Short-term variation of plankton spatial distribution at a subtropical mixed estuarine system

Abstract

The horizontal distribution of plankton communities in a subtropical mixed estuarine system over one tidal cycle was investigated. Hydrological and planktonic samples were obtained twice on 17 July 2007 in a transect with ten stations in the Babitonga Bay estuary, south Brazil (~26°S). Hydrological variables did not vary spatially or tidally during samplings. However, in the cluster analyses both phyto and zooplankton were structured according to their estuarine position and in the inner stations also by the tidal condition. Phytoplankton abundances were higher during flood tide in the inner estuary (max. 122,583 ind.L^-1), where diatoms dominated, particularly Diploneis bombus. However, the density at ebb tide increased towards outer estuary (max. >100,000 ind.L^-1) and flagellates, mostly Gymnodinium spp., became abundant. Zooplankton abundances were higher at intermediate stations during both tides (max. 13,691 ind.m^-3). The innermost stations were dominated by the copepod Acartia tonsa, while in the outermost stations Temora turbinata and the polychaete larvae Loimia sp. dominated. The results demonstrate how variable the estuarine plankton horizontal structure can be over short time-scales even in mixed estuarine systems under relatively homogeneous conditions, highlighting the importance to consider such temporal scales for a more accurate understanding of the dynamics of these communities.

Key words
Babitonga Bay; mixed estuaries; phytoplankton; plankton dynamics; tidal variation; zooplankton

INTRODUCTION

The time-scales for physical processes in estuaries are variable and driven primarily by the relative intensity of daily tidal fluctuations and seasonal changes in the freshwater flow (Boero 1994, Day et al. 2013). Tidal oscillation is especially important for plankton variability (Menéndez et al. 2012, 2015, Day et al. 2013), and rapid fluctuations in physical-chemical factors may be experienced by organisms through the tidal cycle in both horizontal and vertical axes (Laprise & Dodson 1993). Thus, biological responses to environmental variability in estuaries are difficult to predict because of the simultaneous and multifactorial relationships of environmental variables (Elliott & McLusky 2002). Besides this, interspecific differences mostly in salinity tolerance also account for shifts in the species dominance along the estuary and/or the tidal condition, emphasizing the role of this variable in the spatial and/or short-scale temporal structuring of these communities (Telesh 2004, Telesh & Khlebovich 2010, Menéndez et al. 2012, 2015, Day et al. 2013).

Numerous studies have focused on short-term plankton variability in estuaries (Dalal & Goswami 2001, Menéndez et al. 2012, Guenther et al. 2012, 2015, Sin & Jeong 2019). Most of such studies have sampled one fixed station many times all over the tidal cycle (Chandran 1985, Garcia-Soto et al. 1990, Bernát et al. 1994, Araujo et al. 2008, Marques et al. 2009, Guenther et al. 2012, Menéndez et al. 2012, 2015, Sin & Jeong 2019). This approach allows describing fine temporal changes in the assemblages, providing valuable information on the influence of tidal condition through time. However, it has limited spatial resolution, hampering a better understanding of how tidal cycle modifies the horizontal structure of plankton communities. Moreover, most of these studies have been conducted in estuaries with large physical-chemical gradients, and mixed estuaries with more homogeneous conditions have been considerably less studied. Thus, one question that remains open is how tide condition may affect the horizontal structure of the plankton assemblages in these estuaries.

The Babitonga Bay estuary (BBE) is a mixed subtropical estuary situated at a high priority area for conservation on the Brazilian coast (IBAMA 1998, MMA 2007). The region has a marked seasonality both in temperature and rainfall, with a rainy summer and a dry winter (Cremer et al. 2006, Alvares et al. 2013). Previous studies in the BBE have showed that the salinity gradient is one of the most important factors structuring the horizontal distribution of planktonic communities (Brandini et al. 2006, Costa & Souza Conceição 2009, Nogueira Júnior & Oliveira 2017). However, plankton distribution has been previously analyzed only considering seasonal time-scale, and nothing is locally known about short-term dynamics (Nogueira Júnior & Costa 2019). In the present study, we aim to test differences in the horizontal structure of the phyto and zooplankton assemblages during ebb and flood tide in this mixed estuary. We developed the present study in the winter and neap tide to be representative of a condition of reduced continental runoff and lower tidal range, respectively.

MATERIALS AND METHODS

Study area

The Babitonga Bay estuary (BBE; 26°13’44”S 48°40’40”W), southern Brazil, is a permanently open basin with 21 km in length, maximum width of 2 km in the central channel and area of 1567 km² (Supplementary Material - Figure S1) (IBAMA 1998). The depth in the central channel is 10 m, with the maximum of 28 m at the mouth. The innermost area of the estuary is shallower (<5 m), composed of extensive mangroves and tidal flats (Noernberg et al. 2020). Although the estuary receives water flows from many rivers, it is considered vertically homogeneous to weakly stratified estuary in its physical-chemical parameters (IBAMA 1998, Noernberg et al. 2020). The microtidal regime is mixed with semidiurnal dominance (with duration of nearly six hours between low and high tide). The mean tidal height is 0.84 m and the maximum is 1.9 m during spring tide, with tide amplification in the innermost portions (Truccolo & Schettini 1999, Knie 2002). The average annual rainfall is around 2265 mm, reaching higher values in spring-summer (October to March), average of 672 mm, and lower ones in autumn-winter (April to August), average of 190 mm (Cremer et al. 2006).

Sampling methods

The samplings occurred on 17 July 2007 in 10 stations ~2-4 km apart from each other, during the winter and neap tide, over one tidal cycle. Samplings were performed twice in shallow estuarine waters: i) during the day in the flood tide (~9:30-13:00) from the inner to the outer estuary in the transect (station 1 to 10; Figure S1); ii) during the night in the ebb tide (~18:00-21:30) from outer to the inner estuary (station 10 to 1). The samples from station 10 during the ebb tide were lost and consequently were not included in the present study. During the samplings the wind blew mostly from SSE and the highest speed was 3.6 m/s at 18:00 and the lowest was 0.3 m/s at midnight. The tidal amplitude varied from 0.1 m at 9:24 to 1.6 m at 17:38. Wind and tidal data used in the present study is available at the National Meteorological Institute (INMET) and at the Brazilian Navy Hydrography Center, in the São Francisco do Sul Harbor station (26°14.7’S, 48°38.4’W), respectively.

