Next Article in Journal
Evaluating Sediment Yield Response to Watershed Management Practices (WMP) by Employing the Concept of Sediment Connectivity
Previous Article in Journal
A Sensemaking Perspective of Digitalisation in Construction Organisations
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Sustainability
Volume 15
Issue 3
10.3390/su15032345
sustainability-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Not a Good Place to Live for Most, but Excellent for a Few—Diversity of Zooplankton in a Shallow Coastal Ecosystem

by
Maciej Karpowicz
1,*,
Ryszard Kornijów
2 and
Jolanta Ejsmont-Karabin
3
1
Department of Hydrobiology, Faculty of Biology, University of Białystok, Ciołkowskiego 1J, 15-245 Białystok, Poland
2
Department of Fisheries Oceanography and Marine Ecology, National Marine Fisheries Research Institute, Kołłątaja 1, 81-332 Gdynia, Poland
3
Research Station in Mikołajki, Nencki Institute of Experimental Biology, Polish Academy of Sciences, Pasteur 3, 02-093 Warsaw, Poland
*
Author to whom correspondence should be addressed.
Sustainability 2023, 15(3), 2345; https://doi.org/10.3390/su15032345
Submission received: 21 December 2022 / Revised: 17 January 2023 / Accepted: 25 January 2023 / Published: 27 January 2023
Browse Figures
Review Reports Versions Notes

Abstract

Shallow brackish water habitats are characterized by highly unstable environmental conditions, which result in low species diversity. We performed our research in the Vistula Lagoon in three seasons in the years 2019–2021. This lagoon is characterized by extremely variable environmental conditions, and our research covered the period of hydro-technical works before opening the canal through the Vistula Spit, which could be an additional stress factor. The aim of our study was to present the particularities of zooplankton communities (Rotifera; Crustacea) in the shallow coastal ecosystem. Our results pointed out very low diversity of zooplankton which could be caused by multi-stress conditions related to increased turbidity and low salinity. Nevertheless, under these conditions, some species achieved an advantage and strongly dominated the zooplankton communities. Domination of Eurytemora affinis in the Vistula Lagoon as well as in other brackish habitats is a well-known phenomenon. Moreover, the Vistula Lagoon offered favorable conditions for the intense development of non-indigenous, or alien, species like Diaphanosoma mongolianum, D. orghidani, and Acanthocyclops americanus. Therefore, brackish waters seem to be favorable transitional areas for non-native fauna that may subsequently spread into adjacent freshwater and marine systems.

1. Introduction

Shallow brackish water habitats are often characterized by unstable environmental conditions, primarily due to dynamics in salinity, temperature, turbidity, and algae concentrations [1,2]. These environmental changes are considered as main stressors affecting the biodiversity of shallow coastal ecosystems [3]. Among the most important are rapid variations in salinity due to mixing brackish water with sea and freshwater inflows [3,4], which can cause physiological stress for freshwater organisms as a result of limited osmoregulatory capabilities [5,6]. However, many freshwater Cladocera and Copepoda can tolerate moderate levels of salinity [5], and shallow brackish habitats can be colonized by freshwater and seawater euryhaline species, as well as by typical inhabitants of brackish habitats. Despite this, brackish water is considered a habitat with lower species diversity compared to fresh and marine waters. The lowest number of taxa tends to occur at salinity levels between 5 and 8 PSU, which is known as a paradox of brackish waters [2,7]. Changes in salinity are the main cause of the disappearance of some species and the occurrence of others [8]. The inflow of seawater, apart from salinity, is often associated with strong temperature fluctuations, which can be an additional stress factor for zooplankton [9,10]. Water turbidity, often as a result of resuspension, is another factor that strongly affects the functioning of many shallow aquatic ecosystems [11,12]. It is caused mainly by the presence of mineral (clay and sand) and organic particles, as well as humic substances [13]. Elevated turbidity is frequently related to an increase in water color and high primary productivity, often with associated algal blooms and bacterial decay [12,14], and may significantly affect the abundance of filter-feeding zooplankton [15,16,17].
The Vistula Lagoon (southern Baltic Sea) is a shallow brackish water body with extremely variable environmental conditions, including salinity, water transparency, temperature, oxygenation, trophic state, wind speed, and water level [10,18,19]. Zooplankton in the lagoon has been studied for over 60 years [20,21,22,23]. In the 1970s, changes in the structure of zooplankton were visible due to eutrophication with dominations of rotifers [21], and at the beginning of the 21st century, a decrease in biodiversity and zooplankton biomass was observed [22]. This was accompanied by a gradual decline in phytoplankton biomass [24].
The Vistula Lagoon is relatively isolated, with an inflow of seawater across the Strait of Baltiysk in the eastern part on Russian territory; therefore, there was a salinity gradient, with the lowest salinity at the western part of the lagoon [19,23]. The Polish part of the Vistula Lagoon was characterized by differentiated habitat heterogeneity, whereas the Middle Basin was phytoplankton-dominated, Elbląg Bay was macrophyte-dominated, and the West Basin was in a transition state between the two former ones [19].
For decades, almost every year, hydro-technical works are carried out in various parts of the lagoon. These are mainly dredging works aimed at deepening the approaches to ports. The largest investment during our research was digging a canal through the Vistula Spit, a project still ongoing before our research was completed. The main aim of our work is to present particularities of zooplankton communities (Rotifera, Crustacea) in this shallow coastal ecosystem. We analyzed seasonal changes in zooplankton structures and present our results on the background of the long-term changes. We hypothesize that construction works on the Vistula Split, as an additional strong anthropogenic environmental stressor, substantially contribute to decline in the diversity and density of zooplankton communities. Furthermore, the results of our research could be relevant for the analysis of future changes in plankton communities after increasing the exchange of waters with the Baltic Sea.

