Changes in the Plankton Community According to Oceanographic Variability in a Shallow Subtropical Shelf: SW Atlantic

Hydrobiologia

https://doi.org/10.1007/s10750-019-3936-5 (0123456789().,-volV)(0123456789().,-volV)

PRIMARY RESEARCH PAPER

Changes in the plankton community according to oceanographic variability in a shallow subtropical shelf: SW Atlantic

Ba´rbara Santos Menezes . Luis Carlos Pinto de Macedo-Soares . Andrea Santarosa Freire

Received: 6 December 2017 / Revised: 6 March 2019 / Accepted: 8 March 2019 Ó Springer Nature Switzerland AG 2019

Abstract Copepods play a key role in marine revealed distinct seasonal communities. During winter ecosystems, acting as major primary consumers graz- the water was homogeneous, which supported the ing on phytoplankton or feeding on microzooplankton. even distribution of the dominant species and the Plankton communities are mostly structured by nutri- prevalence of the herbivore food chain throughout the ent availability and water temperature. The Subtrop- area. During summer the herbivore food chain ical Southwestern Atlantic Shelf has oligotrophic occurred in the bay area, being displaced by the conditions due to the predominance of the Tropical microbial food chain toward the shelf. The plankton Water in the upper layers. Its condition can change due community is determined by the homogeneity of the to cold water upwelling in summer, the northwards water during winter and by the environmental hetero- spreading of the Plata Plume Water in winter, and geneity during summer. local freshwater discharges. This study aimed to investigate the temporal and spatial variability in Keywords Copepods Á Microplankton Á Geometric plankton community in the shallow shelf off the shapes Á Plata Plume Water Á South Atlantic Central Brazilian coast (* 27°Sto48°W). Results of the Water PERMANOVA analysis and co-occurrence networks