Phytoplankton was sampled with vertical hauls using a conical plankton net with 20 μm mesh and mouth diameter of 30 cm, from near the bottom to the surface. Samples were fixed with 0.4% formaldehyde. Using a bottle sampler, water samples were taken from the subsurface for the study of the taxonomic composition and quantitative analysis of densities and biomass of the phytoplankton. Water aliquots were removed from the water-sampler, fixed with 0.8% acetic Lugol (Edler 1978) and stored in amber glass bottles for later laboratory analyses. Subsurface water samples were taken and filtered with Whatman filters (25 mm diameter, GF/F) for latter chlorophyll-a measurements in the laboratory.

Zooplankton samples were taken by five-minute oblique hauls through most of the water column using a cylindrical-conical plankton net, with 60 cm mouth diameter, 200 µm mesh-size, and a calibrated Hydrobios mechanic flowmeter attached (the average volume filtered was ±SD 24±8.2 m³ ranging between 10 and 38 m³). The zooplankton collected was preserved in 4% buffered formaldehyde solution.

Vertical profiles of temperature, salinity, pH, dissolved oxygen and total dissolved solids were obtained at each station with a multiprobe YSI-556 MS.

Laboratory and data analyses

In the laboratory, net phytoplankton aliquots were oxidized and mounted on slides and coverslips (Hasle & Fryxell 1970). Taxonomic identifications followed mainly Tomas (1997), Round et al. (2000), Tenenbaum et al. (2004), Landucci & Ludwig (2005), and Sar et al. (2007). Phytoplankton cells were counted in Utermöhl (1958) 10 mL sedimentation chambers using a Zeiss model ED-03 inverted microscope with phase-contrast optics (Hasle 1978).

Nano-sized cells (2–20 µm) were counted at 400x magnification over diameter transects until a minimum of 100 cells was reached. Micro-size cells (>20 µm) were counted at 160x magnification over the entire bottom area of the Utermöhl chamber or in half the chamber, depending on cell density, to reach a minimum count of 300 cells. Cell densities per liter were calculated according to Semina (1978). Chlorophyll-a was read in the laboratory on a Turner Designs – Trilogy calibrated fluorometer (Parsons et al. 1984).

Zooplankton was identified and counted from 10 mL aliquots of each sample, counting 300 organisms at least. The specimens were identified to the lowest taxonomic level possible (following mainly Boltovskoy 1981, 1999). The density of zooplankton was standardized as individuals.m^-3, considering the filtered volume of water. Zooplankton wet weight was estimated from three 10 mL aliquots of each sample. Large macroscopic gelatinous zooplankton were manually removed and the aliquots were rinsed with distilled water in a 100 μm sieve, latter they were dried with blotted paper (Boltovskoy 1981, Omori & Ikeda 1994), and weighed using a digital analytical balance with precision of 0.1 mg.

Multivariate patterns of phytoplankton and zooplankton assemblages were determined and visualized using hierarchical agglomerative clustering techniques based on the Bray-Curtis similarity measures after square-root transformation. The similarity percentage analysis (SIMPER) was used to identify the species that mostly contributed to similarities within each identified group (Clarke & Gorley 2006). These analyses were performed using the PRIMER V.6 software. In order to test the influence of the explanatory variables on dominant phyto and zooplankton taxa, we used a constrained-ordination analysis (Lepš & Šmilauer 2003), using the software CANOCO ver. 4.5. The length of the gradient was short suggesting that most species would exhibit a linear response to the explanatory variables and thus we used the redundancy analysis (RDA; Jongman et al. 1995, ter Braak & Šmilauer 1998, Lepš & Šmilauer 2003). The RDA was performed for phytoplankton and zooplankton separately. The explanatory variables for phytoplankton included total abundance of zooplankton (ind.m^-3), temperature (°C), salinity, dissolved oxygen (mg L^-1), total dissolved solids (g L^-1), and pH. For zooplankton, the following explanatory variables were tested: total abundance of phytoplankton (cells L^-1), temperature, salinity, dissolved oxygen, total dissolved solids, and pH. Before the analyses, the explanatory variables were centered and standardized and the response variables were square root-transformed. The significance (P<0.05) of the canonical axes were tested using the Monte Carlo randomization procedure (999 runs) (Lepš & Šmilauer 2003).

RESULTS

Hydrological variables

The water column was vertically homogeneous during samplings, thus only average values of hydrological variables are presented. The hydrological variables were also mostly horizontally homogeneous and similar in both tide conditions (Figure 1). Mean temperature was slightly higher towards the inner estuary, with a maximum of 18.3°C at station 3, about 2°C warmer than the outermost station (Figure 1a). As expected, salinity, dissolved oxygen, and pH were lower in the inner estuary, increasing in the outer estuary. Salinity varied from the mean of 27.5 to 31.4 (Figure 1b), dissolved oxygen from 6 to 8.4 mg L^-1 (Figure 1c) and pH from 7.8 to 8.1 (Figure 1d). Total dissolved solids was higher in the intermediate stations reaching values around 29 g L^-1 (Figure 1e).

Figure 1
Average (between subsurface and bottom) values of temperature (a), salinity (b), pH (c), dissolved oxygen (d), and total dissolved solids (e) at each sampling station and tide condition in the Babitonga Bay estuary.

