Research papers

Topographical and hydrographical impacts on the structureof microphytoplankton assemblages on the Abrolhos Bankregion, Brazil

Sylvia M.M. Susini-Ribeiro a,n, Mayza Pompeu b, Salvador A. Gaeta b, Júlia S.D. de Souza c,Laura S.D. Masuda c

a Universidade Estadual de Santa Cruz, Departamento de Ciências Biológicas, Rodovia Ilhéus-Itabuna km 16, Salobrinho, 45662-090 Ilhéus, Bahia, Brazilb Instituto Oceanográfico, Universidade de São Paulo, Praça do Oceanográfico 191, Cidade Universitária, 05508-900 São Paulo, SP, Brazilc Mestrado em Sistemas Aquáticos Tropicais, Universidade Estadual de Santa Cruz, Rodovia Ilhéus-Itabuna km 16, Salobrinho, 45662-090 Ilhéus, Bahia, Brazil

a r t i c l e i n f o

Available online 27 September 2013

Keywords:PhytoplanktonIntermediate disturbance hypothesisDiversitySouthwest Atlantic

a b s t r a c t

This study was conducted at the Abrolhos Bank (15160′–21130′S; 37100′–40130′W), Brazil, in July andAugust 2007, to evaluate the topographic and hydrographic influences on microphytoplankton composi-tion and relative abundance. Net phytoplankton was collected from the top 200 m of the water column toassess diversity proxies (species richness, Shannon index, dominance and equitability) and comparedwith thermohaline, nutrient and chlorophyll profiles. A total of 326 taxa occurred in the area. Patterns inspatial distribution of microphytoplankton assemblages were two-fold: a north–south gradient linked tovariations in temperature and nitrite, and a coast-offshore gradient associated with the depth of themixed layer and the Brunt–Väisälä maximum frequency. Microphytoplankton assemblages were typicalof tropical oligotrophic environments. However, the inshore community found on the Abrolhos Bank wasenriched by bottom dwelling, large-sized cells ressuspended from local sediments as a result of thehighly dynamic coastal circulation. Species diversity was high in oceanic sites where water columnstability as measured by the Brunt–Väisälä frequency achieved its maxima, but high values of ecologicalindexes were also found in the southern part of the study area influenced by bottom intrusions ofnutrient-rich oceanic waters, giving support to the notion that phytoplankton diversity increases atintermediate levels of environmental disturbance.

& 2013 Elsevier Ltd. All rights reserved.

1. Introduction

Phytoplankton accounts for approximately 50% of the globalprimary production (Falkowski et al., 1998). Phytoplankton cellsizes range from picoplanktonic cyanobacteria, to microplanktonicdiatoms and dinoflagellates (Chisholm, 1992; Malone, 1980). Cellsize is a key trait impacting phytoplankton access to resources andgrowth. Small cells have several advantages over large ones inoligotrophic waters, such as lower sinking rates and higherefficiency in acquiring limiting nutrients. These adaptations arelinked to their high surface-to-volume (S/V) ratio and smalldiffusion boundary layer, which are less limiting to nutrienttransport (Smayda, 1970; Banse, 1976). The pathways and effi-ciency of energy transfer from primary producers to aquatic foodwebs, including those sustaining upper trophic levels, are stronglyaffected by phytoplankton community composition and size spec-trum (Cloern and Dufford, 2005).

The Abrolhos Bank is the largest extension of the eastern Braziliancontinental shelf. The bank spreads to a maximum of 220 km fromthe coast, and lies directly in the pathway of the southward-flowingBrazil Current (BC). The main water mass in this region is the warmand salty Tropical Water (TW) carried by the BC, with temperaturesfrom 22 to 27 1C and salinities from 36.5 to 37 psu (Castro andMiranda, 1998), which lends an oligotrophic character to the region.The cold and nutrient-rich South Atlantic Central Water (SACW)occurs below the TW in offshore areas. The Abrolhos Bank is atopographic feature which influences the local water circulation bycausing upwelling, eddies, and other physical phenomena. Theseinduce fundamental changes in physical, chemical and biologicalfeatures (Schmid et al., 1995; Ekau and Knoppers, 1999) favoringpelagic production (Gaeta et al., 1999).