Handling editor: Juan Carlos Molinero Introduction Electronic supplementary material The online version of this article (https://doi.org/10.1007/s10750-019-3936-5) con- Zooplankton plays a key role in marine food webs, tains supplementary material, which is available to authorized mainly in the energy transfer from primary producers users. to higher trophic levels. About 70% of the marine B. S. Menezes (&) Á A. S. Freire mesozooplankton in coastal ecosystems are copepods, Laborato´rio de Crustaćeos e Plaˆncton, Programa de Po´s- which act as major primary consumers grazing on Graduaçaõ em Ecologia, Departamento de Ecologia e phytoplankton in the grazing food web or feed on Zoologia, Universidade Federal de Santa Catarina, Floriano´polis, SC 88040-900, Brazil microzooplankton (20–200 lm), thereby linking the e-mail: [email protected] microbial to the grazing food chain (Longhurst, 1985; Calbet & Saiz, 2005; Sommer et al. in press). L. C. P. de Macedo-Soares Although almost all copepods are generalists, many Laborato´rio de Ecologia do Ictioplaˆncton, INCT-Mar COI, Instituto de Oceanografia, Universidade Federal do species are recognized to exhibit preferential trophic Rio Grande, Rio Grande, RS, Brazil regime (Bjo¨rnberg, 1981). The microzooplankton, 123 Hydrobiologia mainly ciliate protists, is considered a trophic link rich South Atlantic Central Water (SACW) (Mo¨ller between the microbial loop and the grazing food et al., 2008). In the SBB northern boundary, phyto- chain, feeding on nano- and picoplankton not captured plankton biomass increased by 80% after SACW by larger predators, such as copepods (Fernandes, upwelling and opportunistic copepods became dom- 2004; Stoecker et al., 2014). inant, establishing the herbivore food chain. In the In oligotrophic marine systems, large diatoms are absence of the SACW, the microbial trophic chain less effective in nutrient acquisition at low concentra- prevailed with pico- and nanophytoplankton domi- tions; thus, picoplankton, tiny diatoms, and dinoflag- nance and high contribution of microzooplankton ellates become dominant (Pomeroy, 1974). In this (Guenther et al., 2008). In winter the northward environment, the copepods diet is based on ingestion spreading of the Plata Plume Water (PPW) carries of ciliates, and a long and complex food chain is nutrients to the region (Acha et al., 2004;Mo¨ller et al., constituted (Calbet & Saiz, 2005). In eutrophic 2008). The expansion of the PPW triggered high environments, large diatoms are dominant and the phytoplankton abundance in the coastal zone (Mo¨ller grazing on phytoplankton by copepods is increased, et al., 2008) and occurrence of fish larvae and forming the classic food chain based on herbivores Argentine anchovy (Engraulis anchoita Hubbs & (Azam et al., 1983). In oligotrophic coastal environ- Marini, 1935) in the southern SBB (Macedo-Soares ments, plankton communities are strongly affected by et al., 2014), but its effect on mesozooplankton is still seasonal nutrient inputs whether by upwelling events, poorly understood. tidal fronts, or plume fronts produced by freshwater Located in the SBB southern boundary, the Santa discharges of continental runoff (Acha et al., 2004; Catarina shelf (* 26 to 29°S and 48°W) is the limit Brandaõ et al., 2015). These seasonal events can between tropical and temperate bioregions (Long- temporarily change the environment from olig- hurst, 2006). This region is recognized as the major otrophic to meso- or eutrophic condition and therefore Brazilian fishing ground (Castello et al., 2009). affect the food chain. Besides, copepods are good Studies on the plankton community associated the hydrological indicators due to their high abundance temporal variation of meroplankton and holoplankton and relatively short life cycle often associated with with the water masses and the SACW upwelling water masses (Bjo¨rnberg, 1981; Bradford-Grieve (Resgalla, 2011; Rutkowski et al., 2011). Copepods et al., 1999). and cladocerans were also associated with water Cell size has been widely studied in phytoplankton masses in the Santa Catarina shallow shelf (Domin- ecology either to estimate carbon fixation, energy gos-Nunes & Resgalla, 2012). In spite of the role of flow, or primary production (Rodrı´guez et al., 2001; copepods in plankton communities, other studies in Cermenõ et al., 2006). In addition to size, the the area were restricted to the occurrence of copepod geometric shape is an important functional trait to species (Lopes et al., 2006; Boos et al., 2012). The understand the dynamics of phytoplankton communi- phytoplankton was also associated with water masses ties (Naselli-Flores & Barone, 2011). However, there and seasonal changes with the dominance of large is still little knowledge about the relation between centric diatoms near the coast, small pennates along geometric shapes and the environment. Recent studies the mid-shelf, and flagellates over the 40- and 120-m in this field were carried out in the Adriatic Sea isobaths prior to SACW intrusion (Brandini et al., (Stanca et al., 2013) and in the Mediterranean Sea 2014). Based on the water mass dynamics in the Santa (Bernardi Aubry et al., 2017) showing phytoplankton Catarina