Phytoplankton

Maximum chlorophyll-a values were recorded at station 2 during flood and ebb tide (Figure 2a, b; 2.3 and 2.2 mg m^-3, respectively) and minimum at station 9 and 10 (0.7 and 0.9 mg m^-3, respectively). During flood tide, phytoplankton total abundances tended to increase in the inner estuary, reaching highest values between 110-123,000 cells L^-1 in the stations 1-3, nearly three times higher than in the ebb tide in the same stations (Figure 2c, d). However, relatively high abundance (80,711 cells L^-1) was also recorded at station 9. During ebb, phytoplankton abundances tended to increase towards the estuarine mouth, reaching the maximum of 85,000 ind.L^-1 at station 9. Abundance was dominated by diatoms in all stations and tidal condition, with centrics and pennates as the most representative groups. Flagellate abundance was usually comparatively lower, tending to increase in the outer estuary in both tide conditions (Figure 2c, d).

Figure 2
Chlorophyll-a concentration (a, b; mg m^-3), total phytoplankton abundance (10³ cells L^-1; c, d) and number of species (e, f) at each sampling station and tide condition (flood and ebb tide) in the Babitonga Bay estuary.

A total of 91 species of phytoplankton were found (Table SI). Maximum number of species was 48 and 49 at station 7 and 8, and minimum of 25 and 27 species at station 4, during flood and ebb tide respectively (Figure 2e, f). In general, the total number of centric and pennate species did not vary between samplings stations, oscillating between 10-16 for centric and between 9-15 species for pennates. Flagellates occurred mostly in the outer estuary, increasing the number of phytoplankton species at these stations (Figure 2e, f).

The cluster analysis identified four distinct assemblage groups for phytoplankton (Figure 3a). The groups reflected the spatial distribution of the outer stations (group 4 – stations 9-10; group 3 stations 7-8) and the tide condition for the intermediate and innermost stations (group 2 stations 1-6 during the ebb tide; group 1 stations 1-6 during the flood). Within groups 1 and 2 occurred a tendency to a further subdivision at the ~50% similarity level, in both cases separating the stations 1-4 from the 5-6. According to the SIMPER routine the diatoms Diploneis bombus and Paralia sulcata, were the most important species for the formation of the groups 1 and 2 (Figure 3a). Diploneis bombus was also the most important species for group 3, along with the dinoflagellate Gymnodinium spp. and the diatom Fallacia spp. For group 4, Thalassionema nitzschoides and Gymnodinium spp. were the most representative species.

Figure 3
Hierarchical clustering between samples based on Bray-Curtis similarity (%) of phytoplankton (a) and zooplankton (b) assemblages from the Babitonga Bay estuary showing the formed groups and the results of the SIMPER analysis (boxes). Between parentheses is shown the average similarity within each group and the mean abundance (Ab) and percentage of contribution (% C) of each species to the formation of the groups; f - flood tide, e - ebb tide.

The Monte Carlo test indicated significant relationships between the canonical axes of the RDA and the environmental variables (P<0.001). The first four canonical axes explained 61.5% of the total variance of the phytoplankton assemblage. The first axis explained 37.8% and was mostly negatively related to temperature and total dissolved solids (Table SII, Figure 4a). The second axis explained a further 12.1% of the data variance and was mostly negatively related to zooplankton abundance and total dissolved solids. The third and fourth axes were mostly positively related to pH and dissolved oxygen and negatively to temperature, and together explained a further 11.6% of the assemblage variance (Table SII). Temperature was positively related mostly to Skeletonema costatum and Dynophysis acuminata, and also to Eucampia zodiacus, Thalassiothrix sp., and Pleurosigma angulatum in a lesser extent. Temperature was negatively associated with Gymnodinium spp., Fallacia spp. and Prorocentrum spp. Higher values of total dissolved solids were mainly associated with Diploneis bombus, Thalassiosira mala and Actinoptychus senarius, while lower values were related to Actinocyclus normanii and Thalassionema nitzschoides. Pleurosigma angulatum, unidentified pennate, Eucampia zodiacus and Thalassiothrix spp. were negatively associated with salinity, dissolved oxygen and pH (Figure 4a).

Figure 4
Ordination diagrams of the Redundancy Analysis of the phyto (a) and zooplankton (b) assemblages from Babitonga Bay estuary showing the first and second canonical axes. Dotted black vectors are the explanatory variables and grey vectors are the dependent variables. Circles represent the distribution of the stations during flood (open circles) and ebb (gray circles) tide. The percentage of the species data variation explained by each axis is shown in parentheses. Explanatory variables codes: sal = salinity; DO = dissolved oxygen; zoopl = total zooplankton abundance; TDS = total dissolved solids; temp = temperature; phytopl = total phytoplankton abundance. Phytoplankton taxa codes: Anor = Actinocyclus normanii; Asen = Actinoptychus senarius; CNI = centric diatom not identified; Dac = Dinophysis acuminata; Dbom = Diploneis bombus; Din = dinoflagette not identified; Dsur = Delphineis surirella; Ezod = Eucampia zodiacus; Fal = Fallacia spp.; Gym = Gymnodinium spp.; Ldan = Leptocylindrus danicus; Pang = Pleurosigma angulatum; PNI = Pennate not identified; Pror = Prorocentrum spp.; Psul = Paralia sulcata; Scos = Skeletonema costatum; Tcoa = Tryblionella coarctata; Thals = Thalassiosira spp.; Thalt = Thalassiothrix sp.; Tmal = Thalassiosira mala; Tnit = Thalassionema nitzschioides. Zooplankton taxa codes: Alil = Acartia lilljerborgi; Aton = Acartia tonsa; Biv = Bivalve; Cory = Corycaeus spp.; Eacu = Euterpina acutifrons; Dec = Decapoda sp.2; Loim = Loimia sp.; Odio = Oikopluera dioica; Oheb = Oithona hebes; Oplu = Oithona plumifera; Pavi = Penilia avirostris; Pcra = Paracalanus crassirostris; Pleo = Pleopis polyphemoides; Pqua = Paracalanus quasimodo; Proc = Procerastea spp.; Sre = Stauridiosarsia reesi; Ttur = Temora turbinata.