Recent phytoplankton studies in the Abrolhos region describedthe contribution of auto- and heterotrophic size fractions (pico-,nano- and microplankton) to total carbon biomass or cell concen-tration (Cupelo, 2000; Masuda, 2009; Souza, 2010; Susini-Ribeiro,1999; Tenenbaum et al., 2007). These studies showed that thehighest biomass and cell concentration in all phytoplanktonsize ranges were found south of, and on the Abrolhos Bank itself,

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Continental Shelf Research

0278-4343/$ - see front matter & 2013 Elsevier Ltd. All rights reserved.http://dx.doi.org/10.1016/j.csr.2013.09.023

n Corresponding author. Tel.: þ55 73 3680 5307; fax: þ55 73 3680 5226.E-mail addresses: sylsusini@gmail.com, ssusini@uesc.br (S.M.M. Susini-Ribeiro).

Continental Shelf Research 70 (2013) 88–96

indicating the key role of this topographic feature in the regionalbiological production. These studies reported on the importantcontribution of small-sized phytoplankton fractions and the het-erotrophic compartment to total carbon biomass, suggesting awell-established recycling microbial web (Cupelo, 2000; Ekau,1999; Susini-Ribeiro, 1999; Tenenbaum et al., 2007).

It is well known that large phytoplankton cells are inefficient intaking up nutrients at low concentrations and depend on turbu-lence to remain in the euphotic zone, which makes microphyto-plankton a good indicator of turbulent processes and nutrientinjection through the pycnocline in oligotrophic oceans.

The specific aim of the present study was to detail the mostimportant factors in regulating the structure of microphytoplank-ton assemblages, and to evaluate how individual species andfunctional groups are adapted to the topographic and hydrologicalinfluences of the Abrolhos Bank.

2. Material and methods

The study was conducted on board RV Prof. W. Besnard, from 25July to 15 August 2007, in shelf and oceanic waters of the Abrolhosregion between Ilhéus (15130′S) and Cabo de São Tomé (22100′S).

2.1. Hydrography, nutrients and chlorophyll-a

Hydrographic data were obtained from profiles with a CTDcoupled to a rosette, from surface down to 200-m depth (Fig. 1).Water samples were collected in four to six depths on shallowstations, and at ten depths (0, 5, 10, 25, 50, 75, 100, 125, 150 and200 m) in the oceanic region. Nitrite, nitrate, ammonium, phos-phate and silicate were determined according to Grasshoff et al.(1983), and chlorophyll-a was estimated by fluorescence using aTurner 10-AU fluorometer (Yentsch and Menzel, 1963).

The Brunt–Väisälä frequency square (in Hz² – hereafter referredto as BV), a proxy for surface water stability, was calculated usingthe package Gibbs-Seawater Oceanographic Toolbox “Thermody-namic Equation of Seawater” (TEOS-10, 2009).

2.2. Microphytoplankton assemblage

For microphytoplankton analysis, samples were collected with aconical net (20-μmmesh aperture) in vertical hauls from 200-m depthto the surface at oceanic stations, and from close to the bottom to thesurface at continental shelf stations (Fig. 1). Samples were preservedwith 4% buffered formaldehyde in glass flasks (200 mL).

At least 300 cells were counted and identified in each of thewell-mixed net samples to provide reliable values of diversity(Margalef, 1978). The following ecological indexes were calculated:species richness, Shannon diversity index, dominance index andPielou's equitability index.

2.3. Statistical analysis

A cluster analysis was performed on a matrix of relativeabundance of microphytoplankton species. Data were standar-dized and fourth-root transformed. A similarity matrix of sampleswas constructed based on the Bray–Curtis similarity index, and adendrogram was generated by average clustering (UPGMA tech-nique). A similarity profile test was conducted to search forstatistically significant cluster groups (SIMPROF routine). A simi-larity/dissimilarity test was performed to evaluate the percentagecontribution of individual species to the splitting of clusters and tothe closeness of samples within a group (SIMPER routine).

A Principal Components Analysis (PCA) was performed on areduced matrix of environmental data. The most frequent value

(mode) of each environmental variable from the surface to 200-mdepth was selected to represent the environmental conditions in thewater column, and to enable comparison with integrated verticalnet hauls.

The analog of the univariate analysis of variance (ANOSIMroutine) was used to test for differences between sample groupscombined according to potential environmental gradients, as follows:(1) a north–south gradient, with three groups – regions north ofAbrolhos Bank, over Abrolhos Bank, and south of Abrolhos Bank; and(2) a coast-offshore gradient based on the local depth, with threegroups – continental shelf, shelf break, and offshore stations.

A stepwise test was performed to evaluate which environ-mental variables explained the observed microphytoplanktonassemblage patterns (BEST routine). A test was performed toinvestigate the null hypothesis, that there was no relationshipbetween biotic assemblages and a specific abiotic pattern (RELATEtest). All multivariate analysis and statistical tests were carried outwith PRIMER v.6, except for the PCA, which was performed withMVSP – Multivariate Statistical Package, v. 3.1.

