pattern of fish larvae when seen as a whole.

A higher concentration of eggs in the region of the outer continental shelf may also be related to a spawning strategy in response to favorable environmental conditions (Franco & Muelbert 2003FRANCO BC & MUELBERT JH. 2003. Distribuição e composição do ictioplâncton na quebra de plataforma do sul do Brasil. Atlântica 25: 75-86., Okazaki & Nakata 2007OKAZAKI Y & NAKATA H. 2007. Effect of the mesoscale hydrographic features on larval fish distribution across the shelf break od East China Sea. Cont Shelf Res 27: 1616-1628.), such as an increase in the phytoplanktonic production (González-Quirós et al. 2003GONZÁLEZ-QUIRÓS R, CABAL J, ÁLVAREZ-MARQUÉS F & ISLA A. 2003. Ichthyoplankton distribution and plankton production related to the shelf break at the Avilés Canyon. ICES J Mar Sci 60: 198-210.) and a higher availability of prey for the future larvae (Boehlert & Mundy 1994BOEHLERT GW & MUNDY BC. 1994. Vertical and onshore-offshore distributional patterns of tuna larvae in relation to physical habitat features. Mar Ecol Prog Ser 107: 1-13.). Indeed, fluorescence measures indicated that the lowest availability of phytoplanktonic cells at the outer continental shelf was higher than its lowest availability at the continental slope areas. Furthermore, stomach content analyses are also revealing that these larvae are feeding on microplanktonic organisms such as centric and pennate diatoms, as well as tintinnid ciliates ( JR Santana, unpublished data). Another possibility is that spawning in the shelf break during a given time may aid to transport eggs and larvae to a nursery ground found in another place, as has been observed in other areas (e.g. Landaeta & Castro 2002LANDAETA MF & CASTRO LR. 2002. Spring spawning and early nursery zone of the mesopelagic fish Maurolicus parvipinnis at the coastal upwelling zone off Talcahuano, central Chile. Mar Ecol Prog Ser 226: 179-191.).

The ability of fish larvae and other zooplanktonic organisms – such as copepods and decapods – to avoid net sampling is a long-known phenomenon (e.g. Ahlstrom 1954AHLSTROM EH. 1954. Distribution and abundance of egg and larval populations of the Pacific sardine. Fish Bull 56: 83-140., Bridger 1956BRIDGER JP. 1956. On day and night variation in catches of fish larvae. ICES J Mar Sci 22: 42-57.). During the night, the catches were significantly higher than during the day, e.g. night/day ratios of 1.62:1 (Morse 1989MORSE WW. 1989. Catchability, growth, and mortality of larval fishes. Fish Bull 87: 417-446.) and 15.2:1 (Bridger 1956BRIDGER JP. 1956. On day and night variation in catches of fish larvae. ICES J Mar Sci 22: 42-57.). The higher total density values observed during the nocturnal period are in agreement with these estimates, since an average night/day ratio of 1.53:1 was estimated for the study area.

Taxonomic composition

The high abundance of the family Myctophidae at oceanic regions of the western South Atlantic was previously observed (e.g. Franco & Muelbert 2003FRANCO BC & MUELBERT JH. 2003. Distribuição e composição do ictioplâncton na quebra de plataforma do sul do Brasil. Atlântica 25: 75-86., Franco et al. 2006FRANCO BC, MUELBERT JH & MATA MM. 2006. Mesoscale physical processes and the distribution and composition of ichthyoplankton on the Southern Brazilian shelf break. Fish Oceanogr 15: 37-43., Katsuragawa et al. 2014KATSURAGAWA M, DIAS JF, HARARI J, NAMIKI C & ZANI-TEIXEIRA ML. 2014. Patterns in larval fish assemblages under the influence of the Brazil current. Cont Shelf Res 89: 103-117.). Myctophidae is a characteristically oceanic and mesopelagic family (Franco & Muelbert 2003FRANCO BC & MUELBERT JH. 2003. Distribuição e composição do ictioplâncton na quebra de plataforma do sul do Brasil. Atlântica 25: 75-86., Katsuragawa et al. 2014KATSURAGAWA M, DIAS JF, HARARI J, NAMIKI C & ZANI-TEIXEIRA ML. 2014. Patterns in larval fish assemblages under the influence of the Brazil current. Cont Shelf Res 89: 103-117.), associated with the Tropical Water (TW) and very abundant at the continental shelf break, as well as at oceanic areas (Franco & Muelbert 2003FRANCO BC & MUELBERT JH. 2003. Distribuição e composição do ictioplâncton na quebra de plataforma do sul do Brasil. Atlântica 25: 75-86.).