shelf and the plankton trophic structure geometric shapes can be impacted by environmental driven by nutrient enrichment, our hypotheses are variability. that copepods and microplankton should also respond The Southern Brazilian Bight (SBB) located at * to the seasonality of the water masses establishing two 22° to 28°S is an oligotrophic system due to the types of the food chain. First, the herbivore food chain predominance of Tropical Water (TW) in the upper should occur under the nutrients input of SACW layers. However, during summer the interaction intrusion and the dispersion of coastal plumes, based between the northeastern wind and the bottom topog- on diatoms and herbivore copepods. Second, under raphy improves the availability of nutrients in the oligotrophic conditions, the food chain based on euphotic zone, through upwelling of cold and nutrient- heterotrophic plankton such as ciliates and 123 Hydrobiologia dinoflagellates as well as detritivores and carnivore Seawater and plankton were sampled in 6 of the 11 copepods should be established. sampling stations (Fig. 1). Water was collected with This study investigated the spatial variability in Van Dorn bottles at three selected depths (0.5 m, copepods and microplankton composition in distinct intermediary depth, and close to the bottom) for situations: (i) in the coastal area under the influence of analysis of dissolved nutrients and chlorophyll-a con- local river plume during winter and summer, (ii) in the centration. The intermediary depth was determined as 50-m isobath, influenced by shelf waters in winter and the depth of fluorescence peak, the thermocline depth, South Atlantic Central Water intrusion in summer. or half of the water column when both were absent. The nutrient and chlorophyll-a data were provided by the MAArE project team. Samples of 250 ml for Method quantitative analysis of microplankton were collected using Van Dorn bottles on subsurface of the water Study area column. Zooplankton was sampled using the cylindri- cal-conical net with 0.5-m diameter mouth and Oceanographic cruises were carried out in the central 200-lm mesh size, coupled with General Oceanics area of the Santa Catarina coast, which is part of the flowmeter. At each station, horizontal tows were Southern Brazilian Bight. The Santa Catarina shelf is a performed on the water column subsurface over 3 min subtropical system and represents the boundary for coastal stations and 5 min for Iso50 stations. The between tropical and temperate marine fauna (Long- mean (± SE) volume of water filtered by the net was hurst, 2006). The area includes the Arvoredo archipe- 45.0 ± 4.1 m3. All samples were preserved in 4% lago, which composes the no-take Arvoredo Marine buffered seawater-formaldehyde solution. Biological Reserve, referred to as REBIO Arvoredo (27°110–27°160S and 48°190–48°240W). The system is Samples processing oligotrophic due to the predominance of warm and saline Tropical Water (TW) at upper layers (Mo¨ller Microplankton was estimated in settling chambers et al., 2008). Eventually, the SACW upwelling, the using the Olympus IX-81 inverted microscope at PPW expansion, and the drainage of Tijucas River 9200 magnification. The volume examined was 10, improve nutrient enrichment (Acha et al., 2004; 25, or 50 ml with sedimentation time between 24 and Mo¨ller et al., 2008; Freire et al., 2017). The Tijucas 48 h, and the entire chambers were analyzed. All River continental runoff forms a brackish plume that organisms were identified to the lowest possible spreads throughout the region, hereafter referred to as taxonomic level according to Tomas (1997) and ‘‘Tijucas River Plume’’ (PRT) (MAArE, 2017a). Fernandes (2004). The phytoplankton taxonomic levels included family, genus, and species. Phyto- Sampling plankton taxa were also classified in morphotypes according to the geometric shapes following Sun & Sampling was conducted in the framework of the Liu (2003) and Olenina et al. (2006). The list of MAArE project (Monitoring Program of the Arvoredo phytoplankton morphotypes based on shape cells is Marine Biological Reserve) during August 2014 shown in the supplementary data (Online Appendix (austral winter) and February 2015 (austral summer). A). Aloricate ciliates were identified as spherical Sampling stations were distributed along two tran- (ACiS) or conical shape (ACiC), and tintinnids were sects: T1, perpendicular to the coast with seven kept at the lowest possible taxonomic level due to the stations (10 to 16); T2, in the 50-m isobath (Iso50) singularities of each one. Microplankton abundance with five stations [4, 5, 16, 17, and 22] (Fig. 1). was standardized in individuals per liter (ind. l-1) Salinity, temperature, depth, and dissolved oxygen according to the analyzed sample volume per (DO) were obtained in all stations using a Sea-Bird chamber. Electronics (SBE) 19 plus CTD with an SBE 43 To identify copepods, zooplankton samples were oxygen sensor. A Secchi disc was used to evaluate the subsampled into fractions that varied from 1/2 to 1/64 depth of the euphotic zone (ZEU). with Folsom splitter. The fraction chosen was diluted up to 1,000 ml, homogenized, and aliquots of 10 ml 123 Hydrobiologia