3. Results

3.1. Hydrography, nutrients and chlorophyll-a

The warm TW transported by the BC encompassed the surfacelayer of the entire region, with temperatures ranging from 23.23 to

Fig. 1. Selected stations in the Abrolhos Bank (AB) region: (a) north of AB; (b) onthe AB; and (c) south of AB. Black dots represent hydrographic stations andtriangles stations where plankton samples were collected.

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25.97 1C (mean 24.6870.64 1C) and salinity from 36.57 to 37.61 psu(mean 37.3270.15). The nutrient-rich SACW occurred below theTW in oceanic regions, at approximately 125–200 m depth, withtemperatures from 14.75 to 24.92 1C (mean 21.1572.43 1C) andsalinities from 35.43 to 37.33 psu (mean 36.5670.47). At shallowstations on the continental shelf, including the Abrolhos Bank itself,the mixed layer extended down to the bottom, temperature andsalinity were vertically homogeneous, and the chlorophyll-a max-imum was at the subsurface or near the bottom, ranging from 0.11to 1.33 mg m�3 (mean 0.5970.32 mg m�3). In general, the mixedlayer depth was shallower (80–100 m) at stations near the con-tinental shelf break, and deeper (125–200 m) at offshore stations.The depth of the subsurface chlorophyll-a maximum (SCM) wasbetween 125 and 150 m, and the chlorophyll-a concentration at theSCM ranged from 0.21 to 0.89 mg m�3 (mean 0.3870.15 mg m�3).At some stations, the SCM coincided with the nitracline depth.Some selected vertical profiles of temperature, density and BV arepresented to illustrate the nitrate diffusion up through the pycno-cline, and the chlorophyll-a concentration (Fig. 2). Shallow stationshad a well-mixed layer with nearly homogeneous temperature,BVmax at different depths within the mixed layer, and chlorophyll-amaxima ranging from 20–25 m depth to the bottom (Fig. 2a). Deepoceanic stations were characterized by a gradual increase in densityand decrease in temperature with depth, and BVmax at the bottomof the mixed layer (Fig. 2b and c). At station 11, near the shelf break(Fig. 2b), the chlorophyll-a concentration at the SCM was higherthan at offshore stations (e.g., Station 42, Fig. 2c).

3.2. Microphytoplankton assemblages

A total of 326 microphytoplankton taxa were identified fromthe net samples, including 170 Bacillariophyceae, 143 Dinophy-ceae, 9 Prymnesiophyceae (coccolithophorids), 1 Dictyochophyceaeand 3 Cyanobacteria.

The dendrogram displayed three main groups (A, B, and C) at30% similarity, with seven statistically significant subgroups(Fig. 3). Group A was composed of shallow coastal stations locatedon the Abrolhos Bank and towards the north (Figs. 3 and 4). GroupB comprised mainly deep oceanic stations and was split into twosubgroups: intermediate stations (B1, B2 and B3) and offshorestations (B4 and B5). Group C was formed by two oceanic stationsnorth of Abrolhos Bank, near the shelf break and over a seamount.Stations 12, 30 and 69 did not cluster with any group (Fig. 3).

The coastal microphytoplankton assemblage (Group A) wasformed by 134 species and dominated by pennate diatoms, with ahigh proportion of tychoplanktonic species. The nine species listedin Table 1 contributed about 50% of total similarity within thegroup. The microphytoplankton assemblage occurring at inter-mediate stations (B1, B2 and B3) comprised 191 species (64%diatoms, 34% dinoflagellates and 2% other groups), and theoffshore assemblage (stations B4 and B5) was formed by 183species (52% dinoflagellates, 44% diatoms and 5% other groups)always present at low concentrations (Table 1). The microphyto-plankton assemblage of Group C (82 spp.) with a high proportionof dinoflagellates (60% of the total) was enriched by diatom speciessuch as Rhabdonema adriaticum and Asterolampra marylandica,some of them occurring at high concentration. Ten speciesaccounted for 56% of total similarity within this group (Table 1).

The mean dissimilarity between groups A, B and C was high:87.7% (A�C), 78.3% (B�C) and 72.5% (A�B), even though theindividual contribution of each taxon was low. Mean dissimila-rities between oceanic stations (B groups) were lower: 61.9%(B1�B2), 54.8% (B2�B3), 54.6% (B1�B3) and 53.3% (B4�B5).

