Vertical distribution of benthic invertebrate larvae during an upwelling event along a transect off the tropical Brazilian continental margin

Journal of Marine Systems 79 (2010) 124–133

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Journal of Marine Systems j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / j m a r s y s

Vertical distribution of benthic invertebrate larvae during an upwelling event along a transect off the tropical Brazilian continental margin Marcos Y. Yoshinaga a,⁎,1, Paulo Y.G. Sumida a, Ilson C.A. Silveira a, Áurea M. Ciotti b, Salvador A. Gaeta a, Luiz F.C.M. Pacheco a, Andréa G. Koettker a a b

Instituto Oceanográfico da Universidade de São Paulo, São Paulo, CEP: 05508-120, Brazil UNESP Campus do Litoral Paulista. Praça Infante Dom Henrique s/n° São Vicente, SP, CEP: 11330-900, Brazil

a r t i c l e

i n f o

Article history: Received 18 September 2008 Received in revised form 21 July 2009 Accepted 22 July 2009 Available online 6 August 2009 Keywords: SE Brazilian coast (23°S and 42°W) Shelf dynamics Coastal upwelling Zooplankton Invertebrate larvae

a b s t r a c t Abundance and composition of marine benthic communities have been relatively well studied in the SE Brazilian coast, but little is known on patterns controlling the distribution of their planktonic larval stages. A survey of larval abundance in the continental margin, using a Multi-Plankton Sampler, was conducted in a cross-shelf transect off Cabo Frio (23°S and 42°W) during a costal upwelling event. Hydrographic conditions were monitored through discrete CDT casts. Chlorophyll-a in the top 100 m of the water column was determined and changes in surface chlorophyll-a was estimated using SeaWiFS images. Based on the larval abundances and the meso-scale hydrodynamics scenario, our results suggest two different processes affecting larval distributions. High larval densities were found nearshore due to the upwelling event associated with high chlorophyll a and strong along shore current. On the continental slope, high larval abundance was associated with a clockwise rotating meander, which may have entrapped larvae from a region located further north (Cabo de São Tomé, 22°S and 41°W). In mid-shelf areas, our data suggests that vertical migration may likely occur as a response to avoid offshore transport by upwelling plumes and/or cyclonic meanders. The hydrodynamic scenario observed in the study area has two distinct yet extremely important consequences: larval retention on food-rich upwelling areas and the broadening of the tropical domain to southernmost subtropical areas. © 2009 Elsevier B.V. All rights reserved.

1. Introduction The vast majority of marine benthic invertebrate groups possess a planktonic larval stage, which can spend from hours to months in the water column before settling on a suitable habitat (Thorson, 1950). The distribution of adult populations is a direct consequence of larval dispersal and survival (Shanks, 1995), and over the past 20 years, efforts have been made to investigate the interactions among physical oceanography, larval distribution, dispersal and recruitment of larvae (Roughgarden et al., 1991; Poulin et al., 2002; Shanks and Eckert, 2005; Shanks and Brink, 2005). Spatial and temporal patterns in larval distribution can be explained through a number of different processes, such as physical advection of larvae and the local production of larval food (Nakata et al., 2000; Botsford, 2001; Garland et al., 2002; Poulin et al., 2002). The ability to control larval vertical position will affect the net transport for a particular species (Shanks, 1995), as behavioral patterns in conjunction to physical processes will determine whether ⁎ Corresponding author. Tel.: +55 11 30916543. E-mail address: [email protected] (M.Y. Yoshinaga). 1 Present Address: MARUM, University of Bremen, Leobener Straße, 28359 Bremen, Germany. 0924-7963/$ – see front matter © 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.jmarsys.2009.07.007

larvae are exported, retained, or concentrated in specific locations (Clough et al., 1997; Cowen et al., 2000; Paris et al., 2002). Cross-shelf transport of larvae has been attributed to wind-driven drifting, internal tidal waves, meso- and large-scale circulation features, and upwelling and downwelling (e.g., Roughgarden et al., 1991; Shanks, 1995; Nakata et al., 2000; Botsford, 2001; Poulin et al., 2002; Shanks and Eckert, 2005; Ma et al., 2006; dos Santos et al., 2008). The effects of upwelling or downwelling on larval distribution can be accessed from the knowledge of vertical distribution of larvae (Shanks and Brink, 2005). The upwelling system of Cabo Frio is an important site of primary productivity in the Brazilian coast (Gonzalez-Rodriguez et al., 1992; Gonzalez-Rodriguez, 1994), although it is generally considered weak compared to eastern boundary coastal upwelling systems. Here, we present data on vertical distribution of benthic invertebrate larvae during a coastal upwelling event off the tropical Brazilian coast (Cabo Frio, between 22°58'S, 42°03'W and 24°33'S, 41°23'W) and its relationship to local oceanographic conditions during repeated cross-shelf transects. Our goal is to provide some insights on probable mechanisms of larval dispersion in the area. Similar research was conducted in different oceanographic settings including the persistent upwelling off Chile (Poulin et al., 2002), the seasonal upwelling off the coast of California (e.g., Roughgarden et al., 1991; Wing et al., 1995),

