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Article

Impact of the Construction of New Port Facilities on the Biomass and Species Composition of Phytoplankton in the Neva Estuary (Baltic Sea)

by
Mikhail S. Golubkov
*,
Vera N. Nikulina
and
Sergey M. Golubkov
Zoological Institute of Russian Academy of Sciences, Universitetskaya Emb. 1, 199034 Saint-Petersburg, Russia
*
Author to whom correspondence should be addressed.
J. Mar. Sci. Eng. 2023, 11(1), 32; https://doi.org/10.3390/jmse11010032
Submission received: 29 November 2022 / Revised: 12 December 2022 / Accepted: 21 December 2022 / Published: 27 December 2022
(This article belongs to the Section Marine Biology)
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Abstract

:
The construction of new port facilities and the creation of new lands is a natural consequence of the rapid growth in the population of ocean coastlines. Despite the fact that such human activity is becoming more and more widespread, its impact on various components of aquatic ecosystems, including phytoplankton, is still poorly understood. The aim of the study was to assess the effect of the large-scale construction of new port facilities on biomass and taxonomic composition of phytoplankton in the Neva Estuary (northeastern Baltic Sea). Studies have shown that digging and displacing large amounts of bottom sediments during these works led to a significant increase in suspended mineral matter and a decrease in water transparency in the estuary. This significantly reduced the species richness and biomass of phytoplankton. However, the analysis of beta diversity did not show significant changes in the phytoplankton community during the periods of port construction and the periods when no works were carried out. The changes mainly concerned rare species, while the occurrence and biomass of dominant and subdominant species changed to a lesser extent. Due to various adaptations, the phytoplankton species common in the estuary are apparently able to survive under prolonged shading and successfully compete with species that are unable to withstand the lack of light for a long time. To correctly take into account the effects of the construction of new port facilities on phytoplankton and, if possible, minimize it, additional studies of the ecology of certain phytoplankton species, their relationships, and physiological responses to various environmental factors are required.

1. Introduction

The rapid increase in the economic use of sea coasts inevitably affects the ecosystems of coastal waters [1,2]. Despite the widespread occurrence of the construction of new port facilities in coastal areas, their impact on various components of near-shore ecosystems, including phytoplankton, is still poorly understood [3]. This environmental problem has now become especially relevant for the eastern part of the Gulf of Finland. In recent decades, new lands, ports, and fairways have been created at the mouth of the Neva River, which have become the infrastructure of St. Petersburg, located on the northeastern coast of the Baltic Sea [4]. These led to the appearance of a large amount of suspended matter in the waters of the Neva Estuary which affected its ecosystem [3,5].
Previously, the short-term effects of suspended matter on phytoplankton have been studied in detail in shallow waters, where significant amounts of suspended matter can enter the water column as a result of intense resuspension of bottom sediments during storms [6,7,8,9] or tides [10,11]. In addition, coastal ecosystems will more frequently become turbid due to terrestrial sediment runoff caused by future increases in precipitation, as predicted by climate models [12].
A significant increase in the concentration of suspended matter reduces the depth of light penetration into the water and worsens the conditions for the development of phytoplankton [3,6,7,13]. On the other hand, the nutrients accumulated in the sediments flow back into the water column [7,8,14] and this may stimulate phytoplankton growth due to reduced nutrient limitation [6,7]. Sediment resuspension can also affect phytoplankton biomass because algae cells or cysts from the surface layer of bottom sediments enter the water column [6,14,15,16].
The combined effect of light and nutrients may be also significant [6,13,15,17]. At times of extreme turbidity, phytoplankton is likely to be light-limited, but its light limitation depends on nutrient concentrations [6]. There may also be some delay between the inhibition and stimulation effects of phytoplankton biomass. For instance, typhoon-induced sediment resuspension led to light limitations for algal growth in shallow Lake Taihu (eastern China), whereas after the typhoon had passed, water column conditions (light penetration and nutrient availability) favored the growth and production of algae [18]. Thus, the response of phytoplankton to the resuspension of bottom sediments is rather complicated. In addition, one must take into account that resuspension events resulting from strong winds or tides usually last for several hours or days [10,19,20]. On the contrary, the resuspension of bottom sediments can last for months or even years in the case of the creation of new lands or port infrastructure. For example, the construction of new port facilities at the mouth of the Neva River took several years [4]. Digging and dredging of bottom sediments in its estuary results in the increase in suspended particulate matter by one order of magnitude, which mostly consisted of sand and clayed deposits. This, in turn, led to a significant decrease in water transparency and an increase in the concentration of phosphorus in the water column compared to the long-term average values [3]. However, the increase in nutrients was less important for phytoplankton growth than expected. The analysis of variance and stepwise multiple regression analyses showed that the main predictor of the primary production of plankton in the periods of construction was water transparency. As a result, gross primary production decreased significantly during periods of port infrastructure construction [3].
It should also be taken into account that the response of phytoplankton to the resuspension of bottom sediments may depend on the species composition of algae [8,21]. For example, a mesocosm experiment conducted in the northern part of the Baltic Sea showed that the various groups of phytoplankton react differently to nutrient enrichment and the presence of bottom sediments [21]. Increased water turbidity can affect the morphological and physiological characteristics of phytoplankton algae, and different groups of algae are able to adapt to changing environmental conditions to varying degrees [22,23,24,25]. Charalampous et al. [26] showed that with a decrease in illumination, the average ratio of the surface area of algal cells to their volume in the phytoplankton community increased by more than three times. Moreover, such changes also occurred even within the population of certain species. The average cell volume in a population of some species decreased with a lack of light since a smaller size results in greater light acquisition [27]. The appearance of such changes in the phytoplankton community depended on the duration of the resuspension events [28]. This makes predicting the impact of hydrotechnical works on the phytoplankton community even more difficult.
This study aimed to assess the effect of large-scale construction of new port facilities on the biomass and taxonomic composition of phytoplankton in the Neva Estuary, the largest estuary in the Baltic Sea. We tested the hypothesis that a prolonged increase in the concentration of suspended matter in the estuary could lead to significant changes in the diversity and biomass of the phytoplankton community.