A non-identified species of the genus Diaphus was the most abundant species at the studied area, occurring in all the stations and being classified as an indicator species of the continental slope areas (isobaths B and C). Diaphus is an oceanic genus, which belongs to the family Myctophidae and is also associated to the TW (Franco & Muelbert 2003FRANCO BC & MUELBERT JH. 2003. Distribuição e composição do ictioplâncton na quebra de plataforma do sul do Brasil. Atlântica 25: 75-86.), since it is common in waters with higher temperature values (Okazaki & Nakata 2007OKAZAKI Y & NAKATA H. 2007. Effect of the mesoscale hydrographic features on larval fish distribution across the shelf break od East China Sea. Cont Shelf Res 27: 1616-1628.). Although the genus is oceanic, its larvae and adult forms also occur over the inner and outer continental shelf, with a vertical distribution relatively superficial (Okazaki & Nakata 2007OKAZAKI Y & NAKATA H. 2007. Effect of the mesoscale hydrographic features on larval fish distribution across the shelf break od East China Sea. Cont Shelf Res 27: 1616-1628.). Diaphus may be found between 20 and 30 m (Sassa et al. 2002SASSA C, MOSER HG & KAWAGUCHI K. 2002. Horizontal and vertical distribution patterns of larval Myctophid fishes in the Kuroshio Current region. Fish Oceanogr 11: 1-10.), what explains the fact that it was so well distributed across the studied area.

Several taxonomic groups occurred exclusively at the continental slope areas and formed a group of associated species common to the continental slope, as Lestidium atlanticum (Paralepididae) and Cyclothone braueri (Gonostomatidae). Lestidium atlanticum was one of the deep continental slope indicator species. This result agrees with Okazaki & Nakata (2007)OKAZAKI Y & NAKATA H. 2007. Effect of the mesoscale hydrographic features on larval fish distribution across the shelf break od East China Sea. Cont Shelf Res 27: 1616-1628., which state that species belonging to the family Paralepididae and of the genus Cyclothone would probably not be affected by fronts and eddies, since according to Sassa et al. (2002)SASSA C, MOSER HG & KAWAGUCHI K. 2002. Horizontal and vertical distribution patterns of larval Myctophid fishes in the Kuroshio Current region. Fish Oceanogr 11: 1-10., both taxa are related with a deep vertical distribution.

The neritic taxonomic groups of the present study are also associated by its ecology and most of them were concentrated at the outer continental shelf. The main families were Carangidae, Sciaenidae, Mullidae, Serranidae, Syngnathidae, Clupeidae, Lutjanidae, among other. Adult individuals of the families Sciaenidae, Carangidae, Serranidae, Clupeidae and Bothidae are abundant at Brazilian’s continental shelf areas (Haimovici et al. 1996HAIMOVICI M, MARTINS AS & VIEIRA PC. 1996. Distribuição e abundância de peixes teleósteos demersais sobre a plataforma continental do sul do Brasil. Rev Bra Bio 56: 27-50.). Thus, both larvae and adult individuals are well distributed over the continental shelf. Many of these groups were represented by species known to be associated with reef environments, such as Acanthurus sp., Caranx crysus, Caranx sp. and Myripristes jacobus, as well as species known to be associated to estuaries, e.g. Opisthonema oglinum (Lessa & Nóbrega 2000LESSA R & NÓBREGA MF. 2000. Guia de identificação de peixes marinhos da região Nordeste. Programa REVIZEE/SCORE-NE - UFRPE-DIMAR, Recife, 128 p.).