Fig. 1 a Map of the Southern Brazilian Bight and b REBIO (white dots): nutrients, chlorophyll-a, microplankton, and Arvoredo (dashed polygon), showing the sampling stations zooplankton sampling and CTD profiles; CTD stations (black distributed along two transects (T1 and T2). Plankton stations dots): salinity, temperature, and oxygen profiles were obtained. At least 100 copepods from each eigenvalues were validated for PC1 and PC2 by the sample were identified under the Nikon SMZ800 Kaiser-Guttman criterion. The PCA was run using HH stereoscopic and Olympus CX21 optical microscope and Vegan packages (Heiberger, 2013; Oksanen et al., and classified according to Bjo¨rnberg (1981), Brad- 2013). ford-Grieve et al. (1999), Razouls et al. (2005–2017), The SIMPER test (similarity percentages) was used and Walter & Boxshall (2017). Copepoda abundance to identify which copepod species most contributed to was standardized in individuals per m3 (ind. m-3). the similarities between winter and summer samples. For all following analyses, copepods and microplank- Data analysis ton abundances were fourth-root transformed to reduce the weight of abundant taxa. Two Procrustes Water masses were characterized according to the Rotation analyses (Legendre & Legendre, 1998) were thermohaline indices provided by Mo¨ller et al. (2008). carried out to verify whether copepods fitted to Principal components analysis (PCA) was performed microplankton. In both analyses, tintinnids taxonomic to investigate spatial and temporal patterns of the levels were included, but phytoplankton and aloricate sampling stations and their relationships with physical ciliates were addressed in one analysis as taxonomic and chemical variables (Legendre & Legendre, 1998). levels and in the other as geometric shape morpho- The data matrix was standardized, and the variance types. The function protest was used to check the inflation factor (VIF) was applied to diagnose significance of fits. Permutational Multivariate Anal- collinearity among physical and chemical variables; ysis of Variance (PERMANOVA) was performed depth, organic and inorganic suspended materials using a Bray–Curtis dissimilarity resemblance matrix were removed from the analysis (VIF [ 10). The to test the hypothesis that there are different 123 Hydrobiologia compositions of copepod species and microplankton Results between winter and summer and between the coast (stations 10, 12, and 14) and Iso50 (stations 4, 16, and Oceanographic conditions 22). To evaluate the occurrence of copepod species in The following water masses were identified in the relation to phytoplankton morphotypes and ciliates study area: Subtropical Shelf Water (STSW) and taxa four co-occurrence networks were performed. South Atlantic Central Water (SACW) (Fig. 2). The Two types of matrices of co-occurrence were con- STSW was prevalent in both seasons from the surface structed: first, one matrix with copepods as columns to 25 m depth in summer and 50 m in winter. During and microplankton morphotypes as rows and second, winter, low salinity levels (* 31 to 33) at T1 were one with ciliates as rows. The matrices were prepared associated with the plume of continental runoff from for winter and summer samples; each pair of cope- the Tijucas River (PRT). In addition to STSW, TW pod/phytoplankton and copepod/ciliates received a occurred at a depth of 20 m in T2 during the summer value that ranged from zero to six matching the (MAArE, 2017a). The SACW intrusion was registered number of samples where each pair co-occurred. The at T2 up to 35 m depth and reached the euphotic zone networks were constructed with the bipartite package only in station 16. The surface temperature ranged (Dormann et al., 2009) and the number of nodes, links from 18.4 to 19.6°C during winter and was around and connectance were calculated for each network. In 26.5°C during summer. Except for the low salinity of the network depiction, taxa are visualized as nodes and PRT, the water column was homogeneous in relation the links between nodes indicate the co-occurrence to both temperature and salinity in winter, while in between the taxa. The size of each node is proportional summer there was thermohaline stratification in T2 to the frequency of occurrence of the taxa. The link due to the presence of SACW and its mixture with TW width is proportional to the number of the co- and STSW (Fig. 2). occurrences between pairs of taxa. The connectance The first two PCs eigenvalues (2.72 and 1.89, is the ratio between the maximum number of possible respectively) explained 54.5% of the variability co-occurrences and the number of registered co- (Fig. 3). PC1 was the temporal axis (37.7%) with occurrences. low salinity and high dissolved oxygen (DO) in winter In addition, nestedness and modularity of each due to the intense mixture of water, depicted also by network were calculated and their significance was the lack of stratification (Fig. 2). Saline waters with tested with null models. Null models were generated high concentrations of nitrate and phosphate charac- constructing random matrices that retain row and terized the summer intermediate and bottom waters. column sums of the empirical networks (Gotelli, 2000; This axis disclosed the homogeneity of winter and the Hardy, 2008; Oksanen et al., 2013). The modules are environment stratification in summer. Due to summer groups of taxa more closely connected with each other thermal stratification, the temperature was not the than with taxa belonging to other modules (Olesen primary distinction between winter and summer. PC2 et al., 2007). Here modularity is an indicator of the (19.7%) axis represented the productivity in contrast- existence of distinct groups of copepods co-occurring ing waters: a high concentration of chlorophyll-a in with various phytoplankton morphotypes or ciliates the cold waters in winter and mid/bottom summer taxa. Nestedness implies that specialist taxa interact samples opposed to low chlorophyll-a concentration only with a part of the large group, being mainly linked in the warm surface summer waters in the 50 m to generalist taxa (Bascompte et al., 2003). isobath under oligotrophic TW influence. High chloro- The PCA, Procrustes, PERMANOVA, and net- phyll-a concentrations were associated with ammo- works analyses as well as all figures, except the nium in shallow stations of the PRT and with nitrate vertical profiles (Ocean Data View, Schlitzer, 2016), and phosphate enrichment of the SACW in summer. were performed in R (v3.2.4; R Core Team, 2016). The SIMPER analysis was carried out in PRIMER Copepoda assemblages v6.1 (Clarke & Gorley, 2006). We identified 52 copepod taxa of which 36 were identified to species level (Online Appendix B, 123 Hydrobiologia