2. Materials and Methods

The non-tidal Vistula Lagoon is the second-largest inner marine water basin in Europe and is located in the southern Baltic Sea. It is strongly elongated and NE–SW oriented, and its surface area is 838 km2 (Figure 1). It is separated from the open sea by the Vistula Spit—a narrow belt of sandy land—and contact with sea waters occurs through the Baltiysk Strait which has a length of 2 km. The lagoon is very shallow (mean depth 2.5 m; max depth 5.2 m). Its large surface area and shallowness contribute to continuous water mixing and therefore prevent thermal and oxygen stratification while favoring sediment resuspension. The lagoon is highly eutrophic [25]. The water level is subject to large fluctuations with an amplitude of up to 1.2 m, especially in the period of the autumn–winter storms [26].
The research was carried out in three seasons (spring, summer, and autumn) in the years 2019–2021 at six sampling sites in the western part of the lagoon, where the impact of anthropogenic stress factors, in connection with the ongoing investment of the Vistula Spit digging and the construction of a new waterway, seemed to be the greatest. Four sites (no. 1–4) were located on the planned fairway between the Vistula Split and Elbląg city (Figure 1) at a depth of 2.6–2.9 m. Two sampling stations (no. 5–6) were located near the shore in the littoral zone at the depth of 1.4–1.5 m (Figure 1).
The sampling was made in the middle of spring, summer, and autumn each year. Water samples were collected from the surface to the bottom using a 6 cm-diameter acrylic pipe [23]. Ten liters of water were filtered through a 50-µm plankton net and fixed with 4% formalin. Field measurements include water transparency with a Secchi disc, and temperature, dissolved oxygen concentration, and salinity with a portable multiparameter Elmetron CPC- 401 m probe (ELMETRON, Poland).
In 2019–2021, the average water temperature in the study area was 13.9 ± 4.3 °C, salinity 3.6 ± 0.8 PSU, oxygenation 96.4 ± 15.9%, Secchi depth 0.47 ± 0.24 m, and turbidity 38.2 ± 22 FNU (Kornijów, unpublished data). The emergent vegetation was represented mainly by a discontinuous belt of reed Phragmites australis (Cav.) Trin. ex Steud, and by round shape clumps of a common club-rush Schoenoplectus lacustris (L.) Palla at the side adjacent to the open water. Meadows of submerged macrophytes, represented mostly by a Eurasian watermilfoil Myriophyllum spicatum L. and by hornwort Ceratophyllum demersum L. occurred only at the north-western shore in the vicinity of the Kąty Bay. In 2019, they reached the lagoon for a distance of 2700 m; in 2020, their range shrank to 850 m, and in 2021, their presence was not found (Kornijów, unpublished data).
In each sample, all rotifers and crustaceans were counted by species. The length of body in 10 individuals of each species was measured. The biomass of crustaceans was calculated from the relationship between the body length and weight according to [27], whereas that of rotifers after [28].
Statistical analyses were performed with XLSTAT Life Sciences (Addinsoft, New York, NY, USA). Basic descriptive statistics for the abundance and diversity of zooplankton were presented as box plots (Figure 2 and Figure 3). The lower and upper limits of the boxes are the first and third quartiles, respectively. The central horizontal bars are the medians, and the crosses are the means. The whiskers represented the minimum and maximum, and points above or below are outliers. One-way ANOVA followed by Tukey’s HSD (Honestly Significantly Different) was used to test all pairwise differences between means. The agglomerative hierarchical cluster analysis based on the Bray–Curtis similarity matrix and biodiversity indices (Shannon index and dominance B-P index) were calculated using Biodiversity Pro: Free Statistics Software for Ecology [29].

3. Results

A total of 18 crustacean species (3 Calanoida, 4 Cyclopoida, 11 Cladocera) were identified (including 3 Diaphanosoma species) (Table 1). Furthermore, representatives of Harpacticoida were found mostly in spring and autumn, but were not determined to species level. The number of crustacean species ranged from 1 to 6, with an average of 2.9 ± 1.2 species. The lowest species number was recorded in autumn (Figure 2D). The average Shannon index was 0.56 ± 0.64, with the lowest values in spring and the highest in summer (Figure 2E). The average dominance B-P index was 0.79 ± 0.22, with the lowest values in summer and the highest in spring and autumn (Figure 2F).
A total of 26 Rotifera species were recorded (Table 1), but among them, 11 species were single records, two species were found twice, and three species were found 3 times. The average number of Rotifera species was 3.6 ± 2.6, with the highest number of species in summer (Figure 3B). The average values of the Shannon diversity index and B–P dominance index were 0.69 ± 0.37 and 0.47 ± 0.22, respectively. The lowest values and greatest variability of both indices were observed in spring (Figure 3C,D). We found no significant differences in the diversity parameters of crustaceans and rotifers between the years. We also did not find any differences in zooplankton communities between sampling sites, which indicated homogeneous conditions on the whole studied area of the Vistula Lagoon.
The average density of Crustacea was 339 ± 295 ind. L−1, but there were differences between seasons, with the highest values in spring and the lowest in autumn (Figure 2A). The abundance of copepod nauplii was the highest in spring (Figure 2C), while the abundance of adults (without nauplii and copepodites) peaked in summer (Figure 2B). Rotifers were most numerous in summer, while in spring and autumn the density of rotifers was low (Figure 3A). Interestingly, we did not find any rotifers in spring 2019.
The biomass of zooplankton ranged from 0.04 to 23.6 mg L−1 (Figure 4), with an average of 4.50 ± 4.49 mg L−1. The crustaceans strongly dominated over Rotifera (Figure 4), with average biomasses of 4.40 ± 4.51 mg L−1 and 0.09 ± 0.17 mg L−1, respectively. High biomasses of zooplankton were recorded in summer and spring and low biomasses were recorded in autumn. Additionally, the year 2019 was distinguished by higher zooplankton biomasses (Figure 4).
The crustacean communities were strongly dominated by one or two species. The most common species during the whole study period was calanoid Eurytemora affinis (Table 1). It dominated in spring and autumn. The number of nauplii was the highest in spring (Figure 2C). In summer, there was a rapid growth of Diaphanosoma species (even to 541 ind. L−1), which was the dominant component of zooplankton. Diaphanosoma mongolianum was dominant, but we found also D. brachyurum and D. orghidani. In the summer of 2021, we observed high biomass of Cyclopoida (Figure 4) due to the development of Acanthocyclops americanus. In autumn, populations of Diaphanosoma declined, and E. affinis dominated again. Other calanoids, Acartia bifilosa were frequently found (Table 1) and coexisted with E. affinis but with low numbers. Therefore, crustacean communities showed a high similarity in spring and autumn, which differed from summer (Figure 5A).
The communities of Rotifera were strongly dominated by species of the genus Keratella (Table 1), which accounted for 95% of the average numbers of all rotifers. In spring, K. quadrata dominated but did not reach numbers higher than several dozen individuals per liter. In summer and autumn, an extremely strong dominance of small detritivorous K. cochlearis was noted. Both morphological forms were present, with a predominance of typica over tecta. Keratella cruciformis, the only brackish-water rotifer species encountered in this study, occurred mainly in spring. Although relatively frequent, the species did not exceed the density of 5 ind. L−1. In the year 2021, its presence was not recorded. In the springs of 2020–2021, the community of rotifers was extremely poor in species (4–5), which was also accompanied by very low density. The most abundant of them, Hexarthra fennica, reached a maximum of 30 ind. L−1. The summer and autumn communities had a similar species structure, with a strong dominance of Brachionidae, and were also characterized by much higher densities, up to ca. 4500 ind. L−1 in the year 2020. The Rotifera communities showed a high similarity in summer and autumn, which differed from spring (Figure 5B).