Zooplankton

Higher zooplankton biomass (>80 mg m^-3) was observed at intermediate stations (5, 6 and 7) in both tides, especially during ebb when reached the highest value of 164 mg m^-3 at station 6 (Figure 5a, b). Minimum values were registered at station 9 during flood tide (5.4 mg m^-3) and 1 during ebb (3 mg m^-3). In general, zooplankton was more numerous in the intermediate-outer stations during both tide conditions, with highest values at stations 5, 6, and 8 (max. of 13,691 ind.m^-3 during ebb tide at station 6; Figure 5c-f). During the flood tide, maximum abundance was recorded at station 5 (7870 ind.m^-3). The lowest densities were recorded in the innermost station (station 1) for both tides, with minimum of 23 and 279 ind.m^-3 respectively during flood and ebb tide. Copepods dominated the zooplankton, with maximum of 7684 ind.m^-3 at station 5 and 12,700 ind.m^-3 at station 6, during flood and ebb tide respectively (Figure 5c, d). In general, copepods represented 87.5% of the total zooplankton except for station 9 during the flood tide, when they were only 14% and polychaetes 83%. Polychaetes occurred abundantly from the intermediate stations towards the estuarine mouth, reaching densities >400 ind.m^-3 at the stations 8-10 during the flood tide and at station 9 during ebb (Figure 5e, f). Cladocerans also were more abundant in the outer estuary, reaching up to 600 ind.m^-3 during ebb tide at station 8 and 350 ind.m^-3 during flood tide at station 7. Decapod larvae were more abundant at the intermediate estuary, especially during ebb tide, reaching 462 ind.m^-3 at station 6.

Figure 5
Zooplankton biomass (mg m^-3; a, b), copepods abundance (10³ ind. m^-3; c, d), zooplankton abundance without copepods (10³ ind. m^-3; e, f ), and number of species of main higher taxa (g, h) at each sampling station and tide condition in the Babitonga Bay estuary.

A total of 64 species of zooplankton were sampled (Table SIII). As well as for phytoplankton, higher zooplankton diversity was registered in the outer estuary, with a maximum of 30 and 33 species at station 9 in both tide conditions and minimum of 8 in the flood tide (station 1) and 14 in the ebb (station 2) (Figure 5g, h). Copepods (maximum of 12 spp.), polychaetes (max. 5 spp.) and other taxa were more diverse in the outermost stations. Decapods were more representative in the intermediate-outer estuary, reaching a total of 10 spp. at station 5 during ebb tide and 5 spp. at station 7 during both tides (Figure 5g, h).

As for phytoplankton, the cluster analysis identified distinct zooplankton assemblages structured according to the horizontal distribution and/or tide condition of the samples (Figure 3b). Six groups were formed at 55% similarity level. Two groups were formed by inner stations (1-4) according to the tide condition (group 1 - flood; group 2 - ebb). Group 3 was formed by the stations 5 and 6 during ebb; group 4 by the stations 5-8 during flood tide; group 5 by the stations 7 and 8 during ebb tide, and group 6 included the outermost stations (9 and 10) during both tides conditions. Acartia tonsa was the main species contributing to the similarity in group 1 and 2. Oithona hebes was also important for group 1, and Acartia lilljeborgi for group 2. Group 3 was mainly composed by Temora turbinata and Acartia tonsa. The copepods Temora turbinata, Acartia tonsa, and Oithona hebes were also the most representative species from group 4. For group 5 Temora turbinata was also the most representative species. Group 6 was mainly formed by the polychaete Loimia sp. and the copepod Temora turbinata, along with the cladoceran Penilia avirostris (Figure 3b).

The Monte Carlo test indicated significant relationships between the canonical axes of the RDA and the environmental variables (P<0.001). The first four canonical axes explained 84.0% of the total variance of the zooplankton assemblage (Table SIV). The first axis explained 52.9% and was mostly positively related to dissolved oxygen, salinity, pH and negatively to temperature. The second axis explained 20.3% of the data variance and was mostly positively related to phytoplankton abundance and negatively to total dissolved solids (Table SIV; Figure 4b). Loimia sp., Penilia avirostris, Paracalanus quasimodo, Corycaeus spp. and bivalvians were negatively related to temperature and positively mostly to salinity and dissolved oxygen. Differently, species such as Oithona hebes, Acartia tonsa, Acartia lilljeborgi and Oikopleura dioica had the opposite distribution, positive with temperature and negative with salinity, dissolved oxygen and pH (Figure 4b). Phytoplankton abundance was mostly negatively associated with Temora turbinata, but also to Paracalanus crassirostris and Pleopis polyphemoides. in a lesser extent.

DISCUSSION

In the present study, both spatial gradients and tidal oscillations were important to structure the plankton assemblages at a short-term perspective, in spite of the relatively small environmental variability during our samplings. Phyto and zooplankton formed relatively similar patterns following the estuarine horizontal gradients and/or tide condition (Figure 3a, b). From cluster results, we observed that the tidal variation influenced the planktonic community structure in the inner sites and such influence was less noticeable near the estuarine mouth. In general, the innermost stations (1-5) were split according to the tidal condition while in the other stations the pattern of clustering followed mostly the transect stations.

The analysis of plankton distribution at a short-term perspective is complex and highly influenced by local advection and turbulent mixing processes (Garcia-Soto et al. 1990, Dalal & Goswami 2001, Menendez et al. 2012). Diel and/or tidal zooplankton vertical migration also may include further complexities to our data (Anger et al. 1994, Meester & Vyverman 1997, Mecalco-Hernández et al. 2018). However, our samplings integrated the whole water column diminishing the bias these migrations may cause, and thus the observed patterns are unlikely to have been strongly influenced by them.

Most of the species captured in the present study are euryhaline and typically found in warm brackish-water ecosystems worldwide (Devassy & Goes 1988, Sassi 1991, Huang et al. 2004, Li et al. 2006, Madhu et al. 2007, Araujo et al. 2008, Dias et al. 2018). The abundance and diversity levels, as well as species composition and assemblage structure of both zoo and phytoplankton found here can be considered as typical of winter conditions from BBE and other nearby Southwestern Atlantic subtropical estuaries (Montú & Cordeiro 1988, Brandini et al. 2006, Miyashita et al. 2012, Salvador & Bersano 2017, Nogueira Júnior & Costa 2019).