Fig. 2 - Vertical distribution of temperature (color) and salinity Arvoredo surroundings. PRT Plume of the Tijucas River, SACW (contour) during winter 2014 (top) and summer 2015 (bottom) at South Atlantic Central Water, STSW Subtropical Shelf Water, T1 (perpendicular to the coast) and T2 (Iso50) in the Rebio TW Tropical Water

Table S2), being mainly omnivorous or generalist. Nine species were responsible for 91% of similarity High copepod density, represented by Acartia (Odon- (SIMPER test) of summer samples: T. turbinata tacartia) lilljeborgi Giesbrecht, 1889, was recorded (23%), O. giesbrechti (18%), T. stylifera (12%), C. near Tijucas River mouth during the summer furcatus and A. lilljeborgi (8%), O. venusta (7%), (Table S1 and Fig. 4). Excluding station 10, mean Agetus limbatus (Brady, 1883) (6%), Undinula vul- abundance (± SE) in winter (2,972 ± 895 ind. m-3) garis (Dana, 1849) (5%), and O. hebes (4%). In was higher than in summer (1,461 ± 672 ind. m-3). summer, the assemblages were dominated by few Eleven species, most omnivore-herbivore copepods, species. The coastal area showed the dominance of were found exclusively in winter, while six oceanic omnivore–herbivore species: station 10 had a high species—half carnivores—were registered only in relative abundance (RA) of A. lilljeborgi (97%), while summer samples (Table S2). in station 12 the dominance was shared between A. Species responsible for 89% of winter samples lilljeborgi and T. turbinata. At station 14, T. turbinata similarity (SIMPER test) were Temora turbinata became dominant. The Iso50 had the dominance of (Dana, 1849) (19%), Onychocorycaeus giesbrechti oceanic species with different trophic regimes: omni- (Dahl F., 1894) (14%), Temora stylifera (Dana, 1849) vore–herbivores as T. turbinata and Clausocalanus and Paracalanus indicus Wolfenden, 1905 (11%), copepodids and carnivore species of Corycaeidae Oithona plumifera Baird, 1843 (9%), Clausocalanus family (Fig. 4). furcatus (Brady, 1883) and Oncaea venusta Philippi, The procrustes analysis results showed a strong and 1843 (8%), Calocalanus styliremis Giesbrecht, 1888 signiﬁcant correlation between copepod assemblages (5%), and Oncaea cf. media Giesbrecht, 1891 (4%). and microplankton communities (Table 1) only when The winter assemblage consisted mainly of omnivore- phytoplankton and aloricate ciliates were classiﬁed herbivore species of the genera Paracalanus, Temora, into morphotypes (Online Appendix A). This result and the estuarine omnivore species Oithona hebes points out that the copepods were coupled to the Giesbrecht, 1891 throughout the entire coast, while in geometric shapes (morphotypes) of phytoplankton and Iso50 these species were replaced by omnivores and non-loricate ciliates and not to their taxonomic carnivores as O. plumifera, and O. giesbrechti identity. Based on this, the following results are (Fig. 4). 123 Hydrobiologia

Fig. 3 - First and second axes of the principal components analysis (PCA) performed with environmental data collected at: surface (S); intermediary depth (M); bottom (B) waters during winter 2014 (blue dots) and summer 2015 (red dots) in the Rebio Arvoredo surroundings. Amon ammonium, Cla chlorophyll-a, DO dissolved oxygen, Phos phosphate, Nitr nitrite ? nitrate, Sal salinity, Sil silicate, Temp temperature, ZEU euphotic zone depth, numbers— oceanographic stations

shown only for the geometric shapes of phytoplankton was dominated throughout the area by elongated and ciliates taxa. diatoms (Pen15), sharing with centric cylinder diatoms (Cdia8) at the coast (Online Appendix B, Microplankton community Fig. S1). In summer, ciliates accounted for about 40% of the microplankton in the entire area, except at The microplankton showed higher abundance in station 10. Dinoﬂagellates with rounded or combined winter with a smooth decrease towards the 50 m shapes (e.g., cone ? half sphere) showed an increased isobaths, excepting for the highest value at station 22, contribution toward the shelf. In summer, the station while in summer there was a high value only near near Tijucas River mouth had a similar composition to Tijucas River mouth (Table S1). Phytoplankton was the winter, with a high abundance of elongated always dominant among the microplankton, with the diatoms such as Pen15 and Cdia8. These diatoms highest and singular value at the PRT in summer, were responsible for peaks of abundance in Iso50 followed by the Iso50 in winter. Mean phytoplankton during the winter and on the coast in the summer. density (± SE) was higher in winter than in summer Microzooplankton showed high densities at the (14,653 ± 1,506 ind. l-1 and 5,663 ± 3,660 ind. l-1, Tijucas River plume in winter (Table S1), resulting in respectively). a higher mean (± SE) abundance in winter than in Phytoplankton taxa were classiﬁed into 18 mor- summer (1,853 ± 654 ind. l-1 and 1,200 ± 182 ind. photypes represented by 16 geometric shapes (Online l-1, respectively). Tintinnids as Coxliella spp., Appendix A). In winter, the community composition Eutintinnus spp. and Salpingella spp. were more

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Fig. 4 Copepoda composition showing species and taxa with Arvoredo surroundings. Species or taxa with RA B 4% were relative abundance C 4% at each sampling station of the coast grouped in the category ‘‘Other’’. The tones and hatch variation and Iso50 during winter 2014 and summer 2015 in the Rebio within the colors correspond to the species of the same family