4. Discussion

The low diversity of zooplankton is a common phenomenon in brackish habitats [1,7]. Our results also indicated a very low diversity of zooplankton, even lower than previously reported. The decline in zooplankton diversity in the Vistula Lagoon in the early 21st century was reported by Paturej et al. (2014) [22]. In the years 1977–1988, the Shannon index was 2.65 ± 0.15, while in the years 2007–2009 it was only 1.33 ± 0.2 [21,22]. Our 2019–2021 studies also showed even lower Shannon index values for Crustacea and Rotifera, i.e., 0.56 ± 0.64 and 0.69 ± 0.37, respectively. The number of Rotifera species also decreased from 28 species in the 1970s [21] to 15 species in 2007–2009 [10]. The results of this study reported 26 species of Rotifera, however, 16 of them were rare (or single record). Nevertheless, we observed a very low share of Rotifera in the zooplankton biomass, whereas they were the dominant component of zooplankton biomass in the 1970s [21]. The number of crustacean species was relatively similar with 16–17 species during the last 50 years, but there were differences between species composition in each study period [21,22]. On the other hand, simultaneously with a decrease in zooplankton species diversity, we observed high zooplankton biomass throughout the research period, much higher than in previous years [22]. This was caused by the intense development of one species (Eurytemora affinis or Diaphanosma mongolianum), which strongly dominated zooplankton communities.
We suppos that multi-stress conditions, mainly related to salinity and increased turbidity, may be responsible for low zooplankton diversity in Vistula Lagoon. The paradox of brackish waters assumed the lowest species at salinity levels 5–8 PSU [2,7], and the results of our studies pointed out that even lower levels of salinity (3.6 ± 0.8 PSU) could significantly affect zooplankton communities. The results of our study demonstrated that typical brackish species E. affinis dominated zooplankton communities, and this level of salinity was high enough to prevent the development of typical freshwater species, as well as marine species. Especially, development of rotifers and cladocerans (except Diaphanosoma mongolianum), and thus organisms of freshwater origin sensitive to salinity [2,30,31], were limited. Typically freshwater cladocerans that used to be common in the Vistula Lagoon (e.g., Bosmina longirostris, Ceriodaphnia quadrangula, Chydorus sphaericus) now are rare. Similarly, the development of freshwater Cyclopoida was strongly reduced and their contribution to the zooplankton biomass was negligible. Only intense development of cyclopoid Acanthocyclops americanus, which is considered an invasive species in Europe [32] was observed in the summer of 2021. On the other hand, Keratella cruciformis, the typical brackish-water rotifer species, almost disappeared, whereas other freshwater species of the genus Keratella remained abundant.
The large surface area and small depth of Vistula Lagoon favor continuous water mixing, which leads to intensive sediment resuspension [19,33]. We conducted our research in the area of hydro-technical works, which could additionally increase turbidity. Inorganic suspended solids disrupt food collection [16] and dilute gut contents, as a result, less food could be assimilated [34,35,36]. High concentrations of suspended clay and other mineral substances could suppress the development of filter feeder cladocerans and favor rotifers [15]. However, the results of our research indicat a declining rotifer share in zooplankton biomass in favor of crustaceans. This may be a result of the negative effect of increased salinity because rotifers are very sensitive to this variable [2,37,38] as organisms of clearly freshwater origin [39]. Rotifers can also be suppressed by large crustacean zooplankton through mechanical interference, exploitative competition, and predation [40,41]. On the other hand, Paturej et al. (2014) suggested that significant qualitative and quantitative changes over the 30-year period may have not been caused by trophic changes in the estuary [22]. In the community of rotifers in this period, as in our research, a strong increase in the share of Keratella cochlearis was observed, as well as a decrease in species diversity of zooplankton and the disappearance of species typical for brackish waters.
Nevertheless, under conditions that are difficult for most species, some of them have achieved a significant advantage. The zooplankton communities were strongly dominated by one species—Eurytemora affinis in spring and autumn, and Diaphanosoma mongolianum in summer. Furthermore, in the summer of 2021, Acanthocyclops americanus achieved high abundance. A similar situation was also noted in the case of rotifers, which were strongly dominated by one species, Keratella cochlearis. The dominance of small detritovores with a high rate of phosphorus regeneration may favor accelerating eutrophication processes [42].