2. Materials and Methods

2.1. Study Sites

The Neva Estuary (Figure 1) is located in the eastern part of the Gulf of Finland in the Baltic Sea. The Neva River is the largest flow of water among the rivers flowing into the Baltic Sea. Its average water discharge rate is 2490 m3 s−1 (78.6 km3 yr−1) and the catchment area is about 280,000 km2 [29]. The Neva Estuary is located on the border between the northern temperate and subpolar climatic zones [30]. The climate type in the region is Dfc—snowy, fully humid, with cool summers [31].
The Neva Estuary is non-tidal with a gradual increase in salinity from fresh water in its upper reaches (UR) to slightly saline in the middle reaches (MR) [29]. The five-million populated city of St. Petersburg, located on the coast of the estuary, has an intense anthropogenic impact on the ecosystem of the estuary [33,34]. Since the late 1980s, the UR of the estuary has been separated from the MR by the Flood Protective Facility, which includes 11 dams (Figure 1). There is no temperature stratification in the estuary UR, and low water transparency hinders the development of benthic aquatic vegetation.
The estuary MR is located to the west of Kotlin Island up to the conditional boundary of 29°10′ E. Temperature stratification in summer was observed at all sampling stations in this part of the estuary. The temperature and salinity of the water in summer varied within rather narrow limits (Table 1). A more detailed description of environmental conditions in the UR and MR of the estuary is given in previous articles [29,35].
The new passenger port of St. Petersburg was built at the mouth of the Neva River in 2006–2007, A total of 476.7 hectares of new land were created in the upper reaches of the Neva Estuary for its construction (Figure 1). At the same time, the shipping channel was deepened to 14 m for the passage of large ferries. The construction of the new multifunctional maritime Port Bronka was carried out in 2014–2015 in the southwestern part of the upper reach (Figure 1). During the construction of new port facilities, large amounts of bottom sediment were dredged, removed, and transferred from one part of the estuary to another [3,4]. This led to the appearance of large amounts of suspended matter in the water.

2.2. Sampling

Water and phytoplankton samples were collected at 17 stations in the upper and middle reaches of the Neva Estuary (Figure 1) in 2003–2020 from late July to early August. Water transparency was measured with a Secchi disk. Using a CTD90m probe (Sea & Sun Tech., Trappenkamp, Germany), the water temperature (T) and salinity (S) were measured every 20 cm from the surface to the bottom. We collected five water samples (2 L each) from the surface, half a meter from the bottom, and at three equal depths between them in the non-stratified UR of the estuary. A pooled sample (10 L) was compiled by mixing samples taken at different depths. This was done in order to avoid errors caused by possible uneven distribution in biomass and composition of phytoplankton with depth. From these pooled samples, samples of suspended particulate matter (SM) and particulate organic matter (SOM) were taken in three replicates.
In the stratified middle reaches, water samples were collected from the layer above the thermocline. Water samples (2 L each) were collected from the surface, from the thermocline, and at three equal depths between them. The pooled sample (10 L) was made up of water samples taken from different depths. Samples SM and SOM (three replicates) were taken from pooled samples.

2.3. Sample Analysis

The SM concentration was determined gravimetrically [36] by filtering water through preweighed and precombusted Whatman GF/F filters. To determine SOM, water was filtered through Whatman GF/F filters and oxidized with dichromic acid [36]. The concentration of suspended mineral matter (SMM) in water was calculated from the difference between the concentrations of SM and SOM.

2.4. Phytoplankton Community

Phytoplankton samples (volume 0.3 L) were taken in one replicate from the LAT pooled samples in the MR of the estuary and from the whole column pooled samples in the shallow UR of the estuary, and fixed with an acidic Lugol solution. Phytoplankton species were identified and counted in sedimentation chambers (10–25 mL) using an inverted Hydro-Bios microscope with 600-fold magnification. Phytoplankton biomass expressed in wet weight (WW mg M−3) was calculated according to Olenina et al. [37] as the total volume of algae cells. Phytoplankton species were identified according to Kiselev [38], Pankov [39], and Tikkanen [40]. They have been listed in the updated nomenclature according to Guiry and Guiry [41]. To calculate the average biomass of the species, we used data from all stations. If the species was absent at the station, its biomass value was equal to zero. The average biomass for all stations was calculated considering these zeros.