Species richness by sample ranged from 29 (Station 52) to 72species (Station 42) (Table 2). The highest values of the Shannondiversity index (5.60 bits cell�1) and equitability (0.92) were observed

at Station 17, and the lowest diversity (1.29 bits cell�1) and highestdominance (0.86) at Station 58 (Table 2). In general, lower diversityvalues were observed on the continental shelf, near the shelf break, ornear seamounts, while high values were observed offshore or atintermediate stations south of the Abrolhos Bank (Fig. 4).

Some patterns were observed between BVmax frequency anddiversity (Fig. 5). The coastal stations were concentrated near the yaxis at lower frequencies. At higher frequencies, the oceanicstations aligned above the curve, and the coastal or shelf-breakstations below the curve were those positioned on the AbrolhosBank and towards the north.

The PCA of the reduced matrix of environmental variablesexplained 71% of the data variability (Fig. 6, Table 3). Axis1 accounted for 31% of total variance, and represented thenorth–south gradient. Samples from south of Abrolhos Bank arelocated on the negative side of this axis; those from the bankregion in the center; and on the opposite side are those from northof Abrolhos Bank, with high temperature and salinity, and highcontents of silicate, nitrite and ammonium (Fig. 6). Axis 2 (25%) isrelated on the negative side with mixed layer depth and BVmax

frequency, characterizing the deep oceanic stations, and on thepositive side, with shallow and coastal stations associated mainlywith high phosphate, nitrite, and silicate concentrations. Thus, thisaxis reflects the coastal-oceanic gradient (Fig. 6). Axis 3 (14%)allocated on the positive side some oceanic and coastal stationssouth of Abrolhos Bank and one station (41) at the Abrolhos Bankshelf break (Fig. 7). This axis seems to express nitrate enrichmentas those stations were associated with high nitrate and ammo-nium concentrations.

There was statistical difference between groups of samplesalong the north–south gradient across the Abrolhos Bank, basedon both microphytoplankton assemblages and environmental data(Tables 4 and 5A). The same was observed considering the coastal-offshore gradient in microphytoplankton assemblages, but onlybetween the continental shelf and offshore stations, or betweenshelf break and offshore stations. No difference was observedbetween the continental shelf and shelf break stations (Table 4B).For the environmental data, there were statistical differences onlybetween continental shelf and offshore stations (Table 5B).

Results of both the BEST routine and the RELATE test indicatedthat temperature, nitrite, mixed layer depth, and BVmax formed theset of environmental variables that best explained the variabilityin microphytoplankton assemblages (ρ¼0.60).

4. Discussion

4.1. Hydrodynamics

In tropical marine regions, water stratification and verticalmixing have strong impacts on phytoplankton biomass andcomposition. Under low turbulence, the euphotic zone becomesnutrient depleted as a result of phytoplankton uptake. A perma-nently two-layered euphotic zone, with high nutrient concentra-tion below and low concentration above the pycnocline, is knownas the “Typical Tropical Situation-TTS” (Herbland and Voituriez,1979). The Abrolhos Bank region is a typical tropical system withhigh radiant energy and reduced vertical transport, the latter dueto the persistent stable stratification. In general, the thermocline,nitracline and SCM vertical positions were very similar to the TTSscenario.

The Brunt–Väisälä buoyancy frequency (BV) increases when thepycnocline is displaced and then returns to its original position(Mann and Lazier, 1991). The BV frequency can be considered as asimple measure of stability of surface waters in a stratified fluid; thestronger the stratification, the faster the oscillation (Harris, 1986).

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Deep oceanic stations of the Abrolhos Bank had a gradual increasein water density and decrease in temperature with depth, andBVmax frequencies at the bottom of the mixed layer coincident withthe SCM. It appears that nutrients slowly diffusing through thepycnocline were rapidly taken up by phytoplankton at the SCM,where light intensity was high enough for photosynthesis tofunction. At stations near the shelf break, the thermocline wasshallower and the chlorophyll-a concentration at the SCM washigher than at offshore stations. In the shallow coastal waters, themixed layer depth was determined by local topography and hydro-graphy, and nutrient replenishment into the euphotic zone waslikely provided by turbulent mixing.

4.2. Dynamics of microphytoplankton assemblages

Microphytoplankton assemblages comprise morpho-functionalgroups including phylogenetically unrelated taxa. These groupscan be established in terms of their size and S/V ratio and eachcategory corresponds to a life strategy related to light and nutrientavailability and turbulence levels.

Colonist-invasive species (C) are small- to medium-sized, fastgrowing species with high S/V ratios. Nutrient stress-tolerantspecies (S) are large acquisitive cells with low S/V ratios and slowgrowth. Disturbance-tolerant “ruderal” species (R) are elongatedin shape and, despite their large size, have a high S/V ratio whichaffords them harvesting light energy under high mixing condi-tions, but with high nutrient concentrations (Reynolds, 1988,2002; Smayda and Reynolds, 2001).