Table 1 Results of the Procrustes analysis evaluating the Spatial and temporal changes in the plankton relationships between copepods and microplankton taxa and community networks between copepods and microplankton geometric shapes (morphotypes) The results of the PERMANOVA showed the plank- Protest/procrustes Sum of Correlation Signiﬁcance ton communities differed between winter and summer squares and between the coast and Iso50 (Table 2). Overall, Copepods versus 0.75 0.494 0.1 the spatial difference in copepod and microplankton microplankton (taxa) compositions was more pronounced in summer Copepods versus 0.55 0.664 0.011* (Figs. 4, S1). Winter showed a greater richness with microplankton 30 species of copepods, 17 phytoplankton morpho- (morphotypes) types, and 11 ciliates taxa. In contrast, in summer we *P \ 0.05 found 25, 14, and 8, respectively. In summer, microplankton and copepods abundances were coupled, with high values near Tijucas River mouth and abundant in winter especially in the PRT plume low values toward the 50-m isobath (Table S1). (Table S1). Tintinnopsis gracilis Kofoid & Campbell, The co-occurrence networks reﬂected the highest 1929, was recorded only at the coast in both seasons. richness of taxa in winter, when more nodes and links During summer, non-loricate ciliates became domi- were present compared to summer (Fig. 5, Table 3, nant among the ciliates in the entire area. and Online Appendix B: Fig. S2). Overall, the summer network of copepods vs. ciliates showed lower

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Table 2 Results of the PERMANOVA analysis testing for differences in the plankton communities Source Df Copepod species Microplankton morphotypes MS Pseudo-F Pr MS Pseudo-F Pr

Time 1 0.56 3.70 0.001*** 0.18 3.34 0.001*** Space 1 0.43 2.86 0.003** 0.13 2.36 0.032* Residuals 9 0.15 0.05 Total 11 PERMANOVA test for copepod species and microplankton morphotypes between winter and summer samples (Time) and the coast and Iso50 samples (Space) *P \ 0.05; **P \ 0.01; ***P \ 0.001 descriptor values than the other networks. During the throughout the area in winter and co-occurred with winter, this network had a trend to be less nested than Oithona, Temora, and Paracalanidae species. The the others, although the nestedness values were not uniform winter conditions yielded high plankton significantly different from the expected values of the richness and abundance. Especially in summer, the random networks constructed by the null model plankton communities were different in the coast- (P [ 0.05; Table 3). Opposed this, modularity was shallow shelf direction due to the stratification of the higher for the copepods vs. ciliates summer network water masses. In the shallow, shelf Clausocalanus and and also was not statistically significant (P [ 0.07; many other taxa co-occurred with non-loricate ciliates Table 3). Pennate diatoms with elongated shape and dinoflagellates. Toward the coast, the diatoms (Pen15) occurred throughout winter and summer gradually become dominant over the protists and (Fig. S1) being essential in both networks, linked to Acartia lilljeborgi and T. turbinata established their the main copepod species such as Clausocalanus dominance. Temora turbinata is an invasive species furcatus, O. giesbrechti, Oncaea venusta, and Temora established in Brazilian waters (Elmoor-Loureiro (Fig. 5). The omnivore–herbivore species as A. lillje- et al., 2016) with diversified diet including particulate borgi and O. hebes, and omnivore-carnivore Labido- matter, dinoflagellates and diatoms (Sant’Anna, cera fluviatilis Dahl F., 1894, co-occurred mainly with 2013), thereby adapting well to all environmental dinoflagellates and elongated diatoms in both seasons features. (Fig. 5). In relation to the ciliates, these copepod Copepods and microplankton were also organized species co-occurred mainly with Tintinnopsis in according to the extension of the plume of the Tijucas winter and with non-loricate ciliates in summer River. Estuarine-coastal species, such as Parvo- (Fig. S2). During the summer, omnivore–herbivore calanus crassirostris (Dahl F., 1894) and O. hebes and detritivore species such as Calocalanus pavo during winter and A. lilljeborgi during the summer, (Dana, 1852), Oithona tenuis Rosendorn, 1917, were highly abundant only close to the Tijucas River, Macrosetella gracilis (Dana, 1847), and the carnivores while gradually coastal-oceanic species become dom- Farranula gracilis (Dana, 1849) and Agetus limbatus inant further from the coast. During both seasons, the co-occurred mainly with dinoflagellates and non- cross-shelf gradient was indicated mainly by the loricate ciliates in the Iso50 (Figs. 5, S2). occurrence of A. lilljeborgi in opposition to M. gracilis, Calocalanus pavo, and Corycaeus speciosus Dana, 1849. A. lilljeborgi is an estuarine-coastal Discussion species and an indicator of coastal warm waters (Araujo et al., 2017) along the Brazilian coast, while Our findings showed the coupling of copepods and the other species are typical of the oceanic salty waters microplankton to the oceanographic variability with of the Brazil Current (Bjo¨rnberg, 1981). Acartia distinct winter and summer plankton communities. lilljeborgi was also previously recorded with high Elongated pennate diatoms were dominant and spread abundance in the nearby coast (Domingos-Nunes &