2.5. Statistical Analyses

The Secchi depth and concentration of SMM were averaged for each station for periods 2006–2007, 2014–2015, and 2003–2020 excluding the previous periods, and visualized using SURFER 8.0.
Statistical analysis was performed using R software (version 4.2.2) [42]. An analysis of the beta diversity between the species composition of phytoplankton at stations in the Neva Estuary during the periods of port construction and during periods when construction was not carried out was performed using the “betadiver” function in the R package “vegan” [43]. The “adonis” function in the R package “vegan” [43] implements the analysis of variance using distance matrices—for partitioning distance matrices among sources of variation and fitting linear models (e.g., factors, and polynomial regression) to distance matrices using a permutation test with pseudo-F ratios. The “adonis” function can handle both continuous and factor predictors. As an environmental factor, we chose the implementation or absence of port construction works. We defined beta diversity as the slope of the species-area curve or the exponent BD of the Arrhenius model, where the number of species S depends on the size X of the study area. In our case, X of the study area was expressed as the number of stations at which species were encountered. For pairwise comparison of the periods of work (DC) and their absence (NC), the slope angle BD was found by the “adonis” function in the R package “vegan” [43], taking into account the number of species common for each station during two periods (a) and the number of species unique for each station of each period.
Using the method of principal coordinate analysis (PCoA), the “betadisper” function of the “vegan” R package [43], we examined the differences in beta diversity in the “DC” and “NC” periods and evaluated the differences in group homogeneity. In addition, we performed a Tukey test, function “TukeyHSD” of the R package “vegan” [43], to analyze the significance of the difference between the DC–NC pair.
An increased concentration of suspended matter and low water transparency in shallow waters often occurs due to natural causes (as a result of wind resuspension, river runoff, etc.). Therefore, it is not always possible to distinguish the effect of an increased concentration of suspended matter caused by anthropogenic or natural factors. Considering these difficulties, we analyzed the impact of fluctuations in Sec and SMM across all data, without dividing them into periods of port construction in the Neva Estuary and periods when such construction was not carried out. Before the analysis of the pairwise Pearson’s correlation, the original data were converted into a natural logarithm. The pairwise Pearson correlation coefficients between concentrations of Sec, SMM, and phytoplankton biomass and species number were produced using the ‘chart.Correlation’ function in the PerformanceAnalytics package in R ver. 1.5.2. [44].
Non-metric multidimensional scaling (NMDS) was used to analyze changes within the phytoplankton species biomass by ordinating samples based on the dissimilarities of Secchi depth and concentration of suspended particulate mineral matter (function “metaMDS”, R package “vegan” [43]). NMDS is an ordination technique that uses rank orders to collapse information from multiple dimensions so that they can be visualized and interpreted. Before analysis, the original data were square root transformed and then submitted to Wisconsin double standardization. In this standardization, each element is divided by its column maximum and then divided by the row total. We used the Bray–Curtis dissimilarity as the distance metric in the NMDS. In the NMDS ordination space, the samples position themselves based on their taxon-specific biomass. To overlay environmental information onto ordination diagrams we used the “envfit” function (R package “vegan”, [43]). The arrow points to the direction of the most rapid change in the environmental variable. This is called the direction of the gradient. The length of the arrow is proportional to the correlation between ordination and environmental variable. This is called the strength of the gradient. We added the fitted vectors to an ordination using the “plot” command with the argument “p.max = 0.05”.

3. Results

3.1. Abiotic Environmental Factors

The transparency of the water in the estuary significantly decreased during the construction of new port facilities (Figure 2). In 2006–2007, the Sec value was significantly lower than 1 m at most of the sampling stations (Figure 2a). In 2014–2015, low water transparency was observed mainly in the southwestern part of the estuary (Figure 2b), where the new Port Bronka was constructed in those years (Figure 1). For comparison, in the years when no work was carried out, the low Sec values of 1.2 m were measured only in small areas in the UR of the estuary (Figure 2c).
During the period of the port construction in 2006–2007, in most of the estuary, the concentration of mineral-suspended matter exceeded 20 g m−3 (Figure 2d), and at some stations, it reached 180 g m−3. In 2014–2015, the concentration of suspended mineral matter exceeded 20 g m−3 in the southwestern part of the estuary (Figure 2e) as a result of the construction of Port Bronka.

3.2. Algae Biomass and Species Richness of Phytoplankton

The full list of species composition in the Neva Estuary during the study period is given in Table S1. The biomass and the average number of phytoplankton species at sampling stations decreased during periods of intensive construction of the new port facilities compared to periods when such work was not carried out (Figure 3). However, changes in these indicators differed in various groups of phytoplankton. The average biomass of Cyanophyceae decreased the most. The biomass of Chlorophyceae, Bacillariophyceae and Chrysophyceae also decreased, although to a lesser extent compared to Cyanophyceae (Figure 3a). The average biomass of Cryptophycea, Xanthophyceae, and Euglenophyceae species, taking into account the standard deviation, did not change. Only Dinophyceae algae showed an increase in biomass during the construction of the port facilities (Figure 3a).
The largest decrease in the average number of species at the sampling station was observed among the Bacillariophyceae and Chlorophyceae algae. During periods when the construction of the port facilities was not carried out, the number of species at one station averaged five species of Bacillariophyceae and nine species of Chlorophyceae algae. Their number decreased to three and five species, respectively, during port construction periods (Figure 3b). At many stations, Cryptophyceae, Euglenophyceae, and Xanthophyceae algae were not found. Because of this, the average number of species of these algae per station in different periods was close to zero (Figure 3).
The decrease in the total species richness in each taxonomic group of phytoplankton during periods of intensive construction of the new port facilities was more significant than the average for one station. During these periods, the number of species of Bacillariophyceae, Chlorophyceae, and Cyanophyceae found in the studied part of the estuary were two times less than in the years when port construction was not carried out (Table 2). However, the species dominating the biomass of many phytoplankton groups remained the same. Only two of the dominant species, Pantocsekiella kuetzingiana (Thwaites) K.T.Kiss and E.Ács 2016 from Bacillariophyceae and the Chlorophyceae alga Mougeotia sp., ceased to dominate the phytoplankton during periods of port construction. Instead, Sceletonema sp. from Bacillariophyceae and Chlamidomonas sp. from Chlorophyceae became the dominant species of phytoplankton in these periods. Among the Cyanophyceae, Aphanizomenon flos-aquae Ralfs ex Bornet and Flahault 1886 ceased to dominate and Limnothrix planctonica (Woloszynska) Meffert 1988 became the dominant species during the years of port construction (Table 2).
The analysis of beta diversity of the phytoplankton community during the construction of port infrastructure in the Neva Estuary and in the years when such construction was not carried out showed that the phytoplankton community did not differ significantly in these periods (Figure 4a), because the median BD values in our case were 0.46 and 0.48 (Figure 4b). In addition, the Tukey test (TukeyHSD) showed the difference between the DC–NC pair as 0.02, i.e., there was no significant difference between these periods (p adj. = 0.304). At the same time, the multivariate homogeneity of the beta dispersion was less during periods of port construction than when such work was not carried out (Figure 4b). This suggests that there were fewer rare species in the community at the time of port construction, although the area occupied by the common species did not change (Figure 4b).