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the vicinity of Cabo Frio, with upwelling cells and plumes frequently found southwards from Cabo Frio and Cabo de São Tomé, as well as northward (Lorenzzetti and Gaeta, 1996; Carbonel, 1998). This mechanism was described by Calado et al. (2006) as coastal waters excursions onto oceanic areas promoted by meanders of the BC.

and the weak upwelling off the central-east coast of the US (e.g., Shanks et al., 2000; Garland et al., 2002; Shanks et al., 2003; Shanks and Brink, 2005; Ma et al., 2006). Is worth to note that previous studies (Shanks et al., 2000; Garland et al., 2002; Poulin et al., 2002; Shanks and Brink, 2005; Ma et al., 2006) concentrated efforts within the first 30 km of the coast, directly influenced by the upwelling front. Our study was expanded to a region out to ~ 100 km from the coast, and consequently, deeper zones in the water column were sampled. We observed simultaneous occurrence of coastal upwelling and upwelling filaments flowing southwards from the coast at Cabo Frio, which may represent additional constrain to the distribution of benthic population along the boundary between tropical and subtropical domains in the SE Brazilian coast. Given the circulation scenario, we propose a physical/biological interaction that explains the association of benthic larvae in the water column and the specific hydrodynamic features of this region.

3. Methods Samples were collected during the multidisciplinary DEPROAS Experiment (Ecosystem Dynamics of the Southwest Atlantic Continental Shelf) in February 7th to 13th 2001 aboard the R/V Prof. W. Besnard (Oceanographic Institute, University of São Paulo). A total of 19 stations were sampled along a single transect, oriented perpendicular to Cabo Frio, which extended up to 200 km off the coast. The transect was visited four times and samples were collected at 3, 5 or 6 stations within a two-day average sampling per transect. Local depths varied from 40 to 2500 m, thus covering coastal, shelf and slope waters (Table 1 and Fig. 1). At each station, CTD casts and discrete water sampling were followed by deployments of a Multi-Plankton Sampler (MPS, 333 µm mesh size) set to sample five strata in the top 100 m of the water column (at 20 m intervals). In nearshore areas (b100 m depth) we sampled only 2–3 strata using 10 m intervals. Flow meters were used to compute the volume of water filtered in each net. Samples were preserved in 4% buffered seawater formalin, sorted under a stereomicroscope and the larvae were enumerated to major taxa (echinoderms, gastropods, bivalves, cirripedians, brachyurans, stomatopods and anomurans). Brachyuran larvae present in shelf and slope waters were identified to the lowest possible taxonomic level. Water samples for chlorophyll-a (chl-a) analysis were collected with Niskin bottles coupled to the CDT-rosette system. Water was filtered on board using GF/F filters and chl-a concentrations (mg m2) were measured fluorimetrically (Turner Designs AU-10) in the laboratory (Holm-Hansen et al., 1965) using 90% acetone and 24 h extraction. Surface chl-a was also estimated through satellite data. SeaWiFs radiometric data (Fig. 1) at Level 1A and nadir resolution of 1.1 km, as well as daily meteorological data, were obtained from the NASA GSFC's Distributed Active Archive Center (DAAC). Chl-a (mg m3) was estimated by the Oc2 version 4 algorithm using SEADAS 4.4 standard atmospheric correction and masks. Images were mapped to a cylindrical projection and colored coded to illustrate surface chlorophyll in mg m− 3 (Fig. 1).