The coastal assemblage (Group A) dominated by diatoms wasfound on the Abrolhos Bank and spread over the continental shelfto the north. In shallow regions, the benthic system is of greatimportance since the input of inorganic nutrients and organicgrowth factors following physical events affect the compositionand cell density of phytoplankton species, selecting mainly oppor-tunist diatoms and others with diverse strategic behaviors(Smetacek, 1988). Thalassionema nitzschioides was the most abun-dant species in this coastal assemblage. This pelagic pennatediatom occurs in all marine habitats and tends to be moreabundant near the coast (Raymont, 1980). The presence of benthicpennate diatoms or tychoplankton species in the water column is a

Fig. 2. Selected vertical profiles of temperature (T); density (D); Brunt–Väisälä frequency (BV); nitrate (Na) and chlorophyll-a (Chl): (A) coastal station, (B) oceanic stationnear the shelf break, and (C) offshore station.

S.M.M. Susini-Ribeiro et al. / Continental Shelf Research 70 (2013) 88–96 91

useful indicator of ressuspended sediment. They include Paraliasulcata, Surirella fastuosa and Pleurosigma mormanii. In shallowwaters tychoplanktonic behavior appears to be an efficient lifestrategy. Non-motility could be advantageous if sedimentationallows nutrient-depleted diatoms to take up nutrients from thesediment surface and thus resume photosynthesis after ressus-pension (Sicko-Goad et al., 1986). Some other pennate diatoms(Nitzschiella spp. and species of Naviculaceae and Thalassionema-taceae) are elongated, which increases the S/V ratio; these speciesare adapted to unstable environments with high nutrient concen-tration and highly variable light intensity (possibly R-strategistssensu Reynolds et al., 2001). The coastal and shelf-break micro-phytoplankton assemblages south of the Abrolhos Bank (Station 12and Group B1) differed from other coastal assemblages. Datasuggest that the SACW influence is stronger to the south of theAbrolhos Bank than to the north. One reason for this differencemay be the effect of the Abrolhos Bank topography on thesouthward-flowing BC, which is diverted, creating upwelling andvortices (Ekau and Knoppers, 1999; Gaeta et al., 1999). A second

Fig. 3. Dendrogram for stations derived from the similarity matrix of abundance ofmicrophytoplankton species, using the Bray–Curtis index and UPGMA technique.Numbers at the base of dendrogram correspond to sample sites (see Fig. 1 forlocations).

Fig. 4. Horizontal dispersion of the groups extracted from the cluster analysis andthe Shannon diversity index. Symbols of the diversity index: o4.0 bits ind�1,empty circles; 44.0 bits ind�1, light gray circles; 44.5 bits ind�1, dark graycircles, and 45.0 bits ind�1, black circles.

Table 1Percentage contribution (SIMPER) of the taxa that most contributed to the meanBray–Curtis similarity within groups defined by cluster analysis.

Average similarity within eachgroup (%)

A39.4

B151.3

B253.5

B351.9

B452.2

B555.5

C33.4

Thalassionema nitzschioides 11.7 5.85 5.76 3.63 0.96 3.47Nizschiella 8.25 3.91 3.13Naviculaceae 6.90 3.91Trichodesmium erythraeum 6.21 4.40 3.92 4.92Nizschia sigma 5.39Paralia sulcata 5.28 2.94Pleurosigmataceae 4.21Thalassionemataceae 3.62 3.63 3.50 2.49 3.05Surirella fastuosa 3.52Dictyocha fibula 4.95Bacteriastrum hyalinum 4.92 3.20Chaetoceros lorenzianus 4.65 5.39 2.94 4.41Meuniera membranacea 3.91Ceratium tripos 3.89Bacteriastrum delicatulum 7.14 3.56 2.86 3.12Pseudo-nitzschia 6.88 4.83 2.94Guinardia striata 5.91 3.63Cerataulina pelagica 5.01 4.20Rhizosolenia hebetata 4.23 3.81Rhizosolenia styliformis 4.11Ceratium fusus 3.57 2.40 4.89Guinardia flaccida 3.54Ceratium teres 4.48 2.87 5.81Asterolampra marylandica 3.76 2.75 5.81Ceratium pulchellum 3.31Leptocylindrus mediterraneus 3.11Chaetoceros atlanticus 3.00 3.67Ceratium declinatum 2.98Podolampas palmipes 2.66Pyrocystis robusta 2.61Podolampas spinifer 2.53Asteromphalus heptactis 2.47 2.53Gossleriella tropica 2.46Spatangidium arachne 2.46Hemiaulus hauckii 2.4Dinophysis rotundata 2.4 2.71Pyrocystis lunula 2.4Chaetoceros aequatorialis 3.12Eucampia cornuta 2.79Chaetoceros decipiens 2.57Gonyaulax fragilis 2.56Chaetoceros peruvianus 2.42Gonyaulax birostris 2.38 4.89Rhabdonema adriaticum 9.2Goniodoma polyedricum 5.81Asterionellopsis glacialis 4.89Palmerina hardmaniana 4.89Podocystis adriatica 4.89