3.3. Relationships between Environmental Factors and Phytoplankton Community Structure

The Pearson’s analysis of pairwise correlations showed that a greater number of phytoplankton species during the study period were reliably observed at stations where water transparency was higher (Figure 5). At stations where the concentration of mineral suspension was higher, lower phytoplankton biomasses and fewer species were reliably observed. Accordingly, it can be assumed that an increase in the concentration of SMM because of the construction of the port infrastructure led to a decrease in the phytoplankton biomass and its species richness. At the same time, data analysis by the method of NMDS showed that changes in the biomass of various groups and species of phytoplankton differed in relation to Sec and SMM (Figure 6).
The biomass of some Bacillariophyceae species responded positively to an increase in the concentration of mineral-suspended matter and negatively to a decrease in Sec. For example, the biomass of Asterionella formosa Hassall 1850 and Aulacoseira islandica (O.Müller) Simonsen 1979, which dominated diatoms during construction activities, was positively correlated with the concentration of suspended matter (Figure 6a). However, the biomass of a large group of species did not respond in any way to changes in Sec and SMM. For example, the biomass of P. kuetzingiana, which dominated Bacillariophyceae biomass during non-concentration periods and was not among the dominant species during port construction periods, did not show an association with changes in Sec and SMM (Figure 6a).
Chlorophyceae species, including Mougeotia sp., which dominated the phytoplankton biomasses during periods when no port construction was carried out (Table 2), generally showed higher biomass under conditions of higher Sec and lower SMM (Figure 6b). The remaining two dominant Chlorophyceae species, like many other species from this group, did not show relationships with Sec and SMM (Figure 6b, Table 2). Among Chlorophyceae, only the biomass of Micractinium pussilum Fresenius 1858 showed a positive relationship with SMM and a negative one with Sec (Figure 6b).
Cyanophyceae were more affected by the increase in Sec and SMM. Many species lined up along the axis of change in Sec and SMM, their high biomass was observed at a high Sec and low SMM (Figure 6c). For example, Planktothrix agardhii (Gomont) Anagnostidis and Komárek 1988, which dominated in average biomass among Cyanophyceae both during the port construction periods and when the construction was not carried out, showed a positive relationship between biomass and an increase in Sec and a decrease in SMM (Figure 6c, Table 2). However, the average biomass of this species during the periods of port construction was half as much, and the maximum biomass was four times less in comparison with the periods when such works were not carried out (Table 2).
The biomasses of algae groups with a small number of species in the Neva Estuary, Chrysophyceae, Cryptophyceae, Dinophyceae, Euglenophyceae, and Xanthophyceae, mostly either did not respond to changes in Sec and SMM or showed large biomasses at lower values of Sec and high SMM. For example, most of the Chrysophyceae species that dominated during port construction periods (Table 2) also showed high biomass with an increasing SMM and decreasing Sec (Figure 6d). In contrast, the biomass of dominant Cryptophyceae species did not respond to Sec and SMM changes (Figure 6d). Their average and maximum biomasses during the periods of port construction work and during the periods of their absence practically did not differ (Table 2).
According to NMDS analysis, the Dinophyceae species did not respond to changes in Sec and SMM (Figure 6d), but their average biomass increased during the periods of port construction (Figure 3a, Table 2). It can be assumed that water transparency was not very important for this group and under conditions of a decrease in the biomass of other phytoplankton groups, these algae gained some advantage.
The species of Euglenophyceae also did not significantly respond to changes in water transparency (Figure 6d). Taking into account standard deviations, the biomass of Euglenophyceae did not decrease during the periods of port construction works (Figure 3a), i.e., this decrease could be due to interannual fluctuations in their biomass rather than construction activities.
The biomass of a single species from the Xanthophyceae group Tribonema affine (Kützing) G.S.West 1904 also did not show a relationship to changes in Sec and SMM (Figure 6d), although the values of average and maximum biomass of this species during the periods of port construction were lower than during periods when no construction works were carried out (Table 2).