The abundant centric diatoms Diploneis bombus and Paralia sulcata were the most important phytoplankton species for the formation of the inner groups in both flood and ebb tide (groups 1 and 2). These species are commonly found at tidal flats and salt marshes (McQuoida & Nordberg 2003), including tropical and subtropical estuaries from southwestern Atlantic (Procopiak et al. 2006, Haraguchi et al. 2015, Gonçalves-Araujo et al. 2018). Tidal flats and salt marshes are mainly found in the inner – and shallower – regions of the BBE (Vieira & Horn Filho 2017), which may have contributed to an increase in their abundance at this portion in the present study. Among the mechanisms responsible for suspending benthic microalgae on the water column, waves generated by winds (Holland et al. 1974) and tidal currents (Shaffer & Sullivan 1988) are common. Previous studies already discussed that the turbulence may favor microalgae suspension and its entrainment into the water column, especially during flood tide when currents are stronger in the BBE (Truccolo & Schettini 1999), and during winter also with stronger winds (Brandini et al. 2006). Indeed, the positive relation of both D. bombus and P. sulcata to total dissolved solids in the water column in the present study (Figure 4a) also support this view and suggest an association with resuspension processes.

The copepods Acartia tonsa and Oithona hebes dominated zooplankton communities in the inner stations in both tide conditions, while Temora turbinata was more important in the outer estuary. The cyclopoid O. hebes is commonly found in mangrove habitats (Rocha 1986), while the calanoids A. tonsa and T. turbinata preferentially colonize areas of the inner and outer estuary, respectively (Lopes et al. 1998, David et al. 2005, Brandini et al. 2006, Miyashita et al. 2012). Indeed, A. tonsa and O. hebes were related to lower values of salinity, dissolved oxygen and pH (Figure 4b) registered in the innermost stations in the estuary.

In the outer and deeper estuary, the pennate diatom Thalassionema nitzschioides and the dinoflagellate Gymnodinium spp. were the most important phytoplankton species. They are indeed commonly associated with intermediate and higher salinities and are mainly found in the outer estuarine portions (Mani & Khrishnamurty 1989) and shelf waters (Gonçalves-Araujo et al. 2018). For zooplankton, the high densities of the copepod Temora turbinata and the cladoceran Penilia avirostris in the outer portions also evidences the mixing of neritic coastal waters within the estuary (Li et al. 2006). Both species are very frequent and abundant at the adjacent shallow shelf (Brandini et al. 2014, Domingos-Nunes & Resgalla Jr 2017, Becker et al. 2018), being also commonly captured in the outer estuary (Brandini et al. 2006, Teixeira-Amaral et al. 2017, this study). The sites near the estuarine mouth (stations. 9-10; group 6) were largely defined by the polychaeta larvae Loimia sp., what is in accordance to previous observations in the BBE that associated this taxon with higher salinities in the outer BBE (Nogueira Júnior & Oliveira 2017).

Although the methodology applied here is adequate to assess the horizontal distribution of zooplankton, it is important to note that there are limitations. Due to the small boat used and distances between sampling stations (2-4 km), we spent about 3.5 hours at each transect and we could not observe finer spatiotemporal changes in the plankton assemblages. Besides this, only one day was investigated and more days of sampling in different environmental conditions are necessary. In any case, considering that the knowledge of the variability of the estuarine plankton composition and abundance at different temporal and spatial scales is a prerequisite for understanding the coastal dynamics, the present study is relevant because is a pioneering attempt to depict the horizontal pattern of plankton along a tidal scale in a subtropical, mixed estuary. Particularly considering that most of the previous studies analyzed large environmental gradients and short-temporal changes over a single or few stations (Chandran 1985, Guenther et al. 2015, Wan Maznah et al. 2016), hampering the understanding of tidal variations in the horizontal structuring of these communities.

In conclusion, our results suggest that the environmental gradients and tidal oscillation do structure the spatial patterns on plankton communities even in mixed estuaries under small gradients and relatively homogeneous conditions. We observed communities tending to group according to the horizontal estuarine gradients and tidal cycle, with higher differentiation between ebb and flood tide in the inner parts of the BBE for both phyto and zooplankton compartments. This may suggest influence of tidal oscillation on community structure was higher in the inner estuarine areas, what should be further tested. In mixed systems, the short-term plankton distribution seems to be species-dependent and further studies on biotic and abiotic regulations must be considered, like light and tidal currents influences, beyond their own ability to swim to migrate.

ACKNOWLEDGMENTS

During the development of this study MNJ received a Doctoral scholarship from “Conselho Nacional de Desenvolvimento científico e Tecnólogico (CNPq, Grant no. 140945/2007-5); MSS received a Master scholarship from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES); LSN received a Doctoral scholarship from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES).