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factor may be the effect of the shallow banks on tidal currents,generating internal tides and upwelling, especially along thesouthern flank of the Abrolhos Bank (Pereira et al., 2005).In addition, the BC is a western boundary contour current formedby the sum of the Tropical Water (TW) and SACW. At 20 1S latitudethe BC receives a significant contribution from the SACW, becom-ing deeper and stronger (Silveira et al., 2000). These factors mayhelp to explain the north–south gradient observed in the euphoticlayer of the BC in the entire area.

The tropical enriched assemblage (B1, B2 and B3) located southof the Abrolhos Bank or at the Abrolhos Bank shelf break, is ahighly diversified subgroup composed of large species with lowS/V ratios occurring in TW (possibly S-strategists sensu Reynolds

et al., 2001), and enriched by many opportunistic species.The presence of the latter species result from different mixingprocesses injecting nutrients (nitrate) from the SACW into theeuphotic layer. Such opportunists may have high S/V ratios eitherby being small or elongated (respectively, C-strategists andR-strategists sensu Reynolds et al., 2001). The diatom predomi-nance (64%) denotes a rapid response of this group followingphysically driven events such as upwelling and tidal currents. Theprincipal species of diatoms in these assemblages were smallchain-formers (Bacteriastrum spp., Chaetoceros spp.) and mediumto large, elongated taxa (Thalassionema nitzschioides, Rhisozoleniaspp., Leptocylindrus mediterraneus, Proboscia alata, Eucampia cor-nuta, Guinardia spp., Cerataulina pelagica, Corethron criophylum,Dactyliosolen phuketensis, Pseudo-nitzschia and Nitzschiella groups,Thalassionematacea and Naviculaceae).

The typical tropical offshore assemblage (B4 and B5) developsunder conditions of prolonged stratification such as those occurringon eastern continental shelves. This highly diversified microphyto-plankton assemblage included large numbers of dinoflagellates (52%)and diatoms (44%). Although phytoplankton biomass is largelyconcentrated in the nanoplankton fraction, the tropical system hasmany large-celled species (a highly diversified microphytoplankton),particularly dinoflagellates and diatoms, which are always present insmall numbers. Dinoflagellates have evolved different adaptations inoligotrophic conditions to compensate for the ecological disadvan-tage of their high nutrient requirements, such as nutrient-recoverymigrations, mixotrophic nutrition, allelochemically enhanced inter-specific competition, and allelopathic anti-predation defense mecha-nisms (Smayda, 1997; Smayda and Reynolds, 2001). Large dinofla-gellates are typically S-strategists (sensu Reynolds et al., 2001). Theyare often highly ornamented and capable of depth control throughmotility or auto-regulated buoyancy, and frequently have endosym-bionts. The genera Amphisolenia, Histioneis, Ornithocercus, Dinophysis,Heterodinium, Podolampas and Pyrocystis are typical of tropical off-shore waters (Smayda and Reynolds, 2001) and were present inthese assemblages, as were more than 30 species of Ceratium. Thegenus Ceratium appears to include species with C, S and R strategies(Smayda and Reynolds, 2001). The phytoplankton of oligotrophicopen seas also contains very large, rare, non-motile diatoms cellscapable of positive buoyancy at rates of several meters per hour(Villareal and Carpenter, 1989; Moore and Villareal, 1996; Villarealet al., 1999; Singler and Villareal, 2005). These are Ethmodiscus spp.,Rhizosolenia spp. and Rhizosolenia mats (macroscopic assemblages ofup to seven Rhizosolenia species). These species migrate as solitarycells or aggregates (mats) between deep nutrient pools (below 80–100 m) and the surface (Villareal et al., 1999) contributing to newproduction because of the concomitant upward transport and releaseof nitrate in the mixed layer (Singler and Villareal, 2005; Villarealet al., 1996). Some large diatoms common in oligotrophic environ-ments and in the Abrolhos region are Planktoniella sol, Gossleriellatropica, Asterolampra marylandica, and some Rhizosolenia spp. withRichelia intracellularis. These are considered to be bio-indicators ofstratified warm waters (Hasle and Syvertsen, 1997; Smayda, 1978;Villareal, 1992).