4. Discussion

Understanding how the community composition is created and maintained is critical to natural resource management and biological conservation. The Neva Estuary has been under strong anthropogenic impact for many years [34,45]. The construction of the St. Petersburg flood protection facility in the estuary occurred in the 1980s, which periodically led to multiple increases in the concentration of suspended particulate matter and turbidity in different parts of the estuary [3,4,46]. Engineering work has also resulted in increased turbidity in other regions of the Baltic Sea. For instance, the SM concentration reached 126 g m−3, and the Secchi disk depth decreased to 0.2 m along the Estonian coast during the dredging period [47].
Light conditions are an important driver of phytoplankton growth in turbid estuaries [48]. In the Neva Estuary, an increase in SMM concentration during the periods of port construction in the 2000s had a negative impact on water transparency, which significantly decreased during these periods (Figure 2). This was accompanied by a decrease in the phytoplankton biomass (Figure 3 and Figure 5; Table 2), apparently associated with the deterioration of light conditions. Similar results were previously obtained in some other estuaries. For instance, an experimental study showed that light limitation of phytoplankton growth occurred in the turbid shallow upper reaches of the Guadiana estuary and that various groups of algae responded differently to the lack of light [48]. However, studies in the German Bight in the North Sea have shown a dual response of phytoplankton to the resuspension of bottom sediments [7]. In spring, during the resuspension resulting from the tide, there was an increase in the growth of phytoplankton because of additional nutrients released from the pore water of bottom sediments. However, with wind resuspension in autumn during the storm season, phytoplankton was suppressed, since, despite the high concentration of nutrients, the amount of light penetrating the water column greatly decreased [7]. In the Neva Estuary, an increase in turbidity because of port construction works led to a decrease in water transparency, as a result, despite the increase in nutrient concentrations, the primary production of phytoplankton greatly decreased [3].
Light is one of the major factors affecting phytoplankton composition [27,48,49]. A long-term decrease in water transparency during the periods of port construction in the Neva Estuary caused a significant decrease in the species richness of phytoplankton (Figure 3 and Figure 5; Table 2). However, an analysis of the beta diversity of phytoplankton in the years of infrastructure construction and in the years when such construction was not carried out showed that phytoplankton communities did not differ significantly during these periods (Figure 4a). The species dominating the biomasses of many phytoplankton groups remained practically unchanged, but the numbers and biomass of relatively rare species decreased significantly during the periods of port construction, and, as a result, the community became more homogeneous (Figure 4b). This process is known as biotic homogenization. It implies a decrease in beta diversity due to the elimination of sensitive taxa from the regional pool of species under the influence of disturbance [50,51,52]. Among the various groups of phytoplankton in the Neva Estuary, the biomass and species richness of Bacillariophyceae and Chlorophyceae, as well as Cyanophyceae decreased most significantly (Figure 3). These taxonomic groups had the highest species richness in summer phytoplankton during both the periods of port construction in the estuary and when construction was not carried out (Table 2). These groups also contain the largest number of rare species that enter the estuary with river runoff from its catchment area [24,25]. Such rare species were apparently less adapted to the conditions in the estuary and disappeared under conditions of lack of light, increasing the homogeneity of the phytoplankton community.
The species-sorting model of beta diversity emphasizes organisms’ abilities to select and occupy areas with suitable environmental conditions. Various groups and species of phytoplankton tolerate changes in solar irradiation to varying degrees [23,27]. Therefore, the dominance of some phytoplankton species during the periods of port construction in the Neva Estuary may be related to their resistance to low illumination. For example, Bacillariophyceae A. islandica, which showed resistance to light deficiency and a high concentration of suspended matter (Figure 6a), was one of the dominant species in average biomass among Bacillariophyceae during the construction of the port facilities in the Neva Estuary (Table 2). This species is common in well-mixed mesotrophic lakes where the resuspension of bottom sediments often occurs [53]. However, the average and maximum values of its biomass during the periods of construction work in the Neva Estuary were lower than during the periods when such work was not carried out (Table 2). A similar significant decrease in the biomass of Aulocoseira spp. was observed in the subtropical Lake Okeechobee (Florida, USA) during a long-term light deficit due to high water turbidity during strong hurricanes [54]. Another Bacillariophyceae species, Skeletonema sp., which increased its share in phytoplankton biomass during the port construction works in the Neva Estuary (Table 2), also has a low demand for light [55]. However, the NMDS analysis showed that the biomass of Skeletonema subsalsum (Cleve-Euler) Bethge 1928 and Skeletonema sp. was not related to the change in Sec and SMM in the estuary (Figure 6a). Previously, it was shown that the biomasses of A. islandica, Skeletonema sp., and S. subsalsum in the Neva Estuary were most significantly positively correlated with water salinity [25]. Apparently, the effect of this factor under estuary conditions was more significant for these species than light conditions because they are already preadapted to low water transparency. The adaptations of diatoms to the lack of light include, for example, the ability to increase the surface-to-volume ratio and the number of chloroplasts in cells [26]. Mesocosm experiments showed that species with long spines and chloroplasts in them, such as A. formosa, which increased its biomass at high SMM and low Sec in the Neva Estuary (Figure 6a), began to dominate among diatoms with a lack of light [26].
Under normal conditions, the biomasses of most species of Chlorophyceae in the Neva Estuary were positively correlated with the concentration of total phosphorus [25]. However total biomass and species richness of these algae decreased during the periods of port construction (Figure 3a,b), despite the high concentrations of total phosphorus that were observed during these periods due to the resuspension of bottom sediments [3]. However, not all species of this group of phytoplankton reacted negatively to increased water turbidity. For example, the biomass of Micractinium pussilum Fresenius 1858 responded positively to high concentrations of SMM and low Sec (Figure 6b). As shown in laboratory experiments, this species is capable of mixotrophic feeding both in the dark and in the light [56].
The biomass of another Chlorophyceae Chlamidomonas sp. positively responded to the increase in water transparency (Figure 6b). However, it remained among the dominant species during the periods of port construction (Table 2). The species of this genus are able to regulate the concentration of carotenoids in cells [23]. These auxiliary pigments collect additional radiation from a part of the light spectrum such as green light, which is poorly absorbed by chlorophyll. As a result, the Chlamidomonas species are preadapted to low-light conditions.
Cyanophyceae generally need lower illumination values than Chlorophyceae to achieve high biomasses [48]. However, the decrease in species richness in this group during the construction of ports was as significant as in Chlorophyceae (Table 2). Obviously, the species of Cyanophyceae, which are less adapted to conditions of low water transparency, disappeared from the phytoplankton group during port construction, which reduced the species richness of this phytoplankton group during construction periods. On the contrary, some species well adapted to the lack of light, such as Planktothrix agardhii (Gomont) Anagnostidis and Komárek 1988, continued to dominate, although their biomass decreased (Table 2; Figure 3a).
Some species of Cyanophyceae are capable of very rapid rearrangement of the internal structure of cells in response to light conditions [23,57]. Changes in the proportions of different pigments in cells depending on the intensity and fluctuations of light illumination have also been found [17]. For example, it was found that, depending on the light conditions, the concentration of chlorophyll a in the cells of Cyanophyceae of the genus Planktothrix changed up to nine times [22]. The intensive development of P. agardhii was observed in winter in a German mesotrophic lake at very low irradiation [58]. This may explain why the dominant species P. agardhii continued to dominate the phytoplankton during the periods of port construction (Table 2), although its biomass showed a positive relationship with water transparency in the Neva Estuary (Figure 6c).
The biomass and species richness of Cryptophyceae practically did not change during the periods of port construction and the decrease in water transparency in the estuary. (Figure 3). Cryptomonas erosa Ehrenberg 1832, which dominated the Cryptophyceae under normal conditions, continued to dominate their biomass during the periods of port construction (Table 2). This species is common for the deep-layer maximum of chlorophyll in lakes with a reduced intensity of illumination [59]. The concentration of chlorophyll in cells of Cryptophyceae can also increase with the deterioration in light conditions, for example, in Cryptomonas ovata Ehrenberg 1832, it increases by 1.5 times at low illumination [22]. This species became one of the dominant cryptophytes during the construction of new port facilities (Table 2).
The biomass of dinoflagellates increased during the construction of port infrastructure (Figure 3a). This could be due to the effective recruitment of their cysts along with resuspended bottom sediments. It has previously been emphasized that benthic resting stages provide an abundant seed bank for these algae in the eastern Baltic Sea [16,60]. During construction periods, the average biomass of the one dominant species in the Neva Estuary, Peridinium cinctum (O.F.Müller) Ehrenberg 1832, increased (Table 2).
Dinoflagellate Ceratium hirundinella (O.F.Müller) Dujardin 1841 was one of the most common and dominant species of photosynthetic dinoflagellates in summer phytoplankton in the Neva Estuary throughout the 2000s [24]. This species forms the largest biomass at moderate levels of irradiation and has a complex cell configuration with horns [61], which increases the surface area of the cells and can apparently contribute to the resistance of the species to a lack of light. In addition, this species has flagella and can actively move in the water column, choosing depths at which the irradiation level is in the tolerant range [62,63]. Apparently, due to these various adaptations, the average biomass of dinoflagellates at sampling stations approximately doubled during the construction of new port facilities in the Neva Estuary (Figure 3a). P. cinctum, one of the dominant dinoflagellates in the Neva Estuary, is also well adapted to low-light conditions [64]. Its average biomass during the port construction works was higher than in their absence (Table 2). Previously, it was shown that the biomass of this species reached high values in the upper freshwater reaches of the Neva Estuary, where increased water turbidity often occurred [24]. This species is also capable of vertical migrations (of up to 10 m), rising into layers of water with better light conditions [63]. In addition, many species of Dinophyceae and Cryptophyceae are mixotrophs, which helps them withstand the lack of light [62,65,66].
Other phytoplankton algae common in the Neva Estuary have similar adaptations to poor light conditions. For instance, Dinobryon divergens O.E.Imhof 1887 was one of the dominant species of Chrysophyceae both during the periods of port construction and when construction was not carried out. (Table 2). According to Bird and Kalff [67], Chrysophyceae from the genus Dinobryon can switch to phagotrophy in low-light conditions, consuming bacteria and organic particles up to 0.23 μm in size. In a freshwater Canadian lake, these algae were mainly concentrated in the metalimnion, where, as experiments showed, their growth depended more on the number of consumed bacteria than on light conditions [67]. It is known that Euglenophyceae are also capable of mixotrophy [68], which should help them resist the lack of light.
Some species of Euglenophyceae have specific adaptations that allow them to withstand mechanical damage from suspended mineral particles. For instance, species from the genus Trachelomonas, including Trachelomonas volvocina (Ehrenberg) Ehrenberg 1834, which dominated in the Neva Estuary (Table 2) have symbiotic bacteria on the outer side of its lorica [69,70]. It has been shown that these bacteria can secrete fibers, forming a network between them. Such a layer of bacteria can protect algal cells from the mechanical damaging effect of suspended mineral particles.