2. Study site The upper 100 m of the water column of the Southeast Brazilian Bight (SBB, 23°S to 28°S) is influenced by three water masses: the Tropical Water (TW, T N 20° and S N 36.4) flowing as the surface expression of the Brazil Current (BC); the cold and nutrient rich South Atlantic Central Water (SACW, T b 20 °C and S b 36.4) flowing below TW and as the thermocline portion of the BC; and the Coastal Water (CW), a low salinity water resulting from fresh water input of small to medium sized estuaries along the SBB (Campos et al., 1996, 2000; Silveira et al., 2000). At Cabo Frio, the SBB is characterized by a relatively narrow shelf (~50 km wide) with an abrupt change (N–S to E–W) in coastline orientation (Campos et al., 2000; Rodrigues and Lorenzzetti, 2001). Under N–NE winds, which are common during summer and blow parallel to the coast in Cabo Frio, surface water moves offshore (via Ekman transport) resulting in the upwelling of SACW (Castro and Miranda, 1998). Blooms of phytoplankton are commonly observed as a consequence of SACW upwelling in coastal areas off Cabo Frio (Valentin, 1984; Gonzalez-Rodriguez et al., 1992). Matsuura (1996) studying the sardine spawning off the SE Brazilian coast identified the coastal upwelling of Cabo Frio as the key factor supporting the regional fisheries productivity. Except for Cabo Frio, primary production in continental shelf and open waters off the SBB can be considered under oligotrophic conditions, with a strong depletion of nutrients in the euphotic zone associated with the warm TW (Metzler et al., 1997). Alongshore variations are observed in

Table 1 Information on sampling date, time of the MPS, local depth, integrated chl-a, total larvae and individual major taxa densities for the first 100 m depth in each station sampled in this study. Station # Distance offshore Date (km)

Local time Depth chl-a Larvae Echinodermata Polychaeta Gastropoda Bivalvia Cirripedia Stomatopoda Brachyura (m) (mg m− 2) (ind. m− 3)

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19

7:55 PM 10:18 AM 2:47 PM 8:48 PM 5:12 AM 10:19 AM 8:05 PM 11:28 PM 3:27 AM 7:06 AM 12:45 PM 4:48 PM 8:57 PM 11:42 PM 4:45 AM 8:57 AM 1:02 PM 3:38 PM 9:25 PM

191 153 116 77 40 3 40 58 77 107 107 78 58 40 22 5 40 22 3

2/7/01 2/8/01 2/8/01 2/8/01 2/9/01 2/9/01 2/9/01 2/9/01 2/10/01 2/10/01 2/11/01 2/11/01 2/11/01 2/11/01 2/12/01 2/12/01 2/12/01 2/13/01 2/13/01

2474 1960 1191 160 120 40 123 142 160 713 708 161 145 122 116 40 123 113 36

13.5 14.0 12.0 11.8 22.2 45.0 19.4 18.5 12.9 15.8 19.2 14.9 18.4 31.3 19.6 35.2 15.6 16.1 37.2

22.1 6.2 2.4 6.5 18.4 29.2 20.8 49.2 4.8 5.6 7.2 2.3 9.8 12.8 66.9 18.0 24.4 26.1 5.4

4.0 0.4 0.4 0.1 0.0 0.0 0.1 0.0 0.0 0.0 0.1 0.0 0.1 0.0 0.3 0.1 0.0 0.0 0.0

1.9 1.5 0.6 0.5 0.7 0.1 0.7 0.3 0.0 0.5 0.5 0.3 0.5 0.2 2.8 0.0 0.2 0.1 0.2

14.4 3.6 1.1 5.7 14.9 0.0 8.6 8.1 3.2 4.6 4.7 1.4 7.5 6.5 47.6 0.2 19.0 5.6 0.3

1.3 0.3 0.0 0.0 0.1 0.0 0.3 0.0 0.1 0.0 0.1 0.1 0.1 0.0 0.4 0.0 0.1 0.4 0.1

0.2 0.0 0.0 0.0 0.1 0.1 4.3 39.5 0.4 0.1 0.0 0.1 0.0 0.2 0.7 0.0 2.1 0.3 0.2

0.0 0.1 0.0 0.0 0.7 19.6 0.9 0.1 0.1 0.1 0.5 0.1 0.5 0.3 0.5 4.9 0.9 0.9 1.1

0.3 0.1 0.1 0.2 1.8 8.2 5.9 1.2 0.8 0.3 1.4 0.3 1.1 4.8 14.6 12.5 1.8 17.7 3.5

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Fig. 1. SeaWiFS image from 02/13/2001 showing the study area transect and the depths sampled (open squares). 1 represents a plume of upwelled and chlorophyll rich water, 2 the coastal upwelling event under investigation, 3 and 4 the excursion of coastal waters to offshore areas.