REFERENCES

• ALVARES CA, STAPE JL, SENTELHAS PC, DE MORAES G, LEONARDO J & SPAROVEK G. 2013. Köppen’s climate classification map for Brazil. Meteorol Z 22(6): 711-728.
• ANGER K, SPIVAK E, BAS C, ISMAEL D & LUPPI T. 1994. Hatching rhythms and dispersion of decapod crustacean larvae in a brackish coastal lagoon in Argentina. Helgol Meeresunters 48(4): 445.
• ARAUJO HMP, NASCIMENTO-VIEIRA DA, NEUMANN-LEITÃO S, SCHWAMBORN R, LUCAS APO & ALVES JPH. 2008. Zooplankton community dynamics in relation to the seasonal cycle and nutrient inputs in an urban tropical estuary in Brazil. Braz J Biol 68(4): 751-762.
• BECKER ÉC, GARCIA CAE & FREIRE AS. 2018. Mesozooplankton distribution, especially copepods, according to water masses dynamics in the upper layer of the Southwestern Atlantic shelf (26° S to 29° S). Cont Shelf Res 166: 10-21.
• BERNÁT N, KÖPCKE B, YASSERI S, THIEL R & WOLFSTEIN K. 1994. Tidal variation in bacteria, phytoplankton, zooplankton, mysids, fish and suspended particulate matter in the turbidity zone of the Elbe estuary; interrelationships and causes. Neth J Aquat Ecol 28(3-4): 467-476.
• BOERO F. 1994. Fluctuations and variations in coastal marine environments. Mar Ecol 15(1): 3-25.
• BOLTOVSKOY D. 1981. Atlas del Zooplancton del Atlántico Sudoccidental, Mar del Plata: Publicación Especial del Instituto Nacional de Investigación y Desarrollo Pesquero, 936 p.
• BOLTOVSKOY D. 1999. South Atlantic Zooplankton, Leiden: Backhuys Publishers (1): 1706.
• BRANDINI FP, ALQUINI F, PEREIRA RB & LEITE RL. 2006. Abundância e estrutura populacional da comunidade planctônica na Baía da Babitonga: Subsídios para a avaliação de impactos ambientais. In: Cremer MJ, Morales PR & Oliveira TMN (Eds), Diagnóstico Ambiental da Baía da Babitonga, Joinville, Editora da Univille, Joinville, 112-134 p.
• BRANDINI FP, NOGUEIRA M, SIMIÃO M, CODINA JCU & NOERNBERG MA. 2014. Deep chlorophyll maximum and plankton community response to oceanic bottom intrusions on the continental shelf in the South Brazilian Bight. Cont Shelf Res 89: 61-75.
• CHANDRAN R. 1985. Seasonal and tidal variations of phytoplankton in the gradient zone of Vellar estuary. Mahasagar 18(1): 37-48.
• CLARKE KR & GORLEY RN. 2006. PRIMER, 6th Ed, PRIMER-E Ltd.: Plymouth, UK.
• COSTA MD & SOUZA-CONCEIÇÃO JM. 2009. Composição e abundância de ovos e larvas de peixes na baía da Babitonga, Santa Catarina, Brasil. Pan-Am J Aquat Sci 4(3): 372-382.
• CREMER MJ, MORALES PRD & OLIVEIRA TMN. 2006. Diagnóstico ambiental da Baía da Babitonga, Joinville: Editora Univille, 256 p.
• DALAL SG & GOSWAMI SC. 2001. Temporal and ephemeral variations in copepod community in the estuaries of Mandovi and Zuari—west coast of India. J Plankton Res 23(1): 19-26.
• DAVID V, SAUTOUR B, CHARDY P & LECONTE M. 2005. Long-term changes of the zooplankton variability in a turbid environment: the Gironde estuary (France). Estuar Coast Shelf Sci 64(2-3): 171-184.
• DAY JR JW, YAÑEZ-ARANCIBIA A, KEMP WM & CRUMP BC. 2013. Introduction to estuarine ecology. In: Day Jr JW, Crump BC & Kemp WM (Eds), Estuarine Ecology, 2nd Ed, New Jersey, Wiley-Blackwell: Hoboken, New Jersey, p. 1-18.
• DEVASSY VP & GOES JI. 1988. Phytoplankton community structure and succession in a tropical estuarine complex (central west coast of India). Estuar Coast Shelf Sci 27(6): 671-685.
• DIAS CO, DE CARVALHO PF, BONECKER ACT & BONECKER SLC. 2018. Biomonitoring of the mesoplanktonic community in a polluted tropical bay as a basis for coastal management. Ocean Coast Manag 161: 189-200.
• DOMINGOS-NUNES R & RESGALLA JR C. 2017. The zooplankton of Santa Catarina continental shelf in southern Brazil with emphasis on Copepoda and Cladocera and their relationship with physical coastal processes. Lat Am J Aquat Res 40(4): 893-913.
• EDLER L. 1978. Recommendations for marine biological studies in the Baltic sea: phytoplankton and chlorophyll. Baltic Mar Biol Publ 5: 1-38.
• ELLIOTT M & MCLUSKY DS. 2002. The need for definitions in understanding estuaries. Estuar Coast Shelf Sci 55(6): 815-827.
• GARCIA-SOTO C, DE MADARIAGA I, VILLATE F & ORIVE E. 1990. Day-to-day variability in the plankton community of a coastal shallow embayment in response to changes in river runoff and water turbulence. Estuar Coast Shelf Sci 31(3): 217-229.
• GONÇALVES-ARAUJO R, DE SOUZA MS, TAVANO VM, MENDES CR, DE SOUZA RB, SCHULTZ C & POLLERY RC. 2018. Phyto- and protozooplankton assemblages and hydrographic variability during an early winter survey in the Southern Brazilian Continental Shelf. J Mar Syst 184: 36-49.
• GUENTHER M, LIMA I, MUGRABE G, TENENBAUM DR, GONZALEZ-RODRIGUEZ E & VALENTIN JL. 2012. Small time scale plankton structure variations at the entrance of a tropical eutrophic bay (Guanabara Bay, Brazil). Braz J Oceanogr 60(4): 405-414.
• GUENTHER M, ROYER SJ, DE OLIVEIRA CAMPOS D & LEITÃO SN. 2015. Spatial variation of the plankton community over a short-term survey at a tropical hypereutrophic estuary. Arq Ciênc Mar 48(1): 39-48.