The dominant species Eurytemora affinis is widespread in coastal and estuarine waters in the northern hemisphere [43], as well as in the Baltic Sea [44], including the Vistula Lagoon [22]. It often dominates crustacean zooplankton in both freshwater and coastal estuaries [45,46]. The population peaks of E. affinis in the Baltic Sea usually were found in late summer [47]. In our research, the peaks of E. affinis population in the Vistula Lagoon occurred in spring, with a decline in summer when it was replaced by Diaphanosoma spp. However, the highest number of nauplii of Calanoida was recorded in summer, and in autumn, E. affinis dominated again. A similar pattern of E. affinis population dynamics was observed in the Chesapeake Bay (USA), with peaks in early spring and late winter [48]. Eurytemora affini, being a typical opportunistic (r) life strategist, has a development time that is as short as physiologically possible when conditions are favorable [47]. This species may have an advantage in the Vistula Lagoon because it is well-adapted to highly turbid environments while other estuarine copepods (Acartia spp.) would be rather food-limited [49]. Temperature and salinity also seem to favor the development of this species, because its optimal temperature range is 5–10°C and salinities 3–8 PSU [50,51]. We did not find non-native invader Eurytemora carolleeae, which were found in estuaries of the Baltic Sea [52,53] and has recently penetrated the Oder River system in Poland [43].
The summer zooplankton was dominated by Diaphanosoma species, and this is a common phenomenon in the Vistula Lagoon [54]. Only Diaphanosoma brachyurum was previously reported from the Polish part of the Vistula Lagoon [21,22], as well as from Poland [27]. The latest detailed morphological and genetic results indicated the presence of 3–4 species in the Vistula Lagoon, D. brachyurum, D. mongolianum, and D. orghidani [55]. Furthermore, genetic results indicated that one individual in the Vistula Lagoon was closely related to Diaphanosoma lacustris, but it had intermediate features between D. mongolianum and D. lacustris. This research also pointed out to close affinity (genetic and morphology) between D. mongolianum and D. lacustris [55]. The results of this study indicat that Diaphanosoma mongolianum strongly dominated summer zooplankton in the Vistula Lagoon, but we have found also D. brachyurum and D. orghidani. The presence and domination of D. mongolianum were previously reported from the Russian part of the Vistula Lagoon [54]. The co-occurrence of 2–4 species of Diaphanosoma in one waterbody is a common phenomenon [56,57,58]. However, the factors that favor the development of D. mongolianum in the Vistula Lagoon are ambiguous. It is considered that D. mongolianum and D. orghidani are more thermophilous species compared to D. brachyurum [59], however, the temperature of the Vistula Lagoon water is much lower than in lakes of this region. On the other hand, D. mongolianum prefers more lotic and turbid habitats than D. brachyurum [57]. Diaphanosoma mongolianum and D. orghidani are non-native to Poland, and the second species is even considered an invasive one in Europe [57]. These species were rarely found in the natural Polish lakes [55,60], but begin to penetrate Central Europe via rivers [55,57,61,62].
The other potential invader, Acanthocyclops americanus (= A. trajani) reached high densities in the Vistula Lagoon in summer of 2021. Alekseev et al. (2021) advocated a Nearctic origin and an alien status in Eurasia for A. americanus [32]. In the warm season, this species strongly dominated in many eutrophic reservoirs in Belgium, France, Spain, and in newly built reservoirs in Europe [63,64]. The high trophy and high turbidity of the Vistula Lagoon seem to favor this species. However, the taxonomy of the Acanthocyclops robustus group is confusing [32,65]. Miracle et al. (2013) designed a neotype of Acanthocyclops americanus (Marsh, 1893) and placed A. trajani Mirabdullayev and Defaye 2002 as a synonym of A. americanus [65]. Another closely related species A. einslei Mirabdullayev and Defaye 2004 was recently assigned as a synonym of A. robustus (G.O. Sars, 1863) [32]. However, this synonymizing could be questionable, and A. americanus, A. trajani, A. robustus, and A. einslei could be separate species (Hołyńska pers. comm.) [66]. Nevertheless, A. trajani (A. americanus) was previously commonly reported from Poland [67,68,69] as well as other Central Europe countries [27,70].
Our results may indicate that a low level of salinity and increased turbidity could be related to the declining diversity of zooplankton in the Vistula Lagoon. These conditions turned out to be favorable for some species that gained the upper hand and strongly dominated zooplankton communities. Domination of E. affinis in Vistula Lagoon as well as in other brackish habitats is a well-known phenomenon. Moreover, the Vistula lagoon offer favorable conditions for the intense development of non-indigenous or alien species like D. mongolianum, D. orghidani, and A. americanus. However, we did not find Eurytemora carolleeae which recently spread in Europe and Poland [43], and Cercopagis pengoi which were known from the Vistula Lagoon [54,71]. Nevertheless, brackish waters are hospitable transitional areas for non-native fauna that may subsequently spread into adjacent freshwater and marine systems [72].