5. Conclusions

The study showed that the construction of new ports led to long-term multiple increases in the concentration of suspended mineral matter and a decrease in water transparency in the Neva Estuary. This significantly reduced the total biomass of phytoplankton in the estuary and the species richness, especially of the most abundant groups of Bacillariophyceae, Chlorophyceae, and Cyanophyceae. On the contrary, the biomass of some less important phytoplankton groups under normal conditions, such as Dinophyceae and Euglenophyceae increased during the periods of the work. The analysis of beta diversity did not show significant changes between the phytoplankton community during the periods of construction of the port and its community during the periods when the work was not carried out. This suggests that, despite a significant decrease in the productivity of phytoplankton during periods of port construction, its community is quite resistant to a lack of light. The changes mainly concerned rare species, while the occurrence and biomass of dominant and subdominant species changed to a lesser extent. This indicates that the most common phytoplankton species in the estuary are preadapted to a lack of light and, under conditions of prolonged shading, can successfully compete with species that are unable to withstand a lack of light for a long time. Such adaptations in various groups of phytoplankton include an increase in the ratio of the surface area of algal cells to their volume, an increase in the concentration of chlorophyll a in cells, chromatic adaptations, the use of flagella to reach depths where the irradiation level is in the tolerant range, and mixotrophy. All of these adaptations appear to be common in estuarine phytoplankton because increased water turbidity is often observed in estuaries due to natural causes, such as the resuspension of bottom sediments during wind-induced events or tides. They also allow key phytoplankton species to withstand the long periods of increased turbidity and lack of light that occur during the construction of port infrastructure in estuaries. To correctly take into account the negative impact of the construction of new port facilities on phytoplankton and, if possible, minimize it, additional studies of the ecology of certain phytoplankton species, their relationships, and physiological responses to various environmental factors are required.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/jmse11010032/s1, Table S1: Phytoplankton species composition, number of occurrences, and biomass of algae in the Neva Estuary in 2003–2020.

Author Contributions

Conceptualization, M.S.G. and S.M.G.; field sampling, M.S.G. and S.M.G.; laboratory analyses, M.S.G. and V.N.N.; data analysis, M.S.G.; visualization, M.S.G.; writing—original draft preparation, M.S.G. and S.M.G.; writing—review and editing, M.S.G. and S.M.G.; project administration, S.M.G.; funding acquisition, S.M.G. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Zoological Institute RAS, grant number 122031100274-7.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The original contributions presented in the study are included in the article/Supplementary Material. Further inquiries can be directed to the corresponding author.