• HARAGUCHI L, CARSTENSEN J, ABREU PC & ODEBRECHT C. 2015. Long-term changes of the phytoplankton community and biomass in the subtropical shallow Patos Lagoon Estuary, Brazil. Estuar Coast Shelf Sci 162: 76-87.
• HASLE GR. 1978. The inverted microscope. In: Sournia A (Ed), Phytoplankton Manual, Paris: Monographs on Oceanographic Methodology 6, UNESCO, p. 88-96.
• HASLE GR & FRYXELL GA. 1970. Diatoms: cleaning and mounting for light and electron microscope. Trans Am Microsc Soc 89: 469-474.
• HOLLAND AF, ZINGMARK RG & DEAN JM. 1974. Quantitative evidence concerning the stabilization of sediments by marine benthic diatoms. Mar Biol 27(3): 191-196.
• HUANG L, JIAN W, SONG X, HUANG X, LIU S, QIAN P, KEDONG Y & WU M. 2004. Species diversity and distribution for phytoplankton of the Pearl River estuary during rainy and dry seasons. Mar Pollut Bull 49(7-8): 588-596.
• IBAMA - INSTITUTO BRASILEIRO DO MEIO AMBIENTE E RECURSOS RENOVÁVEIS. 1998. Proteção e Controle de Ecossistemas Brasileiros: Manguezal da Baía da Babitonga. Coleção Meio Ambiente, Brasília.
• JONGMAN RHG, TER BRAAK CJF & VAN TONGEREN OFR. 1995. Data analysis in community and landscape ecology. Cambridge University Press, Cambridge.
• KNIE J. 2002. Atlas Ambiental da Região de Joinville: Complexo hídrico da baía da Babitonga. Joinville: Fundação do Meio Ambiente de Santa Catarina, 144 p.
• LANDUCCI M & LUDWIG TAV. 2005. Diatomáceas de rios da bacia hidrográfica Litorânea, PR, Brasil: Coscinodiscophyceae e Fragilariophyceae. Acta Bot Bras 19(2): 345-357.
• LAPRISE R & DODSON JJ. 1993. Nature of environmental variability experienced by benthic and pelagic animals in the St. Lawrence Estuary, Canada. Mar Ecol Prog Ser 94: 129-139.
• LEPŠ J & ŠMILAUER P. 2003. Multivariate analysis of ecological data using CANOCO. Cambridge University Press, Cambridge.
• LI KZ, YIN JQ, HUANG LM & TAN YH. 2006. Spatial and temporal variations of mesozooplankton in the Pearl River estuary, China. Estuar Coast Shelf Sci 67(4): 543-552.
• LOPES RM, DO VALE R & BRANDINI FP. 1998. Composição, abundância e distribuição espacial do zooplâncton no complexo estuarino de Paranaguá durante o inverno de 1993 e o verão de 1994. Rev Bras Oceanogr 46(2): 195-211.
• MADHU NV, JYOTHIBABU R, BALACHANDRAN KK, HONEY UK, MARTIN GD, VIJAY JG, SHUYAS CA, GUPTA VM & ACHUTHANKUTTY CT. 2007. Monsoonal impact on planktonic standing stock and abundance in a tropical estuary (Cochin backwaters–India). Estuar Coast Shelf Sci 73(1-2): 54-64.
• MANI P & KRISHNAMURTHY K. 1989. Variation of phytoplankton in a tropical estuary (Vellar estuary, Bay of Bengal, India). Int Rev ges Hydrobiol Hydrogr 74(1): 109-115.
• MARQUES SC, AZEITEIRO UM, MARTINHO F, VIEGAS I & PARDAL MÂ. 2009. Evaluation of estuarine mesozooplankton dynamics at a fine temporal scale: the role of seasonal, lunar and diel cycles. J Plankton Res 31(10): 1249-1263.
• MCQUOIDA NR & NORDBERG K. 2003. The diatom Paralia sulcata as an environmental indicator species in coastal sediments. Estuar Coast Shelf Sci 56: 339-354.
• MECALCO-HERNÁNDEZ Á, CASTILLO-RIVERA MA, SANVICENTE-AÑORVE L, FLORES-COTO C & ÁLVAREZ-SILVA C. 2018. Variación estacional y nictímera en la distribución del zooplancton dominante en una laguna costera tropical. Rev Biol Mar Oceanogr 53(1): 39-49.
• MEESTER LD & VYVERMAN W. 1997. Diurnal residence of the larger stages of the calanoid copepod Acartia tonsa in the anoxic monimolimnion of a tropical meromictic lake in New Guinea. J Plankton Res 19(4): 425-434.
• MENÉNDEZ MC, DELGADO AL, BERASATEGUI AA, PICCOLO MC & HOFFMEYER MS. 2015. Seasonal and tidal dynamics of water temperature, salinity, chlorophyll-a, suspended particulate matter, particulate organic matter, and zooplankton abundance in a shallow, mixed estuary (Bahía Blanca, Argentina). J Coast Res 32(5): 1051-1061.
• MENÉNDEZ MC, PICCOLO MC & HOFFMEYER MS. 2012. Short-term variability on mesozooplankton community in a shallow mixed estuary (Bahía Blanca, Argentina): Influence of tidal cycles and local winds. Estuar Coast Shelf Sci 112: 11-22.
• MIYASHITA LK, BRANDINI FP, MARTINELLI-FILHO JE, FERNANDES LF & LOPES RM. 2012. Comparison of zooplankton community structure between impacted and non-impacted areas of Paranaguá Bay Estuarine Complex, South Brazil. J Nat Hist 46(25-26): 1557-1571.
• MMA. 2007. Áreas Prioritárias para a Conservação, Uso Sustentável e Repartição de Benefícios da Biodiversidade Brasileira: Atualização Portaria n°09, de 23 de janeiro de 2007. MMA, Brasília, Brasil.
• MONTÚ M & CORDEIRO AT. 1988. Zooplâncton del complejo estuarial de la Bahía de Paranaguá. I. Composición, dinámica de las especies, ritmos reproductivos y acción de los factores ambientales sobre la comunidad. Nerítica 3(1): 61-83.