Author Contributions

M.K.: writing—original draft preparation, conceptualization, analyzed the crustacean zooplankton, performed statistical analysis, visualization; R.K.: conceptualization, field analyses and sampling, writing—review and editing; J.E.-K.: analyzed the Rotifera zooplankton, writing—review and editing. All authors have read and agreed to the published version of the manuscript.

Funding

The study was funded by the National Marine Fisheries Research Institute in Gdynia, Poland (project: DOT21/ANZAWI), and by the Faculty of Biology, University of Białystok, Poland.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Cognetti, G.; Maltagliati, F. Biodiversity and adaptive mechanisms in brackish water fauna. Mar. Pollut. Bull. 2000, 40, 7–14. [Google Scholar] [CrossRef]
  2. Paturej, E.; Gutkowska, A. The effect of salinity levels on the structure of zooplankton communities. Arch. Biol. Sci. 2015, 67, 483–492. [Google Scholar] [CrossRef]
  3. Vilas-Boas, J.A.; Arenas-Sánchez, A.; Vighi, M.; Romo, S.; Van den Brink, P.J.; Pedroso Dias, R.J.; Rico, A. Multiple stressors in Mediterranean coastal wetland ecosystems: Influence of salinity and an insecticide on zooplankton communities under different temperature conditions. Chemosphere 2021, 269, 129381. [Google Scholar] [CrossRef] [PubMed]
  4. Wooldridge, T.H.; Deyzel, S.H.P. Temperature and salinity as abiotic drivers of zooplankton community dynamics in the Great Berg Estuary. Trans. R. Soc. S. Afr. 2009, 62, 219–237. [Google Scholar] [CrossRef]
  5. Aladin, N.V. Salinity tolerance and morphology of the osmoregulation organs in Cladocera with special reference to Cladocera from the Aral Sea. Hydrobiologia 1991, 225, 291–299. [Google Scholar] [CrossRef]
  6. Frey, D.G. The penetration of cladocerans into saline waters. Hydrobiologia 1993, 267, 233–248. [Google Scholar] [CrossRef]
  7. Remane, A.; Schlieper, C. Biology of brackish waters. Binnengewässer 1972, 25, 1–372. [Google Scholar]
  8. Ojaveer, H.; Jaanus, A.; MacKenzie, B.; Martin, G.; Olenin, S.; Radziejewska, T.; Telesh, I.; Zettler, M.L.; Zaiko, A. Status of biodiversity in the Baltic Sea. PLoS ONE 2010, 5, e12467. [Google Scholar] [CrossRef]
  9. Tunowski, J. Zooplankton structure in heated lakes with differing thermal regimes and water retention. Arch. Pol. Fish. 2009, 17, 291–303. [Google Scholar] [CrossRef]
  10. Paturej, E.; Gutkowska, A.; Koszałka, J.; Bowszys, M. Effect of physicochemical parameters on zooplankton in the brackish, coastal Vistula Lagoon. Oceanologia 2017, 59, 49–56. [Google Scholar] [CrossRef]
  11. Zettler, E.R.; Carter, J.C.H. Zooplankton community and species responses to a natural turbidity gradient in Lake Temiskaming, Ontario-Quebec. Can. J. Fish. Aquat. Sci. 1986, 43, 665–673. [Google Scholar] [CrossRef]
  12. Goździejewska, A.M.; Kruk, M. Zooplankton network conditioned by turbidity gradient in small anthropogenic reservoirs. Sci. Rep. 2022, 12, 3938. [Google Scholar] [CrossRef]
  13. APHA. Standard Methods for the Examination of Water and Wastewater, 20th ed.; American Public Health Association: Washington, DC, USA, 1999. [Google Scholar]
  14. Paaijmans, K.P.; Takken, W.; Githeko, A.K.; Jacobs, A.F.G. The effect of water turbidity on the near-surface water temperature of larval habitats of the malaria mosquito Anopheles gambiae. Int. J. Biometeorol. 2008, 52, 747–753. [Google Scholar] [CrossRef]
  15. Kirk, K.L.; Gilbert, J.J. Suspended clay and the population dynamics of planktonic rotifers and cladocerans. Ecology 1990, 71, 1741–1755. [Google Scholar] [CrossRef]
  16. Kirk, K.L. Effects of suspended clay on Daphnia body growth and fitness. Freshw. Biol. 1992, 28, 103–109. [Google Scholar] [CrossRef]
  17. Levine, S.N.; Zehrer, R.F.; Burns, C.W. Impact of resuspended sediment on zooplankton feeding in Lake Waihola, New Zealand. Freshw. Biol. 2005, 50, 1515–1536. [Google Scholar] [CrossRef]
  18. Paturej, E.; Kruk, M. The impact of environmental factors on zooplankton communities in the Vistula Lagoon. Oceanol. Hydrobiol. Stud. 2011, 40, 37–48. [Google Scholar] [CrossRef]
  19. Kornijów, R. Ecosystem of the Polish part of the Vistula Lagoon from the perspective of alternative stable states concept, with implications for management issues. Oceanologia 2018, 60, 390–404. [Google Scholar] [CrossRef]
  20. Różańska, Z. Zooplankton of the Vistula Lagoon. Zesz. Nauk. Wyższej Szkoły Rol. W Olszt. 1963, 16, 41–57. (In Polish) [Google Scholar]
  21. Adamkiewicz-Chojnacka, B. Dynamics of the Vistula Lagoon zooplankton numbers. Oceanologia 1983, 16, 97–132. [Google Scholar]
  22. Paturej, E.; Gutkowska, A.; Mierzejewska, J. Long-term quantitative and qualitative changes in the zooplankton community of the Vistula Lagoon. J. Coast. Res. 2014, 30, 337–343. [Google Scholar] [CrossRef]
  23. Kornijów, R.; Karpowicz, M.; Ejsmont-Karabin, J.; Nawrocka, L.; de Eyto, E.; Grzonkowski, K.; Magnuszewski, A.; Jakubowska, A.; Wodzinowski, T.; Woźniczka, A. Patchy distribution of phyto- and zooplankton in large and shallow lagoon under ice cover and resulting trophic interactions. Mar. Freshw. Res. 2020, 71, 1327–1341. [Google Scholar] [CrossRef]
  24. Kownacka, J.; Całkiewicz, J.; Kornijów, R. A turning point in the development of phytoplankton in the Vistula Lagoon (southern Baltic Sea) at the beginning of the 21st century. Oceanologia 2020, 62, 538–555. [Google Scholar] [CrossRef]
  25. Nawrocka, L.; Kobos, J. The trophic state of the Vistula Lagoon: An assessment based on selected biotic and abiotic parameters according to the Water Framework Directive. Oceanologia 2011, 53, 881–894. [Google Scholar] [CrossRef]