Acknowledgments

The authors give thanks to the three anonymous reviewers for their constructive comments that significantly improved the early version of the manuscript.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. The upper (UR) and middle (MR) reaches of the Neva Estuary with an indication of sampling stations (1–17) and new lands (violet) created in 2006–2007 (A) and 2014–2015 (B). Blue lines: isobaths of 5, 10, and 20 m. Areas with dots indicate dense reeds. Dam—the St. Petersburg Flood Protection Facility. Red points—Dam sluices. The red circle in the top section is the location of the Neva Estuary. Two-letter country codes are given according to ISO 3166-1 alpha-2 [32].
Figure 1. The upper (UR) and middle (MR) reaches of the Neva Estuary with an indication of sampling stations (1–17) and new lands (violet) created in 2006–2007 (A) and 2014–2015 (B). Blue lines: isobaths of 5, 10, and 20 m. Areas with dots indicate dense reeds. Dam—the St. Petersburg Flood Protection Facility. Red points—Dam sluices. The red circle in the top section is the location of the Neva Estuary. Two-letter country codes are given according to ISO 3166-1 alpha-2 [32].
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Figure 2. Average Secchi depth during the periods of construction of new port facilities in 2006–2007 (a), and in 2014–2015 (b), and on average in the 2000s, without data for 2006–2007 and 2014–2015 (c), the average concentration of suspended particulate mineral matter in 2006–2007 (d) and 2014–2015 (e), and on average for the 2000s, without data for 2006–2007 and 2014–2015 (f) in the Neva Estuary in midsummer. Sec—Secchi depth; SMM—concentration of suspended particulate mineral matter.
Figure 2. Average Secchi depth during the periods of construction of new port facilities in 2006–2007 (a), and in 2014–2015 (b), and on average in the 2000s, without data for 2006–2007 and 2014–2015 (c), the average concentration of suspended particulate mineral matter in 2006–2007 (d) and 2014–2015 (e), and on average for the 2000s, without data for 2006–2007 and 2014–2015 (f) in the Neva Estuary in midsummer. Sec—Secchi depth; SMM—concentration of suspended particulate mineral matter.
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Figure 3. Average biomass (a), and species richness (b) of various algae groups with standard deviation (black bars) at the station during the periods of construction of new port facilities (DC) and in their absence (NC) in the Neva Estuary in the 2000s. DC—averaged values for all stations for 2006–2007 and 2014–2015. NC—averaged values for all stations for 2003–2005; 2008–2013; 2016–2020. B—biomass; SP—species; BCL—Bacillariophyceae; CLR—Chlorophyceae; CHR—Chrysophyceae; CRP—Cryptophyceae; CYA—Cyanophyceae; DNP—Dinophyceae; EUG—Euglenophyceae; XAN—Xanthophyceae.
Figure 3. Average biomass (a), and species richness (b) of various algae groups with standard deviation (black bars) at the station during the periods of construction of new port facilities (DC) and in their absence (NC) in the Neva Estuary in the 2000s. DC—averaged values for all stations for 2006–2007 and 2014–2015. NC—averaged values for all stations for 2003–2005; 2008–2013; 2016–2020. B—biomass; SP—species; BCL—Bacillariophyceae; CLR—Chlorophyceae; CHR—Chrysophyceae; CRP—Cryptophyceae; CYA—Cyanophyceae; DNP—Dinophyceae; EUG—Euglenophyceae; XAN—Xanthophyceae.
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Figure 4. Principal coordinate analysis (PCoA) plot for the differences in group homogeneities based on beta diversity between phytoplankton communities during the periods of port construction (DC) and in the absence (NC) of such works (a); homogeneity of multidimensional dispersions of the phytoplankton community of the Neva Estuary during the periods of construction (DC) and in the absence (NC) of hydrotechnical works (b); the thick line is the average distance to the median value of the variance of beta diversity, the block boundaries are for the variance of beta diversity for frequently occurring species, the black lines are the variance of all community species.
Figure 4. Principal coordinate analysis (PCoA) plot for the differences in group homogeneities based on beta diversity between phytoplankton communities during the periods of port construction (DC) and in the absence (NC) of such works (a); homogeneity of multidimensional dispersions of the phytoplankton community of the Neva Estuary during the periods of construction (DC) and in the absence (NC) of hydrotechnical works (b); the thick line is the average distance to the median value of the variance of beta diversity, the block boundaries are for the variance of beta diversity for frequently occurring species, the black lines are the variance of all community species.
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Figure 5. Relationships between Secchi depth (Sec), the concentration of suspended particulate mineral matter (SMM), biomass (B), and species richness (SP) in the Neva Estuary in 2003–2020. The graphs on the left are the bivariate scatterplots, with a fitted line; the central histograms show the residuals from the linear model; and the values on the right are Pearson’s correlation coefficients. Asterisks indicate the significance of the correlation. (* p < 0.05; ** p < 0.01; *** p < 0.001). ns—not significant; m—meter; m3—cubic meter; g—gramm; mg—milligram; num—number; st—station.