The microphytoplankton assemblage of Group C is a typicaltropical assemblage with a high proportion (60%) of dinoflagellates(mostly Dinophysis, Amphysolenia, Histioneis, Ornithocercus, Pyrocys-tis, Ceratium spp., Ceratium teres and Goniodoma polyedricum). Theassemblage is enriched by some diatom species (Rhabdonemaadriaticum, Asterolampra marylandica and Thalassiosira cf. bioculata),some of which are benthic and present in large numbers. Indeed,those two stations are located near the shelf break and seamountsnorth of the Abrolhos Bank, where the interaction of the barotropictide with the complex topography may generate residual barotropiccurrents and diurnal or semi-diurnal internal tides, which result inupwelling on the southern flank and downwelling on the northern

Table 2Values of species richness, Shannon diversity index, dominance and equitability at32 stations in the Abrolhos Bank region, July 2007.

Station Richness Diversity Dominance Equability

75 68 5.5 0.07 0.9070 51 4.5 0.20 0.7869 50 4 0.25 0.7068 68 4.5 0.34 0.7464 60 4.3 0.35 0.7259 46 4.0 0.25 0.7158 40 1.3 0.86 0.2457 68 4.3 0.39 0.753 46 3.9 0.27 0.7152 29 3.4 0.27 0.6950 31 1.8 0.76 0.3848 32 3.0 0.45 0.5942 72 5.4 0.11 0.8841 41 4.2 0.27 0.7839 31 4.3 0.19 0.8137 48 4.5 0.15 0.8035 34 3.7 0.29 0.7334 69 4.9 0.24 0.8033 58 4.8 0.17 0.8230 38 4.8 0.10 0.9028 63 4.8 0.21 0.8127 69 5 0.15 0.8325 60 5.1 0.11 0.8623 59 4.9 0.15 0.8321 50 4.2 0.32 0.7417 65 5.6 0.11 0.9215 58 5.0 0.17 0.8613 59 5.0 0.16 0.8512 52 4.4 0.19 0.7711 54 4.5 0.21 0.7810 55 4.9 0.15 0.858 67 5.6 0.09 0.91

Fig. 5. Relationship between microphytoplankton Shannon diversity index(bits cell�1) and Brunt–Väisälä maximum frequency (Hz²) for each station. Stationnumbers are indicated (see Fig. 1 for locations).

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side of the Abrolhos Bank (Pereira et al., 2005). The interaction ofthe tidally induced currents and downwelling on the northern sideof the Abrolhos Bank and above seamounts may explain the

formation of phytoplankton assemblages with large numbers ofbenthic species despite of the large distance from the coast, and thehigh degree of heterogeneity among samples in this area.

Fig. 6. Distribution of samples in PCA factorial planes 1–2 based on the reduced matrix of environmental data. Symbols: Temperature (T); Salinity (Sal); Nitrate (Na); Nitrite(Ni); Ammonium (Am); Phosphate (P); Silicate (Si); mixed layer depth (ZT); and maximum value of Brunt–Väisälä frequency (BVmax); triangules, squares and circlesrepresent stations north, on and south of Abrolhos Bank (AB), respectively; gray color represents coastal stations and black color the oceanic stations.

Table 3Coefficients of linear correlations of environmental variables of reduced matrix with the three main axes of the PCA analysis (40.05% are in bold).

Axis 1 Axis 2 Axis 3

Temperature (T) 0.533 �0.207 �0.126Salinity (Sal) 0.466 �0.249 �0.126Nitrite (Ni) 0.307 0.311 �0.256Nitrate (Na) 0.004 0.019 0.762Silicate (Si) 0.453 0.199 0.038Phosphate (P) 0.074 0.581 0.047Ammonium (Am) 0.299 �0.004 0.562Depth of the mixed layer (ZT) �0.227 �0.459 �0.001Maximum value of Brunt–Väisälä frequency (BV max) 0.23 �0.459 0.055

Fig. 7. Distribution of samples in PCA factorial planes 1–3 based on the reduced matrix of environmental data. Symbols: Temperature (T); Salinity (Sal); Nitrate (Na); Nitrite(Ni); Ammonium (Am); Phosphate (P); Silicate (Si); mixed layer depth (ZT); and maximum value of Brunt-Väisälä frequency (BVmax); triangules, squares and circles representstations north, on and south of Abrolhos Bank (AB), respectively; gray color represents coastal stations and black color the oceanic stations.