  26. Chubarenko, B.V.; Leitsina, L.V.; Esiukova, E.E.; Kurennoy, D.N. Model analysis of the currents and wind waves in the Vistula Lagoon of the Baltic Sea. Oceanology 2012, 52, 748–753. [Google Scholar] [CrossRef]
  27. Błędzki, L.A.; Rybak, J.I. Freshwater Crustacean Zooplankton of Europe; Springer: Cham, Switzerland, 2016; 918p. [Google Scholar]
  28. Ejsmont-Karabin, J. Empirical equations for biomass calculation of planktonic rotifers. Pol. Arch. Hydrobiol. 1998, 45, 513–522. [Google Scholar]
  29. McAleece, N.; Gage, J.D.G.; Lambshead, P.J.D.; Paterson, G.L.J. BioDiversity Professional Statistics Analysis Software; Publishing Physics Web: Bristol, UK, 1997. [Google Scholar]
  30. Dumont, H.J.; Segers, H. Estimating lacustrine zooplankton species richness and complementarity. Hydrobiologia 1996, 341, 125–132. [Google Scholar] [CrossRef]
  31. Brucet, S.; Boix, D.; Gascón, S.; Sala, J.; Quintana, X.; Badosa, A.; Søndergaard, M.; Lauridsen, T.L.; Jeppesen, E. Species richness of crustacean zooplankton and trophic structure of brackish lagoons in contrasting climate zones: North temperate Denmark and Mediterranean Catalonia (Spain). Ecography 2009, 32, 692–702. [Google Scholar] [CrossRef]
  32. Alekseev, V.R. Confusing Invader: Acanthocyclops americanus (Copepoda: Cyclopoida) and Its Biological, Anthropogenic and Climate-Dependent Mechanisms of Rapid Distribution in Eurasia. Water 2021, 13, 1423. [Google Scholar] [CrossRef]
  33. Szymczak, E. Characteristics of Sediments in a Changing Environmental Conditions in Vistula Lagoon (Poland). IOP Conf. Ser. Earth Environ. Sci. 2019, 362, 012048. [Google Scholar] [CrossRef]
  34. Arruda, J.A.; Marzolf, G.R.; Faulk, R.T. The role of suspended sediments in the nutrition of zooplankton in turbid reservoirs. Ecology 1983, 65, 1225–1235. [Google Scholar] [CrossRef]
  35. McCabe, G.D.; O’Brien, W.J. The effects of suspended silt on feeding and reproduction of Daphnia pulex. Am. Midl. Nat. 1983, 110, 324–337. [Google Scholar] [CrossRef]
  36. Gliwicz, Z.M. Suspended clay concentration controlled by filter-feeding zooplankton in a tropical reservoir. Nature 1986, 323, 330–332. [Google Scholar] [CrossRef]
  37. Hammer, U.T. Zooplankton distribution and abundance in saline lakes of Alberta and Saskatchewan, Canada. Int. J. Salt Lake Res. 1993, 2, 111–132. [Google Scholar] [CrossRef]
  38. Bielańska-Grajner, I.; Cudak, A. Effects of Salinity on Species Diversity of Rotifers in Anthropogenic Water Bodies. Pol. J. Environ. Stud. 2014, 23, 27–34. [Google Scholar]
  39. Wetzel, R.G. Limnology. Lake and River Ecosystems, 3rd ed.; Academic Press: San Diego, CA, USA, 2001; 1006p. [Google Scholar]
  40. Gilbert, J.J. Competition between rotifers and Daphnia. Ecology 1985, 66, 1943–1950. [Google Scholar] [CrossRef]
  41. Karpowicz, M.; Ejsmont-Karabin, J.; Więcko, A.; Górniak, A.; Cudowski, A. A place in space—The horizontal vs vertical factors that influence zooplankton (Rotifera, Crustacea) communities in a mesotrophic lake. J. Limnol. 2019, 78, 243–258. [Google Scholar] [CrossRef]
  42. Ejsmont-Karabin, J.; Gorelysheva, Z.; Kalinowska, K.; Weglenska, T. Role of Zooplankton (Ciliata, Rotifera and Crustacea) in phosphorus removal from cycling: Lakes of the river Jorka watershed (Masuria Lakeland, Poland). Pol. J. Ecol. 2004, 52, 275–284. [Google Scholar]
  43. Sługocki, Ł.; Rymaszewska, A.; Kirczuk, L. To fit or to belong: Characterization of the non-native invader Eurytemora carolleeae (Copepoda: Calanoida) in the Oder River system (Central Europe). Aquat. Invasions 2021, 16, 443–460. [Google Scholar] [CrossRef]
  44. Karlsson, K.; Winder, M. Adaptation potential of the copepod Eurytemora affinis to a future warmer Baltic Sea. Ecol. Evol. 2020, 10, 5135–5151. [Google Scholar] [CrossRef]
  45. Diekmann, A.B.S.; Clemmesen, C.; John, M.A.S.; Paulsen, M.; Peck, M.A. Environmental cues and constraints affecting the seasonality of dominant calanoid copepods in brackish, coastal waters: A case study of Acartia, Temora and Eurytemora species in the south-west Baltic. Mar. Biol. 2012, 159, 2399–2414. [Google Scholar] [CrossRef]
  46. Rajasilta, M.; Hänninen, J.; Vuorinen, I. Decreasing salinity improves the feeding conditions of the Baltic herring (Clupea harengus membras) during spring in the Bothnian Sea, northern Baltic. ICES Mar. Sci. Symp. 2014, 71, 1148–1152. [Google Scholar] [CrossRef]
  47. Hernroth, L.; Ackefors, H. The zooplankton of the Baltic Proper: A long-term investigation of the fauna, its biology and ecology. Rep. Inst. Mar. Res. Uddevalla 1979, 2, 1–60. [Google Scholar]
  48. Sellner, K.G.; Bundy, M.H. Preliminary results of experiments to determine the effects of suspended sediments on the estuarine copepod Eurytemora affinis. Cont. Shelf Res. 1987, 7, 1435–1438. [Google Scholar] [CrossRef]
  49. Gasparini, S.; Castel, J.; Irigoien, X. Impact of suspended particulate matter on egg production of the estuarine copepod, Eurytemora affinis. J. Mar. Syst. 1999, 22, 195–205. [Google Scholar] [CrossRef]
  50. Kimmel, D.G.; Bradley, B.P. Specific protein responses in the calanoid copepod Eurytemora affinis (Poppe, 1880) to salinity and temperature variation. J. Exp. Mar. Biol. Ecol. 2001, 266, 135–149. [Google Scholar] [CrossRef]
  51. Seuront, L. Effect of salinity on the swimming behaviour of the estuarine calanoid copepod Eurytemora affinis. J. Plankton Res. 2006, 28, 805–813. [Google Scholar] [CrossRef]