A north-south velocity field (Fig. 2) was calculated from the observed temperature and salinity data in the DEPROAS Experiment, using the sectional version of the Princeton Ocean Model (POM). This method is detailed in Silveira et al. (2004) and was applied to the region off Cabo Frio. The dynamical interaction between coastal circulation and the meandering pattern of the BC in the DEPROAS Experiment of 2001 was also described by Calado et al. (2006).

Spearman's Rank correlation test was performed to identify possible relationships between distance offshore, percentage of the water column influenced by the SACW (T b 20 °C and S b 36.4, here after defined according to Silveira et al. (2000)), larvae densities and chl-a concentrations integrated for the upper 100 m. 4. Results 4.1. Physical oceanographic conditions, chl-a concentrations and larvae vertical distribution

Fig. 2. North-South current velocities during a coastal upwelling event off Cabo Frio (see Silveira et al., 2004). Negative velocities are southwestwards and contours intervals are 0.1 m s− 1.

Sampling was initiated on February 7th of 2001 at the offshore St. 1 (Table 1). Low bottom water temperatures and high chl-a concentrations in nearshore areas of the first transect (Fig. 3), as well as the satellite image from February 8th (Fig. 1), evidenced the presence of a coastal upwelling associated with a consistent bloom of phytoplankton. The north-south circulation pattern was computed only for the first transect since the time scales at which the velocity field evolved was slow compared to the duration of the DEPROAS Experiment (see details in Silveira et al., 2004). During the sampling of transect 1, there were two distinct flow patterns (Fig. 2). The first was the southward coastal current flow associated with the upwelling regime centered at approximately 20 km from the coast and occupying the first 20 m of the water column. We could also identify the vertical shear, with weaker bottom currents flowing in the opposite direction (Fig. 2). Off

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Fig. 3. Larval spatial distributions in transect #1. Upper two panels showing temperature (°C) and chlorophyll-a concentration (mg m− 3) profiles with dots representing total larval densities (ind. m− 3). Shaded areas represent stations sampled at night. Note that horizontal axes showing stations number (above) and the distance from the coast (below). Lower panels showing the vertical distribution of the four most abundant taxonomic groups in each station.

the shelf, a robust clockwise rotating BC meander was observed in areas 100 to 200 km offshore (Fig. 2). Corroborating this feature were both satellite sea surface temperature (Calado et al., 2006) and ocean color images showing an excursion of coastal waters from further north of Cabo Frio into the oceanic realm (Fig. 1). The abundances of larvae at St. 1 and St. 5 were higher than stations located at the outershelf or shelf-break areas of transect 1 (Table 1), and high larvae concentrations were observed in subsurface strata 20–40 m (Fig. 3). At St. 1, gastropods, followed by echinoderms, polychaetes and bivalves dominated larval abundance (Table 1). In fact, the three latter taxonomic groups were associated with offshore stations. High densities of those organisms at St. 1 (Fig. 3) were coincidently related to the external edge of the rotating meander of the BC (Figs. 1 and 2). Gastropods density was considerably higher than the other abundant taxa (brachyurans, polychaetes and stomatopods) in continental shelf areas (Table 1). The second sampling of the transect was initiated on 9 February at St. 6, located 3 km from the shore (Table 1), where SACW dominated the water column (Fig. 4). As during in the first transect, section 2 showed high chl-a concentrations within 60 km offshore (Figs. 3 and 4), mostly positioned close to the sea bottom (~70 m) where SACW was flowing towards the coast with the persistence of the upwelling event. The highest larval concentration was observed at St. 6 (Table 1), with stomatopods and brachyurans accounting for 97% of the sample, coinciding with high concentrations of chl-a (Fig. 4). At St. 7, the dominant taxa were gastropods, cirripedians and brachyurans. Most of