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Fig. 5 Co-occurrence networks between species of copepods exclusive of winter; orange—exclusive of summer. E-c estuar- and phytoplankton morphotypes (geometric shapes) in winter ine-coastal species, Oc oceanic species. Codes of copepod and summer. The size node corresponds to the occurrence species are shown in Table S2; codes of phytoplankton are number; the link thickness corresponds to the number of co- shown in Online Appendix A occurrences between nodes. Highlighted species: blue—

Resgalla, 2012). This species was strongly associated Ctenocalanus vanus Giesbrecht, 1888, Oithona setig- with the Tijucas River plume in summer, co-occurring era (Dana, 1849)) (Bradford-Grieve et al., 1999). with the high amounts of diatoms. The genus Acartia Moreover, most of the winter species are considered is a small omnivorous and opportunistic taxon, using small omnivores or generalist copepods that use the the resource that is most available (Benedetti et al., phytoplankton as an important food resource (Bene- 2016). detti et al., 2016). The high amounts of chlorophyll-a, Most of the exclusive winter species were recorded high abundance of phytoplankton, mainly diatoms, the in the Iso50 and are oceanic species (e.g., Nanno- presence of largest cells of Thalassionemataceae calanus minor (Claus, 1863), Calocalanus equali- Round, 1990, the low contribution of ciliates, together cauda (Bernard, 1958), C. pavoninus Farran, 1936), with the high dissolved oxygen and the lower apparent and/or indicative of cold coastal waters (e.g., oxygen utilization (MAArE, 2017a) in winter may

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Table 3 Values of descriptors for networks among copepods species and phytoplankton morphotypes and among copepods species and ciliates taxa during winter 2014 and summer 2015 Winter Summer Copepods versus Copepods versus Copepods versus Copepods versus phytoplankton ciliates phytoplankton ciliates

Nodes 47 41 39 33 Links 400 243 272 133 Connectance 0.78 0.73 0.77 0.66 Nestedness* 54.80 54.80 55.89 37.80 Modularity** 0.05 0.07 0.08 0.14 *P [ 0.05 for all networks; **P [ 0.07 for all networks indicate an autotrophic food web. The presence of showed that copepod assemblages responded to the herbivore copepods and the high abundance of phytoplankton shapes, there was no clear pattern of co- diatoms are an evidence of a grazing food chain occurrence of copepod species and phytoplankton (Brandini et al., 2014). The same condition was shapes. Some phytoplankton traits could have either registered close to the river mouth during summer enhanced or inhibited the interaction with the cope- indicating that the grazing food chain was restricted to pods. For example, particular geometric shapes can the shallow coast. facilitate the manipulation of the cells by herbivores The summer copepod assemblage had fewer (Naselli-Flores et al., 2007), while taxa with spines or species and of the six unique species, five were toxicity can reduce the grazing pressure of zooplank- oceanic species (e.g., Candacia pachydactyla (Dana, ton (e.g., Chaetoceros, Gymnodinium) (Tomas, 1997). 1849), Acrocalanus longicornis Giesbrecht, 1888, Although the co-occurrence among planktonic Corycaeus speciosus) and/or associated with the saline organisms cannot be directly interpreted as feeding waters of the Tropical Water and the South Atlantic interactions, the network descriptors can help in Central Water (e.g., Farranula gracilis, Undinula characterizing the community structure. The whole vulgaris) (Bjo¨rnberg, 1981; Bradford-Grieve et al., winter community and the summer copepod and 1999). Most species, especially those occurring in the phytoplankton network tended to be organized in a Iso50, are carnivorous copepods, feeding on dinoflag- nested way, although without a detected significance. ellates and ciliates (Benedetti et al., 2016). Moreover, Therefore, the community is less structured compared there were more ciliates and dinoflagellates than to perfectly nested networks (Bascompte et al., 2003), diatoms in the Iso50 during summer, which may meaning that there were no taxa or key species that indicate a microbial food web, where the microzoo- structured the plankton co-occurrence. For example, plankton acts as a link between the nanoplankton and the nested structure occurs in trophic networks when larger predators such as copepods (Guenther et al., the diet of the specialist taxa is a subset of the diet of 2008). the generalist taxa, indicating high feeding diversity The dominant geometric shapes of the phytoplank- and the decrease of competition (Delmas et al., 2017). ton during winter were elongated shapes of diatoms, Environmental heterogeneity and trophic specializa- while during summer, rounded and combined shapes tion lead to modular networks (Olesen et al., 2007), were dominant. These results suggest the effect of the where some taxa of a module interact more frequently environment on the selection of phytoplankton shapes. among themselves than with taxa of another module The same variability of shapes was registered for (Delmas et al., 2017). The copepods and ciliates coastal waters in the Adriatic Sea, under also similar network in summer displayed higher modularity than oceanographic shifts, with higher nutrient levels, a the other networks, suggesting the effect of the vertical mixture in winter, and a thermal stratification environmental heterogeneity. The dominance of gen- in summer (Stanca et al., 2013). Although the analysis eralist copepods with low trophic specialization