Among the neritic families, Carangidae was one of the most abundant and the species Decapterus punctatus was the one with the broadest distribution. The distribution of this species extends from the coast at approximately 16 m to the continental shelf break and may even reach the oceanic zone (Katsuragawa & Matsuura 1992KATSURAGAWA M & MATSUURA Y. 1992. Distribution and abundance of Carangid Larvae in the Southeastern Brazilian Bight during 1975–1981. Bol Inst Oceanogr São Paulo 40: 55-78., Souza & Mafalda Jr 2008). This species was pointed out as the most abundant in the neritic zone of the northeastern region of Brazil (Souza & Mafalda Jr 2008).

A continental shelf-slope gradient in the composition of the fish larvae assemblage was clear because of the formation of a neritic, an oceanic and a transition species association group, the last with neritic and oceanic species. This pattern was registered by other authors (Ekau et al. 1999EKAU W, WESTHAUS-EKAU P & MEDEIROS C. 1999. Large scale distribution of fish larvae in the continental shelf waters off North-East Brazil. Arch Fish Mar Res 47: 183-200., Franco & Muelbert 2003FRANCO BC & MUELBERT JH. 2003. Distribuição e composição do ictioplâncton na quebra de plataforma do sul do Brasil. Atlântica 25: 75-86., Katsuragawa et al. 2014KATSURAGAWA M, DIAS JF, HARARI J, NAMIKI C & ZANI-TEIXEIRA ML. 2014. Patterns in larval fish assemblages under the influence of the Brazil current. Cont Shelf Res 89: 103-117.).

Species richness increased towards oceanic waters. According to Franco & Muelbert (2003)FRANCO BC & MUELBERT JH. 2003. Distribuição e composição do ictioplâncton na quebra de plataforma do sul do Brasil. Atlântica 25: 75-86., when there is a predominance of the TSW and SACW water masses over the Brazilian south continental shelf, there is an increase in the number of fish families. This may explain the increase in species richness towards the oceanic waters, since at the upper and deep continental slope areas (isobaths B and C), both the TSW and the SACW are present. In addition to water masses, physical processes such as eddies also interfere in the composition of fish larvae assemblage (Katsuragawa et al. 2014KATSURAGAWA M, DIAS JF, HARARI J, NAMIKI C & ZANI-TEIXEIRA ML. 2014. Patterns in larval fish assemblages under the influence of the Brazil current. Cont Shelf Res 89: 103-117.). Anticyclonic eddies that are present in the Brazilian south continental shelf, as an example, transport Engraulidae, Bregmacerotidae and Carangidae larvae from one place to other (Franco & Muelbert 2003FRANCO BC & MUELBERT JH. 2003. Distribuição e composição do ictioplâncton na quebra de plataforma do sul do Brasil. Atlântica 25: 75-86., Franco et al. 2006FRANCO BC, MUELBERT JH & MATA MM. 2006. Mesoscale physical processes and the distribution and composition of ichthyoplankton on the Southern Brazilian shelf break. Fish Oceanogr 15: 37-43.).

The present study indicated that in the northeast region of Brazil, the outer continental shelf is an important area of concentration of fish eggs and larvae at early stages, which indicates a spawning area. The North Brazil Undercurrent may aid in the transport of these organisms towards the continental shelf, once they have low or no swimming capability. The distribution and composition of the fish larvae were influenced by the spatial-temporal variables leading to the formation of three species association groups. A neritic group representing the outer continental shelf, an oceanic group representing the continental slope, and a transition group formed by neritic and oceanic species.

ACKNOWLEGMENTS

This work is a contribution of the Projects Camadas Finas I and II. The Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) supported JRS with a PhD scholarship, and RS with a productivity fellowship. The Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) supported AESFC with a PhD scholarship. The authors acknowledge Dr. Werner Ekau for his critical review of the manuscript, which has led to a significant improvement of its quality; the Marinha do Brasil and the crew members and researchers aboard of the NHO Cruzeiro do Sul for their support in the fieldwork; and the Ministério da Ciência e Tecnologia (MCT), INCT AmbTropic (CNPq/CAPES/FAPESB), and the Departamento de Oceanografia of the Universidade Federal de Pernambuco for providing facilities and support.

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Publication Dates

  • Publication in this collection
    05 June 2020
  • Date of issue
    2020

History

  • Received
    17 Aug 2018
  • Accepted
    17 Dec 2018
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