the larvae at St. 7 were found in surface waters, and decreased in abundance with depth (Fig. 4). At St. 8, the most abundant larvae were cirripedians (80.3%), which were mostly found at 80–100 m (Fig. 4). Larval concentrations at St. 9 and St. 10 were lower than at the shelf stations (Table 1). At St. 9, gastropod larvae were most abundant, although cirripedians and brachyurans were numerically important as well, with high numbers of individuals caught in the 80–100 m strata (Fig. 4). At St. 10, gastropods again were the most abundant (81.9%), however they were caught at greater depths than at stations St. 7 and St. 9 (Fig. 4). On 11 February, the section was visited a third time with sampling starting on the slope and progressing towards the coast (Fig. 5). In order to track the dynamics of the coastal upwelling event, the second and third sections were limited to 150 km offshore, and consequently stations located in areasN 1000 m depth were not visited. Gastropods followed by brachyurans were the most abundant larvae at stations St. 11, 12 and 13 (stations N 60 km from shore). At St. 11 those organisms were positioned in subsurface waters (20–60 m depth), in deeper layers at St. 12 (mostly in the strata 60–80 m, together with cirripedians), and in surface waters at St. 13 (Fig. 5). However, at St. 14, brachyurans occupied the first strata, whereas gastropods were more abundant at the 40–60 m layer (Fig. 5). While gastropods dominated the larval abundance at St. 15 (71.2%), brachyurans and stomatopods represented almost 99% of total larvae at St. 16 (Table 1 and Fig. 5). On 12 February the fourth transect covered ~100 km and larvae were only sampled at three stations within 40 km offshore (Fig. 6).

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Fig. 4. Same as Fig. 3 for transect #2.

The coastal upwelling event persisted throughout the DEPROAS Experiment, and as observed in transect 3 (Figs. 5 and 6), highest chl-a concentrations were associated with the SACW, both near the coast and in subsurface waters 40 km from the coast. At St. 17, there was a dominance of gastropods followed by cirripedians and both larvae were most abundant at the deeper strata sampled (Fig. 6). Brachyurans and gastropods accounted for the highest densities at St. 18 and the most abundant taxa were found in the first strata of the water column (Fig. 6). At the last station sampled, brachyurans and stomatopods showed the highest densities and were associated with the first 20 m of the water column, whereas gastropods and cirripedians were found down to 20–30 m strata (Fig. 6). 4.2. Larvae spatial distribution and correlation analysis The spatial distribution of larvae show that the highest densities occurred at St. 15 (66.9 ind. m− 3), St. 8 (49.2 ind. m− 3), St. 6 (29.2 ind. m− 3), St. 18 (26.1 ind. m− 3), St. 17 (24.4 ind. m− 3) and St. 1 (22.1 ind. m− 3) the most offshore station (Table 1). The dominant groups were gastropods (42%), followed by brachyurans (24%), cirripedians and stomatopods (13%) and polychaetes (3%). Gastropod larvae were particularly abundant at St. 15, where numbers reached 47.6 ind. m− 3, representing 72% of the total. Larval abundance across shelf showed a U-shaped distribution with higher numbers at the coastal upwelling and in the gyre (Fig. 7). Crustacean larvae were more abundant nearshore, and at St. 16 they represented more than 90% of the larvae sampled, with brachyurans density of 12.5 ind. m− 3. This trend was observed for

all crustaceans including Brachyura, Stomatopoda, Cirripedia, Anomura and Palinuridea. Cirripedians reached a conspicuous peak of 39.5 ind. m− 3 at St. 8 and stomatopods were more abundant particularly at St. 6 with 19.6 ind. m− 3. At the most offshore St. 1, St. 2 and St. 3, however, crustaceans accounted for less than 10% of the total. Polychaete larvae were abundant at St. 2 and 3, with 28 and 24% of the total, respectively, and reached maximum integrated density at St. 15 (2.8 ind. m− 3). Echinoderm abundance was high at the deeper stations, reaching a maximum of 19% (4.1 ind. m− 3) of the total larvae at St. 1. In shallower stations, echinoderms were not numerically abundant, accounting for less than 5% of total larvae. The analysis of correlation showed, as expected, significant negative relationships between distance of the coast and several biotic variables (chl-a, total larval density and crustaceans) and % of SACW (Table 2). Brachyura and Stomatopoda were the only major taxa of larvae positively correlated to the % of SACW in the water column, whereas significant negative correlations were found between % of SACW and bivalves, gastropods and polychaetes (Table 2). Integrated concentrations of chl-a correlated positively with integrated larval, brachyuran and stomatopod densities. 4.3. Brachyuran larvae A total of 351 brachyuran larvae were identified in 31 taxa. Twenty out of 31 taxa belonged to coastal and shelf species with their adult counterpart distribution ranging from the intertidal to depths of approximately 160 m (Table 3). The remaining taxa included species with wider bathymetric distribution or individuals only identified at

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Fig. 5. Same as Fig. 3 for transect #3.