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(Bjo¨rnberg, 1981), the high richness and summer Conclusions spatial variability shaped the co-occurrence networks. The increase in copepods and microplankton driven The copepod and microplankton community in the by the plume of the Tijucas River (PRT) was restricted shallow subtropical shelf unveiled the seasonality of to the shallow coastal area. Apart from that area, the the water masses and the local coastal plume effect. A abundance of copepods and microplankton was high in plentiful plankton community, based on elongated winter, indicating another source of enrichment in the diatoms and herbivorous copepods, inhabited the well- shelf. Sea surface temperature and chlorophyll con- mixed cold winter waters, enriched by the arrival of centration satellite images (Freire et al., 2017) and the remote water mass with continental properties. Local reverse thermocline (MAArE, 2017a) showed the continental runoff allowed also the establishment of presence of Plata Plume Water (PPW). Nutrients the herbivorous food chain in the coastal area in both carried by PPW in winter are significant for the seasons. In summer, the coastal community was Southern Brazilian Bight due to its oligotrophic characterized by low diversity and high density and characteristic (Acha et al., 2004;Mo¨ller et al., 2008). changed progressively to a rich assemblage of cope- In summer, the plankton diversity enhanced toward pods, ciliates, and dinoflagellates in the warm surface the shelf, but the SACW intrusion in the mid layer did shelf waters. Although the copepod assemblage dis- not improve the abundance of copepods in the surface closed the effect of the South Atlantic Central Water waters. intrusion in the mid layer, its nutrient enrichment did Regional oceanographic conditions are strongly not lead to a grazing food web in the surface waters as regulated by wind pattern (Castro et al., 2006), and this was expected. The nutrient enrichment by the local study was conducted under typical weather conditions, river, coupled with the expansion of Plata Plume with the predominance of northeast winds in summer Water, was pivotal to change the oligotrophic charac- and southern winds in winter (MAArE, 2017b). The teristics of the environment. The plankton community complex hydrodynamic field and unstable weather was structured by the seasonal environmental condi- conditions can lead to interannual variability in tions of the subtropical realm, while the high richness summer and winter (Brandini et al., 2018; Fontes typical of tropical waters together with the dominance et al., 2018). Nevertheless, the shifts between oceano- of generalist copepods contributed to weak co-occur- graphic conditions of summer and winter are so rence networks. The community structure and the prominent (Brandini et al., 2018) that our findings can oceanography complexity depicted the transitional be considered proxies of the region. properties of the southern boundary of the South High plankton abundance during the winter impacts Brazil Bight. the whole marine food web. The region is recognized as major fishing ground in the Brazilian coast (Castello Acknowledgements We would like to thank the MAArE et al., 2009), with high capture of planktivorous project team for logistical support, especially Dr. Charles Gorri for the zooplankton sampling and processing. Dra. Melissa ichthyofauna, such as Mugil spp., Sardinella Carvalho and Prof. Alessandra L. Fonseca provided chlorophyll brasiliensis (Steindachner, 1879), and Engraulis and nutrient data, respectively. We are also grateful to a couple anchoita—the latter being strongly associated to the of researchers for help with the fieldwork and plankton sorting. ´ Plata Plume Water (Macedo-Soares et al., 2014). M.Sc. Erica C. Becker helped with microplankton identification, Dra. Cristina O. Dias assisted in copepod identification and Dra. During summer, the high temperature and low nutri- Denise R. Tenenbaum for the initial discussion. We thank Prof. ents at the surface favored the presence of gelatinous Miguel P. Guerra and Dr. Hugo P. F. Fraga for providing the zooplankton like the carnivorous chaetognaths and the inverted microscope and Dr. Eduardo L. H. Giehl, Prof. Fa´bio G. filter feeders salps toward the shelf (Freire et al., Daura Jorge, and Dr. Mauricio Cantor for guidance regarding Procrustes and network analysis. We also thank CAPES (first 2017). Thus, the wind patterns and oceanographic author Grant); CNPq (312644/2013-2 and 311994/2016-4 Grant dynamics change the plankton food web and, conse- to ASF and 150476/2017-5 Grant to LCPMS), the Chico quently, the entire pelagic ecosystem since most of Mendes Institute of Biodiversity Conservation (ICMBio), and these organisms feed on plankton at some life stage. PETROBRAS. The implementation of the project MAArE— Monitoramento Ambiental da Reserva Biolo´gica Marinha do Arvoredo e Entorno—is a condition set by the ICMBio in the context of IBAMA’s environmental licensing process. We also

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