S.M.M. Susini-Ribeiro et al. / Continental Shelf Research 70 (2013) 88–9694

4.3. Diversity and the intermediate disturbance hypothesis

The diversity index, in bits per cell, is usually between 1 and2.5 in coastal waters. Values between 3.5 and 4.5 are mostfrequent in oceanic plankton; in ultra-oligotrophic oceanic areasdiversity values are close to 5 (Margalef, 1978). In the Abrolhosarea the estimated specific diversity indexes were within suchrange. Usually, lower diversity values were observed on thecontinental shelf, near the shelf break and near seamounts, thatis, in shallower areas with more frequent external disturbances.Diversity was higher at the deep, highly stratified and moreenvironmentally stable offshore stations.

In more stable waters, the organization accumulated by pre-vious populations can be preserved and built upon. Therefore, asspecies composition progresses during succession due to watercolumn stabilization, the order in the community increases(Margalef, 1963). In Margalef's view, order refers to predictability– as order increases, the probabilities of transition become muchmore limited. Order may be increased by tight feedback loops,increased grazing efficiency, and reduction in time lags betweenpools (Harris, 1986). Therefore, as order increases, the phytoplank-ton community acquires a pre-adapted capacity (predictability),such as the information carried by their constituent species, whichlimits the resilience of the system when faced with a differentintensity of disturbance.

The intermediate disturbance hypothesis states that, at anintermediate level of disturbance, competition is relaxed andspecies diversity is highest (Connell, 1978). When the frequencyor intensity of these disturbances is high compared to generationtime, the environment is more appropriate for C-strategists andthe diversity is reduced because species are eliminated by stress.Alternatively, when perturbations occur at very low frequencies orintensities, diversity is also reduced due to competitive exclusionbetween species, and S-strategists prevail. We should point outthat the classical trend of increasing diversities at intermediate

levels of disturbance observed in this area (Fig. 5) was heavilyinfluenced by only one station with high BVmax.

In addition to the influence of the BVmax frequency, the mixedlayer depth (ZT) and the vertical eddy diffusivity (Kv) play importantroles in determining the intensity of phytoplankton responses tonutrient injection into the mixed layer, and consequently, in deter-mining the diversity. As expected, BVmax was an efficient measure-ment of stability in a stratified water column, but not at the shallowstations where mixing prevailed. In those areas, Kv may provide abetter indication of nutrient injection into the mixed layer, whichexplains why BVmax was lower at coastal stations. The mixed layerdepth was deeper in the southern area, suggesting that physicalprocesses enhancing nutrient injection south of the Abrolhos Bankwere less turbulent compared to the north. In addition, the moreeffective SACW contribution probably induced a more diversifiedmicrophytoplankton assemblage in the area.

5. Conclusions

Microphytoplankton assemblages of the Abrolhos Bank regionare highly diversified and affected by hydrodynamic forcing asso-ciated with changes in bottom topography along north–south andcoastal-oceanic gradients. The large coastal extension (�200 kmfrom shore) of the bank is characterized by a homogeneous mixedlayer enriched with ressuspended nutrients, high chlorophyll-abiomass and a significant contribution of benthic-dwelling diatomsand other large-sized cells. The prolonged vertical stratification inthe oceanic domain associated with low disturbance levels con-tribute to the development of a mature microphytoplankton assem-blage comprised by several large, ornamented dinoflagellate anddiatom species, most of them S-strategists. The high speciesdiversity observed offshore and south of Abrolhos Bank, with asignificant number of large-sized cells with low S/V ratios seems tobe linked to mid-scale fluctuations of the Brunt–Väisälä buoyancyfrequency at the mixed layer depth. In summary, microphytoplank-ton assemblages in the Abrolhos area were typical of tropicaloligotrophic environments, enhanced with benthic species in shal-low sites, and with increased diversity levels in offshore areas atintermediate levels of environmental disturbance.

Acknowledgments

This research was supported by PROABROLHOS project (CNPqno. 4202119/2005-6). We are grateful to Dr. Rubens Lopes, pro-ject's PI, for his support and participation. We also thank GustavoP. Ortiz and Welder R. Araújo for the Brunt–Väisälä frequencycalculations; Gustavo Q. Oliveira for nutrient analysis; João F. C.Santos for assistance with graphics; Dr. Guisla Boehs for readingthe article and Dr. Maria Célia Villac for the numerous suggestionsand comments that helped to improve this work.

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