Figure 5. Relationships between Secchi depth (Sec), the concentration of suspended particulate mineral matter (SMM), biomass (B), and species richness (SP) in the Neva Estuary in 2003–2020. The graphs on the left are the bivariate scatterplots, with a fitted line; the central histograms show the residuals from the linear model; and the values on the right are Pearson’s correlation coefficients. Asterisks indicate the significance of the correlation. (* p < 0.05; ** p < 0.01; *** p < 0.001). ns—not significant; m—meter; m3—cubic meter; g—gramm; mg—milligram; num—number; st—station.
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Figure 6. Phytoplankton biomass vectors based on NMDS results and environmental variables, water transparency [Sec, m], and concentrations of suspended particulate mineral matter [SMM, g m−3] in the Neva Estuary in 2003–2020. Plot (a): Bacillariophyceae; plot (b): Chlorophyceae; plot (c): Cyanophyceae; and plot (d): Dinophyceae, Cryptophyceae, Chrysophyceae, Euglenophyceae, and Xanthophyceae.
Figure 6. Phytoplankton biomass vectors based on NMDS results and environmental variables, water transparency [Sec, m], and concentrations of suspended particulate mineral matter [SMM, g m−3] in the Neva Estuary in 2003–2020. Plot (a): Bacillariophyceae; plot (b): Chlorophyceae; plot (c): Cyanophyceae; and plot (d): Dinophyceae, Cryptophyceae, Chrysophyceae, Euglenophyceae, and Xanthophyceae.
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Table
Table 1. Average water salinity and temperature in midsummer during the periods of construction of new port facilities (2006–2007; 2014–2015) and in their absence (2003–2005; 2008–2013; 2016–2020). S—water salinity; T—water temperature; ± standard error.
Table 1. Average water salinity and temperature in midsummer during the periods of construction of new port facilities (2006–2007; 2014–2015) and in their absence (2003–2005; 2008–2013; 2016–2020). S—water salinity; T—water temperature; ± standard error.
Periods of Observation2006–20072014–20152003–2020
S [PSU]0.33 ± 0.040.35 ± 0.020.37 ± 0.01
T [°C]18.27 ± 0.1920.86 ± 0.1720.30 ± 0.02
Table
Table 2. Species richness and the most dominant species in the phytoplankton biomass in the Neva Estuary during the construction of new port facilities (DC) and during the period when this construction was not carried out (NC).
Table 2. Species richness and the most dominant species in the phytoplankton biomass in the Neva Estuary during the construction of new port facilities (DC) and during the period when this construction was not carried out (NC).
Groups of
Phytoplankton		Number of
Species		Predominant Species and Their Biomass
(Minimum–Average–Maximum)
[Wet Weight mg m−3]
DCNCDCNC
Bacillariophyceae1223Skeletonema sp.
(0–219.0–2409.0)		Skeletonema subsalsum
(0–310.8–2528.1)
Skeletonema subsalsum
(0–167.0–636.8)		Pantocsekiella kuetzingiana
(0–302.2–16,127.4)
Aulacoseira islandica
(0–96.6–678.3)		Aulacoseira islandica
(0–247.4–3155.7)
Chlorophyceae2556Chlamidomonas sp.
(0–81.4–747.8)		Mougeotia sp.
(0–158.1–2744)
Coelastrum microporum
(0–32.4–288.0)		Mucidosphaerium pulchellum
(0–145.8–7833.6)
Mucidosphaerium pulchellum
(0–31.4–288.0)		Chlamidomonas sp.
(0–63.4–2928.8)
Cyanophyceae1928Planktothrix agardhii
(0–300.0–2279.4)		Planktothrix agardhii
(0–433.1–8800.0)
Limnothrix planctonica
(0–137.1–686.2)		Dolichospermum
flos-aquae
(0–353.9–5153.8)
Dolichospermum flos-aquae
(0–64.7–331.9)		Aphanizomenon
flos-aquae
(0–324.1–6389.9)
Chrysophyceae311Mallomonas charkoviensis
(0–18.1–198.8)		Dinobryon divergens
(0–43.3–1680.0)
Dinobryon divergens
(0–2.1–21.6)		Mallomonas sp.
(0–4.6–107.4)
Synura uvella
(0–0.6–6.3)		Mallomonas harkoviensis
(0–3.8–258.4)
Cryptophyceae46Cryptomonas erosa
(0–544.1–1644.0)		Cryptomonas erosa
(0–474.7–4384.0)
Cryptomonas ovata
(0–299.9–3024.0)		Cryptomonas marssonii
(0–258.1–2491.2)
Komma caudata
(0–91.3–373.3)		Komma caudata
(0–213.6–1296.9)
Dinophyceae68Gymnodinium sp.
(0–269.8–2304.0)		Ceratium hirundinella
(0–125.0–3200.0)
Peridinium cinctum
(0–194.4–1200.0)		Peridinium cinctum
(0–120.9–2662.4)
Ceratium hirundinella
(0–46.6–296.0)		Apocalathium aciculiferum
(0–72.4–2349.5)
Euglenophyceae34Trachelomonas sp.
(0–265.8–2356.0)		Trachelomonas volvocina
(0–125.8–4680.0)
Trachelomonas volvocina
(0–5.0–33.9)		Lepocinclis acus
(0–13.5–825.0)
Lepocinclis acus
(0–0.6–6.6)		Trachelomonas sp.
(0–10.9–876.4)
Xanthophyceae11Tribonema affine
(0–12.1–187.0)		Tribonema affine
(0–19.9–1177.5)
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Golubkov, M.S.; Nikulina, V.N.; Golubkov, S.M. Impact of the Construction of New Port Facilities on the Biomass and Species Composition of Phytoplankton in the Neva Estuary (Baltic Sea). J. Mar. Sci. Eng. 2023, 11, 32. https://doi.org/10.3390/jmse11010032

AMA Style

Golubkov MS, Nikulina VN, Golubkov SM. Impact of the Construction of New Port Facilities on the Biomass and Species Composition of Phytoplankton in the Neva Estuary (Baltic Sea). Journal of Marine Science and Engineering. 2023; 11(1):32. https://doi.org/10.3390/jmse11010032

Chicago/Turabian Style

Golubkov, Mikhail S., Vera N. Nikulina, and Sergey M. Golubkov. 2023. "Impact of the Construction of New Port Facilities on the Biomass and Species Composition of Phytoplankton in the Neva Estuary (Baltic Sea)" Journal of Marine Science and Engineering 11, no. 1: 32. https://doi.org/10.3390/jmse11010032

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