• NOERNBERG MA, RODRIGO PA & LUERSEN DM. 2020. Seasonal and fortnightly variability of the hydrodynamic regime at Babitonga Bay, Southern of Brazil. Reg Stud Mar Sci 40: 101518.
• NOGUEIRA JÚNIOR MN & COSTA MDP. 2019. Zooplâncton da Baía da Babitonga e plataforma continental adjacente: diagnóstico e revisão bibliográfica. Revista CEPSUL-Biodiversidade e Conservação Marinha 8: eb2019001.
• NOGUEIRA JÚNIOR MN & DE OLIVEIRA VM. 2017. Strategies of plankton occupation by polychaete assemblages in a subtropical estuary (south Brazil). J Mar Biol Assoc U K 97(8): 1651-1661.
• OMORI M & IKEDA T. 1994. Methods in marine zooplankton ecology. New York: Wiley, 332 p.
• PARSONS TR, HARRISON PJ, ACREMAN JC, DOVEY HM, THOMPSON PA, LALLI CM, LEE K, GUANGO C & XIAOLIN C. 1984. An experimental marine ecosystem response to crude oil and Corexit 9527: Part II - Biological Effects. Mar Envir Res 13(4): 265-275.
• PROCOPIAK LK, FERNANDES LF & MOREIRA-FILHO H. 2006. Diatomáceas (Bacillariophyta) marinhas e estuarinas do Paraná, Sul do Brasil: lista de espécies com ênfase em espécies nocivas. Biota Neotrop 6(3): bn02306032006.
• ROCHA CEF. 1986. Copepods of the genus Oithona Baird, 1843 from mangrove areas of Central and South America. Hydrobiologia 135(1-2): 95-107.
• ROUND FE, CRAWFORD RM & MANN DG. 2000. The Diatoms: Biology and Morphology of the Genera. Cambridge: Cambridge University Press, p. 1-751.
• SALVADOR B & BERSANO JGF. 2017. Zooplankton variability in the subtropical estuarine system of Paranaguá Bay, Brazil, in 2012 and 2013. Estuar Coast Shelf Sci 199: 1-13.
• SAR E, SUNESEN I & FERNÁNDEZ PV. 2007. Marine diatoms from Buenos Aires coastal waters (Argentina) II Thalassionemataceae and Raphoneidaceae. Rev Chil Hist Nat 80: 63-79.
• SASSI R. 1991. Phytoplankton and environmental factors in the Paraíba do Norte River Estuary, northeastern Brazil: composition, distribution and quantitative remarks. Bol Inst Oceanogr 39(2): 93-115.
• SEMINA HJ. 1978. The size of cells. Phytoplankton manual. UNESCO Monogr Oceanogr Methodol 6: 233-237.
• SHAFFER GP & SULLIVAN MJ. 1988. Water column productivity attributable to displaced benthic diatoms in well-mixed shallow estuaries. J Phycol 24(2): 132-140.
• SIN Y & JEONG B. 2019. Anthropogenic Disturbance of Tidal Variation in the Water Properties and Phytoplankton Community of an Estuarine System. Estuar Coast: 1-13.
• TEIXEIRA-AMARAL P, AMARAL WJA, DE ORTIZ DO, AGOSTINI VO & MUXAGATA E. 2017. The mesozooplankton of the Patos Lagoon Estuary, Brazil: trends in community structure and secondary production. Mar Biol Res 13(1): 48-61.
• TELESH IV. 2004. Plankton of the Baltic estuarine ecosystems with emphasis on Neva Estuary: A review of present knowledge and research perspectives. Mar Pollut Bull 49: 206-219.
• TELESH IV & KHLEBOVICH VV. 2010. Principal processes within the estuarine salinity gradient: a review. Mar Pollut Bull 61(4-6): 149-155.
• TENENBAUM DR, VILLAC MC, VIANA SC, MATOS MC, HATHERLY MMF, LIMA IV & MENEZES M. 2004. Phytoplankton Atlas of Sepetiba Bay, Rio de Janeiro. GloBallast Monography Series, n. 16. London: IMO, 132 p.
• TER BRAAK CJF & ŠMILAUER P. 1998. CANOCO Reference Manual and User’s Guide to Canoco for Windows: Software for Canonical Community Ordination (version 4). Microcomputer Power: Ithaca, New York, 352 p.
• TOMAS CR. 1997. Identifying Marine Phytoplankton, 2nd ed., San Diego: Academic Press, 858 p.
• TRUCCOLO EC & SCHETTINI CAF. 1999. Marés astronômicas na baía da Babitonga, SC. Braz J Aquat Sci Tech 3: 57-66.
• UTERMÖHL H. 1958. Zur Vervolkomnung der quantitativen Phytoplankton: methodik. Mitt Internat Verein Theor Angew Limnol 9: 1-38
• VIEIRA CV & HORN FILHO NO. 2017. Paisagem marinha da baía da Babitonga, nordeste do estado de Santa Catarina (Marine landscape of the Babitonga bay, northeast of Santa Catarina state). Rev Bras Geogr Fís 10(5): 1677-1689.
• WAN MAZNAH WO, RAHMAH S, LIM CC, LEE WP, FATEMA K & ISA MM. 2016. Effects of tidal events on the composition and distribution of phytoplankton in Merbok river estuary Kedah, Malaysia. Trop Ecol 57(2): 213-229.

SUPPLEMENTARY MATERIAL

Figure S1. Study area and sampling stations in the Babitonga Bay estuary.

Table SI. Phytoplankton taxa found in the Babitonga Bay estuary. RA: relative abundance. FO: frequency of occurrence. Species list according to the most abundant groups.

Table SII. Summary of the Redundancy Analysis (RDA) performed between the 21 most abundant phytoplankton taxa and six environmental explanatory variables from Babitonga Bay, Brazil.

Table SIII. Zooplankton taxa found in Babitonga Bay estuary. RA: relative abundance. FO: frequency of occurrence.

Table SIV. Summary of the Redundancy Analysis (RDA) performed between the 17 most abundant zooplankton taxa and six environmental explanatory variables from Babitonga Bay, Brazil.

Publication Dates

• Publication in this collection
  12 Nov 2021
• Date of issue
  2021

History

• Received
  13 Feb 2020
• Accepted
  22 Feb 2021