  52. Labuce, A.; Ikauniece, A.; Strāķe, S.; Souissi, A. Survey of Presence of Non-Indigenous Eurytemora carolleeae in the Gulf of Riga (Baltic Sea) Five Years After its First Discovery. Proc. Latv. Acad. Sci. 2018, 72, 230–235. [Google Scholar] [CrossRef][Green Version]
  53. Sukhikh, N.; Souissi, A.; Souissi, S.; Holl, A.C.; Schizas, N.V.; Alekseev, V. Life in sympatry: Coexistence of native Eurytemora affinis and invasive Eurytemora carolleeae in the Gulf of Finland (Baltic Sea). Oceanologia 2019, 61, 227–238. [Google Scholar] [CrossRef]
  54. Semenova, A.S.; Tchougounov, V.K. The distribution of Moina micrura Kurz, 1875 (Crustacea: Moinidae) in the Russian part of the Vistula Lagoon (Baltic Sea). Russ. J. Biol. Invasions 2018, 9, 175–183. [Google Scholar] [CrossRef]
  55. Karpowicz, M.; Świsłocka, M.; Sługocki, Ł.; Czerniawski, R.; López, C.; Kornijów, R. Distribution of Diaphanosoma (Diplostraca: Sididae) genus in Central Europe—Morphological and molecular approach. Eur. Zool. J. 2022, 89, 1115–1128. [Google Scholar] [CrossRef]
  56. Korovchinsky, N.M.; Sanoamuang, L.-O. Overview of Sididae (Crustacea: Cladocera: Ctenopoda) of Northeast and East Thailand, with description of a new species of the genus Diaphanosoma. Zootaxa 2008, 1682, 45–61. [Google Scholar] [CrossRef]
  57. Lazareva, V.I.; Bolotov, S.E. Analysis of coexistence of the recent invader Diaphanosoma orghidani Negrea with the aboriginal species D. brachyurum (Lievin) (Crustacea, Cladocera) in the Rybinsk Reservoir. Russ. J. Biol. Invasions 2013, 4, 161–173. [Google Scholar] [CrossRef]
  58. Liu, P.; Xu, L.; Xu, S.-L.; Martínez, A.; Chen, H.; Cheng, D.; Dumont, H.J.; Han, B.-P.; Fontaneto, D. Species and hybrids in the genus Diaphanosoma Fischer, 1850 (Crustacea: Branchiopoda: Cladocera). Mol. Phylogenet. Evol. 2018, 118, 369–378. [Google Scholar] [CrossRef]
  59. Lazareva, V.I.; Bolotov, S.E. Peculiarities of the biology of two Diaphanosoma species (Crustacea, Cladocera) in Rybinsk Reservoir. Inland Water Biol. 2014, 7, 108–116. [Google Scholar] [CrossRef]
  60. Karpowicz, M.; Ejsmont-Karabin, J. Diversity and Structure of Pelagic Zooplankton (Crustacea, Rotifera) in NE Poland. Water 2021, 13, 456. [Google Scholar] [CrossRef]
  61. Weiler, W. Erstfund von Diaphanosoma orghidani Negrea 1982 (Crustacea: Sididae) für Deutschland und ihre Begleitarten [First record of Diaphanosoma orghidani Negrea 1982 (Crustacea: Sididae) in Germany and its companions]. Lauterbornia H 1997, 32, 73–77. [Google Scholar]
  62. Illyova, M.; Nemethova, D. Long-term changes in cladoceran assemblages in the Danube floodplain area (Slovak-Hungarian stretch). Limnologica 2005, 35, 274–282. [Google Scholar] [CrossRef][Green Version]
  63. Alekseev, V.R.; Fefilova, E.; Dumont, H.J. Some noteworthy free-living copepods from surface freshwater in Belgium. Belg. J. Zool. 2002, 132, 133–139. [Google Scholar]
  64. Sahuquillo, M.; Miracle, M.R. The role of historic and climatic factors in the distribution of crustacean communities in Iberian Mediterranean ponds. Freshw. Biol. 2013, 58, 1251–1266. [Google Scholar] [CrossRef]
  65. Miracle, M.R.; Alekseev, V.R.; Monchenko, V.; Sentandreu, V.; Vicente, E. Molecular-genetic-based contribution to the taxonomy of the Acanthocyclops robustus group. J. Nat. Hist. 2013, 47, 863–888. [Google Scholar] [CrossRef]
  66. Anufriieva, E.; Hołyńska, M.; Shadrin, N. Current Invasions of Asian Cyclopid Species (Copepoda: Cyclopidae) in Crimea, with Taxonomical and Zoogeographical Remarks on the Hypersaline and Freshwater Fauna. Annal. Zool. 2014, 64, 109–130. [Google Scholar] [CrossRef]
  67. Karabin, A.; Ejsmont-Karabin, J. Zespoły zooplanktonu jezior Suwalskiego Parku Krajobrazowego (Zooplankton communities in the lakes of Suwałki Lanscape Park). In Jeziora Suwalskiego Parku Krajobrazowego; Hillbricht-Ilkowska, A., Wisniewski, R.J., Eds.; Zesz Nauk Komitetu Człowiek i Środowisko, PAN: Warsaw, Poland, 1994; Volume 7, pp. 215–242. (In Polish) [Google Scholar]
  68. Karpowicz, M. Biodiversity of microcrustaceans (Cladocera, Copepoda) in a lowland river ecosystem. J. Limnol. 2017, 76, 15–22. [Google Scholar] [CrossRef]
  69. Ejsmont-Karabin, J.; Kalinowska, K.; Karpowicz, M. Structure of ciliate, rotifer, and crustacean communities in lake systems of Northeastern Poland. In Polish River Basins and Lakes—Part II; Springer: Cham, Switzerland, 2020; Volume 87, pp. 77–101. [Google Scholar] [CrossRef]
  70. Bláha, M. Descriptions of copepodid and adult Acanthocyclops trajani (Mirabdullayev Defaye 2002) and A. einslei (Mirabdullayev Defaye 2004) (Copepoda: Cyclopoida) with notes on their discrimination. Fundam. Appl. Limnol. 2010, 177, 223–240. [Google Scholar] [CrossRef]
  71. Linkowski, T.B.; Kornijów, R.; Karpowicz, M. Comparison of methods for nocturnal sampling of predatory zooplankters in shallow waters. Oceanologia 2021, 63, 71–79. [Google Scholar] [CrossRef]
  72. Tang, F. Biological Invasions in Brackish Waters. Ph.D. Thesis, Churchill College, University of Cambridge, Cambridge, UK, August 2020. [Google Scholar] [CrossRef]
Sustainability 15 02345 g001
Figure 1. Location of the sampling stations marked with dots (no. 1–6) in the western part of Vistula Lagoon (southern Baltic Sea, Poland). Grey lines present the planned Vistula Split and fairway with the range of investment impact (according to https://www.umgdy.gov.pl/wp-content/uploads/2015/07/TI_Karta_Informacyjna_Przedsiewziecia.pdf (accessed on 20 December 2022), modified).