Fig. 6. Same as Fig. 3 for transect #4.

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nopeus sp. larvae were found mainly in deeper strata even at night samples. It is worth noting that larvae of estuarine species such as Uca sp., Sesarma rectum and Sesarmidae sp. were sampled very far from coast (St. 1). 5. Discussion In this study, physical and biological time-series taken at a crossshelf transect were used to infer the vertical and cross shelf distribution patterns of benthic invertebrate larvae during a consistent coastal upwelling event off Cabo Frio. This area is analogous to the east coast of the US, where several authors have investigated larval transport mechanisms during coastal upwelling and downwelling events (e.g., Shanks et al., 2000; Garland et al., 2002; Shanks et al., 2003; Shanks and Brink, 2005; Ma et al., 2006). Those studies demonstrated that some types of larvae remained in inner-shelf areas (b30 km offshore) through depth-keeping mechanisms (Shanks and Brink, 2005) thus, avoiding passive cross-shelf transportation. Here, we revisited this question for a broader spatial scale (~100 km offshore). During our sampling, the upper water column (100 m) was vertically stratified (Figs. 3, 4, 5 and 6) with SACW moving onshore at

Fig. 7. Total density of larvae against distance from the shore. Upwelling and eddy zones are approximate and may vary over time.

higher larval taxon level, preventing an accurate determination of their bathymetric range. Zoea larvae of Parthenopidae sp. and Portunus cf. spinicarpus were the most frequent and abundant, occurring from nearshore stations up to 116 km offshore. Early stages of these species were sampled only at coastal stations (inner and mid shelf) in various depths, whereas later stages occurred in the outer shelf and slope at relatively deeper waters (Table 4). Pinnixa sp. and Eurypa-

Table 2 Spearman's Rank correlation yields among variables used in this study.

Depth %SACW Chl-a Larvae

Depth

%SACW

Chl-a

Larvae

Echinodermata

Polychaeta

Gastropoda

Bivalvia

Cirripedia

Brachyura

Stomatopoda

1

− 0.658 1

− 0.794 0.393 1

− 0.611 0.110 0.637 1

0.336 − 0.301 − 0.262 0.107

0.464 − 0.591 − 0.220 − 0.014

0.122 − 0.631 − 0.070 0.346

0.142 − 0.472 − 0.171 0.108

− 0.510 0.171 0.429 0.606

− 0.890 0.465 0.844 0.705

− 0.797 0.578 0.733 0.432

We used integrated values of chl-a and larvae densities, station depths and percentage of SACW in the 5 strata (0–100 m) sampled. In bold correlation coefficients with p b 0.05, bold and underlined coefficients with p b 0.01.

Table 3 Densities of Brachyura zoeae (ind. m− 3) and spatial distributions of corresponding adult taxa. Taxa/station #

Shelf waters 19

Brachyura sp.1 Brachyura sp.2 Brachyura sp.3 Homolidae sp. Calappidae sp. Calappa sp. Hepatus sp. Leucosiidae sp. Majidae sp. Anasimus latus Stenorhynchus seticornis Parthenopidae sp. Cancroidea sp.1 Portunus cf. spinicarpus Callinectes sp.1 Callinectes sp.2 Arenaeus cribarius Goneplacidae sp. Xanthidae spp.1 Xanthidae spp.2 Eriphiidae sp. Eriphia gonagra Menippe nodifrons Eurypanopeus sp. Hexapanopeus sp. Pinnixa sp. Uca sp. Sesarmidae sp. Sesarma rectum Pachygrapsus sp. Pachygrapsus gracilis Not identified Total

Slope waters 15

7

13

4

11

3

Adults distribution 2

1

0.02 0.50 0.03 0.03 0.09

0.06

0.03 0.04 0.12 0.08

0.91

0.38

0.05

0.02 0.09 0.05

0.03

0.21 0.56

0.09

0.03 0.07 0.02 0.03 3.40 0.12

0.14

0.03

0.18

0.21

0.20 0.03 0.14 0.09

0.11 0.14

0.01 0.01 0.02 0.01 0.02 0.04

0.03 0.02

0.03

0.01 0.04

0.02

0.02 0.09 0.02 0.02

0.02

0.03 0.03

0.09 0.07 0.02 0.30 0.28

0.03 0.03 0.24 0.14

0.03

0.02 0.02

2.44 3.43

0.05 13.04 14.60

0.26 5.39

0.09 1.10

0 0.13

0.42 1.39

0 0.16

0.03 0.09

0.14 0.27

Depend on species Depend on species Depend on species Depend on species Coastal waters — 220 m Coastal waters — 220 m Coastal waters — 160 m Coastal waters — 160 m Depend on species coastal waters — 160 m Coastal waters — great depths Coastal waters — 200 m Depend on species Coastal waters — 120 m Coastal waters — 90 m Coastal waters — 90 m Coastal waters — 70 m Depend on species Depend on species Depend on species 0–5 m 0–5 m 0–5 m 0–5 m 0–25 m 0–75 m Estuarine species Estuarine/coastal species Estuarine species Coastal waters Coastal waters

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Table 4 Range distribution of brachyurans taxa in the water column and their zoeal developmental stage. Taxa/station #

Shelf waters

Slope waters

Inner

Mid

19

15

Outer 7

13

4

11

Callinectes sp.1

3

2

Hexapanopeus sp.

20–40 m II

Pachygrapsus sp.

0–20 m V

Parthenopidae sp. Portunus spinicarpus

0–30 m I

0–20 m I 0–20 m I–II

0–60 m I–II 0–40 m VI

Arenaeus cribarius Callinectes sp.2

Eriphiidae sp.

0–20 m III

Pinnixa sp.

0–40 m I–II 0–40 m I–IV

Sesarmidae sp.

0–20 m II

Hepatus sp.

Anasimus latus Menippe nodifrons Eriphia gonagra

0–20 m IV

40–80 m IV–V

80–100 m IV–V 20–60 m VI 0–20 m VI 0–20 m III

0–20 m VI

0–20 m V

20–40 m I 0–20 m III 60–80 m III–IV 20–40 m I–III 0–20 m II

60–80 m III–IV

20–80 m II–III

0–20 m I

Calappa sp.

Leucosiidae sp.

60–80 m I 0–20 m III 20–40 m V

0–20 m I–III

Sesarma rectum

Pachygrapsus gracilis

0–20 m II 20–40 m VI 0–20 m VI

0–20 m II

Eurypanopeus sp.

Uca sp.

1

0–20 m IV

0–20 m final 60–100 m II 0–20 m II

0–20 m II 0–20 m III–IV

0–20 m III–IV 0–20 m II

0–20 m III

subsurface depths. The increased number of coastal species, such as barnacle, brachyuran, stomatopod and other crustacean larvae, as well as positive correlations between larvae abundance and chl-a (Tables 1 and 2) suggest an association with the upwelling event. In the Cabo Frio region, the vertical movement of the 18 °C isotherm was used to estimate upwelling speed; vertical current speed in nearshore areas was estimated at the order of 0.1 mm s− 1 (Valentin et al., 1987). However, the observed strong shore-parallel flow in surface waters, flowing southwards within the first 40 km with up to 20 cm s− 1 (Fig. 2), is likely the most important factor determining the net larval transport. The coastline irregularities of Cabo Frio and the spatial variation in wind stress can force the formation of a cool upwelled water plume, which intensifies in the offshore direction (Carbonel, 1998). In addition, several authors have described the connection of this plume with the meandering pattern of the BC (Campos et al., 2000; Silveira et al., 2004; Calado et al., 2006). Coastal jets of cold and chlorophyll-rich waters could be seen not only off Cabo de São Tomé (22.5°S and 41.5°W, north of the study area, see also Calado et al., 2006), but also southwards of Cabo Frio (Fig. 1), and according to Lorenzzetti and Gaeta (1996) they can be found up to 300 km south from Cabo Frio. It is likely that coastal larvae entrapped in these plumes are advected along the continental margin to offshore regions; otherwise some larvae must have the ability to avoid offshore transport.

Elevated larval abundances at St. 1 were associated with the BC meso-scale meander observed in Figs. 1 and 2, coming from the Cabo of São Tomé shelf area. This scenario becomes particularly clear when the meander pattern (Fig. 2), thermal structure and larval concentration (Fig. 3) are confronted. It seems that the higher abundances of larvae were located at the offshore (and intense) border of the meander (St. 1). From the offshore edge of the clockwise meander (St. 1) to the center of the meander (St. 2 and 3, where the velocities are basically nil, Fig. 2), the number of larvae decreased considerably (Fig. 3, Table 1). Although gastropod was the most abundant group in offshore waters, larval composition, with highest abundances of echinoderm, polychaete, bivalve and sipunculan larvae, was relatively distinct compared to coastal larvae (Table 1). In the case of gastropods, a significant number of larvae were probably transported by meanders drifting cross-shelf to offshore areas (Fig. 3 and Table 1). Few larvae of coastal brachyuran species were identified in stations 1, 2 and 3 (Table 3). Nevertheless, larvae of Uca sp., Sesarma rectum and Sesarmidae sp.1 were sampled over 30 km offshore (Table 3), which is unusual since estuarine species rarely occur in distances further than 10 km from the coast (Shanks and Eckert, 2005; dos Santos et al., 2008). On the other hand, larvae of coastal species such as Hepatus sp., Leucosiidae sp., Anasimus latus, Menippe nodifrons, Calappa sp. and Eriphia gonagra were not sampled further than 58 km offshore in the present work, despite being found at surface (Tables 3 and 4) where offshore transport tends to be more important. Our results

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suggest that larval vertical migration may prevent the loss of larvae from local populations through offshore surface advection to oligotrophic open waters off the Brazilian coast by strong cross-shelf transport during upwelling events off Cabo Frio region (Figs. 1 and 2). Moving to deeper layers, larvae may be carried back to the coast in the colder SACW. However, it is clear that our results could be biased by the single sample taken at the most offshore stations and the lack of identification to the species level, thus we are limited to suggest that upwelling plumes as wells as meso-scale meanders and eddies could potentially play an important role for larvae dispersal in the tropical Brazilian coast. Larval dispersal due to shelf hydrography depends greatly on their vertical distribution and time spent in different water layers. In order to remain close to suitable areas for settlement, coastal species must avoid seaward advection by sinking towards SACW depths. dos Santos et al. (2008) reported a decapod diel vertical migration on the Portuguese coast, where larvae remained between 20–55 m during day time, migrating towards the surface at night. A similar strategy was reported in central Chile, where competent gastropod larvae avoid large-scale offshore transport by linking reverse diel vertical migration and upwelling circulation, and thus restricting their position to a zone delimited by the upwelling plume (Poulin et al., 2002). However, no clear pattern on diel vertical migration was observed during our sampling period. Cirripedia and Brachyura sampled at night, for example, were positioned in high numbers at the surface (0–40 m interval) at St. 7, whereas in St. 9 the majority of larvae were found at 80–100 m strata (Fig. 4). On the other hand, Parthenopidae sp. and Portunus cf. spinicarpus, the most abundant and frequent Brachyuran taxa, were collected near surface during nocturnal sampling and in greater depths during the day, corroborating the most common diel vertical migration pattern among decapods larvae (Queiroga and Blanton, 2005). By partitioning time between the surface layer moving seaward and the bottom layer, where the compensating counter-current develops, larvae can avoid seaward dispersal (Peterson, 1998). From an evolutionary perspective, Shanks and Brink (2005) highlighted the potential of slow-swimming coastal larvae to adjust their vertical distribution and, thus, remain close to suitable settlement areas. Larvae sinking to subsurface layers would be transported back to the inner shelf, if a continuous intrusion of SACW occurs. This behavior may also maintain larval populations close to high food supply zones (i.e., over inner and mid-shelf chlorophyll-rich areas; Figs. 1, 3, 4, 5 and 6), particularly in the study area. Gastropoda, Cirripedia and Brachyura were the most abundant larvae in shelf waters, and all of them showed a vertical displacement consistent to the depth-keeping mechanism suggested by Shanks and Brink (2005). The stations where high number of larvae was observed down to N60 m in the water column were located in areas N 40 km from the coast (at Sts. 8, 9, 12 and 17, see Figs. 4, 5 and 6). Those areas are off the zone delimited by the shore-parallel coastal current (Fig. 2). Consistently, the highest larval densities occurred at surface waters in areas b 40 km from the coast, which are characterized by high chl-a concentrations (at Sts. 6, 15 and 18). 6. Conclusions Despite limitations concerning larval identification and spatiotemporal scales used in the present study, our findings revealed that even estuarine and coastal species experiencing excursions to midshelf areas (N50 km from the coast, St. 8 in Fig. 4) can avoid offshore transport by sinking down to 80–100 m in the water column, where SACW could potentially transport them back to coastal areas during upwelling events. Alternatively, excursions of upwelling plumes could serve as corridors for tropical larvae dispersion along subtropical areas in the Brazilian continental margin. Future studies in the study area, employing technological advances on sampling, processing and

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