Figure 1. Location of the sampling stations marked with dots (no. 1–6) in the western part of Vistula Lagoon (southern Baltic Sea, Poland). Grey lines present the planned Vistula Split and fairway with the range of investment impact (according to https://www.umgdy.gov.pl/wp-content/uploads/2015/07/TI_Karta_Informacyjna_Przedsiewziecia.pdf (accessed on 20 December 2022), modified).
Sustainability 15 02345 g001
Sustainability 15 02345 g002
Figure 2. Seasonal changes of abundance (A)—abundance total; (B)—abundance of adult form, without copepodites and nauplii; (C)—abundance of nauplii) and diversity (D)—number of species; (E)—Shannon index; (F)—dominance B–P index) of crustacean zooplankton in Vistula Lagoon (2019–2021). The different italics letters (a, b, c) above the box plots indicated significantly different values at p < 0.05, while the same letters mean no significant differences.
Figure 2. Seasonal changes of abundance (A)—abundance total; (B)—abundance of adult form, without copepodites and nauplii; (C)—abundance of nauplii) and diversity (D)—number of species; (E)—Shannon index; (F)—dominance B–P index) of crustacean zooplankton in Vistula Lagoon (2019–2021). The different italics letters (a, b, c) above the box plots indicated significantly different values at p < 0.05, while the same letters mean no significant differences.
Sustainability 15 02345 g002
Sustainability 15 02345 g003
Figure 3. Seasonal changes of (A) abundance and diversity; (B) number of species; (C) Shannon index; and (D) dominance B–P index of Rotifera in Vistula Lagoon (2019–2021). The different italics letters (a, b) above the box plots indicated significantly different values at p < 0.05, while the same letters mean no significant differences.
Figure 3. Seasonal changes of (A) abundance and diversity; (B) number of species; (C) Shannon index; and (D) dominance B–P index of Rotifera in Vistula Lagoon (2019–2021). The different italics letters (a, b) above the box plots indicated significantly different values at p < 0.05, while the same letters mean no significant differences.
Sustainability 15 02345 g003
Sustainability 15 02345 g004
Figure 4. Zooplankton biomass with the share of Rotifera, Calanoida, Cladocera, Cyclopoida, and Harpacticoida.
Figure 4. Zooplankton biomass with the share of Rotifera, Calanoida, Cladocera, Cyclopoida, and Harpacticoida.
Sustainability 15 02345 g004
Sustainability 15 02345 g005
Figure 5. The similarity of Crustacea (A) and Rotifera (B) communities visualized by agglomerative hierarchical cluster analysis (AHC) based on the Bray–Curtis similarity matrix.
Figure 5. The similarity of Crustacea (A) and Rotifera (B) communities visualized by agglomerative hierarchical cluster analysis (AHC) based on the Bray–Curtis similarity matrix.
Sustainability 15 02345 g005
Table 1. List of pelagic zooplankton species and their frequency in the Vistula Lagoon (2019–2021).
Table 1. List of pelagic zooplankton species and their frequency in the Vistula Lagoon (2019–2021).
Calanoida Cephalodella gibba (Ehrenberg, 1830)*
Acartia bifilosa (Giesbrecht, 1881)***Collotheca pelagica (Rousselet, 1893)*
Eurytemora affinis (Poppe, 1880)****Colurella colurus (Ehrenberg, 1830)*
Centropages hamatus (Lilljeborg, 1853)*Colurella dicentra (Gosse, 1887)*
Cyclopoida Euchlanis deflexa (Gosse, 1851)*
Acanthocyclops americanus (Marsh, 1893)***Euchlanis dilatata Ehrenberg, 1832*
Cyclops vicinus Uljanin, 1875*Filinia brachiata (Rousselet, 1901)*
Mesocyclops leuckarti (Claus, 1857)*Filinia longiseta (Ehrenberg, 1834)**
Thermocyclops oithonoides (Sars G.O., 1863)*Hexarthra fennica (Levander, 1892)**
Harpacticoida spp.***Keratella cochlearis Gosse, 1851****
Cladocera Keratella cruciformis (Thompson, 1892)****
Acroperus harpae (Baird, 1834)*Keratella quadrata Müller, 1786****
Bosmina (Eubosmina) coregoni Baird, 1857*Keratella tecta (Gosse, 1851)****
Bosmina (Bosmina) longirostris (O.F. Müller, 1785)*Keratella testudo (Ehrenberg, 1832)*
Chydorus sphaericus (O.F. Müller, 1776)**Lecane closterocerca (Schmarda, 1859)*
Coronatella rectangula (Sars, 1862)*Lecane luna (Müller, 1776)*
Daphnia cucullata G.O. Sars, 1862*Notholca acuminata (Ehrenberg 1832)*
Diaphanosoma spp.***Polyarthra dolichoptera Idelson, 1925*
Sida crystallina (O.F. Müller, 1776)*Polyarthra vulgaris Carlin, 1943*
Leptodora kindtii (Focke, 1844)*Synchaeta cecilia Rousselet, 1902*
Rotifera Synchaeta sp.**
Brachionus angularis Gosse, 1851**Synchaeta stylata Wierzejski, 1893*
Brachionus calyciflorus Pallas, 1776***Trichocerca dixon-nuttallii (Jennings, 1903)**
Brachionus urceolaris Müller, 1773*
Frequencies: * <10%, ** 10–25%, *** 26–50%, **** >50%.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Karpowicz, M.; Kornijów, R.; Ejsmont-Karabin, J. Not a Good Place to Live for Most, but Excellent for a Few—Diversity of Zooplankton in a Shallow Coastal Ecosystem. Sustainability 2023, 15, 2345. https://doi.org/10.3390/su15032345

AMA Style

Karpowicz M, Kornijów R, Ejsmont-Karabin J. Not a Good Place to Live for Most, but Excellent for a Few—Diversity of Zooplankton in a Shallow Coastal Ecosystem. Sustainability. 2023; 15(3):2345. https://doi.org/10.3390/su15032345

Chicago/Turabian Style

Karpowicz, Maciej, Ryszard Kornijów, and Jolanta Ejsmont-Karabin. 2023. "Not a Good Place to Live for Most, but Excellent for a Few—Diversity of Zooplankton in a Shallow Coastal Ecosystem" Sustainability 15, no. 3: 2345. https://doi.org/10.3390/su15032345

APA Style

Karpowicz, M., Kornijów, R., & Ejsmont-Karabin, J. (2023). Not a Good Place to Live for Most, but Excellent for a Few—Diversity of Zooplankton in a Shallow Coastal Ecosystem. Sustainability, 15(3), 2345. https://doi.org/10.3390/su15032345

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop